BIODIVERSITY JOURNAL

2016,7 (1): 1-200

Quaternly scientific journal

edited by Edizioni Danaus,

viaV. Di Marco 43,90143 Palermo, Italy

www.biodiversityjournal.com

biodiversityjournal@gmail.com

Official authorization no. 40 (28.12.2010)

ISSN 2039-0394 (Print Edition)

ISSN 2039-0408 (Online Edition)

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Managing Editor

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Chief Editor

Maria Stella Colomba

University of Urbino “Carlo Bo”, Italy

Secretary

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Assistant Editors

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University of Urbino “Carlo Bo”, Italy

Tommaso La Mantia - Univ. of Palermo, Italy

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Agatino Reitano - Catania, Italy

Giorgio Sparacio - Palermo

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SCIENTIFIC COMMITTEE

Vittorio Aliquo - Palermo, Italy

Pietro Alicata - University of Catania, Italy

Marco Arculeo - University of Palermo, Italy

Paolo Audisio, Sapienza University of Rome, Italy

Alberto Ballerio - Brescia, Italy

Rostislav Bekchiev - National Museum of Natural History, Sofia, Bulgaria

Christoph Buckle - Tubingen, Germany

Attilio Carapezza - Palermo, Italy

Donald S. Chandler - University of New Hampshire, Durham, U.S.A

Renato Chemello - University of Palermo, Italy

Giulio Cuccodoro -The Natural History Museum of Geneva, Switzerland

Vera D'Urso - University of Catania, Italy

Alan Deidun - University of Malta, Msida, Malta

Gianniantonio Domina - University of Palermo, Italy

Gerhard Falkner - Deutsche Malakozoologische Gesellschaft, Germany

Paola Gianguzza - University of Palermo, Italy

Ilia Gjonov -Sofia University, Bulgaria

Adalgisa Guglielmino,Tuscia University, Viterbo, Italy

Peter Hlavac - Prague, Czech Republic

Ren Hirayama -Waseda University, Shinjuku-ku, Tokyo, Japan

Rumyana Kostova - Sofia University, Bulgaria

Sergey A. Kurbatov - Moscow, Russia

Albena Lapeva-Gjonova - Sofia University, Bulgaria

Oscar List - University of Catania, Italy

Pietro Lo Cascio - Associazione “Nesos”, Lipari, Italy

Nathalie Yonow - Swansea University, Swansea, Wales, U.K.

Federico Marrone - University of Palermo, Italy

Bruno Massa - University of Palermo, Italy

Pietro Mazzola - University of Palermo, Italy

David Mifsud - University of Malta, Msida, Malta

Alessandro Minelli - University of Padova, Italy

Pietro Minissale - University of Catania, Italy

Marco Oliverio - University of Roma, Italy

Roberto A. Pantaleoni - CNR National Research Council, Sassari, Italy

Salvatore Pasta - Palermo, Italy

Alfredo Petralia - University of Catania, Italy

Roberto Poggi - Museo civico di Storia naturale“G. Doria”, Genova, Italy

Francesco Maria Raimondo - University of Palermo, Italy

Marcello Romano - Capaci, Italy

Giorgio Sabella - University of Catania, Italy

Danilo Scuderi - Catania, Italy

Giuseppe FabrizioTurrisi - Catania, Italy

Errol Vela - Universite Montpellier, France

Polycera quadrilineata (O.F. Muller, 1776) (Gastropoda Polyceridae). Order Nudibranchia (Mollusca,

Opisthobranchia). Nudibranchs are commonly known as “sea slugs” because they are not shelled molluscs. The evolution

of the shell in gastropods followed a complexity plan of development, starting from simply low spiral, patelliform

structures to highly twisted shells, the most safety house where a soft-body animal could hide from predators. How could

shells be more efficient? After the “invention” of the shell, gastropods - which became heavy and slow - started to produce a

thin shell. Increasing mobility conducted to shell reduction and this latter required a new plan of defense from predators.

Probably around 3 or 4 hundreds of years ago, nudibranchs evolved from shelled molluscs and diversified. What is the

successful of this new branch of gastropods due to? Toxicity or simply disgust to predators. This condition was reached by

nudibranchs in two different ways. Some accumulate chemical active molecules throughout their tissues from the natural

host upon which they feed, thus resulting venomous or stodgy. Some others build an internal equipment of spicules, which

make them very hard to eat. How to infonn their potential predators of their dangerous internal items? Nudibranchs are very

beautiful marine organisms, showing delicate external soft parts and spectacular colors, often comparable to butterflies.

The reason of these showy colorations is the aposematic message; warning colorations mean: “I am venomous” so that

predators immediately learn it is better to avoid these striking animals.

The photograph shows a specimen of P. quadrilineata crawling on an ascidian looking for some encrusting bryozoans to eat

(Summer 2004, Riposto, Catania, Eastern Sicily) (cover photo by Danilo Scuderi).

Danilo Scuderi. Via Mauro de Mauro 1 5b, Belpasso, Catania; e-mail: danscu@tin.it

Biodiversity Journal, 2016, 7 (1): 3-6

Nesting of the Black Stork Ciconia nigra Linnaeus, 1 758 (Aves

Ciconiidae) in the FiumaraVitravo Valley (Calabria, Italy)

Francesco Lamanna

Alcimo street 88815 Strongoli Marina, Crotone, Italy; e-mail: niphargus@libero.it

ABSTRACT The Fiumara Vitravo Valley in the province of Crotone in Italy, is a Site of National Interest

for its rich biodiversity and peculiar habitat, and also a strategic area for the nesting of Black

Stork, Ciconia nigra Linnaeus, 1758 (Aves Ciconiidae). The river morphology, the harshness

of this wild territory, the luxuriant vegetation, the presence of a hydrographic network rich of

trophic resources and the crucial position along the migratory routes, are fundamental for the

reproductive biology and the evolution of this species. This work will expose the results of

the monitoring activities that were carried out in 2015 by which it was possible to document

the Black Stork nesting on rocky areas in the valley of Fiumara Vitravo. The ecological im-

portance of the area is strongly in need of greater scientific attention and a suitable site pre-

servation in order to favor the population increment of the Black Stork also in Calabria, where

the active reproductive population was present only until 2001. The results are in evident

countertrend with respect to older statistical data, which provide negative and sparse data for

black stork presence in the “Alto Crotonese” region.

KEY WORDS Ciconia nigra; Crotone; Calabria; nesting site.

Received 03.12.2015; accepted 19.01.2016; printed 30.03.2016

INTRODUCTION

The Black Stork, Ciconia nigra Linnaeus, 1758

(Aves Ciconiidae) is a bird with a wide territorial

distribution. Its nesting area goes from Spain to

Sachalin island between the 35° and 60° North

parallel, with a separate population nesting in South

Africa (Del Hoyo et al., 1992). The species, having

a palearctic afro-tropical chorology, is very rare in

western Europe, where it has suffered from drastic

reduction with a complete disappearance in some

states due to the destruction of its natural habitat.

In Italy, the black stork is a migrating nesting

species rarely wintering. Its biological characteristic

is of long range flyer, able to travel over large

portions of the sea, allowing it to migrate from win-

tering zones to nesting areas travelling for thou-

sands of kilometers.

The populations move along not well defined

routes, crossing the Mediterranean sea on a wide

frontline. Some groups travel through the Strait of

Gibraltar, others through the Red Sea along the Suez

Canal to the Caucasian regions, others from the

Black Sea go through the Bosphorus. One group

crosses the eastern Mediterranean from Peloponnese

partially exploiting the bridge fomied by the Egeo

islands. A small group proceeds along the Sicily

channel and the Italian peninsula (Petretti, 1993).

Francesco Lamanna

The passage of Black Stork in Calabria is not well

documented for the lack of an observation network

throughout the territory. Small groups of isolated in-

dividuals, observed during the passage, may lead

one to think both the Tyrrhenian and Ionic side of

Calabria as preferential migratory routes, although

the crossing of the Sila plateau cannot be excluded.

In general, the reproduction area of the species

should include Eurasia, Southern Africa and

Western Spain at the border with Portugal. Isolated

populations are also found in central Europe and

Balkans. The eastern reproduction area is more

continuous including the north-east of Turkey, the

Caucasus, and a wide region of Russia. In Italy, the

first verified nesting was in 1994 in the natural park

of Monte Fenera in the bassa Valsesia in the Pied-

mont region. In the last years a gradual increment

of the number of nesting couples has been observed

in several Italian regions with a preference for the

southern regions (Bordignon, 2006).

THE BLACK STORK IN CALABRIA

At the end of the 19th century Lucifero (2003),

a man of wide cultural interests, published the first

information on the presence of the black stork in

Calabria. In that essay the Black Stork is classified

as accidental and very rare and its presence was

signaled in the area close to Crotone and Isola Capo

Rizzuto. In the same essay some statements made

by Moschella (in Lucifero, 2003), for the Reggio

Calabria province, ensured the presence of the

species in that region.

The information was very scarce in the begin-

ning of the century, and only starting from the

1970s, reliable data recorded the species as avail-

able in the Calabria region. After 1970 the obser-

vations became more frequent with several

sightings. In 1994, the Black Stork nested in Ca-

labria, with only one couple bringing four young

birds to fly (Bordignon, 1995). The next year an-

other couple brought two to flight. In 1996 no

nesting was registered despite the presence of some

individuals (G. Rocca personal observation) on the

Lese and Neto rivers in the Crotone region. In 1997

only one couple was present bringing two young

birds to flight. In the years 1998 and 1999 no

nesting was registered but just the presence of isol-

ated individuals on the Lese river (G. Rocca per-

sonal observation). In 2000 only one couple nested

in the Crotone region with four flying young birds

(Bordignon et al., 2011). In 2001 the same nest was

used by a couple for the deposition of four eggs

and the flight of four young birds (Rocca, 2002).

In the same year a second couple was detected by

A. Digiorgio in the same reproduction area. In

2002 the presence of a couple with two immature

individuals was registered in the nesting and

feeding area. In March 2014, a serious event

occurred in one of the most important migratory

routes for migrating avifauna. In the core of the

Parco Nazionale della Sila an adult black stork was

found dead, shot by an unknown poacher in the S.

Nicola location in the zone 2 of the park in the

Serra Pedace district. In August 2014, during a

research campaign, conducted by myself in the

valley of Lese river, the presence of an isolated

individual was detected. In February 2015, another

disappointing event happened on the Amato river

near Terzi di Lamezia Terme (Catanzaro) where

one specimen was seen with a broken leg in an

evident difficult condition but still able to fly

(Lega Italiana Protezione Uccelli Sez. Rende,

www.lipurende.it). In the present year an intensive

search activity to individuate nesting black storks

was successfully accomplished finding a couple

regularly nesting on a rock face in the SIN of

“Vallone Vitravo”.

SIN (SITE OF NATIONAL INTEREST)

“VALLONE VITRAVO”

The Fiumana Vitravo is one of the major rivers

of the “Alto Crotonese” district situated in the North

East part of the Calabria region, having a major

branch length of 43 Km. In its medium highest por-

tion it has a torrential regime, while in the medium

part water flows in a deep canyon. Downstream the

morphology is like the Calabrian rivers’ with a wide

bed and holm oaks.

The site “Vallone Vitravo” (IT9300192), be-

longing to the biogeographic mediterranean region

with an abundance of wet fluvial habitat, includes

8 Km of riverbed of this important river extending

in its median portion on a surface of about 800 ha.

The area is characterized by a very dense ri-

parian vegetation, with mixed forest of deciduous,

sclerophyllous and brushwood, and Mediterranean

Nesting of the Black Stork Ciconia nigra (Aves Ciconiidae) in the Fiumara Vitravo Valley (Calabria, Italy)

low. Ichthyic-fauna based on salmons populates the

zones where water flows more rapidly and creates

wide and deep potholes, while Cyprinidae stand in

the valley areas.

The biotic characterization of Vallone Vitravo

was performed since the high naturalistic value of

the site makes it a unique habitat for the preserva-

tion of important floristic species, peculiar endemic

floras and faunas and endangered birds. The geo-

morphological characteristics of the area, with

mighty and inaccessible rock walls, permit the

nesting of animal species of the european com-

munity interest included into the Attachment 1 of

Direttiva “Uccelli” 79/409/CEE as Black Stork,

Ciconia nigra , nesting area until 2001.

THE NESTING SITE

In August 2014, on the Lese river, close to the

confluence with Neto river, a single individual of

black stork was accidentally observed. It was an

individual of which it was not possible to obtain any

ethological information due to the late reproduction

period and the difficulty in finding the feeding sites.

In that circumstance the presence of any other indi-

vidual or nesting site was not detected. This ap-

pearance, of great ornithological importance, and

related data on spring migration flows pushed us to

plan for 201 5 a search campaign in the valley of the

Fiumara Vitravo, nesting site of the species (Rocca,

2005).

In May 2015 it was identified the pair and the

nesting site. The nest was built within a natural

cavity at the base of a shelf of rock, on a sandstone

rock face in the valley of Fiumara Vitravo. The nest

was at an altitude of 370 m on the see level at the

top of the sandstone rock face which is 80 m long

with East exposition. The great distance of the nest

from the possible observation points, at least 300

m, together with the peculiar conformation of the

valley, which barely offer a suitable observation

prospective, did not permit to get information on

the number of laid eggs. In the first decades of June,

two nestlings, apparently one week old, were fed

by both parents. In the last decade of July the

feeding phase was regularly concluded and the

young birds took their first flight.

The nesting site were monitored visually from

three observation points at a minimum distance of

Figure 1. Black Stork flying over the Vitravo Valley.

300 m. After hatching, observations were made

periodically with short cyclical 1 0 day visits on the

sites in order to avoid disturbing the reproductive

cycle of the couple.

CONCLUSIONS

N esting of black stork in the valley of Fiumara

Vitravo brings the attention of the researchers to a

site of greatest importance for the survival of this

extraordinary bird. The reproduction success in the

Alto Crotonese region shows, in this delicate

phase of the geographic expansion of the species,

a positive trend in the conquering of the habitats

where black stork had disappeared for years. The

natural preservation of these fragile and unique

ecosystems imposes a collective effort to the

scientific community. It should be necessary in the

future to continue the monitoring of the site in

order to remove or to reduce all the factors (pollu-

tion, fire, anthropic impact, etc.) that limit the

expansion of the species.

REFERENCES

Bordignon L., 1995. Prima nidificazione di cicogna nera,

Ciconia nigra, in Italia. Rivista italiana di omitologia,

64: 106-116.

Francesco Lamanna

Bordignon L., Branelli M., Buoninconti F., Caldarella

M., Fraissinet M., Francione M., Fulco E., Gatti

F., Marrese M., Rizzi V. & Visceglia M., 2011. La

cicogna nera in Italia. Status e problemi di conser-

vazione della popolazione nidificante, 2011.

Del Hoyo J., Elliot A. & Sargatal J. (Eds.), 1992. Hand-

book of the birds of the World. Vol. 1, Ostrichto

Ducks. Lynx Edictions, Barcellona.

Lucifero A., 2003. Avifauna e Mammiferi della Calabria,

Selezione di Scritti Naturalistici. Greentime editori,

Bologna, 60 pp.

Petretti F., 1993. La nera sentinella dei boschi e delle

rocce. Oasis, 9: 74-87.

Rocca G., 2002. Nuovi dati sulla Cicogna nera, Ciconia

nigra, in Calabria. Rivista italiana di ornitologia, 7 1 :

218-219.

Rocca G., 2005. La cicogna nera in Calabria. In: Bor-

dignon L. (Ed.). La cicogna nera in Italia. Parco Nat-

urale del Monte Fenera. Tipolitografia di Borgosesia,

Borgosesia (VC).

Biodiversity Journal, 2016, 7 (1): 7-10

The amphioxus Epigonichthys maldivensis (Forster Cooper,

1 903) (Cephalochordata Branchiostomatidae) larvae in the

plankton from Rapa Nui (Chile) and ecological implications

Erika Meerhoff 1,2 *; David Veliz 2,3 ; Caren Vega-Retter 2,3 & BeatrizYannicelli 1,2

'Centro de Estudios Avanzados en Zonas Aridas (CEAZA), Coquimbo, Chile

2 Millennium Nucleus for Ecology and Sustainable Management of Oceanic Islands (ESMOI), Universidad Catolica del Norte, Lar-

rondo 1281, Coquimbo, Chile

3 Departamento de Ciencias Ecologicas, Facultad de Ciencias, Universidad de Chile

Corresponding author, e-mail: erikameerhoff@udec.cl

ABSTRACT We report the first record of amphioxus larvae in the plankton from Rapa Nui island (Chile).

Zooplankton was sampled using an oblique Bongo net during an oceanograhic survey in April

and September 2015. A total of four larvae were collected in the coastal area of Rapa Nui in

April and 13 in September. The larvae were identified as Epigonichthys maldivensis (Forster

Cooper, 1903) (Cephalochordata Branchiostomatidae) using both morphological and genetic

characters. The water column in this area presented a mean temperature of 21.2°C, a mean

salinity of 35.7 %o and 4.94 ml/L dissolved oxygen in April, and 20°C and 35.75 %o mean

salinity in September. Amphioxus have been reported as playing a key role in marine food

webs transferring important amounts of microbial production to higher trophic levels, due to

this their role in the Rapa Nui plankton and benthos as adults could be interesting because

Easter island is located in the oligotrophic gyre of the South Pacific ocean where a microbial

trophic web is expected to dominate. This record increases the biodiversity of Rapa Nui

plankton and widens the geographic distribution of E. maldivensis that was restricted only to

the Western and Central Pacific and Indian Ocean.

KEY WORDS amphioxus larvae; Pacific Ocean; plankton.

Received 03.12.2015; accepted 19.01.2016; printed 30.03.2016

INTRODUCTION

The Amphioxus or lancelets (Chordata) com-

prise the subphylum Cephalochordata (Schubert et

al., 2006); which is formed by three genera: Bran-

chiostoma Costa, 1 834, Epigonichthys Peters, 1876

and Asymmetron Andrews, 1893 (Konetal., 2007).

The amphioxus are filter-feeding marine organisms

that as adults burrow in the sand, gravel or shell

deposits in tropical and/or temperate waters around

the world ocean (Bertrand & Escriva, 2011). The

filtering is performed through jawless ciliated

mouths (Vergara et al., 2011).

Amphioxus are found in general in shallow wa-

ters close to the shore (0.5 to 40 m depths) and

many species prefer habitats of coarse sand and

gravel (Desdevises et al., 2011). They live in a vari-

ety of coastal habitats, estuaries, coastal lagoons,

open coasts and river deltas (Laudien et al., 2007;

Chen, 2008). However, little is known about the

ecological role of these organisms (Vergara et al.,

201 1). In addition, some amphioxus have been con-

sidered as endangered species (Kubokawa et al.,

1998). Environmental factors as temperature and

salinity changes are determinant in the life cycle of

some amphioxus species (Webb, 1956a; Webb,

Erika Meerhoff etalii

1956b; Webb & Hill, 1958). As a consequence, the

amphioxus populations migrate between winter and

summer (Webb, 1971), and the larvae are described

as restricted to waters of high salinity and temper-

ature (Webb & Hill, 1958). The duration and timing

of the spawning season varies between species

(Stokes & Holland, 1996; Holland, 2011). When

the gametes are released in the water, fecundation

occurs and the embryos persist in the plankton (Ber-

trand & Escriva, 2011) until metamorphosis, when

they migrate to the sand and become benthic adults.

Some authors have studied the zooplankton and

meroplankton around Easter Island (Castro &

Landaeta, 2002; Palma & Siva, 2006; Mujica, 2006)

most zooplankton results are from CIMAR islands

cruise in November 1999. However, there are no

records of amphioxus larvae or adults in the area. In

this work we describe the presence of amphioxus

larvae from Rapa Nui plankton (Chile) for the first

time. Larvae were found in stations close to the coast

around the island in April and September 2015.

MATERIAL AND METHODS

Zooplankton samples and hydrographic meas-

urements were gathered in the coastal area of Easter

Island or Rapa Nui (27° 13’ S - 109°37’ W), Chile,

in April and September 2015. The hydrographic

characterization of the water column was done using

a set of CTD profiles in both months (Seabird 1 8).

Zooplankton samples were collected by oblique

tows from a depth of 300 m up to the surface, using

a Bongo net with 300 pm mesh and 60 cm mouth

diameter. The volume of sampled water was estim-

ated using a mechanical flowmeter (General Ocean-

ics) attached to the net. Samples were preserved in

96% ethanol, until laboratory identification and

quantification. In these samples seventeen amphi-

oxus larvae were found. Considering that no in-

formation about amphioxus larvae morphology is

available, three larvae were used to perform the

genetic identification. After that a simple morpho-

logical description of the larvae is also supplied.

Genetic identification

Three larvae were used for the genetic analysis.

The DN A extraction was conducted using the Qiagen

QIAamp kit (Mississauga, Canada). The mitochon-

drial COI gene was amplified using the protocol and

primers described by Folmer et al. (1994) with 56°C

as annealing temperature. Forward and reverse

sequencing was performed at Pontificia Universidad

Catolica de Chile and aligned by eye using the

ProSeq v.2.9 software (Filatov, 2002). The haplotype

was deposited in Genbank (Accession Number:

KU201542). The Blast tool was used to determine

similarities with sequences deposited in Genbank.

In order to determine the nucleotide relationship

among lancelets, a neighbour-joining based phylo-

genetic (NJ) analysis was performed using Mega

6.0 software (Tamura et al., 2013). Using a boot-

strap of 10,000 replicates, the analysis tested the

consistency of each branch in the tree, grouping

sequences with similar nucleotide composition.

Using this method, unidentified sequence obtained

in this study could be grouped with conspecific

sampled in other geographical areas.

RESULTS AND DISCUSSION

A total of 4 amphioxus larvae were found in the

coastal area of Rapa Nui in April and 13 in Septem-

ber 2015. The larvae were identified as Epi-

gonichthys maldivensis (Forster Cooper, 1903)

(Cephalochordata Branchiostomatidae) (Fig. 1). In

April, in the south station, larvae were found up to

200 m depth and the abundance was 0.8 individual

per 1000 m 3 , while in the south-east station, the

abundance of E. maldivensis larvae was 2 indi-

viduals per 1000 m 3 and were found between 300

m depth and surface. The amphioxus larvae mean

abundance in September was 2 individuals per 1000

m 3 and they were found in the south station. The

environmental characteristics of the area were mean

water temperature of 21.2°C, mean salinity of 35.7

%o and 4.94 ml/L dissolved oxygen in April, and

20°C and 35.75 %o mean salinity in September.

Genetic identification. One haplotype of 550 bp

was obtained for the larvae. The analysis of the COI

gene showed a clear relationship of our sequence with

Epigonichthys maldivensis (Fig. 2). The Blast ana-

lysis showed a similarity of 99% with one sequence

of E. maldivensis (Accession Number: AB1 10093. 1),

deposited by Nohara et al. (2005) and obtained from

one individual collected in the Kuroshira Island,

Japan. Both sequences differ only in 6 bp.

Epigonichthys maldivensis is a tropical species

whose distribution was restricted only to the

Western and Central Pacific and Indian Ocean

The first record of the amphioxus Epigonichthys maldivensis larvae in the plankton from Rapa Nui (Chile)

(Richardson & McKenzie, 1994; Poss & Boschung,

1996; Lin et al., 2015), the present results expand

the geographic range of this species to Rapa Nui

island. Lancelets exhibit a week- to month long

planktonic larval stage (Wiclcstead, 1970; Wu et al.,

1994; Stokes & Holland, 1996) and in Eastern

Island these were present in April and September

2015.

The benthic communities from Rapa Nui are

extremely species-poor compared with reefs in the

central and western Pacific (Friedlander et al.,

2013), the presence of the amphioxus larvae,

implies that amphioxus adults probably live in the

benthos that would contribute to the benthos species

richness. Moreover, anecdotal histories from the

local fisherman of Rapa Nui reporting, in some

areas and dates, the presence of white filaments like

hairs in the bottom, are likely to corroborate our

findings; these filaments could be the adult amphi-

oxus. This record increases the biodiversity value

of Rapa Nui. In addition, since amphioxus have

been reported as playing a key role in marine food

webs transferring important amounts of microbial

production to higher trophic levels (Chen et al.,

2008), their role in the Rapa Nui plankton and

benthos as adults could be interesting since Easter

island is located in the oligotrophic gyre of the South

Pacific ocean where a microbial trophic web is ex-

pected to dominate. Finally, new amphioxus genome

sequences will be of great importance for compar-

ative genomics at the inter and intra species levels.

ACKNOWLEDGEMENTS

Authors acknowledge the support from the

Chilean army at Easter Island and the ORC A diving

center to conduct the samplings. EM acknowledges

the support from Postdoctoral-FONDECYT/Chile

3150419. EM acknowledges the support of Millen-

nium Nucleus for Ecology and Sustainable Man-

agement of Oceanic Islands (ESMOI). CV

acknowledges the support of Fondecyt de Iniciacion

N° 11150213. Authors also acknowledge Carolina

Paz Concha Molina from CFRD University of

Concepcion for her contribution with the drawing.

Figure 1. Above: schematic views of the amphioxus larva,

basic anatomy the oral cirri, the segmented muscles, and the

notochord are signaled. Below: Epigonichthys maldivensis

larval individual collected from Rapa Nui.

100

93 | Epigonichthys maldivensis 1

I Epigonichthys maldivensis2

Ernaldrvensis

Epigonichthys cultellusl

100 1 Epigonichthys cultellus2

-Branchiostoma betchen'2

- Branchiostoma beichen3

1Q0

100

3 □□ | — Branchiostoma malayanum2

I Branchiostoma maiayanum3

Branchiostoma floridae3

^ | — Branchiostoma fioridael

S5^ — Branchiostoma florrdae2

— Branchiostoma japomcum3

p Branchiostoma japonicuml

70 L Branchiostoma japomcum2

Branchiostoma lanceolatum3

100

i Branchiostoma lanceolatuml

100 < Branchiostoma lanceolatum2

100 lAsymmetron spl

' Asymmetron sp2

ICO lAsymmetron mfeaiml

I Asymmetron inferum2

( ■ Asymmetron lucayanuml

Asymmetron Iuc3yanum2

Asymmetron Iucayanum3

Figure 2. Neighbour-joining tree of the COI sequences for

the Branchiostomidae species. The number at the tree nodes

indicates the bootstrap values from 10,000 replicates. The

figure shows also the GenBank Accession Numbers.

REFERENCES

Bertrand S. & Escriva H., 2011. Evolutionary crossroads

in developmental biology: amphioxus. Development,

138: 4819-4830.

Castro L.R. & Landaeta M.F., 2002. Patrones de dis-

tribucion y acumulacion larval en tomo de las islas

oceanicas: Islas de Pascua y Salas y Gomez. Ciencia

y Tecnologia del Mar, 25: 131-145.

Erika Meerhoff etalii

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Biodiversity Journal, 2016, 7 (1): 11-16

Description of three new subspecies of Carabus Linnaeus, 1 758

(subgenus Coptolabrus Solier, 1 848) and taxonomic changing

on some Carabus from Far East of Russia (Coleoptera Cara-

bidae Carabinae)

Ivan Rapuzzi

Via Cialla 47, 33040 Prepotto, Udine, Italy; email: info@ronchidicialla.it

ABSTRACT Three new Carabus Linnaeus, 1758 (subgenus Coptolabrus Solier, 1848) subspecies from

Far East of Russia and Central China (Anhui Province, Chongqing Province) are described

and figured: C. ( Coptolabrus ) smaragdinus losevi n. ssp., C. ( Coptolabrus ) elysii wangguofeni

n. ssp. and C. ( Coptolabrus ) ignigena tenuitarsatus n. ssp. Comparative notes with the closest

taxa are provided. Carabus ( Morphocarabus ) hummeli vladobydovi Obydov, 2007, C.

(A ulonocarabus) gossarei mareschii Rapuzzi, 2010, C. ( Megodontus ) vietinghoffii rugicolor

Rapuzzi, 2010 and C. ( Coptolabrus ) smaragdinus robinzoni Rapuzzi, 2010 recently con-

sidered as synonyms are resurrected as valid subspecies.

KEY WORDS Carabus', Coptolabrus; new subspecies; Far East Russia; China; taxonomic changing.

Received 22.01.2016; accepted 24.02.2016; printed 30.03.2016

INTRODUCTION

The study of some Coleoptera Carabidae of the

genus Carabus Linnaeus, 1758 (subgenus Copto-

labrus Solier, 1848 see Hauser, 1921, 1932a,

1932b; Deuve & Font, 1998; Deuve, 2004) pre-

served in the author's collection in part provided by

Mr. Oleg Losev (Pavlovo, Russia) and Mr. Xi

Huangshun (Shanghai, China) gives the opportunity

to individuate three new subspecies: C. ( Copto-

labrus ) smaragdinus losevi n. ssp. from South

Primorye in the Far East of Russia, C. ( Copto-

labrus ) elysii wangguofeni n. ssp. from Anhui

province, Central China and and C. ( Coptolabrus )

ignigena tenuitarsatus n. ssp. from Chongqing

province, Central China.

In the second part of this paper five Carabus

taxa recentely considered as synonyms by Sun-

dukov (2013) are resurrected as valid subspecies.

RESULTS

New taxa

Carabus ( Coptolabrus ) smaragdinus losevi n. ssp.

Examined material. Holotype: 1 male, Far East

of Russia, South Primorye, Khasanskiy district,

Furugelm Island, 11/13.VII.2013, O. Losev legit;

preserved in the author’s collection. Paratypes: 6

males and 3 females, Far East of Russia, South

Primorye, Khasanskiy district, Furugelm Island,

11/13.VIL2013, 0. Losev legit; 6 males and 3 females,

Far East of Russia, South Primorye, Khasanskiy

district, Krabbe peninsula, 30.VI/11.VII.2012, O.

Losev legit; 25 males and 3 females, Far East of

Russia, South Primorye, Khasanskiy district,

Krabbe peninsula, 7/18.VII.2013, O. Losev legit;

24 males and 3 females, Far East of Russia, South-

Ivan Rapuzzi

west Primorskiy region, Khasanskiy district,

Mramomyy cape env., 42°34’N; 130°48’E,

28.VII/12.VIIL2012, A. Plutenko legit.

The paratypes are preserved in the author’s col-

lection, O. Losev collection and A. Plutenko collec-

tion (Russia).

Description of Holotype male. Length includ-

ing mandibles: 31 mm, maximum width of elytra:

9.8 mm (Pig. 1). Head and pronotum cupper-red,

elytra cupper-red with cupper-green sides, relatively

shiny; primary and secondary relieved intervals of

elytra black. Ventral side of pronotum and epipleura

cupper-red, metallic, abdomen dark violet; palpi

antennae and legs black. Head elongate; surface

strongly and uniformly punctured; supra-antennary

ridge bent upwards; clypeus relieved, lateral ridges

very deep and punctured. Mandibles very long and

thin, of “cychrisanf ’ shape. Eyes emispheric and

prominent. Labrum bilobate, multi-setulose. Very

long and developed palpi, sub-apical segment of

labial palpi bi-setose; apical segment of maxillary

and labial palpi dilated. Antennae thin, extending

with 4 antennomers beyond the base of pronotum

and extending more or less the third of elytra. Disc

of pronotum nearly flat; sides of pronotum narrow

margined, slightly bent upwards at the base; hind

angles rounded and very slightly protruding behind

its base; surface of pronotum uniformly and very

densely punctured, faintly roughly. Elytra quite

elongate, oval, very convex, maximum width at the

middle; shoulders narrow, slightly pronounced;

sculpture triploid heterodyname type: primary

intervals forming tubercles of oval shape, smooth;

secondary smaller, rounded and veiy smooth;

tertiary completely reduced. Legs very long and

strong. Aedeagus: the median lobe in lateral view

(Fig. 2) is regularly curved, apex long and curved;

dorsal view in figure 3.

Variability. Paratypes have a small variability:

the length of the body ranges from 27.5 mm to 32

mm for the males and from 27 mm to 34 mm for

the females. The colour of the specimens from

Krabbe peninsula is cupper green; the specimens

from Furugelm island and Mramornyy cape have

constantly the holotype colour.

Etimology. This new interesting Coptolabrus

subspecies is very cordially dedicated to Mr. Oleg

Losev (Pavlovo, Nizhegorodskaya region, Russia)

who collected part of the specimens.

Remarks. The small size, the convex shape of

elytra with smooth intervals, the quite transverse

and of hexagonal shape pronotum, the very small

and elongate head and the dominant cupper-red

colour characterize the new subspecies.

From C. ( Coptolabrus ) smaragdinus mandschu-

ricus Semenov, 1898 the new subspecies is distin-

guish for the smaller size and for the sculpture of

elytra formed by larger and smoother intervals.

From C. smaragdinus coreicus Hauser, 1921 the

new subspecies is geographically separate by the

large Tumen Jiang river valley and differs for the

smaller head, the smaller size, the longer mucrons

of elytra, the larger pronotum and smoother sculp-

ture of elytra.

The closest subspecies is C. smaragdinus robin-

zoni Rapuzzi, 2010 described from Reyneke Island

near Vladivostok (Rapuzzi, 2010; 2012). With the

new subspecies it shares the same small size but

differs for the dominant red colour, the transverse

pronotum of hexagonal shape, the very convex

elytra, the less raised sculpture of elytra and for the

shape of aedeagus more curved with longer apex.

Carabus ( Coptolabrus ) elysii wangguofeni Ra-

puzzi et Huangshun n. ssp.

Examined material. Holotype: male, China,

Anhui province, Taihu, Wangling vill., South slope

of Mt. Dabieshan, 400 m, 10/30.IV.2015, (30°31T8"

N; 116°16'39" E), Xihuangshun legit; preserved in

Ivan Rapuzzi collection. Paratypes: 9 males and 11

females, China, Anhui province, Taihu, Wangling

vill., North slope of Mt. Dabieshan, 400 m,

10/30.IV.2015, Xihuangshun legit; 3 females, idem,

except V.2014; the paratypes are preserved in Ivan

Rapuzzi collection.

Description of Holotype male. Length in-

cluding mandibles: 41 mm, maximum width of

elytra: 13 mm (Fig. 4). Upper surface metallic,

dull; head green; pronotum and side of elytra gold-

green; disc of elytra olive green; primary and

secondary intervals of elytra black. Ventral side of

pronotum and epipleura green, metallic, abdomen

dark violet; appendix black. Head elongate; surface

strongly punctured, frons convex and punctured;

clypeus very sparsely punctured; clypeus fovea

deep and punctured. Mandible long, sickled shape.

Palps long with the apical segment strongly dilated;

Three newsubspecies of Carabus (Coptolabrus) and taxonomic changing on some Carabus from Far East of Russia 13

Figures 1-3. Carabus ( Coptolabrus ) smaragdinus losevi n.

ssp. holotype male. Fig. 1: holotype. Fig. 2: holotype male

aedeagus: median lobe in lateral view. Fig. 3: idem, apex

in dorsal view.

Figures 4-6. Carabus ( Coptolabrus ) elysii wangguofeni n.

ssp. holotype male. Fig. 4: holotype. Fig. 5: holotype male

aedeagus: median lobe in lateral view. Fig. 6: idem, apex

in dorsal view.

penultimate segment of labial palps bi-setose.

Pronotum of hexagonal shape, transverse (1.21

times as long as broad); base of pronotum large;

sides quite rounded, marginated, bent upwards;

basal lobes large and rounded, protruding its base;

surface of pronotum densely and shallow punc-

tured. Elytra oval; disc convex; mucrones short;

sculpture triploid heterodyname type: primary

tubercles rounded and close; secondary smaller and

rounded; tertiary forming grains strongly rough;

ground roughly sculptured. Legs quite short. Male

aedeagus (Figs. 5,6).

Variability. Very variable in colour: green,

bluish-green, blue, golden-green; the margins often

differ from the discs of pronotum and elytra; colour

of head and pronotum often contrasting with that of

elytra. The colour always has cold tints. The length

of the body ranges from 37 mm to 41 mm for the

males and from 40 mm to 44 mm for the females.

One female specimens has the sculpture of elytra

with tubercles more elongate.

Etimology. The beautiful new Coptolabrus

taxa is very cordially dedicated to Mrs. Wang Guo-

fen (Shanghai, China) wife of Mr. Xi Huangshun.

The co-author of this new subspecies is Huangshun

Xi from Shanghai, China

Remarks. From Southern Anhui several Copto-

labrus taxa are known:

Carabus ( Coptolabrus ) elysii elysii Thomson,

1846: Ngang-Wei, Anking (= Anhui, Anqing)

(Hauser, 1921);

Carabus ( Coptolabrus ) elysii connectens

Hauser, 1912: Ngang-Wei, sudlicher Teil (= Anhui,

Southern part) (Hauser, 1921);

Carabus ( Coptolabrus ) elysii anhweiensis

Hauser, 1932: Anking (= Anqing) (Hauser, 1932a

loc. typ.; 1932b). Very close to C. elysii connectens

it is considered as a synonym by Brezina (2003);

Carabus ( Coptolabrus ) lafossei tungchengensis

Li, 1993: Tongcheng Xian, Longming, Shanling,

locus typicus (Li, 1993);

Carabus ( Coptolabrus ) lafossei dabieshanus

Imura, 1996: Anhui: Dabie Shan, Yuexi, Mt.

Miaodaoshan, locus typicus (Imura, 1996); Hetupu

(Deuve, 1997); Qianshan Xian, Tianzhu Mt. (Imura,

1996); Qian Shan; Jiuhua Shan; Baima Jian

Ivan Rapuzzi

(Kleinfeld, 1997). Very close to C. ( Coptolabrus )

lafossei tungchengensis it is considered as a syn-

onym by Brezina (2003)

Carabus ( Coptolabrus ) lafossei jingdensis

Deuve et Li, 2006: Anhui, Jingde Xian, Junle,

30°20’N; 118°30’E, locus typicus (Deuve et Li,

2006).

From the adjacent area were described:

Carabus ( Coptolabrus ) lafossei tiantai Klein-

feld, 1997: NE-Hubei: Hong’an, Mt.Tiantai,

31:23N/114:37E, locus typicus (Kleinfeld, 1997);

Carabus ( Coptolabrus ) lafossei pseudocoelestis

Kleinfeld, 1999: N-Hubei, Shuizhou, Dahong Mt.,

3 1 :29N/1 12:58E, 1200 m, locus typicus (Kleinfeld,

1999);

Carabus ( Coptolabrus ) elysii pulcher Kleinfeld,

1997: S-Henan, S of Xinyang, Jigong Shan,

31:49N/114:06E, locus typicus (Kleinfeld, 1997).

The closest form is C. elysii pulcher from which

the new subspecies is easily distinguished by the

following characters: smaller size, very different

colour with domination of cold tints; larger pro-

notum with smoother sides (less angulate); more

convex elytra; shorter elytral mucrones; primary

intervals forming smaller and nearly perfect

rounded tubercles.

From C. elysii elysii and C. elysii anhweiensis

the new subspecies differs by: larger size; more

elongate and slender body shape; hexagonal pro-

notum; rounded and raised primary tubercles

(smoother in C. elysii elysii and C. elysii anhweien-

sis); longer elytral mucrones.

The range of the new subspecies is geograph-

ically very close to that of C. lafossei dabiesanus

but very easily distinguishable by several strong

characters: different colour (in C. lafossei dabies-

anus constantly with black elytra and dark blue

elytra margins, head and pronotum); more trans-

verse and less angulate pronotum; upper surface of

head and pronotum strongly punctured (smooth in

C. lafossei lafossei ); different sculpture of elytra

and shorter mucrons of elytra.

From C. lafossei tiantai, C. lafossei pseudoce-

lestis and C. lafossei jingdensis the new taxon has

all the distinctive characters of the species that

permit to separate C. elysii elysii from C. lafossei

lafossei. Carabus lafossei tiantai and the new sub-

species show, in part, the same colour.

Carabus ( Coptolabrus ) ignigena tenuitarsatus

n. ssp.

Examined material. Holotype: male, China,

Chongqing province, Pengshui county, Mt.

Heimending, local collector legit; preserved in the

author’s collection. Paratype: 1 male, China,

Chongqing province, Pengshui county, Mt.

Heimending, local collector legit; the paratype

is preserved in the author’s collection.

Description of holotype male. Small size

and very thin shape for the species, length includ-

ing mandibles 38.5 mm; maximum width of elytra

11.8 mm (Fig. 7). Upper surface metallic, rather

mat; head with supra antennary ridges green; pro-

notum with sides gold green, disk darker; elytra

uniformly green, sides very shine, brilliant;

primary and secondary intervals black. Ventral

face of head black; ventral face of pronotum and

epipleura dark green, metallic; abdomen black

with violet shades, metallic; appendix black. Head

long and very slender; surface of head densely

punctured, frons very convex. Mandibles elong-

ate. Eyes quite small and slightly salient. Palpi

long with the apical segment strongly dilated;

penultimate segment of labial palpi bisetose. Pro-

notum long and very narrow for the species, as

broad as long, sides of pronotum very sinuate,

rounded; hind angles salient and very few pro-

truding behind the base; upper surface flat;

surface of pronotum densely punctured, median

sulcus very superficial. Elytra narrow and very

elongate for the species, ovals; disc convex.

Primary intervals perfectly rounded or slightly

elongate, very prominent; secondary forming

aligned grains; tertiary reduced. Long mucrones.

Legs quite short. First and second protarsal

segments of male slightly dilated with complete

adhesive soles; the third male protarsal segment

not dilated and with very rudimental adhesive

soles.

Male aedeagus (Figs. 8, 9) is characteristic for

the species but quite slender and of narrower

shape.

Variability. No significant variability of the

paratypes

Etimology. The new subspecies is named after

the slightly dilated male protarsal segments.

Three newsubspecies of Carabus (Coptolabrus) and taxonomic changing on some Carabus from Far East of Russia 15

Remarks. As expected the new taxa is morpho-

logically close to the northern most subspecies of

C. ignigena : C. ( Coptolabrus ) ignigena cristiano-

fonti Deuve et Font, 2008 and C. ( Coptolabrus )

ignigena tongrenensis Deuve et Li, 2006.

From C. (C.) ignigena cristianofonti, that it is

the closest form, it is easily distinguished by the

following characters: slender shape of head and

pronotum; sides of pronotum sinuate but not

angled; much elongate elytra with primary intervals

more relieved; protarsal segments of male slightly

dilated, the third segment not dilated and with very

rudimental adhesive soles. From C. (C.) ignigena

tongrenensis the new subspecies is distinguished by

the following characters: smaller size; slender shape

of head and pronotum; primary intervals of elytral

sculpture more prominent; shorter legs; protarsal

segments of male slightly dilated, the third segment

not dilated and with veiy rudimental adhesive soles.

Up to now the new subspecies is the northernmost

population of the whole range of C. ignigena and it

is the first record of the species for the Chongqing

province.

Figures 7-9. Carabus ( Coptolabrus ) ignigena tenuitarsatus

n. ssp. holotype male. Fig. 7: holotype. Fig. 8: holotype male

aedeagus: median lobe in lateral view. Fig. 9: idem, apex

in dorsal view.

Taxonomic notes

Recently Sundukov (2013) established as syn-

onyms four Carabus subspecies described from the

Peter the Great Gulf Islands, Vladivostok area, Far

East of Russia: C. (Morph ocarabus) hummeli

smaragdulus Kraatz, 1878 = C. (M.) hummeli

vladobydovi Obydov, 2007); Carabus (Aulono-

carabus ) gossarei gossarei Haury, 1879 = C. (A.)

gossarei mareschii Rapuzzi, 2010; Carabus

(Megodontus) vietinghoff bowringi Chaudoir, 1 863

= C. (M.) vietinghoff rugicolor Rapuzzi, 2010 and

C. ( Coptolabrus ) smaragdinus mandschuricus

Semenov, 1898 = C. (C.) smaragdinus robinzoni

Rapuzzi, 2010. For the significant morphological

characters and the perfect isolation under insular

conditions all these taxa will be resurrect:

- Carabus (Morphocarabus) hummeli vladoby-

dovi Obydov, 2007 stat. resurr. Described from

Popov Island (Obydov, 2007) C. hummeli vladoby-

dovi has good morphological characters that permit

to separate it from the populations from the main-

land as well as from C. hummeli putyatini Rapuzzi

(2012) from Putyatin island. Carabus hummeli

vladobydovi differs from all the other known hum-

meli subspecies for its veiy peculiar coloration:

violet-pink or red-pink pronotum, pink with gold or

green shades elytra and purple margins.

- Carabus (Aulonocarabus) gossarei mareschii

Rapuzzi, 2010 stat. resurr. Described and known

only from the Askol’d Island C. gossarei mareschii

is easily separable from C. gossarei gossarei by

several characters: larger size and more developed

elytra of ovate-elongate shape. The pronotum is less

punctate with larger and dipper basal impressions.

Elytral sculpture with less interrupted and less

prominent primary intervals. Male aedeagus longer

and larger with the median lobe more developed.

- Carabus (Megodontus) vietinghoffii rugicolor

Rapuzzi, 2010 stat. resurr. Described from Reyneke

Island it is one of the most distinctive subspecies of

C. vietinghoffii. It is easily distinguished from C.

vietinghoffii bowringi by significant and constant

characters: in general bigger and stronger shape;

very different colour: upper surface dark red to

black-violet, rather mat, margins of elytra of the

same colour. Male aedeagus differs for: in lateral

view the median lobe is more developed and the

apical lobe is longer; apex in frontal view curved

on the left.

Ivan Rapuzzi

- Carabus ( Coptolabrus ) smaragdinus robinzoni

Rapuzzi, 2010 stat. resurr. Described from Reyneke

Island it differs from C. smaragdinus mandschuri-

cus by the following characters: smaller size;

slender and flatter shape; pronotum as broad as

long, not transverse; stronger elytral sculpture;

apical lobe of male aedeagus longer and slender. It

is interesting to note that C. smaragdinus robinzoni

is very constant in his type locality.

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Biodiversity Journal, 2016, 7 (1): 17-20

On the presence of the Andaman lobster, Metanephrops

andamanicus (Wood-Mason, 1891) (Crustacea Astacidea

Nephropidae) in Palabuhanratu bay (S-Java, Indonesia)

Yusli Wardiatno 1 *, AgusAlim Hakim 1 , Ali Mashar 1 , Nurlisa Alias Butet 1 , LukyAdrianto 1 &Achmad Farajallah 2

'Department of Aquatic Resources Management, Faculty of Fisheries and Marine Science, Bogor Agricultural University, Kampus

IPB Darmaga, Bogor 16680, West Java, Indonesia.

department of Biology, Faculty of Mathematics and Natural Sciences, Bogor Agricultural University, Kampus IPB Darmaga,

Bogor 16680, West Java, Indonesia.

*Corresponding author: email: yusli@ipb.ac.id

ABSTRACT The first Andaman lobster, Metanephrops andamanicus (Wood-Mason, 1891) (Crustacea

Astacidea Nephropidae) record from south of Java waters, part of Indian Ocean is reported

in this paper. A total of 3 specimens were collected at a fish harbor in Palabuhanratu bay in

May 2015. Morphological characters are illustrated and described. This finding enhances the

biodiversity lists of Indonesian crustaceans.

KEY WORDS Andaman lobster; Decapoda; Indian Ocean; Java Island; morphological descriptions.

Received 23.01.2016; accepted 02.03.2016; printed 30.03.2016

INTRODUCTION

The lobsters of the family Nephropidae are

deep-sea forms and commonly found at depths

from 150 to more than 1893 m (Chang et al., 2014).

In general nephropid lobsters are bottom-dwellers

with a preference for soft sediments, and living

within their self-made burrows is the biological

behavior in some species (Chan, 1998).

The family Nephropidae currently includes 57

species belonging to 14 genera (Holthuis, 1991;

Chan, 1998; Tiirkay, 2001; Chan, 2010; Ahyong

et al., 2012; Chan et al., 2014). Previously, genus

Metanephrops Jenkins, 1972 was divided into four

morphological groups, namely thomsoni (Bate,

1888), binghami (Boone, 1927), arafurensis (De

Man, 1905) and japonicus (Tapparone-Canefri,

1873) (Holthuis, 1991). However, with molecular

analysis approach, Chan et al. (2009) refuted mono-

phyly of the arafurensis and thomsoni groups.

Among the groups, japonicus has the highest num-

ber of species.

Some of the current researches on Indonesian

crustaceans, reported the presence of first records

species, especially hippoid crabs, such as Albunea

symmysta (Linnaeus, 1758) (Mashar et al., 2015),

Hippa marmorata Hombron et Jacquinot, 1846)

(Wardiatno et al., 2015), Hippa adactyla Fabricius,

1787 (Ardika et al., 2015).

This paper presents a new record of the Anda-

man lobster, Metanephrops andamanicus (Wood-

Mason, 1891) from south of Java, Indonesia.

MATERIAL AND METHODS

Three M. andamanicus specimens were collec-

ted in May 2015, from a fish harbor in Palabuhan-

ratu bay, District Sukabumi, South of Java,

Indonesia (Fig. 1). They were preserved in 96%

Yusli Wardiatno etalii

alcohol and taken to the laboratory for analysis.

Identification was based on the morphological

characters using taxonomic key books from FAO

(Holthuis, 1991; Chan, 1998). One example of the

specimens is presented in figure 2. The specimens

were lodged in the Department of Aquatic Re-

sources Management, Bogor Agricultural Univer-

sity, Indonesia.

RESULTS

SYSTEMATICS

Infraorder ASTACIDEA Scho Its et Richter, 1995

Family NEPHROPIDAE Dana, 1852

Genus Metanephrops Jenkins, 1972

Metanephrops andamanicus (Wood-Mason, 1891)

Examined material. 3 males: carapace length

51.04, 55.97, and 57.20 mm, total length 141.82,

149.34, and 154.23 mm, weight 65, 78, and 88

gram. 17.V.2015, Palabuhanratu fishing harbor,

South of Java, Indonesia.

Diagnosis. Carapace ofM andamanicus smooth

between ridges and large spines (Fig. 3). Eyes large

and black, postrostral carinae with three teeth (Fig.

4). Surface of abdominal tergites conspicuously

sculptured; raised parts of dorsal surface of

abdominal somites smooth and naked; second to

fifth abdominal somites with marked dorsomedian

carina, flanked by pair of conspicuous longitudinal

grooves (Fig. 5). Fifth abdominal somite without

distinct spines on carina separating tergite from

pleuron. Dorsomedian carina of sixth abdominal

somite without submedian spines. Spine in middle

of lateral margin of sixth abdominal somite short,

tip far from posterolateral margin of somite. Chelae

of first pereiopods heavily ridged and spinulose,

without large spines; no prominent basal spine on

outer edge of movable finger of large chela. Inner

margin of merus of first pereiopod weakly spinu-

lose (Fig. 6).

Distribution. Indo-West Pacific region: East

Africa (Tanzania, Zanzibar, Kenya and Somalia),

the Andaman Sea, the South China Sea (not includ-

ing the Philippines), and Indonesia, and perhaps

also Papua New Guinea (Holthuis, 1991; Chan,

1998; Tshudy et al., 2007).

DISCUSSION

Holthuis (1991), Chan (1998) and Tshudy et al.

(2007) revealed the distribution of M. andamanicus

in Indo-West Pacific region from eastern Africa to

the Andaman Sea, the South China Sea (but not the

Philippines), Indonesia, and perhaps also Papua

New Guinea. According to the IUCN Red List of

Threathened Species the occurence of the species

in Indonesia was reported in Kalimantan, Sumatra

and Sulawesi. However, in a short survey on May

2015 we could find this species in Palabuhanratu

bay located in south of Java and it is a new record.

Some lobster species were previously reported from

several parts of Indonesia, and they were highly

valuable species, such as Panulirus penicillatus

(Olivier, 1791) (Chow et al., 2011; Kalih, 2012;

Abdullah et al., 2014), Linuparus somniosus Berry

et George, 1972 (Wowor, 1999), P. versicolor

(Latreille, 1804) (Ongkers et al., 2014), P. homarus,

(Linnaeus, 1758), P. longipes (A. Milne-Edwards,

1868), P ornatus (Fabricius, 1798), Parribacus

antarcticus (Lund, 1793) (Kalih, 2012). Con-

sequently, the presence of M. andamanicus in

Palabuhanratu bay increases the list of lobster biod-

iversity in Indonesian waters.

In fishery point of view, some species of genus

Metanephrops have commercial potential and

become the deep water fishery targets lobster and

catched by trawl; those species are M. mozambicus

(Macpherson, 1990) in Africa (Fennessy &

Groeneveld, 1997; Groeneveld & Everett, 2015),

M. thomsoni in northern part of the East China Sea

(Choi et al., 2008), M. challengeri (Balls, 1914) in

New Zeland (Tuck et al., 2015), M. andamanicus

in east coast of Southern Africa (Mutagyera, 1979).

In the fish market located in Palabuhanratu bay,

south of Java M. andamanicus can be regularly

found indicating its economical value in the area.

As fishery target, biological information of this

species is needed for its sustainable management.

Exploration in biological aspects of M. andamani-

cus is open for future studies.

AKNOWLEDGEMENTS

The research was funded by Indonesian Gover-

nment through Directorate General of Higher Edu-

cation, Ministry of Education and Culture from

Andaman lobster, Metanephrops andamanicus (Crustacea Nephropidae) in Palabuhanratu bay (S-Java, Indonesia) 19

Figure 1. Map of Java Island with the insert map of Indonesia. Palabuhanratu bay is indicated by open-square and pointed

with an arrow. Figure 2. Metanephrops andamanicus (male) collected from a fish harbor in Palabuhanratu Bay, south of

Java, Indonesia. Figures 3-6. Metanephrops andamanicus , south of Java (Indian Ocean), male (carapace length 55.97 mm).

Fig. 3: carapace, lateral view. Fig. 4: carapace, dorsal view. Fig. 5: abdomen, dorsal view. Fig. 6: first pereiopod. Scale bars

10 mm.

Yusli Wardiatno etalii

Fiscal Year 2015. The authors wish to thank to Mr.

Agus for his assistance during specimen collection.

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offshore trawl fishery for crustaceans on the east

coast of South Africa. Fisheries management and

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Biodiversity Journal, 2016, 7 (1): 21-24

Does local knowledge change after a species long term ab-

sence? The case of giant river otters Pteronum brasiliensis

Gmelin, 1 788 (Carnivora Mustelidae)

O. Eric Rami'rez-Bravo

Departamento de Ciencias Qiumico-Biologicas, Universidad de las Americas, Puebla, Santa Catarina Martir, SinNumero, Cholula,

Puebla; e-mail: ermex02@yahoo.com

ABSTRACT Public participation could be useful to determine species presence and ecological aspects,

however it is possible that local knowledge of species whose populations had suffered a

decrease could have changed. To determine current knowledge of giant river otter, Pteronura

brasiliensis Gmelin, 1788 (Carnivora Mustelidae), we undertook a preliminary assessment

based on 35 interviews preformed between June and August 2014 with natural resources users

in the Pacaya-Samiria Reserve (Peru) aimed to determine the presence, feeding habits, re-

production periods, and threats. It was possible to determine that current knowledge cor-

respond with available information in literature thus, I consider that it is possible to use public

participation in cases of little known species that are recovering.

KEY WORDS Public monitoring; Pteronura', Pacaya-Samiria Reserve; endangered species.

Received 03.01.2016; accepted 31.01.2016; printed 30.03.2016

Habitat loss, fragmentation, and degradation,

along with other human-related causes have

put most ecosystems and the species that inhabit

them at risk (Myers, 1988). Therefore, conserva-

tion strategies rely on the prioritization of areas that

are key for the long term survival of many species.

Such prioritization becomes more important in

areas with high biodiversity; and even more so

when these areas are related with high human dens-

ities, where actions are needed sooner rather than

later (Sanderson et al., 2002). However, information

on both ecosystems and species at regional level is

often missing making it necessary to generate a

strategy that could help to increase knowledge at

this level. It has been proposed that this kind of

information can be obtained from the general public

as a first step for management; as scientific research

is usually limited in space and time (i.e. short term

studies in a specific site) making some changes to

go either unperceived or identified after a huge gap

of time (Scholte, 2011). Just to mention, in Mada-

gascar local knowledge has been used to shape

distribution of carnivore species (Kotschwar et al.,

2015) and in Zimbabwe to determine population

trends of different carnivore and game species

(Gandiwa, 2012).

However, there is not enough information on

how local knowledge and perception changes after

a charismatic species disappears from a region such

as in the case of the giant river otter, Pteronura

brasiliensis Gmelin, 1788 (Carnivora Mustelidae).

This species was once distributed in most fresh-

water streams of South America, from Venezuela to

Argentina (Eisenberg, 1989). Its numbers have

O. Eric Ramirez-Bravo

decreased significantly up to the extent that some

populations have disappeared from its former range

due hunting and habitat loss (Carter & Rosas, 1997;

Recharte & Bodmer, 2010). The species is currently

listed as endangered by the red list (IUCN, 2016)

with a projected population decrease of about 50%

within the next twenty years (Shostell & Ruiz-

Garcia, 2013). Fortunately, due a ban on hunting

and a decrease on its commercial demand in Peru,

giant river otter populations have increased in

certain areas such as in the Yavari River (Recharte

& Bodmer, 2010) and in the Pacaya-Samiria Na-

tional Reserve in Pern (Groenendijk et al., 2001).

The species is important at local level as it is con-

sidered a top predator and due its potential as a bio

indicator as it is especially sensitive to disturbance

and resource availability, preferring conserved areas

with good fish stocks (Carter & Rosas, 1997; Groen-

endijk et al., 2001; Recharte & Bodmer, 2010). Un-

fortunately, scientific information of the species

along its range is scarce except for a few areas (e.g.

Madre de Dios: Flajek & Groenendijk, 2006) and

Pacaya-Samiria National Reserve (Groenendijk et

al., 2001). However, there is not enough informa-

tion on how local knowledge and perception

changed after the long term absence of the species

in the region. Thus, it is important to determine if

users of natural resources are aware of the giant

Figure 1. Pacaya-Samiria National Reserve in

Northeastern Peru.

river otter presence and ecology in order to include

their knowledge in management plans.

I undertook semi structured interviews with the

natural resource users of the Pacaya-Samiria Na-

tional Reserve in northeastern Peru to assess their

actual knowledge on giant river otters (Fig. 1). The

Pacaya-Samiria National Reserve is located in the

Amazon Basin and is considered the largest protec-

ted area of flooded forest in the Amazon with

20,800 km 2 (Bodmer et al., 2011). Its average

annual rainfall is 2000-3000 mm and a mean tem-

perature between 20 and 33°C (Bodmer et al.,

2011). The reserve and its buffer zone have 203

rural settlements; most of them (89%) are small

villages with less than 500 inhabitants located on

the borders of the Maranon and Ucayali/Puinahua

rivers (Gonzalez, 2003). The households in the area

include people of mixed origins (mestizos), natives

from the ethnic groups Cocama-Cocamilla and

Shipibo-Conibo, whose major economic activities

include fishing, agriculture, game hunting, and

extraction of forest products (Gonzalez, 2003).

Some communities have been actively involved in

groups of natural resources management in the

Reserve (Puertas et al., 2000; Piana et al., 2003). I

concentrated my efforts in the Samiria River, a

black water river preferred by giant river otters

(Carter & Rosas, 1997). I used the vigilance point

2 known as “Tacshacocha” as interviewing place,

since visitors and members of the community man-

agement groups have to register when travelling

upriver.

I made a total of 35 interviews between June and

August 2014. The survey consisted in a set of 22

questions aimed to determine the presence of the

species, habitat preferences, reproduction patterns

and potential threats to giant river otters. Inter-

viewed persons belong to five different communit-

ies: Leoncio Pradro (47%), San Martin de Tipishca

(29%), San Carlos (12%), Santa Rita (3%) and

Victoria (9%). On average, the interviewees were

41 years old. Half of them (50%) belong to one of

the local community-based conservation groups

which were formed aiming for the sustainable use

of natural resources as well as turtle management

and conservation; they also serve as guides for

scientific groups (19%). Sixty-nine percent of the

interviewees typically use the reserve throughout

the year, another 22% use it only during the dry

season. Therefore, I considered that responses were

based on field experience.

Does local knowledge change after a species long term absence? The case of giant river otters Pteronura brasiliensis 23

Locals stated that otters can be observed

throughout the year (40% of interviewees), but that

are easier to detect during the dry season (43%).

These observations can be explained because their

movements are concentrated to lakes and rivers

during the dry season, while they move to flooded

forests and small creeks during the wet season

(Hajek & Groenendijk, 2006), becoming scattered

and harder to detect. Moreover, 53% of the respond-

ents identified both river and rainforest as preferred

habitats and another 41% considered river as the

main one. Locals also reported diurnal observations

(54% of interviewees), especially during the early

hours of the morning (34%). This is supported by

Carter & Rosas (1997), who identified giant river

otters as diurnal. Interviewees reported that the main

activities conducted by the river otters were playing,

feeding, fishing, and vigilance, which correspond

with previous reports about their daily activity

(Carter & Rosas, 1997; Hajek & Groenendijk, 2006).

The diet of the giant river otter varies with

habitat type and species diversity in the area (Hajek

& Groenendijk, 2006). Fish are the main diet

component (Carter & Rosas, 1997; Hajek &

Groenendijk, 2006), but other groups such as mam-

mals and crabs have also been recorded (Hajek &

Groenendijk, 2006). Preferred fish consumed by the

giant river otter belong to the suborders Characoidei

(characins), Percoidei (perch) and Siluroidei (cat-

fish) (Carter & Rosas, 1997). Accordingly, inter-

viewees identified fish of different species such as

carachama ( Pseudorinelepis spp.) and different

types of piranha (Characoidei) as the main diet

component of the species.

Knowledge about reproduction and cub devel-

opment tended to vary. All interviewees considered

that otters reproduce in the Samiria River, but only

80% have seen cubs. Eighty-eight percent of locals

reported that otters breed during the dry season

(May-September), which corresponds with obser-

vations in other areas (Duplaix, 1980; Hajek &

Groenendijk, 2006). Although litter size is known

to vaiy between one and five cubs per season

(Carter & Rosas, 1997; Hajek & Groenendijk,

2006), locals have little knowledge about this fact

as just 29% consider that the species had just one

cub per year. It is noteworthy that interviewees

claimed they cannot differentiate pregnant from

non-pregnant females (62%); but they can differen-

tiate adults and cubs by size (76%).

The success on conservation measures that have

resulted in river otter population increase (Recharte

& Bodmer, 2010) has been noted by interviewees,

where 91% considered that the otter population was

growing. Otter population increases may lead to a

raise in human-otter conflicts. In fact, 49% of them

considered the species as harmful to fishing nets

and fish stocks, 46% stated that locals are afraid of

the giant river otter, and 21% reported known

previous attacks to humans. This corresponds with

observations made by Carter & Rosas (1997),

where people in recently colonized areas of the

Amazon forest feared giant river otters. Inter-

viewees suggest fears result from lack of know-

ledge about the species. Regardless, 91% of the

interviewees claimed local communities know that

the giant otter is protected. Also, 91% of the re-

spondents considered the giant otter as an important

and emblematic species in the area because it

represents the reserve and is part of the ecosystem.

This is supported by the fact that 92% of them

reported that this species is no longer hunted in the

area as it is extremely prohibited, except occasion-

ally when cubs are captured to be kept as pets or to

be sold to zoos, as previously reported (Duplaix,

1980; Carter & Rosas, 1997).

Our results indicate that, despite the species is

still at low densities and was carried almost to the

point of local extinction, local people who visit this

reserve are well informed about the presence, eco-

logy and distribution of the species. The latter can

be confirmed by comparing published information

from zoos and field observations about the species

with local knowledge. In the specific case of the

giant river otter, results showed that it is possible to

use local knowledge as baseline information to

generate conservation projects and community

projects. Thus, it can be considered that for regions

with limited information about species and eco-

systems it is possible to use public participation,

especially of community conservation groups,

where available, in order to generate management

plans or even monitoring programs.

ACKNOWLEDGEMENTS

I would like to thank the Servicio Nacional de

Areas Naturales Protegidas (SERNANP) and to

Fundamazonia for all their support during the field

work.

O. Eric Ramirez-Bravo

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Biodiversity Journal, 2016, 7 (1): 25-32

Patterns of Butterfly distribution in Alabama, USA (Lepidop-

tera)

Xiongwen Chen* &Tuo Feng

Department of Biological and Environmental Sciences, Alabama A & M University, Normal, AL 35762, USA

* Corresponding author, e-mail: xiongwen.chen@aamu.edu

ABSTRACT Butterflies (Lepidoptera) are an iconic group of insects and are emphasized in ecological

research and biodiversity conservation due to the role in ecological processes. Alabama (USA)

has 139 species of butterflies in 6 families based on the previous field surveys. In this study

the information from the previous field survey was analyzed with environmental information

for the general patterns across 67 counties of Alabama. The results indicate that the counties

with the higher butterfly species are mainly within the metropolitan areas; power-law

relationship exists between average species number and occupied county number; there is

higher number of butterfly species at counties with either the highest or the lowest forest

coverage; there is positive correlation between latitude and butterfly species density; counties

with the lowest or the highest species number usually have higher standard deviations in

annual air temperature or precipitation; butterflies with a big distribution area do not have

significantly bigger wing size in comparison to ones with a small distribution area; and with

the increase of latitude, the average wing size of butterflies increases. The results provide

new understanding for the butterfly distribution at a regional level.

KEY WORDS Alabama; butterflies; climate; latitude; species number; wing size.

Received 02.02.2015; accepted 21.03.2016; printed 30.03.2016

INTRODUCTION

The Butterflies (Lepidoptera) play an important

role in ecosystems and conduct ecological services

(Tiple et al., 2006), such as pollination and herbi-

vores. Butterflies are considered as good ecological

indicators of the health of some terrestrial eco-

systems (New, 1991; Thomas, 2005; Bonebrake et

al., 2010). The beautiful color of butterflies and

unique features also provide recreation resource to

human society. Butterflies are greater sensitive than

other taxonomic groups to reflect human disturb-

ance (Thomas, 2005). Monitoring butterfly species

at an area can indicate human mismanagement and

pollution (Wilson, 1997). Due to climate change,

altered land use (e.g., habitat loss), and pollutants

(e.g., pesticides and herbicides), the butterflies are

in declining, such as in Europe (van Swaay et al.,

2006). The loss of native plants, which are food for

leaf-eating caterpillars and nectar sipping adult

butterflies, by the replacement of exotic invasive

species has devastated butterflies. Butterflies are an

iconic group of insects and are emphasized in eco-

logy and biodiversity conservation.

The state of Alabama (USA) has 139 species of

butterflies in six families (Hesperiidae, Papilionidae,

Pieridae, Lycaenidae, Riodinidae, and Nymphal-

idae). The information of distribution, habitat, food,

life history and wingspan for all 139 species is listed

in the book “Butterflies of Alabama” based on the

Xiongwen Chen &Tuo Feng

field records (Howell & Charny, 2010). This in-

formation provides an opportunity for integrated

study, such as analyzing patterns of butterfly distri-

bution and uncovering the related factors.

One of the important features of butterflies is

their wingspan or body size. Body size is a key trait

related to the life history of individuals, the wing

size (a proxy for body size) of butterflies signi-

ficantly decreased in response to warmer summers

in high arctic area (Bowden et al., 2015). Based on

the Bergmann’s rule, larger individuals occur at

higher latitudes and in colder environments (Sand

et al., 1995). Similarly, smaller adult size should be

in higher temperatures or southern area. Although

both Bergmann’s rule and the temperature-size rule

predict larger individuals in colder environments,

however, the opposite pattern also reported (Blanck-

enhorn & Demont, 2004; Angilletta, 2009). Several

ways were proposed that temperature may affect

body size.

Two mechanisms related to external temperat-

ures may impact body size in different directions.

First, the metabolic rates increase with warmer

temperatures, organisms become smaller if they

cannot offset energy losses under high metabolic

costs.

Second, rising temperatures in seasonal environ-

ment make longer growing seasons, which may let

organisms grow larger.

The extended seasons could also low plant-food

quality during late season (Awmack & Leather,

2002). Baguette & Stevens (2013) suggested that

wingsize of butterflies is positively related to min-

imum area requirements. Butterflies with big wing

size should have a big distribution area. Host-range

relationship may be primarily determined by eco-

logical and population-genetic factors (Barrett &

Heil, 2012). For example, generalists should be

promoted by volatile host communities, while

specialists should be favored in places where host

communities are stable (Jaenike, 1990). This means

that harsh and volatile climate in a temperate region

could have more generalists and favorable and

static climate have more specialists. For the distri-

bution area, plants are food and habitats to butter-

flies, forests harbor between 50% and 90% of

Earth’s terrestrial species including diverse of plant

species (World Resources Institute et al., 1992),

there should have more butterfly species in forest

areas than at less or none forest areas.

It is also known that butterflies are sensitive to

habitat fragmentation (Ockinger et al., 2010), so

with the increased landscape fragmentation in one

region, such as in a metropolitan area, butterfly

species number may decrease. Therefore, the goal

of this study is to use the collected butterfly inform-

ation from Howell & Charny (2010) combined with

climate and environmental information to indicate

the general patterns of butterfly distribution in the

state of Alabama and test the above hypotheses. The

specific objectives include (i) distribution pattern

of butterfly species along latitude; (ii) relationship

between wing size of butterflies and latitude; (iii)

relationship between butterfly species number and

plant species number and forest cover at county

level; and (iv) relationship between butterfly

species number and urbanization at the county

level. This study will provide understanding of the

patterns of butterfly distribution in Alabama.

MATERIAL AND METHODS

Study area

Alabama is located in the southern region of

USA. and between the southern foothills of the

Appalachian Mountain Range and the Gulf of

Mexico. There are total 67 counties in Alabama

(Fig. 1). Since the State of Alabama runs roughly

from 31° to 35°N, the climate in the southern part

is warmer than the northern part. Northern Alabama

has a warm, humid, temperate climate, and the

south has a subtropical climate. Summers are hot

and humid with an average high temperature around

33°C; winters are typified by a series of cold fronts.

The annual precipitation varies from 150 cm to 162

cm in the northern part and 180 cm to 195 cm in the

southern part (Carter & Carter, 1984). Based the

inventory data from Alabama Forestry Commission

(www.forestry.state.al.us), 70% of the state is

covered by forests. Due to mild climate and hetero-

geneous landscape, Alabama has great species

diversity. The county level is selected in this study

because most data are only available at this level.

Data

Butterflies: the butterfly information is from the

book of Howell & Charny (2010), which was based

Patterns of Butterfly distribution in Alabama, USA (Lepidoptera)

on the year-round field observations from 2001 to

2009 by the authors, their students and colleagues.

Photographic survey which is broadly applied for

biodiversity research (e.g, McGrath, 2015) was

conducted at each county. The spatial resolution of

butterfly distribution is at county level, which

means the distribution covers the entire county as

long as this butterfly species is found at one loca-

tion. More information can be found in Howell &

Chamy (2010). In this study, the information of

distribution and the average wing size is used.

Climate: the climate information is from local

weather stations in each county from 2001 to 2009.

Plants and forest: the information of plant

species diversity in each county of Alabama is from

http://www.alabamaplants.com. The forest cover-

age (%) in each county at that time is from Chen

(2009).

Human population: the human population at

each county during the corresponding time period

is obtained from Alabama Quick Facts at the

USCensus Bureau (http://quickfacts.cencus.gov/

qfd/index).

1 11 -26 Number

| 19 -49

I 50-79

0 30 60 120 Kilometers

Li-i-i J . l.L-lJ

Statistical method

Standard deviation was used to characterize the

fluctuation in air temperature and precipitation in

each county. The commonly used least squares

technique was used in correlation analysis and T-

test of SAS (SAS Institute Inc., NC, USA.). The

statistical test was considered significant at p<0.05.

Data aggregation was applied when the statistical

test on individual county data was not significant,

but the trend might exist, such as the bin of [0, 10],

[11, 20],... [70, 80] was applied for the rank of

butterfly species number while testing power-law

between the average species number and appeared

county number. The butterfly species density in

each county was estimated by the total butterfly

species number /county area.

RESULTS

Jefferson County has 79 butterfly species, which

is the highest number. The counties with the cat-

egory of highest butterfly species (50-79) include

Madison, Jackson, Tuscaloosa, Jefferson, Ribb,

Shelby, and Baldwin (Fig. 1). These counties are

Figure 1 . The butterfly distribution across the counties of

Alabama (bold lines indicate metropolitan area).

mainly within the metropolitan areas of Hunts-

ville, Birmingham, and Mobile cities. There are six

counties (Choctaw, Coffee, Crenshaw, Dale,

Greene, and Lamar) without any butterflies or with

veiy limited species number. There is a power-law re-

lationship between the average of butterfly species

number and appeared county number (Fig. 2).

The relationship between county size and

butterfly species number is not obvious (Fig. 3).

The correlation between human population in each

county and butterfly species is not significant (p>

0.05) (Fig. 4). The relationship between plant species

number and butterfly species number among all the

counties is not obvious (Fig. 5). There is higher

number of butterfly species at areas with either the

highest or the lowest forest coverage (Fig. 6).

There is positive correlation between latitude

and butterfly species density (Fig. 7). The correla-

tion between the average annual air temperature or

average annual precipitation and species density is

not significant (p>0.05) (Fig. 8), but there is a

general trend of decreased species density with

Xiongwen Chen &Tuo Feng

Figure 2. The correlation between average butterfly

species number and appeared county number.

Figure 5. The relationship between plant species number

and butterfly species number in counties.

▼

5 60

i so

S 40

*-♦—

4 ♦

— $ —

♦♦

444

4 4

♦ 4

4 Tittit

♦ * 2 * ♦ Y

♦♦44

4 "

— *

9.1 9.2

9.3

9.4 9.5 9.6 9.7 9.8

log (countYarea, m')

Figure 3. The relationship between county size and

butterfly species number.

Figure 6. The relationship between forest coverage

and butterfly species number in counties.

Figure 4. The relationship between human population

and butterfly species number among counties.

Figure 7. The relationship between latitude and

density of butterfly species.

Patterns of Butterfly distribution in Alabama, USA (Lepidoptera)

Figure 8. The relationship between butterfly species number

and average annual air temperature (a) and average annual

precipitation (b).

Figure 9. The relationship between butterfly species number

and standard deviation of annual air temperature (a) and

standard deviation of annual precipitation (b).

Figure 10. The relationship between average wingsize of

butterfly and the diameter of the distribution area.

Figure 11. The relationship between latitude

and butterfly wingsize.

Xiongwen Chen &Tuo Feng

increased temperature or precipitation. There is a

pattern that counties with the lowest or the highest

species number have higher standard deviations in

annual air temperature or precipitation (Fig. 9).

The correlation between the average wingsize

and diameter of distribution area at each county

level is not significant (p>0.05). However, after

the data aggregation in wingsize, there is a gen-

eral trend between the average wingsize and the

diameter of distribution area (Fig. 10). The aver-

age wingsize of the broadly distributed species (or

generalists) is 53. 7± 25.7 mm and 51.0 ± 23.7 mm

for narrow distributed species (or specialists). The

difference in wing size between generalists and

specialists is not statistically significant (p> 0.05).

With the increase of latitude, the average wingsize

increases for all species polled over (Fig. 11).

DISCUSSION AND CONCLUSIONS

There are some patterns of butterfly distribution

in Alabama after the integrated analysis with other

information. Some counties have a high species

number, but others have limited species. The

power-law relationship between average species

number and appeared county number is similar to

those with plants and animals in California (Chen

et al., 2006). The phenomena may be related to the

spatial occupying process and tolerance of habitat

for all the species, but the mechanism is not known.

With the increase of county size in area, this does

not necessary lead to the increase in the number of

butterfly species, which means big counties may not

have more butterfly species. The island biogeo-

graphy theory does not apply to butterfly species

here. The counties with higher number of butterfly

species are mainly within these metropolitan areas

(e.g., major cities of Birmingham, Huntsville and

Mobile areas). It seems that the higher number of

butterfly species is related to human population and

land use change, although the correlation between

butterfly species number and human population in

each county is not significant. This is consistent to

that (i) no obvious relationship between butterfly

species number and plant species number among all

counties; (ii) there is high species number at areas

with either the lowest or highest forest coverage.

After comparing the butterfly species diversity in

urban, suburban and rural areas, Mukherjee et al.

(2015) indicated that butterfly species diversity is

related to landscape heterogeneity. Usually there is

higher landscape heterogeneity at the metropolitan

areas due to diverse vegetation pattern under

different land uses from land owners, but relatively

homogeneity landscape in urban and rural areas.

Earlier studies suggested that butterfly diversity is

attributed to plant species (Kuussaari et al., 2007).

But in this study, there is no obvious correlation

between plant species and butterfly species at

county level. These butterfly species may only like

some specific plants for hosting (Howell & Chamy,

2010 ).

Usually in warmer area, such as tropical areas,

there is higher species diversity. However, in this

study the relationship between latitude and butterfly

species is on the opposite. There is higher density

of butterfly species in northern Alabama. This result

is also consistent with that there is a general trend

of decreased species density with increased tem-

perature. The possible cause may be that the rule at

continental (or global) level may not always work

at a regional level. Some additional factors may

attract to butterfly species diversity at a regional

level. Also, in low latitude areas there are high

species number as overall, but not necessary for

butterfly species.

The results in this study also identify that

counties with large fluctuations in annual air

temperature and precipitation have either the

highest or the lowest species number of butterfly.

Under the stable climate condition (e.g., lower

standard deviation in annual temperature or pre-

cipitation) there is an intermediate high number of

butterfly species. The changing climate may

provide more niche space for various butterfly

species if they can tolerate. The degree to which

phenotypic plasticity and adaptation ultimately play

a role under this changing climate remains to be

further studied (Bowden et al., 2015). Bergmann’s

rule, describing the relation between latitudinal

and body size, is confirmed in this study. Our res-

ults indicate that the average wingsize of butter-

fly increases with the increase of latitude in

Alabama.

There are generalists of butterfly with a large

distribution area from the south to north and also

several specialists with limited distribution in Ala-

bama (such as only one county). But the sizes of

their wingspans are not significantly different. This

Patterns of Butterfly distribution in Alabama, USA (Lepidoptera)

result may indicate that butterfly species with big

wingspans may not necessary show greater migra-

tion capacity or the specialists may also be distrib-

uted broadly if resource is suitable. The size of

wingspan may not determine the fate of some

specialist of butterflies under changing environment

which was considered as venerable (Dapporto &

Dennis, 2013).

After analyzing the records of butterfly species

and the environmental factors in Alabama, the

emergent patterns at a regional level appear for the

distribution of butterfly. The uneven distribution of

butterfly species may be related to land use and

climate fluctuations. The species diversity and body

size related with latitude and temperature may

provide helpful information for butterfly conserva-

tion and mitigation under climate change. This

study may provide a background map for study of

butterfly distribution under environmental change

(McGrath, 2015). Periodically monitoring the body

size and distribution of butterfly species and

other biodiversity may be necessary for sustainable

regional development.

ACKNOWLEDGMENTS

This work was partially supported by the

USD A National Institute of Food and Agriculture

Mclntire Stennis project (1008643).

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Biodiversity Journal, 2016, 7 (1): 33-38

First record of a Humpback Whale Megaptera novaeangliae

(Borowski, 1 78 1) in theTyrrhenian Sea (Cetacea Balaenopte-

ridae)

Nicola Maio 1 *, Vincenzo Maione 2 & Riccardo Sgammato 2

'Dipartimento di Biologia, Complesso Universitario di Monte Sant’Angelo, Universita degli Studi di Napoli Federico II, Edificio

7, via Cinthia 26, 80126 Napoli, Italy.

2 Centro Sub Campi Flegrei, Via Miliscola 165, 80078, Pozzuoli, Frazione Lucrino, Napoli, Italy.

^Corresponding author: e-mail: nicomaio@unina.it

ABSTRACT It is reported the sighting of a Humpback Whale Megaptera novaeangliae (Borowski, 1781)

(Cetacea Balaenopteridae) in the Gulf of Pozzuoli, near the coast of Baia (Bacoli, Napoli,

Campania, Southern Italy). This record represents the first in the Tyrrenian Sea, the eighth in

the Italian Seas and the twenty-fourth in the Mediterranean Sea.

KEY WORDS Megaptera novaeangliae', Humpback Whale; sighting; Tyrrhenian Sea.

Received 19.02.2016; accepted 07.03.2016; printed 30.03.2016

INTRODUCTION

The Humpback Whale, Megaptera novaeangliae

(Borowski, 1781) (Order Cetacea, Suborder Mys-

ticeti, Family Balaenopteridae) is a cosmopolitan

species widely distributed and far-ranging migrant,

found in both hemispheres and in all the major

ocean basins. During the winter, at the period of

mating and calving grounds, all the populations mi-

grate to tropical waters, usually near continental

coastlines or island groups; during spring, summer

and autumn they move to productive colder waters

in temperate and high latitudes, where most of the

feeding takes place. In the North Atlantic, during

the summer the Humpback Whale ranges from the

Gulf of Maine in the West and Ireland in the East,

and in the North but not into the pack ice; the

northern extent of the Humpback's range includes

the Barents Sea, Greenland Sea and Davis Strait

(but not the Canadian Arctic), where they occur

mainly in specific feeding areas. During the winter,

the majority of whales migrate to wintering grounds

in the West Indies, and an apparently small number

use breeding areas around the Cape Verde Islands.

In the Mediterranean Sea, the Humpback Whale

is not regularly present; in fact it is considered as

an irregular or occasional “visitor species”, accord-

ing to the Reports of Agreement on the Conserva-

tion of Cetaceans of the Black Sea, Mediterranean

Sea and Contiguous Atlantic Area (ACCOBAMS),

entering the region from the Strait of Gibraltar

(Reeves & Notarbartolo di Sciara, 2006; Notarbar-

tolo di Sciara & Birkun, 2010; Cagnolaro et al.,

2015). Since 1990 the number of observations has

increased and the range of sighting locations has

expanded so as to include both basins of the Mediter-

ranean Sea (Frantzis et al., 2004).

Humpback Whale, Megaptera novaeangliae , is

well known for his long pectoral fms, which can

be up to 4.6 meters in length. The dorsal fin is

Nicola Maio et alii

variable in size and shape, from small triangular

knob to larger sickle-shaped, placed nearly two-

thirds along back. Head and body are black or grey,

white on throat and belly. The adult can measure

up to 17 m.

MATERIAL AND METHODS

We take into consideration the sighting of one

individual photographed in the Bay of Pozzuoli; the

sighting occurred from the Aragonese Castle of

Baia (District of Bacoli Municipality, Province of

Naples) at about 70 m of height. The camera equip-

ment consisted of a Digital single-lens reflex

camera Canon EOS 650D with 75-300mmEF-S

lens mounted.

RESULTS AND DISCUSSION

Here we report the sighting of a Humpback

Figure 1. The locations of sightings of Humpback Whales, Megaptera novaeangliae, in the Italian Seas.

First record of a HumpbackWhale Megaptera novaeangliae in the Tyrrhenian Sea (Cetacea Balaenopteridae)

Figures 2-4. Humpback Whale, Megaptera novaeangliae, recorded near Baia, in the Bay of Pozzuoli, apparently

in good conditions (Photos by R. Sgammato).

Nicola Maio et alii

DATE

LOCATION

EVENT

ANIMALS,

SIZE

SOURCE AND

NOTES

1998, 24 January

Gulf of Oristano (Sardinia)

Sardinian Sea

Sighting

1 (7-9 m)

(Lrantzis et al.,

2004)

2002, 4 August

Senigallia (Province of

Ancona, Marche) Adriatic Sea

Sighting

(Affronte et al.,

2003)

2004, 2 April

Syracuse (Sicily)

Ionian Sea

Accidentally by-caught

and released

1 (about 10 m)

Centro Studi

Cetacei, 2006

2010, 26-28 August

Eastern Ligurian Sea: Versilia

(Prov. of Lucca, Tuscany) Sestri

Levante (Prov. of Genoa,

Liguria)

Repeated sightings of

one individual

1 (about 10- 13m)

(Cagnolaro et al.,

2015)

2011,24 March

Near Savona (Liguria)

Ligurian Sea

Sighting

(Cagnolaro et al.,

2015)

2013, 12 March

Lampedusa Island (Sicily)

Sicily Channel

Sighting of one indivi-

dual already observed

in Trench Ligurian Sea

1 (8-9 m)

(Panigada et al.,

2014)

2013, August

Ligurian Sea

Sighting of the same

individual of Lampedusa

1 (8-9 m)

(Panigada et al.,

2014)

2015, 10 December

Baia, Bay of Pozzuoli (Province

of Naples, Campania) Tyrrenian

Sea

Sighting

Present work

Table 1. Reports concerning specimens of Humpback Whale, Megaptera novaeangliae, recorded in the Italian seas.

Whale, Megaptera novaeangliae, in the Bay of Poz-

zuoli near Baia, a District of Bacoli Municipality

(Province of Naples, Campania Region) occurred

on 10 December 2015. The animal has been obser-

ved near the coast at a depth of about six meters, it

was approximately 8-9 meters long (probably a ju-

venile) and with the uppersides of both pectoral fins

of white color, apparently in good conditions (Figs.

2-4). This is the first documented record of a Hum-

pback Whale in the Tyrrenian Sea, and the first si-

ghting for Campania Region (Maio & Quercia,

2006; Maio et al., 2012). Our finding suggests that

the Tyrrenian waters offer suitable habitats also for

this species.

Since 1885, 24 records (16 sightings of which

four with two individuals, three strandings and 5

by-caught individuals) have been reported from dif-

ferent locations across the Mediterranean basin. All

individuals, ranging between 7 and 12 meters, were

estimated to be 2-3 years old juveniles (Panigada

et al., 2014).

The first occurrence in the Mediterranean Sea

was a juvenile caught in 1885 off 15 km West of

Toulon (France) (Pouchet, 1885; Beauregard, 1885;

VanBeneden, 1889; Aguilar, 1989). Occurrences of

Flumpback Whales, Megaptera novaeangliae, are

extremely rare in the Italian Seas being known only

six sightings and one captures of single specimens.

Date, location and size are given in Table 1 . The

first occurrence was of a 7-9 m long individual

reported in the Gulf of Oristano (Sardinia), in

January 1998 (Frantzis et al., 2004).

The last sighting was an individual approxim-

ately 8-9 meters long, observed in three different

First record of a HumpbackWhale Megaptera novaeangliae in the Tyrrhenian Sea (Cetacea Balaenopteridae)

locations: the first time it was observed in the

French Liguria Sea, NW Mediterranean, in June

2012; then, the same animal was re-sighted off

Lampedusa Island, Sicily Channel, in March 2013

over 1,000 km away in a straight line from the

previous location and again in August 2013, in the

“Italian” Ligurian Sea (Panigada et al., 2014). No

specimens from Mediterranean Sea are preserved

in Italian museums (Cagnolaro et al., 2014).

The Humpback Whale, Megaptera novaeangliae ,

is a species listed in the Appendix I of CITES, and

it is considered an “Endangered or threatened

species” in the Annex II of the Barcelona Conven-

tion for Protection against Pollution in the Mediter-

ranean Sea. It is also included in the Appendix II

of the Bern Convention on the Conservation

of European Wildlife and Natural Habitats, con-

sidered as “Strictly protected fauna species”,

and is a “species in need of strict protection” in

European Union by the Annex IV of the Council

Directive 92/43/EEC of May 21thl992 on the

conservation of natural habitats and of wild fauna

and flora, known as “Habitats Directive”. Further-

more the species is classified as “Least Concern”

on the IUCN Red List of Threatned Species (vers.

2015.4) (Reilly et al., 2008).

AKNOWLEDGEMENT

We wish to thank Gennaro Bianco (University

of Naples “Parthenope”, Italy), Lucia Borrelli,

Elena Confalone and Roberta De Stasio (Univer-

sity of Naples Federico II, Italy), Gianfranco Pol-

laro (Centro Studi Ecosistemi Mediterranei,

Pollica, Salerno, Italy).

REFERENCES

Affronte M., Stanzani L.A. & Stanzani G., 2003. First re-

cord of the humpback whale, Megaptera novaeangliae

(Borowski, 1781), from the Adriatic Sea. Annales,

Series Historia Naturalis, 13: 51-54.

Aguilar A., 1989. A record of two Humpback Whales,

Megaptera novaeangliae, in the Western Mediter-

ranean Sea. Marine Mammal Science, 5: 306-309.

doi: 10. 1 1 1 1/j. 1 748-7692. 1989. tb00344.x

Beauregard H., 1885. Note sur une Megaptere echouee

au Bmsc pres Toulon. Seances du 19 Decembre 1885.

Comptes Rendus Hebdomadaires des Seances et

Memories de la Societe de Biologie, Paris [Compt.

Rend. Mem. Soc. Biol. Paris], 37 (tome 2, serie 8):

753.

Cagnolaro L., Cozzi B., Notarbartolo di Sciara G. &

Podesta M. (Eds.), 2015. Fauna d’ltalia Vol. XLIX.

Mammalia IV. Cetacea. Calderini, Bologna, 390 pp.

Cagnolaro L., Maio N. & Vomero V. (Eds.), 2014. The

Cetacean collections of italian museums. First part

(living Cetaceans). Museologia Scientifica. Memorie,

12: 1-420.

Centro Studi Cetacei Onlus & Museo Civico di Storia

Naturale di Milano, 2006. Cetacei spiaggiati lungo le

coste italiane. XIX. Rendiconto 2004. Atti della

Sociea italiana di Scienze naturali Museo civico di

Storia naturale di Milano, 147: 147-157.

Frantzis A., Nikolaou O., Bompar J.-M. & Cammedda

A., 2004. Humpbackwhale (Megaptera novaeangliae )

occurrence in the Mediterranean Sea. The Journal of

Cetacean Research Management, 6: 25-28.

Maio N., Pollaro F., Di Nocera F., De Carlo E. & Galiero

G., 2012. Cetacei spiaggiati lungo le coste della

Campania dal 2006 al 2011 (Mammalia: Cetacea).

Atti della Sociea italiana di Scienze naturali Museo

civico di Storia naturale di Milano, 153: 241-255.

Maio N. & Quercia F., 2006. Cetacei spiaggiati lungo il

litorale campano: ricerca e conservazione. In:

Gugliemi R. & Nappi A. (Eds.). Atti Convegno: “Fa

Natura in Campania: aspetti biotici e abiotici”.

Napoli, 18 novembre 2004, 158-164.

Notarbartolo di Sciara G. & Birkun A. Jr., 2010. Con-

serving whales, dolphins and porpoises in the Mediter-

ranean and Black Seas: an ACCOBAMS status re-

port, 2010. ACCOBAMS, Monaco.

Panigada S., Frey S., Pierantonio N., Garziglia P. &

Giardina F., 2014. Are humpback whales electing the

Mediterranean Sea as new residence? 28th Con-

ference of the European Cetacean Society. Fiege,

Belgium 5th-9th April 2014. Conference Paper: 203.

Pouchet G., 1885. Sur Fechouages d’une Megaptere pres

de la Syene. Seances du lundi 7 Decembre 1885.

Comptes Rendus Hebdomadaires des Seances de

FAcademie des Sciences, Paris, 101: 1172.

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editors), 2006. The status and distribution of Ceta-

ceans in the Black Sea and Mediterranean Sea.

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Brownell Jr. R.L., Butterworth D.S., Clapham P.J.,

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Biodiversity Journal, 2016, 7 (1): 39-50

Systematic account of Orthoptera fauna of Bastar district,

Chhattisgarh, India

Sunil Kumar Gupta

Zoological Survey of India, Prani Vigyan Bhawan, 'M' Block, New Alipore, Kolkata, 700053 West Bengal, India; e-mail:

skumarento@gmail.com

ABSTRACT A faunistic survey in Bastar district, Chhattisgarh (India) revealed 52 species belonging to

45 genera, 8 families, including five species which are new record to the Orthoptera fauna of

Chhattisgarh: Calliptamus barbarus bar bar us (Costa, 1836), Ceracris fasciata (Brunner

von Wattenwyl, 1893), Oedaleus senegalensis (Krauss, 1877), A u larches miliaris miliaris

(Linnaeus, 1758), and Loxoblemmus haani Saussure, 1877.

KEY WORDS Distribution; Bastar; Orthoptera; Chhattisgarh.

Received 23.02.2016; accepted 08.03.2016; printed 30.03.2016

INTRODUCTION

The major works on Orthopteran fauna of India

were published by Kirby (1914) and Chopard

(1969). Notable papers on Orthoptera fauna of

Chhattisgarh state were also done by Dwivedi

(1978, 1990), Dixit & Sinha (1982), Agrawal &

Sinha (1987), Chandra & Gupta (2005), Chandra et

al. (2007), Gupta et al. (2008), Gupta & Chandra

(2010) and Gupta & Shishodia (2014), but so far no

comprehensive account on Orthoptera of Bastar is

available a part from a few exceptions including:

Chopard (1970) who described Arachnomimus sub-

alatus Chopard, 1970 and Sinha & Agrawal (1973)

who described Kempiola shankari (Sinha et Agrawal,

1973) both from the same locality, i.e. Kutums war

cave. Shishodia, (1995) reported 15 species belong-

ing 15 genera under 6 families from Indravati Tiger

Reserve, Bastar. Shishodia (2000) reported 77

species of crickets and grasshoppers from Bastar.

MATERIAL AND METHODS

A total of 514 specimens representing 52 species

belonging 45 genera under 8 families viz. Ac-

rididae 28 species 21 genera, Pyrgomorphidae 4

species 4 genera, Tetrigidae 4 species 4 genera,

Tridactylidae 1 species and 1 genus, Gryllidae 6

species 6 genera, Trigonidiidae 2 species 2 genera,

Gryllotalpidae 1 species 1 genus, Tettigoniidae 6

species 6 genera, are known from Bastar district

of Chhattisgarh. Of these, five species are reported

for the first time.

In Table 1 are showen coordinates of collection

localities. The species recorded for the first time are

marked with an asterisk (*). All specimens are

preserved in collection R.P. Gupta & co-workers

collection.

SYSTEMATIC

Order ORTHOPTERA

Suborder CAELIFERA

Superfamily ACRIDOIDEA

Family ACRIDIDAE

Subfamily ACRID IN AE

Genus Acrida Linnaeus, 1758

Sunil Kumar Gupta

S. No.

Site

Latitude N Longitude E

Altitude

Asna Village

19°7T5.4"

82°01' 20.9"

539

Amaguda

19°9'45.4"

82°0T5.1"

553

Bhanpuri

19°19T7.4"

81°51T7.0"

514

Bhatiguda

Village

19°2'53.4"

82°3'3.5"

515

Belguda

Village

19°13'03"

81°58'55.1"

552

Chidaipadar

19°10T.7"

81°58T9.9"

543

Dongaghatpara

19°00'28.5"

81°05'08"

485

Erikpal Village

19°07T7.9"

82°03'34.9"

542

Gariya

bahar river

19°4'53.2"

82°3T.9"

547

Hathguda

19°5'45.6"

82°3' 9.7"

561

Jagdalpur City

19°4'33.4"

82°1’51.7"

478

Jeeragaon

19°2'7.9"

82°9'39.1"

563

Kalcha

19°6'36.8"

82°6T8.9"

559

Kohkapal

19°8'32.1"

82°6'21.4"

562

Kolchur

19°10'5.8"

81°57'31.9"

555

Kopaguda

Village

19°3'34.7"

82°6'43.1"

600

Kotamsar

18°52'45"

81°55'21.1"

487

Kurandi

19°1'49.5"

82°6T3.1"

578

Machkote

range

19°0'52.4"

82°8'2.3"

555

Malgaon

19°8'6.9"

82°4'47.9"

551

Magedha

19°46'0.4"

81°53T6.9"

592

Makdi FRH

19°46'22.3"

81°54T2.8"

671

Mongrapal

Village

19°H'26.9"

81°59'27.1"

572

Nakaguda

Village

19°10'7.8"

81°2'47.4"

579

Neganar

Village

19°12T.7"

81°1'3.3"

488

Piplavand

19°19'24.5"

81°55'39.2"

513

Pushpal

18°15'23.5"

82°4'53.2"

584

Rampal

19°13'39.9"

82°00'41.5"

599

Sonarpal beat

19°18'37.5"

81°51'51.5"

486

Taraguda

1909 - 25 "

82°6T7.1"

554

Tiwasguda

19°10'3"

82°2'48.5"

579

Ulnar

19°10'20.3"

82°7'28"

568

Umargaon

Village

19°10'40.2"

82°1'36.2"

568

Table 1. Coordinates of collection localities of Bastar

district, Chhattisgarh (India).

Acrida exaltata (Walker, 1859)

Truxalis exaltata - Walker, 1859: 222

Acrida exaltata - Dey & Hazra, 2003: 24

Examined material. Chhattisgarh; Bastar,

Malgaon, 23.XI.2011, 1 male; 18.IV.2012, 1 male;

Belaguda, 16.1.2012, 1 male; Jhariya Bahara Nala,

20. 111. 2012, 3 males; Kurandi, 23.III.2012, 2

males and 2 females; Erikpal Village, 24.11.2012,

1 male.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

2. Acrida gigantea (Herbst, 1786)

Truxalis gigantea - Herbst, 1786: 191

Acrida gigantea - Joshi et al., 2004: 71

Examined material. Chhattisgarh; Bastar,

Rampal Village, 19.1.2012, 1 female; Bhanpuri,

20.X.2011, 2 females; Neganar Village, 4.1.2012, 1

male; Dongraghat para, 6.II.2012, 1 male; Jag-

dalpur city, 13.11.2012, 1 male; Taraguda,

13.11.2012, 4 females; Ericpal Village, 25.11.2012,

1 female; Malgaon, 9.III.2012, 1 female;

10. 111. 2012, 1 female; Kohkapal, 14.III.2012, 2

females; Kumndi, 23.III.2012, 1 male and 1 female;

Gariya Bahar river, 24.III.2012, 1 female;

Machkote Range, 7.VI.2012, 2 males and 2 fe-

males; Kopaguda, 22.V.2012, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

3. Acrida turrita (Linnaeus, 1758)

Gryllus ( Acrida ) turritus - Linnaeus, 1758: 427

Gryllus {Acrida) nasutus - Linnaeus, 1764: 118

Acrida turrita - Kirby, 1914: 98

Examined material. Chhattisgarh; Bastar,

Mangra para, 7.1.2012, 1 male and 1 female; Be-

laguda, 18.1.2012, 1 male; Dongaghat para,

7.11.2012, 1 female; 8.II.2012, 1 female; Malgaon,

7. II. 2012, 2 males; 10.III.2012, 1 male and 2 fe-

males; Erikpal Village, 24.11.2012, 1 female;

Kurandi, 23.III.2012, 1 male; Kolchur, 18.IV.2012,

1 male; 7.VI.2012, 1 male; Kopaguda, 22.V.2012,

1 female.

Distribution in Chhattisgarh. Bastar and

Raipur.

Genus Phlaeoba Stal, 1860

Systematic account of Orthoptera fauna of Bastar district, Chhattisgarh, India

4. Phlaeoba infumata Brunner, 1893

Phlaeoba infumata - Brunner, 1893: 124

Phlaeoba infumata - Dey & Hazra, 2003: 25.

Examined material. Chhattisgarh; Bastar,

Sonarpal Beat, 17.X.2011, 1 male; Neganar Village,

4.1.2012, 1 male; Nakaguda Village, 24.1.2012, 1

female; Malgaon, 9.II.2012, 1 female; 10.III.2012

1 male; Erickpal Village, 24.11.2012, 1 male;

Kohkapal, 14.III.2012, 3 males and 4 females;

Kalcha, 24.IV.2012, 2 males; 18.VI.2012, 1 male;

Machkote range, 7.VI.2012, 1 male and 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

5. Phlaeoba panteli Bolivar, 1902

Phlaeoba panteli - Bolivar, 1902: 589

Phleoba panteli - Dey & Hazra, 2003: 27

Examined material. Chhattisgarh; Bastar,

Jagdalpur range, 29.VIII.2011, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily CALLIPTAMINAE

Genus Calliptamus Audinet-Serville, 1831

6. Calliptamus barbarus barbarus (Costa, 1 836) (*)

Acridium barbarum - Costa, 1836: 13

Caloptenopsis punctata - Kirby, 1914: 208

Calliptamus barbarus barbarus - Massa, 2009: 81

Examined material. Chhattisarh; Bastar,

Amaguda, 24.VIII.2011, 1 female.

Distribution in Chhattisgarh. Bastar.

Remark. New record from Chhattisgarh state.

Subfamily CATANTOPINAE

Genus Choroedocus Bolivar 1914

7. Choroedocus illustris (Walker, 1870)

Heteracris illustris - Walker, 1870: 662, 663

Chroedocus illustris - Uvarov, 1921a: 109

Examined material. Chhattisgarh; Bastar,

Jagdalpur range, 19.VIII.2011, 1 female.

Distribution in Chhattisgarh. Bastar.

8 . Diabolocatantops innotabilis (Walker, 1870)

Acridium innotabile - Walker, 1870: 629

Diabolocatantops innotabilis - Jago, 1984: 371

Examined material. Chhattisgarh; Bastar, Jag-

dalpur range, 29.VIII.2011, 2 females; Neganar Vil-

lage, 4.1.2012, 1 female; Mograpal Village,

6.1.2012, 2 females; Chidaipadar, 20.1.2012, 1 fe-

male; Asna Village, 2.II.2012, 1 female; 4.II.2012,

2 females; Erikpal Village, 24.11.2012, 1 male;

Malgaon, 9.III.2012, 2 males and 1 female;

Kohkapal, 14.III.2012, 2 females; Gariya bahar

river, 22.III.2012, 1 female; Machkote range,

7. VI. 2012, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Packyacris Uvarov, 1923

9. Pachyacris vinosa (Walker, 1870)

Acridium vinosum - Walker, 1870: 587

Pachyacris vinosa - Shishodia & Dey, 2006: 107

Examined material. Chhattisgrah; Bastar,

Makdi range, 8.XI.2011, 1 male.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Stenocatantops Dirsh et Uvarov, 1953

10. Stenocatantops splendens (Thunberg, 1815)

Gryllus splendens - Thunberg, 1815: 236

Stenocatantops splendens - Shishodia, 2000: 63

Examined material. Chhattisgrah; Bastar,

Mograpal Village, 7.1.2012, 1 males and 1 female;

Asna Village, 4.II.2012, 1 female; Malgaon,

9. 111. 2012, 1 male; 10.III.2012, lmale and 3 fe-

males; Kohkapal, 14.III.2012, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Xenocatantops Dirsh et Uvarov, 1953

11. Xenocatantops humilis humilis (Audinet-

Serville, 1839)

Acridium humile - Audinet-Serville, 1839: 662

Xenocatantops humilis humilis - Shishodia, 2000: 62

Sunil Kumar Gupta

Examined material. Chhattisgarh; Bastar,

MakdiPond, 9.IX.2011, 1 female; 7.VI.2012, 1 fe-

male; Mograpal Village, 7.1.2012, 1 male; Malgaon,

9. III. 2012, 1 male; 9.XII.2012, 1 female; Ko-

hkapal, 14.III.2012, 1 male; Kurundi, 23.III.2012,

1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

12 . Xenocatantops karnyi (Kirby, 1910)

Catantops karnyi - Kirby, 1910: 483

Xenocatantops karnyi - Shishodia, 2000: 62

Examined material. Chhattisgarh; Bastar,

Belguda Village, 16.1.2012, 1 female; 18.1.2012, 1

female; Dongaghatpara, 7.II.2012, 1 female;

Amaguda, 2.III.2012, 1 male; Malgaon, 10.III.2012,

1 male and 1 female; Kohlcapal, 14.III.2012, 1 male

and 1 female; Jeeragaon, 26.III.2012, 1 female.

Distribution in Chhattisgarh. Bastar and

Raipur.

Subfamily COPTACRID1NAE

Genus Eucoptacra Bolivar, 1902

13. Eucoptacra praemorsa (Walker, 1870)

Acridium saturatum - Walker, 1870: 628

Eucoptacra saturata - Uvarov, 1921b: 503

Eucoptacra praemorsa - Tandon, 1976: 10

Examined material. Chhattisgarh; Bastar, Mal-

gaon, 10.III.2012, 1 female; Taraguda, 16.IV.20 12,

1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily CYRTACANTHACRIDINAE

Genus Cyrtacanthacris Walker, 1870

14. Cyrtacanthacris tatarica (Linnaeus, 1758)

Gryllus locusta tataricus - Linnaeus, 1758: 432

Cyrtacanthacris tatarica - Shishodia, 2000: 58

Examined material. Chhattisgarh; Bastar,

Amaguda, 23.VIII.2011, 1 female; 24.VIII.2011, 1

male.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily EYEPREPOCNEMIDINAE

Genus Tylotropidius Stal, 1860

15. Tylotropidius varicornis (Walker, 1870)

Heteracris varicornis - Walker, 1870: 667

Tylotropidius varicornis - Shishodia, 2000: 60

Examined material. Chhattisgarh; Bastar,

Belaguda, 18.1.2012, 1 male; Jagdalpur range,

15. VII. 2012, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily GOMPHOCERINAE

Genus Leva Bolivar, 1909

16. Leva indica (Bolivar, 1902)

Gymnobothrus indicus - Bolivar, 1902: 596

Leva cruciata - Bolivar, 1914: 65

Leva indica - Jago, 1996: 94

Examined material. Chhattisgarh; Bastar, Jag-

dalpur range, 24.VIII.2011, 1 male; Malgaon,

23.XI.2011, 2 males and 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily HEMIACRIDINAE

Genus C/onacris Uvarov, 1943

17. Clonacris kirbyi (Finot, 1903)

Euthymia kirbyi - Finot, 1903: 622-629

Clonacris kirbyi - Tandon, 1976: 3

Examined material. Chhattisgarh; Bastar,

Nakaguda, 19.1.2012, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily OEDIPODINAE

Genus A iolopus Fieber, 1853

18 . Aiolopus thalassinus tamulus (Fabricius, 1798)

Gryllus tamulus - Fabricius, 1798: 195

Aiolopus thalassinus tamulus - Shishodia, 2000: 49

Examined material. Chhattisgarh; Bastar, Mal-

gaon, 23.XI.2011, 2 males and 1 female; 9.III.2012,

1 female; 1 0.III.20 12, 1 male and 1 female; Jag-

Systematic account of Orthoptera fauna of Bastar district, Chhattisgarh, India

dalpur city, 13.11.2012, 1 female; Ericpal Village,

24.11.2012, 1 female; Kohkapal, 14.III.2012, 3

males and 2 females; Machkote Range, 7.VI.2012,

1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Ceracris Walker, 1870

19. Ceracris fasciata (Brunner von Wattenwyl,

1893) (*)

Parapleurus fasciata - Brunner von Wattenwyl,

1893: 127

Rammeacris gracilis - Willemse, 1951: 66

Ceracris fasciata - Ingrisch, 1989: 235

Examined material. Chhattisgarh; Bastar, Jag-

dalpur range, 29.VIII.2011, 2 females.

Distribution in Chhattisgarh. Bastar.

Remark. New record from Chhattisgarh state.

20. Ceracris nigricornis nigricornis Walker, 1870

Ceracris nigricornis - Walker, 1870: 791

Ceracris nigricornis - Kirby, 1914: 110

Examined material. Chhattisgarh; Bastar,

Taraguda, 16.IV.20 12, 1 male.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Kabirdham, Raipur.

Genus Gastrimargus Saussure, 1884

21. Gastrimargus africanus africanus (Saus-

sure, 1888)

Oedaleus ( Gastrimargus ) marmoratus var. Afric-

anus - Saussure, 1888: 39

Gastrimargus africanus africanus - Shishodia,

2000: 51

Examined material. Chhattisgarh; Bastar,

Ranker, 27.VII.2011, 2 females; Amaguda,

25.VIII.2011, 1 female; Jagdalpur, 29. VIII.201 1,2 fe-

males; Asna Village, 2.II.2012, 1 female; Machkote

range, 7.VI.2012, 1 male and 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Kabirdham, Raipur.

Genus Morphacris Walker, 1870

22 . Morphacris fasciata (Thunberg, 1815)

Gryllus fasciatus - Thunberg, 1815: 230

Morphacris fasciata sulcata - Shishodia, 2000: 50

Examined material. Chhattisgarh; Bastar,

Jagdalpur city, 29.III.2012, 1 male; Hathguda,

29. 111. 2012, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Oedaleus Fieber, 1853

23. Oedaleus abruptus (Thunberg, 1815)

Gryllus abruptus - Thunberg, 1815: 233

Oedaleus abruptus - Ritchie, 1981: 104

Examined material. Chhattisgarh; Bastar,

Chitrakot, 25.VIII.2011, 1 female; Nandpur Beat,

20.X.2011, 1 female; Pipalvond, 22.X.2011, 1 fe-

male; Ulnar, 22.XI.20 11,1 female; Malegaon,

23. XI.2011, 3 females; 9.III.2012, 1 male and 2 fe-

males; 1 0.III.20 12, 8 males and 1 female; Neganar

Village, 5.1.2012, 1 female; Mangrapara, 6.1.2012,

1 male; Mograpal Village, 7.1.2012, 1 male and 2

females; Belguda Village, 16.1.2012, 1 female;

Rampal, 19.1.2012, 1 female; Asna Village,

2.11.2012, 1 female; 4.II.2012, 2 males; Dongaghat-

para, 7. II. 2012, 2 females; Erikpal Village,

24.11.2012, 1 female); 25.11.2012, 3 females; Gariya

bahar river, 24.III.2012, 1 female; Taraguda,

16.IV.2012, 1 female; Kopaguda, 22.V.2012,

1 male; Machkote range, 7.VI.2012, 1 male;

Hathguda, 29.XII.20 12, 2 males.

Distribution in Chhattisgarh. Bastar, Kabird-

ham Raipur.

24. Oedaleus senegalensis (Krauss, 1877) (*)

Pachytylus senegalensis - Krauss, 1877: 56

Oedaleus senegalensis - Ritchie, 1981: 94

Examined material. Chhattisgarh; Bastar,

Kohkapal, 14.III.2012, 1 female.

Distribution in Chhattisgarh. Bastar.

Remark. New record from Chhattisgarh State.

Genus Trilophidia Stal, 1873

25. Trilophidia annulata (Thunberg, 1815)

Sunil Kumar Gupta

Gryllus annulatus - Thunberg, 1815: 234

Trilophidia annulata - Shishodia, 2000: 52

Examined material. Chhattisgarh; Bastar,

Ulnar, 22.XI.2011, 1 male; Malgaon, 23.XI.2011, 1

female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Kabirdham, Raipur.

Subfamily OXYINAE

Genus Oxya Audinet-Serville, 1831

26. Oxya hyla hyla Audinet-Serville, 1831

Oxya hyla - Audinet-Serville, 1831: 287

Oxya hyla hyla - Shishodia, 2000: 55

Examined material. Chhattisgarh; Bastar,

Sonarpal Beat, 17.X.2011, 1 male and 1 female;

Ericpal Village, 24.11.2012, 2 females; Mal-

gaon, 9.III.2012, 5 females; Kohkapal Village,

14. 111. 2012, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Kabirdham, Raipur.

Subfamily SPATHOSTERNINAE

Genus Spathosternum Krauss, 1877

27. Spathosternum prasiniferum prasiniferum

(Walker, 1871)

Heteracris prasinifera - Walker, 1871: 65

Spathosternum prasiniferum prasiniferum - Shisho-

dia, 2000: 53

Examined material. Chhattisgarh; Bastar,

Chitrkote, 23.VIII.2011, 1 male; Nandpur Beat,

20. X.2011, 1 female; Sonarpal Beat, 17.X.2011, 3

males and 1 female; Bhanpuri, 19.X.2011, 1 male;

21. X.2011, 1 female; Asna, 1.XI.2011, 2 females;

4.H.2012, 2 females; Makdi Pond, 9.XI.2011, 2 males

and 3 females; Mageda, 9.XI.2011, 1 female; Makdi

Range, 11.XI.2011, 1 female; Malgaon, 23.XI.2011,

8 females; 7.III.2012, 1 male; 9.III.2012, 1 male and

4 females; 10.III.2012, 2 males and 5 females;

Mograpal Village, 6.1.2012, 1 female; 7.1.2012, 1 fe-

male; Belguda Village, 16.1.2012, 1 female;

18.1.2012, 1 female; Rampal Village, 19.1.2012, 1

male; Tiwasguda, 23.1.2012, 1 male; Dongraghat

Para, 7.II.2012, 1 female; Taraguda, 13.11.2012, 2 fe-

males; 12.III.20 12, 2 females; Kohkapal, 14.11.2012,

1 male; Erikpal Village, 24.11.2012, 1 male;

25.11.2012. 1 male; 10.III.2012, 1 male and 4 females;

Kohkapal, 14.III.2012, 1 male and 1 female; Ulner

Village, 16.III.2012, 1 male and 1 female; Gariya

bahar river, 20.III.2012, 2 males and 6 female; Kur-

undia, 23 .111.20 12, 1 male; Jeeragaon, 26.III.2012,

1 male and 1 female; Hatguda, 29.III.2012, 1 male;

Taraguda, 16.IV.20 12, 3 males and 3 females; Kalcha,

24.IV.20 12, 1 male; Bhatiguda, 2.VI.2012, 1 male;

Machkote Range, 7.VI.2012, 1 female; Rawanapat,

23.X.2013, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily TERATODINAE

Genus Teratodes Brulle, 1835

28. Teratodes monticollis (Gray, 1832)

Gryllus monticollis - Gray, 1832: 215

Teratodes monticollis - Shishodia, 2000: 52

Examined material. Chhattisgarh; Bastar, Jag-

dalpur range, 29.VIII.2011, 2 females.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Superfamily PYRGOMORPHOIDEA

Family PYRGOMORPHIDAE

Genus Atractomorpha Saussure, 1862

29 . Atractomorpha crenulata (Fabricius, 1793)

Truxalis crenulata - Fabricius, 1793: 28

Atractomorpha crenulata - Shishodia, 2000: 42

Examined material. Chhattisgarh; Bastar, Mal-

gaon, 23. XI. 2011,1 male; 28.VII.2011, 1 female;

Dagania, 29.VIII.2011, 1 female; Sonarpara Beat,

17.X. 2011, 1 male; Makdi range, 10.XI.2011, 1

male; Neganar Village, 4.1.2012, 1 male; Nathguda

Village, 24.1.2012, 1 male; Taraguda, 12.III.2012,

1 male; Ulnar Village, 16.III.2012, 1 male; Kurundi,

23. 111. 2012. 1 male; Hatguda, 29.III.2012, 1 female;

Machkot range, 7.VI.2012, 2 males; Bhatiguda Vil-

lage, 18.VII.2012, 1 male; Pushpal, 1.VIII.2013, 2

males.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Aularches Stal, 1873

Systematic account of Orthoptera fauna of Bastar district, Chhattisgarh, India

30. Autarches miliaris miliaris (Linnaeus, 175 8) (*)

Gryllus ( Locusta ) miliaris - Linnaeus, 1758: 432

Aularches miliaris miliaris - Mandal & Yadav,

2007: 190

Examined material. Chhattisgarh; Bastar,

Erikpal Village, 16.VIII.2011, 1 female; Kanker,

27.VII.2011, 1 female; 28.VII.2011, 1 female; Jag-

dalpur city, 29.VIII.2011, 1 female; Jagdlapur

range, 30. VIII. 2011, 1 female; Asna Village,

2. 11. 2012, 1 female; Malegaon, 10.III.2012, 1 fe-

male; Jhiriya Bahara, 20.III.2012, 1 female.

Distribution in Chhattisgarh. Bastar.

Remark. New record from Chhattisgarh State.

Genus Chrotogonus Audinet-Serville, 1838

31. Chrotogonus ( Chrotogonus ) trachypterus

trachypterus (Blanchard, 1836)

Ommexycha trachypterus - Blanchard, 1836: 618

Chrotogonus (C.) trachypterus trachypterus -

Shishodia, 2000: 40

Examined material. Chhattisgarh; Bastar,

Amaguda, 24.VIII.2011, 1 male and 1 female;

Bhanpur, 19.X.2011, 2 females; 21.X.2011, 1 male

and 1 female; Pipalvond Beat, 22.X.2011, 1 male

and 1 female; Malegaon, 23.XI.2011, 1 female; Bel-

guda Village, 16.1.2012, 3 females; Natguda Vil-

lage, 24.1.2012 2 males and 3 females; Neganar

Village, 4.1.2012, 1 male; Malegaon, 10.III.2012, 1

female; Kohkapal, 14.III.2012, 1 male and 5 fe-

males; Hathguda, 29.III.2012, 1 female; Taraguda,

16.IV.2012, 1 female; Kalcha, 24.IV.2012, 2 males;

Ulnar, 22. XI. 2011, 1 male and 1 female.

Distribution in Chhattisgarh. Bstar, Bilaspur,

Kabirdham, Raipur.

Genus Poekilocerus Audinet-Serville, 1831

32 . Poekilocerus pictus (Fabricius, 1775)

Gryllus pictus - Fabricius, 1775: 289

Poekilocerus pictus - Kirby, 1914: 172

Examined material. Chhattisgarh; Bastar, Mo-

grapol Village, 7.1.2012, 1 female; Nakaguda,

19.1.2012, 1 male; Amaguda, 2.III.2012, 1 male.

Distribution in Chhattisgarh. Bastar and

Raipur.

Superfamily TETRIGOIDEA

Family TETRIGIDAE

Subfamily SCELIMENINAE

Genus Criotettix Bolivar, 1887

33. Criotettix bispinosus (Dalman, 1818)

Acrydium bispinosum - Dalman, 1818: 77

Criotettix bispinosus - Bolivar, 1887: 185, 223, 226

Criotettix bispinosus - Gunther, 1938: 134

Examined material. Chhattisgarh; Bastar,

Sonarpal Beat, 17.X.2011, 1 female.

Distribution in Chhattisgarh. Bastar.

Genus Euscelimena Gunther, 1938

34 . Euscelimena harpago (Audinet-Serville, 1839)

Tetrix harpago - Audinet-Serville, 1839: 763

Euscelimena harpago - Hebard, 1929: 572

Examined material. Chhattisgarh; Bastar, Na-

kaguda, 19.1.2012, 1 male; Asna Village, 2.II.2012,

2 females; 4.II.2012, 1 female; Malgaon, 10.III.2012,

2 females; Kohkapal, 14.III.2012, 2 females;

Machkote Range, 7.VI.2012, 1 male and 1 female;

Amaguda, 2.III.2012, 1 male; Kurundi, 23.III.2012,

1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily TETRIG1N AE

Genus Ergatettix Kirby, 1914

35. Ergatettix dorsiferus (Walker, 1871)

Tettix dorsifera - Walker, 1871: 825

Ergatettix dorsifera - Shishodia, 1999: 42

Examined material. Chhattisgarh; Bastar,

Makdi, 9.XI.201, 1 male; Nakaguda, 19.1.2012, 1

male; Amaguda, 2.III.2012, 1 male; Malgaon,

9. III. 2012, 1 male; Ulner Village, 16.III.2012, 1

male.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Hedotettix Bolivar, 1887

36. Hedotettix gracilis (de Haan, 1842)

Acridium {Tetrix) gracile - de Haan, 1842: 167-169

Hedotettix gracilis - Shishodia, 2000: 36

Sunil Kumar Gupta

Examined material. Chhattisgarh; Bastar, Jag-

dalpur range, 28. VII. 2011, 2 males and 1 female;

Sonarpali Beat, 17.X.20011, 2 males.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Infraorder TRIDACTYLIDEA

Superfamily TRIDACTYLOIDEA

Family TRIDACTYLIDAE Brunner, 1882

Subfamily TRIDACTYLINAE

Genus Tridactylus Olivier, 1789

37. Tridactylus thoracicus Guerin, 1844

Tridactylus thoracicus - Guerin, 1844: 336

Tridactylus thoracicus - Shishodia & Tandon, 1987:

128

Examined material. Chhattisgarh; Bastar,

Neganar Village, 5.1.2012, 1 male, DC; 31.1.2012,

1 female, DC; Amaguda, 2.III.2012, 1 female, DC;

Gariya bahar river, 24.III.2012, 1 male, DC; Mon-

grapal Village, 1.1.2012, 1 male, DC; 7.1.2012, 1 fe-

male, DC.

Distribution in Chhattisgarh. Bilaspur and

Raipur.

Suborder ENSIFERA

Infraorder OEDISCHIOIDEA

Superfamily GRYLLOIDEA

Family Gryllidae

Subfamily Gryllinae

Genus Loxohlemmus Saussure, 1877

38. Loxoblemmus haani Saussure, 1877 (*)

Loxohlemmus haani - Saussure, 1877: 257

Loxohlemmus haani - Vasanth, 1993: 46

Examined material. Chhattisgarh; Bastar,

Nandpurabeat, 20.X.2011, 1 male.

Distribution in Chhattisgarh. Basatr, Bilaspur.

Remark. New record from Chhattisgarh State.

Genus Modicogryllus Chopard, 1961

Subgenus Modicogryl l us Chopard, 1961

39 . Modicogryllus (Modicogryllus) confirma-

tus (Walker, 1859)

Acheta confirmata - Walker, 1859: 221

Modicogryllus confirmatus - Tandon et al., 1976: 170

Examined material. Chhattisgarh; Bastar,

Nandpura Beat, 20.X.2011, 1 female; Jagdalpur

range, 11. XI. 2011, 1 female; Gariya bahar river,

20. 111. 2012, 1 female; Malgaon, 10.III.2012, 1 fe-

male.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Phonarellus (Gorochov, 1983)

Subgenus Phonarellus Gorochov, 1983

40. Phonarellus ( Phonarellus ) minor Chopard, 1959

Gymnogryllus minor - Chopard, 1959: 1

Phonarellus ( Phonarellus ) minor - Gorochov, 1983:

323

Examined material. Chhattisgarh; Bastar,

Bhanpuri, 20.X.2011, 1 female; Mongrapal Village,

7.1.2012, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Teleogryllus Chopard, 1961

Subgenus Macroteleogryllus Gorochov, 1988

41. Teleogryllus {Macroteleogryllus) mitratus

(Burmeister, 1838)

Gryllus mitratus - Burmeister, 1838: 734

Teleogryllus mitratus - Gupta et al., 2008: 120

Examined material. Chhattisgarh; Bastar, Jag-

dalpur range, 24.VIII.2011, 1 female.

Distribution in Chhattisgarh. Bastar and

Bilaspur.

Subfamily NEMOBIINAE

Genus Paranemohius Saussure, 1877

42. Paranemobius pictus (Saussure, 1877)

Pseudonemobius pictus - Saussure, 1877: 67

Paranemohius pictus - Shishodia, 2000: 70

Examined material. Chhattisgarh; Bastar,

Neganar Village, 4.1.2012, 1 female.

Distribution in Chhattisgarh. Bastar.

Subfamily OECANTHINAE

Genus Oecanthus Audinet-Serville, 1831

Systematic account of Orthoptera fauna of Bastar district, Chhattisgarh, India

43. Oecanthus indicus Saussure, 1878

Oecanthus indicus - Saussure, 1878: 454.

Oecanthus indicus - Shishodia, 2000: 71

Examined material. Chhattisgarh; Bastar,

Ericpal Village, 24.11.2012, 1 female.

Distribution in Chhattisgarh. Bastar and

Bilaspur.

Family TRIGONIDIIDAE

Genus Anaxipha Saussure, 1874

44. Anaxipha sp.

Anaxipha - Saussure, 1874: 370

Anaxipha - Vasanth, 1993: 108

Examined material. Chhattisgarh; Bsatar, Jag-

dalpur Forest, 15.VII.2011, 1 male and 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Trigonidium Rambur, 1839

Subgenus Trigonidium Rambur, 1839

45. Trigonidium ( Trigonidium ) cicindeloides

Rambur, 1839

Trigonidium cicindeloides - Rambur, 1839: 39

Trigonidium cicindeloides - Shishodia, 2000: 74

Examined material. Chhattisgarh; Bastar,

Bhanpuri, 19.X.2011, 1 female.

Distribution in Chhattisgarh. Bastar, Raipur.

Family GRYLLOTALPIDAE

Genus Gryllotalpa Latreille, 1802

46. Gryllotalpa africana Beauvois, 1805

Gryllotalpa africana - Palisot de Beauvois, 1 805 : 229

Gryllotalpa africana - Shishodia, 2000: 64

Examined material. Chhattisgarh; Bastar, Nand-

pura Village, 20.X.2011, 1 male; Bhanpur,

21.X.2011, 1 male; Rampal, 19.i.2012, 1 female;

Hathguda, 29.III.2012, 1 male.

Distribution in Chhattisgarh. Bastar, Bila-

spur, Raipur.

Superfamily TETTIGONIOIDEA

Family TETTIGONIIDAE

Subfamily CONOCEPEtALINAE

Genus Conocephalus Thunberg, 1815

Subgenus An isoptera Latreille, 1829

47. Conocephalus ( Anisoptera ) maculatus (Le

Guillou, 1841)

Xiphidion maculatum - Le Guillou, 1841: 294

Conocephalus maculatus - Chandra et al., 2007: 2684

Examined material. Chhattisgarh; Bastar, Jag-

dalpur Forest, 15. VII. 2011, 1 female; Bhanpuri

Forest, 20.X.2011, 1 female; Mangrapal Village,

7.1.2012, 2 females; Belguda Village, 16.1.2012, 1

female; 18.1.2012, 1 female; Naganar Village,

31.1.2012, 1 male; Asna Village, 4. II. 2012, 1 fe-

male; Dongaghat, 8.II.2012, 1 female; Amaguda

Village, 2. III. 2012, 1 male; Malegaon, 10.III.2012,

1 female; Jagdalpur, 12.III.2012, 1 male; Taraguda,

12. 111. 2012, 1 male; Bhanpuri, 15.III.2012, 1 fe-

male; Bhatiguda Village, 2.VI.2012, 1 male.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily MECOPODINAE

Genus Mecopoda Audinet-Serville, 1831

48. Mecopoda elongata elongata (Linnaeus, 1758)

Gryllus ( Tettigonia ) elongatus - Linnaeus, 1758: 429

Mecopoda elongata - Barman, 2003: 195

Examined material. Chhattisgarh; Bastar,

Taraguda, 16.IV.20 12, 1 female.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily PHANEROPTERINAE

Genus Elimaea Stal, 1874

Subgenus Orthelimaea Karny, 1926

49. Elimaea ( Orthelimaea ) securigera Brunner

von Wattenwyl, 1878

Elimaea ( Orthelimaea ) securigera - Brunner von

Wattenwyl, 1878: 93

Elimaea ( Orthelimaea ) securigera - Barman, 2000:

264

Examined material. Chhattisgarh; Bastar,

Kotamsur, 27.VII.2011, 1 male.

Sunil Kumar Gupta

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Genus Himertula Uvarov, 1 940

50 . Himertula kinneari (Uvarov, 1923)

Himerta kinneari - Uvarov, 1923: 661

Himertula kinneari - Ingrisch & Shishodia, 2000: 20

Examined material. Chhattisgarh; Bastar,

Jagdalpur range, 30.VIII.2011, 1 female.

Distribution in Chhattisgarh. Bastar and

Raipur.

Genus Phaneroptera Audinet-Serville, 1831

Subgenus Phaneroptera Audinet-Serville, 1831

51. Phaneroptera gracilis Burmeister, 1838

Phaneroptera gracilis - Burmeister, 1838: 690

Phaneroptera gracilis - Shishodia, 1999: 36

Examined material. Chhattisgarh; Bastar,

Ericpal, 24.11.2012, 1 male.

Distribution in Chhattisgarh. Bastar, Bilaspur,

Raipur.

Subfamily Pseudophyllinae

Genus Sathrophyllia Stal, 1874

52. Sathrophyllia rugosa (Linnaeus, 1758)

Gry llus ( Tettignonia ) rugosa - Linnaeus, 1758: 430

Sathrophyllia rugosa - Beier, 1962: 199-200

Examined material. Chhattisgarh; Bastar,

Erikpal, 22.VII.2011, 1 female.

Distribution in Chhattisgarh. Bastar, Raipur.

ACKNOWLEDGEMENTS

The author is grateful to Dr. Kailash Chandra,

Director, Zoological Survey of India (Kolkata) for

providing necessary facilities and encourage-

ments. Thanks are also due to CAMPA (Compens-

atory Afforestation Fund Management and

Planning Authority) for funding the project, and to

Chhattisgarh Forest Department for providing

necessary permissions and support to carry out the

present work.

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Biodiversity Journal, 2016, 7 (1): 51-54

First record of Brachytron pratense (Miiller, 1764) in Sicily

(Odonata Aeshnidae)

Paolo Galasso 1 *, Nadia Curcuraci 1 & Alessandro Marietta 2

'Stiftung Pro Artenvielfalt®, MeisenstraBe 65, 33607 Bielefeld, Germany; email: paolo_galasso@hotmail.com,

nadiacurcuraci@yahoo . it

department of Biological, Geological and Environmental Sciences - section of Animal Biology “M. La Greca”. University of

Catania, via Androne 81, 95124 Catania, Italy; email: amarlet@unict.it

^Corresponding autor

ABSTRACT Brachytron pratense (Muller, 1764) is a small Odonata Aeshnidae widespread throughout

most of Europe and Central-northern Italy, but up to now never recorded in Sicily. During

the spring 2015, some specimens of this species were observed and photographed for the first

time at the swamp lake “Pantano Cuba”, in the southeast coast of Sicily, near to Pachino

(Syracuse). This record represents now the southernmost Italian locality for this species.

KEY WORDS Pantano Cuba; Odonata; dragonflies; Stiftung Pro Artenvielfalt; Sicily.

Received 08.03.2016; accepted 22.03.2016; printed 30.03.2016

INTRODUCTION

Brachytron pratense (Muller, 1764) is a small

Odonata Aeshnidae that is often confused with

others species belonging to the genus Aeshna

Vander Linden, 1820; however, unlike these, it can

be observed in flight early in March and it presents

some peculiar morphological characters. It is a

generally localised species, with a Central European

distribution which extends to Balkan and Mediter-

ranean region. Its range includes the west of the

Urals, France (Corsica included), Netherlands,

Ireland, United Kingdom, Switzerland, Austria,

Germany, Slovenia, Croatia, Czech Republic,

Slovakia, Greece, Denmark, Finland, Norway,

Sweden, Poland, Romania, Estonia, Fatvia,

Fithuania, Belarus and Russia (Askew 2004;

Dijkstra & Fewington, 2006).

In Italy it is an uncommon species and appears

more widespread in northern regions, with the

exception of Figuria and Val D' Aosta (Fig. 1).

However, in the central and southern regions only

few isolated localities are known, so that a good

definition of areal borders is precluded (Riservato

et al., 2014a). Until now the species had never been

reported for Sicily (Riservato et al., 2014b) and the

known southernmost record was in Calabria, near

Famezia Terme (Fig. 1). Therefore, this new record

extends southward the known Italian distribution of

this species and represents now its southernmost

Italian locality.

MATERIAL AND METHODS

During a biodiversity monitoring program

promoted by the German "Stiftung Pro Artenvielfalt

- Pro Biodiversity Foundation" at the swamp lake

“Pantano Cuba”, since April 2015 we have ob-

served and photographed some specimens of B.

Paolo Galasso et alii

pratense. Data were collected during odonatologic

surveys from March 2015 to December 2015. Sur-

veys have been conducted regularly every week at

the same location and with the same method: tran-

sects traversed on foot, collecting and releasing

the specimens with aerial nets for identification.

Moreover several macrophotos have been made on-

site using a digital SLR camera.

The species shows characters so unmistakable

that it was not necessary to kill and preserve the

Figure 1. Distribution map of Brachytron pratense in Italy.

Red arrow shows the new record area (edit from CKmap).

Figure 2. Location of "Riserva dei Pantani della Sicilia

sud-orientale" (Pachino, Syracuse), new locality record for

Brachytron pratense (from Google Earth).

specimens captured. So they were released imme-

diately after the identification.

The place of occurrence, Pantano Cuba

(36°42’26.71”N; 15°1 , 39.15 ,, E), along a complex

of others 7 swamp lakes with different sizes, con-

stitute a very important coastal wetland which was

part of a natural reserve named "Riserva dei Pantani

della Sicilia Sud-orientale" (Fig. 2), whose estab-

lishment was cancelled on May 2015. The swamp,

which is located less than 500 meters from the sea,

lies entirely in the municipality of Pachino, in the

province of Syracuse; it has an extension of 63 hec-

tares and it is characterized by brackish and still wa-

ters with abundant aquatic vegetation represented

mainly by Ruppia maritima L., vegetation helo-

phytic with Phragmites australis (Cav.), Bol-

boschoenus maritimus (L.) Palla, Juncus acutus L.,

Juncus maritimus Lam. and Tamarix africana Poir.,

as well as by halophytic vegetation zones with Arth-

rocnemum fruticosum (L.) and Inula crithmoides L.

Near to the swamp shores there are also idle land,

now entirely covered by grassy vegetation and

several trees of Acacia saligna Labill.

RESULTS

Brachytron pratense adults have a length of 54-

63 mm and a wingspan of 68-74 mm. They are

unmistakable, characterized by hairy thorax and

abdomen, densely covered by thin setae (Figs. 3-

6). The sides of thorax are green, distinctly inter-

rupted by two complete black lines (Fig. 3). The

wings with a narrow and elongated pterostigma

(Fig. 4). Males abdomen black and cylindrical, not

narrowed at the base, with pairs of elongated blue

spots on almost all segments and a diagnostic

central yellow dot on the first abdominal tergite S 1

(Figs. 4, 6). The females (Figs. 3, 5) are similar to

males, except for abdomen stout, browner with

greenish-yellow (not blue) spots (Askew, 2004;

Dijkstra & Fewington, 2006).

During the surveys at Pantano Cuba, several

specimens of B. pratense were observed in at least

four different occasions, always in the same site;

they were adults of both sexes:

- April 9, 2015, 1 female (Figs. 3, 5): it was

caught near one of the fallow fields, about 60

meters from the main water body; it was photo-

graphed and released.

First record of Brachytron pratense (Muller, I 764) in Sicily (Odonata Aeshnidae)

Figures 3. Brachytron pratense female (Pachino, Pantano Cuba; 9.IV.2015): in hand (ventral-lateral view), showing the

typical hairy body. Figure 5. Dorsal view of the same specimen. Figure 4. Brachytron pratense male (Pachino, Pantano

Cuba; 1.V.2015): dorsal view (pt, pterostigma). Figure 6. Brachytron pratense male (Pachino, Pantano Cuba; 23.IV.2015):

dorsal-lateral view (Photos by P. Galasso).

-April 23, 2015, 1 male (Fig. 6): it was observed

and photographed on a branch of Acacia saligna

near a small ditch about 130 meters from the main

water body.

- May 1, 2015, 2 males: they showed territorial

behaviour, one of them was photographed (Fig. 4);

they were observed in a wet meadow of Inula

crithmoides a few meters from the main water body.

- May 7, 2015, 1 male (not photographed): it

was observed in full predatory activities through

open meadows about 100 meters from the main

water body.

CONCLUSIONS

These records add an important and valuable

contribution to the Italian and European odonato-

logy and especially to the study of B. pratense dis-

tribution and ecology.

Paolo Galasso et alii

Pantano Cuba is the first Sicilian site for this

species and the southernmost of Italy and Europe;

it also highlights the undoubted importance of

research projects and monitoring of high conserva-

tion value areas such as the Pantano Cuba, often

underestimated and not subject to the strict retention

policies and management of biodiversity which

they would deserve.

ACKNOWLEDGEMENTS

We wish to thank “ODONATA.IT - Societa

Italiana per lo Studio e la Conservazione delle

Libellule” (Carmagnola, Torino, Italy), for further

confirmation of identification through the analysis

of the photographic material.

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Biodiversity Journal, 2016, 7 (1): 55-57

First record of Callistochiton pachylasmae (Monterosato, 1 879)

for the Adriatic Sea (Polyplacophora Callistoplacidae)

Bruno Amati 1 & Marco Oliverio 2

'Largo Giuseppe Veratti 37/D, 00146 Rome, Italy; e-mail: bnmo_amati@yahoo.it

2 Dipartimento di Biologia e Biotecnologie ‘Charles Darwin’, Sapienza Universita di Roma, Viale dell’Universita 32, 00185 Rome,

Italy; e-mail: marco.oliverio@uniromal.it

ABSTRACT It is reported the first record of Callistochiton pachylasmae (Monterosato, 1879) for the

Adriatic Sea. It a very rare and peculiar polyplacophoran species (Callistoplacidae Pilsbry,

1893). Actually, The few known records span a wide Mediterranean range and extend to the

neighbouring Atlantic.

KEY WORDS Callistochiton pachylasmae', polyplacophoran species; first record; Adriatic Sea.

Received 17.01.2016; accepted 09.02.2016; printed 30.03.2016

INTRODUCTION

Callistochiton pachylasmae (Monterosato,

1879) (original combination: Chiton pachylasmae

Monterosato, 1879 ex Seguenza G. ms) is a very

peculiar polyplacophoran species ( Callistoplacidae

Pilsbry, 1893: Bouchet et al., 2016; Gofas & Le

Renard, 2016), easily recognizable by its peculiar

sculpture, in particular for the presence of 7 radial

ridges on the cephalic plate. Its distinctiveness,

along with its apparently isolated fossil history in

Europe, traced back to at least the Pleistocene

(Dell’ Angelo et al., 1998), brougth Dell’ Angelo &

Oliverio (1997) to allocate it in a subgenus on its

own: Allerychiton Dell’ Angelo et Oliverio, 1997.

DISCUSSION AND CONCLUSION

Callistochiton pachylasmae is a rare species,

and it has been treated seldom in the literature

(Monterosato, 1879; Sabelli, 1971; Ferreira, 1979;

Kaas, 1981; van Belle, 1983, 1988; Gaglini, 1985;

Pizzini & Oliverio, 1993; Giovine & Dell’ Angelo,

1993; Kaas & van Belle, 1994; Dell’ Angelo &

Oliverio, 1997; Dell’Angelo et al., 1998; Anto-

niadou et al., 2005; Koulcouras, 2010). The few

known records span a wide Mediterranean range

and extend to the neighboring Atlantic (Fig. 1). It

is noteworthy that the generic record from Spain in

the Iberian Fauna Databank (Ramos, 2010) could

not be linked to an actual, published record (J.

Templado, pers. comm.) and therefore could not be

plotted in the map (Fig. 1). However, despite the

wide range, there was so far remarkable lack of

findings in the Adriatic Sea.

The present record consist of a single cephalic

plate, 0.82 x 1.37 mm (Fig. 2), retrieved by sorting

a sample of bioclastic sediment with limited or-

ganogenous component, collected by SCUBA

diving at Lastovo Island (Croatia), 38 m depth

(Alessandro Raveggi, Florence, legit). This is the

first record from the Adriatic Sea, and represents

the northernmost known record for the species.

Bruno Amati & Marco Oliverio

Figure 1. Known records of Callistochiton pachylasmae (Monterosato, 1879). 1) W of Cape Yubi, Morocco, -500 m, 1 spe-

cimen now lost (Kaas, 1981). 2) Punta Longa “Secca Galera”, Favignana Island -33 m, 1 cephalic plate (Dell’ Angelo &

Oliverio, 1997). 3) Pantelleria Island, -53.4 m (Pizzini & Oliverio, 1993). 4) Strait of Messina, coralligenous, 1 specimen

(holotype: Monterosato, 1879). 5) S. Maria di Catanzaro, Pleistocene, 1 cephalic plate (Dell’ Angelo et al., 1998). 6) Lastovo

Island (Croatia), -38 m (this work). 7) Kelyfos Island, -30 m, 1 specimen (Antoniadou et al., 2005; Koukouras, 2010). 8)

Ormos Panagias -35/40 m, Sithonia, 1 intermediate plate (Dell’ Angelo & Oliverio, 1997).

Figure 2. Callistochiton pachylasmae (Monterosato, 1879).

Lastovo Island (Croatia), 38 m depth. Cephalic plate, height

0.82, width 1.37 mm.

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Monograph

Jujubinus errinae n. sp. (Gastropoda rochidae from the Strait

of Messina, Mediterranean Sea

Carlo Smriglio 1 , Paolo Mariottini 1 * & Salvatore Giacobbe 2

'Dipartimento di Scienze, Universita “Roma Tre”, Viale Marconi, 446, 00146 Roma, Italy; e-mail: csmriglio@alice.it; paolo.

mariottini@uniroma3 . it

2 Dipartimento di Scienze Biologiche e Ambientali, Universita di Messina, Viale Stagno D'Alcontres, 98166 Messina, Italy; e-mail:

sgiacobbe@unime.it

Corresponding author, email: paolo.mariottini@uniroma3.it

ABSTRACT A new species of the gastropod family Trochidae, Jujubinus errinae n. sp., from the Mediter-

ranean Sea is described based on shell characters. The new taxon was compared with the most

closely related species showing marked sculpture and from relatively deep water habitat, J.

catenatus Ardovini, 2006, J. montagui (Wood, 1828) and J. tumidulus (Aradas, 1846). The

species, which is known from the type locality only, the Strait of Messina, might be strictly

associated to the endemic hydrocoral Errina aspera (Linnaeus, 1767) beds (Hydrozoa Stylas-

teridae).

KEY WORDS Trochidae; Recent; Jujubinus errinae', new species; Mediterranean Sea.

Received 30.10.2015; accepted 16.01.2016; printed 30.03.2016

Proceedings of the Ninth Malacological Pontine Meeting, October 3rd-4th, 2015 - San Felice Circeo, Italy

INTRODUCTION

The Strait of Messina has been considered a

separate Mediterranean biogeographic microsector

inhabited by rich benthic communities and some

peculiar assemblages that are unknown in other

Mediterranean regions (Bianchi, 2004). From this

specific area, a survey of the species of the genus

Jujubinus Monterosato, 1884 (Gastropoda Trochidae)

has been carried out on samples from hard and soft

circalittoral bottoms, which revealed the presence

of trochidae shells not recognizable as a known

species. The specimens, once compared with Juju-

binus catenatus Ardovini, 2006, J. montagui

(Wood, 1828) and J. tumidulus (Aradas, 1846), the

most closely related species showing marked sculp-

ture and from relatively deep water habitat, were

attributed to a new species of this genus, J. errinae

n. sp., which is here described.

ACRONYMS. The materials used for this study

are deposited in the following private and Museum

collections: Carlo Smriglio and Paolo Mariottini,

Rome, Italy (CS-PM); DiSBA Benthic Ecology

laboratory Messina, Italy (DiSBA); Giuseppe

Notaristefano, Messina, Italy (GN); Museo Civico

di Zoologia, Rome, Italy (MCZR); Museo di

Zoologia Bologna, Bologna, Italy (MZB); Renato

Marconcini, Reggio Calabria, Italy (RM); Walter

Renda collection, Reggio Calabria, Italy (WR);

Bruno Amati, Roma, Italy (BA); Ermanno

Quaggiotto, Logare, Vicenza, Italy (EQ). Other

acronyms used in the text: Height (H); Interdepar-

tmental Laboratory of Electron Microscopy, Rome,

Italy (LIME); Monterosato (MTS); Scanning Elec-

tron Microscopy (SEM); specimens (sps); station

(st); Width (W).

Carlo Smriglio etalii

MATERIAL AND METHODS

Hard and soft bottom samples containing the

new species were collected in the Strait of Messina,

central Mediterranean, in several cruises sponsored

by the University of Messina. In particular,

dredging was carried out during the “POP 95”

cruise (13 to 31 July 2015), at 100 m depth (DG04:

38°14'45" N, 15°37'36" E), and arising fromll5 m

to 90 m, along a steep rocky floor (DG001:

38°14'45" N, 15°37'28" E).

During the same cruise, van Veen grab samples

were collected in Rada Paradiso [Station (St) 02:

38°13'27"N, 15°36'02"E], 201 m depth. A further

grab sample, collected by the R/V Coopernaut

Franca in the framework of the POR-CAL 2008

project, was carried out in October 2008, on the

slope of the Gioia Basin (St IB: 38°18'6941N,

15°45'5710E), 371 m depth. Bioclastic sediment

samples were also collected during SCUBA diving

on the bottoms of the Strait of Messina, at a depth

of 40-50 m (38°15 , 36”N, 15°43 , 08”E). Sediment

samples were sieved through a 1 mm mesh and the

residue was sorted using a stereomicroscope.

Among the sorted material, shells of an undescribed

species of Jujubinus, represented by 21 sps, to-

gether juveniles and fragments not included in the

type series, were separated and described herein as

J. errinae n. sp.

Additional material examined from CS-PM

collection: 3 sps of J. catenatus from the Sicily

Channel, estimated depth 90 m; about 100 sps of

J. montagui from Anzio, Central Tyrrhenian Sea,

50 m; 9 sps from Sfax, Tunisia, 100 m; over 200

sps of J. tumidulus from Lampedusa Island, Sicily

Channel, dredged by fishing boats, estimated

depth 70-80 m; 11 sps from Linosa Island (Punta

Calcarello), Sicily Channel, 36 m. Current system-

atics is based on WoRMS (Gofas & Bouchet,

2015).

Scanning Electron Microscopy (SEM) photo-

graphs were taken at the Interdepartmental Laborat-

ory of Electron Microscopy (LIME, Universita

“Roma Tre”, Rome, Italy), using a Philips XL30.

SYSTEMATICS

Classis GASTROPODA Cuvier, 1795

Familia TROCHIDAE Rafmesque, 1815

Genus Jujubinus Monterosato, 1884

Type species (by subsequent designation of Crosse,

1885) Trochus matoni Payraudeau, 1826

Jujubinus errinae n. sp.

(Figs. 1-18,37)

Diagnosis. Small and slightly turriculate shell;

sculpture of incised spiral lines; strong prosocline

lamellae between spiral cords.

Examined material. The holotype (MZB60155)

and paratypes A-H (DiSBA) from the type loc-

ality: Strait of Messina, (38°14'45”N 15°37'36”E),

Sicily, Mediterranean Sea, dredging DG04, 100 m

depth; paratypes I (DiSBA) from 38°14'45" N,

15°37'28" E, dredging DG001, St 5, 90-115 m;

paratype L (DiSBA) from 38 0 13'27’’ N, 15°36'02"

E, dredging PIC02, Rada Paradiso, St 2, 90-115 m;

paratype M (WR) from 38°14'45" N, 15°37'28" E,

dredging DG001, St 5, 90-115 m; paratype N-R

(CS-PM) from 38°15'36" N, 15°43'08" E, 40-50 m

depth; paratypes S-U (GN); paratype V (RM)

from 38°15'36" N, 15°43'08" E, 40-50 m depth;

paratype X (BA) from 38°15'36" N, 15°43'08" E,

44 m depth; paratype Y (EQ), from 38°15'36" N,

15°43'08" E, 40-50 m depth.

Description of holotype. Shell of relatively

small size for the genus, height (H) 4.9 mm, width

(W) 4.0 mm, conical, slightly shiny. Protoconch

about 1.5 whorls, smooth, with a diameter of 280

pm. Teleoconch of 4.5 slightly convex whorls.

Sculpture of 6 closely set abapical spiral cords of

about the same strength, strongly carved by strong

tubercles, including the 2 peripheral ones forming

the basal cord, and 6 regularly spaced, basal spiral

cords narrow and well engraved, with very evident

lamellae in the interspaces. First two whorls of the

teleoconch showing the basal cord strongly rippled,

remaining teleoconch whorls with a flat basal cord.

Suture incised. Teleoconch surface covered by

barely visible prosocline growth striae, irregularly

set. Base convex, umbilicus closed and covered

with a white callus. Aperture quadrangular, with the

columellar callus thickened in the middle portion

and internally whitish nacreous. Colour of proto-

conch whitish, teleoconch reddish-creamy, with red

spiral cords interrupted by short white spots. The

same chromatic pattern is shown by the basal cords.

Animal unknown.

A new Jujubinus from the Mediterranean Sea

Variability. Shell H ranging from 4.5 to 6.0

mm and W from 3.8 to 4.7 mm. Protoconch dia-

meter from 260 to 290 pm. Teleoconch varying

from 4 to 4.5 whorls. Spiral and basal cords both

ranging from 5 to 6, according to the H of the

shell (6 in adult specimens). Umbilicus is closed

also in juveniles shells. Colours of protoconch,

teleoconch and base very constant in all speci-

mens observed.

Etymology. The species is named after Errina

aspera (Linnaeus, 1767) the Hydrozoan Stylas-

teridae whose beds characterize the type locality in

Strait of Messina, Sicily.

Distribution. Currently only known from the

type locality.

DISCUSSION

After the institution of the genus Jujubinus by

Monterosato (1884), in recent years an increasing

number of studies have greatly contributed to a bet-

ter knowledge of this group of small trochids, with

the description of new species and the rediscovery

of some not yet well understood ones (Bogi & Cam-

pani, 2005; Spanu, 2011; Mariottini et al., 2013;

Smriglio et al., 2014; Smriglio et al., 2015). With

this note we described/, errinae n. sp. (Figs. 1-18,

37), so increasing the number of the typical Juju-

binus species [i.e. shell with prosocline lamellae

between the spiral threads of variable strength,

often beaded (Monterosato, 1884)] to be quoted for

the Italian coast. The new taxon has been compared

Figures 1-3. Jujubinus errinae n. sp., holotype (MZB60155), 4.9 mm (H) x 4.0 mm (W), from type locality (Strait of

Messina), 100 m depth. Figures 4-5. Jujubinus errinae n. sp., paratype A (SG), 6.0 mm (H) x 4.7 mm (W) from type locality

(Strait of Messina), 100 m depth.

Carlo Smriglio etalii

Figures 7-15. Jujubinus errinae n. sp., holotype, SEM analyses, details of the shell. Figures 16-18. Jujubinus errinae n. sp.,

Strait of Messina, paratype R, 1.8 m (H) x 1.9 mm (W), CS-PM collection. Subadult specimen with basal cord sculptured

by very pronounced tubercles.

A new Jujubinus from the Mediterranean Sea

with three species showing a similar sculpture and

occurring in the near Sicily Channel, J. catenatus,

J. montagui and J. tumidulus (Curini & Palazzi,

1982). In particular, J. errinae n. sp. differs from/.

catenatus (Figs. 19-36), the most closely related

species which has an evident “pear-shaped” shell

outline and shows a stronger sculptured orna- men-

tation of the spiral cord interspaces, as well as a

different background colour, being uniformly red-

dish-greenish in J. catenatus , while the spiral cords

of J. errinae n. sp. are white-spotted producing a

typical shell pattern of irregular and interrupted

axial stripes. The new species differs from J.

montagui for its lower ratio H/W, the sculpture

more tuberculate and densely ornamented with

growth striae, producing a more jagged appearance

of the shell surface, and the different shell chro-

matic pattern. The shell colour of J. montagui is

generally whitish or greyish with irregular brown

axial stripes and basal cords with equally spaced

and alternate brown-white dashes (Scaperrotta et

al., 2010). Jujubinus errinae n. sp. differs from J.

tumidulus being greater in size, having a much

stronger sculpture, higher ratio H/W and a different

shell colour, which in the latter species is generally

uniformly creamy-whitish with brown spotted

spiral cords (Scaperrotta et al., 2009). Noteworthy,

the new taxon shows in the initial teleoconch

whorls the basal cord strongly rippled, which

becomes flat in the following whorls. This morpho-

logical feature, very evident in juvenile shells (Figs.

16-18), regularly disappears during the shell devel-

opment (Figs. 7-15). More generally, J. errinae n.

sp. differs from most of the Atlantic and Mediter-

Figures 19-21 .Jujubinus catenatus Ardovini, 2006. Sicily Channel. Figures 22-24. Jujubinus catenatus. Sicily Channel.

Carlo Smriglio etalii

Figures 25-32. Jujubinus catenatus Ardovini, 2006. Specimen of figure 19. Sicily Channel, SEM analyses, details of the

shell. Figure 33. Jujubinus catenatus. Strait of Messina, CS-PM collection. Subadult specimen. Figures 34-36. Jujubinus

catenatus. Specimen of figure 22. Sicily Channel, SEM analyses, details of the shell.

A new Jujubinus from the Mediterranean Sea

ranean Jujubinus species by its strongly tuberculate

and jagged teleoconch sculpture, with evident

lamellae in the interspaces and for its diagnostic

coloration (see Description), never observed in any

Recent Jujubinus distributed in Atlantic Ocean and

Mediterranean Sea.

The new species is known currently so far only

from the type locality, in the Strait of Messina, sug-

gesting to be another new endemism for this area

(Fig. 37). The Strait of Messina is a complex and

diversified environment having in the tidal-induced

upwelling its main physical constraint. The up-

welling, causing nutrient enrichment and temper-

ature lowering of surface water both supports ex-

ceptionally dense populations of suspension feeders

(Mistri & Ceccherelli, 1995; De Domenico et al.,

2009) and allows the settlement of Pliocene Atlantic

remnants (Fredj & Giaccone, 1995). In this area,

hard substrate corresponding to the Colantoni et al.

(1981) “ rough bottoms with pinnacles' 1 ’, are charac-

terized by dense and extensive colonies of the

Hydrozoan Stylasteridae Errina aspera, known

only for Gibraltar and the Messina Straits, which

hosts an abundant and peculiar benthic fauna of

Atlantic origin (Giacobbe & Spano, 2001;

Giacobbe et al., 2007). Such well-known associated

fauna was found in the sampled E. aspera beds

(DG001 and DG04; 90-115 m depth), together with

less frequent “accessory” species, as the bivalve

Spondylus gussoni O.G. Costa, 1829, and the here

described J. errinae n. sp. Such associated fauna

was also found deeper (St 02; 201 m depth), on

partially consolidated coarse sediment, colonized

by E. aspera together with the giant barnacle

4 -

Figure 37. Distribution of Jujubinus errinae n. sp.

Pachylasma giganteum (Philippi, 1836). Differ-

ently, the bathyal bottom sediment collected on the

Gioia Basin slope (St IB; 371 m), characterized by

terrigenous gravelly sands, showed a mixture of

autochthonous (bathyal) and allochthonous (sub-

tidal) bioclastic remains, which included J. errinae

n. sp. specimens. Interestingly, in the same geo-

graphical area is present Jujubinus curinii Bogi et

Campani, 2005, another endemism belonging to the

so-called “smooth” Jujubinus complex (Smriglio

et al., 2014 and references therein). Such co-occur-

rence of congeneric endemisms is not surprising,

since the two species are living in different habitats

whose peculiarities have been put in evidence in

literature. Jujuubinus errinae n.sp., as accessory

species in the E. aspera assemblages, might rep-

resent a further Atlantic relict fauna having in the

Strait of Messina its areal distribution.

ACKNOWLEDGEMENTS

Sincere thanks are due to Andrea Di Giulio and

Patrizio Tratzi (Dipartimento di Scienze, Universita

“Roma Tre”, Rome, Italy), for the SEM photo-

graphs carried out at the LIME. We would like to

express our gratitude to Massimo Appolloni (Museo

Civico di Zoologia, Rome, Italy) for the ex-

amination of the Jujubinus material kept in the

Monterosato collection. A special thanks to Walter

Renda (Reggio Calabria, Italy) for his great and

disinterested help in this research.

REFERENCES

Barbero Bianchi C.N., 2004. Proposta di suddivisione dei

mari italiani in settori biogeografici. Notiziario

SIBM, 46: 57-59.

Bogi C. & Campani E., 2005. Jujubinus curinii n. sp. una

nuova specie di Trochidae per le coste della Sicilia.

Bollettino Malacologico, 41: 99-101.

Colantoni R, Fabbri A. & Gallignani P., 1981. Seismic

stratigraphic interpretation of high resolution profiles;

some applied examples. Bollettino di Geofisica

Teorica e Applicata, 23: 89-106.

Curini M. & Palazzi S., 1982. Note ai Trochidae, V,

Jujubinus tumidulus (Aradas, 1846) (Mollusca,

Gastropoda). Naturalista Siciliano, 6: 67-80.

De Domenico F., Giacobbe S. & Rinelli P., 2009. The

genus Antedon (Crinoidea, Echinodermata) in the

Strait of Messina and the nearby Tyrrhenian Sea

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(Central Mediterranean). Italian Journal of Zoology,

76: 70-75.

Fredj G. & Giaccone G., 1995. Particularity des peuple-

ments benthiques du detroit de Messine. In:

Guglielmo L., Manganaro A. & De Domenico, E.

(Eds.). The Strait of Messina ecosystem, pp. 1 19—

128.

Giacobbe S. & Spano N., 2001. Pilumnus inermis

(Decapoda, Brachyura) in the Straits of Messina

(Mediterranean Sea): distribution and some aspects

of its ecology. Crustaceana, 74: 659-672.

Giacobbe S., Laria G. & Spano N., 2007. Hard bottom

assemblages in the strait of Messina: distribution of

Errina aspera L. (Hydrozoa: Stylasteridae). Rapports

Commission International Mer Mediterranee, 38:

485.

Gofas S. & Bouchet P., 2015. Jujubinus. Accessed

through: World Register of Marine Species at

http://www.marinespecies.org/aphia.php7pMaxde-

tails&id=138591 on 2015-09-12.

Mariottini P., Di Giulio A., Apolloni M. & Smriglio C.,

2013. Phenotypic diversity, taxonomic remarks

and updated distribution of the Mediterranean Juju-

binus baudoni (Monterosato,1891) (Gastropoda

Trochidae). Biodiversity Journal, 4: 343-354.

Mistri M. & Ceccherelli V.U., 1995. Produzione sec-

ondaria di organsmi coloniali di substrato duro: i

gorgonacei. S.IT.E. atti, 16: 463-465.

Monterosato T.A. di Maria di, 1884. Conchiglie littorali

mediterranee. Naturalista Siciliano, Palermo, 3: 102—

111 .

Scaperrotta M., Bartolini S. & Bogi C., 2009. Accresci-

menti. Stadi di accrescimento dei Molluschi marini

del Mediterraneo. I. L'lnformatore Piceno, Ancona,

167 pp.

Scaperrotta M., Bartolini S. & Bogi C., 2010. Accresci-

menti. Stadi di accrescimento dei Molluschi marini

del Mediterraneo. II. L'lnformatore Piceno, Ancona,

176 pp.

Smriglio C., Di Giulio A. & Mariottini P., 2014. Descrip-

tion of two new Jujubinus species (Gastropoda:

Trochidae) from the Sicily Channel with notes on the

Jujubinus curinii species complex. Zootaxa, 3815:

583-590.

Smriglio C., Mariottini P. & Oliverio M., 2015. A new

species of the Jujubinus curinii species complex: J.

alboranensis n. sp. (Gastropoda: Trochidae) from the

Alboran Sea. Iberus, 33: 151-157.

Spanu M.T., 2011. Prima segnalazione di Jujubinus

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ropoda: Trochidae) per la Sardegna e le acque

italiane. Bollettino Malacologico, 47: 135-137.

Biodiversity Journal, 2016, 7 (1): 67-78

Monograph

Check-list of the Nudibranchs (Mollusca Gastropoda) from

the biodiversity hot spot “Scoglio del Corallo” (Argentario

promontory, Tuscany)

Giulia Furfaro* & Paolo Mariottini

Dipartimento di Scienze, Universita “Roma Tre”, Viale G. Marconi 446, 1-00146 Rome, Italy

’Corresponding author: giulia.furfaro@uniroma3.it

ABSTRACT The Mediterranean nudibranch (Mollusca Gastropoda) fauna is part of complex communities

belonging to the Mediterranean endemic “Coralligenous”. This important ecosystem shows

a high species richness and functional diversity with assemblages of species tied together

by major trophic and ecological relationships. A first check-list for the biodiversity hot spot

“Scoglio del Corallo”, located along the coast of the Argentario promontory (Tuscany,

Tyrrhenian Sea) is here reported.

KEY WORDS Nudibranchs; biodiversity; check-list; Tyrrhenian Sea.

Received 28.01.2016; accepted 27.02.2016; printed 30.03.2016

Proceedings of the Ninth Malacological Pontine Meeting, October 3rd-4th, 2015 - San Felice Circeo, Italy

INTRODUCTION

Nudibranchs are molluscs brightly coloured and

frequently photographed by Scuba diver amateurs,

since these sea slugs can be found in most coastal

areas of the world, from polar to tropical waters.

The most Nudibranchia diversity is known for

shallow waters, ranging 0-30 m depth, but deep-sea

research is unravelling high levels of previously

unknown diversity of these molluscs at high depths

too (Valdes, 2008; Oskars et al., 2015). The Mediter-

ranean nudibranch diversity to date is of about 270

species, according to more recent checklists (Oztiirk

et al., 2014; Trainito & Doneddu, 2014), regional

faunal catalogues and Internet forum (WoRMS,

Sea-slug forum). Although Mediterranean nud-

ibranch species richness is smaller than that of the

Indo-Pacific biogeographic region or the Caribbean

Sea (Atlantic Ocean), the Mediterranean fauna has

a high level of endemic diversity. Their scarce

mobility in some cases leads them to live their

entire life cycle associated to their trophic source

and this is the reason why they are deeply related

to the most important endemic habitats of the semi-

closed Mediterranean Sea. In fact, they are common

inhabitants of the Mediterranean benthic ecosystem

defined as “Coralligenous” (Ballesteros, 2006),

where they livefeeding on a broad range of different

substrates (Sponges, Cnidarians, Bryozoans,

Tunicates and other sessile animals) (Gutierrez,

2015). These complex communities are composed

of a wide variety of suspension feeders, exhibiting

high species richness and functional diversity (Gili

& Coma, 1998). Recent molecular studies (e.g.,

Schrodl et al., 2011; Zapata et al., 2014) have

proposed a new classification on the base of the

polyphyly showed by this group that nowadays is

split into 3 different Suborders (WoRMS: Gofas,

2015). This work aims to produce the first compre-

hensive catalogue of the nudibrachs for the Biod-

Giulia Furfaro & Paolo Mariottini

iversity hot spot “Scoglio del Corallo”, located

along the coast of the Argentario Promontory

(Tuscany, Tyrrhenian Sea) (Figs. 1-3), based on a

fieldwork carried out by the authors in the last two

years. An annotated Nudibranch checklist is pro-

duced discussing taxonomic problems and new eco-

logical data (association with other organisms,

parasitism, cryptic species and geographical distri-

bution) whenever relevant. Each species observed has

been photographed in field and ecological and di-

stribution data are provided for all species recorded.

MATERIAL AND METHODS

Sampling area

“Scoglio del Corallo” is an underwater rocky hab-

itat located in the in National Park of “Arcipelago

Toscano” (42°23’60.00”N, 11°5 , 30.00”E, Central

Tyrrhenian Sea). This submarine formation out-

crops just for a few centimetres (depending on the

marine tide) from the surface and slopes down

vertically to a depth of 35 meters (Figs. 3,4). The

most relevant inhabitant of this area is the Octocoral

Corallium rubrum (Linnaeus, 1758) (Cnidarian), a

Mediterranean endemic species included in several

European and International protocols for conserva-

tion, like the FAO General Fisheries Commission

for the Mediterranean (GFCM) and the Convention

on International Trade in Endangered Species

(CITES). The presence of C. rubrum seems to be

closely related to the high level of biodiversity

characteristic of this area (Gili & Coma, 1998)

(Figs. 5-9). This site is very small in extent (about

500 m 2 ), but nevertheless characterized by a set of

rocks and walls forming canyons, caves and

platforms placed on a muddy substrate creating a

lot of microhabitats where a conspicuous number

of species live and reproduce (Fig. 5).

Protocol Sampling

Sampling took place between the years 2013 to

2015 as a part of a broader research project (“Pro-

ject Baseline Corallium rubrum ”, directed by the

“Global Underwater Explorer” No-Profit Organiza-

tion) aiming to produce the first characterization of

this biota and of its associated biocoenoses. The

produced preliminary data will become the starting

Figures 1-3. Study area. Location of the “Scoglio del

Corallo” (“Arcipelago Toscano”, 42°23’60.00”N,

1 1°5’30.00”E, Central Tyrrhenian Sea) in the Mediter-

ranean Sea.

Check-list of the Nudibranchs from the biodiversityhot spot “Scoglio del Corallo ” (Argentario promontory, Tuscany) 69

point for monitoring future environmental changes

and to evaluate possible conservation strategies.

Materials were sampled using SCUBA diving

techniques. Specimens were obtained by manual

collecting, photographed and fixed for future DNA

extraction and anatomical studies in 96 % ethanol.

Some species were observed and photographed on

their natural habitat during field campaigns, but not

captured.

RESULTS AND DISCUSSION

For the first time a Nudibranchs catalogue from

a Tyrrhenian Sea submarine hot spot of biodiversity

is here provided. A total of 23 species of nud-

ibranchs belonging to 9 different families were col-

lected during the project. Among these, 4 are

endemics of the Mediterranean Sea showing the

importance of this Mediterranean coralligenous as-

semblage. All collected species coexist in this small

area according to the high biodiversity showed by

this hot spot marine site. The list of the sampled

species is here reported, with notes on their ecology

and distribution according to OPK-Opistobranquis

(Available from http://opistobranquis.info/en/), Sea

Slug Forum (Australian Museum, Sydney, Avail-

able from http://www.seaslugforum.net/), World

from http://www.marinespecies.org at VLIZ), ‘'Sea

slug of the Algarve” (Calado & Silva, 2012), “Nud-

ihranchi del Mediterraneo ” (Trainito & Doneddu,

2014) and personal underwater observations.

Phylum MOLLUSCA

Classis GASTROPODA

Subclass HETEROBRANCHIA

Infraclass OPISTHOBRANCHIA

Order NUDIBRANCHIA

Suborder DEXIARCHIA

Infraorder CLADOBRANCHIA

Parvorder AEOLIDIDA

Familia FACELINIDAE Bergh, 1889

Genus Craten a Bergh, 1864

1. Cratena peregrina (Gmelin, 1791) (Fig. 10)

Ecology. This species commonly feeds on hy-

droids of the genus Eudendrium Ehrenberg, 1834

on which it usually lays eggs. Cratena peregrina

lives between a few meters from the surface till

about 50 meters depth.

Distribution. It has been found from Western

to Eastern basin of the Mediterranean Sea, in the

Portuguese and Andalusian Atlantic coasts and in

the Canary Islands. It was also informally recorded

from Senegal, South Africa, India and in Western

Atlantic.

Genus Facelina Alder et Hancock, 1855

2. Facelina annulicornis (Chamisso et Eysenhardt,

1821) (Fig. 11)

Ecology. This species has a varied diet con-

sisting on different genera of Hydrozoans: Eu-

dendrium Ehrenberg, 1834, Obelia Peron et

Lesueur, 1810, Pennaria Goldfuss, 1820 and Tubu-

laria Linnaeus, 1758.

Distribution. WoRMS (2015) recorded it from

Mediterranean Sea and Atlantic Ocean (Ireland,

United Kingdom, Azores, Portugal). The recent

work of Oztiirk et al. (2014) expands its distribution

range to the Turkish coasts of Aegean Sea.

3. Facelina rubrovittata (Costa A., 1866) (Fig. 12)

Ecology. The few pictures of this rare nud-

ibranch often show it staying on algae substratum.

On the diet of F. rubrovittata little is known but it

seems to feed on hydrozoans as well as most of the

aeolids do.

Distribution. It is distributed from the whole

Mediterranean Sea till the Atlantic coasts of Spain.

Familia FLABELLINIDAE Bergh, 1889

Genus Calmella Eliot, 1910

4. Calmella cavolini (Verany, 1846) (Figs. 13, 14)

Ecology. This aeolid species usually feeds on

Halecium pusillum Sars, 1856 and Eudendrium

racemosum (Cavolini, 1785) but can be found on

different substrates. This small nudibranch can be

easily misidentied with the sibling species Pisei-

notecus gaditanus Cervera, Garcia-Gomez et

Garcia, 1987 from which it can be recognized by

the absence, on its cerata, of the little white spots

typical of P. gaditanus. Interestingly we could

observe some individuals (Fig. 14) with very few

Giulia Furfaro & Paolo Mariottini

white dots, whose identification needs possibly a

DNA barcoding approach.

Distribution. This endemic species originally

was found only in the western coast of Mediter-

ranean Sea but on the base of recent records its dis-

tribution range now includes also the Turkish coasts

and the Atlantic coast of the Iberian Peninsula.

Genus Flabellina Gray, 1833

5 . Flabellina affinis (Gmelin, 1791) (Fig. 15)

Ecology. Flabellina affinis is a very common

species present all year long often feeding on colon-

ies of Eudendrium spp. and belongs to the complex

of the ‘pink Flabellinidae species’, see below F.

ischitana and F. pedata. This species usually co-

exists in the same arborescent hydrozoan colony

with C. peregrina and can be parasitized by Cope-

pods of the family Splanchnotrophidae, whose eggs

often can be seen extruding from the notum of the

host.

Distribution. This is one of the most common

European species ranging it from the eastern coast

of Mediterranean Sea to the Atlantic basin of Spain

and Portugal and in the Canarias islands.

6 Flabellina babai Schmekel, 1972 (Fig. 16)

Ecology. This species shows a large body size

atypical for a common ‘Flabellinid’. It can be found

easily on different substrates mostly on hydroids of

the genus Campanularia Lamarck, 1816, Eu-

dendrium Ehrenberg, 1834 and Bougainvilla

Lesson, 1 830, but is still unclear if it feeds on them.

Distribution. This species has been recorded

throughout the Mediterranean Sea and also in

Senegal.

7. Flabellina ischitana Hirano et Thompson,

1990 (Fig. 17)

Ecology. This species feeds on two different

species of athecate hydrozoans of the genus Eu-

dendrium , i.e. E. racemosum (Cavolini, 1785) and

E. glomeratum Picard, 1952 often coexisting with

F. affinis. They are morphologically very similar

and easily confused with each other and, as

mentioned above, both belong to the complex of the

‘pink Flabellinidae species’.

Distribution. Its distribution overlap with the

geographical range of F. affinis going from eastern

basin of Mediterranean sea to the Atlantic coast of

Iberian peninsula.

8. Flabellina lineata (Loven, 1846) (Fig. 18)

Ecology. Mediterranean specimens of this ‘Fla-

bellinid’ usually feed on Eudendrium spp. while the

extra-Mediterranean individuals were observed on

different species of hydroids like Tubularia indivisa

Linnaeus, 1758, Coryne eximia Allman, 1859, Hy-

drallmania falcata (Linnaeus, 1758) and Sertularia

argen tea Linnaeus, 1758.

Distribution. This species is distributed in the

Atlantic Ocean, from the Arctic Circle to the French

Atlantic coast, and in the European waters.

9. Flabellina pedata (Montagu, 1816) (Fig. 19)

Ecology. Flabellina pedata also belongs to the

complex of the ‘pink Flabellinidae species’, see

above, being very similar to F. affinis and F. is-

chitana from which differs on the base of possess-

ing single cerata, not clustered together on a single

peduncles, and by a smoothed rhinophores. It feeds

on athecate hydrozoans of genus Eudendrium

(especially in the Mediterranean Sea), but also on

sertularids of genus Abietinaria Kirchenpauer, 1884

and on the plumularid genus Aglaophenia Lamour-

oux, 1812. Recently was discover a new species

of Flabellinid, Flabellina albomaculata Pola,

Carmona, Calado et Cervera, 2014, very similar to

F. pedata and easily confused with it.

Distribution. This common Flabellinid is dis-

tributed from eastern basin of the Mediterranean

Sea to the Strait of Gibraltar and in the Atlantic

Ocean from the Azores to the North Atlantic Coast

of Norway.

Parvorder CLADOBRANCHIA

Familia PROCTONOTIDAE Gray, 1853

Genus Janolus Bergh, 1884

10. Janulus cristatus (Delle Chiaje, 1841) (Fig. 20)

Ecology. This species lives between 10 and 40

m deep on a rocky substrate. Usually it was asso-

ciated to different Bryozoans on which J. cristatus

seemed to feed on. Alcyonidium gelatinosum (Hud-

Check-list of the Nudibranchs from the biodiversityhot spot “Scoglio del Corallo ” (Argentario promontory, Tuscany) 7 1

son) J.V. Lamouroux, Bicellariella ciliata (Lin-

naeus, 1758), Bugulina avicularia (Linnaeus,

1758), B. flabellata (Thompson in Gray, 1848), B.

turbinata (Alder, 1857), Bugula neritina (Linnaeus,

1758) and species of genus Cellaria Ellis et Solan-

der, 1786 were cited as a presumed preys.

Distribution. It is commonly found throughout

the Mediterranean Sea and in the North-eastern

Atlantic Ocean from Norway to Morocco coasts.

Parvorder DENDRONOTIDA

Familia TRITONIIDAE Lamarck, 1809

Genus Marionia Vayssiere, 1877

11 .Marionia blainvillea (Risso, 1818) (Fig. 21)

Ecology. It is recorded to feed on different

preys like Alcyonium acaule Marion, 1878, A. pal-

matum Pallas, 1766, Eunicella cavolinii (Koch,

1887), E. singularis (Esper, 1791), Eunicella sp.,

Leptogorgia sarmentosa (Esper, 1789), Para-

muricea clavata (Risso, 1826). The juveniles have

different body colours; in particular they are com-

pletely white while the adults range in colour from

a pale translucent orange to a deeper reddish brown

with irregular white patches. They can be parasit-

ized by Copepods like the ectoparasitic Doridicola

comai Conradi, Megina et Lopez-Gonzalez, 2004

and the endoparasitic Linaresia bouligandi Stock,

1979 and L. mammillifera Zulueta, 1908.

Distribution. Its geographical range goes from

the whole Mediterranean Sea to the North-eastern

and South-eastern Atlantic Ocean (Angola).

Genus Tritonia Cuvier, 1798

12. Tritonia manicata Deshayes, 1853 (Fig. 22)

Ecology. This species lives in shallow and very

bright waters between the rhizomes of Posidonia

oceanica (Linnaeus) Delile, 1 8 1 3 or on a rocky sub-

strates where it can find a lot of Anthozoan (Cnid-

aria) species. The Stoloniferous group is the one on

which T. manicata seems to feed on, in particular

on genus Cornularia Lamarck, 1816 and Clavu-

laria Greville, 1865.

Distribution. Present along the coasts of the

Mediterranean Sea and also recorded from coast of

Morocco and North- Atlantic British islands.

13. Tritonia striata Haefelfmger, 1963 (Fig. 23)

Ecology. This species lives in shallow waters

on rocky substrates full of algae, sponges and cnid-

arians. It has been recorded to feed on the soft coral

Paralcyoniums pinulosum Delle Chiaje, 1822.

Distribution. Tritonia striata is known to be

endemic of the Mediterranean Sea but recently it

has been also recorded from the Gulf of Biscay in

North Atlantic Ocean.

Suborder EUCTENIDIACEA

Infraorder DORIDACEA

Familia ONCHIDORIDIDAE Gray, 1827

Genus Diaphorodoris Iredale et O'Donoghue, 1923

14. Diaphorodoris papillata Portmann et Sand-

meier, 1960 (Fig. 24)

Ecology. It feeds on Bryozoans so it is often

observed in habitats rich in algae and sessile inver-

tebrate fauna.

Distribution. This species is endemic of the

Mediterranean Sea but recorded also from coasts of

Portugal and Strait of Gibraltar.

15. Diaphorodoris luteocincta var. alba (M.

Sars, 1870) (Fig. 25)

Ecology. It is reported to feed on different bryo-

zoans genus Smittina Norman, 1903, Cellepora

Linnaeus, 1767 and Crisia Lamouroux, 1812. It

can be found in a rock walls hosting bryozoans,

scyaphilic algae, hy droids and sponges.

Distribution. There are two different morpho-

types referring to D. luteocincta var. alba and D.

luteocincta var. reticulata on the base of a dorsal

notum completely white (var. alba) or red coloured

(var. reticulata). These two morpho variants share

the same wide distribution inhabiting the Mediter-

ranean Sea and North-Eastern Atlantic Ocean

(Trainito & Doneddu, 2014).

Familia POLYCERIDAE Alder et Hancock, 1845

Genus Polycera Cuvier, 1816

16. Polycera quadrilineata (O. F. Muller, 1776)

(Fig. 26)

Ecology. Different species of Bryozoans were

reported to be the substrate (possibly food) of the

Giulia Furfaro & Paolo Mariottini

P. quadrilineata. This species lives in a rocky hab-

itats where is relatively common. This species is

often parasitized by Copepod Crustaceans belong-

ing to the genus Splanchnotrophus Hancock et

Norman, 1863 with the injection of its eggs into the

body tissues of its host.

Distribution. This species is distributed in

Western Europe from Iceland and Greenland to the

entire Mediterranean Sea.

Familia CHROMODORIDIDAE Bergh, 1891

Genus Felimare Ev. Marcus et Er. Marcus, 1967

17. Felimare fontandraui (Pruvot-Fol, 1951)

(Fig. 27)

Ecology. Felimare fontandraui feeds on Sponges

belonging to the genus Dysidea Johnston, 1842.

This species can be found during all the year from

the intertidal zone to about forty meters deep. It is

very variable in colour morphs and some specimens

can be misidentified with the sister species Feli-

mare tricolor (Cantraine, 1835) from which can be

recognized by the presents of a white basal spots on

the rhinophores and other diagnostic characters.

Distribution. Its distribution ranges from both

the eastern and western Mediterranean basins to the

North-eastern Atlantic coasts.

18. Felimare picta (Schultz in Philippi, 1836)

(Fig. 28)

Ecology. This species feeds on different sponges

like species belonging to genus Ircinia Nardo, 1833,

Crella Gray, 1867 and Dysidea Johnston, 1842.

This common species lives on rocky substrate and

shows different colour morphotypes described in

the past like different subspecies.

Distribution. Felimare picta has a wide spread

distribution. It lives from the western coast of the

Atlantic Ocean, Brazil and Florida, to the eastern

Atlantic, Spanish and African coast as well and in

the entire Mediterranean Sea.

19 . Felimare tricolor (Cantraine, 1835) (Fig. 29)

Ecology. Felimare tricolor lives in rocky sub-

strates from intertidal zone to about hundred meters

deep. It feeds on different genera of sponges;

Dysidea Johnston, 1842, Scalarispongia Cook et

Bergquist, 2000 and Spongia Linnaeus, 1759.

Distribution. This common species is distribu-

ted in the Mediterranean Sea and in the North-ea-

stern Atlantic Ocean.

Genus Felimida Ev. Marcus, 1971

20 Felimida krohni (Verany, 1846) (Fig. 30)

Ecology. This species has a morphology si-

milar to the sister species Felimida britoi (Ortea&

Perez, 1983), from which can be recognized by

differences in the shape of the rhinophores and the

mantle colour pattern. Its bathymetric range goes

from subtidal zone down to 50 meters depth

where it lives on different sponges like Hymenia-

cidon perlevis (Montagu, 1814) and species of

genus Ircinia Nardo, 1833. Its diet is still not

clear.

Distribution. The distribution of this species

goes from the eastern basin of the Mediterranean

Sea to the Strait of Gibraltar. It lives also in the

North eastern Atlantic Ocean from Canary Islands

and north coasts of Africa to the Atlantic coasts of

Spain and France.

21. Felimida luteorosea (Rapp, 1827) (Fig. 31)

Ecology. It lives under stones and on illumin-

ated precoralligenous walls from 10 to 50 meters

deep. It is reported to feeds on sponges like

Aplysilla rosea (Barrois, 1876) and Spongionella

pulchella (Sowerby, 1804).

Distribution. It is distributed in the Mediter-

ranean Sea and in the North Atlantic Ocean from

the north coast of France and Spain to Angola and

Canary islands.

Familia DISCODORIDAE Bergh, 1891

Genus Peltodoris Bergh, 1880

22. Peltodoris atromaculata Bergh, 1880 (Fig. 32)

Ecology. This common nudibranch lives on

rocky bottoms usually associated to its prey, the

sponge Petrosia ( Petrosia ) ficiformis (Poiret, 1789).

It is extremely abundant in the coralligenous where

it lives searching for its food or staying on it. This

sea slug is very sedentary so it can be found on the

same sponge for different days.

Check-list of the Nudibranchs from the biodiversityhot spot “Scoglio del Corallo ” (Argentario promontory, Tuscany)

Figures 4-9. Underwater photographs of the “Scoglio del Corallo”, showing

the Cor allium rubrum assemblages.

Giulia Furfaro & Paolo Mariottini

Figures 10-15. Fig. 10: Cratena peregrina (Gmelin, 1791). Fig. 11: Facelina annulicornis (Chamisso et

Eysenhardt, 1821). Fig. 12: Facelina rubrovittata (Costa A., 1866). Figs. 13,14: Calmella cavolini (Verany,

1846). Fig. 15: Flabellina affinis (Gmelin, 1791).

Check-list of the Nudibranchs from the biodiversityhot spot “Scoglio del Corallo” (Argentario promontory, Tuscany) 75

Figures 16-21. Fig. 16: Flabellina babai Schmekel, 1972. Fig. 17. Flabellina ischitana Hirano et Thompson,

1990. Fig. 18. Flabellina lineata (Loven, 1846). Fig. 19: Flabellina pedata (Montagu, 1816). Fig. 20: Janulus

cristatus (Delle Chiaje, 1841). Fig. 21: Marionia blainvillea (Risso, 1818).

Giulia Furfaro & Paolo Mariottini

Figures 22-27. Fig. 22: Tritonia manicata Deshayes, 1853. Fig. 23: Tritonia striata Haefelfmger, 1963. Fig. 24:

Diaphorodoris papillata Portmann et Sandmeier, 1960. Fig. 25: Diaphorodoris luteocincta var. alba (M. Sars,

1870). Fig. 26: Polycera quadrilineata (O. F. Muller, 1776). Fig. 27: Felimare fontandraui (Pruvot-Fol, 1951).

Check-list of the Nudibranchs from the biodiversityhot spot “Scoglio del Corallo” (Argentario promontory, Tuscany) 77

Figures 28-33. Fig. 28: Felimare picta (Schultz in Philippi, 1836). Fig. 29. Felimare tricolor (Cantraine, 1835).

Fig. 30: Felimida krohni (Verany, 1846). Fig. 31: Felimida luteorosea (Rapp, 1827). Fig. 32: Peltodoris at-

romaculata Bergh, 1880. Fig. 33: Phyllidia flava Aradas, 1847.

Giulia Furfaro & Paolo Mariottini

Distribution. This is one of the most common

species of the Mediterranean Sea. It is also recorded

from Western Atlantic Ocean from Portuguese

coasts to Canary Islands.

Familia PHYLLIDIIDAE Rafinesque, 1814

Genus Phyllidia Cuvier, 1797

23 . Phyllidia flava Aradas, 1847 (Fig. 33)

Ecology. This interesting sea slug has a charac-

teristic body colour that can camouflage it when it

is associated to sponges like Axinella cannabina

(Esper, 1794), A. polypoides Schmidt, 1862 and

Acanthella acuta Schmidt, 1862. It has been known

to feed on the latter sponge.

Distribution. This species is rare and distrib-

uted throughout the Mediterranean Sea, it has been

also recorded from the Canary Islands.

AKNOWLEDGEMENT

The authors gratefully acknowledge the GUE

instructor Luca Malentacchi (Arezzo, Italy), the

“Project Baseline Cor allium rubrum ” manager, for

its help during sampling and monitoring and for

providing underwater photographs and videos.

Thanks to the big community of volunteers that

work for “Project Baseline Corallium rubrum ”.

We are indebted to Monica Valdambrini (Arezzo,

Italy), Massimiliano Falleri, Massimiliano Orsi and

Gianluca Cireddu (Rome, Italy, Italy) for providing

underwater photographs. We thank people from

“Gruppo Malacologico Mediterraneo” (Rome,

Italy) for their assistance during samplings. GF and

PM wish to thank the University of Roma Tre for

financial funding.

REFERENCES

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ography and Marine Biology: An Annual Review, 44:

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25/10/2012 Accessed: 17/11/2015 at (http://opisto-

branquis.info/en/#gse.tab=0).

Calado G. & Silva J.P., 2012. Sea slug of the Algarve -

Opisthobranch Guide for the Southern Coast of

Portugal. Ed. Subnauta, Lisbon, 164 pp.

Gili J.M. & Coma R., 1998. Benthic suspension feeders

in marine food webs. Trends in Ecology & Evolution,

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&id=1762

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quias M.A.E. & Narciso S., 2015. The opistho-

branch gastropods (Mollusca: Heterobranchia) from

Venezuela: an annotated and illustrated inventory of

species. Zootaxa 2: 201-256, doi.org/10.11646/zoo-

taxa. 4034.2.1

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new phylogeny of the Cephalaspidea (Gastropoda:

Heterobranchia) based on expanded taxon sampling

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Mediterraneo. Ed. 11 Castello, Milano, 192 pp.

Valdes A., 2008. Deep sea “cephalaspidean” hetero-

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(Eds.), Tropical Deep-Sea Benthos 25. Memoires du

Museum national d’Histoire naturelle, 196: 587-792.

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rspb. 2014.1739

Biodiversity Journal, 2016, 7 (1): 79-88

Monograph

Barycypmea teulerei (Cazenavette, 1 845) (Gastropoda Cypraeidae):

a successful species or an evolutionary dead-end?

Marco Passamonti

Dipartimento di Scienze Biologiche Geologiche e Ambientali (BiGeA), Via Selmi 3, 40126 Bologna, Italy; email: marco.

passamonti@unibo.it

ABSTRACT Barycypraea teulerei (Cazenavette, 1845) (Gastropoda Cypraeidae) is an unusual cowrie

species, showing remarkable adaptations to an uncommon environment. It lives intertidally

on flat sand/mud salt marshes, in a limited range, in Oman. On Masirah Island, humans

probably drove it to extinction because of shell collecting. A new population, with a limited

range, has recently been discovered, and this article describes observations I made on site in

2014. Evolution shaped this species into a rather specialized and successful life, but has also

put it at risk. Barycypraea teulerei is well adapted to survive in its habitat, but at the same

time is easily visible and accessible to humans, and this puts it at high risk of extinction.

Evolution is indeed a blind watchmaker that ‘ has no vision, no foresight, no sight at all' . And

B. teulerei was just plain unlucky to encounter our species on its journey on our planet.

KEY WORDS Cypraeidae; Barycypraea teulerei ; Biology; Evolution; Blind Watchmaker.

Received 23.02.2016; accepted 22.03.2016; printed 30.03.2016

Proceedings of the Ninth Malacological Pontine Meeting, October 3rd-4th, 2015 - San Felice Circeo, Italy

INTRODUCTION

“ Natural selection, the blind, unconscious, auto-

matic process which Darwin discovered, and which

we now know is the explanation for the existence

and apparently purposeful form of all life, has no

purpose in mind. It has no mind and no mind's eye.

It does not plan for the future. It has no vision, no

foresight, no sight at all. If it can be said to play the

role of watchmaker in nature, it is the blind watch-

maker".

R. Dawkins, The Blind Watchmaker, 1986.

Barycypraea teiderei (Cazenavette, 1845) (Gast-

ropoda Cypraeidae) (Fig. 1) is one of only two relic

species of the genus Barycypraea Schilder, 1927,

along with the South African Barycypraea fultoni

(Sowerby III, 1899) (Fig. 2). This genus is charac-

terized by squat, heavy shells with a roughly trian-

gular/pyriform shape. The mantle is always thin and

almost transparent, whitish or pale brown, with

little (. B . fultoni ) or no papillae (B. teulerei ). Both

species appear to be well adapted to sand and/

or mud bottoms, although at very different depths.

Barycypraea fultoni is a deep water species (Ber-

gonzoni, 2012) while, as we will see in detail, B.

teiderei is an intertidal one.

The genus comprises few fossil species, among

them B. ziestmani Liltved et Le Roux, 1988 from

the Alexandria Formation (Neogene), Port Eliza-

beth, S. Africa (Liltved, 2000), and the B. caputvi-

perae species-complex from Indonesia (Miocene).

The genus Barycypraea is morphologically and ge-

netically linked to the genus Zoila Jousseaume,

Marco Passamonti

1884, which is endemic to Western and Southern

Australia. In this sense, the entire evolution of this

cowrie lineage has always been strictly related to

the Indian Ocean basin. The supposed similarity to

the Venezuelan/Colombian Muracypraea mus

(Linnaeus, 1758) and other allied fossil species of

the Caribbean genus Siphocypraea Heilprin, 1897

[f.i. S. problematica (Heilprin, 1887)], seems not

fully supported by molecular studies (Meyer,

2004).

A STORY OF A ONCE RARE SPECIES

Barycypraea teulerei was once an extremely

rare species. In 1964, only 35 specimens were

present in European collections (Schilder, 1964).

Since 1969, only guesses were available about its

distribution and habitat, since no one had ever

reported a precise locality for the species. Speci-

mens were labeled from different localities, includ-

ing the Persian Gulf, Hormuz Strait, Aden, Arabian

Sea, Red Sea, Port Sudan etc. (see Scali, 2013 for a

detailed list), but in fact, no one knew where this

species came from.

In March 1969, the very first specimens of B.

teulerei were collected at Masirah Island (wrongly

reported as Museera Island; Cross, 1969), a very re-

mote island along the Oman coastline. Barycypraea

teulerei appeared to live in very shallow water on

sand/mud beds, and even outside the water during

low tide. Since then, several malacologists made

their way to Masirah to obtain specimens (see f.i.

Williams, 1969; Luther, 1972; Charter, 1983) which

soon became available for study and collection. One

of the main sources was actually Dr. Donald ‘Don’

T. Bosch, who had a long service as a surgeon for

the Sultanate of Oman. Dr. Bosch was the only

surgeon in the entire country of 1 .5 million people,

and contributed to the modernization of health care

in Oman. In recognition of his achievements, the

Sultan of Oman awarded him with the "Order of

Oman" in 1972. Don was also an extensive shell

collector and a pioneer of Oman malacology. Many

Oman species have been named by or after him

(e.g. Conus boschi Clover, 1972, Cymatium boschi

Abbott et Lewis, 1970, etc.), and he also dedicated

some to his wife Eloise (e.g. Acteon eloisae Abbott,

1970). Because of Don Bosch and other shell col-

lectors, thousand of specimens were easily available

for a while, and the species became quite common

in collections.

Eventually, in the early 90s, new fresh-collected

B. teulerei began to disappear. By then, many col-

lectors traveled to Masirah to collect specimens,

without success. The species seemed to have simply

vanished, probably due to over-collection and the

relative ease of finding specimens by simply

walking the flat beaches of the Island. Rumors were

growing that this species had to be considered

extinct.

In December 2012, after some unsuccessful trips

to Oman, B. teulerei was found again by Massimo

Scali and his family along the coastline of Oman

(Scali, 2013; 2014), in a locality kept secret since

then. The population was very healthy, with several

thousand specimens freely grazing on a muddy flat

bottom. Again, it was confirmed that this species

lives in the intertidal zone. At low tide, B. teulerei

does not hide itself under stones, as most cowries

would do, and it is quite often completely exposed.

In figure 3 you can see some in situ specimens

during the sygyzian tide of 2014.

In December 2014, I was fortunate enough to

join Massimo in his field trip to see this species on

site. This article is basically a series of observations

Eve made that I hope will be of interest to the

readers. I will discuss some of the aspects of the

biology of this species, and I will express some con-

siderations about its evolution.

THE HABITAT

Once I arrived at the place during the sygyzial

tide of December 2014, 1 soon realized we were in

an unusual habitat for a cowrie species. What I saw

was basically a muddy salt marsh, covered with

patches of algal mats and a few dark gray and

orange sponges (Figs. 4, 5). No rock or evident

coral to be found for kilometers. The only available

hard substrate was a few Pinna sp. standing out of

the bottom and a few dead bivalve shells. The mud

was very anoxic, dark colored and stinking of sul-

fur. It was hard to walk on, at every step I remained

glued in the mud. Despite this environment seeming

quite inhospitable, a few minutes walking from the

beach I found the first living B. teulerei. This mud

flat is a relatively large area and we were walking,

on average, 10-15 kilometers per day to observe B.

Barycypraea teulerei (Gastropoda Cypraeidae): a successful species or an evolutionary dead-end?

Figure 1 . Barycypraea teulerei. Examples of variability of pattern of the species. Oman. Photo courtesy Massimo Scali and

Beautifulcowries Magazine. Figure 2. Barycypraea fultoni. Examples of pattern and variability of the species. Mozambique

and South Africa. Photo courtesy Mirco Bergonzoni and Beautifulcowries Magazine.

Marco Passamonti

teulerei in situ. The other animals I was able to see

were crabs, cuttlefishes, many bivalves, muricids,

and some other cowrie species. Nevertheless, B.

teulerei is by far the most common species in this

environment. Its distribution is not even, however.

Barycypraea teulerei tends to aggregate, and you

can find dozens of specimens together in the same

patch, then walk for minutes and not find one. What

I observed is that the animals are active during the

daytime, especially the small ones that I think may

be males (see below). In many cases, they are

heedless of being completely outside of the water.

Walking on the flat for hours, I was also able to ob-

serve a few species of sea birds including small

waders, flamingos and seagulls.

In comparing this to the previous known habitat

of B. teulerei (which I indeed visited), the main dif-

ference is that at Masirah Island the sediment is

sand, and the bottom is not anoxic. In Masirah, the

above-mentioned algal mats and sponges are nowa-

days very rare, and the area looks more like a big

sandy beach with scattered rocky patches. Never-

theless historical records, as well as a few very dead

shells, witness that the area once hosted B. teulerei.

My guess is that, besides collection pressure, there

could have been some environmental change.

Figure 3. Barycypraea teulerei wandering on a mud flat

outside water at sygyzial low tide in December 2014.

Oman.

Figure 4. The typical environment, at low tide, where

Barycypraea teulerei are commonly found. Please note

the algal patches. Oman. Figure 5. A close look of the

sponge, common in the area, on which Barycypraea teulerei

was seen eating. Oman.

Barycypraea teulerei (Gastropoda Cypraeidae): a successful species or an evolutionary dead-end?

In my opinion, B. teulerei needs the presence

of sponges to establish a healthy population. Dur-

ing my observations, I was able to see a B. teulerei

feeding on a dark gray/black sponge (Fig. 5), so I

can confirm this species is spongivorous. How-

ever, I cannot exclude it feeding on algae too, but

I have not seen any doing so. This is another char-

acteristic that joins B. teulerei to the spongivorous

Zoila.

REPRODUCTION AND LIFE CYCLE

Two other things are, in my opinion, necessary

for B. teulerei to establish a healthy population.

Firstly, dead bivalve shells. Barycypraea teulerei

uses these shells to nest its eggs. When a female is

brooding eggs (as all cowries do), she hides herself

and the eggs on the underside of the valve. Females

are hidden by the bivalve shell, but you can spot

them because several males are commonly found

close to them (Fig. 6). Females, on average, tend to

be bigger than males, although this is not always

true. Massimo Scali also spotted a male fecundating

a female on eggs (Fig. 7). This may be an indication

that eggs are fecundated while females lay them, and

a reason why males compete for laying females.

Egg clusters are comprised of transparent cap-

sules with brownish eggs inside. Immature capsules

contain many eggs, but as development continues,

only a few embryos per capsule are found. Embryos

are easy to spot because they already have a formed

shell (Fig. 8). Likely most of the eggs inside the

capsule are only for embryo nutrition (nurse cells

or intracapsular cannibalism?). It is therefore

evident that this species has direct development and

only one (or a few) newborns are hatching from

each capsule. Direct development is, in cowries,

considered an adaptation when a species depends

on a limited food source (in this case sponges), so

that newborns hatch close to their food source

instead of being spread throughout wide areas as

veligers. This direct development is again another

similarity to Zoila.

When we arrived in December, many speci-

mens were brooding eggs and we seemed to be

right in the middle of the reproductive season. Air

temperatures in Oman during December are not ex-

tremely hot, and during the day can reach 25-30°C.

However, at night it can be as cold as 10°C or less.

Figure 6. The typical behavior of a female breeding eggs.

Above: the female is hidden under a dead bivalve shells,

and two males are trying to fecundate. Below: same an-

imals, after I turned the bivalve to make the female visible.

Oman.

Figur 7. A male Barycypraea teulerei fertilizes with his penis

(A) a female that sits on a bivalve shell (B). Oman. Photo

courtesy Massimo Scali.

Marco Passamonti

Figure 8. Two views of egg clusters inside bivalve shells.

Please note that each capsule may contain different numbers

of brownish eggs, and as soon as the embryos get bigger,

the number of them decreases. Intracapsular cannibalism?

Oman. Photo courtesy Massimo Scali and Beautifulcowries

Magazine.

Our time at the site was basically the coldest part

of the year, and I guess this is the main reason why

B. teulerei reproduce during winter. This species is

intertidal, so it is strongly influenced by solar heat

and desiccation, and winter is the time of the year

in which that is least likely to happen. The mud

itself may also help in maintaining mollusk wetness

and lowering temperature during air exposure.

Moreover, water patches and little canals are still

present in the mud flat, and some specimens (espe-

cially males) seem to take refuge in these when the

tide is very low. Finally, almost no specimen

showed an expanded mantle, and this is certainly a

behavior for retaining moisture and reducing de-

hydration.

Another surprising observation, confirmed by

previous reports at Masirah, is that we couldn’t find

any juvenile B. teulerei. All specimens were adults

or, slightly sub-adult. Another important observa-

tion is that while adults are very visible and active,

sub-adults are more mimetic and tend to hide

below the algal mats. The fact that no young B.

teulerei were found points sharply to the possibility

that this species has a synchronized life cycle, and

all reproducing mollusks found are the ones born

from eggs of the previous year. Moreover, another

observation is important: although B. teulerei shells

are very heavy, no shell seems gerontic and most

of them are undamaged. It seems likely they had

no time to be damaged, and maybe this is because

all those reproducing shells are just one year old

and reached sexual maturity only a few weeks

before we arrived.

If my hypothesis is correct, this would mean that

B. teulerei is a cowrie with a very fast life cycle.

Soon after December/January they hatch as small

crawling snails. The snails, having thin shells,

protect themselves from predators and desiccation

by hiding inside the algal mats, which are actually

quite intricate, and I guess these may also help in

cooling the mollusks during the hot season low

tides. Sponges are too small to be a suitable refuge

even for the youngest snails. They develop this way

until the beginning of the next reproductive season,

when they complete development and start wander-

ing for dead bivalve shells (if female) or other

females (if males). Again, this peculiar life cycle, if

confirmed, coincides quite remarkably with Zoila.

Actually, Zoila newborns are very cryptic, as they

hide inside sponges as protection from predation,

and they only venture out into the open during

reproductive season, when they reach adulthood

and shells get thicker. Zoila friendii, for instance,

broods eggs in the open (personal observation) just

as B. teulerei does.

The complete development of B. teulerei is there-

fore spanning along the hot season. Oman is very

hot during summer, easily reaching 40° C or more.

I may imagine that, especially during low tide, the

water could reach a very high temperature. Please

Barycypraea teulerei (Gastropoda Cypraeidae): a successful species or an evolutionary dead-end?

Figure 9. Examples of the variability of the dorsum in Barycypraea teulerei, some resembling a false aperture. Oman.

remember that this is a large lagoon flat and that the

open ocean, which may be cooler, is quite distant.

It is quite unbelievable, but apparently young B.

teulerei are able to deal with these harsh conditions

and reach adulthood with good success. A possib-

ility is that B. teulerei migrates into shallow waters

only to reproduce, and lives most of the year in

deeper waters, where conditions are more stable. I

do not think this is the case, because this species is

not capable of fast movement, and the mud flat is

several kilometers wide. Plus, I found most indi-

viduals very far from the deeper areas (actually the

closer we searched to the open ocean, the less spe-

cimens were found). Moreover, it is unlikely that

young B. teulerei are able to migrate back to the

deeper water during their development, when they

Marco Passamonti

are most vulnerable due to their thin shells. We also

dredged for a few hours along the edge of the

flat at a depth of 5-10 meters, and we found no B.

teulerei , not even dead ones.

Finally, what is the fate of the specimens that

reached the first reproductive season? Do they

survive to the next year? Is this species annual or

not? Hard to say, but the fact that I could see very

few damaged and no gerontic shells suggests that

this species is rather annual, and after reproduction

B. teulerei dies. If this is true, the population

renews itself every year. It may seem strange that

a mollusk forms such a hard, heavy shell in only

one year, but there is no biological reason to

disregard this hypothesis. On the other hand, it is

true that we found very few dead shells, and there

should be many more if they all die each year. It

is also true that they can be easily burrowed into

the soft mud bottom, so they would easily disap-

pear. Nevertheless some dead shells are found

beached as well.

PREDATION

How does B. teulerei deal with predators? As

we mentioned, this species lives in open

sand/mud flats, and they do not hide when adult.

Moreover, several hundred specimens are found

in relatively small areas. Barycypraea teulerei

actually seems quite a successful species and, in

fact, it is by far the most common cowrie in that

particular habitat. Its behavior is quite the oppos-

ite of other cowries inhabiting the same area, f.i.

Naria turdus (Lamarck, 1810) and Palmadusta

lentiginosa (J.E. Gray, 1825), which are found

hiding inside the algal coating of the numerous

Pinna sp. found on the muddy bottom. And this

is not because they are smaller, since some local

N. turdus may be as big as B. teiderei, and with a

similarly thick shell.

Among candidate predators, I may mention

seagulls and crabs, which are common in the area,

as well as other mollusks. However, very few shells

(almost none) show signs of predation, and I have

not seen any cracked shells on site or beached. Dead

shells are also very rare, and when found, they do

not show any sign of attack. It seems that predators

are completely ignoring B. teulerei , an observation

that was quite puzzling. Why should this species not

be predated, and why does it actually seem to ignore

predators? Is B. teulerei toxic, poisonous, or have a

disgusting taste? Hard to say, but as far as I know,

no toxic cowrie has ever been reported in literature.

It is not unconceivable that perhaps they become

toxic, repellent or disgusting by absorbing sub-

stances from their food sponges. Only targeted

chemical analyses would possibly solve this issue.

Some clues may also come from the shell. As

mentioned, B. teulerei has a very heavy shell. Its

thickness is certainly an adaptation to prevent

cracking by fishes, crabs or sea birds, as well as

drilling by muricids or naticids. Moreover, its

squat shape might also be an adaptation to per-

fectly adhere it to the bottom (as in many other

cowries). However, I may also argue that the

peculiar pattern of the dorsum could have an ad-

aptive function, although this is just a guess.

In fact, even if the dorsum is characterized by a

variable pattern (basically no two specimens are

alike), most shells show a neat double dorsal line,

framing a central groove, especially when the shell

is thicker. More uncommonly, they show a dark

blotch in the middle of the dorsum. Other kinds of

patterns are rarer. In figure 9 you can see an over-

view of the variability of the dorsal patterns. Con-

trarily to the dorsum, the mouth is quite wide and

uncolored. Considering all this, my guess is that

the flashy dorsal color in this species might be

either an aposematic coloration (in case the mol-

lusk is toxic or has a bad taste), or, maybe, could

represent a sort of ‘false aperture’ that may distract

sea birds from the vulnerable parts of the animal.

I may imagine seabirds being fooled and peck at

the dorsum of the cowrie, which is actually a very

hard part of the shell, completely disregarding the

real aperture, where the mollusk would be more

vulnerable. Of course this is just a guess, but it is

of course not the first such case known in nature:

for instance, you may find something similar in

false eyes of fishes, which are adaptations to drive

predators’ attacks to parts of the body that are less

sensitive or critical for survival.

Finally, please also note that this species has no

teeth along its aperture, a characteristic that is very

rare in cowries, even if some specimens may have

some little denticles. Teeth in cowries have a par-

ticular function, i.e. to narrow the aperture to pre-

vent attacks from predators, since cowries have

no operculum. Evidently this species has no need

Barycypraea teulerei (Gastropoda Cypraeidae): a successful species or an evolutionary dead-end?

for teeth, and teeth, which are found in all other

Barycypraea , are on their way to being lost. This is

a very well known evolutionary process: no select-

ive constraints (i.e. no need for teeth) allow accu-

mulation of mutations, which result in the gene

products having less or no function (i.e., the genes

or the proteins involved in teeth production being

partially or wholly inactivated).

AN EVOLUTIONARY DEAD END?

All this considered, B. teulerei shows a pleth-

ora of remarkable adaptations to a very specific

environment, which makes this species an outlier

among cowries: i) it lives in the intertidal zone on

sand/mud flats, where other cowries are rarer;

ii) it is active during the day, at variance to other

cowries; and iii) it is strictly dependent on a

specific habitat and food source. Nevertheless it

performs quite well when all these conditions are

present, so we can say that this species appears

very well adapted to its environment. Evolution

has done “a good job” with this species. And, in

fact, B. teulerei has no significant predators, at

least when they are adult and freely grazing and

mating in the open.

On the other hand, its distribution range seems

quite limited, maybe because of its specialist way

of life. The absence of free-swimming larvae is

certainly another concurring factor. We tried to find

B. teulerei elsewhere along the Oman coast, with

no success, although more research needs to be

done. Unfortunately, the very limited distribution

makes this species a highly vulnerable one.

Actually the main concern for the survival of B.

teulerei does not come from predators, but from

humans. It was quite bad luck for B. teulerei to find

a species collecting it in large numbers for its

beauty, rather than for its taste. And it was bad luck

indeed that this species is commercially valuable to

collectors. The limited range does the rest. The

story of the Masirah population teaches us that B.

teulerei is indeed in high danger of extinction. That

is why the new locality should absolutely remain

secret, and I am not giving any precise indication

as to where it is. It is also my opinion that this

species should be protected by law.

The life history of B. teulerei is, no doubt, a

remarkable one. Evolution shaped this species to a

rather specialized and successful life. At the same

time, it has put B. teulerei at risk. Evolution is a

blind process and of course it could not foresee that,

at a certain point, this species would have en-

countered another one: humans, predating it for its

shine, beauty and striking colors. Evolution shaped

B. teulerei to survive in its habitat, but at the same

time made it so easily accessible to humans, and its

highly specialized life puts it at risk of extinction.

Evolution is indeed a blind watchmaker that ‘ has

no vision, no foresight, no sight at alV (Dawkins,

1986). And B. teulerei was just plain unlucky to

encounter our species during its journey on our

planet.

ACKNOWLEDGMENTS

I wish to thank you very much Massimo Scali

(Imola, Italy) for giving me the opportunity to

visit and observe on site the new population of B.

teulerei in Oman, and for providing some of the

pictures. I also wish to thank very much the organ-

izers of the VIII Pontine Malacological Congress,

Silvia Alfinito and Bruno Fumanti (Sabaudia, Italy),

as well as the Malalcos 2002 association and mem-

bers, for inviting me to talk about B. teulerei.

Finally, my acknowledgement goes to Federico

Plazzi (Bologna, Italy) and Rex Stilwill (Grand Ra-

pids, MI, USA), for their review of the manuscript.

REFERENCES

Bergonzoni M., 2012. Barycypraea fultoni, a tale of a

fallen star. Beautifulcowries Magazine, 2:4-19.

Charter B., 1983. Masirah, the teulerei island, revisited.

Hawaiian Shell News, 31: 1,9.

Cross E.R., 1969. The case history of a rare shell.

Hawaiian Shell News, 17: 1,4.

Dawkins R., 1986. The blind watchmaker. Norton &

Company Inc., New York, U.S.A.

Liltved W.R., 2000. Cowries and their relatives of

southern Africa. II Edition revisited. Seacomber

Publications, Cape Town, S. Africa, 232 pp.

Luther F., 1972. A1 Masira - teuleri island. Hawaiian

Shell News, 20: 1, 3.

Meyer C.P., 2004. Towards comprensiveness: increased

molecular sampling with Cypraeidae and its phylo-

genetic implications. Malacologia, 46: 127-156.

Schilder F.A., 1964. The true habitat of a rare cowry.

Hawaiian Shell News, 12: 2.

Marco Passamonti

Scali M., 2013. Barycypraea teulerei (Cazenavette,

1846). The rediscovery. Beautifulcowries Magazine

3: 4-11.

Scali M., 2014. Barycypraea teulerei, going back to the

recently discovered new population. Beautiful-

cowries Magazine 5: 31-35.

Williams M., 1969. Cypraea teulerei follow up. Letter

from Arabia. Hawaiian Shell News, 17: 1,9.

Biodiversity Journal, 2016, 7 (1): 89-92

Monograph

Contribution to the knowledge of the molluscan thanato-

coenosis of Zannone Island (Pontine Archipelago, Latium,

ltaly).Additional reports

Bruno Fumanti 1 & Italo Nofroni 2

'Via del Villaggio 108, 04010 Sabaudia, Latina, Italy; e-mail: bmno.fumanti@libero.it

2 Via Benedetto Croce 97, 00142 Rome, Italy; e-mail: italo.nofroni@uniromal.it

"■Corresponding author

ABSTRACT In this second paper concerning the molluscan fauna of Zannone Island (Pontine Archipelago,

Italy) one sediment sample collected by scuba diving at a depth of 36.5 meters at SW of the

isle was investigated. Altogether, 47 taxa, not yet reported for Zannone, were identified, brin-

ging the total number of the molluscan thanatocoenosis of the island at 327 taxa.

KEY WORDS Mollusca; thanatocoenosis; Zannone Island; Italy.

Received 02.03.2016; accepted 18.03.2016; printed 30.03.2016

Proceedings of the Ninth Malacological Pontine Meeting, October 3rd-4th, 2015 - San Felice Circeo, Italy

INTRODUCTION

In a previous paper on the Mollusca of Zannone

Island, Fumanti (2014) reported 280 malacological

taxa. Recently prof. Riccardo Lubrano has provided

one of us (I. N.) with a sediment sample collected

on August 1 1th 2013 by means of scuba diving by

Mr. Nino Baglio at 36.5 m depth SW of Zannone

Island. The study of the sample has led to the iden-

tification of several taxa, 47 of these, representing

an increase of 14.4 % of the total, were not previ-

ously reported.

Finally, thanks to the finding of Spinoaglaja wil-

pretii (Ortea, Bacallado et Noro, 2003) by Romani

& Pagli (2014), the molluscan thanatocoenosis of

the Isle of Zannone consists now of 327 taxa. Fur-

thermore, in this paper, other species, indicated with

an asterisk, already reported in Fumanti (2014)

have been added with revised and updated nomen-

clature recording the latest publication.

RESULTS

Taxonomic list

Classis GASTROPODA Cuvier, 1797

Ordo PATELLOGASTROPODALindenberg, 1986

Familia LOTTED AE Gray, 1840

Genus Tectura Gray, 1 847

Tectura virginea (O.F. Muller, 1776)

Ordo VETIGASTROPODA Salvini-Plawen, 1980

Familia SCISSURELLIDAE Gray, 1847

Genus Sinezona Finlay, 1926

Sinezona cingulata (O.G.Costa, 1861)

Familia SKENEIDAE Clark, 1851

Genus Skenea Fleming, 1 825

Skenea serpuloides (Montagu, 1808)

Bruno Fumanti & Italo Nofroni

Ordo CAENOGASTROPODA Cox, 1960

Familia SILIQUARIIDAE Anton, 1838

Genus Petalopoma Schiapparelli, 2002

Petalopoma elisabettae Schiapparelli, 2002

Familia SKENEOPSIDAE Iridale, 1815

Genus Skeneopsis Iridale, 1915

Skeneopsis planorbis (O. Fabricius, 1780)

Familia JANTHINIDAE Lamarck, 1822

Genus Janthina Roding, 1798

Janthina pallida W. Thompson, 1840

Familia RISSOIDAE J.E. Gray, 1847

Genus Alvania Leach in Risso, 1826

Alvania dictyophora (Philippi, 1844) group

Notes. Actually this species is under investiga-

tion by Bruno Amati (Rome).

Genus Setia H. Adams et A. Adams, 1852

Setia turriculata Monterosato, 1884

Familia CYPRAEIDAE Rafmesque, 1815

Genus Nana Broderip, 1837

Naria spurca (Linnaeus, 1758)

Familia LIMACINIDAE Gray, 1840

Genus Thielea Strebel, 1908

Thielea inflata (d’Orbigny, 1836)

Genus Limacina Bose, 1817

Limacina trochifovmis (d’Orbigny, 1836)

Familia PERACLIDAE Tesch, 1913

Genus Peracle Forbes, 1844

Peracle reticulata (d’Orbigny, 1836)

Familia MURICIDAE Rafmesque, 1815

Genus Dermomurex Monterosato, 1890

Dermomure x scalaroides (Blainville, 1826)

Genus Murexsul Iridale, 1915

Murexsul aradasii (Monterosato in Poirer, 1883)

Familia MITROMORPHIDAE Casey, 1904

Genus Mitromorpha Carpenter, 1865

*Mitromorpha columbellaris (Scacchi, 1836)

* Mitromorpha olivoidea (Cantraine, 1835)

Notes. The nomenclature of the two species

belonging to the genus Mitromorpha , previously

reported in Fumanti (2014) are here updated ac-

cording to Amati et al. (2015).

Ordo HETEROSTROPHAP. Fischer, 1885

Familia OMALOGYRIDAE G.O. Sars, 1878

Genus Omalogyra Jeffreys, 1859

Omalogyra atomus (Philippi, 1841)

Genus Ammonicera Vayssiere, 1893

Ammonicera cfr. andresi Oliver et Rolan, 2015

* Ammonicera cW.fisclieriana (Monterosato, 1869)

Ammonicera cfr. superstriata Oliver et Rolan, 2015

Notes. The determination of the species belong-

ing to the genus Ammonicera , according to the

recent review of this genus (Oliver & Rolan, 2015)

and without SEM observations, has led to consid-

erable difficulties and is proposed here with a wide

margin of uncertainty.

Familia PYRAMIDELLIDAE Gray, 1840

Genus Parthenina Bucquoy, Dautzenberg et Dollfiis,

1883

Parthenina clathrata (Jeffreys, 1848)

* Parthenina dollfusi (Kobelt, 1903)

* Parthenina emaciata (Brusina, 1866)

* Parthenina interstincta (J. Adams, 1797)

* Parthenina monozona (Brusina, 1869)

*Partenina moolenbeechi (Amati, 1987)

*Partenina penchynati (Bucquoy, Dautzen-

berg et Dollfiis, 1883)

Partenina suturalis (Philippi, 1844)

Notes. As regards to Pyramidellidae we decided

to include the full list of the genera and species

The molluscan thanatocoenosis of Zannone Island (Pontine Archipelago, Latium, Italy). Additional reports

reported for Zannone (both in this paper and in

Fumanti, 2014) with the nomenclature updated

according to Giannuzzi-Savelli et al. (2014).

Genus Folinella Dali et Bartsch, 1904

*Folinella excavata (Philippi, 1844)

Genus Odostomella Bucquoy, Dautzenberg et

Dollfus, 1883

* Odostomella doliolum (Philippi, 1844)

Odostomella bicincta (Tiberi, 1868)

Genus Euparthenia Thiele, 1931

*Euparthenia humboldti (Risso, 1826)

Genus Eulimella Forbes et Mac Andrew, 1846

Eulimella acicula (Philippi, 1836)

*Eulimella ventricosa (Forbes, 1844)

Genus Odostomia Fleming, 1813

*Odostomia carrozzai Van Aartsen, 1987

*Odostomia eulimoides Hanley, 1844

* Odostomia lukisii Jeffreys, 1859

* Odostomia scalaris Mac Gillivray, 1843

Odostomia striolata (Forbes etHanlay, 1850)

* Odostomia turrita Hanley, 1844

* Odostomia unidentata (Montagu, 1803)

Genus Megastomia Monterosato, 1884

Megastomia alungata (Nordsieck, 1972)

* Megastomia conoidea (Brocchi, 1814)

Genus Ondina De Folin, 1870

*Ondina vitrea (Brusina, 1866)

Ondina scadens (Monterosato, 1844)

Genus Pyrgostylus Monterosato, 1884

*Pyrgostylus striatulus (Linnaeus, 1758)

Genus Turbonilla Risso, 1826

*Turbonilla pumila G. Seguenza, 1876

Genus Careliopsis Morch, 1875

Careliopsis modesta (De Folin, 1870)

Familia MURCHISONELLIDAE Casey, 1904

Genus Ebala Gray, 1 847

Ebala pointeli (De Folin, 1867)

Familia CIMIDAE Waren, 1993

Genus Cima Chaster, 1896

Cima cylindrica (Jeffreys, 1856)

Cima minima (Jeffreys, 1858)

Familia TOFANELLIDAE Bandel, 1995

Genus Graphis Jeffreys, 1867

Graphys albida (Kanmacher, 1798)

Ordo CEPHALAPSIDEA Fischer, 1883

Familia PLEUROBRANCHIDAE Gray, 1827

Genus Berthella Blainville, 1 824

Berthella sp.

Familia RETUSIDAE Thiele, 1925

Genus Volvulella Newton, 1891

Volvulella acuminata (Broguiere, 1792)

Familia PHIL1NIDAE Gray, 1850

Genus Philine Ascanius, 1772

Philine catena (Montagu, 1803)

Philine angulata Jeffreys, 1867

Genus Petalifera Gray, 1 847

Petalifera cf. gravieri (Vayssiere, 1906)

Familia AGLAJIDAE Pilsbry, 1895

Genus Spinoaglaja Ortea, Moro et Espinosa, 2007

Spinoaglaja wilpretii (Ortea, Bacallado et

Noro, 2003)

Notes. Species reported on the basis of one

specimen (3.3 mm) devoid of soft part at 36 m of

depth.

Bruno Fumanti & Italo Nofroni

Classis BIVALVIA Linnaeus, 1758

Ordo SOLEMYOIDA Dali, 1889

Familia NUCULIDAE Gray, 1824

Genus Nucula Lamarck, 1799

Nucula sp. (juv.)

Ordo MYTILOIDA Ferussac, 1822

Familia MYTILIDAE Rafmesque, 1815

Genus Crenella T. Brown, 1 827

Crenella pellucida (Jeffreys, 1850)

Genus Dacrydium Torell, 1859

Dacrydium hyalinum Monterosato, 1875

Familia ANOMIIDAE Rafmesque, 1815

Genus Pododesmus Philippi, 1837

Pododesmus sp.

Ordo LUCINIDAE Gray, 1854

Familia LUCINIDAE Fleming, 1828

Genus Anodontia Link, 1807

Anodontia fragilis Philippi, 1836

Genus Loripes Poli, 1791

Loripes lucinalis (Lamarck, 1818)

Familia MONTACUTIDAE W. Clark, 1855

Genus Montacuta Turton, 1 822

Montacuta substriata (Montagu, 1808)

Ordo VENEROID A Gray, 1854

Familia CARDIIDAE Lamarck, 1809

Genus Laevicardium Swainson, 1 846

Laevicardium crassum (Gmelin, 1791)

Familia TELLINIDAE Blainville, 1814

Genus Arcopagia Brown, 1877

Arcopagia balaustina (Linnaeus, 1758)

Familia PSAMMOBIIDAE Fleming, 1828

Genus Gari Schumacher, 1817

Gari costulata Turton, 1822

Gari depress a (Pennant, 1777)

Classis SCAPHOPODA Broun, 1862

Ordo DENTALIIDAE da Costa, 1776

Familia DENTAL ID AE J.E. Gray, 1834

Genus Antalis H. Adams et A. Adams, 1854

Antalis vulgaris da Costa, 1778

REFERENCES

Amati B., Smriglio C. & Oliverio M., 2015. Revision of

the recent mediterranean species of Mitromorpha

Carpenter, 1865 (Gastropoda, Conoidea, Mitro-

morphidae) with the descriptions of seven new

species. Zootaxa, 293 1 : 151-195.

Fumanti B., 2014. Contribution to the knowledge of

benthic molluscan thanatocoenosis of Zannone Island

(Pontine Archipelago, Latium, Italy). Biodiversity

Journal, 5: 97-106.

Giannuzzi-Savelli R., Pusateri F., Micali P., Nofroni I. &

Bartolini S., 2014. Atlante delle conchiglie marine

del Mediterraneo. Vol. 5. Heterobranchia. Edizioni

Danaus, Palermo. Ill + 91 pp.

Oliver J.D. & Rolan E., 2015. The genus Ammonicera

(Heterobranchia, Omalogyridae) in the Eastern

Atlantic, 1 : the species of Iberian Peninsula. Iberus,

33: 45-95.

Romani L. & Pagli A., 2014. The Genus Spinoaglaja

Ortea, Moro et Espinosa, 2007 in the Mediterranean

Sea: new records and observations on shell variability

(Opisthobranchia, Aglajidae). Bollettino Malacolo-

gico, 50: 137-139.

Biodiversity Journal, 2016, 7 (1): 93-102

Monograph

Terrestrial gastropods (Mollusca Gastropoda) from Lepini

Mountains (Latium, Italy): a first contribution

Alessandro Hallgass 1 & Angelo Van nozzi 2

'Via della Divina Provvidenza 16, 00166 Rome, Italy; e-mail: hallgass@hotmail.com

2 Via M.L. Longo 8, 00151 Rome, Italy; e-mail: ang.vannozzi@gmail.com

ABSTRACT Lepini Mountains are a calcareous massif that forms the southern pre- Apennines of Latium

(Italy), reaching a maximum altitude of 1536 m. Notwithstanding their central position and

the low height reached, the malacofauna of Lepini Mountains has been long neglected and

species composition was never reported so far. In this contribution, a preliminary investigation

of the terrestrial gastropods (Mollusca Gastropoda) occurring in the Lepini Mountains is

reported. At least 43 species are recorded. Several species already reported from Central Apen-

nines occur. The most remarkable findings include a hitherto unrecorded population of

Medora sp. (Clausiliidae) and the occurrence of two distinct forms ascribable to Jaminia

quadridens s.l.

KEY WORDS Terrestrial gastropods; biodiversity; Lepini Mountains; Italy.

Received 28.02.2016; accepted 20.03.2016; printed 30.03.2016

Proceedings of the Ninth Malacological Pontine Meeting, October 3rd-4th, 2015 - San Felice Circeo, Italy

INTRODUCTION

Lepini Mountains, together with Aurunci and

Ausoni Mountains, form the southern pre-Apen-

nines of Latium (Italy). They are positioned about

50 km SE of Rome and extend in NE-SW direction

(Fig. 1). They are separated from Central Apennines

by the Sacco Valley and face the Pontine alluvial

plain in the south. Lepini Mountains are comprised

of two parallel chains directed in NE-SW direction,

separated by the deep Montelanico-Carpineto-

Maenza tectonic line. The western chain is com-

prised by Mount Lupone (1378 m) and Mount

Semprevisa group (1536 m, the highest peak),

whereas the eastern chain quickly slopes down

to the Sacco Valley and is comprised of Mount

Gemma, Mount Malaina, Mount S. Marino and

Mount Alto, all of which reach heights around 1400

Lepini Mountains are mainly comprised of

limestone of Cretaceous age (Sani et al., 2004). The

whole massif shows to intense karst phenomena. As

a consequence, in the Lepini Mountains no per-

manent water body occurs, whereas several springs

appear at the base of the massif, the best known of

which gives rise to the Oasis of Ninfa (Amori et al.,

2002 ).

The vegetation is mainly comprised of holm

oak, chestnut and mixed woods at medium-low

altitudes and beech forests at medium-high alti-

tudes. Large portions of territory are occupied by

grassland mainly used as pasture.

The invertebrate fauna of Lepini Mountains

have been studied in some detail with regard to

arthropods (Corsetti et al., 2015). Several studies

focused on hypogean fauna (Sbordoni, 1971;

Latella, 1995; Nardi et al., 2002). Moreover, some

endemisms have been reported (Sbordoni, 1971;

Alessandro Hallgass & Angelo Vannozzi

Figure 1. Studied area: Lepini Mountains (southern Latium, Italy).

Numbers indicate the sampled stations listed in Table 1 .

Stn.

Locality

Coordinates

Alt. (m)

Environment

Pass to Campo di Segni

41.672649° N, 12.987930° E

1015

Pasture with stones

After pass to Campo

di Segni

41.670720° N, 12.993717° E

960

Rocks with low vegetation

Close to Campo di Segni

41.667926° N, 12.990029° E

880

Pasture and bushes wit

stones

Mount Erdigheta

41.56410° N, 13.119629° E

1046

Beech forest with rocks

Mount Erdigheta

41.562092° N, 13.120613° E

1115

Pasture with stones

Mount Semprevisa

41.572228° N, 13.092678° E

1250-

1400

Beech forest with rocks

Mount Semprevisa, top

41.571147° N, 13.091063° E

1490

Stones on the top

Carpineto, Pian della

Faggeta

41.575702° N, 13.103665° E

930

Rocks with low vegetation

and residuary beeches

Bassiano, road to Sempre-

visa, near the spring

41.552975° N, 13.047529° E

590

Holm oak wood with

rocks

Bassiano, road to

Semprevisa

41.558473° N, 13.059121° E

864

Clearing in holm oak

wood

Campo Rosello

41.563711° N, 13.077542° E

1174

Pasture with stones

Campo Rosello

41.571987° N, 13.072649° E

41.574551° N, 13.074571° E

1250-

1410

Pasture with stones

Table 1. List of the stations: Lepini Mountains (southern Latium, Italy).

Terrestrial gastropods (Mollusca Gastropoda) from Lepini Mountains (Latium, Italy): a first contribution

Pace, 1975; Magrini, 2005). However, the mol-

luscan fauna of Lepini Mountains was never studied

so far. Only four species occurring in hypogean

environments were reported ( Discus rotundatus,

Campylaea planospira, Daudebardia brevipes and

Oxychilus draparnaudi ), none of which strictly

hypogean (Latella, 1995).

In this contribution, we report the results of a

first survey aimed at assessing the biodiversity of

terrestrial gastropods of Lepini Mountains.

MATERIAL AND METHODS

A total of 1 2 stations along the western chain

have been sampled between April and June 2015

(see Table 1). Sampling was carried out only in

natural environments. As a consequence, species

recorded only from urban areas, such as Cornu

aspersum (O.F. Muller, 1774) found in the town of

Bassiano, were ruled out. Additionally, freshwater

or hypogean environments were not considered. For

the nomenclature, we mainly referred to the check-

list of the species of the Italian fauna (Bodon et al.,

1995; Manganelli et al., 1995, 1998, 2000). For the

suprageneric nomenclature, we referred to Bouchet

& Rocroi (2005). All specimens here illustrated

were collected from the Lepini Mountains. Shell

length and width were measured parallel and

perpendicular to the axis of the shell, respectively,

with calipers to the nearest 0.1 mm.

RESULTS AND DISCUSSION

At least 44 species of terrestrial gastropods

occur in the Lepini Mountains (see Table 2). The

most speciose family is the Clausiliidae, with 7

recorded species. The clausiliid Leucostigma can-

didescens is by far the commonest and widespread

species, occurring in almost all calcareous outcrops,

either exposed or shaded, often associated with

other calciophilous species such as Cochlostoma cf.

adamii, Marmorana signata, Granaria apennina

and Medora sp. We agree with Feher et al. (2010)

who indicate th species of the genus Granaria Held,

1838 occurring in the Italian peninsula as G. apen-

nina. Medora sp. was found only in a single station

inside the beech forest of Mount Semprevisa. The

unexpected finding of this population confirms that

the current knowledge of the genus Medora H. et

A. Adams, 1855 in Italy is far from being exhaust-

ive (Giusti et al., 1986; Nordsieck, 2012; Colomba

et al., 2012). Cochlodina laminata and C. bidens

occur in sympatry in the beech forest. According to

Opinion 2355, the Apennine species so far known

as Cochlodina incisa (Kuster, 1876) should be

indicated as C. bidens (Linnaeus, 1758) (Kadolsky,

2009; ICZN, 2015). They are readily distinguished

by the development of palatal plicae. In fact, while

in the former palatal plicae are truncated at the level

of the clausilium, in the latter both the principal and

the lower palatal plicae prolong internally. Moreover,

an additional intermediate palatal plica often occurs

in the latter. Cochlodina bidens in Lepini Mountains

shows a stout shell also found in specimens from

other localities of Latium, such as the holm oak

woods of Mount Circeo and Macchia Grande (Fi-

umicino) (Hallgass & Vannozzi, 2014).

The populations of Cochlostoma cf. adamii

have been studied by Zallot et al. (2015) in the

generic revision of the family Cochlostomatidae

and assigned to the subgenus Turritus Westerlund,

1883. Cochlostoma adamii group is comprised of

several forms reported with different nominal taxa

occurring from Central Apennines to Sicily, whose

taxonomy needs to be clarified. The marquise

Paulucci (1881) noted the occurrence of foims close

to Pomatias adamii in the Central Apennines and

described “ Pomatias adamii Var. Carseolanus“

from Carsoli (Abruzzi). Cochlostoma cf. adamii

from Lepini Mountains is different from C. cassi-

niacum (Saint Simon in Paulucci, 1878) from Cas-

sino and Sterrone (both Latium), though belonging

to the same subgenus Turritus (Zallot, comm,

pers.).

On the whole, the beech forest shows the

greatest biodiversity, with 28 recorded species.

Among them, there are several species commonly

found in beech forests of Central Apennines (Giusti

et al., 1985). However, a few of them deserve some

comments. Acicula sp. was recorded from a worn

fragment. The closest finding of this genus is A.

szigethyannae Subai, 1977 from Val d’Arano

(Ovindoli, Abruzzi). Conversely, Platyla similis is

recorded from several localities of the Italian penin-

sula. In particular, it has been reported from the

neighbouring Aurunci Mountains (Bodon &

Cianfanelli, 2008). Umax cf. maximus appears with

different patterns (Figs. 8 and 9). A completely

Alessandro Hallgass & Angelo Vannozzi

Family

Species

Stn.

COCHLOSTOMATIDAE

Cochlostoma cf. adamii (Paulucci, 1879)

4-9, 11, 12

ACICULIDAE

Acicula sp.

Platyla similis (Reinhardt, 1880)

POMATIIDAE

Pomatias elegans (O.F. Muller, 1774)

2,3,9

ORCUL1DAE

Sphyradium doliolum (Bruguiere, 1792)

6, 8

VALLONIIDAE

Acanthinula aculeata (O.F. Muller, 1774)

8,9

Gittenbergia sororcula (Benoit, 1857)

CHONDRINIDAE

Granaria apenninci (Kuster, 1850)

4,8

Chondrina avenacea (Bruguiere, 1792)

6,9

VERTIGINIDAE

Truncatellina callicratis (Scacchi, 1833)

ENIDAE

Jaminia quadridens (O.F. Muller, 1774) (small morphotype)

7,8

5, 18

Jaminia quadridens (O.F. Muller, 1774) (large morphotype)

4, 5, 7, 8, 12

4, 19

Merdigera obscura (O.F. Muller, 1774)

6, 8

FERUSSACIIDAE

Cecilioides acicula (O.F. Muller, 1774)

SUBULINIDAE

Rumina decollata (Linnaeus, 1758)

1,3,9

CLAU SILIID AE

Medora sp.

Leucostigma candidescens (Rossmassler, 1835)

1-6, 8, 9, 11, 12

3,21

Cochlodina laminata (Montagu, 1803)

Cochlodina bidens (Linnaeus, 1758)

Siciliaria paestana (Philippi, 1836)

3, 5, 6, 9

Macrogastra plicatula (Draparnaud, 1801)

Clausilia cruciata Studer, 1 820

PUNCTIDAE

Punctum pygmaeum (Draparnaud, 1801)

DISCIDAE

Discus rotundatus (O.F. Muller, 1774)

6,9

PRISTILOMATIDAE

Vi Ire a botterii (Pfeiffer, 1853)

4, 6,8

Vitrea subrimata (Reinhardt, 1871)

6, 8

OXY CHIL1D AE

Daudebardia rufa (Draparnaud, 1805)

Daudebardia brevipes (Draparnaud, 1805)

Oxy chilus cf. draparnaudi (Beck, 1837)

2, 6, 8,10

MILACIDAE

Tandonia sowerbyi (Ferussac, 1823)

6, 10

VITRINIDAE

Semilimacella bonellii (Targioni Tozzetti, 1873)

LIMACIDAE

Umax cf. maximus Linnaeus, 1758

3, 6, 10

8,9

Umax sp. A (black)

3,6, 8

Umax sp. B (brown)

AGRIOLIMACIDAE

Deroceras cf. lothari Giusti, 1973

H Y GROMIID AE

Monacha cf. cantiana (Montagu, 1803)

Monacha cf. campanica (Paulucci, 1881)

1,3, 5, 8, 11, 12

Cernuellopsis ghisottii Manganelli et Giusti, 1988

1,4, 5,7, 8,11,12

Cernuella cisalpina (Rossmassler, 1837)

Hygromia cinctella (Draparnaud, 1801)

HELICIDAE

Campylaea planospira Lamarck, 1 822

Marmorana signata (Ferussac, 1821)

6, 9, 11

Cantareus apertus (Bom, 1778)

Helix ligata O.F. Muller, 1774

1,3, 12

Table 2. List of the species recorded in the sampled stations, Lepini Mountains (southern Latium, Italy).

Terrestrial gastropods (Mollusca Gastropoda) from Lepini Mountains (Latium, Italy): a first contribution

Figures 2-9. Terrestrial gastropods from Lepini Mountains. Fig. 2: Cochlostoma cf. adamii. Fig. 3: Leucostigma candides-

cens. Fig. 4: Jaminia qnadridens (large morphotype). Fig. 5: Jaminia quadridens (small morphotype). Fig. 6: Daudebardia

rufa. Fig. 7: Tandonia sowerbyi. Fig. 8: Umax cf. maximus. Fig. 9: Limax sp. A (black) and L. cf. maximus.

Alessandro Hallgass & Angelo Vannozzi

Figures 10-17. Terrestrial gastropods from Lepini Mountains. Fig. 10: Platyla similis. Fig. 1 1 : Acicula sp. Fig. 12: Punctum

pygmaeum. Fig. 13: Acanlhinula aculeata. Fig. 14: Truncatellina callicratis. Fig. 15: Gittenbergia sororcula. Fig. 16: Vitrea

subrimata. Fig. 17: Vitrea botterii. Scale bar: 1 mm.

Terrestrial gastropods (Mollusca Gastropoda) from Lepini Mountains (Latium, Italy): a first contribution

Figures 18-23. Terrestrial gastropods from Lepini Mountains. Fig. 18: Jaminia quadridens (small morphotype). Fig. 19:

Jaminia quadridens (large morphotype). Fig. 20: Medora sp. Fig. 21: Leucostigma candidescens . Fig. 22: Cochlodina

bidens. Fig. 23: Cochlodina laminata. Scale bar: 5 mm (whole specimens); 2.5 mm (details).

100

Alessandro Hallgass & Angelo Vannozzi

black specimens of Limax Linnaeus, 1758 was

found in different stations, also in sympatiy with L.

cf. maximus (Fig. 9). A further Limax species with

uniform brown colour was recorded.

A small black specimen of Deroceras Rafinesque,

1820 was collected in Stn. 8, externally resembling

Deroceras lothari, a species described as endemic

to Reatini Mountains (northen Latium) (Giusti,

1973). It is provisionally reported as Deroceras cf.

lothari pending further study.

Holm oak and mixed woods are poorer in terms

of both species and number of specimens. Pastures

show a relatively reduced number of species as

well, some of which deserve some comments.

Jaminia quadridens occurs in two distinct forms,

here referred to as small and large morphotype,

respectively (Figs. 4, 5, 19, 20). At a conchological

level, they mainly differ with regard to shell size.

Measurements on over 60 specimens show that

these two forms can be readily distinguished by the

shell width, which shows a clear gap between the

two morphotypes (Fig. 25). Moreover, the large

morphotype seems to show a proportionally larger

width. However, this feature needs confirmation

due to the small amount of recorded specimens of

the small morphotype. The large morphotype is

widespread and was recorded from several stations.

Conversely, the small morphotype is uncommon

and was recorded only at higher altitudes. A similar

scenario with different morphs of J. quadridens

occurring syntopically have been recorded also in

other localities of Central Apennines, often with the

occurrence of an additional, dextral morph.

Monacha campanica, which we regard as a dis-

tinct species, is found throughout the Liri Valley up

to high altitude. The genitalia of M. campanica are

characterized by a very short penis provided with a

large penial papilla and a slender epiphallus. The

flagellum is as long as the epiphallus. The bursa

copulatrix shows a thick duct, widened at the base.

Specimens from Lepini Mountains share the same

anatomy but show a rather different shell. In fact,

they are smaller (max. diam. 16 mm) and lighter

than those described by the marquise Paulucci

(1881) (max. diam. 21 mm). Moreover, they show

a less depressed spire and a narrower umbilicus. As

a consequence, they are reported in Table 2 as

Monacha cf. campanica , pending further study.

In Stn. 9 (Bassiano, road to Semprevisa, near

the spring) an empty shell clearly different from

Figure 24. Helix ligata, height 35 mm, with genitalia (scale bar: 5 mm).

Terrestrial gastropods (Mollusca Gastropoda) from Lepini Mountains (Latium, Italy): a first contribution

101

Jaminia quadridens s.l.

Fig. 25. Height and width measurements of Jaminia quad-

ridens s.l. specimens from Lepini Mountains. Best-fit lines

for the two morphotypes are shown.

Monaca cf. campanica has been collected. It is

provisionally reported as Monacha cf. cantiana

waiting for anatomical data.

Cernuellopsis ghisottii is the most abundant

species in grasslands and pastures above 1000 m.

This species shows a disjunct distribution in the

Apennines. Southern populations occur in the

Pollino (Calabria-Basilicata) and Sirino (Basilicata)

massifs and extend up to Albumi Mountains (Cam-

pania), wherease populations from Central Apen-

nines are frequent on the western coastal chains and

extend up to Simbruini Mountains (Latium). The

species was never recorded from intermediate

mountains of central-northen Campania.

Helix ligata is widespread in Lepini Mountains

but never abundant. Different populations show a

variable appearance. Specimens from Carpinetana

Valley were genetically studied by Fiorentino et al.

(2016) and are very similar to specimens from

Apennine valley floors showing a yellowish

background due to the presence of periostracum,

whereas specimens from Stn. 1 (pass to Campo di

Segni) living in exposed pasture with stones show

a whitish background (Fig. 24) likely due to the loss

of periostracum that make it resemble Helix delpre-

tiana Paulucci, 1878 (Giusti, 1973). However, the

anatomy of specimens from Stn. 1 corresponds to

Helix ligata , even though they are genetically dis-

tinct from populations from Central Apennines

(Fiorentino et al., 2016).

CONCLUSIONS

The preliminary checklist here presented shows

that at least 43 species of terrestrial gastropods

occur in the Lepini Mountains. The richest environ-

ment is represented by beech forests, with 28 recor-

ded species. Along with species already reported

from Central Apennines, a new isolated population

of Medora is recorded. Due to the extremely limited

distribution, this population can be considered vul-

nerable and likely in need of protection. Jaminia

quadridens occurs in two clearly distinct morphs

without intermediate forms, mainly differing in

their size. Further research is required in order to

ascertain whether they actually belong to different

species. Some species remain undetermined,

whereas others were determined by comparison,

pending further research.

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logico, 36: 125-130.

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Biodiversity Journal, 2016, 7 (1): 103-115

Monograph

A revision of the Mediterranean Raphitomidae, 3: on the

Raphitoma pupoides (Monterosato, 1 884) complex, with the

description of a new species (Mollusca Gastropoda)

Francesco Pusateri 1 , Riccardo Giannuzzi-Savelli 2 * & Stefano Bartolini 3

'Via Castellana 64, 90135 Palermo, Italy; e-mail: francesco@pusateri.it

2 Via Mater Dolorosa 54, 90146 Palermo, Italy; e-mail: malakos@tin.it

3 Via E. Zacconi 16, 50137 Firenze, Italy; e-mail: stefmaria.bartolini@libero.it

’Corresponding author

ABSTRACT In the present work we present a complex of species of the family Raphitomidae (Mollusca

Gastropoda) comprising three entities: two have multispiral protoconchs, Raphitoma pupoides

(Monterosato, 1884), the less known R. radula (Monterosato, 1884) and a new species with

paucispiral protoconch.

KEY WORDS Mollusca; Conoidea; Raphitomidae; new species; Mediterranean Sea.

Received 02.03.2016; accepted 24.03.2016; printed 30.03.2016

Proceedings of the Ninth Malacological Pontine Meeting, October 3rd-4th, 2015 - San Felice Circeo, Italy

INTRODUCTION

The family of Raphitomidae is a well supported

clade of the Conoidea (Bouchet et al., 2011). The

genus Raphitoma Bellardi, 1847 as currently

conceived includes, based on our estimates, ca. 40

Mediterranean species, some of which are still

undescribed. Propaedeutic to the general revision

of the Mediterranean Raphitoma s.l., we have

focused on several pairs of species, differing only

or mostly in the size and shape of the protoconch

(Pusateri et al., 2012, 2013). The specific distinction

is based on the assumption that the dichotomy

multispiral protoconch/planktrotrophic develop-

ment vs. paucispiral protoconch/lecithotrophic de-

velopment (Jablonski & Lutz, 1980) can be used in

caenogastropods to recognise distinct sister species

(Bouchet, 1989; Oliverio, 1996a, 1996b, 1997).

Anyway, it should not be abused to create poly-

phyletic genera by artificially separating closely

related species among different genera only based

on their larval development (Bouchet, 1990).

In the present work we present the results on

a complex of species comprising three entities:

two have multispiral protoconchs, R. pupoides

(Monterosato, 1884), and the less known R. radula

(Monterosato, 1884); the other was discovered

while revising the materials in the Monterosato

collection, where a lot (MCZR 16905) included

some specimens with paucispiral protoconch, la-

belled by Monterosato himself “K tomentosa/

Monts. /Palermo’', never published, that we describe

hereby as new to Science.

ABBREVIATIONS AND ACRONYMS, d =

diameter; h = height; sh = empty shell(s); LMG-NS:

Leeds Museums and Galleries - Natural Science;

MNHN: Musee Nationale Histoire Naturelle, Paris,

France; MRSNT: Museo Regionale Storia Naturale,

Terras ini, Italy; NMW: National Museum of Wales,

United Kingdom; SMF: Senckenberg Museum,

104

Francesco Pusateri etalii

Frankfurt/M, Germany; SMNH: Swedish Museum

of Natural History, Stockholm, Sweden; MCZR:

Museo Civico di Zoologia, Roma, Italy; HUJ:

Hebrew University of Jerusalem, Israel; ARD:

Roberto Ardovini collection (Rome, Italy); BOG:

Cesare Bogi collection (Livorno, Italy); DUR:

Sergio Duraccio collection (Napoli, Italy); GER:

Alfio Germana collection (Trecastagni, Catania,

Italy); GOR: Sandro Gori collection (Livorno,

Italy); HOA: Andre Hoarau collection (Frejus,

France); MAC: Gabriele Macri collection (Scor-

rano, Lecce, Italy); MAR: Alessandro Margelli

collection (Livorno, Italy); PAG: Attilio Pagli

collection (Lari, Pisa, Italy); PAO: Paolo Paolini

collection (Livorno, Italy); PRK: Jakov Prlcic

collection (Split, Croatia); PSI: Peter Sossi collec-

tion (Trieste, Italy); PUS: Francesco Pusateri col-

lection (Palermo, Italy); SBR: Carlo Sbrana

collection (Livorno, Italy); SER: Gabriele Sercia

collection (Palermo, Italy); SPA: Gianni Spada

collection (Vagrigneuse, France); SQU: Ennio

Squizzato collection (Loreggia, Padova, Italy); TIS:

Morena Tisselli collection (S. Zaccaria, Ravenna,

Italy); TRI: Lionello Tringali collection (Rome,

Italy); VAZ: Angelo Vazzana collection (Reggio

Calabria, Italy).

RESULTS

Systematic

Citation of unpublished names is not intended for

taxonomic purposes.

Familia RAPHITOMIDAE Bellardi, 1875

Genus Raphitoma Bellardi, 1 847

Type species: Pleurotoma hystrix Cristofori et Jan,

1832 (nomen nudum, validated by Bellardi, 1847

as " Pleurotoma histrix Jan.") by subsequent des-

ignation (Monterosato, 1872: 54).

Raphitoma pupoides (Monterosato, 1884)

Figs. 1-9, 24

Pleurotoma rudis Scacchi, 1836 non G.B. Sowerby

I, 1834 nee Philippi, 1836

Pleurotoma rudis Scacchi, Weinkauff, 1868: 130

(see Remarks)

Pleurotoma reticulatum var. rudis Sc., Petit de la

Saussaye, 1869: 154

Pleurotoma ( Defrancia ) rudis Sc., Monterosato,

1875: 44 (see Remarks)

Pleur. rude Scacchi, Aradas & Benoit, 1876: 249 n.

662 (see Remarks)

Pleurotoma rudis Sc., Monterosato, 1878: 106 (see

Remarks)

Clathurella rudis Scacchi, B.D.D., 1883: 94 pi. 14

figs. 8, 9

Cordieria pupoides Monterosato, 1884: 132

[nomen novum]

Clathurella pupoidea Monterosato, Locard, 1886:

114 [error pro pupoides]

Clathurella pupoidea Monterosato, Locard, 1891:

66 fig. 52 [error pro pupoides]

Clathurella rudis (B.D.D.), Cams, 1893: 426

Clathurella pupoidea de Monterosato, Locard &

Caziot, 1900: 248

Clathurella pupoidea var. major, Locard & Caziot,

1900: 248 (nomen nudum)

Clathurella pupoidea var. minor, Locard & Caziot,

1900: 248 (nomen nudum)

Clathurella pupoidea var. ventricosa, Locard &

Caziot, 1900: 248 (nomen nudum)

Clathurella pupoidea var. curta, Locard & Caziot,

1900: 248 (nomen nudum)

Clathurella pupoidea Mtrs., Kobelt, 1905: 351

Mangilia ( Clathurella ) pupoides Monterosato,

Cipolla, 1914: 146, pi. 13, figs. 16 (fossil)-17

(recent)

Cordieria pupoides Montrs., Bellini, 1929: 32

Philbertia ( Philbertia ) rudis Scacchi, Priolo, 1967:

697

Raphitoma ( Cyrtoides ) rudis (Scacchi), Nordsieck,

1968: 176 pi. 30, fig. 20

Raphitoma ( Cyrtoides ) rudis pupoidea (Monterosato),

Nordsieck, 1968: 176 pi. 30 fig. 21

Raphitoma rudis pupoidea Monts, Parenzan, 1970:

207 pi. 44, fig. 842

Raphitoma (C.) pupoidea (Monterosato), Nordsieck,

1977: 52, pi. 16, fig. 126 (error pro pupoides )

Raphitoma (C.) neapolitana Nordsieck, 1977: 52,

pi. 16 figs. 124, 125 (nomen vanum)

Raphitoma pupoides (Mts), Terreni, 1981 : 40 n. 328

Raphitoma pupoidea (Monterosato), Nordsieck,

1982: 272, pi. 101, fig. 98.11

Raphitoma neapolitana Nordsieck, 1982: 272, pi.

101, fig. 98.10

Raphitoma neapolitana form a Nordsieck, 1982:

272, pi. 101, fig. 98.10a

Mediterranean Raphitomidae, 3: on the Raphitoma pupoides complex, with the description of a new species

105

Raphitoma (R. ) pupoides (Monterosato), Van Aartsen

etal., 1984: 91

Raphitoma pupoides (Monterosato), Orlando &

Palazzi, 1986: 44

Raphitoma pupoides (Monterosato), Tenekidis,

1989: n. 58.50

Raphitoma {Raphitoma) pupoides (Monterosato),

Sabelli et al., 1990-1992: 44, 216, 411

Raphitoma pupoides (Monterosato), Poppe & Goto,

1991: 174

Raphitoma ( Cyrtoides ) pupoides (Monterosato),

Delamotte & Vardala-Theodorou, 1994: 287

Raphitoma pupoides (Monterosato), Cecalupo &

Quadri, 1995: 109

Raphitoma pupoides (Monterosato), Giribet &

Penas, 1997: 53

Raphitoma pupoides (Monterosato), Marquet,

1998: 276

Raphitoma pupoides (Monterosato), Oztiirk et al.,

2004: 59

Raphitoma pupoides (Monterosato), Repetto et al.,

2005:220% 910

Pleurotoma rudis Scacchi, Cretella et al., 2005: 125

Raphitoma pupoides (Monterosato), Cretella et al.,

2005: 125

Raphitoma pupoides (Monterosato), Cossignani &

Ardovini, 2011: 31, 328

Raphitoma pupoides (Monterosato, 1884), Scuderi

& Terlizzi, 2012 (see Remarks)

Type locality. Coast of Provence, France,

Mediterranean Sea.

Examined material. Type material: neotype,

from “Artufel/Provenza” [Provence, M. Artufel

legit] (18.7 x 7.7 mm) (MCZR 16492).

Other examined material. France. “Artufel/

Provenza” 3 sh (MCZR 16492, with Monts label

“H. pupoides”); Marseille, 4 sh (coll. Locard

MNHN); St. Raphael, 3 sh coll. Locard (MNHN),

1 sh (coll. Hoarau); Cassis, 2 sh coll. (Locard

MNFIN); Le Brusc, 4 sh (coll. Locard MNHN, 4

sh); Coste di Provenza, 2 sh (coll. Chaster NMW n.

01894); Bastia, 2 sh (coll. Monterosato, MCZR lot

16861).

Italy. Gulf of Baratti, 7 sh (PAO), 1 sh (PAG);

Punta Ripalti (Elba Isl.), 2 sh -25 m (GOR); Lazio

1 sh (PAG); Circeo, 1 sh (TRI); Napoli, 1 sh

(coll. Coen HUJ, n. 8082c sub nomine “ Philbertia

( Cordieria ) cordieri cancellatd’y Sorrento

(Napoli), 2 sh (DUR); Palinuro (Salerno), 1 sh (SPA);

Scilla (Reggio Calabria), 4 sh (VAZ); Palermo,

Sicily, 10 sh with Monterosato handwritten label

“pupoides /Monts. /ValU/et/v. decolorata, Pallary”,

1 sh with non-Monterosato label “Cordieria/ pup-

oides Monts./dr. Golfo di Palermo” and 15 sh with

non-Monterosato label “Cordieria/ pupoides Monts./

drag. Golfo di Palermo” (MCZR 16492, with

Monts label “H. pupoides ”); Porticello (Palermo),

2 sh sub nomine R. reticulata (coll. MRSNT n.

4759); Isola delle Femmine (Palermo), 1 sh (SER),

8 sh (PUS); Trapani, 1 sh (SER); Catania, 1 sh

(GER); Pozzillo Inferiore (Catania), 1 sh (PAG);

Canale di Sicilia, 1 sh (TRI), 1 sh (coll. MRSNT n.

7312); Sicilia, 6 sh sub nomine R. purpurea (coll.

MRSNT n. 29824); Jesolo (Venezia), 1 sh (SQU).

“Coste d'Africa”. 1 sh, coll. Monterosato

MCZR, lot 16901.

Croatia. Unprecised locality, 1 sh (DEL); Dal-

matia, 1 sh (PRK).

Description. In squared parentheses data of the

neotype. Shell of medium size for the genus, height

10-21 mm [18.7] (mean 15.05, std 3.81), width 5-

8 mm [7.7] (mean 6.57, std 1.27), cirto-pupoid,

slender, h/d 2.1-2.57 [2.43] (mean 2.26, std 0.19).

Protoconch multispiral, only part of the last whorl

known, with traces of diagonally cancellate sculp-

ture. Teleoconch of 6-8 [7] whorls, evenly convex

(more convex in juveniles). Suture fine and undu-

late. Axial sculpture of 12-24 [18] sligthly opistho-

cline, non-equidistant ribs, and interspaces broader

than the ribs (with interspace width varying with

shell size). Axial sculpture evident, but becoming

obsolescent in largest shells. In particularly large

shells (gerontic), axial ribs revert to same strength

as the spiral cords on the last quarter of whorl. Spiral

sculpture on the last whorl of 7-10 [9] cordlets, thin-

ner that axial ribs. Cancellation squared in juveniles,

becoming rectangular in adults. Secondary cordlets

appearing occasionally and thereafter becoming as

strong as the others. Subsutural ramp narrow, devoid

of evident sculpture. Columella simple, slightly

sinuous anteriorly, gently angled posteriorly. Outer

lip thickened and crenulated externally, with 11-13

[12] strong inner denticles, the most posterior smal-

ler, delimiting the wide and short anal sinus, the

most anterior more robust and delimiting the funnel-

like siphonal canal. Siphonal fasciole of 6 nodulose

cordlets, neatly spaced from the last spiral cordlet.

Colour uniformly ligth chestnut brown in the back-

106

Francesco Pusateri etalii

ground, with darker blotches, more evident in larger

shells (>20 mm), and same darker colour bordering

the siphonal fasciole and inside the aperture. Violet

hue on the first 3^4 whorls of particularly fresh spe-

cimens. Comma- shaped white spots on the sub-

sutural ramp, arrow-like white spots inside some

cancellation interspaces. Soft parts unknown.

Distribution. Western and Central Mediter-

ranean. Adriatic. The records under this name from

Greece by Koukouras (2010) and Delamotte &

Vardala-Theodorou (1994: 287) were in turn based

on Tenekides (1989) who reported under this name

another species (probably R. echinata ).

Remarks. The protoconch was always either

lacking, broken or corroded in almost specimens

studied. Anyway parts of the apical whorls showing

traces of a diagonally cancellate sculpture, indic-

ating a multispiral protoconch.

Pleurotoma rudis Scacchi, 1836 was introduced

with the following diagnosis: “Testa fusca fascis

pallidioribus, anfractibus rotundatis, cancellatis et

muricatis; labro crasso interne striato, cauda vix

ultra labrum producta. Alta lin. 10—11. R echinatae

similis; at labro crassiore, cauda breviore, et minus

aspera; saepe fascis pallidioribus ornata. In sinu

neapolitano et tarentino ” (Scacchi, 1836), Fig. 17.

Weinkauff (1868), Petit de la Saussaye (1869)

and Aradas & Benoit (1876) considered it as a

variety or synonym of R. echinata (as Defrancia

reticulata Renier). Monterosato (1875, 1878) at first

included it within Pleurotoma purpurea sensu

Philippi non Montagu. Thereafter (Monterosato,

1884), he separated to two species and introduced

the replacement name Cordieria pupoides noticing

an alleged homonymy with “P. rudis Broderip”. Ac-

tually, Broderip introduced, in 1834, Placunanomia

rudis (a bivalve), the abbreviation P rudis having

possibly mislead Monterosato. However, Pleuro-

toma rudis Sacchi is preoccupied by P. rudis G.B.

Sowerby I, 1 834 (currently accepted as Crassispira

rudis ) and by P rudis Philippi, 1836 (currently

accepted as Clathromangelia granum (Philippi,

1844): note that Philippi’s work preceeds Scacchi’s

one according to Cretella et al., 2005: 115), and the

replacement name by Monterosato still holds valid.

Regrettably, the type material of Pleurotoma rudis

Scacchi is lost (Cretella et al., 2005: 123) and

we have established hereby a neotype based on

Monterosato ’s material. The original material of

Pleurotoma rudis Scacchi has gone lost. We des-

ignate, for the sake of stability, a shell from the

Monterosato collection, upon which he based his

concept of Cordieria pupoides , as the neotype of

Pleurotoma rudis Scacchi.

Some Authors (Bucquoy et al., 1883: 93) in-

cluded, in the synonymy of R. rudis , Pleurotoma

reticulata var. brevis Requien, 1848. However,

this is a nomen nudum and thus, not available.

Nordsieck (1977) used this name ( brevis ) and

provided the first valid introduction, but referring

to a distinct species.

Nordsieck (1968: 176) split R. rudis Scacchi into

four subspecies: R. rudis rudis, R. rudis pupoidea

[sic!], R. rudis cylindrica and R. rudis intermedia.

Descriptions of R. rudis rudis and R. rudis pupoidea

[sic! emor pro pupoides ] are quite similar and migth

be referred to the same species (R. pupoides). Con-

cerning the two other “subspecies”, R. cylindrica

(erroneously ascribed to Monterosato, actually

introduced by Locard & Caziot, 1899) is a distinct

unrelated species; “R. rudis intermedia n. ssp.” had

a scanty description and was not figured. Sub-

sequently, Nordsieck raised it to species level and

provided a description and figure of R. intermedia

(Nordsieck, 1977: 56, pi. 18 fig. 140). This is R.

laviae, as confirmed by the study of a syntype (SMF,

sine numero, with autograph Nordsieck’s label). To

increase confusion, Nordsieck (1977: 52) also intro-

duced R. ( Cyrtoides ) neapolitana as a replacement

name pro Pleurotoma rudis Scacchi, 1836 non Bro-

derip, evidently neglecting Monterosato’s introduc-

tion: R. neapolitana is thus not available. Material

on which Nordsieck based his concept of R. neapol-

itana (SMF 340337, 3403379 and 340338) included

small size specimens of R. laviae and R. bicolor.

Raphitoma cfr. pupoides as figured by Cavallo

& Repetto (1992: 147 fig. 401) andR. cfr. pupoides

as figured by Cachia et al. (2001: 69 pi. 10 fig. 9)

are not referable to the present species. Raphitoma

pupoides as figured by Scuderi & Terlizzi (2012: pi.

XVIII n. 6) is rather to be referred to R. cordieri

sensu Auctores.

Raphitoma pupoides can be easily distinguished

from R. echinata sensu Auctores by its cyrtoconoid

not stepped outline and the shorter siphonal canal.

Specimens of R. pupoides with strong sculpture on

the last whorls may be confused with R. radula,

which is however diagnosed by its more acute spire,

the ligther colour without blotches or spots.

Mediterranean Raphitomidae, 3: on the Raphitoma pupoides complex, with the description of a new species

107

Figures 1-8. Shells of Raphitoma pupoides (Monterosato, 1884). Fig. 1: Lectotype: Provenza, (MCZR lotto 16492), h: 18.7

mm with label of the lot; Fig. 2: sine locus (MNHN-IM-2000-3240), h: 16.5 mm; Fig. 3: Palinuro, close-up of the sculpture;

Fig. 4: Anzio, h: 20 mm; Fig. 5: Anzio, h: 17 mm; Fig. 6: Jesolo (Venezia), h: 20 mm; Fig. 7: Saint-Raphael, Est La

Chretienne (France), h: 15.7; Fig. 8: Isola delle Femmine (Palermo), juveniles, h: 9.1 mm.

108

Francesco Pusateri etalii

Figure 9. Raphitoma pupoides (Monterosato, 1884), Adriatic, h: 12 mm.

Figure 10. Raphitoma radula (Monterosato, 1884), Palermo, coll. Melville-Tomlin, NMW, h: 11.5 mm, with label.

Raphitoma alida Pusateri et Giannuzzi-Savelli

n. sp. - Figs. 11-15, 25

Examined material. Holotype and 3 paratypes

from Palermo (coll. Monterosato, MCZR 16905),

with handwritten Monterosato label: “K tomentosal

Monts./Palermo”; 2 paratypes, Gulf of Palermo

(PUS).

Other examined material. Italy. Gulf of Bar-

atti, 1 sh (MAR), 1 sh (BOG); Livorno, 1 sh (BOG);

Scilla (Reggio Calabria), 3 sh (VAZ); Palermo, 1 sh

sub nomine ms. “ perfecta ” (coll. Monterosato,

16905); sine loco probably Palermo, 1 sh, (coll.

Monterosato, MCZR 16905); Gulf of Palermo, 2 sh

(PUS).

“Coste d’Africa”. 1 sh (coll. Monterosato,

MCZR 16905).

Description of holotype. Shell of medium size

for the genus, height 17.1 mm, width 7 mm, fusi-

form-pupoid, slender, h/d 2.44 mm. Protoconch

paucispiral, only protoconch I of of 1.5 convex

whorls, height 540 pm, width 480 pm; sculpture

orthogonally cancellate. Teleoconch of 7 convex

whorls. Suture not incised, evident. Axial sculpture

of 1 6 sligthly opisthocline (somethimes orthocline),

elevated and strong ribs, and interspaces twices as

broad as the ribs. Spiral sculpture on the last whorl

of 6 cordlets, thinner that axial ribs and interspaces

twices as broad as the cordlets. Cancellation rectan-

gular, with spinulose tubercles at the intersections.

Secondary cordlets appearing occasionally and

thereafter becoming as strong as the others.

Subsutural ramp wide, devoid of evident sculpture.

Columella simple, slightly sinuous anteriorly,

gently angled posteriorly. Outer lip thickened and

crenulated externally, with 9 strong inner denticles,

the most posterior smaller, delimiting the wide and

deep anal sinus, the most anterior more robust and

delimiting the funnel-like siphonal canal. Siphonal

fasciole of 7 nodulose cordlets, neatly spaced from

the last spiral cordlet. Colour straw yellow, becom-

ing gradually orange-brownish in the subsutural

area, and with an orange-brown band visible inside

the aperture. Comma-shaped white spots on the

subsutural ramp, arrow-like white spots inside some

cancellation interspaces. Soft parts are unknown.

Variability. Paratypes shells: height 12-17 mm

(mean 14.4, std 1.66), width 5.5-7 mm (mean 6.36,

Mediterranean Raphitomidae, 3: on the Raphitoma pupoides complex, with the description of a new species

109

Figures 11-14. Shells of Raphitoma alida n. sp. Fig. 11: Holotype, Palermo (coll. Monterosato MCZ, lot 16905), h: 17.1

mm; Fig. 12: Paratype A, Palermo (coll. Monterosato MCZR, lot 16905), h: 14.8 mm; Fig. 13: Paratype E, Gulf of Palermo,

(PUS n. 405), h: 12.1 mm (sz = subsutural zone; sc = secondary cordlet); Fig. 14: Gulf of Palermo, h: 12.8 mm. Figure 15.

Raphitoma alida n.sp., protoconch of the holotype.

110

Francesco Pusateri etalii

std 0.57), h/d 2.12-2.36 mm (mean 2.26, std 0.10);

axial sculpture of 14-16 ribs; outer lip with 9-10

denticles. Soft parts are unknown.

Etymology. From the two granddaughters of the

authors (Alice Giannuzzi Savelli and Ida Pusateri),

ali[ce]+ida, used as a noun in apposition.

Distribution. This new species is known only

for the examined material, from Tyrrhenian and

Central Mediterranean. Type locality is Palermo.

Remarks. Raphitoma alida n. sp. differ from R.

pupoides mainly in its paucispiral protoconch (v.

multispiral in R. pupoides ). Shells without proto-

conch of the new species could be confused with

shells of R. pupoides with a non-obsolete sculpture

on the last whorl; R. alida n. sp. can be distin-

guished by its different background colour (chestnut

v. yellowish), 7 nodulose cordlet on the fasciole v.

6 less nodulose in R. pupoides , and the less pupoid

and more fusiform outline.

Some recent Authors (Nordsieck, 1968, 1977;

Piani, 1980) erroneously ascribed to Monterosato

a validly published “ Raphitoma tomentosa”.

Although the epithet “ tomentosa ” was evidently

especially liked by Monterosato, he has never

published such binomen. The epithet " tomentosa "

was, for mysterious reasons, to be particularly dear

and pleasing to Monterosato so that in schedis, gave

this name to various entities: - Philbertia tomentosa ,

lot 16682 = some mixed specimens of R. philberti

var. - D. tomentosa, lotto 16901 = 4 specimens of

R. horrida. - P tomentosa lotto 16696 = 5 spe-

cimens of R. lineolata. - Philbertia tomentosa,

Monterosato’s label in coll Coen lot 1912 = 2 spe-

cimens of R. pruinosa.

Nordsieck (1968: 177) reported Raphitoma phil-

berti tomentosa with a useless scanty description

(“ kleiner ; gedrungen mit konvexen Umgangen.

Schlanker stiel. Hell reh-weiss ”; small, stout, with

convex whorls. Slender tail. Light fawn and white)

and without any figure. Nordsieck (1977: 58 n.

A 149) again reported Raphitoma (Philbertia) to-

mentosa ascribing it to Monterosato, 1884, with

an apparently good description and a figure (Nord-

sieck, 1977: pis. 19 n. 149). However, the four lots

labelled under this name in the coll. Nordsieck

inckluded the following materials:

SMF 341803/1, labelled “ Philbertia tomentosa

Mtrs. Egina”, one worn shell, 5.4 mm long, with

two holes, protoconch missing, probably R. laviae;

SMF 341804/1, labelled “ Philbertia tomentosa

Mtrs. Karpathos”, one very worn shell, 3.2 mm

long, protoconch missing, probably R. bicolor juv.;

SMF 341805/1, labelled “ Philbertia tomentosa

Mtrs, Cataldo (Brindisi)”, one very worn shell, 5.9

mm long, protoronch missing, indeterminable.

Nordsieck (1977: 58) reported “Palermo, Cataldo”:

although there is a beach called San Cataldo near

Terrasini (Palermo), it is more likely that the true

locality was San Cataldo, not far from Brindisi;

SMF 341802/5, labelled as “ Philbertia tomentosa

Mtrs., Ibiza”, 5 shells, 2. 5-6. 5 mm long, four too

worn to be identified, one referable to R. bicolor

juv., with a portion of multispiral protoconch.

None of these shells matched the description,

the size (7 x 3.2 mm) or the figure provided by

Nordsieck, including the described paucispiral

protoconch, whilst all but one shells (with traces

of multispiral protoconch) lacked the apex. It is

worthy of notice that Nordsieck's "descriptions"

were not necessarily based (only) on actual speci-

mens but frequently included also a compilation

from literature. Same holds for his drawings, often

compound artwork of actual specimens and figures

from the literature. This explains why so rarely spe-

cimens can be found which match his figures (our

unpublished observations and R. Janssen, SMF,

personal communication). Nordsieck included this

entity in the subgenus Philbertia, which in his

scheme comprised species (R. philberti, R. laviae,

R. lineolata, R. atropurpurea, R. densa, etc.) that

have nothing to do with the R. pupoides- complex.

Parenzan (1970: 212 n. 862) cited R. philberti var.

tomentosa Monterosato evidently mutuating it after

Nordsieck (1968). This name is anyway unavail-

able, having been introduced as a varietal name

after 1960 (ICZN, 1999: art. 15.2).

Raphitoma radula (Monterosato, 1884) [Cordieria]

Figs. 10, 16-23,26

Cordieria radula Monterosato, 1884: 132

Clathurella radula de Monterosato, Locard, 1886:

117

Clathurella radula de Monterosato, Locard, 1891: 67

Clathurella radula de Monterosato, Locard &

Caziot, 1899: 250

Clathurella radula var. elongata, Locard & Caziot,

1899: 250 (nomen nudum)

Mediterranean Raphitomidae, 3: on the Raphitoma pupoides complex, with the description of a new species

111

Figures 16-22. Shells of Raphitoma radula (Monterosato, 1884). Fig. 16: Lectotype, Palermo, (MCZR), h: 14.8 mm; Fig.

17: particular (sc = secondary cordlet); Fig. 18: Palermo (coll. Monterosato MCZR), Paralectotype A, h: 17 mm; Fig. 19:

Isola d’Elba, h: 1 8 mm; Fig. 20; Palermo (coll. Monterosato MCZR), Paralectotype F, h: 6 mm; Fig. 2 1 : Antignano (Livorno),

h: 9.9 mm; Fig. 22: Gulf of Palermo, h: 12.7 mm. Figure 23. Raphitoma radula , protoconch of paralectotype F.

112

Francesco Pusateri etalii

Figures 24-26. Siphonal fasciole of Raphitoma pupoides (Fig. 24), R. alida (Fig. 25), and R. radula (Fig. 26).

Clathurella radula var. fuscescens, Locard &

Caziot, 1899: 250 (nomen nudum)

Clathurella radula var. lutescens, Locard & Caziot,

1899: 250 (nomen nudum)

Clathurella radula var. minor , Locard & Caziot,

1899: 250 (nomen nudum)

Clathurella radula var. ventricosa , Locard &

Caziot, 1899: 250 (nomen nudum)

Cordieria radula Monterosato, Pallary, 1900: 256

Raphitoma reticulata radula Nordsieck, 1968: 175,

pi. 29 fig. 94.16

Raphitoma echinata cordieri form d (radula)

Monterosato, Nordsieck, 1977: 51

Cordieria radula (Monterosato), Sabelli et al.,

1990: 217

Type locality. Palermo.

Examined material. Lectotype (here design-

ated, 14.8 x 6.4 mm) Monterosato coll (MCZR

16476), with handwritten label by Monterosato

“Cordieria/ radula, Monts/Nomencl. p. 132/Palenuo”;

and 11 paralectotypes Monterosato coll (MCZR

16476) with handwritten label by Monterosato “C.

radula/ Pal!!”. Spain. Alboran, -80 m, 1 sh, (SBR);

Cadiz, 1 sh (MNHN).

France. St. Henry (Marseille), 4 sh (coll. Locard

MNHN); Marseille, 5 sh (coll. Locard MNHN);

Toulon, 1 sh (coll. Locard MNHN); St. Raphael, 1

sh (coll. Locard MNHN); Sete, 2 sh (coll. Locard

MNHN).

Italy. Secca delle Vedove, -120/130 m, 2 sh

(PAO); Castiglioncello (Livorno), 1 sh (MAR);

Capraia Isl., 1 sh (BOG); Napoli, 2 sh (coll.

Monterosato, MCZR, sine numero, sub nomine ms.

var. aspera); Puolo (Napoli), 1 sh (DUR); Ischia Isl.,

1 sh (TRI); Gulf of Palermo, 10 sh (PUS); Gulf

of Palermo, 3 sh (coll. Monterosato, MCZR lot

16492, 3), 2 sh (coll. Monterosato, MCZR lot

17342); Porto di Palermo, 2 sh (coll. Monterosato,

MCZR lot 16476); Palermo, 3 sh (coll. Melville-

Tomlin, NMW); Mondello (Palermo), 1 sh (coll.

Monterosato sine numero, sub nomine “ purpurea

albino ”); Sciacca, 1 sh (coll. Monterosato, MCZR

lot 16492); Catania, (coll. Monterosato ex Aradas,

MCZR, lot 16476, 2 sh).

Algeria. Sine loco, 2 sh (coll. Monterosato,

MCZR lot 16492); Orano, 1 sh (coll. Pallary

MNHN).

Croatia. Between Pula and Ligthouse of Porer,

1 sh, legit W. Koers (SMNH lot 70484).

Mediterranean Raphitomidae, 3: on the Raphitoma pupoides complex, with the description of a new species

113

Description. In squared parentheses data of the

lectotype. Shell of medium size for the genus,

height 9-19 mm [14.8] (mean 13.81, std 2.90),

width 4-8 mm [6.4] (mean 5.90, std 1.10), fusi-

form-pupoid, slender, h/d 2. 2-2. 5 [2.31] (mean

2.32, std 0.09). Protoconch multispiral of 2.7 con-

vex whorls, height 580 pm, width 440 pm; proto-

conch I of 1.1 whorls, width 210 pm, with

irregularly placed small tubercles and orthogonally

cancellate sculpture; protoconch II of 1.6 whorls,

with a diagonally cancellate sculpture. Teleoconch

of 7-8 [7] convex whorls. Suture not impressed.

Axial sculpture of 12-17 [16] sligthly opisthocline,

elevate, strong ribs, and interspaces as broad as the

ribs (or sligthly broader). Growth lines visible

between the ribs on the last whorl. Spiral sculpture

on the last whorl of 5-6 [5] cordlets above the

aperture, thinner than axial ribs, with interspaces

three times as broad as the cordlets, and a secondary

cordlet bordering the subsutural ramp. Cancellation

squared. Secondary cordlets appearing occasionally

and thereafter becoming as strong as the others.

Subsutural ramp narrow, devoid of evident sculp-

ture. Columella simple, slightly sinuous anteriorly,

gently angled posteriorly. Outer lip thickened and

crenulated externally, with 8-9 [9] (rarely up to 11)

strong inner denticles, the most posterior smaller,

delimiting the wide and deep anal sinus, the most

anterior more robust and delimiting the funnel-like

siphonal canal. Siphonal fasciole of 7-8 [7] nodu-

lose cordlets, neatly spaced from the last spiral

cordlet. Colour from uniformly whitish to very ligth

chestnut brown, with darker subsutural ramp and

darker band on the lower part of the last whorl.

Violet hue on the background in particularly fresh

specimens. Comma-shaped white spots on the sub-

sutural ramp, arrow-like white spots inside some

cancellation interspaces. Soft parts are unknown.

Distribution. Provence, Western Mediter-

ranean and Tyrrhenian. A single record from neigh-

bouring Atlantic (Cadiz).

Remarks. Raphitoma radula could be confused

with shells of R. pupoides with non-obsolescent

sculpture, but it is easily diagnosed by its homo-

geneous ligth coloration with violet hue. It could

me mixed with very ligth or albinistic shells of R.

echinata (of similar size) from which it differs in

the less elevate spirals, the shorter and more roun-

ded aperture and the violet hue in fresh specimens.

Monterosato (1884: 132) introduced Cordieria

radula for the erroneously identified P. pur-

pureum sensu Philippi (non Mtg.), referring to the

examen (ex typo) of a specimen provided by

Philippi himself to Sylvanus Hanley. According

to Clare Brown (Leeds Museum Discovery

Centre) “Hanley’s collection came to us [LMG-

NS] in the 1950s after being broken up and many

parts sold on. Sadly, it seems as if the Philippi P.

purpurea didn’t make it to Leeds”. However, there

is little doubt that the type material of Cordieria

radula Monterosato consists of the type series at

MCZR.

ACKNOWLEDGEMENTS

Roberto Ardovini (Rome, Italy), Cesare Bogi

(Livorno, Italy), Philippe Bouchet (MNHN), Clare

Brown (LMG-NS), Sergio Duraccio (Napoli,

Italy), Jennifer Gallichan (NMW), Alfio Germana

(Trecastagni, Catania, Italy), Sandro Gori (Livorno,

Italy), Virginie Heros (MNHN), Andre Hoarau

(Frejus, France), Piera Iacovelli (MRSNT), Ronald

Janssen (SFM), Gabriele Macri (Scorrano, Lecce,

Italy), Alessandro Margelli (Livorno, Italy), Paolo

Mariottini (Rome, Italy), Henk Mienis (HUJ),

Attilio Pagli (Lari, Pisa, Italy), Paolo Paolini

(Livorno, Italy), Jakov Prkic (Split, Croatia), Paolo

Russo (Venezia, Italy), Carlo Sbrana (Livorno,

Italy), Gabriele Sercia (Palermo, Italy), Carlo

Smriglio (Rome, Italy), Peter Sossi (Trieste, Italy),

Gianni Spada (Vagrigneuse, France), Ennio

Squizzato (Loreggia, Padova, Italy), Morena

Tisselli (S. Zaccaria, Ravenna, Italy), Lionello

Tringali (Rome, Italy), Evi Vardala-Theodoru

(Athens, Greece), Angelo Vazzana (Reggio Ca-

labria, Italy), Anders Waren (SMNH), provided ma-

terial and informations. The staff at the Museo

Civico di Zoologia di Roma (MCZR), and particu-

larly Director Claudio Manicastri and Curator

Massimo Appolloni, continuously supported our

researches. Gianni Repetto (Alba, Italy) provided

precious bibliographic material. SEM photographs

were done at the “LIME” (Interdepartmental

Laboratory of Electron Microscopy) by Andrea Di

Giulio (Dept, of Biology, “Roma Tre” University,

Rome). Marco Oliverio (Rome, Italy) for the crit-

ical review of the manuscript and for helpful sug-

gestions.

114

Francesco Pusateri etalii

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Biodiversity Journal, 2016, 7 (1): 117-198

Monograph

On the origin of allopatric primate species

Marc G.M. van Roosmalen* &Tomas van Roosmalen

‘MVRS - Marc van Roosmalen Stichting, Leiden, The Nether lands

Corresponding author, e-m ail: marc.mvrs@gmail.com

ABSTRACT Here we present a theory on the origin of allopatric primate species that follows - at least in

Neotropical primates - the irreversible trend to albinotic skin and coat color, called “meta-

chromic bleaching”. It explains why primates constitute such an exceptionally diverse,

species-rich, and colorful Order in the Class Mammalia. The theory is in tune with the

principle of evolutionary change in tegumentary colors called “m etachrom ism ”, a hypothesis

propounded by the late Philip Hershkovitz. Metachromism holds the evolutionary change in

hair, skin, and eye melanins following an orderly and irreversible sequence that ends in loss

of pigment becoming albinotic, cream to silvery or white. In about all extant sociable Neo-

tropical monkeys we identified an irreversible trend according to which metachromic varieties

depart from the saturated eumelanin (agouti, black or blackish brown) archetypic form and

then speciate into allopatric taxa following the trend to albinotic skin and coat color. Speci-

ation goes either along the eumelanin pathway (from gray to silvery to cream to white), or

the pheomelanin pathway (from red to orange to yellow to white), or a combination of the

two. The theory represents a new and original evolutionary concept that seems to act indef-

initely in a non-adaptive way in the population dynamics of male-hierarchic societies of all

sociable primates that defend a common territory. We have successfully tested the theory in

all 19 extant Neotropical monkey genera. Our theory suggests the trend to allopatry among

metachromic varieties in a social group or population to be the principal behavioral factor

that empowers metachromic processes in sociable N eo tropical monkeys. It may well represent

the principal mechanism behind speciation, radiation, niche separation, and phy logeography

in all sociable primates that hold male-defended territories. We urge field biologists who study

primate distributions, demography and phy logeography in the Old World to take our theory

to the test in the equally colorful Catarrhini.

KEYWORDS Neotropical primates; phylogeography ; metachromic bleaching; speciation; radiation.

Received 20.12.2015; accepted 09.02.2016; printed 30.03.2016

INTRODUCTION

We could ask ourselves (Darwin, 1 859): “ Why

primates constitute by far the most diverse, species-

rich and colorful Order in the Class Mammalia?

Do primate diversity, metachromism and meta-

chromic processes relate directly to sexual selection ?

Or, rather to its generally complex, hierarchically

organized social structure and male territoriality?

If not sexual selection, what could be the principal

factor(s) in primate social behavior to be held

responsible for metachromic processes, speciation,

radiation, niche separation, and phylogeography?”

Inspired by A lfred Russel Wallace whose concept

of the “Origin of Species” was laid down in a paper

118

Marc G.M. van Roosmalen & Tomas van Roosmalen

he sent for review to Charles Darwin, here we

introduce a new and original theory about species

evolution taking place in particular in sociable

territorial prim ates. Our theory “ On the tendency of

metachromic varieties in sociable primates to

depart indefinitely from the agouti archetype and

evolve in advanced eumelanin, pheomelanin to

albinotic bleached allopatric taxa” is equally rooted

in life-long fieldwork on socio-ecology of all Neo-

tropical monkey genera, both in captivity and in the

wild. It closely follows the principle of evolutionary

change in tegumentary colors called “meta-

chromism”, a hypothesis propounded by Philip

Hershkovitz (1968; 1977).Metachromism holds the

evolutionary change in hair, skin, and eye melanins

following an orderly and irreversible sequence that

ends in loss of pigment through which a taxon of a

given genus or phylogenetic clade eventually be-

comes albinotic, cream to white. Individual hair

color or the entire coat changes from agouti (char-

acterized by alternating blackish-brown and reddish

bands on the terminal half of the hair) to uniformly

blackish -brow n , and thereafter to gray, and even-

tually to white or colorless, called the eumelanin

pathway; or, it changes from agouti to uniformly

reddish to orange to yellow to cream, and even-

tually white, called the pheomelanin pathway. The

process itself is called saturation, which means the

change from the primitive agouti pattern of the hair,

or part of the pelage, or the entire coat, to a satur-

ated eumelanin (blackish) or saturated pheomelanin

(reddish) coloration. The dilution, or gradual reduc-

tion in the amount of pigment deposited in the

growing hair, and disappearance of pigmentary

colors is called bleaching (Fig. 1). In the color of

the skin and iris of the eye, it follows the eumelanin

pathway (brown to drab, to gray, or blue), and then

it is termed depigmentation. Metachromism applies

to all mammalian species. It is thought to also occur

in bird feathers.

Our theory suggests that among social groups

or populations of advanced intelligent, socially

organized, male-territorial mammals, in particular

primates, phenotypical varieties (mutants) that

show slightly bleached eumelanin or pheomelanin

colored skin or coat characteristics do arise indef-

initely. Their melanocytes (skin cells that produce

the black pigment melanin) are smaller, and for that

or any other reason produce less melanin. In gen-

eral, the tendency of these metachromic varieties is

Figure 1. Bleaching from saturated eumelanin and saturated

pheomelanin fie Ids to white or colorless. Gradual reduction

in the amount of pigment deposited in the growing hair re-

sults in apparent change from blackish through brown, drab

gray to white or colorless in the eumelanin pathway, and

from reddish through orange, yellow, cream to white in the

pheomelanin pathway. Switching from the eumelanin to the

pheomelanin pathway occurs in saturation but not in blea-

ching (modified from Hershkovitz, 1977).

neotonic, taking place locally (e.g., naked muzzle,

bald head, euchromic blaze/forehead or part of the

coat, depilation of skin) or all over the body. Social

structure in most primate societies, in particular

those of the more advanced monkeys and apes, is

hierarchically organized, whereas male over female

dominance is the rule, with very few exceptions

(e.g., spider monkeys in the Neotropics and pygmy

chimpanzees in Central Africa adopted a matri-

archal social system, in which males patrol and

defend a common territory, and females are allowed

to transfer to neighboring social groups). Social

selection is the recognition of and preference for the

parental (or foster parental) phenotype in societal

grouping and mating. Social selection for color or

color pattern through assortative mating tends to

stabilize within a chromatic range recognized and

accepted by free-ranging but chrom otypically

imprinted members of the social group. Slightly

depilated or somewhat eumelanin or pheomelanin

bleached individuals deviant from the socially

selected skin or hair color pattern, in particular

when it is detected in adolescent to subadult males,

may be discriminated against by high-ranking

(alpha)-m ales. For that reason alone they can be

pushed into the periphery of the group. Depending

on the primate taxon or genus, such individual

young males may also be expelled from the parental

On the origin of allopatric primate species

119

group, and then become social ‘outcasts’. Peri-

pheral or outcast males do suffer on a daily base

from less and shorter access to the group’s prefer-

ential, comparatively more nutritious food sources.

They may join one another for reasons of social

comfort and during ranging or foraging they tend

to hang out together at the periphery of the group.

Eventually, they may decide to leave the pack as

all-male parties and roam around in much larger

areas than just the home range or territory of the

parental group. They then may attract young fe-

males from neighboring social groups. Together,

they may seek some hitherto overlooked, ‘empty’

or little-used living space in an attempt to settle

down and start their own family or social group. In

case the taxon or genus it belongs to shows ter-

ritorial behavior - which is the case in almost all

Neotropical monkeys - these emigrants will be sub-

sequently pushed out from neighboring territories

as well. Consequently, they will die from starvation,

parasite load and/or diseases forthcoming the

dietary constraints they are suffering from. Or, as a

mat ter of luck, in the end they may find some living

space that is not (yet) occupied, most likely at

considerable distance from the taxon’s core distri-

bution. Sometimes, such emigrant parties can be

forced to survive in peripheral habitat that has to be

considered marginal for that species to occur in.

In extremely rare cases, such parties might even

manage to circumvent a certain geographical barrier

and beyond it find for the species appropriate hab-

itat, where their specific ecological niche is not

occupied, as such involving a range extension. In

case that habitat is already occupied by a closely

related species, a battle for life will take place and

the best fitted taxon will drive the other to extinc-

tion, the red-handed tarn arin Saguinus lTlidas that is

replacing the bare-face tam arin S. bicolov. Only

over geological spans of time, for example after a

vicariance has taken place, suitable habitat may

open up where the taxon’s niche is not occupied by

another primate. One may imagine that along these

paths sm all reproductively isolated founder-colon-

ies that contain somewhat bleached and/or depilated

individuals may establish them selves there. For the

sake of survival alone they would unselectively

interbreed or hybridize. Inbreeding then may relax

stabilizing forces and stimulate or accelerate meta-

chromic and other degenerative (= non-adaptive)

processes. The more metachromic advanced each

successively isolated breeding colony is, or the

farther it has moved from the center of that taxon’s

dispersion, the nearer it will come to the end of its

metachromic evolution. And, the narrower will be

its range of chromic fitness (e.g., prey and predator

camouflage). This degenerative process, though,

may be counterbalanced if under strong natural

selection newly diverged forms, that evolve in a, for

the original species marginal or new habitat, niche

or landscape, at the same time selectively become

better fitted, more cooperative, more inventive, or

smarter in the adaptation process. This may happen

every time founder-colonies successfully travel

across existing geographical barriers, such as rivers,

watersheds, mountain ranges, or open areas with

arid scrub vegetation. Completion of the processes

of metachromic bleaching, depigmentation, or de-

pilation, whether taking place single or combined,

eventually will result in extinction of the race or

species. Unless the founder-colony or population in

time does find and manage to occupy hitherto

empty, but suitable habitat. Or: if it adapts to a dif-

ferent ecological niche, where skin and coat color

do not have survival value by lack of competition

from closely related species. Dead-end, isolated,

peripheral, or new habitats may be occupied by

metachromic dead-end populations, such as has

happened over and over in the Neotropics in ad-

vanced albinotic callitrichids, uakaris, sakis, titis,

capuchins, howlers, spider, woolly, and woolly

spider m onkey s.

RESULTS

In non-territorial, peaceable Dwarf Marmosets

Callibella humilis neotony and euchromism are

clearly demonstrated as infants are overall much

lighter colored than adults, showing a tendency to

albinotic. Their overall pelage is light brown, their

tail alternately light and dark-brown banded, and

their face flesh-colored with a circumference of

long, bright white hairs. From three months on, they

pass through a complete metachromic metamorph-

osis. Their overall coat turns into saturated eu-

melanin, the muzzle of their faces into pinkish, and

their semicrescent ocular rings or eyebrows into

white (Fig. 2). This natural process may be related

to slightly smaller melanocytes (skin cells that

produce the black pigment melanin) producing

overall less melanin.

120

Marc G.M. van Roosmalen & Tomas van Roosmalen

Callibella stands at the base of the phylogenetic

tree from which all extant A m azonian marmosets,

Cebuella and Mico, have derived (Van Roosmalen

& Van Roosmalen, 2003). It finds itself at the verge

of extinction, for it occupies the niche of exudate

gouging - that is feeding on resins ouzing out of

little holes they themselves have gnawed in the bark

of certain gum trees and climbers. That niche is

filled in by the advanced, larger, highly territorial

Amazonian marmoset genus Mico (its distributions

are shown in figures 5-7). We believe that these

aggressive, over twice as big callitrich id monkeys

have displaced the non-territorial dwarf marmoset

and taken over its specific feeding niche all over

its former, much larger range - the entire interfluve

delineated by the Rios Madeira, Amazonas and

Tapajos. The genus Callibella is thought to have

evolved there in the late-Pliocene to early-Pleisto-

cene landscape that was dominated by lacustrine

seasonally inundated clear-water igapo wetlands.

Being peaceable monkeys that like their neighbor’s

company instead of attacking or trying to kill them

apparently has not been an evolutionary success

among primates (Van Roosmalen, 2013a, b; 2015).

Contrastingly, the pygmy marmoset Cebuella

that derived from prototypic Callibella nowadays

occupies the entire western Amazon Basin. We

believe it was so successful because Cebuella ,

being allopatric with Callibella and Mico, could

occupy the ecological feeding niche of exudate

gouger west of the Rio Madeira. There, it did not

have to face competition from other callitrichids

over exudate food sources. Indeed, Amazonian

tamarins (genus Saguinus) that range west of the

Rio Madeira (Figs. 7-13) lack the elongated tusked

mandibular second incisors needed for tapping sap

Figure 2. Ontogeny in Black-crowned D w arf M arm o sets Callibella hwnilis V an Roosmalen & Van Roosmalen

(2003) based on photos of captive and wild individuals (Van Roosmalen et al., 1998).

On the origin of allopatric primate species

121

from tree barks. As such, tamarins do not directly

compete with pygmy marmosets over gum.

Instead, tamarins of different taxa are reported

to parasitize on pygmy marmosets by licking the

resins from tap holes made by the latter.

Cebuella pygmaea being overall agouti colored

is clearly the most archetypic among the two extant

taxa of pygmy marmoset. Distributed north of the

Upper Amazon River(Rio Solimoes/Rio Maranon)

and specialized in exudate gouging, the species (or

its precursor) seems to have adapted to seasonally

white-water inundated floodplain forest (varzea)

habitat. Somewhat pheomelanin bleached colon-

izers of ancestral C. pygmaea (having an orange

colored tail and breast, progressively bleached yel-

low to white belly, yellow-white mustache, naked

pink-colored muzzle and circumocular rings) fol-

lowing the trend to allopatry once must have man-

aged to traverse the Amazon River proper, on floa-

ting varzea islands and/or passively through ri-

verbend cut-offs (oxbow lakes). By lack of

competitors the nearest to albinotic taxon Cebuella

tliveiventris - the form that derived from allopatric

archetypic C. pygmaea - could then have extended

its range from the Rios Javari and Jurua east as far

as the Rio Madeira and south of the Amazon River

as far as the Bolivian Amazon (Fig. 3). There, it

secondarily adapted to never inundating terra firm e

high forest. Nowadays, it is found there, especially

at edges of treefall clearings and in secondary

growth. As C. tliveiventris is fully allopatric with C.

pygmaea and, moreover, shows completely dif-

ferent habitat preferences, we here propose to at-

tribute both taxa full-species status naming them

C. pygmaea and C. niveiventris. During our system-

atic surveys of primate distributions and diversity

Figure 3. Present-day distributions are here depicted for Black-crowned Dwarf Marmosets genus Ccillibellci and Pygmy

M arm osets genus Cebuella, representing the sm allest m onkey s in the w orld .The current distribution of the m onotypic genus

Callibella perhaps has to be considered the sm allest of any prim ate in the N eotropics.

122

Marc G.M. van Roosmalen & Tomas van Roosmalen

carried out in the matrix terra firme hinterland

stretching out behind the floodplain of white-water

rivers (i.e., the Rios Javari, Jurua, Purus and

Madeira), we were not able to detect any pheno-

typical difference between individuals sighted

at any point along these far-apart rivers. It may

indicate that in highly territorial monkeys like

pygmy marmosets that occupy large distributions

delineated by some of the largest tributaries of the

Amazon River, phenotypical characters of skin and

pelage coloration and/or local hair growth or de-

pilation seem to have stabilized. In other words, we

believe that within a given monkey’s distribution

something like a gradient of slightly differing

phenotypes or color morphs, or geographic races,

in reality does not exist. These and other observa-

tions from the larger field have led us to attribute

full-species status to monkey taxa such as C.

pygmaea and C. niveiventris that we ourselves have

confirmed to be phenoty pically stable throughout

their (sometimes very large) range.

Here, we would like to propose a new species

concept: ecospecies. This species concept is further

corroborated by the here introduced evolution

theory that aims to explain the origin of allopatric

primate species. We define ecospecies as follows:

"An ecospecies is a genetically isolated population

or group of populations of a kind that does not

undergo any gene flow from other populations of

one or more closely related kinds, and that demon-

strates a stabilized, well-defined phenotype over its

entire range, in which it occupies and defends a

specific ecological feeding niche against any out-

side Competitor'’'. This definition of a primate

species avoids the confusing, rather arbitrary dis-

tinction between species and subspecies (or race),

for it adds sociobiological factors to geographical,

geom orphological and phy tosociological ones that

act on the evolutionary process of primate speci-

ation and radiation. Following this concept, for in-

stance, an enclave population of Callibella humilis

that we found living year-round in the seasonally

inundated floodplain forest (igapo) along both

banks of the Rio Atininga - genetically isolated

from the main population occuring in terra firme

forest at least one-hundred km to the north - should

be given its own species name and treated as such.

Or, in case the ranges of two saddle-back tamarins

of the SaguinUS fuscicollis Clad e, hitherto taxonom-

ically treated as subspecies, are separated by a con-

tact zone, where territorial behavior effectively im-

pedes gene flow through hybridizing, both popula-

tions should be attributed full-species status.

The c allitric h id s Goeldi’s Monkey Callimico

and Black-crowned D w arf M arm o set Callibella do

represent the only monospecific (= monotypic)

primate genera in the Neotropics. Callimico lives

in the upper Amazon Basin region of Bolivia,

Brazil, Peru, Colombia, and Ecuador (Fig. 4).

Goeldi’s monkey coat coloration is saturated eu-

melanin, blackish or blackish-brown. It forages in

dense scrubby undergrowth of low mixed forests

with discontinuous canopies and in so-called

‘tabocais’ (low forest dominated by bamboo) at

levels of less than five meters. Social groups consist-

ing of monogamous pairs with single offspring

count on average six individuals. Groups live in

patches of suitable habitat, often separated by miles

of unsuitable vegetation. Goeldi’s monkeys are

vertical dingers and leapers able to leap horizontal

distances of up to four meters between branches. As

they are peaceable monkeys not showing any form

of territoriality, Goeldi’s monkeys often associate

in mixed species groups with different species of

tamarin SaguinUs (Mittermeier et al., 2013). The

fact that this primitive little monkey, just like the

dwarf marmoset Callibella, remained archetypic in

its blackish agouti coat coloration, is peaceable, is

not showing any territorial behavior towards its

neighbors, is occupying a unique feeding niche

(foraging on the ground for fungi and invertebrates,

and for fruits at low levels of a discontinuous

canopy), and over geological time-span did not

diverge into more than one taxon, strongly supports

our doctrine that attributes speciation and radiation

in m ale -territorial Neotropical primates primarily

to the trend to allopatry as expressed in meta-

chromic bleaching.

As shown in the schematic distribution map of

all known Amazonian marmosets (Fig. 5), each in-

terfluve in the area delineated by the most effective

riverine barriers - Rio Amazonas in the north, Rio

Madeira in the west, Rio Guapore in the south, and

Rios Tapajos-Juruena and Xingu in the east- is

inhabited by a different taxon of MicO, which

species phylogeographically and phylogenetically

radiated away from an ancestral, archetypic agouti-

colored form much resembling the extant species

M. melanuruS (Van Roosmalen et al., 2000) from

the upper Rio Aripuana basin - the taxon with the

On the origin of allopatric primate species

123

southernmost distribution of all Amazonian mar-

mosets to be placed at the base of MicO’s phylo-

genetic tree.

Four monophyletic cladistic Groups or Clades

are distinguished: the B are-ear M. OTgentatUS C lade,

the (Tufted-ear or) Tassel-ear M. hwTieralifer Clade,

the W hite-m an tie (w hite-hip) M. melcMUruS Clade,

and the Orange-leg M. tnarcai Clade (Figs. 6, 7).

Within each Clade, the evolutionary pathway

towards advanced metachromic bleached (and

ultimately albinotic) taxa can be plausibly retraced.

Albinotic forms in dead-end distributions may

eventually go extinct (i.e., M. chrysoleuCOS in the

M. humeralifer Clade; the new Mico species that

occurs between the Rios Teles-Pires and Ronuro,

M. leucippe, and M. argentatus in the M. argentatus

Clade; M. acariensis and M. saterei in the M.

melanurus Clade; and M. manicorensis in the M.

marcai Clade). In territorial sociable primates the

principle of metachromic bleaching that seems to

fuel the trend to allopatry is an irreversible, seem-

ingly non-adaptive evolutionary pattern. The meta-

chromic pathway followed within the M. argentatus

Clade is a predominantly pheomelanin one, with

first the nearest to archetypical, dark orange-colored

taxon M. emiliae from the Rio Iriri. From M. eifliliae

diverged in southward direction the moderately

bleached new species that we identified to occur

between the Rios Ronuro and Teles-Pires, and

northward the advanced albinotic taxa M. leucippe

(all white with a pink face) and M. argentatus (all

white with a black tail). The latter occupy dead-end

distributions, as they are pressed at their northern

limit against the u ntraversable Rios Tapajos and

Amazonas, respectively. Within the tufted-ear or

tassel-ear Clade of Mico the metachromic pattern

followed the eumelanin pathway, from the darkest

agouti-colored taxon M. mauesi going straight into

Figure 4. Present-day distribution of monotypic Goeldi’s Monkey CcillitYlicO goeldii.

124

Marc G.M. van Roosmalen & Tomas van Roosmalen

the overall whitish and gray M. hwnercilifer in the

Clade’s northernmost dead-end distribution (delin-

eated by the Amazon and Tapajos Rivers). Along

the pheomelanin pathway it diverged into the

overall orange and white colored golden-white

tassel-ear marmoset chrysoleucos, the species that

occupies the westernmost dead-end distribution

delineated by the Rios Madeira and Aripuana.

W ithin the w hite-m an tie (w hite-hip) C lade of Mico

the pathway followed goes from the nearest ar-

chetypic agouti-colored taxon M. melciYllirus in

northern direction to the advanced pheomelanin

bleached half-way albinotic taxa M. intennediliS ,

M. acariensis , and M. saterei. And within the fourth

Group of Mico, the orange-leg M. MClYCCli Clade, the

pathway followed in northern direction starts from

the metachromic nearest to archetypic taxon M.

ITiarCCli diverging into the advanced euchromic to

almost albinotic taxon M. YYlCOflicOYCYlsis , and in

western direction proto -lTlCirCCli evolved into the

slightly but progressively bleached taxa M. Yligri-

CepS and M. VOYldoni, all three occupying dead-end

distributions delineated by the untraversable Rio

Madeira (after the Amazon River proper the second

strongest river barrier in the entire Amazon Basin).

As all interfluves occupied by a different Mico

species show dead-end distributions delineated by

untraversable rivers at their northern and western

limits, each species represents a different stage

along the eumelanin or pheomelanin pathway that

is frozen in time, but at the end of its metachromic

evolution it invariably will turn into albinotic (Figs.

6, 7). Once arrived there, such primate taxa will in-

evitably go extinct, unless a founder-colony man-

ages in time to cross the geographic (riverine)

barrier by means of a river bend cut-off, by hopping

on varzea forested floating islands, or by circum-

venting a geographical barrier. According to the

doctrine, the evolutionary rate of metachromism is

primarily controlled for by the trend to allopatry,

and secondarily by environmental and genetic

factors which may accelerate, retard, or terminate

metachromic processes, or hold them in dynamic

equilibrium, but cannot alter, reverse, or deflect

them from their course. Hypothetically, growth and

spread of a founder-colony of a certain Amazonian

marmoset across a certain interfluve delineated by

rivers, entails social selection. Effective selection

stabilizes the mean chromotype of the colony at a

color tone or grade inbetween that of the founders

and that of the albinotic ones towards which all

monkeys tend. Amazonian m arm osets (genus Mico )

represent an advanced stock of callitrichids that

evolved as late as the Pleistocene, south of the

Amazon River and east of the Rio Madeira, from

an ancestral stock of the Ccillithrix ouistitis occur-

ring in Central and SE Brazil (Van Roosmalen &

Van Roosmalen, 2003). About 1.5 MYA, a major

vicariance took place - the break-through by the

proto-Madeira River of the continental watershed

running across the Chapada dos Pareds in Rondo-

Tlia (Grabert, 1991). Thereafter, the entire area south

of the Amazon and east of the Madeira drastically

reversed its drainage pattern. Former rivers that

since the beginning of the Pliocene had been drain-

ing the extensive clear-water wetlands in north-

south direction, dried up. New rivers (mostly of the

black-water type) arose and began to drain the area

in opposite direction, from south to north. Most of

these rivers emptied out in the Rio Madeira, some

directly in the Amazon River. Founder-colonies at

different phenotypic stages of metachromic bleach-

ing that derived from archetypic M. melcinurus -

pushed by the trend to allopatry - subsequently

invaded and inhabited the newly formed interfluvial

terra firm e ‘islands’ that new rivers had been

creating. These newly available lands offered them

their preferred habitat of terra firme rainforest, in

which they filled the niche of exudate gouging,

which niche east of the proto-Madeira River was

hitherto exclusively occupied by the much smaller

and peaceable, non-territorial dwarf marmoset

Callibella huinilis (Van Roosmalen & Van Roos-

m alen, 2003). Ever since, Ccdlibcllci hwflilis seem s

to have lost the battle against the aggressively

expanding Mico newcomers. Our assumption is that

the dwarf marmoset has been locally driven to

extinction almost all over its former range since the

genus evolved in the late Pliocene. Presently, the

black-crowned dwarf marmoset hangs on along the

westbank of the lower Rio Aripuana. As a com-

mensal, it takes refuge on the terras pretas (human-

made black-earth farmland) from the deadly attacks

of the local A m azonian m arm oset Mico MClTlicoreYl-

sis (Van Roosmalen et al., 2000; Van Roosmalen &

Van Roosmalen, 2003). This example may well

demonstrate that a specific ecological niche such as

that of specialized gougers and feeders of gum

(exudates) in a certain habitat (e.g., primary rain

forest) can only and exclusively be occupied by a

On the origin of allopatric primate species

125

Amazonas

hvmtrrahtrr f

nov .

Amazonian Marmosets

Cebuella Mico Callibella

I ^

Figure 5. Schematic distributions as delineated by (for Amazonian Marmosets) un traversable rivers drawn

for all known Amazonian Marmosets belonging to the genera Callibella, Cebuella, and Mico.

126

Marc G.M. van Roosmalen & Tomas van Roosmalen

ALL PYGMY, DWARF & AMAZONIAN MARMOSETS

Cebu elf a (pygmaea) pygmaea and C. (p.) nivetvomris

? 1 %Callibeila humilrs

Tassel-ear humeralifer Clade

Mico humeralifer t imauesi chrysoleucos

Bare-ear argentaws Clade

Mico sp, nov, Rio Ronuro

emiliae £ argentaws leucippe

hite-mantle melanurus Clade

Mico melanurus ^ intermedia s

m acariensis saierei

W Orange-leg marcaf Clade

^ Mico rondoni Qmarcai

mantcorensis

Ba ^

_ .* "v** 1 4ft

Figure 6. Geograph ical distribution s delineated by rivers drawn in one map for all known Amazonian Marmosets

that belong to the marmoset genera CcillibellcL, Cebliellci , and Mico.

single taxon that defends it, in this case even

beyond generic bounds.

Figures 5-7 demonstrate that about all inter-

fluves occupied by a single species of Mico show

dead-end distributions delineated by for rainforest

habitat-specialists untraversable rivers at their

northern and western limits.At their southern limits,

all distributions invariably show a mostly narrow

open-end, where a contact zone between two

adjacent distributions must exist. Hybridization

between Amazonian marmosets, though, has never

been seen orreported in the wild. This may well be

attributed to strong social and sexual selection.

Indeed, all Amazonian marmosets of the genus

Mico developed hypertrophied external genitalia in

each gender that are physically greatly differing

among related taxa (Van Roosmalen et al., 2000)

(Figs. 8-11).

We ourselves have kept, raised and bred with a

number of Amazonian marmosets, both in free-

ranging and captive conditions. Expressive and

often violent territorial behavior of all members of

a social group, aside of species-specific sexual

display of external genitalia, pheromones and scent-

marking of one another’s coat, has always preven-

ted our marmosets from hybridizing (interspecific

cross-breeding). For instance, we kept breeding

social groups of all three taxa of the tassel-ear M.

humeralifer Clade (i.e ., M. humeralifer , M. mauesi,

and M. chrysoleUCOS). To avoid one group from

wiping out the other, we had to keep different

species in separate cages, whereas we let only one

group of M. chrySOleUCOS free-ranging in the forest

that surrounded the compound. Even so, adults

were still seen trying to grab and bite one another

through the fine-mess wire. From our unique exper-

On the origin of allopatric primate species

127

Cehttella pygi

nova

argentatus

Clade

Tassel-ear

humeralifet

Clade

hello

hit mil is

White-mantle

Ml co melon it rtts

Clade

Orange-leg

Mi co mttreai Clade

12tm

Figure 7. Radiation and metachromic diversification following eumelanin and pheomelanin pathways of metachromic

bleaching depicted for all recognized phylogenetic C lades of Amazonian ( MicO ), D w arf ( CciUibellci) , and Pygmy Marmosets

( Cebuella) depicted to scale.

128

Marc G.M. van Roosmalen & Tomas van Roosmalen

Figures 8-11. In all taxa of Mico, both m ales and fem ales evolved hypertrophied . species -specific , in anatomical respect very

differently shaped external genitalia. Fig. 8: male M. manicOTensis sexually displaying; Fig. 9: exposed pudenda in adult

female M. acarietisis ; Fig. 10: pudenda with 2 cm long vaginal lips in M. SCLterei, Fig. 11: pudenda in M. CLCClriensis. This

feature supports our view that all taxa of Mico should be considered different species and not just metachromic color morphs.

ience having kept all kinds of marmosets (until

today, not a single zoo in the world has any Mico

on exhibit) and other callitrichids, both in captivity

and free-ranging in a tropical rainforest environ-

ment, we believe that where adjacent distributions

of two species of Mico are not defined by an un tra-

versable river, a sharp-lined contact zone must

exist, where cross- breeding never takes place. This

assumption concurs with the principle of meta-

chromic bleaching being irreversible. In theory,

only through cross-breeding with a darker, overall

more saturated eumelanin taxon the metachromic

pathway to albinotic could be reversed, something,

however, that will never happen in the wild.

As all Mico do display strong interspecific

territorial behavior - each group defending its living

space by means of (often ritualized) territorial

boundary conflicts - within a given contact zone

cross-breeding will not take place between neigh-

boring groups of different but related ecospecies, as

distance is maintained by regularly performed

boundary conflicts. This way, any gene flow

between phenotypically different populations is

impeded. In phylogeographic terms, the farther

radiated away from the origin of a Clade’s disper-

sion - that of the nearest to archetypic species within

a monophyletic Clade - the more progressively

bleached the species will become. Partly or fully

albinotic taxa, therefore, often occur in or near the

Clade’s dead-end distributions.

In figures 12-15, we have visualized the phylo-

geographic distributions, radiation, and supposed

pathways of metachromic bleaching of all known

Tamarin Monkeys genus Sciguinus. We have di-

On the origin of allopatric primate species

129

vided them up in the following monophyletic

Groups or Clades: the Saddle-back Tamarins of the

S. fuscicollis Clade (Fig. 13); the Black-mantle

White- mouth Tamarins of the S. nigricollis Clade

in one map combined with the Mustached Tamarins

of the S. my StttX Clade, the Red-chested Mustached

S. labiatUS Clade, and the Emperor Mustached S.

imperator Clade (Fig. 14); and the Bare-face Tamar-

ins of the S. midas, S. bicolor and S. geoffroyi

Clades (Fig. 15). To complete the c a llitric hid

picture, we have visualized the distributions of the

Fion Tamarins genus LeOYltopitheCUS , and the True

Marmosets or Ouistitis genus Callithrix, from SE

B razil (Fig. 16).

In geological history, speciation and radiation

within the Saddle-back Tamarins of the S. juscicol-

lis Clade (Figure 13) went along two pheomelanin

pathways of metachromic bleaching: one sub-Clade

radiated south of the Amazon River from east to

west, from the most saturated eumelanin, nearest to

archetypic taxon S. MUra (green distribution) to the

completely albinotic all-white taxon S. melanoleii-

CUS (blue distribution) via the taxa S. avilapiresi,

S. fuscicollis, and S. CTUzlimai. The bleaching

process took first place in the head parts - muzzle

and blaze - and, after having traversed the Rio Jurua

back to its right bank, the metachromic bleaching

process completed from the overall orange-colored

taxon S. cruzlimai into the fully albinotic taxon S.

melanoleucus. A nother radiation took place from S.

mura directly into S. Wcddclli, and, after having

traversed the Rio Purus, into the overall light-brown

colored taxon S. primitivUS - both with a fully al-

binotic blaze and muzzle/mouth. A second sub-

Clade of saddle-back tamarins radiated from the

Peruvian Amazon in eastern direction, from the

saturated eumelanin nearest to archetypic taxon S.

leUCOgenys (light blue distribution) into the slightly

ALL PYGMY. DWARF * AMAZONIAN MARMOSETS

Cpjrfpn#**) jTppnM* *nd C

/* WC**+H**+mm

^2 ■*< lltllNir ttirntfMtfftf CUrt*

fcteO ftWIHWllf MM/ tfVyWQ »is€Ot

Bare-eer ifpemaws Clade

T r L • «« «p Rww

Whlte-manUf mrt-anurus Clade

Vxc tmianurut £

******

Orarvpe-ieo m»rc*i Clade

v<9 nmAM §mvui

SADDLE-BACK TAMARINS Sapuimrs fuSCICOMi

WHITE -MOUTH TAMARINS S»gtmit/s mgn colhs Clade

a JHg n pft fcf n fit**** i § a i^/j wAH

MUS TACHED TAMARINS S mysiax Clade

m m pMtMu* 0 m etae

Red "Cheated M- T. S. Clade

Iduhri wtottrm - r momnd

Emperor U , T S rmperarof Clade

Figure 12. D istribu tions of all N eo tropical Tam arin Monkeys, genus SaguiflUS,

com pared with those of all Amazonian Marmosets.

130

Marc G.M. van Roosmalen & Tomas van Roosmalen

bleached taxa S. Uligeri and S. nigrifrons, and after

crossing the upper Amazon River (where it is called

Rio Maranon) northward into the progressively

bleached taxa S. lagOUOtUS, S. fusCUS, and S. tri-

partite, the latter three taxa being distributed north

of the Amazon River in the Ecuadorian, Colombian,

and Brazilian Amazon.

Within the Black-mantle White-mouth Tam ar ins

of the S. nigricollis Clade (Fig. 14) that is dis-

tributed only north of the Amazon River in the

Brazilian, Ecuadorian and Colombian Amazon, the

nearest to archetypic saturated eumelanin taxon is

S. nigricollis. It radiated northwestward and di-

verged into the slightly bleached taxa S. graellsi and

S. hernandezi. The S. nigricollis Clade is sympatric

with the saddle-back tamarins of the taxa S.

lagonotus, S. tripartitus and S. fuscus (Fig . 1 3 ) .

However, they occupy different ecological niches

and therefore can be seen traveling and foraging in

mixed species associations, with the larger-sized

black-mantle tamarins in the lead and staying

higher up in the canopy of the terra firm e rain forest.

Within the Emperor Mustached Tamarins of the S.

imperator Clade both extant taxa are already

progressively bleached, the grayish taxon S. Sllb-

griscescens slightly more so than S. imperator. In

the upper Rio Purus region there must exist a

narrow contact zone between the two taxa along the

southernmost open-end distribution of S. imperator.

Within the Red-chested Mustached Tamarins of the

S. labiatus Clade, Saguinus labiatus occupies the

southernmost distribution and represents the nearest

to archetypic taxon with a dark red chest and

thin-lined white mustache. It radiated north of the

Rio Ipixuna and diverged into the advanced orange-

chested taxon S. rufiventer that has a m ore bleached

white mustache and head-stripe. The third taxon of

the S. labiatUS Clade is S. thomasi the precursor of

which once must have traversed the Rio Solimoes.

It m ight have been replaced later by S. illUStUS north

of the Rio Solimoes as far west as the Rio Japura.

Saguinus thomasi nowadays only occupies the

lower Rios Solimoes /Japura interfluve. It represents

the most progressively pheomelanin bleached taxon

of the S. labiatUS Clade in its light orange-colored

chest and the broad-lined triangular white mus-

tache. Within the mustached tamarins of the S.

mystax Clade, the more saturated eumelanin,

nearest to archetypic form is represented by the

taxon S. mystax that is distributed west of the Rio

Jurua. After traversing the Rio Jurua, the Clade has

radiated eastward while further bleaching along the

pheomelanin pathway into the orange-crowned

taxon S. pileatUS, and along the eumelanin pathway

diverging directly from S. YYVyStaX into S. plutO. The

latter taxon is overall more grayish and has a dis-

tinctive albinotic spot around the base of the tail. In

the lower Rios Jurua /Purus interflu ve we have

sighted S. plutO ranging always in mixed-species

association with the smaller saddle-back tam arin

S. avilapiresi, with S. plutO always in the lead and

S. avilapiresi rushing behind and below the group

of S. plutO in the lower strata of high forest, always

in a hurry feeding on S. plutO’s left-over food items.

A hypothetical pathway of allopatric speciation,

radiation and metachromic bleaching followed by

the B are-face Tamarins of the S. midas, S. bicolor

and S. geoffroyi sub-Clades m ay have had its origin

in the Guianas (Fig. 15). An all-black, saturated

eumelanin archetypic precursor of S. midas may

once have traversed the lower Rio Amazonas and

speciated allop atric ally into the black-handed taxon

S. niger. Or vice-versa (archetypic black-handed

S. niger may once have traversed the lower Rio

Amazonas and speciated allopatrically into the red-

handed S. midas). The same or another all-black

precursor of S. midas may have traversed the Rio

Negro and allopatrically speciated into the taxon S.

inuStUS that is all-black with a white-mottled face.

Saguinus inuStUS nowadays occupies the entire

interfluve between the Rio Negro in the north, and

the Rios Solimoes, Japura and Caqueta in the south.

A founder-colony of a predecessor of S. inuStUS

driven by the trend to allopatry may then have

ventured from the taxon’s westernmost distribution

into the NW Colombian Rio Magdalena basin.

Once having inhabited the Rio Magdalena basin, it

may have diverged along a pheomelanin pathway

into the extant taxon S. leucopus that has a white-

hairy facial circumference similar to S. inUStUS.

Saguinus leucopus then may have radiated further

into the progressively pheomelanin bleached,

almost euchromic taxon S. OedipUS, and from

there into the near-albinotic taxon S. geoffroyi that

is distributed from extreme NW Colombia into

Panama, as such the farthest away from the center

of dispersion of the Bare-face Tam arin Clade. With

respect to the three derived euchromic taxa of the

S. bicolor Clade, as we have mentioned elsewhere,

these taxa find themselves in the process of being

On the origin of allopatric primate species

13 1

rigorously displaced from their respective territories

by the now sympatric archetypic saturated eu-

m elanin red-handed tam arin S. midas. All three taxa

(i.e S. bicolor , S. martinsi, and S. ochraceus) find

themselves pushed with the back against the untra-

versable Rio Negro and/or Rio Amazonas (Fig. 15).

At present, the red-handed tam arin S. midas is

wrapping up the last stage of its range extension

towards the south to the cost of all three Bare-face

Tamarins of the S. bicolor subClade. This battle

over a specific ecological (feeding) niche, in which

two sympatric, closely related primate taxa are

involved, will inevitably lead to the extinction of

the most euchromic among the two, that is the

Bare-face Tamarins of the S. bicolor sub-Clade:

the taxa S. bicolor, S. martinsi, and S. ochraceus

(Fig. 15).

The eumelanin S. midas sub-Clade might have

originated in the Guianas north of the watershed

with the northeastern Amazon formed by the

Tumac-Humac Mo un tains and the open wet savan-

nas of Roraima and Para. A predecessor of the S.

midas sub-Clade, perhaps the extant S. midas itself,

once may have circumvented the watershed

between the Guianas and Brazil by traversing the

Parii Savanna, whereafter it may have penetrated

far southwards into the northeastern quadrant of the

Brazilian Amazon. We assume that before some

vicariance took place this vast territory or a large

part of it was inhabited by precursors of the closely

related Bare-face Tamarins of the S. bicolor sub-

Clade. Apparently, as the two sub-Clades do occupy

the same ecological niche, (proto )-midas sub-

sequently has displaced (proto)-bicolor over most

of its former range. This battle is still being fought

over between S. Iflidas and each taxon of the S.

bicolor sub-Clade, but it seems to come close to its

end. The process of replacement is accelerated by

deforestation and other human disturbance such as

road-building that has taken place north of the rap-

idly expanding megacity of Manaus. This ongoing

story clearly demonstrates interspecific intolerance

in closely related territorial monkeys that occupy

and exploit the same ecological niche. It inevitably

leads to displacement, or sooner or later extermina-

tion of the more progressively bleached (eu-

chromic) taxon. This kind of replacements may take

place after a geographic barrier has been success-

fully overtaken by the more saturated eumelanin

(more adaptive and/or aggressive?) of two related

taxa. Or: after a vicariance has removed a hitherto

gene-flow impeding geographic barrier inbetween

the distributions of two or more closely related

species.

Vicariance (from Latin vicariuS) means a pro-

cess by which the geographic range of an individual

taxon, or an entire biota, is split into discontinuous

parts by the formation of a physical barrier to gene

flow or dispersion .

Today, the S. bicolor sub-Clade only inhabits a

20-30 km narrow strip of terra firm e rain forest

alongside the southernmost edge of the Pre-Cam-

brian Guayanan Shield.

The three bicolor taxa are so to speak pushed

with the back against rivers that happen to be the

widest and most difficult to traverse on the entire

S ou th - A m eric an continent: the Rios Negro and

Amazonas. The three extant taxa of Bare-face

Tamarins each occupy what is called a “dead-end

distribution”. The distribution of the half-brown,

half- w hite taxon S. bicolor measures not m ore than

20-30 x 200 km, delineated in the west and south

by the Rios Cuieiras, Negro, Am azonas, and Urubu.

Bicolor’s neighbor to the east - the almost fully

bleached, ochraceous colored taxon S. Ochraceus -

occupies the interfluve between the Rios Urubu and

Uatuma. To the east of its distribution, the pheo-

m elanin, light orange-colored taxon S. martinsi

occupies the lower interfluve between the Rios

Uatuma and Nhamunda (Fig. 15). Disputedly, a

now extinct precursor of the Bare-face S. bicolor

sub-Clade that once ranged somewhere to the north

of the Amazon River, may have driven the three

extant taxa of the S. bicolor subClade - each at a

different stage of metachromic bleaching - into the

small interfluvial dead-end distributions, that they

occupy today. The saturated eumelanin (blackish-

brown) red-handed tamarin S. midas that later ex-

panded its range to the south, is now simultaneously

invading the three remaining adjacent interfluvial

stronghold territories of the S. bicolor sub-Clade.

A sharp-line contact zone drawn between S.

midas and S. bicolor territory has been notified by

us in the early 1990s to run at 28-30 km north of

and parallel to the Negro and Amazon Rivers.

While running a halfway house for orphaned mon-

keys situated right at the edge of the contact zone,

we have repeatedly witnessed different social

groups of S. midas raiding resident family groups

of S. bicolor. These incidents invariably ended up

132

Marc G.M. van Roosmalen & Tomas van Roosmalen

SADDLE-BACK TAMARINS Saguinus fusticollis Clade

% f avilapiresi f. primrUvus QfJtiigeri

f. wedddli (f) mclanoicucus f. ieucogonys

fuscicottfs fm.) crandaili Af. lagonows

cruzlimai t. nigrifrons

._$((■) trip annus

f, fuscus

t mura

BLACK-MANTLE WHITE-MOUTH TAMARINS Saguinus nigricoUis Clade

n. nigricollis % n. gractlsi 0 n. hamandazi

MUSTACHED TAMARINS S. mystax Clade

m.mystax m. pileatus m. phito

Red-chested M. T. S. labiatus Clade

labiatus I. rufivanter I. thomasi

Emperor M, T. S, imperator Clade

imparmor i. subgrtsascens

Figure 13. Distributions, allopatric speciation. radiation, and supposed pathways of metachromic bleaching in all known

Saddle- back Tamarins of the Saguinus fuscicollis Clade. Figure 14. Idem, in the more robust, larger-sized Black-mantle

White-mouth Tamarins of the S. nigvicollis Clade, the Emperor Mustached Tamarins of the S. iwiperatOV Clade, the Red-

chested M ustached Tam arins of the S. IcibiutliS C lade, and the M ustached Tam arins of the S. tnystClX C lade.

On the origin of allopatric primate species

133

BARE-FACE TAMARINS GLADE

Saguinus gepffroyi

Saguinus ocdipus

Saguinus hucppuS

• ' Saguinus bicolor

Saguinus marlin si ocbraceus

Saguinus maninsi maninsi

9 Saguinus midas

# Saguinus nigpr

Saguinus inustus

LION TAMARINS - Leontopithecus

L. chrysopygus L. cbrysomelas L caissara i L rosaiia

TRUE MARMOSETS OR OUISTIT1S - Catfithrix

X C. jacchus |1C. panklllata .yt C. kuhfii

C, gvoffroyi C. flaviccps C. aurita

Figure 15. Distributions, allopatric speciation, radiation and supposed pathways of metachromic bleaching in all extant

B are-face Tamarins that belong to the SagllinUS midciS, S. bicoloY, and S. geoffvoyi sub-Clades. Figure 16. Distributions,

allopatric speciation. radiation and supposed pathways of metachromic bleaching in all known True (or Atlantic Forest)

Marmosets (genus Cdllithrix ) and Lion Tamarins (genus LeOiltOpitheCUS) from SE Brazil.

134

Marc G.M. van Roosmalen & Tomas van Roosmalen

in the defensive, less aggressive (more sensitive?)

S. bicolor bitten to death. Now, about twenty years

later, S. fflidciS has extended its range at least five

km further to the south to the cost of S. bicolor oc-

cupied territory. As S. midoS is more opportunistic

and flexible in its habitat preferences - venturing

also into secondary growth and edge habitats such

as roadsides - it rapidly penetrates into S. bicolor

territory, at some places (e.g., Ducke Reserve)

already reaching the outskirts of Manaus. Running

a rehabilitation center for orphaned monkeys, we

sometimes received whole families of S. bicolor

that were rescued from isolated pockets of forest in

urbanized areas. After some time spent in quaren-

taine, we used to put them in large cages built on

poles in the middle of the rain forest about thirty

km north of Manaus in an attempt to reintroduce the

species where we assumed it had occurred not long

before. One day before releasing a wild-caught

social group of 8 S. bicolor, we found them all

bitten to death inside the cage that was fenced with

galvanized small-meshed wire. The only animal left

alive in the cage was a wild adult *S. midos that

apparently had not found back the little hole in the

wire through which he and some other family mem-

bers had entered the cage that very morning. On the

other hand, a hand-tame S. lfliddS infant that we

raised free around the compound at the time, one

day was ‘kidnapped’ and adopted by the wild S.

midas group that roam ed around in the project area.

Within the True (Atlantic Forest) Marmosets or

Ouistitis genus Ccillithrix we distinguish two

monophyletic Clades: the Cd. penicillcitCl C lade and

the Cd. OliritO Clade (Fig. 16). Within the first

m onophyletic Clade w e consider Co. penicilloto the

nearest to archetypic, most saturated eumelanin

taxon that occupies the largest distribution (dark

green area). From there, it radiated in northern

direction and diverged into the overall progressively

bleached taxon Co. jocchus that has fully albinotic

ear-tufts. In eastern direction, from it derived and

radiated away the taxa Co. kuhlU and Co. geojfroyi

that are progressively bleached euchromic to al-

binotic in their mantle and head parts (except the

black ear-tufts). Their dead-end distributions are

pressed against the A tlan tic coast. Interestingly, Co.

kuhlifs range fully overlaps with that of LeOUtO-

pithecus chrysomelos. The Co. aurita Clade has Co.

aurita representing the nearest to archetypic, overall

metachromic agouti taxon that ranges allopatric

with the lion tamarins ( LeOUtopitheCUS ) in the

Atlantic forest of SE Brazil. From there derived the

near albinotic taxon Co. floviceps that occupies a

small area in SE Minas Gerais, allopatric with Co.

geojfroyi (M itterm eier et al., 2013).

As for the Lion Tamarin genus LeontopitheCUS,

we consider the overall saturated eumelanin, almost

all-black taxon L. chrySOpygUS the nearest to ar-

chetypic lion tamarin. From it derived in southeast-

ern direction the taxon L. coissoro that followed a

metachromic pathway of pheomelanin bleaching

in its bright orange-colored dorsal parts while

maintaining the saturated eumelanin black tail,

arms, legs, mantle and head of L. chrySOpygUS. Its

small range in coastal Parana State represents the

southernmost distribution of any callitrichid. From

L. chrySOpygUS derived in northeastern direction

along a pathway of pheomelanin bleaching the two

other taxa, L. chrysomelos and L. rosalio. Leonto-

pithecus chrysomelos bleached in the orange colored

lower arms and legs, and in the light orange to

cream-white head and mantle maintaining the rest

of its body saturated eumelanin. LeontopitheCUS

WSolia, in turn, is evenly light orange-colored over

its whole body, with the tail becoming almost al-

binotic. Both taxa occupy small dead-end distribu-

tions in the Atlantic forest along the coast of SE

Brazil (Mittermeier et al., 2013).

In a further attempt to falsify the principle of

metachromic bleaching and the crucial role we

believe it plays in allopatric speciation of (at least)

Neotropical monkeys, we now will proceed to

examine currently known distributions, allopatric

speciation and radiation, and the pathways of

metachromic bleaching supposedly followed in all

other male-territorial Neotropical monkey genera

(i.e., Callicebus, Saimiri, Cacojao , Chiropotes,

Pithecia, Lagothrix, Ateles , Brachyteles, Alouatta,

Cebus, Sapajus, and Aotus).

Titi M onkeys of the genus Callicebus are strongly

territorial in behavior, a family marking its territory

vocally - a pair calling in duet, or a whole family

calling in chorus. In the Amazon, a single taxon of

the Collared Titi Col. torquOtUS Group may occur

in sympatry with a single titi of any of the other

Non-collared Titi cladistic Groups, once the former

titis are only found high up in the canopy of primary

terra firm e rain forest. Collared titis occupy a

different, more frugivorous feeding niche than the

titis that lack the white collar. The latter prefer the

On the origin of allopatric primate species

135

lower strata and edges of terra firm e rain forest,

secondary growth, and savanna forest, being overall

more omnivorous in their diet that contains also

young leaves and insects, in addition to pulpy fruits

(H ershkovitz, 1988; Hershkovitz, 1 990; M itter-

m eier et al., 2013).

In figures 17-20, we show the distributions of

all known Titi Monkeys genus CallicebuS. Within

the titi monkeys five phylogenetic cladistic Groups

or C lades are recognized: Ceil. peVSOnatUS (south-

eastern Brazilian taxa), Cal. torquatUS { Amazonian

collared taxa), Cal. moloch. Cal. ClipreUS and Cal.

donacophilus (Amazonian non-collared taxa) (Van

Roosmalen et al., 2002). Within each titi Clade the

irreversible pathway of metachromic bleaching

towards partly or fully albinotic, from saturated

eumelanin and saturated pheomelanin fields to

white or colorless, is clearly demonstrated. The

farther radiated away from the prototypic agouti or

saturated eumelanin (black or dark brown) taxon -

Cal. melanochir in the Cal. personatus G ro u p , Cal.

medemi in the Cal. torquatus Group, Cal. cineras-

cens in the Cal. moloch Group, Cal. brunneus in the

Cal. cupreus Group, and Cal. modestus in the Cal.

donacophilus G roup - the more its pelage turns into

orange, yellowish or cream to white, first in certain

parts of the body, and eventually all over its coat.

N ear-albinotic forms in dead-end distributions (e.g.,

Cal. pallescens, Rio Xingu titi, Rio Mam uni titi)

are doomed to eventually go extinct, as meta-

chromism with the trend to allopatry as the driving

behavioral factor is an irreversible, initially seem-

ingly non - adaptive evolutionary pattern in all

territorial monkeys. As shown in the maps, in the

Amazon all distributions of titis without a white

collar are occupied by just a single taxon and are

delineated by rivers that function as (for titis that

cannot swim) strong geographic barriers. Narrow

contact zones between adjacent interfluvial distribu-

tions surely do exist, usually near the headwaters, but

nowhere interbreeding or hybridization between the

two neighboring taxa has been reported to take place.

Our extensive primate surveys carried out

throughout the entire Amazon Basin have revealed

that, in general, a given monkey taxon looks

phenoty pically identical throughout its entire range.

In contact zones or across opposite banks of rivers

that dem ographically separate two phy logenetically

related taxa, we have noticed interspecific boundary

conflicts and vocal battles to occur regularly, in

particular performed by social groupings of titis,

howling monkeys and spider monkeys. In at least

one contact zone between two differently looking

titis we have been able to perceive the ‘trend to

allopatry’ put in motion in metachromic bleached

individuals that were deviant from the commonly

seen phenotype. At the far northeastern corner of

the distribution of Hoffmann’s Titi Monkey Cal.

hoffmannsi a small founder-population of an al-

binotic all-cream w hite form, that we provisionally

named the “Rio Mamuru titi”, apparently has been

pushed into a dead-end distribution between the

right bank of the lower Rio Mamuru, the for titis

inhospitable varzeas (seasonally white-water inund-

ated floodplain forest) along the right bank of

the Rio Amazonas, and the parapatric distribution

of Cal. hoffmannsi to the east and south as far as

the lower Rio Tapajos (Fig. 17). Only mtDNA se-

quences may determine what taxonomic status we

should allocate to this new, fully euchromic taxon:

‘color morph’ or ‘taxon in the making’. A color

m orph of Cal. hoffmannsi, a subspecies to be nam ed

Cal. hoffmannsi mamuruensis, or a valid new

species to be described as Cal. mamuruensisl As

mentioned before, here our ecospecies concept

could be applied in case the population has been

confirmed to be allopatric and genetically isolated

(not allowing any gene flow) from the taxon it

derived from, or when the enclave population has

successfully adapted to a different ecological niche

- in this case turning itself into a varzea versus terra

firm e rainforest habitat specialist. Our ecospecies

concept (hereafter named ESC) in combination with

the phylogenetic species concept (PSC) is, at least

in the field, more practical, less arbitrary, and better

defined, in particular when used for the purpose of

species and biodiversity conservation. The ESC

would put an end to the academic discussion about

the arbitrary and controversial subspecies/race

concept.

As Groves (2001a; 2001b; 2004; 2005) points

out: “ There is no official taxonomy ” .The numerous

concepts as to what is and what is not a species are

controversial, and every named species is itself

nothing more than a hypothesis. Our understanding

of the systematics of the primates is constantly

growing, not only through the discovery of new

species but also with new information brought to

bear from diverse fields such as morphology, cyto-

genetics, molecular genetics, paleontology, biogeo-

136

Marc G.M. van Roosmalen & Tomas van Roosmalen

AMAZONIAN NON-COLLARED T1TI MONKEYS

CALLICEBUS

Callicebus moloch Clade

C. cinerascens C. baptista C hoffmannsi

C. moloch &C. vieiraiwC. bernhardi

Callicebus cupreus Clade

C, brunneus C. cupreus%C. caquetensis

C caligaius € C- siephennashi C. aureipalatii

dubius C. dlscolorGC. ornatus

Callicebus donacophilus Clade

C. modesws C. ollalaeM C. donacophilus

C. sp nov. Chiquiianos

oenanthe

Chitjuiianen Titi Rit> Paraguay

Caiiic<ft>ut $p. /tov.

Figure 17. Distributions, allopatric speciation, radiation and supposed pathways of metachromic

bleaching in all known Amazonian N on-collared Titi Monkeys genus Callicebus.

graphy, physiology and behaviour - contributing

to test the hypothesis that a certain organism is a

species distinct from another. Distinct in what

sense? An individual is distinct, a population is

distinct, but when and in what way is it a distinct

species?

Among the Titi Monkeys of the Cal. TTloloch

cladistic Group (Fig. 17), the all-agouti dark-tailed

taxon Cal. cinerascens, ranging along the east bank

of the Rio Aripuana and between the right bank of

the lower Rio Madeira and the left bank of the

Rio Canuma, seems to represent the nearest to ar-

chetypic, most original or ancestral titi from which

all other tax a of the Cal. moloch Group have

derived. Phy logeographically, the current central-

southern Amazonian distribution of Cal. dneras-

CenS is thought to represent the center of dispersion

of the Cal. moloch Clade. In other words, the upper

Aripuana region in Rondonia may be considered the

cradle of Cal. moloch C lade’s evolution and disper-

sion. From there, all taxa of the Cal. moloch Clade

have diverged, radiating away in all (but southern)

directions. A distinct metachromic trend to saturated

pheomelanin (orange beard and sideburns) and al-

binotic (cream to white beard, sideburns, tail and/or

whole body) can be seen, which means that the

most progressively bleached taxa that demograph-

ically radiated the farthest away from the arche-

type’s origin of dispersion tend to euchromic or

albinotic (i.e.. Cal. moloch east of the Rio Tapajos,

and Cal. hoffmannsi in the northernmost dead-

end distribution delineated by the un traversable

Amazon and Tapajos Rivers). The supposed meta-

chromic pathway taken is as follows: Cal. dneras-

CenS radiated first in northern direction, some

founder-colony traversed the Parana do Uraria,

followed the pheomelanin pathway, and diverged

On the origin of allopatric primate species

137

COLLARED Till MONKEYS

CALLICEBUS TORQUATUS CLADE

Callicebus torquaws Subclade

#C. r. torquaws C. t. purinus C. r. regulus

Caflicebus luge ns Sub clade

Figure 18. Distributions, allopatric speciation. radiation and supposed pathways of metachromic bleaching in all known

Amazonian Collared Titi Monkeys of the Callicebus tOVquatUS Clade with two sub-C lades: Cal. tOVquatUS and Cal. lugetlS.

into taxon Cal. baptista (which has dark orange-

colored beard, sideburns, lower extremities, and

belly). Radiating eastwards, it diverged into Cal.

hoffinannsi (its forehead, beard, sideburns, hands,

feet, and belly bleached light gray to cream -w hite).

After Cal. hoffinannsi happens, A to traverse the Rio

Tapajos, most likely where it is called Rio Juruena,

it diverged into the advanced pheomelanin bleached

to albinotic taxon Cal. moloch that now occupies a

large distribution east of the Rio Tapajos and south

of the Amazon River. Callicebus hoffinannsi also

diverged along the upper course of the Rio Tapajos

into the recently described taxon Cal. vieirai (ran-

ging between the Rios Juruena and Teles Pires),

which is near-albinotic.

When a taxon is occupying a given interfluvial

distribution delineated by hard to traverse river

barriers, it has irreversibly changed its pelage or

parts of its coat (e.g., beard, sideburns, ear-tufts,

forehead, tail, hands, feet) following the eumelanin

pathway from agouti or saturated eumelanin to al-

binotic (cream or white), via black, brown, drab,

and gray, and/or the pheomelanin pathway via red,

orange, and yellow, or a combination of the two

pathways in different parts of the body or coat.

The trend to albinotic in the Cal. vnoloch Clade is

completed near its northernmost dead-end distribu-

tion in the all-cream to white new form that we

happened to identify along the right bank of the Rio

Mamuru (Fig. 21). It must have derived from dark-

tailed but cream -bearded and -bellied Cal. hoff-

mannsi. Following the trend to allopatry, this color

morph (or ecospecies or ‘taxon in the making’?) is

pushed with the back against the varzeas (white-

water floodplain forests) and right bank of the

untraversable Rio Amazonas. Callicebus moloch

Clade’s westernmost distribution is represented by

the advanced pheomelanin bleached (bright orange

138

Marc G.M. van Roosmalen & Tomas van Roosmalen

belly, beard and sideburns) to albinotic (white fore-

head, hands, feet and tail tip) taxon Cal. bemhardi

which, in turn, is pushed with the back against the

also u ntraversable Madeira River.

Among the Titi Monkeys of the Cal. ClipreUS

cladistic Group (Fig. 22), we consider Cal. brutl-

neilS the nearest to archetypic taxon. Centrally dis-

tributed, the overall agouti colored taxon Cal.

brUYUlCUS radiated in northwestern direction via the

progressively pheomelanin bleached taxa Cal. du-

biliS and Cal. discolor into the most pheomelanin

bleached (light orange tail base, beard, sideburns,

belly and inner limbs) to albinotic (snowwhite tail,

hands, feet and front/blaze) white-fronted taxon

Cal. OmatUS that is distributed north of the Amazon

in the Colombian Amazon. From Cal. brUYlYieiiS

southwards diverged the advanced pheomelanin

bleached taxon Cal. aureipalatii in the Clade’s

Titi Monkeys

genus CaUicebus

Schematic Map of the Distribution

of the eastern Brazilian taxa

CaUicebus personatus Clade

ATLANTIC OCEAN

Figure 19. Schematic map of the d istribu tion s of the SE Brazilian or Atlantic Forest Titi Monkeys of the

CaUicebus personatus Clade, which are separated by (for these taxa) untraversable rivers.

On the origin of allopatric primate species

139

Figure 20. Distributions, allopatric speciation, radiation and supposed pathways of metachromic bleaching in

all known SE Brazilian or Atlantic Forest Titi M onkeys of the Ctllliccbus pCTSOnCltUS Clade .

southernmost distribution (the Bolivian Amazon

between the Rios M adre de Dios and Beni). From

Cal. brunneus radiated away in northern direction

first the slightly pheomelanin bleached taxon

Cal. CUpreuS that now occupies a large interfluvial

area west of the Rio Purus and south of the Rio

S olim oes.Afteran ancestral founder-colony of Cal.

CUpreUS managed to traverse the Rio Purus to the

east, it diverged into the advanced pheomelanin

bleached all-orange, but white-tailed taxa Cal. Ca-

ligatus and Cal. stephennashi in the north eas tern -

most dead-end part of Cal. CUpreUS Group’s

distribution, as the Rio Madeira represents the

second strongest riverine barrier on the South-

American continent. Last but not least, also from

Cal. CUpreuS derived in northwestern direction the

recently described, advanced pheomelanin bleached

taxon Cal. caquetensis that at present occupies

a small, not yet fully identified area north of the

Amazon and Caqueta Rivers in the Colombian

lowland Amazon, allopatric with and south of the

distribution of the white-fronted titi Cal. OTUatUS

(Fig. 17).

Among the Titi Monkeys of the Cal. donaCO-

philuS cladistic Group (Fig. 17), we consider the

overall agouti-colored taxon Cal. modestUS the

most original, nearest to archetypic taxon. It occu-

pies the Clade’s northernmost distribution deline-

ated by the Rios Beni and Mamore. It radiated

southwards into the slightly pheomelanin bleached

orange-brown taxon ollalae. Following a eumelanin

bleaching pathway. Cal. modestUS also radiated in

southeastern direction, first into the near-albinotic

taxon Cal. donacophilus, and from there into the

fully albinotic taxon Cal. pallescens. The latter

nowadays occupies the southernmost dead-end

140

Marc G.M. van Roosmalen & Tomas van Roosmalen

Figure 21. Distributions of CallicebllS baptista, Ca. Ho ffniCUVlS /, and the “Rio Mamuru titi” - the latter perhaps to be con-

sidered a new taxon or one ‘in the making’. This satellite image shows the location of an enclave population of fully albinotic

titi monkeys that we have found to exist along the right bank of the Rio M amuru. This p op ulatio n is on the verge of extinction

as it is pushed with the back against for titis inhospitable habitat - the seasonally inundated floodplain forest (varzea) along

the Rio Amazonas and the outskirts of the rapidly expanding town of Pari n tins in the north, and lands occupied by Ca. hoff-

mannsi stretching to the east as far as the Rio Tapajos. The species Ca. baptista belonging to the Ca. moloch C lade originally

ranged only north of Parana do Canuma, P. do U raria and P. do Ramos, east of the lower Rio Madeira, south of the Rio

Amazonas and west of the Parana do Ramos. South of this narrow distribution evolved the species Ca. hofftnannsi, which

occupies a large distribution between Rio Canuma in the west, Rio Tapajos in the east, and Rio Amazonas in the north, east

of Parana do Ramos and Rio Mamuru. Baptist's Titi is much more color ful being dark to bright red on the ventral parts and

lower limbs, having a red beard and red sideburns, whereas the rest of its body is grayish to blackish agouti. Hoffmann’s

Titi is basically two-colored grayish and y ello w ish - w h ite to almost white, its sideburns and beard being light cream-white.

H owever, we spotted the Ca. baptista titis also along the west bank of the Rio Uira-Curupa, hence it once must have tra-

versed the Parana do Ramos west of the town of Parintin s, form ing an enclave population there after it displaced Hoffmann’s

titis from the interfluve delineated by the lower Rio Uira-Curupa and Rio Andira. We also spotted advanced metachromic

bleached, near-albinotic, pale yellowish to all-white ‘color morphs’ being phenotypically most related to Ca. hofftnannsi

along the Rio Mamuru, the next river to the east, and classic yellowish- white and gray Ca. hoffmannsi with black tails

along both banks of the middle and upper Rio Andira. These observations may confirm a case of what is called parapatry.

The tw o valid species Ca. hofftnannsi and Ca. baptista that are allopatric for the greater part of their distributions - phy lo-

geographically separated from one anotherby un traversable wa ter bodies - exclude one another where Ca. baptista happened

to traverse a riverine barrier and subsequently replaced the local Ca.hofftnatinsi population. There, both taxa live parapatric,

meaning in adjacent ‘patrias’ not separated by geographic barriers, where gene flow in theory is possible, but in reality does

not occur. A plausible explanation would be that the two taxa have already diverged too far from one another. One could

only speculate about the future of the fully albinotic form seen along the right bank of the Rio Mamuru. It may rep re sent a

founder-colony or population of metachromic progressively bleached individuals that have been driven into parapatry by

the Ca. hofftnannsi populations found to the east and south of R io M am uru as far as the R io Tapajos. The Rio Mamuru titis

eventually might go extinct, unless they manage to adapt to (for titis) inappropriate habitat - the extensive varzeas along the

right bank of the Rio Amazonas. If the founder-colony, following the trend to allopatry, would successfully adapt to the

ecological niche of varzea, then a new taxon could derive from Ca. hofftnannsi. Through inbreeding, the currently adopted

euchromic coat coloration would stabilize phenotypically across the entire population of that new taxon in a relatively short

period of time. The hypothetical evolutionary path would then go from a metachromic fully bleached, near-albinotic color

morph in a dead-end distribution to a new taxon belonging to the monophyletic Ca. moloch C lade . In that case, we would

have to name the Rio Mamuru Titi Monkey Ca. tnattUlVUensis.

On the origin of allopatric primate species

141

distribution of the Cal. donaCOphilus Clad e , penet-

rating far into the arid Chaco of Paraguay and the

pampas ofArgentina.A new species of titi, recently

collected by the Brazilian ornithologist Marcelo

Vasconcellos in the Chiquitanos area along the Rio

Paraguay in the Pantanal of Mato Grosso do Sul

(for which taxon we identified the holotype in the

zoological collection of the AMNH, in 1977 collec-

ted by George Schaller and m isidentified as Cal.

donaCOphilus) , represents the easternmost distrib-

uted taxon of the Cal. donaCOphilus C lade . Except

for its dark gray ears (white in Cal. donaCOphilus),

the Chiquitanos titi is overall more pheomelanin

bleached towards albinotic than Cal. donaCOphilus ,

but less so compared to Cal. pallescens. Further-

more, from Cal. modestUS derived in northwestern

direction the advanced pheomelanin bleached near-

albinotic taxon Cal. Oenanthe that is nowadays

found isolated in a small area in the east-Peru vian

Amazon, south of the Rio Maranon.

Among the Collared Titis of the Cal. torquatUS

cladistic Group (Fig. 18), we consider the saturated

eumelanin black-handed taxon Cal. medemi w ith

the westernmost distribution north of the Amazon

River the nearest to archetypic form from which

derived the all-black but yellow -handed titi from

the southbank of the Rio Negro - a newly identified,

as yet to be described taxon - and from that taxon

derived the all-black, dorsally slightly reddish-

tinged taxon Cal. lugenS with the northernmost

distribution of the Cal. lugeYlS sub-Clade. From

archetypic Cal. medemi south of the Rio Caqueta

derived, first in eastern direction the dorsally pheo-

melanin bleached taxon Cal. lucifer. Some ancestral

founder-colony of the new Rio Negro southbank

species then must have managed to traverse the

lower Rio Solimoes somewhere between the mouth

of the Rio Purus and that of the Rio Madeira. From

there, collared titis could radiate away back in

western direction, though south of the Amazon

River, into the further pheomelanin bleached,

overall reddish-brown colored white-handed taxa

Cal. torquatus and Cal. purinus , and, after tra-

versing the Rio Jurua, into the advanced pheo-

melanin bleached red-handed red-fronted taxon

Cal. regulus.

Within the SE Brazilian Titi Monkeys of the

Cal. personatUS C lade (Figs. 19-20) the nearest to

archetypic, most saturated eumelanin taxon is Ca.

melanochir. It ranges along the Atlantic coast south

of the Rio Paraguagu in the center of dispersion of

the personatus Clade. From Cal. melanochir de-

rived in northern direction along the pheomelanin

pathway the advanced pheomelanin bleached (all-

orange colored) taxon Cal. barbarabrownae, and,

in a small dead-end distribution delineated by the

untraversable lower Rio Sao Francisco in the north

and the Atlantic Ocean in the east derived the

almost fully bleached, near-albinotic taxon Cal.

COimbrai. Radiating in southern direction, ancestral

Cal. melanochir diverged along the eumelanin

pathway into the orange-tailed, but overall dark

brown-colored taxon Cal. nigvifrons , and along the

pheomelanin pathway into the advanced pheo-

melanin bleached, all-orange colored and near-al-

binotic taxon Cal. personatus.

Within the Squirrel Monkeys genus Saimiri

(Fig. 22), we phylogeographically distinguish two

monophyletic Clades: Sa. SCiureus - including the

C entral-A m erican Sa. oerstedii sub-Clade - and Sa.

boliviensis - including the Bare - ear Sa. UStUS sub-

Clade (H ershkovitz, 1 984). It is inferred that the

genus Saimiri evolved relatively recently, with

crown lineages diverging as late as the Pleistocene

(ca. 1.5 MYA) and other major Clades diverging

between 0. 9-1.1 MYA. Concurring with Chiou et

al. (2011), we include Sa. Oerstedii in the mono-

phyletic Sa. SciureUS Clade that originated in the

Guianas. North of the Amazon, it radiated in west-

ern direction and diverged first into Sa. Cassiquiar-

ensis, a taxon that is nowadays distributed across

the entire Rio Negro basin, its distribution in the

south delineated by the Rio Japura/C aqueta and the

lower Rio Solimoes. From Sa. Cassiquiarensis di-

verged in northern direction the advanced bleached,

least colorful taxon Sa. albigena that ranges allo-

patric (north of the Rio Guaviare) in the southwest-

ernmost part of the Rio Orinoco basin. In

concurrence with Chiou et al. (2011), who found

evidence for monophyly in the Sa. SciureUS and Sa.

oerstedii Groups, we suggest that from Sa. albigena

or some ancestral precursor of it derived and radi-

ated away in northwestern direction the advanced

pheomelanin bleached taxa Sa. oerstedii and Sa.

citrinellus. These now range in Sa. SciureUS C lade’s

disjunct northw esternm ost dead-end distribution -

along the Pacific coast of Panama and Costa Rica.

Along a different metachromic pathway derived

from Sa. Cassiquiarensis in southern direction the

advanced bleached taxon Sa. macrodon. Its distri-

142

Marc G.M. van Roosmalen & Tomas van Roosmalen

bution is delineated by the Rios Guaviare and Apa-

poris in Colombia, and the Rio Japura in Brazil, and

south of the Amazon by the upper Rio Maranon in

the west, and the Rio Jurua in the east. Within its

large distribution, Sd. IflClCwdon is excluded from

the Rios H uallaga/U cay ali interfluve in the Per-

uvian Amazon that is occupied by Sd. pevuviensis.

In the Guianas, Sd. SCiureiiS once managed to tra-

verse the lower Amazon River to the south. As it is

a riverbank marsh and mangrove forest specialist,

Sd. SCiureiiS must have colonized the south bank of

the Amazon after reaching it on floating islands

covered with varzea or mangrove vegetation. From

Sd. SCiureuS south of the Amazon subsequently de-

rived the recently described, advanced bleached

near-albinotic taxon Sd. COllillsi that is confined to

M arajo Island - the Sd. SCiureuS Clade’s eastern-

most dead-end distribution delineated by the At-

lantic Ocean, and the Amazon and Para Rivers.

The second monophyletic Clade of Squirrel

Monkeys, the Sd. boliviensis Clade, has origin-

ated in the extensive white-water floodplain forest

(varzea) near the confluence of the Japura and

Solimoes Rivers. The lower Japura/Solim oes inter-

fluve does not contain any terra firme. It is season-

ally flooded over 6-8 months. Here lives the nearest

to archetypic, saturated eumelanin taxon of the Sd.

boliviensis Clade, Sa.vanzolinii. It is overall agouti

and black colored, representing the only extant

squirrel monkey with an all-black tail. A somewhat

bleached Sd. vanzolinH founder-colony once must

have reached (swimming or on a floating varzea is-

land) the south bank of the Rio Solimoes east of its

confluence with the Rio Jurua. There evolved from

it the somewhat pheomelanin bleached, orange to

yellowish taxon Sd. boliviensis. It then occupied

east of the Rio Jurua the entire area delineated

by the lower Purus, upper Madeira and Guapore

S .

S. coliins

SAIMIRI

Saimiri sciureus Clade

S sciureus S, cassiquiarensis

#S, afbigena&S. macrodon

Saimiri oersted// Clade

oersredii eitrinellus

Saimiri boliviensis Clade

^ S. vanzoiinii #S. boliviensis

peruviensis S. usws

Figure 22. Distributions, allopatric speciation, radiation and supposed pathways of nietachromic bleaching

in all known Squirrel Monkeys genus Saimiri divided up in the S. SCiureUS and S. boliviensis C lad e .

On the origin of allopatric primate species

143

Rivers, whereas in the south it extended its range

far into the Peruvian and Bolivian Amazon. After a

founder-colony of somewhat bleached Set. bolivien-

sis happened to traverse the easternmost river bar-

rier, it diverged into Sa. UStUS - the least colorful,

most eumelanin bleached taxon of the Sa. bolivien-

sis C lade. Its distribution is confined by the Amazon

River in the north, the Rio Xingu in the east (sep-

arating the distributions of Sa. UStUS and Sa.

SciureilS) , and the Rio Guapore in the south. Fur-

thermore, from boliviensis in its southw esternm ost

distribution in the Peruvian Amazon derived the

progressively pheomelanin bleached near-albinotic,

most colorful taxon Sa. peruviensis. It occupies a

dead-end distribution - the interfluve delineated by

the Rios Huallaga and Ucayal i - as it is surrounded

by Sa. macrodon occupied territory.

Historically followed metachromic and phylo-

geographic pathways, intraspecifically pushed

ahead by the trend to allopatry and the principle of

metachromic bleaching, within a genus or mono-

phyletic Group of primates may be traced back

most expressively, when we examine the distribu-

tions, speciation and radiation of all extant Uakari

Monkeys genus CacajaO (Figs. 23, 24). This ex-

clusively Amazonian genus contains two mono-

phyletic Groups or Clades: the Black-headed

Uakaris of the Cac. melanocephalus G roup , and the

Bald-headed Uakaris of the Cac. Calvus Group

(H ershkovitz, 1 987a). Among Uakaris, the sup-

posedly nearest to archetypic (prototypic) ancestral

form is represented by the extant Black-headed

Uakaris, more in particular by the saturated eu-

melanin, all-black taxon Cac. ayresi - the north-

easternmost distributed among all Uakaris.

Uakaris are the only monkeys in the Neotropics

that lost a functional tail. All other genera evolved

either a long pendulous, short-hairy to bushy tail

that is in the first place designed to use for balance

while moving through the tree tops; or, a long pre-

hensile tail that is used as a fifth limb during vertical

climbing and walking on top of or brachiating un-

derneath twigs and thin branches in the periphery

of tree tops (where the fruits are hanging). Only

after observing Black-headed Uakaris Cac. hosomi

in the wild along the Rio Cauaburi and in Pico da

Neblina National Park, we came to understand why

the region drained by the Rio Negro has to be con-

sidered the center of dispersion for all uakaris,

in other words the cradle of evolution of the genus

CacajaO. Simultaneously, we came to understand

the very reason why uakaris have lost a functional

tail, whereas in all other canopy-dwelling monkeys

from the Amazon it seems to be a fifth limb of vital

im portance.

Across the entire upper Rio Negro basin the type

of vegetation that dominates the landscape is a very

impoverished sort of thin-stemmed savanna forest.

It stands on poorly drained, highly acidic white-

sand soils that are deposited on top of an imper-

meable, several meters thick layer of coarse

rounded pebbles. This type of forest is called

“caatinga-do-Rio-Negro”, for it resembles much the

arid dry seasonally deciduous vegetation in large

parts of the Brazilian northeast. It seasonally floods

during the long rainy season, but also throughout

the year on a daily base during heavy rainstorms.

Phy siognom ically, this forest type resembles two-

storey mangrove forest, as most of its trees use

pneum atophores (aerial roots) and stilt-roots to

cope with frequent flooding conditions. Phytoso-

ciologically, the ‘caatinga-do-Rio-Negro’ is dom-

inated by trees belonging to families like

Euphorbiaceae and Apocynaceae, known for their

often toxic latex and plant parts, most in particular

full-grown seeds. Surprisingly, this forest lacks

hem i-epiphy tic climbing shrubs, vines, and twiners.

Over geological times Black-headed uakaris seem

to have co-evolved with this natural environment

through specializing themselves in the depredation

of immature seeds. From early maturation on, the

seeds are often loaded with toxic alkaloids and

secondary compounds. Uakaris have guts that are

specially adapted to neutralize these toxins. Their

canines are oversized and wedge-shaped with

razorblade sharp edges, as such adapted to open up

the toughest-husked fruits and kernels (endocarps)

around. Their incisors are procumbent and used to

scoop out the seed content (endosperm) from any

endocarp or pericarp. Uakaris are full-fashioned

seed predators to such length that, if one offers a

uakari a juicy pear or apple, the monkey will in-

stantly bite the pulpy pome in half with its powerful

canines. Then, it will pick the tiny seeds from the

central part, discard the pulp, and delicately split

the tiny seeds one by one with their canines. In the

end, it has its procumbent incisors scoop out the en-

dosperm from the seed coat. Black-headed uakaris

do occupy very large home ranges. They restlessly

travel or forage in very large multi-male dominated

144

Marc G.M. van Roosmalen & Tomas van Roosmalen

social groups that may contain over two-hundred

monkeys. Since their preferred habitat ‘caatinga-

do-Rio-N egro’ basically lacks climbing shrubs, the

tree tops are not interlinked by vines, twiners and

climbing hem i-epiphytes as they are in primary

terra firme rain forest elsewhere in the Amazon. By

lack of a walkway through the tree tops, Black-

headed uakaris co-evolutionarily have adapted

to this ancient impoverished, physiognom ically

discontinuous and frequently inundated forest type

by developing the locomotor pattern of so-called

‘vertical clinging and leaping’. A traveling or for-

aging troop of Black-headed uakaris much re-

sembles Madagascar indris, Indri indri (Gmelin,

1788) that also make enormous leaps, catapulting

themselves for - and upwards by means of their

strong muscular upper legs. Like indris in Mada-

gascar, black-headed uakaris lost most of a func-

tional tail while adapting to this type of locomotion.

The few cm long tail provided with a tuft is only

used for intragroup communication. Black-headed

uakaris can curl it upwards and wave it sideways

like dogs would do with a largely amputated tail.

Black-headed uakaris of the species Cac. ho-

SOtfli and CdC. Ciyresi , distributed north of the Rio

Negro, east of the Cassiquiare and west of the Rio

Demeni, and Cac. melanOCephaluS from south of

the Rio Orinoco, west of the Cassiquiare and north

of the lower Rio Solimoes and Rio Japura /Rio

Caqueta, have a pitch-black face, a black, forward

directed hair-tuft on the forehead, and a short black-

ish, red or orange-tinged tail. Black-headed uakaris

from the Rio Iqana basin, being distributed in -

between the upper Rio Orinoco and the lower Rio

Uaupes, show a black upper back and pheomelanin

bleached, orange to blond bleached lower back.

Perhaps, for that reason they should be taxonom-

ically treated as a valid species (we here suggest

Cac. ouakary).

The Bald-headed Uakaris of the Cac. calvus

cladistic Group, which range south of the Amazon/

Solimoes and Japura Rivers, have a bald head,

bright-red bare face, blue-gray eyes, a shaggy pheo-

melanin bleached, near-alb inotic coat, and a rudi-

mentary tail that is shorter and even less functional

than the tailofBlack-headed U akaris (Figs. 23, 24).

The Cac. CalvUS Group contains five taxa which

according to our phylogenetic ecospecies concept

(ESC) should be all given valid species status: 1)

CaC. CalvUS living exclusively in the white-water

floodplain forests (varzeas) between the lower

Japura and Solimoes Rivers, being cream-white

with pheomelanin bleached, orange-brown ventral

parts; 2) Cac. UOVaesi occuring in disjunct pockets

along both banks of the lower and middle Rio Jurua

as far upstream as its confluence with the Rio Ta-

rauaca, its coat being pheomelanin bleached, orange

brown-colored, but albinotic from the back of the

head to mid-dorsum; 3) Cac. rubicundus, the pheo-

melanin bleached, bright orange-colored (except for

the albinotic cream-white back of the head and

neck) bald-headed Cac. uakaris that occurs in the

white-water floodplain forests (varzeas) along the

left bank of the upper Rio Solimoes in the central-

westernmost Brazilian Amazon; 4) Cac. UCayalU,

its coat overall saturated pheomelanin, dark

brown to orangish colored, ranging in the Peruvian

Amazon along the right bank of the Ucayali River

in the white-water inundated floodplain forest

(varzea) as well as adjacent terra firme rain forest;

5) a form newly identified by us in the year 2000,

its coat near-albinotic, advanced euchromic

bleached to all-white. We provisionally name this

new taxon the “Rio Pauini Bald-headed Uakari”

CacajaO sp., for it is only found in the varzeas along

the upper Rio Pauini, a left-bank tributary of the Rio

Purus (Figs. 23, 24).

The 1 trend to allopatry in metachromic varieties

of sociable, but territorial primates' applies to the

evolutionary path along which a certain primate

race, species, monophyletic clade, or genus has ex-

tended its geographic range in the geological past.

As a founder - colony or - population at the outer

limit of a taxon’s current range represents an ex-

tremely narrow gene pool, through inbreeding

certain phenotypic characters like partial depilation

of the skin, or skin/coat coloration will be rein-

forced in the beginning and therefore advance more

rapidly.

Through the process of metachromism (= evol-

utionary change in tegumentary or hair/skin color-

ation), with the ‘trend to allopatry’ in metachromic

bleached individuals as the principal behavioral

driving force, speciation, radiation, and phylogeo-

graphy can be plausibly retraced and explained for

in all extant N eotropical prim ates. A ccording to the

principle of metachromic bleaching, primate taxa at

the base of a phylogenetic tree or clade being the

nearest to archetypic, prototypic, primitive, or ori-

ginal, in general are agouti or saturated eumelanin,

On the origin of allopatric primate species

145

UAKARIS

CACAJAO

Schematic Map of the Distribution of

melanocephalus and calvus C lades

Orinoco

Cassiqulare

Dcmoni

Pheomelanln pathway

Caquotd

Uaupcs

Branco

Amazonas

Soiimdes

Madeira

Jurutf

Maranon

Pauini

Javan'

Pheometanin to albino

Ucayali

UAKARIS

Cacajao melanocephaius Glade

C. ay rest

C.hosomi

"|-C, melanocephaius

Cacajao calvus Glade

0C. uc ay alii

^C. rubicundus

C, calvus

C. novaesi

kC. sp. nov. Rio Pauinf

i £2^3^

\ \ V ^

ury>

-(jr

i w

Figure 23. Schematic map of the distributions of U akari Monkeys of the CaCCljaO inelcilWCephciluS and C. CCllvUS C lades

div ided up by (for them ) un traversable rivers . F igure 24 . D istribu tion s, allopatric speciation. rad iation and supposed pa th ways

of metachromic bleaching in all known Uakari Monkeys genus Co.CO.jciO.

146

Marc G.M. van Roosmalen & Tomas van Roosmalen

which means the least colorful, agouti, black, or

dark brown colored. Among Uakari Monkeys genus

Cacajao, the origin or center of dispersion is sup-

posed to be located in the northeasternm ost part

of the Brazilian Amazon, south of the watershed

between the Rio Negro and Rio Orinoco basins, an

area delineated by the Rios Demeni and Araca

(Figs. 23, 24; Fig. 27). Within this interfluve

the landscape is dominated by ‘c aating a-do -R io -

Negro’, the most impoverished habitat type ima-

ginable, but preferred by uakaris of the CciC. melci-

nocephalus Clade. Here lives the saturated eu-

melanin, least bleached taxon of the Black-headed

Uakaris, the recently described CciC. ayresi (B oubli

et al., 2008). Its coat is all-black and dark-brown

colored. It may well represent the proto- or ar-

chetypic uakari from which all other uakaris have

derived. From CciC. ay resi in western direction first

diverged along the pheomelanin pathway taxon

CciC. hosomi. It is distributed between the Rio

Marauia, the upper Rio Negro, and the Cassiquiare

Channel (we have confirmed its presence in Pico da

Neblina National Park and along both banks of the

Rio Cauaburi). After an ancestral founder-colony

traversed the Rio Cassiquiare - the channel that

connects the Rio Negro basin with that of the Rio

Orinoco in Venezuela - CciC. IlOSOlfli diverged into

an intermediately pheomelanin bleached taxon that

differs from classic CciC. vnelciYlOCephaluS in the

black shoulders, dark-red legs and tail. If this

phenotype, which is thought to represent a color

morph of Cac. melanocephalus, turns out to occur

throughout the entire distribution delineated in the

north by the Rio Orinoco and in the south by the

Rio Uaupes, one should consider it a new taxon to

be named the “Rio Igana Black-headed Uakari”

Cac. Oliakary. After an ancestral founder- colony of

the latter managed to traverse the Rio Uaupes, it

has diverged into the progressively pheomelanin

bleached blond- backed black-headed uakari taxon

Cac. melanocephalus. Subsequently, blond-backed

Cac. melanocephalus have occupied the entire

interfluve south of the Rio Negro, eastwards as far

as Archipelago de Anavilhanas located about forty

km west of Manaus, and to the west far into the

Colombian Amazon, and south as far as the north

bank of the Rio Japura (Rio Caqueta in Colombia).

We suppose that once upon a time a founder-colony

of slightly bald-headed, advanced pheomelanin

bleached ancestral Cac. melanocephalus , being

pushed out of its westernmost dead-end distribution

in the Colombian Amazon, may have managed to

traverse the upper reaches of the Rio Caqueta. It

then could extend its range southwards, eventually

reaching the Rio M arahon (as the upper Amazon

River is called in Peru). A fo under - colony of

an advanced pheomelanin bleached, bald-headed

ancestral form must then have traversed the Rio

Ucayali. It subsequently occupied terra firm e and

varzea forests in the interfluve between the Rio

Ucayali in the west, the Rio Maranon in the north,

and the Rio Javan in the east. Nowadays, this inter-

fluve is inhabited by the bald-headed dark reddish-

brown taxon Cac. UC ay alii that belongs to the

bald-headed Cac. CalvUS C lade. D isjunct from Cac.

UCayalii's distribution and ranging farther to the east

derived taxon Cac. rubicundus , a progressively

pheomelanin bleached bright- orange colored bald-

headed uakari. It is fully adapted to varzea habitat

found in abundance along the left bank of the upper

Rio Solim oes. From Cac. rubicundus going farther

eastwards, but disjunct from its distribution, along

the same (left) bank of the S olim oes/A m azon River

the almost fully albinotic taxon Cac. CalvUS is

found. It fully adapted to white - water inundated

floodplain forest (varzea) - the only available

habitat in this for the Cac. CalvUS Clade dead-end

distribution situated inbetween the banks of the

Japura and Solimoes Rivers. Directly from Cac.

rubicundus to the south of Cac. calvus ' distribution

derived the bald-headed taxon Cac. UOVaesi that

ranges along both banks of the Rio Jurua as far

south as the confluence with the Rio Tarauaca and

Rio Envira. This taxon is near-albinotic from the

back of the head to beyond the mid-dorsum, and

progressively pheomelanin bleached light orange-

brown on the lateral and ventral parts of the body.

It ranges in the varzeas of the floodplain, but

we have also spotted large troops foraging for

immature seeds in the adjacent terra firm e rain

forest.

In 2000, we identified a fifth taxon of bald-

headed uakari, the completely white, fully al-

binotic taxon that we named “Rio Pauini Bald-

headed U akari” Cacajao sp. It lives along the south

bank of the Rio Pauini, a left-bank tributary of

the upper Rio Purus. It represents the southern-

most distributed and the farthest pheomelanin

bleached most albinotic taxon of all extant uakaris.

It lacks the pheomelanin orange-brown to orange

On the origin of allopatric primate species

147

ventral parts seen in the other near-albinotic taxa

Cac. novaesi and Cac. calvus (Figs. 23, 24).

Analyzing metachromic skin and coat characters

as linear and irreversible progressions within Neo-

tropical primate genera and their monophyletic

Clades does add substantially to the reconstruction

of bio geographic divergence events and phylo-

genetic relationships over a wide range of Neo-

tropical primate taxa, in particular those that defend

their living space or ecological (feeding) niche

through male-dominated, hierarchically organized

societies. So it does to the Bearded Sakis genus

Chiropotes (Figs. 25, 26) even if we have confirm ed

in the field that social groups of (at least) the

Guianan taxon Ch. SagulatUS do freely fuse and

fission on a regular base with neighboring social

groups. The genus Chiropotes clearly shows sexual

dimorphism in the larger, more robust males that

also grow bigger beards and frontal hair lobes on

their heads (H ershkovitz, 1 985). During foraging

and resting, a large social group of bearded sakis,

similar to woolly monkeys, consists of several

polygamous dominant males each taking care of his

‘harem’. The high-ranking males tend to stick to the

center of the foraging troop, whereas lower ranking

males with or without harems are pushed closer to

the periphery of the foraging troop. This way, adult

males do avoid confrontations, for their impress-

ively large wedge-shaped canines designed to crack

hard-husked fruits and kernels in order to get to the

seed pulp would be lethal if used in fights. But ad-

olescent, subadult, and, we assume, also behavior-

ally or pheno typically deviant individual males may

well be pushed into the periphery of the foraging

and ranging troop. More than once, we have

encountered a solitary male, or a couple of males

traveling at high speed through the canopy in an

apparently fixed direction, leaving us no means to

determine if these monkeys only temporarily had

lost contact with the troop, or if they were expelled

from the parental troop, or if they were representing

subtly deviant young males that had been forced to

leave the pack and search for new living grounds

somewhere beyond the limits of the group’s home

range. Only through long-term field studies one

would be able to obtain clear answers to this sort of

questions.

Within the Bearded Sakis genus Chiropotes

we distinguish two monophyletic Groups: the Ch.

SatanaS and the monotypic Ch. albinaSUS Group.

The Ch. SatanaS Clade consists of five taxa, among

which the nominate species Ch. SatanaS represents

the saturated eumelanin, all-black, nearest to ar-

chetypic bearded saki. Its distribution in the NE

Brazilian state of Maranhao is assumed to represent

the cradle of evolution or center of dispersion for

the genus. An equally all-black form that we re-

cently identified west of the headwaters of the Rio

Xingu (e.g., Rios Ronuro, Batovi and Vonden

Steinen) may either represent an enclave population

that became disjunct from that of Ch. SatanaS

(ranging east of the Rio Para/lower Rio Tocantins),

or a new taxon of the Ch. SCltCMClS Clade that still

has to be collected and described. From Ch. SatanaS

diverged in western direction the slightly eumelanin

bleached, overall light-brown colored taxon Ch.

Utahicki. It occupies the entire interfluve delin-

eated by the Rios A m azonas/A napu/Tocantins-

Araguaia/X ingu . An ancestral founder-colony of

somewhat pheomelanin bleached, red to orange-

brown backed Ch. Utahicki once must have man-

aged to traverse the lower Rio Amazonas, from

which then derived taxon Ch. SaglilatUS. This

species occupies the entire area north of the Amazon

River and east of the Rio Branco, including most of

the Guianas east of the Essequibo River. This taxon

is absent from most ofAmapa state, French Guiana

and also from a wide coastal belt of the Guianas. A

founder-colony of ancestral sagulatus once must

have traversed the Rio Branco and radiated in

western direction diverging into the advanced

eumelanin bleached taxon Ch. israelitCL. This

species is characterized by the albinotic (white

instead of pink) genitals and the light-grayish to

brownish coat color of the trunk. Chiropotes israel-

ita ranges west of the Rio Branco as far north as the

Rro Orinoco in Venezuela. It seems to be parapatric

with Black-headed Uakaris, as Chiropotes is a seed-

predating terra firm e rainforest specialist, and Cac.

ayvesi and Cac. hosomi are ‘caatinga-do-Rio-

N egro ’ -habitat specialists. The Rios Marauia and

Cauaburi seem to divide their distributions. O ur ex-

tensive surveys in the Rios Demeni/Araca inter-

fluve did not reveal the occurrence of Ch. israelita,

as the landscape is dominated by ‘caatinga-do-Rio-

Negro’ habitat (Figs. 26, 27).

The second monophyletic Group of Bearded

Sakis is that of monotypic Ch. albinaSUS. The Red-

nosed Bearded Saki is very different from the Ch.

SatanaS Clade, not just in metachromic sense. Its

148

Marc G.M. van Roosmalen & Tomas van Roosmalen

utahicki

10 inches

catvus

ca!vus

catvus

ucayalii

catvus

novaesi

catvus

rubundus

color form

from Icana

hosomi

ayresi

metanocephatus

Figure 25. The hitherto recognized taxa ofBearded Sakis genus Chiwpotes (above) and Uakaris

genus CciCCljciO (below ), all depicted in one plate (Courtesy of Stephen Nash).

On the origin of allopatric primate species

149

BEARDED SAKIS

CHIROPOTES

Chiropotes satanas Clade

Ch. satanas ^Ch. satanas Rio Xingu

Ch. utahicki >Ch. sagulaws

%Ch, israelita (was chiropotes)

Chiropotes aibinasus

Ch, aibinasus

Figure 26. Distributions, allopatric speciation, radiation, and supposedly followed eumelanin pathways

of metachromic bleaching in all known Bearded Sakis genus Chiropotes.

vocalizations are very different, the beard and tail

are shorter-haired, and the genitals of each gender

are brightly red-colored as is the muzzle (the sci-

entific name Ch. albinaSUS - Latin for “white nose”-

relates to the taxonomist, who may never have seen

the monkey he described alive. Furthermore, group

size in Ch. albinaSUS is much larger than that of any

of the taxa belonging to the Ch. satanas Clade,

ranging on average from 30-80 individuals. W here

Ch. albinuSUS occurs in sympatry with woolly mon-

keys (i.e., west of the Rio Tapajos-Juruena, east of

the Rio Madeira, and north of the Rio Ji-Parana),

they are often seen in mixed species associations.

Red-nosed saki groupings mixed with woolly mon-

keys (Lagothrix cana), tufted capuchins ( Sapajus

apella) and/or white-fronted slender capuchins

( Cebus unicolor ) m ay contain as m any as 150 mon-

keys.

In figure 28, we have depicted the distributions,

allopatric speciation, radiation, and supposedly

followed pathways of metachromic bleaching in all

known Saki Monkeys genus Pitheda. Sakis occur

exclusively in the rain forests of lowland Amazonia

and the Guayanan Shield (Hershkovitz, 1987b;

Mittermeier et al., 2013). Within the genus Pitheda

we distinguish three monophyletic cladistic Groups:

P. monachus, P. pitheda , and ^ hirsuta (Fig. 29).

W ithin the P. monachus Clade allopatric specia-

tion is thought to have followed evolutionary path-

ways of metachromic bleaching with P. Monachus

representing the nearest to archetypic precursor of

all extant sakis. Both sexes have an overall satur-

ated eumelanin, slightly bleached silky coat, except

for the cream-white hands and feet. Taxon P. VUOn-

achus ranges along both sides of the Amazon up-

stream from its confluence with the Rios Jurua and

150

Marc G.M. van Roosmalen & Tomas van Roosmalen

Figure 27. Map showing distributions of the Bearded Saki taxa Chiwpotes SClgulcitUS and C. israelita,

and the parapatric Black-headed Uakaris that occur north of the Amazon and Negro Rivers.

Japura, large rivers delineating its distribution in the

east and north. The species is sexually dimorphic,

not in size but in metachromic pelage characters of

the head. Both sexes have a slightly bleached mask

that is light brown in males and cream-white in fe-

males. It surrounds a black face with yellow to

cream eyebrows and malar stripes. Forehead and

cheeks are covered with short, forward directed

hairs resembling much that of members of the P.

pithetia Group. From P. monachliS diverged in

northwestern direction taxon P. milleri, supposedly

after a metachromic deviant founder-colony of

ancestral monachus traversed the Rio Caqueta.

Pithecia milleri nowadays occupies a small part of

the Colombian Amazon that is confined by the Rios

Caguan and Putumayo. Both sexes are overall eu-

melanin bleached, more so in females. The forehead

is covered with long, forward directed hairs forming

a kind of hood that is yellowish in males and cream-

white in females. The black muzzle is contrasted

with the advanced euchromic malar and lip stripes.

From P. milleri derived the taxon P. napensis after

a founder-colony of P. milleri traversed the Rio

Putumayo in southern direction. Pithecia napen-

sis occupies a small area in the Colombian and

Ecuadorian Amazon delineated by the Rio Putu-

mayo in the north and the Rio Napo in the south. In

P. napensis both sexes are progressively pheo-

melanin bleached in the yellowish to orange breast,

more so in males that also differ in the silvery

grayish lower part of a well-defined mask and in the

albinotic hood. After a founder-colony of ancestral

P. napensis once traversed the Rio Napo to the

south, the progressively pheomelanin bleached

taxon P. aequatorialis diverged. It occupies a large

area in the Ecuadorian and Peruvian Amazon delin-

On the origin of allopatric primate species

15 1

eated in the north by the Rio Napo and in the south

by the Rio Tigre. Pitheda aequatorialis, in particu-

lar in the metachromic characters of the male’s head

(fully albinotic mask) and (orange) breast pelage,

represents the most advanced pheomelanin bleached

taxon in the P. TYlOYiachllS Clade. Its dead-end distri-

bution at the end of the phylogeographic radiation

of the P. monachliS Clade is confined at all but

western (Andean Mountain range) sides by P. mOYl-

CtchllS occupied territory. We may ponder about

what would be the result of any hypothetical hy-

bridization between P aequatorialis females and P.

monachliS males at the contact zone that should

exist in the species’ westernmost distribution. Even

if the offspring would remain fertile, it would never

result in parapatric speciation. In concurrence with

our theory, deviant young males with metachromic

genes from P. aequatorialis w ould be expelled by

the dominant male(s) of the P. monachus parental

group, back to P aequatorialis territory .

Within the P. pitheda Clade we consider P.

lotichiusi with the overall darkest agouti (in fe-

males) and saturated eumelanin black (in males)

pelage the nearest to archetypic taxon. This taxon

is only found in the easternmost part of the inter-

fluvial peninsula between the lower Solitudes and

Negro Rivers, from opposite the city of Manaus as

far west as the towns of Manacapuru and Novo

Airao. In the past, P. lotichiusi m ay have occupied

a much larger distribution, for no untraversable

geographic barriers exist when going further west

into the Rios S olim oes/N egro interfluve. If so, the

P. pitheda Clade may have m onophyletically

derived from the P. monachus Clade, when that ra-

diated to the east. A founder-colony of slightly

pheomelanin bleached ancestral P. monachus may

SAKI MONKEYS

PITH EC I A

Pitheda pitheda Clade

fl P paheciaQP, chrysocephala

P. lotichiusi

Pitheda monachus Clade

P. monachus P. mitleri

P. napcnsis Paoquaioriaiis

Pitheda hirsuta Clade

P. irrorata ^P. hirsuta

P. vaniolinii P. albicans

Figure 28. Distributions, allopatric speciation, radiation, and supposedly followed metachromic

pathways of bleaching in all known Saki Monkeys genus Pithedci.

152

Marc G.M. van Roosmalen & Tomas van Roosmalen

have traversed the lower Rio Japura and thereafter

diverged into the allopatric taxon P. lothichiusi. The

latter then extended its range to the east. During one

of the late-Pleistocene glacials, when ocean levels

dropped over up to 120 m, a founder-colony of P.

loti Chius i could well have traversed the lower

Rio Negro and then reached the north bank of the

Amazon. This way, it may have diverged into the

allopatric Golden-faced Saki taxon P. chryso-

cephala. Nowadays,Golden-faced sakis range from

the Rio Branco as far east as the Rio Trombetas.

After a founder-colony of ancestral P. chrySO-

cephala once traversed the Rio Trombetas, taxon

P. pithecia may have diverged. Pithecia pithecia

then expanded its range in northwestern direction

across the states of Roraima, Para and Amapa, and

across the Guianas into Venezuela as far west as the

lower Rio Orinoco. It may have circumvented

either side of the watershed formed by the Tumac

Humac Mountains. Within the sexual dimorphic P.

pithecia Clade, females are progressively pheo-

melanin bleached orange to yellowish brown, whe-

reas males are all-black with a progressively pheo-

melanin bleached to albinotic mask. In the Brazilian

taxa P. lotichiusi and P. chrysocephala the mask that

consists of short, stiff, forward directed hairs is

golden to orange-yellow colored. In the Guianan

white-faced saki P. pithecia the mask is albinotic,

white with orange-colored cheeks in males from

Guyana and Suriname, and overall white in males

from French Guiana.

Sakis of the P. monachus and P. pithecia C lades

Figure 29. Among the Saki Monkeys genus Pithecia three monophyletic clad is tic Groups or Clades are distinguished: the

P. monachus Group containing four taxa ( P. monachus, P. milleri, P. napensis, and P. aequatorialis) , the P. pithecia Group

containing three taxa (P. lotichiusi , P. chvySOCephala , and P. pithecia), and the P. llivSUta Group containing four taxa

( P. hirsuta, P. Prorata, P. vanzolinii, and P. albicans) . We only recognize sexual dimorphism as expressed in metachromic

characters in the monachus and pithecia Clades (Courtesy of Stephen Nash).

On the origin of allopatric primate species

153

distinguish themselves locomotorily from sakis of

the third clade - the P hirsuta Clade. A specific

locomotor pattern called “vertical leaping and

clinging” is performed during foraging and travel-

ing in their preferred habitat, which is the discon-

tinuous lower canopy and understory of terra firme

rain forest. As these sakis have to leap from tree

trunk to tree trunk, they are commonly known as

“flying monkeys”. In contrast, saki taxa of the P.

hirSUta Clade prefer the middle to upper strata of

primary rain and seasonally inundated floodplain

forests, which strata are interconnected by thick-

stemmed vines and hem i-epiphytic climbing

shrubs. For that preferred habitat they have adopted

a different locomotor pattern, that of horizontal

leaping, and quadrupedal running or hopping across

thick horizontal branches and boughs. A significant

difference in limb proportions between taxa belong-

ing to each of the two Clades has been measured,

with those of the P. pitheda Group being longer

relative to trunk length (H ershkovitz, 1 987a;

1 987b). Another important feature in which the P.

hirSUta Clade distinguishes itself from the P. mOYl-

achus and P. pithecici Clades is mean group size

and sexual dimorphism. Social groups of taxa be-

longing to the P. hirSUta C lade are larger and m ulti-

male structured, instead of the extended family

group that contains only one or sometimes two

adult males in taxa belonging to the other Clades.

Moreover, contrary to what recent taxonomies

Rio Solimoes

vdrzea

-Parana' do Salsa

' Lago Uauacu

L Coarf tern firme

Lago Ayapua

varzea

-Rio Pur 6 s

Figure 30. Satellite image taken from the region, where the varzea floodplain of the Rio Solimoes borders on that of the Rio

Purus. Behind each floodplain are locate d black-water backwater lakes (rias), such as Lago Coari, Lago Uauacu, and Lago

Ayapua. A red line indicates where parapatric bald-faced saki Pithecici hlVSUta is encroaching onto huffy saki P. albicans

territory. (Below) Portraits of different adult males of Gray’s saki P. hivSUtd. (Above, left) White-masked mutant male P.

hirSUta that was seen roaming around alone far in to P. dlbicdHS territory north of Lago Uauacu. (Above, right) Adult male

huffy saki P. albicans, note the black face with the showy albinotic eyebrows and white long-haired hood.

154

Marc G.M. van Roosmalen & Tomas van Roosmalen

(merely based on museum collections) suggest, we

were not able to recognize metachromic sexual

dimorphism in any taxon of the P. hirsuta Clade. In

the field, we failed to distinguish gender among

group members of P. hirsuta, P. irrorata, and P.

albicans. N or could we, in captivity, determ ine their

gender without up-close examining the saki mon-

key’s concealed genitals.

Within the Bare-faced Sakis of the P. hirsuta

Clade we suggest the least eumelanin bleached

overall blackish-gray taxon P. hirsuta to be the

nearest to archetypic taxon. It may well have de-

rived from a founder-colony of proto -moiiachus

that once traversed the Rio Jurua in eastern direc-

tion. The following pathways of metachromic blea-

ching and allopatric speciation are recognized.

From P. hirsuta that occupies the entire interfluve

delineated by the Jurua, Solimoes and Madeira Ri-

vers, diverged and radiated away in eastern direc-

tion taxon P. irrorata after a founder-colony of

progressively bleached P hirsuta traversed or cir-

cumvented the Rio M adeira (most likely at its upper

reaches) during one of the late-P leistocene glacials.

Nowadays, taxon P. irrorata occupies the entire

interfluve delineated by the Madeira, Amazonas

and Tapajos-Juruena Rivers. Its overall coat is

advanced eumelanin bleached in comparison with

that of P. hirsuta, and albinotic in the distal half of

the hood, the hands and feet. Its tail is less bushy,

the hairs more curly. Pitheda irrorata has an almost

bare face, and its forehead is only halfway covered

by an albinotic hood that does not conceal the

cheeks and temples. As a result, the monkey’s

profile looks more pronounced. Metachromic skin

and fur characters of the head that play such an

important role in the taxonomy of monkeys like

Pitheda, Sapajus and Ateles are often poorly pre-

served in museum specimens. Hence, the confusion

in most hitherto elaborated taxonomic reviews of

these genera. Zoological collections all over the

world have lumped m isidentified taxa, such as P.

hirsuta and P. irrorata, under the latter. Some lead-

ing taxonomists even attribute sexual dimorphism

to the B are -faced S akis. From P. hirsuta to the west

diverged taxon P. vanzolinii, after a progressively

bleached founder-colony of P. hirsuta traversed the

Rio Envira. Pitheda Vanzolinii is now confined to

the headwaters of the Rio Jurua. It differs in the al-

binotic lower limbs and ventral parts that contrast

much with the blackish-gray dorsal parts and tail.

From P. hirSUta to the north derived the overall

near- a lb in otic taxon P. albicans that is pheomelanin

bleached orangish-yellow only on the lower limbs.

Buffy Sakis P. albicans occupy the northernmost

dead-end distribution of the P. hirsUtaClade, which

is delineated by the u ntraversable lower Solimoes

River in the north, the lower Jurua River in the west,

and the lower Purus River in the east. Buffy Sakis

are parapatric with the more opportunistic Gray’s

Sakis P. hirsuta, from which they once derived. At

its southern limit, its distribution shows an open end

running across the Rio Tapaua axis. After it tra-

versed the Rio Tapaua to the north, Gray’s Saki

P. hirsuta was, and still is expanding its range

northw ards to the cost of the B uffy Saki P. albicans.

This example may well demonstrate that progress-

ively bleached to albinotic primate taxa that occupy

dead-end distributions will eventually go extinct.

East of the Rio Coari and north of the Rio Tapaua -

a left-bank tributary of the Rio Purus - we have con-

firmed the sympatric occurrence of the taxa P. al-

bicans and P. hirsuta, with P hirsuta advancing

onto P. albicans as far north as Lago Ayapua (Fig.

30). North of the Ayapua contact zone in territory

exclusively occupied by P. albicans, we once spot-

ted and photographed a solitary young male, its

head pelage resembling that of male White-faced

Saki P. pitheda from the Guianas (Fig. 30). We as-

sume that this male was a progressively bleached

deviant color morph of taxon P. hirsuta that was

expelled from or forced to leave its parental group.

It may have ventured into adjacent P. albicans

territory north of Lago Uauagu. As we have often

seen P. hirsuta groups opportunistically penetrating

far into white-water floodplain forest (varzea), this

metachromic deviant near-albinotic, sexually

dim orphic m utant m ale of taxon P. hirsuta in theory

could become the founding father of a new taxon.

This could happen after this young male would

have attracted one or a few P. albicans females to

form a small reproductive family group. It then

would have to survive making a year-round living

in the extensive varzeas found along the south bank

of the Rio Solimoes. We have never seen any saki,

uakari or other seed-predating monkey occupying

that ecological feeding niche in the varzeas that

fringe the right bank of the middle Rio SolimSes.

Perhaps, this hypothetical scenario may also explain

how metachromic sexual dimorphism in primates

could have evolved.

On the origin of allopatric primate species

155

In figure 3 1, we have visualized the distribu-

tions, allopatric speciation, radiation and sup-

posedly followed pathways of metachromic bleach-

ing in all known Woolly Monkeys, genus LagO-

thvix. Woolly monkeys are exclusive matrix terra

firm e rainforest dwellers that under normal circum-

stances will never enter white-water floodplain

forest (varzea). For that reason alone, the distribu-

tion of LagOthrix is greatly determined by riverine

barriers. Within the genus only one monophyletic

Clade is recognized. We consider the saturated eu-

melanin, metachromic least bleached Poeppig’s

Woolly Monkey taxon La. poeppigii w ith its overall

black to dark chestnut-brown coat the nearest to ar-

chetypic woolly monkey. In the north, La. poeppi-

glV s distribution is confined by the Amazon River,

in the east by the Rio Jurua that is also fringed with

extensive varzeas, and in the south and west by the

foothills of the Andean Mountain range. From La.

poeppigii derived in western direction the Peruvian

Yellow -tailed Woolly Monkey La. flavicauda,

which has (disputedly) been upgraded to its own

genus Oreonax. It occurs in parapatry with La.

poeppigii , but genetically isolated from it, as it lives

in high-altitude Andean cloud forest. With its al-

binotic lower half of the circumocular rings, facial

muzzle, chin and pheomelanin bleached yellow tail

the taxon is following a pheomelanin pathway

towards albinotic. From a founder-colony of some-

what eumelanin bleached La. poeppigii that tra-

versed or circumvented the upper Rio Jurua and

then radiated to the east and north, the darkbrown

to black headed taxon La. tschudii derived. Its coat

is overall dark gray-brown colored, becoming

blackish on all five limbs. It occupies the entire

interfluve delineated by the Jurua, Solimoes-

WOOLLY MONKEYS LAGOTHRIX

Lagothrix lagotricha

Q Lagothrix poeppigii

Lagothrix carta

'23 Lagothrix Rio Javan

Lagothrix iugens

Lagothrix tschudii

, Lagothrix Rio Aripuana

Lagothrix Rio Jutaf

Lagothrix (Oreonax) flavicauda

Figure 31. Distributions, allopatric speciation, radiation, and supposed eumelanin pathways of

metachromic bleaching in all known Woolly Monkeys genus Lagothrix.

156

Marc G.M. van Roosmalen & Tomas van Roosmalen

Amazonas and Madeira Rivers. From La. tschudii

in eastern direction diverged the Black-headed or

Geoffroy’s Gray Woolly Monkey taxon La. Cana,

its entire coat progressively eumelanin bleached,

light-gray colored, with a dark-gray to black head.

Only as recent as the late- Pleistocene or early

Holocene, an advanced eumelanin bleached

founder- colony of La. tschudii must have traversed

or circumvented the upper Madeira River north of

the Rio Ji-Parana (also known as Rio Machado) in

eastern direction. It then extended its range by

passing the geographic barrier formed by the ex-

tensive Tenharim Savanna in Rondonia alongside

its southern border. This way, it could enter the

interfluve delineated by the Madeira, Amazonas

and Tapajos Rivers. Circumventing the extensive

Tenharim Savanna, taxon La. Cana apparently

missed the narrow entrance to the north that exists

between the upper Rio Ji-Parana and the Rio

Roosevelt. This could well explain why woolly

monkeys are absent from the entire Rios

M adeira/A ripuana interfluve north of the Rio

M armelos. The relatively recent occupation by La.

Cana of the entire interfluve delineated by the

Madeira, Aripuana, Amazonas and Tapajos Rivers

is near to its completion. Taxon La. Cana’s current

northernmost distribution gets to a halt at the lat-

itude running across the upper reaches of the

Abacaxis and A ndira Rivers, not much south of the

untraversable Rio Amazonas. We assume that only

when La. Cana invaded all smaller interfluves east

of the Rio Aripuana and west of the Rio Tapajos, it

began to displace the A 11 -black Woolly Monkey that

in the far geological past evolved in the area east of

the (proto)-M adeira River. This newly identified

woolly monkey still has to be collected and de-

scribed. We here provisionally allocate the common

name “Rio Aripuana Black Woolly Monkey” to this

fully saturated eumelanin, all-black taxon. Ap-

parently, as it occupies the same ecological niche

as newcomer La. Cana , the Rio Aripuana Black

Woolly Monkey finds itself on the verge of ex-

tinction. It is smaller, lives in small, socially less

complex family groups, and its coat is in meta-

chromic respect the most primitive or archetypic. It

lives in sympatry with La. Cana, but only hangs on

in a small enclave distribution situated between the

lower to middle Rio Aripuana and the Rio Acari. It

may well represent the ancient, most original, ar-

chetypic taxon of all Woolly Monkeys genus LagO-

thrix that evolved in the L ate-Pliocene east of the

proto-Madeira River, fully isolated from the rest of

the Amazon.

Woolly monkeys also radiated into the north-

western Amazon, most likely after a founder-colony

of taxon La. poeppigii circumvented or traversed

the upper Amazon River in Peru (where it is called

Rio Maranon). Two progressively eumelanin

bleached forms that derived from La. poeppigii

once must have occupied the Colombian Amazon:

the euchromic light-gray Colombian Woolly Mon-

key taxon La. lugens that occurs at high altitudes in

the foothills of the S outh-C olom bian Andes and in

the upper Rio Magdalena valley, and the Brown or

Humboldt’s Woolly Monkey taxon La. lagOtricha.

The coat of taxon La. lugens is eum elanin bleached

charcoal to light-gray colored, but lacks any mix-

ture with brown. On the head, a mid-dorsal stripe

and a rim across the eyebrows are advanced

bleached to euchromic. Mean body size and weight

in La. lugens are the largest among all extant woolly

monkeys. LagOtvicha' s coat is progressively eu-

melanin bleached light-brown colored, except for

the blackish hands and feet. Its head is light-brown

colored, with a slightly bleached yellowish eyebrow

rim and sideburns aside of the blackish-brown face.

Taxon La. lagOthricha ranges across the Colom-

bian, Venezuelan and NW Brazilian Amazon.

Most interestingly, we confirmed the small

distribution of a newly identified, advanced pheo-

melanin bleached, overall orange-colored taxon in

the upper reaches of the Rio Jutai. A founder-colony

of advanced pheomelanin bleached La. poeppigii

mutants pushed out of La. poeppigii territory must

once have successfully adapted to white-water

seasonally inundated floodplain forest (varzea)

located between the east bank of the upper Rio Jutai

and the west bank of the Rio Jurua, near the town

of Eirunepe. We were not able to determine the

exact range of the Rio Jutai Woolly Monkey, for the

area is inhabited by uncontacted Amerindians of the

Korubo tribe (so-called “cageteiros”) that are

known to kill any non-indigenous intruder.

We encountered in the zoological collection of

the Brazilian Museu Goeldi (MPEG, Belem - PA ) an

overall orange-colored stuffed juvenile specimen

that was deposited without collecting data. This

very animal is depicted in Da Cruz Lima’s 1945

Mammals of Amazonia. We here provisionally

name it the “Rio Jutai Orange Woolly Monkey”.

On the origin of allopatric primate species

157

In addition, we found an albinotic overall

cream -colored taxon that we provisionally named

the “Rio Javan Fair Woolly M onkey” LcigOthrix sp.

It resembles much Humboldt’s Woolly Monkey

taxon La. lagotricha, but its pelage is longer, softer

and silky, besides being overall advanced eu -

chromic to cream-white colored. It has long-haired

white sideburns alongside a pitch-black face,

muzzle and chin. A near-albinotic ancestral fo under-

colony must once have been driven out of La.

poeppigH territory somewhere near the northern-

most border of its distribution. This colony must

have been forced to make a living in the white-

water floodplain forests (varzeas) that stretch out

along the south bank of the Rio Solimoes (near the

town of Tabatinga) all the way to the left-bank

varzeas of the lower Rio Javari. Under normal cir-

cumstances this type of habitat should be conside-

red inappropriate for woolly monkeys to guarantee

a durable and sustainable living. This seems to be

another case where a progressively bleached, near-

albinotic founder-colony of La. poeppigH has been

driven into a (for woolly monkeys) marginal habitat

- seasonally white-water inundated floodplain forest

(varzea). According to our theory of allopatric

primate speciation, albinotic fair woolly monkeys

must have diverged this way from archetypic, sat-

urated eumelanin, dark brown coated La. poeppigH.

Apparently, it has survived until today in geo-

graphic sympatry, but ecological parapatry (inhab-

iting adjacent but different habitats) with taxon La.

poeppigH , the species it derived from. In 2002, the

second author, while at Colombia University, NY,

ran the mtDNA sequences of the Rio Javari Fair

Woolly Monkey using earlier preserved DNA-

samples. He found 4% divergence from sympatric

AMAZONIAN SPIDER MONKEYS

ATELES

Ateles pan isc us Clade 0 A. paniscus

Ateles behebuth Clade

f A. hybridus A. brunneus

4. beliebuth (Rios NegroIOrinoco)

A. variegatus (N PerufSW Colombia]

Ateles chamck Clade

0 A. chamek

A. sp. nov. (Rios RuruslMadeira)

0 A. longimembris

Ewk A. marginatus

A. sp, nov. (Upper Rio

Xingu)

Figure 32. Distributions, allopatric speciation. radiation, and supposed pathways of metachromic bleaching followed in

all known Spider Monkeys genus Ateles that occur in the Amazon and along the P acific coast of Ecuador and Colombia.

158

Marc G.M. van Roosmalen & Tomas van Roosmalen

Lei. poeppigii and over 7% from the allopatric taxon

La. lagOtricha. The AMNH holds three well-

preserved skins of the Rio Javan FairWoolly Mon-

key LagOtrix sp which were collected by the Olalla

Brothers in 1927 along the south bank of the Rio

Solimoes, somewhat upstream from the town of

Tabatinga. All three specimens are m isidentified as

La. lagOtricha (Humboldt, 1 8 1 2 ) .

For Spider Monkeys genus AteleS, allopatric

speciation, radiation, and phy logeography along

different pathways of metachromic bleaching are

depicted in figures 32, 33. Four monop hyletic

cladistic Groups or Clades are recognized: A. pan-

iscus, A. chamek, A. belzebuth, and A. geoffroyi.

Spider monkeys have evolved during the Pliocene

in the Guayanan Shield, most likely from a pre-

cursor of the most ancient of the four extant mono-

phyletic cladistic Groups, the A. panisCUS Clade.

The Red-faced Black Spider Monkey A. panisCUS

from the Guianas represents the nearest to ar-

chetypic extant taxon within the genus. This as-

sumption is based on some unique primitive

characters that are not seen in other spider monkeys.

Here we mention: the presence of a vestigial thumb

or, if lacking, at least the metacarpal of the first digit

that is maintained in the hand; its incapacity of

using the tip of the prehensile tail in picking and

manipulating small objects like food items; the

overall long-haired coat, in particular around the

base of the tail and in the forward directed hairtuft

on the forehead that resembles a cap; the overall

saturated eumelanin black coat without any sign of

early eumelanin bleaching; the advanced pheo-

melanin bleached bright-red bare face lacking

whiskers; the frequent occurrence of albinotic blue-

colored eyes; the albinotic cream-white colored,

hypertrophied, pendulous clitoris in females and

cream-white protruded anus in both sexes, whereas

Figure 33. Phylogeographic distribution, allopatric speciation. radiation and metachromic diversification in all known Spider

M on key s (AteleS) that occur from the Pacific coast ofW Ecuador and NW Colombia far into C Am erica as far N Mexico.

On the origin of allopatric primate species

159

the clitoris is long, flattened and lacking the muscu-

lature to erect during foreplay and copulation (Van

Roosmalen, 1985a). Mo re over, spider-monkey mat-

riarchal social organization is markedly expressed

in (leading) female’s body size, which in A. pan-

isCUS may exceed that of males; and in the per-

manent fu sion -fissio n social structure centered

around alpha-females that lead foraging parties on

day ranges. As such, complete gatherings of all

twenty or so members of a social grouping will

never happen (Van Roosmalen, 1985a). This spe-

cific type of social organization that is unique

am ong N eo tropical prim ates may we 11 be related to

the specific phy tosociological composition, pheno-

logy and physiognomy of the more ancient, more

heterogeneous type of primary terra firme rain

forest that evolved uniquely and without major

interruptions during the last 60-70 million years on

the Guayanan as well as on the Brazilian Shield.

Here, available food sources are generally widely

dispersed, and rarely clumped at any time of the

year. Maturation of nutritious large-seeded fruits -

A. panisCUS is a mature-fruit specialist frugivore -

is slower and species-specifically stretched out over

longer periods of time (Van Roosmalen, 1985b).

Mast-fruiting, as commonly seen in tropical rain-

forests on other continents, is a phenomenon that

does not exist in this ecosystem. Hence, the early

evolution of sem i-brachiation (brachiation with the

help of a prehensile tail) as the principal locomotor

pattern, and the fusion-fission type of social struc-

ture during traveling and foraging took place in an-

cestral spider monkeys as the principal adaptation

of a large-bodied monkey to a well-defined ecolo-

gical feeding niche, in a biome that took over 60

million years to develop. It may well explain why

the A. panisCUS Clade did not speciate and radiate

any further, as the distribution of extant A. panisCUS

is still confined to the larger part of the Guayanan

Shield.

Most plausibly somewhere in the late-Pliocene,

from an agouti or saturated eumelanin all-black an-

cestor of A. panisCUS derived the phylogenetically

distantly related, nearest to archetypic Black Spider

Monkey taxon chain ek of the A. chcilfiek Clade. It

is distributed south of the Amazon as far south as

the Brazilian Shield (in Rondonia and Mato Grosso

states). North of the Amazon, the Brown Spider

Monkey taxon A. brunneus that ranges in N Colom-

bia (in an area confined by the Sierra Nevada

Mountains), may represent the least eumelanin

bleached, nearest to archetypic taxon of the A.

belzebuth Clade. Moreover, in the Pacific coastal

forests of Ecuador and Colombia is found the sat-

urated eumelanin Brown-headed Spider Monkey

taxon A.fusdcepS (form erly A.justiceps filSCWepS).

Along the Pacific coast of N Colombia and S

Panama is found the all-black but dark red-bellied

Colombian Black Sp id er Monkey taxon A. rufiventris

(formerly A. fusdceps robustUS). All-black Brown-

headed Spider Monkey taxon A. fusdceps may

therefore represent the nearest to archetypic taxon

of the A. geoffroyi Clade (Fig. 3 2).

W ithin the A. chciffiek C lade, nom in ate A. chamek

represents the nearest to archetypic taxon. It is sat-

urated eumelanin in its overall black coat color and

blackish or slightly bleached pinkish circumocular

rings and/or facial muzzle, and in the forward

directed black hairtuft on the forehead. It ranges

across a large part of the Amazon basin delineated

by the Amazon River in the north, the Andes Moun-

tains in the west, the highlands of the Brazilian

Shield in the south, and the Purus and Guapore

Rivers in the east. Like the other taxa of the A.

chamek Clade, the Black-faced Black Spider Mon-

key A. chamek is only found in patches of terra

firme rain forest close to major waterbodies, such

as lakes, rivers, and creeks. It frequents in particular

seasonally inundated marsh forest and black- and

clear-water floodplain forest called igapo. We have

never spotted spider monkeys belonging to the A.

chamek Clade in matrix primary rainforest of the

hinterland at distances of over ten km from any

major waterbody. There, spider monkeys of the A.

chamek Clade are commonly replaced by woolly

monkeys ( LagOthvix ) that occupy the same feeding

niche in primary terra firme rain forest. All taxa

of the A. chamek Clade do laterally migrate to the

nearest igapo floodplain forest of clear- and black-

water rivers during the 2-3 months lasting fruiting

season, which coincides with the peak of the flood.

From A. chamek diverged and radiated away in

eastern direction the Rio Purus Black Spider Mon-

key that we identified to be new to science. This

taxon ranges in the interfluve between the Purus

and Madeira Rivers, south of the Rio Ipixuna

and north of the Rio Tahuamanu in the Bolivian

Amazon, a left-bank tributary of the upper Rio

Madeira. The Rio Purus Black Spider Monkey

AtheleS sp. is having a near-albinotic cream to pink

160

Marc G.M. van Roosmalen & Tomas van Roosmalen

colored muzzle, chin, and ears, and a triangular

patch of short, backward directed black hairs on the

forehead instead of a cap . A f ter a founder- colony of

the Rio Purus Black Spider Monkey traversed the

Rio Madeira to the east, the Long-limbed Black

Spider Monkey A. longimembris diverged. This

taxon was already identified as a distinct species by

Da Cruz Lima (1945) based on two specimens that

were collected by Leo E. M iller along the upper Rio

Ji-Parana in M ato Grosso during the first part of the

1914 Roosevelt-R ondon Expedition. It was first de-

scribed as Ateles longimembris by Allen ( 1 9 1 4 ) .

Holotype and paratype of A. longimembris depos-

ited in the zoological collection of the AMNH under

No. 36909 were later m isidentified as A. chamek

and therefore not included in Kellogg & Goldman’s

(1 944) revision of the Spider Monkeys genus Ate-

les. The La tin name thatAllen (1914) attributed to

this taxon relates to the “ excessively long tail and

limbs, the tail length very nearly twice the length of

head and body" . A side of its elongated and slender

limbs, taxon A. longimembris is further character-

ized by the pitch-black face and ears, except for a

pale cream-white albinotic triangular patch on the

nose, and a wide triangular patch on the forehead

that is barely covered with sparse backward direc-

ted, stiff, black hairs. Another character of this

taxon is the relatively robust incisors and canines

that look oversized so that the lips seem unable to

conceal them . This feature gives adult Long-lim bed

Black Spider Monkeys taxon A. longimembris a

bulldog-like appearance. Moreover, its loud or

long-distance calls that are so typical for other

spider monkeys do not carry far. They sound like

bird whistles blowing in the wind. The distribution

of A. longimembris is confined by the Rio Madeira

in the west, the lower Amazon River in the north,

the Rio Tapajos-Juruena in the east and the Rio

Ji-Parana in the south. From a founder-colony of A.

longimembris that once traversed the Rio Tapajos-

Juruena to the east derived the W h ite- w h iskered

B lack Spider M onkey A. marginatUS. It is all-black

and only euchromic in the small triangular forehead

patch or blaze formed by backwards directed white

hairs. However, we have seen also adult free-ran-

ging A. marginatUS that had black forehead patches.

This taxon occupies the interfluve delineated by the

Rios Tapajos and Teles-Pires in the west, the lower

Amazon River in the north, the Rios Tocantins and

Araguaia in the east, and the upper Rio Teles-Pires

or Rio M inisuia-M igu (both right-bank tributaries

of the upper Rio Tapajos) in the south. After a

somewhat eumelanin bleached founder-colony of

A. marginatUS once traversed the upper Rio Teles-

Pires south of the A. marginatUS distribution, a new

taxon diverged that we name the Upper Rio Xingu

White-whiskered Brown Spider Monkey. Its coat is

chestnut-brown dorsally, and lighter brown on the

ventral parts. The snow-white semi-crescent blaze

is much larger than in A. marginatUS. It widens

above the eyes into long sidewards directed streaks.

This newly identified taxon distinguishes itself also

from taxon A. marginatUS in the long white

whiskers that run from below the eyes across the

lips and chin. Moreover, facial skin is pink to flesh-

colored in the circumocular rings, muzzle, lips and

chin.Within the monophyleticA. chamek C lade the

White-whiskered Brown Spider Monkey from the

Upper Rio Xingu represents the furthermost eu-

melanin bleached taxon that, in accordance with our

theory, m etachrom ically and phylogeographically

radiated farthest away from archetypic Black-faced

Black Spider Monkey taxon A. chamek.

W ithin the A. belzebuth Clade, we recognize the

dorsally saturated eumelanin darkbrown Brown

Spider M onkey taxon A. brunneus as the nearest to

archetypic taxon. Belly and inner limbs are eu-

melanin bleached light- brown colored. The trian-

gular forehead patch formed by backward directed

hairs is only slightly bleached brownish-black

colored. Taxon A. brunneUS is found in N Colom-

bia, between the Cauca and Magdalena Rivers.

It is taxonom ically treated as a subspecies of A.

hybridus. In the far geological past, the A. belzebuth

Clade could well have derived from the archetypic,

saturated eumelanin, all-black taxon (A. geoffroyi)

A. fusciceps (form eriy A. fusciceps fusciceps ) of the

A. geoffroyi Clade that occurs west of the Andes

Mountains in the Pacific coastal forests of Ecuador

and Colombia. An ancestral founder-colony of A.

fusciceps once may have circumvented the Sierra

Nevada north of it and diverged into ancestral A.

brunneus in the western part of the lower Rio M ag-

dalena valley. After a progressively eumelanin

bleached founder-colony of A. brunneus traversed

the Rio Magdalena to the east, the light-brown and

silvery-white colored Variegated Spider Monkey

taxon A. hybridus could have derived. It ranges

from the northern Colombian Rio Magdalena Basin

into the southw esternm ost corner of Venezuela, in

On the origin of allopatric primate species

161

the foothills of the Sierra Nevada mountain range

(near the city ofMerida). Inner parts of limbs, belly

and the small triangular forehead patch are silvery

white in taxon A. hybridus , whereas the rest of the

coat is light-brown colored. An advanced eu-

melanin bleached founder-colony of A. Hybridus

once may have circumvented the Sierra Nevada

Mountains to the east and reached the headwa-

ters of some of the Rio Orinoco’s tributaries in

Venezuela’s Amazonas state. It then diverged into

the furthermost pheomelanin bleached White-

bellied Spider M onkey taxon A. belzebuth. It ranges

from north of the Rio Negro and west of the Rio

Branco into the Venezuelan State of Amazonas west

of the Rio Orinoco, and also far into the lowland

Amazon of Colombia. Upper parts, head and dorsal

coat of White-bellied Spider Monkeys taxon A.

belzebuth are light-brown, but their pelage on

ventral parts and inner sides of limbs are silvery

white, often pheomelanin bleached yellow to

orange-colored. The skin of muzzle and chin is pale

brown to pinkish colored. The triangular forehead

patch or blaze is light brown, and the eyebrows,

whiskers, and throat are silvery. From a founder-

colony of A. belzebuth that once traversed the upper

Rio Caqueta derived in southwestern direction the

southernmost distributed taxon of the A. belzebuth

Clade, A. variegatus. This taxon occurs in the N

Peruvian, SW Colombian and eastern part of the

Ecuadorian Amazon, east of the Andes Mountains

and north of the Amazon River (where the river is

called Rio Maranon). Its coat is dorsally eumelanin

blackish to dark gray, and ventrally euchromic to

albinotic silvery-white, except for the dark grayish

hands and feet. The legs are silvery white, as are the

whiskers and the large blaze or triangular patch on

the forehead. Advanced pheomelanin bleached

color traits (yellow and orange) as seen in A. belze-

buth are lacking in A. VCiriegCltUS. In accordance

with our theory and the principle of metachromic

bleaching, within the belzebuth Clade the most eu-

chromic taxon, A. variegatus, has phylogeograph-

ically radiated the farthest away from the dark-

brownish colored, nearest to archetypic taxon A.

brunneus (Fig. 32).

Within the A. geojfroyi Clade (Fig. 33), we re-

cognize the saturated eumelanin Colombian

Black Spider M onkey taxon A. (jusciceps ) rufiventris

(formerly A. fusciceps robustUS ) from the Pacific

coastal forests of Colombia and South Panama west

of the Andes Mountains as the nearest to archetypic

taxon of the A. geoffroyi Clade. Its coat is glossy

pitch-black, whereas color morphs of this taxon

show a saturated pheomelanin dark red colored

belly and genital area. Fur on the fo rehead is

slightly brownish tinged. From taxon A. rufiventris

derived in southern direction the Brown-headed

Black Spider Monkey, the nominate taxon A. (fus -

deeps) fusciceps from the Pacific coastal forests of

Ecuador and Colombia. It is slightly eumelanin

bleached blackish-gray on the belly, brownish black

above, with a yellow-brown anterior crown, grading

from brown to black on the nape. It often has a

white m ustache and beard. Taxa A. fusciceps and A.

rufiventris stand at the base of the monophyletic

C entral-A m erica S pider-M onkey A. geojfroyi C lade,

which radiated away in northwestern direction

across the Isthmus of Panama into CentralAm erica

as far north as Mexico. From the Colombian Black

Spider Monkey A. rufiventris derived the advanced

euchromic, near-albinotic (except for the saturated

eumelanin feet, hands, lower arms and distal part of

the tail) taxon A. ( geoffroyi ) grisescens. However,

the validity of this taxon is doubtful, for it has never

been seen in the wild. It is thought to occupy a

dead-end distribution along the Pacific coast from

the Rio Tuyra valley in SE Panama into the Cor-

dillera de Baudo in NW Colombia. To the east, its

distribution is confined by territory occupied by the

Colombian Black Spider Monkey A. rufiventris.

From A. rufiventris diverged in western direction

the advanced pheomelanin bleached Ornate Spider

Monkey taxon A. ( geoffroyi ) panamensis. it is

argued that the form A. panamensis is a junior

synonym of A. ornatus. Taxon A. panamensis/

OmatUS has a golden brown, dark red to orange

colored back, with saturated eumelanin black pe-

lage on the top of the head, outer sides of legs,

hands, feet and distal part of the tail. It is distributed

throughout Panama (from Chiriqui Province as far

as E of the Canal Zone) and C+E Costa Rica. From

A. ornatus (or A. panamensis ) derived in southern

direction the advanced pheomelanin bleached

Azuero Spider Monkey taxon A. azuerensis. Its

back is gray ish -bro w n , somewhat darker than the

underside. Outer surfaces of the limbs are black,

the top of the head and neck are (brow nish)-black.

Its distribution is delineated by the Panamanian

Pacific coast in the south and east. From the Or-

nate Spider Monkey taxon A. OmatUS derived in

162

Marc G.M. van Roosmalen & Tomas van Roosmalen

northern direction into Nicaragua the advanced

pheomelanin bleached, near-euchrom ic Geoffroyi’s

Spider Monkey taxon A. geojfwyi. It is silvery to

brownish-gray on the back, upper arms, and thighs.

Its coat (except for the black head, elbows, knees,

upper arms, lower legs, hands and feet) is overall

orangish and cream-white colored. Its face is black,

often with flesh -colored ‘spectacles’ around

the eyes. From A. omatUS radiated away, first in

western direction and from coastal Costa Rica

northwards into Nicaragua, the advanced pheo-

melanin bleached Black-browed Spider Monkey

taxon A. ffflntatUS . W ith its orange, black and white

coat A. ffflntatUS is the most colorful taxon of the

entire A. geoffroyi Clade. From taxon A. frOYltatUS

derived the overall most euchromic bleached

Mexican Spider Monkey taxon A. VellewSUS. Its

dorsal surfaces range from black to light brown, and

contrast strongly with its lighter abdomen and inner

limbs. Flesh-colored skin is often present around

the eyes. It occupies the entire northwestern part of

the Isthmus containing El Salvador, Honduras

(along the N coast into the lowlands of La

Mosquitia), Guatemala (including the highlands)

and E & SE Mexico. From taxon A. VelleWSUS to

the north derived the near-albinotic Yucatan Spider

Monkey taxon A. yucatanensis . It is characterized

by the overall advanced eumelanin bleached, light

brown and white colored coat. Its fur is brownish-

black on the head, neck, and shoulders, grading into

lighter brown on the lower back and hips and

contrasting with its silvery-white underside, inner

limbs, and sideburns. Ateles (geojfwyi) yUCCltan-

ensis occupies a large distribution containing NE

Guatemala, all ofBelize, and SE Mexico (Yucatan

Peninsula). The near-albinotic taxa A. VellewSUS

and A. yuCCltanensis that occupy dead-end distribu-

tions confined by u ntraversable geographic barriers

in the northernmost range of the A. geojfwyi C lade,

phenotypically do resemble taxon A. griseSCeilS

(from SW Panama) that occupies the southernmost

distribution of the A. geoffroyi Clade within the

Isthmus. These taxa are equally confined to phylo-

geographic dead-end distributions, therefore fully

concurring with our theory that pretends to unveil

and retrace allopatric primate speciation and radi-

ation along phy logeographic pathways of meta-

chromic bleaching.

Woolly Spider Monkeys or Muriquis genus

Brachyteles (family Atelidae) from SE Brazil are

disputedly the largest among New World monkeys

(adults weighing up to 11-12 kg). It is estimated

that alouattines (howling monkeys) and atelines

(woolly, spider, and woolly spider monkeys) split

about 16 MYA and that the ancestor of Muriquis

( Brachyteles ) and Woolly Monkeys ( Lagothrix )

separated about 10 MYA from the lineage that

would eventually lead to the Spider Monkeys ( Ate -

les). A m azonian LagOthrix and A tlantic Forest Bra-

chyteles are therefore considered to be sister groups

(Mittermeier et a 1 . , 2013). Two species ofMuriquis

are recognized: the Northern Muriqui B. hypox-

anthuS , and the Southern Muriqui B. arachnoides

(Fig. 34). Taxon arachnoides is distributed in SE

Brazil, through the coastal Serra do Mar in the

states of Rio de Janeiro, Sao Paulo, and (the NE

of) Parana. Its northern limits are the Serra da

Mantiqueira and the Rios Paraiba and Paralba do

Sul. Taxon B. hypoxanthus historically ranged

through the Atlantic Forest in the states of Bahia,

Espirito Santo, Minas Gerais, and Rio de Janeiro,

excluding only lowland forests in the extreme S of

Bahia and N Espirito Santo. The northern limit

of its distribution was probably the Rio Jequiriga

or the right bank of the Rio Paraguagu, whereas

the southern limit most likely was the Serra da

Mantiqueira, in S Minas Gerais state. There, it

meets the distribution of the Southern Muriqui

taxon B. arachnoides. Sexual dimorphism is absent

in Muriquis. The Southern Muriqui has a predom-

inantly beige, with light, or dark brown or light

gray-brown colored coat. It retains the black pig-

mentation of the face, palms, and soles of the feet

from infancy into adulthood. Adults of both sexes

develop only minor depigmentation in small pink

or white spots in the pubic region and sometimes

on the face. The Northern Muriqui taxon B. hypOX-

anthliS has a uniformly beige colored pelage, with

light or dark brown or light gray-brown colora-

tion. At birth, the face is black, but at sexual matur-

ity face and genitals lose their pigmentation

and become spotty pink or flesh-colored (Fig.

34). Northern Muriquis have a vestigial thumb,

which character differentiates them from Southern

Muriquis that lack the thumb. The Southern M uriqui

seems to be nearer to archetypic woolly spider mon-

keys than the Northern Muriqui, for the latter is

overall progressively pheomelanin bleached near-

albinotic in the head characters (white eyebrows,

sideburns, and beard), and also in the advanced de-

On the origin of allopatric primate species

163

Brachyieles hypoxanxhus

Brachyreles arachnoides

30 '

Figure 34. Metachromic bleaching in the Woolly Spider Monkey or Muriqui genus

Brachyteles from the Atlantic coast of SE Brazil.

pigmentation of the face, in particular the spotty

flesh- colored muzzle (Mittermeier et al., 2013).

For Amazonian Howling Monkeys, genus Al-

OUCltta, allopatric speciation, radiation, and phylo-

geography along eumelanin and pheomelanin

path ways ofmetachromic bleaching are depicted in

figures 35, 36). Two monophyletic cladistic Groups

or Clades are recognized: AL belzebul and AL

seniculus (M itterm eier et al., 2013). W ithin the Al.

belzebul Clade, distributed south of the Amazon,

saturated eumelanin all-black howling monkeys of

the Amazon Black Howler taxon Al. nigerrima

range between the Tapajos and Madeira Rivers. A

founder-pair or colony of somewhat bleached Al.

nigerrima howlers once must have traversed the

lower Rio Madeira, most likely lifting on floating

logs or on drifting islands covered with chavascal

(low type of varzea) forest. Presently, this howler

also inhabits almost the entire interfluve delineated

by the Rios Amazonas, Purus and Ipixuna, an area

that was formerly occupied by the advanced pheo-

melanin bleached yellowish-orange colored Purus

Red Howler taxon AL pUTUensls (belonging to the

AL seniculus Clade). We have spotted Al. nigerrima

howlers in the varzea near Carreiro (opposite the

city of Manaus) and, also, as far south as the Rios

164

Marc G.M. van Roosmalen & Tomas van Roosmalen

Igapo-Agu and Tupana - black-water rivers that

empty out into the Rio Madeirinha (a white-water

left-bank tributary of the Rio Madeira). It seems

that the overall orange-colored resident howler Al.

puruensis and the all-black invasive Al. nigerrima

howler do co-exist locally. However, the two taxa

do not mix nor interbreed. While conducting a

canoe survey during the peak of the flood season in

the vast igapo floodplain along the Rio Igapo-A<ju

and Igarape Cujubim, we have heard and seen the

two taxa belonging to different Clades (Al. belzeblll

and Al. seniculus, respectively) in the same general

area. The more frugivorous Al. nigerrima howler

was only seen in the middle of seasonally flooded

igapo forest during the peak of fruiting, whereas the

more folivorous puruensis howler stayed back in

the adjacent primary terra firm e rain forest. We

assume that Al. puruensis does so by lack of its

elsewhere preferred habitat - seasonally white-

water inundated floodplain forest (varzea). It there-

fore seems that monkey taxa belonging to different

monophyletic clades locally can co-exist, but only

if they occupy different feeding niches, and within

the local landscape parapatric or partly overlapping

habitats. As these two howler taxa are considered

valid species, they seem to have sufficiently di-

verged from one another to impede interbreeding in

the contact or overlap zone.

Representing the nearest to archetypic taxon of

the Al. belzebul Clade, the range of the Amazon

B lack How ler taxon Al. nigerrima may w ell be con-

sidered the center of the Clade’s dispersion. From

here, the other taxa diverged in eastern direction.

From Al. nigerrima derived east of the Rio Tapajos

the pheomelanin bleached Spix’s Howler Al. dis-

Color. It has an overall dark-brown to mahogany-

AMAZONIAN HOWLERS

ALOUATTA

Alouatta seniculus Clade

o Alouatta (s.) arctoidea

8 Alouatta (s.) seme ulus

Alouatta (s.) maccattnelli

O Alouatta (s.) juara

Alouatta (s.) pitmens is

O Alouatta fs.) sara

Alouatta belzebul Cbde

O Alouatta tb.J nigerrima

Alouatta (b.) discolor

(bj belzebul

(b.) ululata

Figure 35. Distributions, allopatric speciation, radiation, and phylogeography along different pathways

of metachromic bleaching depicted for all known Amazonian Howlers genus Alouatta.

On the origin of allopatric primate species

165

'•4,1 puruenStS

litara

ataoKfea

macconnem

sen k ulus sul>CI:ide

A to not to seme it I us (lade

sum sub- f t ii do

IQ inches

mgettma

discotor

uHiwo

male

uhilata

Fetnale

Atouattn bet zebu l Clade

Figure 36. Metachromic variation, radiation, and phy logeography along eumelanin and pheomelanin pathways of

metachromic bleaching depicted for all known Amazonian Howlers of the Alouatta. SeniculuS and Al. belzeblll C lades .

166

Marc G.M. van Roosmalen & Tomas van Roosmalen

Figure 37.Adultmale Guianan Red Howler AlouattCl mac-

connelli. It was photographed while pulling off a juvenile

that tried to seek protection from the human intruder, some-

where along the black-water Rio Jauaperi, a north-bank

tributary of the Rio N egro (Courtesy of D avid Lem m on ).

red coat and a rufous-chestnut dorsal band, hands,

feet, and tip of the tail. A further pheomelanin

bleached founder- colony of Al. discolov must once

have traversed its eastern distributional limit -

the Rio Xingu, Iriri, or Santa Helena (left-bank

tributary of the Rio Teles-Pires in Mato Grosso).

From Spix’s Howler Al. disColOT derived the dark

brown colored Red-handed Howler Al. belzebul.

This species is progressively pheomelanin bleached

in the reddish-brown to yellow hands, feet, tail tip,

forehead and back. It is distributed south of the

Amazon, east of the Rio Xingu-Iriri, in the states of

Para (including Mexiana, Caviana, and M arajo

Islands in the Amazon estuary), Maranhao,

Tocantins, and Mato Grosso. West of the Atlantic

coast of NE Brazil in the states of Rio Grande do

Norte, Paraiba, Pernambuco, and Alagoas, are

found enclave populations isolated from what is

thought the taxon’s former distribution, which must

have been continuous through the states of Ceara

and Piaui to the Amazonian population. From the

Red-handed Howler Al. belzebul derived the ad-

vanced pheomelanin bleached Maranhao Red-

handed Howler Al. ululdtd. This species distributed

in NE Brazil occurs in remnant forest patches of dry

forest scrub called caatinga. It enters also the

coastal mangrove forests of northern Maranhao,

Piaui, and Ceara. The Maranhao Red-handed

H ow ler Al. ululdta. radiated farthest away from the

archetypic overall black Central Amazon Black

Howler Al. YligewilYlCl. It is sexually dichromatic.

The male is black with rufous to reddish-brown

hands, feet, tip of the tail and flanks. The female is

yellowish-brown with sparse grayish hairs, giving

it an overall olivaceous appearance (Fig. 36).

Within the Al. seniculus Clade we consider the

overall dark reddish-brown Ursine Red Howler

arctoidea from N Venezuela east of Lake Mara-

caibo, and from the coast (including the Islands of

Trinidad and Tobago) extending S thro ugh the

llanos to the Rio Orinoco, the nearest to archetypic

taxon for the m onophyletic Al. seniculus sub -Clade,

which is distributed north of the Amazon. Both

sexes have a coat that is dark reddish-brown on the

body, contrasting with a darker brown to blackish

head, shoulders, limbs, and proximal part of the tail.

Male Ursine Red Howlers often have a blackish

beard, limbs and tail. From a founder-colony that

once traversed the Orinoco River to the east, has de-

rived the advanced pheomelanin bleached Guianan

Red Howler Al. ITICICCOnYielli. This taxon ranges

east of the Rio Orinoco throughout the Guianas, N

Brazil (east of the Rio Negro and north of the Rio

Amazonas, including Guru pa Island in the Amazon

estuary), and S Venezuela (between the Cassiquiare

and Orinoco Rivers). The Guianan Red Howler’s

coat is uniformly dark rufous-brown, the back is

pheomelanin bleached yellowish to golden-brown

with a dark dorsal stripe, and arms to elbows and

legs to thighs are orangish-red . Distal part of the tail

is pale-yellow (Figs. 35, 36).

From a founder-colony of further pheomelanin

bleached Al. macconnelli that once traversed either

the upper Rio Negro in the Colombian Amazon, or

the Orinoco River at its headwaters, has derived the

overall orange-colored Colombian Red Howler Al.

Seniculus. This taxon is now distributed north of the

Amazon across E Ecuador and E Peru (east of the

Rio Huallaga), Colombia, NW Venezuela, and the

Brazilian Amazon inbetween the Rio Solimoes and

Rio Negro. The Colombian Red Howler Al. Sen-

iculus is overall golden-toned to coppery-red on

the body, contrasting with the maroon head,

shoulders, lim bs, and proxim al part of the tail. M ale

Colombian Red Howlers are much bigger than fe-

On the origin of allopatric primate species

167

males. Within the monophyletic Al. SBTliculllS sub-

Clade the bright orange-red Colombian Red Howler

Al. seniculus is phylogeograpically the most ad-

vanced pheomelanin bleached taxon. It radiated the

farthest away from the nearest to archetypic satur-

ated eumelanin, overall dark brown colored Ursine

Red Howler Al. ClfCtoideci, as such fully concurring

with our theory. With respect to the monophyletic

Al. Sara sub-Clade of the Al. SeiliculliS cladistic

Group that is largely distributed south of the

Amazon, we consider the Jurua Red Howler juara

the nearest to archetypic, least eumelanin bleached

(dark brown) taxon. It ranges in the W Brazilian

Amazon south of the Rio Solimdes, and in the

Rio Jurua Basin, extending west into the Peruvian

Amazon. It is not sexually dichromatic. Its coat is

generally dark reddish-brown, with the middle of

the back lighter orange-rufous colored, and limbs

and tail base dark rufous to black. The tail is paler,

more golden from middle to tip. From a pheo-

melanin bleached founder- colony that once tra-

versed the Rio Jurua to the east derived the Purus

Red Howler taxon Al. purueiisis. It is distributed

across the entire Rios Jurua/Purus interfluve as far

east as the middle Rio Madeira. From there, it ex-

tended its range across the upper Rio Aripuana as

far east as the Rio Teles-Pires, and south as far

as the Rio Abuna (which forms Bolivia’s northern

border). The Purus Red Howler Al. puruensis is

sexually dichromatic. Males are dark rufous or red-

brown with a golden upper dorsum and shoulders,

whereas females are golden-orange with distal por-

tions of limbs, tail base, and beard dark rufous.

From a progressively pheomelanin bleached

founder-colony of the Purus Red Howler that

once traversed the Rio Abuna, has derived the quite

distinct Bolivian Red Howler taxon sara. It is dis-

tributed across the Bolivian Amazon including the

entire Rio Beni Basin, and east as far as the Rios

M am ore/G uapore interfluve. The Bolivian Red

Howler’s coat is brick-red above, with limbs, head,

and proximal part of the tail darker, more rufous

colored. It represents the most advanced pheo-

melanin bleached taxon of the Al. Sara sub-Clade

(Fig. 36). It occupies a dead-end distribution in the

south bordering the drier savanna and Chaco area

(Fig. 35). Going further southwards begins the dis-

tribution of the Paraguayan Howler Al. caraya.

For extra-A m azonian Howling Monkeys genus

Alouatta, allopatric speciation, radiation, and phylo-

geography along eumelanin and pheomelanin

pathways of metachromic bleaching are depicted in

figures 38, 39. Four non-Am azonian monophyletic

Clades are recognized: the Brazilian Brown Howler

Al. guariba, the Paraguayan Howler Al. caraya , the

C entral A m eric an M an tied H o w ler Al. palliata, and

the Mexican Black Howler Al. pigra (M it term eier

et al., 2013). The Brown Howler Al. guariba C lade

consists of two populations that may represent dif-

ferent valid taxa or species: the Northern Brown

Howler Al. guariba and the Southern Brown

Howler clamitans. Taxon Al. guariba ranges in the

Atlantic Forest from the Rio Paraguagu, Bahia

State, along the coast south as far as Rio Paraiba in

Rio de Janeiro State. Inland, it extends into Minas

Gerais State. The Southern Brown Howler Al. claiTl-

itans is distributed in the Atlantic Forest south of

Rios Doce and Jequitinhonha, south as far as Rio

Grande do Sul State. Taxon Al. guariba is not sexu-

ally dichromatic and both sexes are red-fawn, with

females usually somewhat duller in color. Taxon Al.

clamitans is generally dark reddish-brown, with

males often being lighter colored than females.

Males from Sao Paulo are orange-red to red-brown

with a red belly, whereas males from Santa Catarina

and Rio Grande do Sul are bright red-orange,

having dark brown feet. Females are overall dark

brown or blackish. The Northern Brown Howler Al.

guariba is the lesser metachromic bleached. Taxon

Al. clamitans derived from it, the males progress-

ively following the pathway of pheomelanin

bleaching. The further south it ranges, the more

the male’s overall coat color tends to red-orange or

bright orange (Fig. 39).

The Paraguayan Howler Al. Caraya forms a

mono ty pic Clade. It is a sister species to the Am azo-

nian red howlers of the Al. seniculus Clade. It di-

verged from a common ancestor about 4 MYA. The

Paraguayan Howler Al. Caraya is distributed across

C Brazil, south of the states of Para, Tocantins,

M aranhao, and Piaui, west into the Pantanal, south

into Paraguay, E and SE Bolivia, and maybe also

into NW Uruguay. Much of its range is in the

‘cerrado’ of central Brazil and semi-arid ‘caatinga’

forest scrub in NE Brazil, where it uses gallery and

riparian forest and patches of seasonal (semi)-

deciduous ‘cerradao’ (a type of savanna forest).

Adults of Al. Caraya are sexually dichromatic,

but both sexes are blond at birth. Mature males are

generally uniformly black. Females and young of

168

Marc G.M. van Roosmalen & Tomas van Roosmalen

either sex are pale grayish-yellow to golden-brown.

Male Paraguayan Howlers AL CCITCiyCl from Bahia

and Goias are black, but those from Mato Grosso

and Parana are black with a brown back and hind

parts. Males from Sao Paulo and Minas Gerais

States are brown-black, with yellowish hands, feet,

belly, and tail tip. In all male individuals the face

is invariably dark, the fur is stiff and lengthy, and

the beard is prominent. The scrotum is rust-red

colored.

The Pacific Coastal and Central American

Mantled Howler Al. pCll licit Cl is, based on geo-

graphic distribution, divided in five taxa that could

well represent distinct valid species: AL palliata

from NE Guatemala, ranging east to E Costa Rica

or W Panama; Al. ClCCJUCltonCllis from the southern

distributional lim its of Al. palliata ranging through

the D arien into W Colombia, W Ecuador, and south

as far as NW Peru; Al. mexicCUia ranging from S to

SE Mexico and Guatemala following the southern-

most distribution of the Central American Black

Howler Al. pigva\ Al. COibensis from Coiba and

Jicaron Islands in SW Panama; and AL trabeata

from the Azuero Peninsula in SW Panama (Fig. 38).

The coat of the Mantled Howler is smooth, very

short and upright, being silky black with a mantle

of longer, gold or yellowish-brown fur along the

flanks. Adult males have a white scrotum.

The Central American Black Howler AL pigTCl

is monotypic. It is distributed across SE Mexico,

Belize, and N to C Guatemala. Fur of AL pigTCl is

notably long, soft, and dense. Adults are not sexu-

ally dichromatic. They are overall black with traces

of brown on the shoulders, cheeks, and back. The

EXTRA AMAZONIAN HOWLERS

ALOUATTA

Ala it alia pigra Clatle

< Alouatta pigra

Alouatta palliata Clade

Alouatta (p.J mexicana

Alouatta (p.) palliata

Alouatta (p.) aequatorialis

Alouatta (p.) trabeata

Alouatta (p i eoihemh

Alouatta caraya CJade

Alouatta caraya

Alouatta guariba Clad c

jt — Q Alouatta (g.) guariba

'f Alouatta (g.) clamitam

A jJifTc

,4. p- acbtctu

A p pillmtc

A etrtfe

A f.

A l tUrnimw

Figure 38. Distributions, allopatric speciation, radiation, and pathways of metachromic bleaching followed in all extra-

Amazon ian Howling Monkeys genus AloUClttCl. Two Clades occur south of the Amazon: Al. gUCiribci from the E Brazilian

A tlan tic forest, and Al. CCLTUyCl from the ‘cerrado ’ and ‘cerradao ’ of the Central Brazilian Plateau. Along the Pacific coast of

Ecuador and Colombia, far into Central America, occur the Al. pcillicitci and Al. pigra Clades.

On the origin of allopatric primate species

169

Figure 39. Pelage color variation, radiation and metachromic bleaching along eum elan in and pheomelanin pathways depicted

for all extra- A m azo nian Howling Monkeys genus AloilClttCl of the Brazilian Al. guaviba, and Al. CCIVCiyCl C lades, and the

C entral-A m erican Al. pigra and Al. palliata Clades.

170

Marc G.M. van Roosmalen & Tomas van Roosmalen

CentralAmerican Black Howler Al. pigra is consi-

dered the most saturated eumelanin, least bleached,

nearest to archetypic form of the Al. pigra and Al.

palliata Clades. It is also by far the largest how ling

m onkey. The Al. palliata C lade is believed to have

diverged from ancestral Al. pigra about 3 MYA

(Mittermeier et al., 2013). Taxon Al. palliata is

sympatric with taxon Al. pigra in Tabasco State,

Mexico and in a small part of Guatemala. From the

Golden-mantled Howler Al. palliata radiating

northwards derived the Mexican Howler A/, mexi-

Cana , and radiating southwards the South Pacific

Blackish Howler Al. aequatorialis, ranging far

south into the Pacific coastal forests of Colombia

and Ecuador. There, it is sympatric with the Colom-

bian Red Howler Al. seniculus. From Al. aequatO-

rialis in SW Panama derived the Azuero Peninsula

Howler Al. trabeata and the Coiba Island Howler

Al. coibensis (Fig. 3 8).

During his long-term fieldwork on the ecology

of all eight monkey species that occur in the

Guianas, the senior author has repeatedly watched

the basic principles of allopatric primate speciation

atwork.Athis study site situated in pristine prim ary

terra firm e rain forest in Central Suriname, local

populations of the Guianan Red Howler Al. UiaC-

connelli (Fig. 37), the most territorial among all

extant howling monkeys when measured by the size

of the hyoid bone, had passed beyond the howler’s

optimal densities (Van Roosmalen, 2013a; 2015).

This was measured by the high frequency of dawn

chorus and vocal battles of neighboring groups

throughout the day and nighttime in the proximity

of territorial boundaries. One day, a subadult male

got pushed out of his parental group that ranged

close to the campsite area. For several days after

being expelled, this young howler male got repe-

atedly involved in vocal battles with neighboring

groups that subsequently chased him out of their

respective territories. Weeks later, far away from the

campsite, a boundary conflict took place that

seemed never ending. The researcher rushed over

to the spot. He arrived just in time to witness this

very subadult male being attacked by the leader of

a resident group in the company of his harem. The

whole group chased the young male into an isolated

tree close to where he could watch the scene. The

subadult male was in the company of a female he

presumably had attracted (‘stolen’) from some re-

sident group that had chased him out earlier. In an

attempt to escape from his attackers, the howler

male almost fell out of the canopy. He just could

get hold on a thick branch and was hanging under-

neath it only secured by the grip of his hands and

tail. Then, they all began to bite in his hands and

tail tip. With a scream, he let loose and came

crashing over forty meters down to the forest floor,

hitting it at a hair width away from the researcher’s

head. The monkey looked dead, his motionless

body covered with blood. After a few minutes,

however, he got back on his feet and slowly clim-

bed up a small tree. Back in the canopy, he sat next

to his mate that had been watching the show from a

distance. The pair was never seen again within the

borders of the 400-ha study area. Some time later,

vocal battling recommenced. It came from the same

direction, sounding only much farther away. In

retrospect, we assume that the couple survived and

in the long run found a place to settle down, start a

family, and defend a small territory squeezed inbe-

tween the territories of some resident howler groups

far away from their respective parental groups. One

may speculate that the howler pair, driven by the

trend to allopatry, also may have survived by ven-

turing into some ‘empty’, marginal, or for howlers

unfamiliar habitat. Or, in case the male was expel-

led from his parental group for his skin or (part of)

coat color being somewhat lighter, he could have

joined other outcast males that were discriminated

upon and pushed out of their parental groups for

other mutant metachromic deviances of skin and/or

coat characters. For the sake of survival alone, such

healthy young individuals may join efforts to stay

alive. Together, they may turn into potential foun-

der-colonies venturing into new lands, where they

can thrive and reproduce unrestrictedly. At least as

long as those lands, in turn, do not reach the taxon’s

optimal population density. By the time they do so,

the generally accepted phenotype of that new para-

patric or allopatric taxon or (eco)-species will have

been stabilized while showing whatever features of

further metachromic bleaching and/or depilation.

Fiving on an island in the Coppename River at

about ten km from his field site, the senior author

has repeatedly witnessed the coming and going of

small groups of potential howler-founders to and

fro Foengoe Island after having been forcefully pu-

shed out from some mainland territory by the ruling

group male(s). Pushed against the riverbank, they

apparently did overcome their natural fear of water

On the origin of allopatric primate species

171

and then swam toward the island. For some time,

such immigrants tried to make a living on the

island. Until it became clear to them they were

trapped on an island too small to sustain a howler

group year-round. Occasionally, such groups were

spotted later while ranging along the opposite river-

bank. We assume they had traversed the river swim-

ming. Interestingly, a female howler that was raised

as a pet and then set free to range across the 30-ha

island, was eager to join any howlers coming onto

the island. Sadly, when the immigrants eventually

swam back to the mainland in search of new lands,

the female stayed back on the island. Perhaps, she

did so for lack of sufficient bonding or for fear of

swimming across the river.

Capuchin Monkeys (genera CebllS and Sapajus )

have diverged from Squirrel Monkeys (Saimiri)

about 15 M YA. They form ed distinct monophyletic

Clades that diverged during the Late Miocene to

Early Pliocene, about 6.2 MYA. The Clades diver-

sified during the Plio-Pleistocene era into two

groups: Gracile or Untufted Capuchins (genus

CebliS ) in what is today the western Amazon, about

2.1 MYA, and Robust or Tufted Capuchins (genus

SapajllS ) in what are today SE Brazil, E Paraguay,

and N Argentina, beginning about 2.7 MYA (M it-

termeier et al., 2013). Gracile Capuchins genus

CebllS are separated into the following five cladi-

stics Groups or Clades: Humboldt’s White-fronted

Capuchin Ce. albifrons with four+ taxa ( Ce . albi-

frons, Ce. yuracus, Ce. unicolor, and Ce. cuscinus ),

G uianan Weeper C apuchin Ce. olivaceus w ith three

taxa (Ce. brunneus, Ce. olivaceus, and Ce. casta-

neuS), White-faced Capuchin capucinus with two

taxa (Colombian White-faced Capuchin Ce. Cdpu-

dnus and Panamanian White-faced Capuchin Ce.

GRACILE CAPUCHINS

CEB VS

Cebus capucinus Clade

Cebus imitator

• Cebus capucinus

Cebus albifrons Clade

• Cebus albifrons

0 Cebus yuracus

• Cebus unicolor

Cebus cuscittus

Cebus aequatorialis

Cebus versicolor CLade

0Cebus malitiosus

Cebus cesarae

Cebus versicolor

0 Cebus leucocephalus

Cebus olivaceus Clade

Cebus brunneus

Cebus olivaceus

0Cebu s castaneus

lU/TmiClX Cebus kaapori

(

V \

Figure 40. D is tribu tio ns, allopatric speciation, radiation, and pa th ways of metachromic bleaching in all hitherto recognized

Gracile Capuchins of the five distinguished phy logeographic Clades: CebllS CCLpUCiflUS, C. olivaCCUS, C. Versicolor, and C.

albifrons. The fifth Clade C. aequatoriaUs is monotypic.

172

Marc G.M. van Roosmalen & Tomas van Roosmalen

GK WILE CAPl CHINS GEM'S CEBL S

10 inches

matitiosus

cesaree

leucocophaUis

Figure 41. Metachromic diversification along eumelanin and pheomelanin pathways of metachromic bleaching (arrowed

lines), speciation and radiation in all hitherto recognized Gracile Capuchins (CebuS) of the five distinguished phylogeo-

graphic c lades: Cebus olivaceus, C. versicolor, Cebus capucinus, and C. albifrons. Cebus aequatorialis from w Ecuador

and NW Peru is monotypic, but may have derived from ancestral C. yUVCLCUS that once traversed the Andes Mts.

On the origin of allopatric primate species

173

imitator), and Varied W hite- fronted Capuchin Ce.

versicolor with four taxa (Ce. versicolor, Ce. leu-

cocephalus, Ce. cesarae, and Ce. malitiosus). The

recently discovered Ka’apor Capuchin Ce. kaapori

ranging S of the lower Rio Amazonas is geo-

graphically closest related to the Guianan Weeper

Capuchin (i.e., taxon Ce. COStaneuS ranging along

the left/north bank of the lower Rio Amazonas)

and, therefore, may form a sister Clade to it (Figs.

40, 41).

Within the Ce. capucinus Clade we consider

the Colombian White-faced taxon Ce. capucinus

(ranging from E Panama, through W Colombia

south as far as NW Ecuador), the nearest to arche-

typic, least metachromic bleached form. Its body,

crown, limbs, and tail are black. The chest is white,

extending forward to the face and front of the crown

and upward to the shoulders and upper arms. The

Gorgona White-faced Capuchin Ce. CUTtUS CUrtUS

is a small and relatively short-tailed subspecies

from Gorgona Island sitting on the Colombian

Pacific coast. From taxon Ce. Capucinus derived

Ce. imitator, the taxon that ranges from N Hon-

duras, C and W Nicaragua, Costa Rica south

into W Panama. It resembles much the typical

Colombian White-faced Capuchin Ce. CapudnuS,

but females have elongated frontal tufts with a

brow nish tinge.

Within the Ce. olivaceUS Clade we consider the

Venezuelan Brown Capuchin Ce. brumWUS fro m N

Venezuela east of the Sierra de Perija and along the

Coastal Range, including the island of Trinidad

(where it is possibly introduced), the nearest to ar-

chetypic, least metachromic bleached form. Its pel-

age is thick and long, the upperparts are generally

darker along the middle of the back than on the

sides, the hairs are dusky basally, with a broad zone

of chestnut in the middle, and black at the tips. Face

and sides of the head are pale yellowish gray. The

crown has a broad V-shaped patch of long hairs,

narrowing to a point in front of which a narrow

black line runs forward to the nose. Chin and lower

parts of cheeks are grayish or fulvous white to

whitish. Underparts are blackish brown, with tips

of the hairs hazel. The throat is lighter than the chest

and belly. Upper arms are maize yellow. Outer

forearms are blackish with yellowish tips, inside

forearms are much darker. Hands are blackish,

hindfeet are nearly black. Tail is colored as back.

From ancestral Ce. brunneUS derived the Guianan

W eeper C apuchin Ce. olivaceUS that is restricted to

the Venezuelan Amazon Basin in forests of the Gu-

ayanan Shield, from the upper Rio Orinoco east to

the left bank of the Rio Essequibo in W Guyana. Its

pelage is overall dark brown or reddish with black-

agouti banding on flanks, limbs, and tail. The face

is naked and pink. Cheeks are buffy-white. It differs

from Ce. brunneUS in the advanced bleached alb i-

notic head and upper arms and the wider V-shaped

black crow n cap .

From ancestral Ce. olivaceUS derived the Chest-

nut Weeper Capuchin Ce. COStaneuS. This taxon

ranges from the Rio Essequibo E through Suriname

and French Guiana into N Brazil, where its distri-

bution is delineated by the Rios Negro, Branco, and

Catrimani in the W, Rio Amazonas in the S, and the

Atlantic coast in the E (it also inhabits Caviana and

Mexiana Islands in Amazon’s estuary). It differs

from Ce. olivaceUS in the narrower black triangle

on the crown and the pelage of the head being ove-

rall yellowish-white, but reddish-chestnut above the

ear and nape, in the advanced pheomelanin ble-

ached reddish-chestnut upperparts of the body and

limbs, and pale yellow shoulders and fronts of arms

above the elbows.A founder-colony of the Chestnut

Weeper Capuchin Ce. ( olivaceUS ) COStaneuS must

once have traversed the lower Rio Amazonas. From

it derived the Ka’apor Capuchin Ce. kaapori that

ranges in NE Brazil south of the lower Amazon

River (NE Para and NW Maranhao). This taxon is

characterized by a longer body in comparison to

other Cebus species. It is grayish agouti-brown, and

lighter on the flanks. Face, shoulders, mantle, and

tail tip are silvery-gray, the limbs are agouti, and the

hands and feet dark brown or black. The crown has

a triangular black cap that extends to a dark stripe

down the nose. The pelage of the Ka’apor Capuchin

is overall advanced eumelanin bleached to nearly

albinotic, as such much contrasting with the satu-

rated eumelanin blackish crown cap, hands and feet.

Being phylogeographically farthest radiated away

from the center of dispersion (NW Venezuela) of

the Ce. olivaceUS Clade, and occupying a dead-end

distribution, where it also has to compete with the

Guianan Brown Capuchin Sapajus apella (Figs.

42-44), Ce. kaapori is clearly the most progressi-

vely bleached, near-albinotic taxon within the Ce.

olivaceUS Clade (Fig. 41).

W ithin the Ce. Versicolor C lade w e consider the

Varied White-fronted Capuchin Ce. Versicolor the

174

Marc G.M. van Roosmalen & Tomas van Roosmalen

ALL ROBUST CAPUCHIN MONKEYS

SAPAJUS

Sapajus ape l In ( lade

# Sapajus a pel la

O Sapajus apella margaritae

Sapajus macrocephalus Clade

Sapajus macrocephalus 4 ssp,

Sapajus nigritus Clade

# Sapajus nigritus + cucullatus

Sapajus cay

# Sapajus libidi nosns

Sapajus robust us

Sapajus xa n thostern os

Sapajus flavins

Figure 42. Phylogeography, allopatric speciation, radiation, and pathways of metachromic bleaching followed in all hitherto

recognized Robust (Tufted) Capuchins of the three distinguished phylogenetic Clades: Sapajus IligritUS, S. apella , and S.

macrocephalus. From an ancestral saturated eumelanin (all-black) form of the S. nigritUS Clade , quite recently (an estimated

400,000 YA) radiated away into the Amazon the pheo melanin bleached species S. apella (including the insular taxon S. a.

margaritae ), and S. macrocephalus , the latter with four different taxa/’species-in-the-m aking' - from SE to N: juruaUUS,

pallidus, maranonis, and fatuellus).

nearest to archetypic, least metachromic bleached

taxon. It is distributed in N Colombia in the middle

Rio Magdalena Basin. It is the darkest among the

Clade’s four taxa, though a rather pale form with

red tones on the mid-dorsal region and foreparts of

the limbs, generally contrasting with the rest of

the body (Fig. 4 1). From Ce. Versicolor derived

towards the NE the Sierra de Perija White-fronted

Capuchin Ce. leUCOCephaluS that ranges in N Co-

lombia from the W slope of the Cordillera Oriental

E to the Rios Zulia and Catatumbo Basins and NW

Venezuela (Zulia State). This taxon is progressively

bleached, near-albinotic in the head, chest, and

shoulder parts. From Ce. Versicolor derived towards

the N first the Rio Cesar White-fronted Capuchin

Ce. cesarae, ranging in N Colombia, in the Rio

Cesar Valley, W into the S and E slopes of the Sierra

Nevada de Santa Marta. From taxon Ce. cesarae,

On the origin of allopatric primate species

175

ROBUST CAPUCHINS SAPAJUS

Figure 43. Radiation and metachromic diversification in the Sapajus nigritUS and S. Cipellci Clades of Robust or Tufted

Capuchins. From an ancestral saturated eumelanin form of S. nigritUS the species Sapajus apella and S. maCWCephalllS

radiated away into the Amazon with different taxa ‘in -the-m aking ’ .

176

Marc G.M. van Roosmalen & Tomas van Roosmalen

in turn, derived the Santa Marta White-fronted

Capuchin Ce. lYialitioSUS that is only known from

the NW base of Sierra de Santa Marta. It may range

also throughout the lower W and N slopes of the

Sierra Nevada in N Colombia. The two taxa are the

palest among the N Colombian and Venezuelan

White-fronted Capuchins. Taxon Ce. cesarae is

buffy in the head and throat parts and pheomelanin

bleached orangish in the cap, middle of the back,

forearms, and forelegs, as such contrasting with the

sides of back and trunk. Taxon Ce. malitioSUS is

advanced eumelanin bleached in the silvery to cin-

namon-brown chest and belly, and a contrasting al-

binotic area of the front extending well over the

upper surfaces of the shoulders and inner sides of

upper arms (Fig. 41).

Within the Ce. albifrons Clad e we consider the

M aranon W hite-fronted Capuchin Ce. yurCICUS the

nearest to archetypic, overall least metachromic

bleached taxon (Fig. 41). This taxon is distributed

north of the Amazon River in S Colombia, E

Ecuador, NE Peru, and presumably W Brazil

between the Rios Iga and Solimoes. It is gray-

fronted on the forehead, sides of the face, chest,

and outer sides of the arms. Its general color is

ochreous-brow n, contrasting sharply with the gray-

ish to buffy outer sides of forelimbs, and with the

pale silvery to orangish underparts. The cap is

black, with a median line running down inbetween

the eyes. The tail is brown like the back, but paler

tow ards the tip. From ancestral Ce. yUTCICUS derived

first Humboldt’s W hite-fronted Capuchin, the nom-

inate taxon Ce. albifrons that is widely distributed

across the upper Amazon Basin of S Venezuela, S

and E Colombia (occurring north of the Rio Amazo-

nas and the Rio Iga-Putum ayo, N as far as the Rio

Meta, and in the lowlands W of the Orinoco, and

NW Brazil (N of the Rio Solimoes, and W of the

Rios Negro and Branco, as far north as the Rio Ur-

aricoeira). Hum bold t’s W hite-fronted Capuchin Ce.

albifrons is overall pale grayish-brown, darker on

the limbs. Hands and feet are yellowish-brown. The

tail is ashy above, whitish below, and brownish-

black towards the tip. The front is creamy white,

and there is a cap of short dark fur on the crown that

is rounded in the front and well demarcated from

the light-colored forehead. The face is naked and

pinkish, flesh-colored. From Ce. yuraCUS derived

also Spix’s White- fronted Capuchin Ce. Unicolor,

most likely after a founder-colony of ancestral Ce.

yuraCUS traversed the upper reaches of the Rio

Ucayali in E Peru. It is nowadays widely distributed

in the upper Brazilian Amazon Basin, south of the

A m azon River and w est of the Rio Tapajos, through-

out the northern parts of Mato Grosso and Rondo-

nia States, and throughout the Rios M adeira, Purus,

Jurua, and Javari Basins as far west as the

Rio Ucayali. CebliS Ullicolor is uniformly bright

ochreous or grayish-brown with darker grayish-

brown flanks and mid-back, with a yellowish or

cream-white front and reddish-yellow to reddish

limbs and tail. From ancestral Ce. linicolor deriv ed

later the Shock-headed Capuchin Ce. CUSCiniiS that

is believed to range from the right bank of the upper

reaches of the Rio Purus in SE Peru, W into the

Cuzco Department including the upper Rio M adre

de Dios, and S and E as far as the Rio Tambopata

Basin, also extending into NW Bolivia. Taxon Ce.

CUSCinus has a longer, silkier fur than Ce. linicolor

and is less brightly colored. Its limbs are browner

and contrast less with the back. The cap is large,

distinct, and dark brown. The forearms are orange-

rufous on the outside, darker on the wrists and

hands. Underparts are ochreous- orange and silvery,

becoming buff on the chest. The fronts of the

shoulders and inner sides of the upper arms are

whitish. The tail is brown, somewhat paler towards

the tip. The male has a broad pale frontal region

sharply defining the dark-brown cap. Overall,

Ce. CUSCiniiS is the most advanced pheomelanin

bleached taxon of the Ce. albifrons Clade. It is the

form that radiated away farthest from the center of

this Clade’s dispersion (Fig. 40). The Ecuadorian

White-fronted Capuchin Ce. aequatorialis is mono-

typic. It may form a sister Clade to the Gracile

Capuchins from the upper Amazon B asin . A ncestral

M aranon W hite-fronted Capuchin Ce. yuraCUS once

must have traversed the Andes Mountains some-

where at the upper reaches of the Rio M aranon and

then diverged into Ce. aequatorialis. Cebus aequat-

orialis is distributed in Ecuador and NW Peru, in

the lowlands west of the Andes (Fig. 34). Its upper-

parts are pale cinnamon rufous, darker along the

midline of the back. Front and sides of the head are

yellowish white, with a narrow black transverse line

on the forehead forming the cap, from which a

narrow median black line descends to the nose.

Hands and feet are a little darker, more brownish

than the arms and legs. The chest is lighter than the

belly (Fig. 41).

On the origin of allopatric primate species

111

During long-term fieldwork in Central Suri-

name, the first author spotted a few times by chance

small parties consisting of phenoty pically deviant

cream-white, long-haired, fluffy-coated males

of the Guianan Weeper Capuchin Ce. ( olivaceus )

castaneus. Such all-male parties seemed to range

randomly while travelling at high speed through the

vast landscape of pristine matrix lowland rain forest

in the middle of which his study area was situated.

It is located at more than one-hundred km north of

Kaiser Mountains, a hilly country of which the foot-

hills seem to form the Guianan Weeper Capuchin’s

core distribution. This region that provides this

monkey with its preferred habitat - ‘mountain

savanna forest’- was found to sustain a very large

population of this elsewhere in the Guianas ex-

tremely rare taxon Ce. ( olivaceus ) castcmeus.

Mountain savanna forest is typified by an under-

story that is dominated by the majestic ‘bergi-

maripa’ palm Attalea speciosa Mart. (Arecales

A recaceae). A bove 400 m altitude, this palm tree is

locally so abundant that one gets the impression to

walk through a monocultural plantation of the

African oil-palm Elaeis guineensis Jacq . (Arecales

Arecaceae). The large fruits of Attalea speciosa

constitute the Guianan Weeper Capuchin’s principal

daily food throughout most of the year. Mountain

savanna forest above 400 m altitude, therefore, may

function as a ‘keystone habitat’ to the Guianan

Weeper Capuchin, hence the high population density.

Two decades later, while conducting biod-

iversity surveys in Pico da Neblina National Park

situated in the extreme northwestern corner of the

Brazilian Amazon, the authors spotted a population

of near-albinotic Weeper Capuchins that were

characterized by a very dense, fluffy, overall long-

haired, cream-white bleached fur. Their coat fea-

tures looked very similar to that of the all-male

parties that were seen sporadically passing through

the Voltzberg study area. The Pico da Neblina

population of weeper capuchins was spotted in a

low type of cloud forest scrub that grows at high

altitudes of 2,000 to 2,500 m. To the astonishment

of the researchers, the capuchins were seen spend-

ing part of the daytime on the ground in the middle

of open tepui (sandstone table-mountain) ‘rock

savanna’. They were seen foraging for inverteb-

rates, mostly snails, other organisms endemic to

tepui mountain tops, in addition to vegetable matter

(e.g., roots, tubers and pseudobulbs of all sorts of

terrestrial bromeliads and orchids). In retrospect,

our sighting may be explained for as follows. In the

past, a founder-colony of near-albinotic Guianan

Weeper Capuchins, driven by the ‘trend to allo-

patry’ out of the center of dispersion of archetypic

Ce. ( olivaceus ) castaneus, may have traversed the

upper Rio Branco and then reached the Pico da

Neblina area. The latter is situated somewhat south

of the Rio Cassiquiare, the channel that runs

through the watershed connecting the basin of the

Rio Negro with that of the Rio Orinoco. The fully

bleached euchromic, long-haired, soft-coated

weeper capuchins that were seen foraging in tepui

cloud forest and open rock-savanna at 500-1,000

m below the 3, 004 m Pico da Neblina summitmuch

resembled the near-albinotic, fluffy-coated Ce.

( olivaceus ) castaneus from Kaiser Mountains,

Central Suriname. If the Pico da Neblina population

turns out to represent a new taxon or one in-the-

making, the ‘Neblina Weeper Capuchin’ would

occupy a dead-end distribution in the southwestern-

most corner of the Ce. olivaceus Clade’s range,

the farthest away from the supposed center of

the Clade’s dispersion (the Guianas or Venezuelan

Coastal Range). The upper Rio Negro forms the di-

vision between the distributions of the Guianan

Weeper Capuchin Ce. olivaceus Clade and the

Humboldt’s White-fronted Capuchin Ce. albiffflUS

Clade (Fig. 39). This example from the field is in

line with our theory of allopatric speciation in male-

defended territorial primates such as CebuS. The

‘Neblina Weeper Capuchin’ may have radiated

away from the Ce. olivaceus Clade’s center of

dispersion in the Guianas following a pathway of

metachromic bleaching driven by the trend to allo-

patry in phenotypically deviant euchromic, long and

flu ffy -h aired males. Interestingly, the mechanism

of allopatric speciation and radiation of a mono-

phyletic clade of monkeys like that of Humboldt’s

Weeper Capuchins at first sight seems non-ad-

aptive, at least in strict Darwinian sense, for it is

solely based on discriminatory behavior performed

exclusively by high-ranking males. The genes for

warm, long and flu ffy -h aired coats are simply

retained in the genes of these capuchin ‘founder-

colonies’. Such a feature would therefore not a

priori be the result of adaptive processes of natural

selection. Its warm coat only secondarily happened

to have survival value. It only turned adaptive when

these gracile capuchins had to adapt in a short

178

Marc G.M. van Roosmalen & Tomas van Roosmalen

period of time to a new habitat or feeding niche that

would not have suited the species they derived

from. Following this rational, one may speculate

about a similar metachromic pathway that our hom-

inid ancestors about 6 MYA must have followed

when exchanging the canopy of tropical rain forest

for a landscape of arid, open savanna scrub. Or a

similar path way ofmetachromic bleaching towards

albinotic (from a black to yellow or white skin

color) and/or depilation of the body that different

hominids followed between 100,000 and 50,000

years ago, when the trend to allopatry (male dis-

criminatory behavior) forced them to leave the

center of hominid dispersion and the cradle of

hominid evolution - C and N Africa - to make a

harsh living of nomadic big-game hunting/gath-

ering in (for hominids) clime - and habitat - wise

new, marginal, unsuitable, or inhospitable land-

scapes of Central Europe, the Middle-East and

SEA sia.

Capuchin Monkeys of the genera CebllS and

SapajuS formed distinct monophyletic Clades that

diverged during the Late Miocene to Early Plio-

cene, about 6.2 MYA. During the Plio-Pleistocene

era the Clades diversified into two groups: Gracile

or Untufted Capuchins genus CebllS, about 2.1

MYA in what is nowadays the western Amazon, and

Robust or Tufted Capuchins genus ScipCljllS, begin-

ning about 2.7 MYA in what are today SE Brazil, E

Paraguay, and N Argentina. There is strong evid-

ence from molecular genetic studies that Robust

Capuchins (genus SapajuS) spent most of their evol-

utionary history in the Atlantic Forest of SE Brazil,

NE Argentina, and E Paraguay.And that the current

wide-ranging sympatry of Robust and Gracile

Capuchins across the larger part of the Amazon

Basin is the result of a single, rapid, Late-Pleisto-

cene invasion of Robust Capuchins from the At-

lantic Forest, first into the ‘Cerrado’ and ‘Cerradao’

of C and NE Brazil, and only recently (about 0.4

MYA) from central South America north into the

Amazon Basin and the Guianas (M it term eier et al.,

2013). Though widespread throughout the Amazon

Basin and the Guayanan Shield, the genetic differ-

entiation of the Amazonian Robust Capuchins is

limited. The fact that the phenotypic diversity of the

Amazonian Robust Capuchins is not mirrored by a

corresponding genetic diversity strongly supports

our theory of allopatric prim ate speciation.A num-

ber of the 16 taxa that are overall recognized in

different taxonomic arrangements (e.g., Groves,

200 1 a; Silva Jr., 2001; Silva Jr., 2002) may well

represent taxa ‘in-the-m aking ’ . Here, we follow

Silva Jr. (200 1) in recognizing only two species: the

Guianan Brown Capuchin Sap. apella with three

subspecies distributed in the eastern Amazon and

the Guianas, and the Large-headed Capuchin Sap.

macrocephalus with four subspecies that are dis-

tributed across the western Amazon. These taxa

form two monophyletic Clades in which little

genetic differentiation is shown. In contrast, the

non- Amazonian species recognized by Silva Jr. are

genetically distinct forming the monophyletic Sap.

TligritliS Clade (Figs. 39, 40). Among the six species

of the extra-A m azonian Sap. YligvitUS Clade we

consider the Black-horned Capuchin Sap. nigvitUS

the nearest to archetypic, less bleached species

(Figs. 42, 43). Its southernmost populations repres-

enting the darkest, overall m ost saturated eum elan in

form may well be a distinct taxon named Sap.

CUCullatUS by Spix in 1 823. The Black-horned

Capuchin is the most S occurring of all robust

capuchins. It is distributed in SE Brazil, S of the

Rios Doce and Grande, extending S through the

Atlantic Forest, and taxon Sap. CUCullatUS further

south E of the Rio Parana into Rio Grande do

Sul State and NE Argentina. The Black-horned

Capuchin is a large-sized species with horn-like

tufts on either side of the head at the temples. Its fur

is overall very dark brown or grayish in nigritus,

and black in Sap. CUCullatUS, often with slightly

pheomelanin bleached, reddish or yellow-fawn

colored underparts. A black to dark-grayish crown

(with tufts in adults) contrasts much with the light

colored face. The tail is black. From Sap. nigritUS

derived the monotypic Crested Capuchin Sap. TO-

bliStUS after a founder-colony of Sap. lligritUS tra-

versed the Rio Doce to the north. It is distributed

in SE Brazil from the Rio Jequitinhonha in Bahia

State S to the Rios Doce and Suagui Grande in Es-

pirito Santo State and E Minas Gerais State, E of

the Serra do Espinhago. This taxon is very dark

wood-brown or blackish above and on the limbs,

with a faint dorsal stripe. The underparts are pheo-

melanin bleached red or yellowish, whereas fore-

arms, hands, lower legs, and feet are deep dark

brown to black. Its face is dark grayish, with some

white hairs on the forehead and temples. The crown

tufts are tall and conical in shape. From a founder-

colony of the northern Black-horned Capuchin Sap.

On the origin of allopatric primate species

179

nigritUS that once traversed the Rio Jequitinhonha

to the north, derived the Yellow -breasted Capuchin

Sap. xanthoSterUOS. Yellow -breasted Capuchins

tend to be much darker in overall color in the

southwestern part (N Minas Gerais State), whereas

they are pale in the northern part of this taxon’s dis-

tribution. The monotypic taxon Sap . XaYlthoSteVYlOS

is further distributed in CE Brazil, S and E of the

Rio Sao Francisco, south to the Rio Jequitinhonha

(in S Bahia State). It is generally pheomelanin

bleached brindled reddish above with a sharply

marked, golden-red underside. Tail and limbs re-

mained saturated eumelanin black. Its crown does

not contrast with the body, the cap is black, and

the face and temples are fawn. It has small back-

ward pointing tufts. From Yellow -breasted Sap.

XanthoSterUOS derived the monotypic Blond

Capuchin Sap. flavius, which was described by

Schreber in 1774. Until it was collected in 2005, the

Blond Capuchin was only known from an early

illustration. Before colonial times, it must have been

distributed in CoastalNE Brazil from S Rio Grande

do Norte State through Paraiba State into NE

Pernambuco. This taxon may extend its range to the

left bank of the Rio Sao Francisco in Alagoas State.

The Blond Capuchin is small, distinctive, and

untufted. Its body and limbs are uniformly ad-

vanced pheomelanin bleached g old en -y ello w ,

whereas its lower-body parts are slightly darker

golden-yellow. Hands and feet are black, whereas

the tail is uniformly golden-blond, but darker on the

dorsal side than the rest of the body. It further has a

rectangular snow-white cap on the front of the head,

to just above the ears, and a furless, pendulous

throat flap. Face and forehead are near-albinotic,

cream to pinkish colored, the eyes are brown.

SapajliS flaviliS occupies degraded CoastalAtlantic

Forest and Montrichardia linifera (Arruda) Schott

(Araceae) swamp in Pernambuco State, and

‘caatinga’ scrub in W Rio Grande do Norte State.

Being advanced pheomelanin bleached to near-

albinotic, taxon flavius occupies a dead-end distri-

bution. It therefore fully concurs with our theory on

the origin of allopatric speciation. The theory

suggests that a founder-colony of progressively

pheomelanin bleached Sap. XaYlthoSteVYlOS o nee was

forced to make a living in the (for Robust Capuchins)

marginal or unsuitable habitat of swamps and low

xerophytic, spiny scrub of profusely branched

bushy vegetation up to 8-10 m in height, mixed

with prickly succulent cacti, and spiny, rigid-leaved

bromeliads. Blond Capuchins are reported to use

even sand dunes and mangroves.

From the northern form of the Black-horned

Capuchin derived to the W the Hooded Capuchin

Sap. cay, and to the N the Bearded Capuchin Sap.

UbidinOSUS (Fig. 42). The monotypic taxon cay is

distributed in SE Bolivia, N Argentina, SW Brazil

- W of the Rio Parana through Mato Grosso State

into SW Goias and Mato Grosso do Sul - and

Paraguay (E of the Rio Paraguay as far as the Rio

Parana). The Hooded Capuchin Sap. cay is a small,

short- limbed species without sexual dimorphism,

typified mainly by its prominent dark dorsal stripe.

SapajliS Cay is very variable in color, but generally

rather pale. Its crown is pale to blackish -brow n ,

with two small hornlike tufts. Dorsal parts of the

body (shoulders, front of the upper arms, saddle,

rump, and thighs) are gray ish -b ro w n . Forearms,

hands, wrists, lower legs, and feet are blackish.

Eyes, nose, and mouth are surrounded by white

hairs. It has a small white beard, and a dark line

extends down from the ears to under the chin. From

the Black-horned Capuchin derived to the north the

monotypic Bearded Capuchin Sap. UbidinOSUS. This

taxon is distributed in C and NE Brazil, W and N

of the Rio Sao Francisco into Maranhao State, and

in the W of Piaui State, and E to C Rio Grande

do Norte, NW Paraiba, W Pernambuco, and W

Alagoas; to the W it extends to the Rio Araguaia,

and its southern limit is the north bank of the Rio

Grande in Minas Gerais. To the west, the Bearded

Capuchin taxon Sap. UbidinOSUS is replaced by Sap.

apella, to the east by Sap. flavius, and to the south

of the Rio Sao Francisco by Sap. Xanthostevnos .

SapajliS nigritUS occurs just south of the Rio

Grande. Some hybridization between Sap. Ubidi-

UOSUS and Sap. nigritUS is reported to occur in

the western part of Minas Gerais. The Bearded

Capuchin Sap. UbidinOSUS is comparatively small

and does not show sexual dimorphism. It differs

from all other Robust Capuchins by the rusty-red

hair on the back of the neck, the dark-brown preau-

ricular stripe running down the side of the face in

front of the ears, and the orange-yellow throat and

dorsal parts of the body, flanks, outer part of arms,

and proximal two-thirds of the tail. Forearms are

dark, and the lower back and outer surface of thighs

are gray ish -brow n , mixed with some reddish hairs.

The crown is black, with rounded, sometimes

bushy, black tufts.

180

Marc G.M. van Roosmalen & Tomas van Roosmalen

Here, we recognize only two Amazonian Robust

or Tufted Capuchins (genus Sapajus)-. the mono-

typic Guianan Brown Capuchin Scip. Cipellci that

is distributed in the eastern Amazon and in the

Guianas, and the Large-headed Capuchin Scip. ITiaC-

rocephalus with a number of forms/morphs/sub-

species that are distributed throughout the western

Amazon as far north as the Magdalena Valley in N

Colombia (Fig. 42). Taxon Scip. Cipellci is found in

the rain forests of the Amazon Basin ofBrazilN of

the lower Rios Negro and Amazonas, E of the Rio

Branco, extending N to the southeastern part of the

Orinoco Delta in Venezuela and the Guianas. Its

distributional limits in the S, SE, and E are defined

by the extent of the Amazon rain forest, in the S and

E of Maranhao State marking the transition zone to

xeric deciduous forest and ‘caatinga’ scrub. In the

West, its distribution is limited by the interfluve of

the Rios Negro and Solimoes and the Rio Madeira

Basin. The Guianan Brown Capuchin species Sap.

apella is relatively large and heavily built, with a

broad head, flat face, and short limbs. Its coat

is long and coarse, with all five extremities darker

colored than the rest of the body. It is generally

gray-fawn to dark brown above, with a yellowish

or red underside. The lower limbs and tail are black,

and there is a variably distinct dorsal stripe. The

face and temples are light gray-brown. The crown

tuft is black and forms short tufts above the ears (the

characteristic ‘horns’). The crown cap extends

down the cheeks forming ‘sideburns’ that often

meet below the chin. There is no sexual dimorph-

ism, but males are slightly heavier and often overall

much darker colored. The M argarita Island Capuchin

taxon Sap. apella margaritae that is endemic to Isla

de M argarita off the Caribbean coast of Venezuela

fatutUus

AMAZONIAN ROBUST CAPUCHINS

SAPAJIS

pallidum

1 union ns

Sapajus apella Guianan Broun Capuchin

) 0 Sapajm apella margaritae

Sapajus macracephalut Large- beaded Capuchin

Colombian morph fatueilm

o ■, Peruvian morph maranonh

. ‘ Bolivian morph pallid us

Brazilian morph juruanus

Figure 44. Phylogeography, allopatric speciation. and metachromic bleaching in all Amazonian Robust Capuchins

disputedly divided up in Sapajus Cipellci and S. maCWCephaluS, the latter with different taxa ’ in -the-m aking ’ .

On the origin of allopatric primate species

181

distinguishes itself from the nominate Guianan

Brown Capuchin by longer dark sideburns in front

of the ears, and progressively bleached, pale-yellow

or straw colored, near-albinotic upper arms and

shoulders. The thighs and rump are pale yellow-

brown, and flanks, lower back, and upper chest are

pale brown, becoming paler from the upper back

to the neck. The face is grayish, tinged pink on

the cheeks and chin. The black cap extends in a “V”

to between the eyes, with small round tufts above

the eyes.

The monotypic Large-headed Capuchin taxon

Sap. macro cephalus is distributed in the western

Amazon Basin, but its taxonomy and distributional

limits are poorly defined. According to Silva Jr.

(2001 ) this species includes the forms/morphs/sub-

species Sap. fatuellus from the upper Magdalena

Valley, Colombia, Sap. maraYlOYlis from Rio Ham-

burgo, Peru, Sap. pallidus from the Rio B eni, C + N

Bolivia, and Sap. jliruanus from the Rio Jurua,

Brazil. Preliminary genetic studies in 2012 failed to

indicate that Sap. apella and Sap. macrocephalus

were distinct taxa. Large-headed Capuchins are

distributed across the upper Amazon Basin in E

Colombia, north as far as the Rio Arauca on the

border with Venezuela, E Ecuador, E Peru, W

Brazil, and C and N Bolivia (S at least as far as the

upper Rio Beni). Their overall coat color is gray-

brown or ochreous to dark brown above, with a

dark dorsal stripe, and yellow-fawn or red-gold

below. Sides of the neck are lighter, upper arms are

pale yellowish, and legs are black with yellow-fawn

or red-gold below. Adults have high, pointed crown

tufts that resemble horns, which become reduced

with age. There is often a gray-white stripe running

from eye to ear. Four forms of the Large-headed

RED NECKED GROUP

uaucyntaae

0 Aotus miconax

Aorus nigriceps

Aotus a zame

fa.) infulaim

fa.) botivieniis

fa.) azarae

GREY-NECKED GROUP

Aotus zonalis

Aotus temunnus

( Aorus jorgeheruandezi

# Aorus griseimembra

Aotus brumbacki

(ft Aotus vociprans

Aotus tririrgatus

Figure 45. Phy logeography, allopatric speciation, radiation, and metachromic diversification

in all hitherto recognized taxa ofNight Monkeys, genus AotUS.

182

Marc G.M. van Roosmalen & Tomas van Roosmalen

Capuchin have been distinguished (Fig. 44). The

Colombian form Sap. fatuelluS is bright brown

above and red below, having a prominent dorsal

stripe. Its face is almost naked and dark-purplish to

flesh-colored. The Peruvian form Sap. mavaYlOYlis

is uniformly dark chestnut-brown above, becoming

more reddish towards the flanks, and deep yellow-

brown below. Its legs, tail, and (sometimes) fore-

arms are black. Its cap is distinctly black, whereas

temples and sides of the crown are often white. It

has a crescent-shaped whitish patch above each eye.

There are no crown tufts or they are minimal. The

Brazilian form Sap. jUTUanilS is reddish-brown

above with a very distinct blackish dorsal stripe.

The throat and upper chest are blackish or pale

reddish-buff, and limbs and tail are dark brown or

black. The Bolivian form Sap. palliduS fro m south

of the Rio M adre de Dios has also been referred to

as a subspecies of Sap. libidinOSUS, but such tax-

onomy would be conflicting with our theory on al-

lopatric speciation, for Sap. libidinOSUS from

CE Brazil is overall more advanced pheomelanin

bleached in comparison with Sap. palliduS. Both the

Colombian morph/taxon Sap. fatuelluS of the

Large-headed Capuchin Sap. maCWCephalus and

the insular Margarita Island Brown Capuchin Sap.

apella rnargaritae are in their overall advanced

pheomelanin bleached coat coloration clearly fol-

lowing the metachromic pathway to albinotic, and

therefore fully concur with our theory of allopatric

speciation (Fig. 44).

NightMonkeys orDouroucoulis genus AotUS rep-

resent a very old lineage that is generally placed in

a family of its own - Aotidae. The molecular genetic

evidence classifies them as a subfamily of the Ce-

bidae. There is also morphological evidence to

place AotUS in the Pitheciidae. There are generally

two Groups distinguished: the “Gray-necked

Group” (characterized by grayish to brownish

agouti sides of the neck and body), which occurs

north of the Amazon River, and the “Red-necked

Group” (characterized by partly or entirely orange

or yellowish sides of the neck and chest, much

contrasting with the grayish to brownish-agouti

colored sides of the body), which occurs south of

the Amazon River (Mittermeier et al., 2013). Re-

cently, up to eleven species have been recognized,

of which at least seven in the Gray-necked Group:

the Lem urine Night Monkey Ao. leiflUritlUS, the

Pan am anian Night Monkey Ao. ZOTialis, B rum back’s

Night Monkey Ao. bvuvnbacki, the Gray-legged

Night monkey Ao. griseiffieiTlbra, Spix’s Night

M on key Ao. VOciferans, Humboldt’s Night Monkey

Ao. trivirgatUS, and Hernandez-Camacho’s Night

Monkey Ao. jorgehemandezi (Figs. 45, 46). In the

Red-necked Group are recognized four species: the

Andean Night Monkey Ao. JfliconaX, Ma’s Night

Monkey Ao. YiancyiTiaae, the Black-headed Night

M onkey Ao. VligricepS, and A zara’s N ight M onkey

A. azarae (Figs. 45-47). Sexual dimorphism in

night monkeys is absent. They are also not sexually

dichromatic in coloration and facial markings. The

coat is in metachromic sense primitive, archetypic

saturated eumelanin, grayish to grayish-tan with a

pheomelanin bleached, lighter tan or yellowish

underside. In Red-necked species, ventral surfaces

of neck, chest, abdomen, and inner sides of arms

and legs are orangish or russet colored. The faces

have white patches over eyes, topped by black

stripes, and a triangular black patch running from

the center of the forehead down between the eyes.

Black stripes are also extending from the lateral side

of each eye to the forehead, varying in width and

darkness, and may or may not converge posteriorly

with the central stripe. Tails are generally agouti-

brown, distally black-tipped. Night Monkeys most

likely descended from a diurnal haplorrhine. They

only are secondarily nocturnal and have retained

their color vision .

Within the Gray-necked Clade Ao. letnurinus is

the nearest to archetypic, saturated eumelanin, less

bleached taxon. It is a montane species of the

Colombian Andes range, at elevations above 1,000-

1,500 m, in the upper Rio Cauca Valley and on the

slopes of the Cordillera Oriental (but not in the

Magdalena Valley that is occupied by the Gray-

legged Night Monkey Ao. griseimetnbra), extend-

ing its range S into Ecuador through the humid sub-

tropical forests of the Cordillera Oriental. The

Lem urine Night Monkey is rather shaggy and long-

haired, with the upperparts of the body often eu-

melanin grayish to buffy-agouti, with a poorly

defined brownish medial dorsal band. The under-

side of the body is pheomelanin bleached yellowish

to pale orange. Inner and outer sides of limbs are

entirely grayish-agouti, or the inner sides have a

yellowish to pale orange tone extending from the

chest and belly to the mid-arm or mid-leg. Hands

and feet are dark. Temporal stripes may be separ-

ated or united behind the head. From ancestral Ao.

On the origin of allopatric primate species

183

lemurinus derived the Gray-legged Night Monkey

taxon Ao. griseimembra. It is distributed in N

Colombia and NW Venezuela. It occurs in the Rio

Magdalena Valley and northern lowland forests of

Colombia (including the Sierra Nevada de Santa

Marta and the Rios Sinu and San Jorge basins),

extending into Venezuela in the vicinity of Lake

Maracaibo. It is grayish to brownish-agouti on the

side of the neck. Upperparts are grayish to buffy;

chest, belly, and inner surfaces of the legs are brown-

ish or yellowish to pale orange. Pelage is relatively

short. Hands and feet are light-brown. From taxon

Ao. griseimembra derived to the NW the mono ty pic

Panamanian Night Monkey zonalis. This taxon is

distributed in NW Colombia in the Pacific low-

lands, S towards the Ecuadorian border, and W into

most of Panama; it is absent from SW Panama

(Chiriqui). Its overall coat color is brownish in the

Canal Zone and Colombia, but it grades into paler

and grayer tones along the upper Rio Tuira, E

Panama. From Ao. ZOYialis derived Hernandez-

Camacho’s Night Monkey Ao. jorgehernandezi.

This monotypic taxon is believed to occur in the

(sub)-m ontane tropical forests on the western

slopes and foothills of the W Colombian Andes

(in Quindio and Riseralda). It is advanced bleached

to albinotic in the head and ventral parts. Its face

has two discrete supraocular white patches separ-

ated by a broad black frontal stripe. Moreover,

subocular white bands of fur are separated by a thin

black malar stripe on each side of the head. Ventral

parts of the arms from the wrists running up into the

chest and belly are of a thick white fur (Fig. 39).

From the Gray-necked Night Monkey Clade’s

nearest to archetypic taxon Ao. lemurinus derived

to the SE first Brumback’s Night Monkey Ao.

brumbacki. This monotypic taxon is distributed in

NC Colombia in the eastern part of Boyaca De-

partment, E to the highlands of Meta (to at least

1,500 m above sea level). Its coat is dorsally

grayish-buffy agouti colored with a dark brown

mid-dorsal zone. Ventral parts extending to the

elbows, knees, and lower throat are pale orange.

Sides of the neck are entirely grayish or brownish

agouti, like the flanks and outer sides of the arms.

The head shows well-marked, thin, brownish-black

temporal stripes. The white above the eyes is yel-

lowish, and the white on the face extends to the

chin. From Ao. brumbacki derived first to the S

Spix’s Night Monkey Ao. VOciferans. This mono-

typic taxon is widespread in the upper Amazon

Basin, extending from NW Brazil (W of the Negro,

Uaupes, and A m azon as-S olim 5 es Rivers) into SE

Colombia (S of the Rio Tomo, Orinoco Basin), and

S into the Ecuadorian Amazon and NE Peru (as far

south as the north bank of the M aranon-Am azonas

River). It occurs also S of the Rio Solimoes in a

small area on the lower Rio Purus. Spix’s Night

Monkey’s coat is brown-toned above, with an over-

all white, slightly orange tinged underside, extend-

ing to the wrists, ankles, and chin. Hands and feet

are black. The proximal one-third to one-half of the

ventral side of the tail is reddish or grayish- red, the

rest is black. The crown stripes on the head are thick

and brownish, with white fur above the eyes con-

fined to two small patches grading into the agouti-

colored crown. The temporal stripes are united

behind, and the malar stripe can be well defined to

absent. The face is white, except for the chin. From

Ao. VOCiferailS derived to the N and E the mono-

typic Humboldt’s Night Monkey taxon Ao. trivir-

gatUS. It is widespread across N Brazil, N of

the Rios Negro and Amazonas and W of the Rio

Trombetas, N into SC Venezuela and E Colombia.

Sides of the neck are grayish-agouti to mainly

brownish-agouti colored. Upper parts of the body

are grayish to buffy-agouti. The inner sides of the

limbs, extending to the wrists and ankles, are sim-

ilar in color to the orange-buffy of chest and belly.

The face has triradiate brown stripes. It is rather

grayish in comparison with the usual white of other

Night Monkeys. Hands and feet are dark-brown.

Taxon Ao. trivirgatUS can be distinguished from all

other Night Monkeys by its parallel temporal stripes

on the head and the lack of an interscapular whorl

or crest (Figs. 45, 46).

Within the Red-necked Clade of Night Mon-

keys, the Black-headed Night Monkey Ao. Yligri-

ceps is the nearest to archetypic, less pheomelanin

bleached taxon (Fig. 47). This monotypic species is

distributed in the Brazilian Amazon, S of the Rio

A m azo n as-S o lim oes and W of the Rio Tapajos-

Juruena, as far south as the right bank of the Rio

Guapore and the left bank of the Rio Madre de Dios

in N Bolivia. It occurs also in SE Peru, west to the

Rio Huallaga, and north as far as the Rio Cush-

abatay. Its coat is iron-gray above and brownish-

agouti on the dorsum. The underside is orange

colored with white tones, extending to the neck,

throat, chin, and sides of the jaw and also to the

184

Marc G.M. van Roosmalen & Tomas van Roosmalen

GRAY-NECKED NIGHT MONKEYS

AOTUS

Figure 46. Radiation and metachromic d iversification in the Gray- necked Night Monkey Group ( AotUS ), folio w in g eum elan in

and pheomelanin pathways of metachromic bleaching, in particular in the head, proximal half of the tail, and ventral parts

of the body.

On the origin of allopatric primate species

185

Figure 47. Radiation and metachromic diversification in the Red-necked Night Monkey Group ( AotUS ), following eu -

melanin and pheomelanin pathways of metachromic bleaching, in particular in the head, tail, and ventral parts of the

body.

186

Marc G.M. van Roosmalen & Tomas van Roosmalen

inner surfaces of the wrists and ankles. The cap is

black, the face stripes are broad, and it has distinct

areas of white on the face.

From the Black-headed Night Monkey Ao. nigri-

ceps derived to the W Ma’s Night Monkey Ao.

TICincy lTiaae . This monotypic taxon ranges in W

Brazil (S of the Rio Solimoes from the Rio Javarr

as far east as the Rio Jandiatuba) and NE Peru (from

the Rio Javari W to the Rio Fluallaga). This taxon

is also found in an enclave between the lower Rios

Tigre and Pastaza. The upper parts of its coat are

grayish-agouti, with a dark mid-dorsal zone and a

pale orange underside, extending up the sides of the

neck and inner limbs. The proximal part of the tail

is orange, with a blackish stripe above; the under-

side is blackish. Its face is grayish-white, the crown

stripes are narrow and dark brown colored, and the

sides of the throat and jaw are colored like the body

(Fig. 41). From Ao. nancymaae derived to the W

the Andean Night Monkey taxon Ao. Uliconax. This

monotypic night monkey is endemic to Peru. It is

confined to a small area S of the Rio Maranon and

W of the Rio Huallaga. It inhabits the primary and

secondary humid, lower-montane cloud forests in

the Andes at elevations of 800-2,800 m.

Upper sides of its coat are light gray with a

brownish tint, often quite infused with red-brown.

Its underside is pale orange, extending forward as

far as the chin and on the inner sides of the limbs.

Outer surface of the body is overall brownish to

buffy-agouti. The tail is bushy, its upper side is

blackish, its lower side reddish-orange. Head parts

and throat are advanced bleached to near-albinotic .

From the nearest to archetypic Red-necked Black-

headed N ight M onkey Ao. nigriceps derived in op-

posite direction (to the S and E) Azara’s Night

Monkey species Ao. azarae. Three subspecies of

Ao. azarae are recognized: the nominate taxon

Ao. azarae, distributed in SC Brazil, S Bolivia,

Paraguay, and N Argentina; taxon Ao. boliviensis,

distributed in SE Peru and Bolivia east of the

Andes; taxon Ao. infulatUS, distributed in Brazil, S

of the Rio Amazonas (but with a small enclave in

the SE tip of Amapa State), including M arajo and

Caviana Islands, extending east into Maranhao

State as far as the Rio Parnalba, S along the west

bank of the Rio Tocantins to the Pantanal of Mato

Grosso. Taxon Ao. azarae inf Hiatus’ s western limit

is the Rio Tapajos-Juruena.Azara’s Night M onkey

Ao. azarae is highly variable. It generally has an in-

terscapular whorl. Taxon Ao. azarae has a long,

thick, and shaggy fur that is grayish to pale buffy-

agouti above and pale w hitish -oran ge below. Facial

stripes are narrow. The basal hairs of the distal l A

of the tail are orange. Taxon Ao. boliviensis has a

relatively short fur, with an olive tone above and

contrastingly grayer on the limbs. The facial stripes

are very narrow except where the middle one ex-

pands on the crown; the black temporal stripe in this

taxon is poorly defined, the black malar stripe is

faint or absent, and there is usually a whitish band

between the eyes and temporal stripe. There is a

conspicuous whorl between the shoulder blades.

The third taxon Ao. infulatUS, the “Feline Night

Monkey”, is very similar to subspecies Ao. bolivi-

ensis, but the white on the face is more prominent.

There is no whitish band between the eyes and the

temporal stripe as there is in Ao. boliviensis. The

temporal stripes are black, well defined, and con-

tinuous with the malar stripe. The tail is reddish

throughout its length except for the black tip. The

orange color of the underparts extends to or above

the ventral one-half of the sides of the neck. The

color of the throat varies from orange, with the

anterior one-half grayish-agouti to entirely orange

colored (Fig. 47).

Our theory suggests that the trend to allopatry

in Neotropical primates resulted from a specific

kind of social selection. That the discrimination of

somewhat deviant mutant young males by high-

ranking males, which push them toward the peri-

phery of the parental group’s range, has been the

true driver behind metachromic bleaching on

the evolutionary path along which a certain race,

species, phylogenetic clade, or genus has extended

its geographic range in the past. As any founder-

colony or population at the limit of a taxon’s current

range will represent a narrow gene pool, through in-

breeding certain phenotypic characters (e.g., local

depilation of the skin, change of coloration of the

skin, pelage or parts of it) will initially be reinforced

and advance more rapidly within the population.

Through the process of metachromism (changing

hair and skin color) with the trend to allopatry as

the behavioral driving force, speciation, radiation,

and phylogeography can be retraced and well

explained for in all extant Neotropical primates.

According to the principle of metachromic bleach-

ing, extant primate taxa at the base of a phylogen-

etic tree or clade are in general agouti or saturated

On the origin of allopatric primate species

187

eumelanin colored. They are the least colorful,

black(ish) or dark brown toned, and therefore con-

sidered to be nearest to the ancestral, archetypic,

primitive or original form.

Geographic variation and diversification in

color patterns of the coat among Neotropical mon-

keys demonstrates with unusual clarity the unilat-

eral direction and irreversibility of processes that

lead to progressively metachromic bleached and

ultimately (near)-albinotic allopatric forms, irre-

spective of environmental factors (Figs. 1-47). The

essentially behavioral and genetic driving forces

behind metachromic processes, though, have never

been studied. They are generally considered enig-

matic. The reason may be that they seem to disobey

commonly accepted Darwinian rules of evolution.

Different from birds, in territorial (Neotropical)

monkeys metachromic changes in coat color toward

bleaching or albinotic and/or all sorts of local hair

growth or loss of hair (depilation) do not seem to

play an essential role in sexual display and mate

selection. Consequently, they may seem to be non-

adaptive. In the wild only rarely one is able to

witness how exactly processes of metachromic

bleaching do work out. For instance: when some-

what bleached or depilated deviant young males are

being pushed from the center into the periphery of

a ranging or foraging group. Or: when ‘outcast’

males do join in all-male parties. Or: when such

parties set out to look beyond the horizon, for mere

survival willing to overtake any habitat delimitation

or geographic barrier found on their ‘path to allo-

patry’. These crucial data will only come available

when fieldw orkers, like we did, do live for pro-

longed periods of time among undisturbed primate

populations in pristine tropical forest environment.

As very few prim atologists have done so, at least in

the Neotropics, and sample sizes are consequently

too small to be published and divulged, it is im-

possible for us to add more references then our own

on the matter. Even though, living over more than

a decade in permanent intimate contact with pristine

nature, both in the Brazilian Amazon and in the over-

all even better preserved Guayanan Shield, led us

to believe that high-ranking males pushing slightly

bleached and/or depilated young males to the peri-

phery of a group’s range, or sometimes beyond its

boundaries, could plausibly be the true and prin-

cipal motor or driver behind allopatric speciation

and radiation of taxa in nearly all Neotropical

primate genera - Pygmy Marmosets ( Cebuella . ),

Tamarins ( SdguiriUS ), Amazonian Marmosets

( Mico ), True Marmosets ( Cdllithfix ), Lion Tamar-

ins ( Leontopithecus ), Sakis ( Pithecia ), Bearded

Sakis ( Chiropotes ), Uakaris ( CacajaO ), Titi Mon-

keys (CaUicebuS ) , Night Monkeys ( AotliS ), Squirrel

Monkeys ( Sciiffliri ) , G racile/U ntu fted Capuchin

Monkeys ( CebliS ), Robust/Tufted Capuchin Mon-

keys ( SapajUS ), Howling Monkeys ( Alouattd ),

Woolly Monkeys {LagOthviX ) , Spider Monkeys

( AteleS ), and Woolly Spider M onkeys (BrachyteleS) .

Interestingly, but concurring with our theory (for

those monkeys that do not defend a common ter-

ritory), metachromic bleaching did not take place

in peaceably living monkeys like the archetypic

agouti and saturated eumelanin colored Black-

crowned Dwarf Marmosets Cdllibellci huiflilis, a

newly identified monotypic genus of diminutive

callitrichid monkeys (Figs. 2, 3). Nor did it take

place in saturated eumelanin all-black Goeldi’s

Monkeys {CdllimicO goeldii) - the only other mono-

typic primate genus in the Neotropics that does not

behave territorial in any sense and therefore does

not defend a common living space against the neigh-

bors of its own kind (Fig. 4). Their external features

showing archetypic agouti and saturated eumelanin

coat coloration without any sign of metachromic

bleaching are in full accordance with their genetics

that put them at the base of their respective phylo-

genetic trees. It further corroborates our theory on

the origin of allopatric speciation in primates and

the principle of metachromic bleaching, for Dwarf

Marmosets and Goeldi’s Monkeys are equally so-

ciable, peaceable little m onkeys that do not demon-

strate any rate of territorial defense. The primitive

agouti and saturated eumelanin (blackish-brown)

Black-crowned D w arf M arm oset stands at the base

of the phylogenetic tree of all Amazonian marmo-

sets (Van Roosmalen & Van Roosmalen, 2003). It

represents the nearest to ancestral, archetypic mar-

moset from which all extant, advanced and highly

territorial Amazonian marmosets (genus MicO ) and

pygmy marmosets (genus Cebuella) have derived

in the Late Pleistocene.

Our theory is firmly rooted in over 30-year field-

work on primates, both in the Guianas and in the

entire lowland Amazon Basin. Lrom the very be-

ginning we have given special attention to issues

like socio-ecology, ecological feeding niches, ter-

ritorial behavior, distributions, and phylogeography.

188

Marc G.M. van Roosmalen & Tomas van Roosmalen

Simultaneously, we have kept, raised, bred, rehab-

ilitated, and reintroduced back into the wild entire

families or social groupings of a multitude of mon-

key taxa representing about all hitherto known Neo-

tropical primate genera. Many unique, extremely

rare or sometimes once- in -a-lifetim e observations

that we gathered in pristine tropical rainforest en-

vironment as well as in captivity (the bulk of it

never published inherent to ‘insignificant’ sample

sizes) now do add up to the validity of our theory.

It basically helps us to better understand the com-

plex distribution patterns, phylogeography, diversi-

fication, speciation, and radiation in Neotropical

primates. Most likely, the theory applies to all the

world’s primates (including man), as long as the

taxa exhibit social groupings that defend a common

living space, home range, or territory. The fact that

only two Neotropical primate genera ( CcilluflicO

and Callibella ) are monotypic strongly supports

our theory, as it does not apply to peaceable, non-

territorial social primates. By boat, canoe, and on

foot we have surveyed entire basins of a number of

major tributaries of the mighty Amazon River to

study primate diversity and distributions across the

entire Amazon Basin, including also large parts of

the Brazilian and Guyanan Shields. We have tested

and empirically come to fully validate Alfred Rus-

sel Wallace’s river-barrier hypothesis that he first

laid down in his 1 852 account On the Monkeys of

the Amazon, and later in his 1876 paper “The Geo-

graphical Distributions of Animals”. Herein, Wal-

lace points at the larger rivers that he sailed as the

principal evolutionary cause of the Amazon’s rich

extant primate diversity and complex biogeography,

since many rivers effectively block off gene flow

between populations along opposite riverbanks

(genetic isolation). As the Amazon still represents

a largely pristine and vast natural realm that is (not

yet) drastically and irreversibly modified by human

interference, no better place to study and retrace

evolutionary processes that may have acted upon

primates and other mammals since the Pliocene era,

no matter on which continent. Moreover, most

rivers that in the course of millions of years have

played a significant role in the demography of

Amazonian primates - the majority of which cannot

swim or fly- remain acting as such. Therefore,

distributions of primate taxa in the Amazon, if

correctly studied, documented, and taxonom ically

treated, do follow a more transparent and rational

overall pattern in comparison with those of the Old

World. In SE Asia, instead of rivers, the ocean

played an equally important role in the island bio-

geography of mammals. And in Africa (including

Madagascar), the landscape with its complex and

diffuse mosaic of vegetation types and habitats

seems to have played a more determinant role than

rivers in primate distributions. Moreover, massive

human disturbance has long irreversibly changed

the landscape of the Old World. This may have

obscured to some extent the principal factors that

influenced and determined distributions and phylo-

geography in catarrhine primates, most importantly

the horn inins.

CONCLUSIONS

Here we discuss the above proposed doctrine on

the origin of allopatric primate species and the prin-

ciple of metachromic bleaching among Neotropical

primates as a conclusive socio-ecological answer to

the question: why primates are such a highly diver-

sified, species-rich, and colorful order in the Class

Mammalia. The Order Primates contains a world

total of 73 genera, 414 IU C N -recognized species,

and 612+ known taxa of which roughly one third

are found in the Neotropics (Mittermeier et al.,

2013) (see also Table 1). Globally, only the rodents

(Order Rodentia) outnumber the Order Primates.

However, compared to primates, rodents are by far

not that diversified. They are mostly opportunists,

not very sociable, and not particularly colorful.

While studying color variation in c a llitric h id mon-

keys, Hershkovitz (1968; 1977) pro posed the

“Theory of M etachrom ism .”. He attributed evolu-

tionary change in mammalian tegumentary colors

to social, sexual, and predatory selection, as it

seems to be the case in birds. He argued that the

highly ‘visually’ adapted primates may be predis-

posed to select mates based on coat color and hair

adornments. However, primates generally do not

sexually display their skin and coat colors, or hair

dresses, except for a few genera in the Old World

(e.g., Theropithecus, Mandrillus). instead, some

display their genitals, like both sexes of Amazonian

Marmosets (genus Mico ) do. Or, both sexes of

Bearded Sakis ( ChiwpOteS ), female Spider Mon-

keys (Ateles) or male Woolly Spider Monkeys

( Brachyteles ) do. In that case, their genitals are

On the origin of allopatric primate species

189

mostly hypertrophied (e.g., MicO, CHiwpOteS, Bva-

chyteles. Pan). Hershkovitz’s key hypothesis of

m etachrom ism , which is tested in tamarins (genus

SaguinuS) and confirmed for many of its predictions

by Jacobs et al. (1995), concerns the orderly, irre-

versible loss of pigment within chrom ogenetic

fields. Its key concept is that genetic drift together

with social selection could fix phenotypes departing

from primitive agouti or saturated eumelanin

(blackish-brown) fields by various degrees of

so-called “metachromic bleaching”. Thus, an al-

binotic (nearly white) coat would represent the end

point of geographic variation in a series of near-al-

lopatric forms (color morphs) deriving ultimately

from an agouti-colored or saturated eumelanin pig-

mented ancestral form. Using m etachrom ism , we

have demonstrated that most Amazonian monkey

genera are monophyletic and composed of two or

more major phylogenetic Groups or Clades. We

found only two genera (i.e., Callibella and Cal-

limico) to be monotypic. Contrary to Hershkovitz,

who followed the Darwinian fallacy of adaptive

evolution by linking evolutionary change in mam-

malian tegumentary colors (‘bleaching’) to social,

sexual, and predatory selection, we suggest to at-

tribute metachromic diversification in extant social

and territorial prim ates exclusively and uniquely to

“male social selection”. We propose the “trend to

allopatry in somewhat metachromic bleached

and/or depilated varieties” to be the principal

mechanism and driver behind speciation, radiation,

and phylogeography in group-living Neotropical

monkeys that defend the group’s living space. It

arguably applies also to any group-living territorial

primate worldwide, including our own species and

its ancestors (be it hominids or hominins). For all

nineteen genera of Neotropical primates we have

presented distribution maps of all known extant

taxa and indicated the geographic barriers (rivers,

lakes, mountain ranges, seasonally inundated flood-

plain forests, open scrub areas, etc.) delineating

each taxon’s distribution. We have also elaborated

the phylogeography and radiation within each

monophyletic cladistic Group or Clade and related

them to the irreversible patterns of metachromic

bleaching. Through the process of metachromism

(changing hair and skin colors) with the trend to al-

lopatry as the behavioral driving force, speciation,

radiation, and phylogeography can be well retraced

and explained for in all extant Neotropical primates.

According to the principle of metachromism, prim-

ate taxa at the base of a phylogenetic tree or clade

are in general agouti or saturated eumelanin (black

or blackish-brown) colored - that is the least color-

ful. Within that Clade they are considered the

nearest to ancestral, archetypic, primitive, or ori-

ginal taxon. Based on metachromic skin and fur

characters, without a single exception, we were able

to retrace phylogeographic pathways of speciation

and radiation that were plausibly followed in the

evolutionary history of each monophyletic Clade.

In all cases we could confirm the trend to allopatry

following irreversible eumelanin and pheomelanin

pathways of metachromic bleaching. The farther a

taxon radiated away from the origin or center of

the Clade’s dispersion, the more progressively eu-

chromic or bleached and eventually albinotic its

coat/pelage, or part of it, will become.

The great majority of primates are sociable,

group-living animals. Group sizes vary from nuc-

lear families (4-7 individuals) to troops of mixed

age and sex classes containing 15 to over 200 indi-

viduals. The far majority of the world’s primate so-

cieties are socially structured in a hierarchic way

and based on male dominance and ranking. Male

defense of the group and its living space within a

population benefits from male social selection.

Even in m atriarchally organized social groups, such

as those of spider monkeys ( Ateles ) and pygmy

chimpanzees or bonobos {Pan), males associate in

all-male parties to jointly patrol and defend the

group’s territory or living space. In social conflicts

among males over ranking, inferior males as well

as mutant males that show somewhat different,

deviant phenotypic characters (such as a slightly

bleached pelage here or there or depilated skin in

certain body parts) will be pushed into the periphery

of the group during ranging and foraging. We have

seen this happening, both in the wild and in semi-

free ranging conditions, in particular in social

groups and societies of monkeys like LagOthrix,

Ateles, Cebus, Sapajus, Saimiri, Cacajao, or Chiro-

potes. Depending on the species, such young males

also happen to be expelled from the parental group.

We have witnessed this in wild and semi-free

ranging populations of Alouatta, CalUcebuS, MicO,

Cebus, Sapajus, and Pithecia. Either way, the

chances of outcast males to survive and pass on

their mutant genes are utterly slim. If this would

happen in other mammals - being comparatively

190

Marc G.M. van Roosmalen & Tomas van Roosmalen

Alouatta Lacepede, 1799

Alouatta arctoidea Cabrera, 1940

Alouatta belzeblll (Linnaeus, 1766)

Alouatta caraya (Humboldt, 1 8 1 2)

Alouatta discolor ( s p ix , 1 8 2 3)

Alouatta guariba guariba (Humboldt, 1 8 1 2 )

Alouatta guariba clamitans Cabrera, 1940

Alouatta macconnelli Elliot, 1 9 1 o

Alouatta nigerrima Lon n berg, 1 9 4 1

Alouatta palliata palliata (Gray, 1 8 4 8)

Alouatta palliata aequatorialis Festa, 1903

Alouatta palliata coibensis Thomas, 1902

Alouatta palliata mexicana m erriam , 19 02

Alouatta palliata trabeata Lawrence, 1933

Alouatta pigra Lawrence, 193 3

Alouatta sara Elliot, 1 9 1 0

Alouatta seniculus seniculus (Linnaeus, 1766)

Alouatta seniculus juara Elliot, 1 9 1 0

Alouatta seniculus puruensis Lonnberg, 1 9 4 1

Alouatta ululata e ilio t, 1 9 1 2

AotUS Illiger, 1811

Aotus azarae azarae (Humboldt, 1 8 1 2 )

Aotus azarae boliviensis Elliot, 1907

Aotus azarae injulatus ( k u h l, 1 8 2 o )

AotUS brumbacki Hershkovitz, 1983

Aotus griseimembra E liiot, 1912

Aotus jorgehernandezi Defier et b ueno, 2 00 7

Aotus lemurinus I. Geoffroy Saint-Hilaire, 1843

Aotus miconax Thomas, 1927

Aotus nancymaae Hershkovitz, 1983

Aotus lligriceps D o 11m a n , 19 09

Aotus trivirgatus (Humboldt, 1811)

Aotus vociferous (Spix, 1 82 3)

Aotus zonalis Goldman, 1914

Ateles E. Geoffroy Saint-Hilaire, 1806

Ateles belzebuth E . Geoffroy Saint-Hilaire, 1806

Ateles chamek (Humboldt, 1 8 1 2 )

Ateles fusciceps fusciceps Gray, 18 65

Ateles fusciceps rufiventris Sciater, 1872

Ateles geoffroy i geoffroyi k u h l , 1 8 2 o

Ateles geoffroyi azuerensis (Bole, 1937)

Ateles geoffroyi frontatus (Gray, 1842)

Ateles geoffroyi grisescens Gray, 1865

Ateles geoffroyi ornatus (Gray, 1 8 7 o )

Ateles geoffroyi vellerosus Gray, 1865

Ateles geoffroyi yucatanensis Kellogg et Goldman, 1944

Ateles (hybridus) hybridus I. Geoffroy Saint-Hilaire, 1829

Ateles (hybridus) br urine us G ray, 1870

Ateles longimembris Allen, 1 9 1 4

Ateles marginatus E. Geoffroy Saint-Hilaire, 1809

Ateles paniscus (Linnaeus, 1758)

Brachyteles Spix, 1823

Brachyteles arachnoides (E. Geoffroy Saint-Hilaire, 1806)

Brachyteles hypoxanthus (K u hi, 1 8 2 o )

Cacajao Lesson, 1840

Cacajao (calvus) calvus ( I. Geoffroy Saint-Hilaire, 1847)

Cacajao (calvus) novaesi Hershkovitz, 1987

Cacajao ( calvus) rubicundus (I. Geoffroy Saint-Hilaire

et D eville, 1848)

Cacajao ( calvus) ucayalii (Thomas, 1928)

Cacajao ( melanocephalus ) melanocephalus

(Humboldt, 1812)

Cacajao (melanocephalus) ayresi Boubli, Silva,

Hrbek, Pontual et Farias, 2008

Cacajao (melanocephalus) hosomi Boubli, Silva,

Hrbek, Pontual et Farias, 2008

Cacajao ouakary ( s p ix , 1 8 2 3)

Callibella van Roosm alen M .G .M . et van Roosm alen T., 2003

Callibella humilis (van Roosmalen M .G.M ., van

Roosmalen T., Mittermeier et de Fonseca, 1998)

Callicebus Thomas, 1903

Callicebus aureipalatii Wallace, Gomez, Felton A.

et Felton A.M., 2006

Callicebus baptista Lonnberg, 1939

Callicebus barbarabrownae Hershkovitz, 1990

Callicebus bernhardi van Roosmalen M.G.M., van

Roosm alen T. et Mittermeier, 2002

Callicebus brunneus (Wagner, 1842)

Callicebus caligatus (Wagner, 1842)

Callicebus caquetensis Defier, Bueno et Garcia, 2010

Callicebus drier ascens ( s p ix , 1 82 3)

Callicebus coimbrai Kobayashi et Langguth, 1999

Callicebus cupreus ( s p ix , 1 8 2 3)

Callicebus donacophilus (d ’ o rb ig ny, 1 8 3 6)

Callicebus dubius Hershkovitz, 1988

Callicebus hoffmannsi Thomas ( 1 9 o 8 )

Callicebus lucifer Thomas, 1914

Callicebus lugens (Humboldt, 1812)

Callicebus medemi Hershkovitz, 1963

Callicebus melanochir ( Wied-Neuwied, 1820)

Callicebus modestus Lonnberg, 1939

Callicebus moloch (H offm annse gg, 1807)

Callicebus nigrifrons (Spix, 1 823)

Callicebus oenanthe Thomas, 1924

Callicebus olallae Lonnberg, 1939

Callicebus ornatus (Gray, 1866)

Callicebus pallescens Thomas, 1907

Callicebus personatus (E . Geoffroy Saint-Hilaire, 1812)

Callicebus purinus Thomas, 1927

Callicebus regulus Thomas, 1927

Table 1/1. References of scientific descriptions of all known Neotropical primates (present paper).

On the origin of allopatric primate species

191

Callicebus stephennashi van Roosm aien m .g .m

van Roosm ale n T. et M ittermeier, 2002

Callicebus torquatus ( H o ffm an ns egg, 1807

Callicebus vieivai Gualda-B arros, Nascimento et

Amaral, 2012

Callimico Miranda Ribeiro, 1912

Callimico goeldii (Thomas, 1904)

Callithrix Erxleben. 1777

Callithrix aurita (E . Geoffroy Saint-H ilaire, 1812)

Callithrix flaviceps (Thomas, 1903)

Call ithrix geoffroy i (Humboldt, 1 8 1 2 )

Callithrix jacchus (Linnaeus, 1 758)

Callithrix kuhlii Coimbra-Filho, 1985

Callithrix penicillata ( E. Geoffroy Saint-H ilaire, 1812)

Cebuella Gray, 1865

Cebuella ( pygmaea) pygmaea ( s p ix , 1 82 3 )

Cebuella (pygmaea) niveiventris Lonnberg, 1940

Cebus Erxleben, 1777

Cebus aequatorialis a lien , 1 9 1 4

Cebus albifrotlS (Humboldt, 1 8 1 2 )

Cebus brunneus a lien , 1 9 1 4

Cebus capucinus capucinus (Linnaeus, 1758)

Cebus capucinus curtus Bangs, 1905

Cebus cesarae Hershkovitz, 1949

Cebus cuscinus Thomas, 1901

Cebus imitator Thomas, 1903

Cebus kaapori Q u e iro z , 19 9 2

Cebus leucocephalus Gray, 18 65

Cebus malitiosus Elliot, 1909

Cebus olivaceus olivaceus Schomburgk, 1848

Cebus olivaceus castaneusl. Geoffroy Saint-Hilaire, 1851

Cebus unicolor s p ix , 18 2 3

Cebus versicolor Pucheran, 1845

Cebus yuracus Hershkovitz, 1949

Chiropotes Lesson. 1840

Chiropotes albinasus (I. Geoffroy Saint-Hilaire et

Deville, 1 848)

Chiropotes chiropotes (Humboldt, 1812)

Chiropotes sagulatus (Traill, 1 8 2 1 )

Ch iropotes sat anas ( H o f f m a n n s e g g , 1 8 0 7 )

Chiropotes Utahickae Hershkovitz, 1985

LdgOthrix E. Geoffroy Saint-Hilaire, 1812

Lagothrix (cana) cana ( E. Geoffroy Saint-Hilaire, 1812)

Lagothrix ( cana ) tschudii Pucheran, 1857

Lagothrix ( lagotricha > lagotricha (Humboldt, 1 8 1 2 )

Lagothrix (lagotricha) lugens Elliot, 1907

Lagothrix poeppigii Schinz, 1844

Leontopithecus Lesson, 1840

Leontopithecus caissara Lorini et Persson, 1990

Leontopithecus chrysomelas (K u h l, 182 0)

Leontopithecus chrysopygus (M ik a n , 1823)

Leontopithecus rosalia (Linnaeus, 1766)

Mico Lesson, 1840

Mico acariensis (van Roosmalen M.G.M., van

Roosmalen T., M itterm eier et Rylands, 2000)

Mi CO argent atus (Linnaeus, 1771)

MicO chrysoleucos (Wagner, 1842)

Mico emiliae (Thomas, 1920)

Mico humeralifer (E . Geoffroy Saint-Hilaire, 1812)

Mico intermedins (Hershkovitz, 1977)

Mico leucippe Thomas, 1922

Mico manicorensis (van Roosm alen M .G .M ., van

Roosmalen T., M itterm eier et Rylands, 2000)

Mico marcai ( A lp erin , 19 9 3)

Mico maiiesi ( M itterm eier, Schwarz et Ayres, 1992)

Mico melanurus (E . Geoffroy Saint-Hilaire, 1812)

Mico nigriceps (Ferrari et Lopes, 1992)

Mico rondoni Ferrari, Sena, Schneider et Silva, 2010

Mico saterei ( Silva etNoronha, 1998)

Oreonax Thomas, 1927

Oreonax flavicauda (Humboldt, 1 8 1 2 )

Pitheda Desmarest, 1804

Pithecia aequatorialis Hershkovitz, 198 7

Pithecia albicans Gray, i860

Pithecia ( irrorata ) hirsuta s p ix , 18 2 3

Pithecia ( irrorata ) irrorata Gray, 1842

Pithecia (irrorata) vanzolinii Hershkovitz, 1987

Pithecia ( monachus) milleri a lien . 1 9 1 4

Pithecia (monachus) monachus (E. Geoffroy

Saint-Hilaire, 1812)

Pithecia ( monachus) napensis Lonnberg, 1938

Pithecia ( pithecia) pithecia (Linnaeus, 1766)

Pithecia (pithecia) chrysocephalai. Geoffroy

Saint-Hilaire, 1850

Pithecia ( pithecia ) lotichiusi m ertens, 1925

Saguinus Hoffmannsegg, 1807

Saguinus bicolor ( s p ix , 1 8 2 3 )

Saguinus fuscicollis fuscicollis ( s p i x , 1 82 3)

Saguinus fuscicollis avilapiresi Hershkovitz, 1966

Saguinus fuscicollis cruzlimai Hershkovitz, 1966

Table 1/2. References of scientific descriptions of all known Neotropical primates (present paper).

192

Marc G.M. van Roosmalen & Tomas van Roosmalen

Sagliinus fuscicollis mura Rohe, Silva Jr., Sampaio

et Rylands, 2009

Saguinus fuscicollis primitivus Hershkovitz, 1977

Saguinus fllSCUS (Lesson, 1840)

Saguinus geoffroyi (Pucheran, 1845)

Saguinus illigeri (Pucheran, 1845)

Saguinus (imperator) imperator (Goeidi, (1907)

Saguinus ( imperator) subgrisescens (L 6 n n b e rg , 19 40)

Saguinus inustus (Schwarz, 1951)

Saguinus labiatus labiatus (E. Geoffroy Saint-Hilaire,

1812)

Saguinus labiatus rufiventer (Gray, 1 8 4 3)

Saguinus labiatus thomasi (Goeidi, 1 9 o 7 )

Saguinus lagonotus (Jimenez de la Espada, 1870)

Saguinus leucogenys (G ray, 1865)

Saguinus leucopus (Gunther, 1876)

Saguinus martinsi martinsi (Thom as, 1 9 1 2)

Saguinus martinsi ochraceus h ershkovitz, 1966

Saguinus midas (Linnaeus, 1758)

Saguinus my s tax my s tax (S p ix , 1 8 2 3)

Saguinus mystax pileatus (I. Geoffroy Saint-Hilaire

et D eville, 1848)

Saguinus mystax plllto (L 6 n nb erg , 19 2 6)

Saguinus niger (E. Geoffroy Saint-Hilaire, 1 803)

Saguinus nig rifrons ( I. Geoffroy Saint Hilaire, 1850)

Saguinus nigricollis nigricollis (S p ix , 1 82 3)

Saguinus nigricollis graellsi ( Jimenez de la Espada, 1870)

Saguinus nigricollis hernandezi h ershkovitz, 1982

Saguinus Oedipus (Linnaeus, 1758)

Saguinus tripartitus (M iln e-E d w ard s, 1 8 7 8)

Saguinus weddell i weddell i ( d e v ill e , 1849)

Saguinus weddelli crandalli Hershkovitz, 1966

Saguinus weddelli melanoleucus (Miranda Ribeiro, 1912)

Saimiri Voigt, 1 83 l

Saimiri boliviensis boliviensis (I. Geoffroy Saint-Hilaire

et de Blainville, 1 834)

Saimiri boliviensis peruviensis Hershkovitz, 1984

Saimiri ( cassiquiarensis ) cassiquiarensis (Lesson, 1840)

Saimiri ( cassiquiarensis ) albigena (von Pusch, 1942)

Saimiri macrodon Elliot, 1907

Saimiri oerstedii oerstedii (Reinhardt, 1872)

Saimiri oerstedii citrinellus (Thomas, 1904)

Saimiri (SCilireuS) SCiureuS (Linnaeus, 1 758)

Saimiri (sciureus) collinsi Osgood. 1 9 1 6

Saimiri UStUS (I. Geoffroy Saint-Hilaire, 1843)

Saimiri vanzolinii Ayres, 19 8 5

Sapajus Kerr, 1792

Sapajus apella apella (Linnaeus, 175 8)

Sapajus apella margaritae ( h oiiister, 1 9 1 4 )

Sapajus cay (iiiiger, 1 8 1 5 )

Sapajus flavins ( S c h re b e r, 17 7 4)

Sapajus libidinosus ( s p ix , 1 82 3)

Sapajus macrocephalus ( s p i x , 1 8 2 3)

Sapajus nigritus ( G o l d f u s s , 1 8 09)

Sapajus robustus (K uh l, 1 8 2 o )

Sapajus xanthosternos (Wied-Neuwied, 1826)

Table 1/3. References of scientific descriptions of all known Neotropical primates (present paper).

less intelligent, sensitive, and sociable than primates

in general are - being forced to live as outcasts

would equal a sure death. But, if it were healthy

male individuals deviant from the socially selected

skin and/or hair color pattern that are discriminated

against merely for being slightly depilated or

having its coat somewhat bleached somewhere,

such young males pushed out of the group’s core

area by high-ranking males will ally for the sake of

survival alone. Their shared forced-upon marginal-

ity could well drive them into looking beyond the

horizon and together leaving the pack in search of

a living space wherever it could be found. Once that

living condition is fulfilled, they can start a new

social group incorporating some females that they

were able to attract from other resident groups on

their way out. This phenomenon is known to com-

monly take place in hierarchically structured

primate societies that are ruled and defended by do-

minant (alpha)-males (e.g., AlouattO) . It guarantees

a certain primate to reach optimal densities in un-

disturbed populations. Furthermore, it selects for

males that are capable to lead and defend a social

group. A 11-m ale parties of slightly eumelanin and/or

pheomelanin bleached, or somewhat depilated

males that are pushed out of their parental group’s

living space and that follow the ‘trend to allopatry’,

will range further and further away from the core

of a taxon’s distribution. If suitable habitat to settle

down is not encountered, the animals eventually

will weaken, suffer from diseases, starve to death,

or get predated upon. Very rarely, they happen to

venture into for that species marginal or unsuitable

habitat, being forced to adapt to an alien habitat or

a different feeding niche. In extremely rare cases,

such founder-groups or -colonies may diverge along

this path into a different subspecies (whatever that

may be) and eventually into a different species

(whatever that may be) or ecospecies. This kind of

sympatric speciation may have taken place in such

cases as the cream-white, near-albinotic fair woolly

monkey living year-round in the varzeas between

On the origin of allopatric primate species

193

the lower Rio Javan and the right bank of the upper

Rio Solimoes. Or, the pheomelanin bleached, over-

all orange-colored woolly monkey from the head-

waters of the Rio Jutai. Somewhat metachromic

bleached founder-colonies of woollies driven by the

‘trend to allopatry’ once must have diverged from

archetypic agouti-colored or saturated eumelanin

ancestral La. poeppigU w hile adapting to a different

ecological niche that was new to woolly monkeys -

in this case that of a frugivorous, canopy-dw elling,

brachiating inhabitant of white-water inundated

floodplain forest (varzea). During our systematic

surveys of primate distribution and diversity carried

out in the matrix terra firme rain forest that stretches

out behind the floodplain of some white-water

rivers (e.g ., Javan, Jurua, Purus, Madeira), we were

not able to detect any differences in phenotype

between individual monkeys of a given taxon that

we observed along the entire course (from source

to headwaters) of each of these far-apart rivers.

Contrary to what is the common presumption

among prim atologists, this would mean that in

territorial monkeys such as pygmy marmosets or

saddle-back tamarins that occupy large distributions

delineated by some of the largest tributaries of the

Amazon, phenotypic characters of skin and pelage

coloration, and/or local hair growth or depilation,

seem to have stabilized across their entire distribu-

tions. In other words, within the distribution of a

given Amazonian monkey there does not exist

something like a gradient of slightly different phen-

otypes, color forms, morphs, or races. These obser-

vations from the larger field have led us attributing

full-species status to primate taxa like Cebuella

pygmaea and C. niveiventris that are phenotypically

stable throughout their (sometimes huge) distribu-

tions. Consequently, we here introduced the concept

of eco-species. This concept is firmly corroborated

by the here proposed theory on the origin of allo-

patric primate species. An ecospecies may be best

defined as: “A genetically isolated population or

group of populations of a kind that does not

undergo gene flow from adjacent populations of one

or more closely related kinds; and that shows a

stabilized phenotype across the entire range in

which it occupies a well-defined ecological niche,

which it defends against any outside competitor,

even beyond generic level:' This eco-species

concept (ESC) avoids the often confusing arbitrary

distinction between species, subspecies, race,

morph, or form, for it adds sociobiological restric-

tions to environmental (geographic, geomorpholo-

gical and phy tosociological) ones that use to act on

speciation and radiation in sociable territorial

primates. Defined as such, the ESC may apply also

to similarly socially structured mammals like coatis,

peccaries, and some canids. In accordance to this

definition, an enclave population of Callibella

humilis that lives year-round in igapo forest fringing

the Rio Atininga - genetically isolated from the

main population that lives at least one hundred km

to the north in primary terra firme rain forest -

should be assigned a different species name in its

own right. Or, in case the ranges of two Saddle-back

Tamarins of the S. fuscicollis Clade, hitherto being

treated as subspecies, are only separated by a nar-

row contact zone - where its aggressive territorial

defense effectively impedes any gene flow through

cross-breeding or hybridization - each population

should be given valid species status. But, wherever

a former distributional boundary between two such

ecospecies has been disrupted, removed by a vi-

cariance, or overtaken by the more aggressive or

opportunistic of two ecospecies, the latter will

expand its distribution to the cost of the other. Then,

a process of replacement is set in motion along a

steadily moving frontline, which inevitably will

lead to the extinction of the less aggressive, more

vulnerable, or more sensitive of the two ecospecies.

According to our doctrine of allopatric primate

speciation this will always be the ecospecies that is

the more advanced metachromic bleached one.

Here we have mentioned at least four cases across

the Amazon where such process of replacement

(through physical extermination) of one primate by

another is ongoing or about to be terminated: 1) the

archetypic agouti, gray, and dark red-brown coated

Lake Baptista Titi Monkey Callicebus baptista

extending its range along the southbank of the Rio

Amazonas to the cost of the advanced bleached,

yellow- and-gray coated Hoffmanns’s Titi Monkey

Callicebus hoffmannsi and the near- a lb in otic eco-

species from the right bank of the Rio Mamuru; 2)

the archetypic saturated eumelanin Midas Tamarin

Saguinus midasvz rsus the progressively bleached,

halfway to fully albinotic Pied Two-colored Tam-

arin S. bicolor (including S. OchraceUS) and Mar-

tins’s B are-face Tamarin S. tnartinsi , the latter three

ecospecies being currently at the verge of extinction

caused by a rapid southern expansion of midas

194

Marc G.M. van Roosmalen & Tomas van Roosmalen

(Fig. 10); 3) the saturated eumelanin Weddell’s

Saddle-back Tamarin S. (fusticollis ) Weddelli ex-

panding its range to the cost of the near-albinotic

Rondon’s Marmoset MlCO rondoni, pushing the

frontline eastward into the interfluve delineated by

the Rios Guapore and Ji- Parana after having

traversed the upper Rio Madeira in the recent past;

4) Gray’s Saki Pithecia hirsuta (or P. mittermeieri)

extending its range northwards to the cost of the

near-albinotic B u ffy Saki taxon P. CllbicCMS. In cases

of replacement it is always the more advanced

metachromic bleached to albinotic ecospecies that

is loosing the battle and eventually will go extinct.

Though only documented by us in semi-captive and

free-ranging, but artificially composed multi- pecies

populations, during social conflicts it was invari-

ably the more advanced metachromic bleached in-

dividual monkey or group of monkeys that suffered

from dominant-male discriminatory behavior, being

bullied, repeatedly physically attacked or violently

assaulted, and eventually forced out of the core

(compound) area, where we provided additional

food on feeding platforms constructed up in the

canopy. If not moving voluntarily to the periphery,

so turning into outcasts, these monkeys could be

bitten to death by the invariably less bleached, more

aggressive, conspecific leading male(s). In retro-

spect, we recall that all neotonic, advanced meta-

chromic bleached and near-albinotic individual

monkeys kept free-ranging in our respective

halfway-houses by comparison were invariably

more soft-hearted, more sensitive, cooperative,

adaptable, and (not surprisingly?) smarter than the

male congeners by whom they were discriminated,

pushed into the periphery, or banned from the core

area. Applying these observations to the wild, the

trend to allopatry boosted by seemingly non-ad-

aptive social selection - leading males that discrim-

inate upon phenotypically deviant mutant young

males - in evolutionary sense could well turn out to

be truly adaptive. To cite Charles Darwin (1 859):

“ In the long history of humankind -and animalkind,

too- those who learned to collaborate and impro-

vise most effectively have prevailed ’ .And: “ It is not

the strongest of the species that survives, or the

most intelligent that survives. It is the one that is

the most adaptable to changer

Applying the doctrine to the evolution of hom-

inins, in particular Homo sapiens, one may ponder

and speculate about questions like the following:

“ Why, and driven by what force about six million

years ago somewhere in Tropical Africa an ape-like

lineage of primates -our hominid ancestors- left the

rain-forest canopy and ventured into an arid open-

savanna scrub landscape ? ”

The common ancestors of the Great Apes and

the human line of hominins ( Homo ) were arboreal

primates that had adopted brachiation (suspended

arm -over-arm -sw inging underneath the twig/branch

substrate) as a special locomotor pattern. Brachi-

ation allows large-bodied arboreal primates to

quickly move through the canopy and get to the

fleshy fruits that are, as is the rule in any tropical

rain-forest environment, distributed in the far peri-

phery (small- branch/twig micro-habitat) of canopy-

and emergent-tree tops. Brachiation is a primarily

arboreal type of locomotion that evolved exclus-

ively in some Neotropical Monkeys (i.e., spider,

woolly and woolly spider monkeys) as well as

in the Old-World Apes (i.e., gibbons, siamangs,

bonobos/pygm y chimps, chimpanzees, orang-utans,

and gorillas). It may never have evolved in Prosimi-

ans, which are the more primitive among all the

world’s primates. It followed an independent evol-

utionary path, a convergent or parallel evolution, in

a physiognom ically similar natural environment -

the tropical forests of Southeast Asia, Central

Africa, and South America (the larger Amazon

Basin). A major intercontinental difference is that

some monkeys in the Neotropics developed a pre-

hensile tail as extra support in suspensory loco-

motion, therefore called “sem i-brachiation”,

whereas apes during the evolutionary process

toward brachiation lost a functional tail. Brachiation

without use of a fifth limb is called “true brachi-

ation”. Most plausibly, our early ape-like hominid

ancestors that about 6 M YA descended from the can-

opy of C entral-A frican rain forest much resembled

extant Spider Monkeys in their general locomotor

pattern and diet. Brachiation is associated with a

dietary preference for ripe, pulpy, nutritious fruits

that contain a single to few large seeds. The upright

position of the trunk associated with an arboreal

life-style involving much brachiation happened to

be a crucial pre-adaptation for later bipedal (two-

legged) upright walking on the ground. It enabled

our early ancestors to leave the trees in the same

way as gorillas once did, but different in that

the Great Apes adopted ‘knuckle-walking’ as the

principal locomotor pattern to walk on the ground.

On the origin of allopatric primate species

195

Similarities between Spider Monkeys and Chim-

panzees are striking as we consider that at least

twenty-five million years of evolution on different

continents do separate these primates from one an-

other. Cognitive features that both brachiating

primates share are the mental capacity to visualize,

pre-plan, and map out in time and space complex

economic foraging routes to be followed that very

day, tomorrow, the day after tomorrow, and perhaps

even over several days ahead. Moreover, these

primates are able to lay out these foraging routes

across a landscape that is covered with dense trop-

ical rain forest containing only few seasonal, widely

dispersed food sources at any given time (Van

Roosmalen, 1 985a; 2013a). Consequently, both

spider monkeys and pygmy chimpanzees (bonobos)

may well depict a marked period or stage in the

evolution of our early ancestors that may have

specialized first in feeding upon ripe, juicy, lip id -

and protein-rich, large-seeded fruits. Perhaps, that

feeding niche may have been the condition that

predestined our ancestors, both locomotorily and

mentally, to leave the trees and become two-legged

ground-dwelling foragers with an advanced use of

the hands (e.g ., dexterity, precision grips, tool-

fashioning). And at the same time growing big

babies and three to four times bigger brains (Lynch

& Granger, 2008). In physical, anatomical, physiolo-

gical, and mental respect, therefore, descending

from the trees and adapting locomotorily to bipedal

walking and running over the ground was not the

‘near-impossible’ step that it may seem to be. If we

put it in Darwinian evolutionary perspective, how-

ever, to let it happen, until now an intraspecific

social driver was missing that must have acted on

the undoubtedly territorially and hierarchically

organized communities of these ape-like ancestors

with the brain size of contemporary chimpanzees

(400 cc). Forthcoming our thirty-five years living

in the Amazon and conducting long-term research

on captive, feral, as well as wild monkeys - the

latter mostly representing pristine populations that

were never in any way disturbed by humans - we

here suggest the ‘trend to allopatry’ among slightly

depilated and/or metachromic bleached male indi-

viduals (mutants) in primate populations being the

principal force that has driven founder-colonies of

our early ancestors - for the mere sake of survival -

out of their preferred habitat -canopy trees- into (to

them) new, with respect to natural enemies risky

and hostile landscapes. A s sociable and intelligent

mammals suffering from intraspecific population

pressures and discriminatory social constraints,

outcast males must have taken on the challenge to

traverse whatever barrier on their way out. So, they

ventured into the arid, in many aspects hostile

natural environment of savanna scrub and open

woodlands. In a similar way as a small population

of Gracile Capuchins on the slopes of tepuis like

Pico da Neblina successfully adapted to a predom -

inantly ground-dwelling life-style; the Mountain

Gorilla successfully adapted to a fully terrestrial

life-style in the cloud forests of the Virunga vulca-

noes in C entral A fric a ; the Western Chimpanzee of

the ‘subspecies’ VerilS once adapted to a predom-

inantly terrestrial life-style in an arid, for specialist

frugivores inappropriate or marginal natural envir-

onment - the open savanna scrub of West Africa

(Patterson et al., 2006); the near-albinotic Rio Javari

Fair Woolly Monkey with an overall cream-white

colored coat, and the Rio Jutai Orange Woolly

Monkey with an overall orange colored coat, ad-

apted to varzea floodplain forest along the upper

Amazon and lower Javari Rivers, and the upper

Jutai River, respectively; the Peruvian Yellow -tailed

Woolly Monkey in complete isolation adapted to

high-altitude cloud forest in the NE Peruvian

Andes; the advanced pheomelanin to near-albinotic

Bald-headed U akaris adapted to seasonally inund-

ated white-water floodplain forest (varzea) along

the Amazon River and some of its southern tributa-

ries that drain the southeastern flanks of the Andes;

among others. Looking at the distribution of

C en tral- A m eric an spider monkeys of the Ateles

geojfroyi Clade, we could speculate about an

imaginary evolutionary path that could have been

followed by an advanced metachromic bleached,

near-albinotic founder- colony of the Central Amer-

ican Yucatan Spider Monkey Ateles ( geojfroyi )

yucatanensis from the tropical forest of Yucatan

Peninsula in SE Mexico. By the ‘trend to allopatry’

forced out of the canopy of a semi-deciduous rain

forest somewhere on the Yucatan Peninsula - the

taxon’s current deadend distribution - some founder-

colony may venture into the savanna and desert

scrub of SE Mexico and from there further into the

Midwest of the US. To survive in such (for spider

monkeys) alien landscape it would quickly have to

loose a functional tail and adopt bipedal upright

walking as its main locomotor pattern. It is tempting

196

Marc G.M. van Roosmalen & Tomas van Roosmalen

to imagine a similar scenario for progressively

metachromic bleached, depilated, red- or white-

skinned near-albinotic early hominids 6 MYA

radiating away from their archetypic, saturated-

eu melanin congeners they had in common with

ancestral chimpanzees. Driven by the trend to allo-

patry, in a similar way founder-colonies may have

left the semi-deciduous rain forests of C Africa and

ventured first into the savannas, plains and desert

scrub of N Africa and, thereafter, into the tem-

perate-clime dominated landscape of S + C Europe,

the Middle East and SE Asia. Recent evidence from

molecular biology suggests that it took several hun-

dreds of thousands years for our early ancestors to

evolve in two distinct animals: the open savanna

explorers leading toward proto-humans, and those

remaining arboreal resulting in chimpanzees (Pat-

terson et al., 2006). In accordance with recent

phylogenetic research, the modern Chimpanzee

Pan troglodytes diverged from the proto- or ar-

chetypic, saturated eumelanin, overall blackish-

brown colored Bonobo (Pygmy Chimpanzee) Pan

panisCUS . The common Chimpanzee is an oppor-

tunist having an omnivorous diet, whereas the

Bonobo holds a predominantly specialist frugivor-

ous diet. In comparison to common Chimpanzees,

Bonobos are egalitarian, peaceable, non-violent

creatures that live in loosely organized, matriarchal

social groups in which the males may defend their

territories, but rather adopt a “M ake Love No War”

philosophy of life. Bonobos have never been repor-

ted to involve in raids on neighboring group males,

whereas common chimpanzees have been seen

performing a kind of troop-hunting culture in which

beta-males led by one alpha-male sometimes do

attack neighboring males or small mixed parties,

killing and eating some of them. Bonobos live in

the dense tropical rain forests of Central Congo.

Their distribution is thought to represent the cradle

of chimpanzee evolution or the center of chimpan-

zee (genus Pan) dispersion. Applying Hershkovitz’

hypothesis of m etachrom ism , Chimpanzees may

well have derived from (proto)-B onobos. Nowadays,

the two species are allopatric. The trend to allopatry

may have forced ancestral chimpanzees to swim

across or circumvent the Congo River that does act

as a geographic barrier in present-day distributions.

The farther in any but southern direction from

the center of Pan troglodytes dispersion, located

just north of the Congo River, the more arid the

landscape becomes, the more often chimps do

descend from the trees and ‘knuckle-walk’ on the

ground, and the more chimps have adapted to what

bonobos would consider inappropriate or marginal

habitat - unsuitable to highly specialized mature

fruit-eaters that bonobos are. At the same time, we

see chimpanzees becoming more pheomelanin

to euchromic bleached, their skin getting lighter

colored (less pigmented), their coat thinner and

locally depilated or almost hairless, and elderly

individuals becoming gray with age.

Another question to ponder about with the doc-

trine in mind: “ Why, and driven by what force some

of our Homo ancestors between 100,000 and

50.000 years ago left the origin and center ofhom-

inid dispersion -Central and North Africa being

considered the cradle of human evolution- to ven-

ture into the clime- and habitat-wise new, but un-

suitable or (at least ) marginal landscape of Europe,

the Middle East and Asia?”

A fter Homo ereCtUS having grown much bigger

brains on the plains, some millions of years later the

trend to allopatry may have been again the principal

driving force for some founder-colonies of Homo

Sapiens to move ‘Out of A frica’ . The pioneers that

ventured into new landscapes to the north could do

so only by occupying an ecological feeding niche

that was new to former small-game hunter-fisher-

gatherers, that of big-gam e hunter-gatherers. H ere by,

the invention to first carrying along fire, soon fol-

lowed by the skill to kindle it, was essential in the

adaptation process to a new feeding niche, as their

(our) digestive system is not apt to decompose raw

meat. It has to be cooked or barbecued. Apparently,

in very low densities - recent estimates place the

population of Europe 30,000 years ago at about

5.000 people - these humans following herds of

prehistoric megafauna (e.g., mammoth) and driving

them to extinction in the Holocene, have spread

rapidly across the whole of Europe and Southeast

Asia, one route taking them as far as Australia and

Tasmania, the other to the far northeastern corner

of Siberia. From these places they eventually could

reach and inhabit some Pacific Islands, and most

amazingly also the continent of South America, first

about 30-40,000 years ago by bordering the Antarc-

tic during one of the glacials, and a second time,

about 15,000 years ago, via Beringia and North

America (Van Roosmalen, 2013c). We could ask

ourselves if these all could have been advanced

On the origin of allopatric primate species

197

metachromic bleached, euchromic to albinotic

founder-colonies or colonizing parties that were

pushed out from dead-end distributions in Africa

and Asia following the male-territorial primate-born

trend to allopatry?

ACKNOWLEDGMENTS

We would like to dedicate the theory laid down

in this paper to the memory of Alfred Russel Wal-

lace (1 823-19 1 3), who inspired us to follow his

early footsteps into the Amazonian realm. We are

also immensely indebted to the late Philip Her-

shkovitz of the Chicago Field Museum of Natural

History, a true pioneer in the fields of primatology

and m etachrom ism . Many thanks are expressed to

Russell A. Mittermeier of Conservation Interna-

tional, who supported our fieldwork in the Amazon

ever since we started our careers in the pristine

ancient forests around the Voltzberg Mt in Suri-

name, also financially through the Margot Marsh

Biodiversity Foundation in the period 1998-2002.

We would like to thank Noel Rowe and Doug

B randon-Jones for reviewing an early draft of the

paper. Special thanks go to Stephen Nash of Con-

servation International who kindly provided us with

his very fine standardized color illustrations of all

known Neotropical monkey taxa. It enabled us to

build our theory on the equally colorful speciation,

radiation and diversification in New World prim-

ates.

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