BIODIVERSITY JOURNAL

2012,3 (I): 1-96.

Quaternly scientific journal

edited by Edizioni Danaus,

via V. Di Marco 4 1 , 90 1 43 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)

EDITORIAL STAFF

Managing Editor

Ignazio Sparacio - Palermo, Italy

Chief Editor

Maria Stella Colomba

University of Urbino “Carlo Bo”, Italy

Secretary

Fabio Liberto - Cefalu, Italy

Assistant Editors

Michele Bellavista - Palermo, Italy

Salvatore Giglio - Cefalu, Italy

Armando Gregorini

University of Urbino “Carlo Bo”, Italy

Tommaso La Mantia - University of Palermo, Italy

Nunzia Oliva - Palermo, Italy

Agatino Reitano - Catania, Italy

SCIENTIFIC COMMITTEE

Vittorio Aliquo - Palermo, Italy

Marco Arculeo - University of Palermo, Italy

Alberto Ballerio - Brescia, Italy

Maurizio Bombace - GMS Palermo, Italy

Attilio Carapezza - Palermo, Italy

Renato Chemello - University of Palermo, Italy

Alan Deidun - University of Malta, Msida, Malta

Gianniantonio Domina - University of Palermo, Italy

Gerhard Falkner - Deutsche Malakozoologische Gesellschaft, Germany

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

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

NathalieYonow - Swansea University, Swansea, Wales, U.K.

Federico Marrone - University of Palermo, Italy

Bruno Massa - University of Palermo, Italy

Pietro Mazzola - University of Palermo, Italy

Alessandro Minelli - University of Padova, Italy

Marco Oliverio - University of Roma, Italy

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

Salvatore Pasta - Palermo, 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 - University of Catania, Italy

Errol Vela - Universite Montpellier, France

upper: Nembrotha guttata (orange spots) with the

only Indian Ocean locality record of N. cristata

(green spots), Maaya Tila, Ari Atoll, 6-8 m depth,

March 1994 (photo H. Voigtmann); lower: N.

kubaryana, Tulamben, Bali, Indonesia, July 2010

(photo K. Lee). Cover: N. megalocera , Red Sea

(photo H. Sjoholm).

The genus Nembrotha (Bergh, 1877). The genus Nembrotha is widely distributed

throughout the tropical Indo-West Pacific, characterised by bright colours and

patterns. It belongs to the family Polyceridae, which are nudibranchs with a reduced

mantle margin, the presence of a frontal veil or ridge, and a group of gills located

forward or at the mid-dorsal point and have no pocket within which to retract. The

rhinophores are lamellate, sometimes a contrasting colour to the body, and issue

from a pocket with a raised rim which may be coloured. Many have large obvious

oral tentacles, often in a contrasting colour. With a long 'tail' many species can swim

using lateral flexions of the body. Species of Nembrotha appear to feed on ascidians:

their radular teeth, a good diagnostic character for most other species and genera, are

not very helpful in identification of species in this genus. The ribbon is narrow, with a

broad central tooth, a large hooked lateral tooth on each side, and a short scries of

small outer lateral plates on each side. N. megalocera Yonow, 1990 is a species

endemic to the Red Sea, and feeds on the violet ascidian Diazona. It is known to

swim, but mating and spawning have not been recorded. It has similarly coloured

sibling species in the Indian and Pacific oceans which never occur in the Red Sea;

equally, N. megalocera has not been recorded outside the Red Sea, even in the Gulfs

of Aden or Oman, which support a few Red Sea endemics. This is fairly typical of

species of Nembrotha, some species having a very limited distribution and no

external variation, whilst others have a large range and vary in colour and pattern.

Another species with a very limited range is N. guttata Yonow, 1994, which is only

found in one Indian Ocean island group, the Maldives archipelago. It belongs to a

small group of black species which have coloured pustules, interesting because most

species are linearly patterned. In this species the pustules are orange, with those

around the frontal margin and on the head edged in green. Nembrotha cristata

Bergh, 1 877 is a Pacific species known only from the Maldives in the Indian Ocean,

and has green pustules, green gills, and green rhinophore sheaths and tentacles. A

third species in this colour group is N. kubaryana Bergh, 1877, found in both the

Indian and Pacific oceans.

Nathalie Yonow. Conservation Ecology Research Team, Department of

Biosciences, College of Science, Swansea University, Singleton Park, Swansea

SA2 8PP, Wales, U.K.; email : n . vono w@swansea .ac.uk

Biodiversity Journal, 2012, 3 (1): 3-12

Lizards and Eleonora’s Falcon (Fa/co eleonorae Gene, 1 839), a

Mediterranean micro-insular commensalism

Michel Delaugerre 1 , Flavia Grita 2 , Pietro Lo Cascio 2 & Ridha Ouni 3

'Conservatoire du littoral, 3, rue Luce de Casabianca F20200 Bastia, France; e-mail: m.delaugerre@conservatoire-du-littoral.fr.

2 Associazione Nesos, via Vittorio Emanuele n. 24, 98055 Lipari (ME), Italy; e-mail: fgrita@gmail.com, plocascio@nesos.org.

Association de Sauvegarde du Patrimoine Environnemental et Naturel, Cap Bon, Sidi Thabet 2020, BP 23, Ariana, Tunis, Tunisia;

e-mail: elanion2003@yahoo.fr.

ABSTRACT Lizards and Eleonora’s falcon occur on many Mediterranean islets. Data given in literature

and new observations concerning their asymmetrical interactions, which have been reviewed

and illustrated, allow to regard those as a commensal relationship typical on these micro-in-

sular ecosystems. Some considerations on the ecological, ecomorphological and phenological

traits involved on this commensalism are also briefly discussed.

KEY WORDS Commensalism; lizards; Falco eleonorae ; island ecology; Mediterranean.

Received 24.01.2012; accepted 23.02.2012; printed 30.03.2012

INTRODUCTION

The Mediterranean micro-insular environments

constitute an apparent paradigm of simplicity. Islets,

usually hosting a low number of vertebrate species,

are generally regarded as ecosystems characterized

by chronic poorness in terms of trophic resources

(Blondel et al., 2010).

This condition can impose severe ecological

constraints to the species inhabiting the islets and,

on the other hand, it stimulates a certain degree

of flexibility and adaptability in their evolutionary

responses.

For instance, the exposition to less potential

competitors and predators, as well as the high po-

pulation densities, which often occur on islets, may

open new possibilities for enlarging trophic niche

and/or for establishing peculiar ecological relation-

ships among the island species.

Within the Mediterranean area, the lizards be-

longing to the suborder Sauria and the Eleonora’s

Falcon, Falco eleonorae Gene, 1839, are generally

the unique representatives of Vertebrates in the fau-

nal assemblages of islets, that also include rats and

few seabirds species.

The present paper aims to review and update the

knowledge concerning an apparently unusual rela-

tionship that occurs between these two emblematic

inhabitants of the Mediterranean small island eco-

systems (Fig. 1).

MATERIALS AND METHODS

Data from literature

Dionysades Archipelago (Crete, Greece)

The Dionysades (or Yianisadhes) Archipelago is

situated 20 km north of the eastern end of Crete,

and includes some uninhabited islets and rocks.

Among those, Paximada (314000 m 2 , 136 m

a.s.l.) harbours about 350 pairs of Falco eleonorae

and represents one of the most important nesting

site for the species at global level (Walter, 1979;

Dimalexis et al., 2007); also, there is a large po-

pulation of the endemic Cretan Wall Lizard, Po-

darcis cretensis Lymberakis et al., 2008 (see

Lymberakis et al., 2008).

M. Delaugerre, F. Grita, P. Lo Cascio & R.Ouni

Figure 1 . Geographical distribution of the sites where interactions between Eleonora’s falcon and lizards have been obser-

ved. 1) Paximada; 2) Skantzoura islets; 3) Cabrera islets; 4) 11 Toro; 5) Galita islets; 6) Scoglio Faraglione.

This islet has been intensely studied and moni-

torized since the Sixties by ornithologists. Walter

(1967) has observed in summer a high concentra-

tion of lizards around the falcons’ colony, which

daily were looking for scraps of preys, fearless in

entering on the nests even in the presence of adults.

According to this author, during the summer

months on this islet, lizards feed largely with the

help of falcons. In particular, he reports the case of

an adult female of Falco eleonorae that plucked a

prey in front a nest occupied by chicks, around

which four lizards were eating the flesh remains at-

tached to the carcass.

Another case concerns a lizard in the early mor-

ning that approached less than 20 cm to 15 days-

aged falcons, that observed with interest but leaving

it undisturbed, although the chicks usually eat eve-

rything that moves around the nest. However, he

also found in a nest some dead lizards that showed

visible signs of predation, but that have not been

eaten by falcons.

As possible explanation given for this finding,

the lizards may have approached too closely to the

chicks (or adults) during meals and, hence, have

been taken together with the prey and then thrown

away. Walter (1967) concludes that these interactions

can result partially unfavourable for the falcons, ha-

ving observed how the preys placed few meters

away from the nests are often quickly discovered

and almost emptied by lizards.

Sporades Islands (Greece)

To Schultze-Westrum (1961) are due the first re-

cords regarding the interactions between lizards and

Eleonora’s falcon. This author has reported obser-

vations carried out in late September 1957 at Ky-

riagos, a tiny islet belonging to the uninhabited

micro-archipelago of Skantzoura.

The local population of Erhard’s Wall Lizard,

Podarcis erhardii (Bedriaga, 1876), was almost ex-

clusively concentrated around the colony, attracted

by the remains of small birds preyed and deposited

close to the nests, as well as by the insects occurring

on the carcasses, while on the rest of the islet he did

not see any lizard.

Schultze-Westrum (1961) emphasizes that the

lizards were not scared by nestlings as well as by

adult falcons that usually do not hunt near their

nests, and considers such behaviour advantageous

also for the Eleonora’s Falcon, as indirect conse-

quence of a continue cleaning from insects and food

remains that would otherwise have rotted near the

nests. Curiously, in a more recent paper Schultze-

Westrum (2010) reminds similar behaviours for the

Lizards and Eleonora’s Falcon (Falco eleonorae Gene, 1 839), a Mediterranean micro-insular commensalism

lizards of another satellite of Skantzoura, namely

Strongylo, while doesn’t mention his previous ob-

servations on Kyriagos. Both islets, occupied by

medium-sized colonies of Falco eleonorae (Dima-

lexis et al., 2007), have a surface lesser than 1 ha

and a maximum altitude of about 50 m a.s.l.

Finally, Valakos et al. (2008) have referred that

on some islets of Sporades Archipelago also the en-

demic Skyros Wall Lizard, Podarcis gaigeae (Wer-

ner, 1930), lives in proximity of gulls and

Eleonora’s falcons, but not mentioning explicitly

the occurrence of interactions among these animals.

Cabrera Archipelago (Balearic, Spain)

This group includes an island and some satellite

islets situated around 10 km south of Mallorca (Ba-

learic Islands) and hosting small colonies of Eleo-

nora’s Falcon (Suarez, 2001) and several

populations of the endemic Lilford’s Wall Lizard,

Podarcis lilfordi (Gunther, 1874).

A number of observations carried out at L’lm-

perial (30500 m 2 , 73 m a.s.l.), Estels Xapat Gran

(11300 m 2 , 35 m a.s.l.) and Estels Xapat Petit (5700

m 2 , 45 m a.s.l.), off the S and SE coast of Cabrera

Gran, have been reported by Salvador (1980),

which visited these islets in early September 1976.

In one case, two lizards have translocated a carcass

of Reed Warbler, Acrocephalus scirpaceus (Her-

mann, 1804), from a nest where it had just been de-

posited by an adult falcon.

Other cases involve observations of lizards who

took the remains of preys in the nests and were cha-

sed away by falcons, but also others in which the li-

zards eat the remains of preys directly into the nests

without being molested by adults in the hatching of

nestlings.In addition, Salvador (1980) has found re-

mains of Song Thrush, Turdus philomelos (Brehm,

1831), European Robin, Erithacns rubecula (Lin-

naeus, 1758), and other three unidentified birds in

the stomach contents of some lizards from the islet

Estels Des Dos Cols (5100 m 2 , 35 m a.s.l.), where

another small colony of Falco eleonorae occurs.

II Toro Islet (Sardinia, Italy)

II Toro islet represents the southernmost point

of Sardinia and it is located 11 km S of Sant’An-

tioco Island. Its area is 132000 m 2 and maximum

altitude is 112 m a.s.l.

The local colony of Eleonora’s Falcon, compo-

sed by 70-80 nesting pairs, has a special historical

significance, as the type-specimen on which was

then described the species was captured in 1836 on

this islet. Two episodes of interaction between the

Tyrrhenian Wall Lizard, Podarcis tiliguerta (Gme-

lin, 1789), and Eleonora’s Falcon have been docu-

mented by Fadda & Medda (2001).

During a visit to the islet in September 2000,

these authors observed up to a maximum of six li-

zards engaged to contend the remains of a Blackcap,

Sylvia atricapilla Linnaeus, 1758, a short distance

from a falcon’s nest.

Furthermore, some lizards were able to steal a

prey, probably a warbler, brought by an adult in a

nest, dragging out it despite the presence of ne-

stlings. Similar cases were previously documented

for the same site also by the naturalist photographer

Domenico Ruju (in “Oasis”, number 5, Septem-

ber/October 1998). For Podarcis tiliguerta , also

Schneider (1986) has reported generically the oc-

currence of commensalism with Eleonora’s Falcon.

New records

Galita Archipelago (Tunisia)

The Galita (or Jalitah) Archipelago is situated

50 km off the northern coast of Tunisia. This island

group harbours about 80 nesting pairs of Eleonora’s

Falcon (Azafzaf, 2005) and some lizard species, wi-

thout those belonging to the genus Podarcis (Lanza

& Bruzzone, 1959; Delaugerre et al., 2011).

Many observations were recorded by one of us

(RO) on the islets of La Fauchelle (136000 m 2 , 137

m a.s.l.), Gallo (89000 m 2 , 119 m a.s.l.), and Gallina

(31000 m 2 , 60 m a.s.l.), during several field resear-

ches carried out in September 1996, 1998 and 2001.

In all the cases, the species interacting with Falco

eleonorae was the Ocellated Skink, Chalcides ocel-

latus (Forskal, 1775) (Fig. 2).

The activity of skinks resulted generally in-

tense in the surroundings of the colonies where

nestlings were aged between few days and about

2 weeks. Inside the nests have been seen up to

seven skinks simultaneously consuming the re-

mains of passerine.

M. Delaugerre, F. Grita, P. Lo Cascio & R.Ouni

This foraging activity took place exclusively on

ripped preys; only in one case, not directly related

to interactions with falcons and observed at La Fau-

chelle, a skink has attempted to extract a dead but

intact nestling from a nest of warblers.

Figure 2. Chalcides ocellatus feeds on remains of passerine

in a falcon’s nest; Gallo Islet, Gal ita Archipelago, September

2001 (photo R. Ouni).

Aeolian Archipelago (Sicily, Italy)

The archipelago is located 20 km off the north-

eastern coast of Sicily and comprises some islands

and a number of islets; one of these, Scoglio Fara-

glione (5700 m 2 , 33 m a.s.l.), is inhabited by the en-

demic Aeolian Wall Lizard, Podarcis raffonei

(Mertens, 1952) and is frequently used as hunting

territory and roost by the Eleonora’s Falcon, which

occurs nearby with 6-15 pairs in the island of Salina

(Lo Cascio, 2000; Corso & Gustin, 2009).

During a visit on 28 October 2011, three of us

(MD, FG & PLC) have observed for a long time se-

veral lizards eating the remains of a Common Sto-

nechat, Saxicola torquata (Linnaeus, 1766), while

they showed to ignore a killed but almost intact Eu-

ropean Robin placed few centimetres away.

The stonechat, although rather fresh, was al-

ready partially decomposed in the gash of the head,

containing ants and some larvae of flies (probably

calliphorids), while this latter perhaps had been just

recently left over by a falcon disturbed by our co-

ming. The occurrence of this food source has led

to a series of complex intraspecific interactions

(Figs. 4-5): a robust male lizard was very aggres-

sive versus other males as they approached the prey

but, at the same time, allowing some females to

feed on the carcass. Initially, lizards have surely in-

gested larvae and ants, but most time has been de-

dicated to an intense consumption of fleshy pieces

(Fig. 3) and feathers (Fig. 6).

During the consumption, the prey is dragged

from its original location by a lizard (Fig. 7); for

another islet of the same archipelago. La Canna

(3400 m 2 , 70 m a.s.l.), inhabited both by Aeolian

wall lizard and by Eleonora’s Falcon, Capula & Lo

Cascio (2011) have previously reported that lizards

often prey upon flies and other insects attracted by

falcon pellets.

DISCUSSION

The complex of interactions occurring between

Eleonora’s Falcon and lizards has been differently

interpreted by authors, e.g. as mutualism (Schultze-

Westrum, 1961; 2010), symbiosis (Salvador, 1980),

or kleptoparasitism (Fadda & Medda, 2001), while

only Walter (1979: 19) has regarded the lizards as

“true commensals” of Falco eleonorae.

Positive interactions among two species include

all non-consumptive interactions benefiting at least

one of the associated species but not impacting the

other; especially in the case of commensal interac-

tions, one species benefits and the other is unaffec-

ted (Dickman, 1992; Bertness & Callaway, 1994).

From this point of view, all the above mentioned

cases which have been documented for lizards and

falcons in the Mediterranean islets seem to fit well

to the widely accepted mean of commensalism.

Anyhow, access to food source by lizards has occa-

sionally involved its removal, outlining an asym-

metrical interaction that can be assimilated to

kleptoparasitism, although it likely began as a non-

antagonistic relationship among these species.

Possible or confirmed commensal interactions

between birds and reptiles are quite uncommon

(Thomas, 1890; Attwell, 1966; Christian, 1980 and

references therein; Gehlbach & Baldridge, 1987;

Gory, 2009), mostly of which may be truly referred

to cleaning symbiosis (sensu MacFarland & Reeder,

1974) rather than trophic commensalism.

This is perhaps also the case of interactions bet-

ween gulls and lizards reported by Kammerer

(1925) for some Adriatic islets, where the latter have

been observed eating ectoparasites of nestlings.

Lizards and Eleonora’s Falcon (Falco eleonorae Gene, 1 839), a Mediterranean micro-insular commensalism

Figure 3. Two Podarcis raffonei on the carcass of a Common Stonechat preyed by Eleonora’s Falcon; Scoglio Faraglione

Islet, Aeolian Archipelago, October 2011 (photo P. Lo Cascio). Figure 4. Intraspecific interactions between two specimens

of Podarcis raffonei'. above, the first lizard feeds on the carcass of a stonechat while the second (top left) approaching that

of a robin; in the middle, the second has neglected the robin and approaches the other one, even if already occupied by the

first lizard; below, the first attacks the second, showing a territorial behaviour. Figure 5. Another territorial behaviour: a

male (top left) and a female basking near the stonechat’ s remains while another female is feeding on the carcass. Figure 6.

A male eats a feather; to better perform the swallowing, the lizard repeatedly rubs its snout on the rocky soil. Figure 7.

During the consumption, the prey is dragged from its original location by a lizard.

M. Delaugerre, F. Grita, P. Lo Cascio & R.Ouni

In this perspective, the occurrence of commen-

salism between lizards and Eleonora’s Falcon takes

on particular interest, both for the extreme rarity

of this interspecific relationship among these ani-

mals and its uniqueness in the context of the Me-

diterranean.

Eleonora’s Falcon is a medium-sized, colonial

raptor, which from April- June to October-Novem-

ber occupies its breeding sites distributed in an area

ranging from Cyprus to Canary Islands.

Islets, especially those of the Aegean Sea that

harbour about 70% of its global population (estima-

ted as 6800-7400 pairs, see Burfield & Kreiser,

2004; Ristow, 2010), are crucial ecosystems for this

species, which needs isolation and the feeling of se-

curity to nest and breed successfully. Indeed, the

difficult access to remote slopes of small islands mi-

nimizes the human presence in these areas.

Falco eleonorae is basically insectivorous; ho-

wever, in coincidence with the hatching of chicks,

it preys almost exclusively upon passerine birds that

in late summer cross the Mediterranean during the

migration (Walter, 1979; Ristow et al., 1986).

Lizards are widely represented on the Mediter-

ranean insular ecosystems, in particular those be-

longing to the clade Gekkota as well as to some

genera (such as the lacertid Podarcis Wagler, 1830

and the scincid Chalcides Laurenti, 1768), but islets

are generally inhabited by few or even one species

(see Corti et al., 2006; Delaugerre & Cheylan, 1992;

Mateo, 1997; Mayol, 1997; Valakos et al., 2008).

Although their main food source is represented

by a wide variety of invertebrates, lacertid and scin-

cid lizards can have unusual feeding behaviours,

especially among islet populations. They include

herbivorism (Perez-Mellado & Corti, 1993; Saez &

Traveset, 1995; Van Damme, 1999; Lo Cascio et

al., 2008), kleptoparasitism (Cooper & Perez-Mel-

lado, 2003), cannibalism (Castilla & Van Damme,

1996; Pafilis et al., 2009; Dappen, 2011) or attacks

to dangerous preys normally avoided from lizards

(Castilla et al., 2008).

Also, a certain propensity to the consumption of

blood, fleshy remains and organic matter of verte-

brates by insular lizards has been empirically docu-

mented: e.g., on Lampione Islet (Channel of Sicily),

Moltoni (1970: 167) has found a maltese wall li-

zard, Podarcis filfolensis (Bedriaga, 1876), licking

“i liquidi che uscivano da un uovo nel quale il pic-

colo aveva gia rotto il guscio” [the fluids issuing

from an egg in which the chick had already broken

the shell]; and on Galitone, one of the islets belon-

ging to the Galita Archipelago, Captain Enrico

D ’Albertis noted that two lizard species, Chalcides

ocellatus and the Large Psammodromus, Psammo-

dromus algirus (Linnaeus, 1758), were mighty at-

tracted by the blood of falcons stored into his

game-bag: “allora spiumato un uccelletto che avevo

trovato presso un nido ne posi il corpicino nella re-

ticella da farfalle che portavo meco e tenni il ma-

nico di questa in una mano ... non tardarono le

incaute bestiole a slanciarsi sulla preda” [then, pluc-

king a bird that I had found in a nest, I put it in a

butterfly net that I had and held the handle in one

hand . . . the misguided creatures were not slow to

rush on the prey] (D’Albertis, 1878: 307).

A first, distinctive trait of the commensal inte-

raction between Eleonora’s Falcon and lizards is

its brief temporal context. Indeed, all the reported

observations were done in September-October,

when i) the diet of falcons becomes strictly orni-

thophagous, and ii) the prey availability for lizards

is substantially reduced (see Lo Cascio & Capula,

2011) and, therefore, the organic material carried

onto islets by falcons may represent a significant

nourishment.

Lizards can use this additional source of food

not only if they live near the colonies, but also when

inhabiting areas regularly used as roosts by falcons,

such as in the case of Scoglio Faraglione Islet.

Other noteworthy trait is represented by the relati-

vely large number of species so far recorded to be

involved as commensals in this interaction: five of

these belong to the lacertid genus Podarcis , and one

is the scincid Chalcides ocellatus.

This latter differs greatly from the others both

morphologically and ecologically: in fact, the ocel-

lated skink is described as semi-fossorial, sit-and-

wait forager in plant litter or under stones (Arnold,

1984; Kalboussi & Nouira, 2004; Lo Cascio et al.,

2008), whereas the foraging activity of lacertids

mainly occurs on the surface (Perez-Mellado &

Corti, 1993).

Nevertheless, both for Podarcis and for Chalcides ,

access to this food source involves an outstanding

effort in bite performance, because their dentition

smoothed and sharp mainly facilitates the crushing

(see Caputo, 2004; Metzger & Herrel, 2005). Ob-

servations carried out at Scoglio Faraglione, where

lizards have preferred a partially gashed bird but

Lizards and Eleonora’s Falcon (Falco eleonorae Gene, 1 839), a Mediterranean micro-insular commensalism

completely avoided another intact prey, may be ex-

plained with this morphological constrain and,

especially, with the difficulty of ripping fleshy pie-

ces from a plumed and more compact tissue.

A still open question, however, is whether this

seasonal switch from insectivory/arthropodivory to

true carnivory may be accompanied by phenotypic

specialisations in the trophic apparatus (Schwenk,

2000). Gut anatomy, enzymatic activity, microbiota

of the gastrointestinal tract may be involved by

physiological adjustments to a different diet (Ka-

rasov & Diamond, 1988; Karasov et al., 2011; see

also Pough, 1973).

Little information available on gastrointestinal

parasites of some lizard populations have so far

shown just their characterization as species typi-

cally associated to animals with insectivorous ra-

ther than herbivorous diet (Roca & Hornero,

1994; Roca et al., 2006), but didn’t give any indi-

cation on this concern.

In contrast, a factor which may have encoura-

ged the establishment of these interactions is re-

presented by the low risk for the lizards to be

predated by falcons.

Although some cases are given in literature

(Kruper, 1864; Araujo et al., 1977; Walter, 1979;

Salvador, 1980; D 0 I 9 Garcia & Dies Jambrino,

1991; Lo Cascio, 2000), there are no doubt that li-

zards appear with negligible percentages in the tro-

phic spectrum of Eleonora’s falcon; Walter (1979)

also observed that all the died lizards found in nests

were essentially untouched except for head and

back injuries, and remarks that these evidences sug-

gest as lizard should not be a food item of falcons,

but an occasional nuisance.

Besides, attendance in proximity to colonies

may provide an indirect protection from other bird

species that are primarily lacertophagous, such as

the Kestrel, Falco tinnunculus Linnaeus, 1758,

which usually are chased out from the breeding

sites by the Eleonora’s falcon.

The balance among these factors has probably

enhanced the development of commensal interac-

tions between lizards and falcons, both characteri-

zed by a long history of coexistence in small insular

ecosystems since many thousands of years (Bailon,

2004; Sanchez Marco, 2004 and references therein).

The occurrence of these interactions has been so far

documented for some islets, as reported in this

paper, but it could result probably more widespread

in the Mediterranean, as suggested by the recurring

finding of feathers and small plumes in the exami-

ned faecal pellets of lizards cohabiting with Falco

eleonorae on islets such as Strombolicchio, in the

Aeolian Archipelago, and Lampione, in the Channel

of Sicily (PLC, unpublished data).

ACKNOWLEDGMENTS

We wish to express our gratitude to Stephanie

Hanke, who has translated some german contribu-

tions; to Hartmut Walter, who gave us useful infor-

mation; to Bruno Massa and Emanuela Canale,

for the identification of the remains of common

stonechat.

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Biodiversity Journal, 2012, 3 (1): 13-40

Nematodes in aquatic environments: adaptations and survival

strategies

QudsiaTahseen

Nematode Research Laboratory, Department of Zoology, Aligarh Muslim University, Aligarh-202002, India;

e-mail: qtahseen@yahoo.com.

ABSTRACT Nematodes are found in all substrata and sediment types with fairly large number of species

that are of considerable ecological importance. Despite their simple body organization, they

are the most complex forms with many metabolic and developmental processes comparable

to higher taxa. Phylum Nematoda represents a diverse array of taxa present in subterranean

environment. It is due to the formative constraints to which these individuals are exposed in

the interstitial system of medium and coarse sediments that they show pertinent characteristic

features to survive successfully in aquatic environments. They represent great degree of mor-

phological adaptations including those associated with cuticle, sensilla, pseudocoelomic in-

clusions, stoma, pharynx and tail. Their life cycles as well as development seem to be

entrained to the environment type. Besides exhibiting feeding adaptations according to the

substrata and sediment type and the kind of food available, the aquatic nematodes tend to wi-

thstand various stresses by undergoing cryobiosis, osmobiosis, anoxybiosis as well as thio-

biosis involving sulphide detoxification mechanism.

KEY WORDS Adaptations; fresh water nematodes; marine nematodes; morphology; ecology; development.

Received 24.01.2012; accepted 23.02.2012; printed 30.03.2012

INTRODUCTION

The diversity of animal life is not distributed

uniformly across the world and its diversification is

not an automated process but requires some charac-

teristics of form and function that allow successful

exploitation of new habitats. Such species are, the-

refore, considered "plastic" or "malleable" that with

modifiable genetic material can change or adapt

when subjected to evolutionary selective pressures.

Nematodes, the most numerous of all Metazoa in

number of individuals, exist in all habitats that can

support life.

Being ubiquitous, they can be as dynamic as the

habitat types and can change through time. With a

deceptively simple anatomical design, they are re-

ferred as typical representatives of Metazoa (Nelson

et al., 1982). However, they are the most complex

forms with many metabolic and developmental pro-

cesses comparable to higher taxa; they demonstrate

remarkable abilities to withstand stress and adverse

conditions. The nematode Caenorhabditis elegans

(Maupas, 1900) survived the crash of space shuttl,

Columbia that hit the ground with an impact 2,295

times the force of Earth's gravity (Cosgrove-Ma-

ther, 2003).

Many species survive the unfavourable condi-

tions by demonstrating anhydrobiosis, cryptobiosis,

osmobiosis or cryobiosis. The key to their success

in all types of ecosystems and biotopes is their mor-

phological plasticity, physiological adaptability and

ecological diversity.

Nematodes are basically aquatic animals that re-

quire a film of water to move. They may exist as

free-living, commensals or parasites in all types of

aquatic habitats viz., freshwater, brackish, marine

systems; in extreme environments including sea-ice

to hydrothermal vents. They may be found in clay,

QudsiaTahseen

gravel, epiphytes, on sea grasses and algae. Their

vermiform, soft and flexible bodies are well suited

to allow bending in the interstitial system of sand

grains/particles (Heip et al., 1985; Strayer, 1985;

Traunspurger, 1996 a, b).

A number of factors affect their distribution viz.,

seasons, latitude, water depth, geochemical proper-

ties of the sediment, temperature, salinity, water

movement, oxygen content, species interaction, re-

source partitioning and predation (Jensen, 1981;

1987a; Joint et al., 1982; Bouwman et al., 1984;

Platt & Lambshead, 1985; Olafsson, 1992; Giere,

1993; Hendelberg & Jensen, 1993; Soetaert et al.,

1994; Modig & Olafsson, 1998; Steyaert et al.,

1999; Wetzel et al., 2002; Armenteros et al., 2009).

The present article highlights the habitat-speci-

fic features of aquatic nematodes, their adaptations

and compatibility to the environmental conditions.

Major aquatic groups

Phylum Nematoda includes a diverse array of

taxa specific to a variety of aquatic habitats. The ty-

pical composition of the freshwater meiofauna dif-

fers much from that in marine realm with

nematodes more numerous in sediments than in the

water columns (Bell & Sherman, 1980; Sibert,

1981). Most species of Chromadorea are found in

fresh water ecosystems with the exception of few

tylenchids, aphelenchids and rhabditids whereas

only few species are reported from polar freshwa-

ters (Maslen, 1979).

The species of Araeolaimida, Monhysterida as

well as Chromadorida inhabit both fresh water as

well as marine environments (De Ley et al., 2005).

In Enoplea, the fresh water representatives mainly

belong to Triplonchida, Mononchida, Dorylaimida

and Mermithida and to a lesser extent Enoplida. The

taxa Enoplida, Desmoscolecida, Chromadorida and

Monhysterida are predominantly marine. About

4000 species of free-living marine forms have been

accounted through various faunal surveys (Jensen,

1981; Sharma & Webster, 1983; Vanreusel et al.,

1992). Estuarine nematodes show greater taxono-

mic affinities to freshwater nematodes and can to-

lerate significant changes in salinity (Forster, 1998;

Warwick, 1981a).

The nematode species with fresh water affilia-

tions are most abundant at the upper edge of the in-

tertidal zone where the marine influence is often

weak (Nicholas et al., 1992).

Morphological characteristics

The aquatic nematodes are quite varied morpho-

logically and no single species can be considered a

true representative. However, the similarity in fresh

water as well as marine forms on account of their

aquatic habitats reflects convergent evolution. Most

aquatic nematodes have elongated cylindrical bo-

dies of about one to several millimeters length ex-

cept ~9 m long whale parasite Placentonema

gigantissima (Gubanov, 1951). The dark subterra-

nean environment has led to loss or reduction in

body pigmentation, hence, the nematodes appear

whitish-semi transparent or transparent.

They are characterized by slender, spindle-

shaped bodies with enhanced swimming abilities.

Wriggling or undulatory propulsion by alternate

pushing and bending, is typically found due to

presence of only longitudinal musculature. Howe-

ver, some aquatic species can "jump" by bending

of their bodies followed by a sudden relaxation

(e.g. Theristus).

The members of Epsilonematidae and Draco-

nematidae move by "looping" with an alternate

adhesion and detachment of their anterior and po-

sterior body ends whereas the desmoscolecids

move by contractive waves.

The cuticle of aquatic nematodes may be smo-

oth (most Enoplidae), annulated (Desmodoridae,

Desmoscolecidae, most Monhysteridae), punctated

(Cyatholaimidae, many Chromadoridae, Comeso-

matidae), or provided with complicated and com-

pact structures (many Chromadoridae).

There may be diverse types of cuticular modifi-

cations (Figs. 1-3, 5, 9, 10). Some nematodes may

have longitudinal ridges or alae (Figs. 11-13, 15,

16, 18) aiding in swimming. Punctations in the

form of dots (punctation) or pores arranged irre-

gularly or in rows, are also common in many aqua-

tic taxa (Figs. 8, 9, 14). The punctations may fuse

into compact structures in many chromadorids

(e.g., SpilophoreUa paradoxa de Man, 1888;

Chromadorella spp.). Often the cuticular surface is

covered with a dense “fur” of ectosymbiotic sulfur-

oxidizing bacteria to thrive in sulfur-rich marine se-

diments (Nussbaumer et al., 2004; Ott et al., 2008).

Aquatic nematodes usually possess long, hair-

like sensilla called setae, relatively more developed

in marine forms, compared to slightly-raised or

mammellate sensilla of terrestrial nematodes. Body

(somatic) sensilla (commonly found in Monhysterida,

Nematodes in aquatic environments: adaptations and survival strategies

Figures 1-9. Cuticular modifications.

Figs. 1-3: Epsilonema pustulatum after Karssen et al. 2000. Fig. 4: Desmoscolex sp. Fig. 5: Glochinema sp.

Fig. 6: Plectus sp. Fig. 7: Goezia leporini after Martins and Yoshitoshi, 2003. Fig. 8: Cruznema sp. Fig. 9: Achroma-

dora sp. (Scale bar: 1-3, 7 =1 pm; 4-6, 8, 9 = 10 pm).

QudsiaTahseen

Figures 10-18. Cuticular modifications.

Fig. 10: Epsilonema pustulatum after Karssen et al., 2000. Fig. 11: Mononchoides sp. Fig. 12: Fictor sp.

Fig. 13: Plectus zelli. Fig. 14: Pelodera teres. Fig. 15: Diplogastrellus sp. Fig. 16: Panagrellus sp. Fig. 17: Dorylaimus

sp. Fig. 18: Chiloplacus sp. (Scale bar: 10 = 1 pm; 11-18 = 10 pm).

Nematodes in aquatic environments: adaptations and survival strategies

Araeolaimida, Chromadorida and Enoplida) may be

arranged in rows or distributed randomly; in ab-

sence of eyes, the symmetry of the tactile sensilla

and the flexible body serve to guide the crawling

worm between sand grains, debris etc. In aquatic

habitats the nematode setae of 5 to 10 pm length

dominate with shortest setae mostly found in nema-

todes of littoral zone. Other types of sensilla include

caudal setae (Figs. 110, 111) and terminal setae

(Figs. 102, 111, 113, 114, 117).

The terrestrial nematodes usually have the pri-

mitive arrangement (Fig. 32) of labial sensilla (6

inner labials + 6 outer labials + 4 cephalics) con-

trary to the configuration in many aquatic nemato-

des (6 + 10) where outer labials are situated at the

level of cephalic sensilla (Fig. 23) or there may be

additional setae (Figs. 24, 28). The jointed setae

(Fig. 23) found in some aquatic nematodes are com-

parable to jointed appendages of arthropods indica-

ting some relationship among these ecdysozoans.

Amphids, the bilaterally symmetrical sensory

structures demonstrating the first evidence of cilia,

are involved in many behavioural functions and are

comparable to olfactory organs. Coomans (1979) sug-

gested a mechanoreceptive, secretory as well as pho-

toreceptive function to amphids.

In aquatic nematodes, the amphids are relatively

complex, conspicuous and post-labial and mainly

circular (Figs. 20, 22, 28), loop-shaped (Figs. 72,

73), spiral, (Figs. 64, 65, 78), shepherd's crook, poc-

ket- like and rarely pore-like compared to the am-

phids of land-dwelling nematodes that are usually

pore-like or slit-like (Figs. 25, 31, 32) and occasio-

nally round or spiral-shaped. Although there is little

physiological evidence for photosensitivity in ne-

matodes, ocelli have been defined as discrete pho-

toreceptors (Croll, 1970) and commonly found in

marine genera viz., Thoracostoma Marion, 1870,

Phanoderma Bastian, 1865, Eurystomina Filipjev,

1921, Calyptronema Filipjev, 1921 etc.

Species may be provided with compact conglo-

merations of pigments (Figs. 81, 94, 95) viz., Eno-

plus spp., Pseudocella trichodes (Feuckart, 1849),

with diffuse pigments in the cervical region inside

pharynx ( Deontostoma Filipjev, 1925; Oncholai-

mus Dujardin, 1845 and Chromadorina Filipjev,

1918) or outside pharynx in epidermis/pseudocoe-

lom {Araeolaimus de Man, 1888). Eye spots are

often provided with a hyaline “lens” or comparable

structure (Fig. 93) e.g., Symplocostoma Bastian,

1865 and Araeolaimus.

The utility of ocelli in aquatic habitats with par-

ticular reference to marine environment, is the ne-

gative phototaxis to move to deeper layers/strata, as

observed in Chromadorina bioculata (Schultze in

Carus, 1857); Oncholaimus vesicarius (Wieser,

1959); Enoplus anisospiculus Nelson et al., 1972

(Croll, 1966; Croll et al., 1972; Bollerup & Burr,

1979; Burr & Burr, 1975; Burr, 1979; Burr, 1984).

It probably explains the absence of ocelli in nema-

todes inhabiting littoral sand. Few nematodes use

photosensitivity to determine the photoperiod for

successful completion of life cycle. Haemoglobin

instead of melanin, in some nematodes including

mermithids, serves an optical and light-shadowing

function (Ellenby, 1964; Ellenby & Smith, 1966;

Croll & Smith, 1975; Burr et al., 2000).

The metanemes (Fig. 92) are spindle-shaped/fi-

lamentous proprioceptors (Hope & Gardiner, 1982)

or stretch receptors (Forenzen, 1978, 1981), found

in the lateral hypodermal chords of marine enoplids

(e.g., Enoplus Dujardin, 1845; Deontostoma and

Oxyonchus Filipjev, 1927) lying parallel or at an

angle of 10-30° to the main body axis. Metanemes

are sensitive to the dorsoventral bending of nema-

tode body thus controlling the body volume.

Some marine enoplids especially Thoracosto-

mopsidae possess a pair of sense organs known as

cephalic slits (de Man, 1886) or cephalic organs (Fi-

lipjev, 1927), latero-ventrally placed between the

circlets of the labial sensilla (Fig. 96). The cephalic

organs may possess club-shaped cirri (chemosen-

sory/mechanosensory) in species having powerful

buccal armature (Wieser, 1953) e.g., Oxyonchus

dentatus (Ditlevsen, 1918) Filipjev, 1927.

Crystalloids (Figs. 82, 83), the crystal-like in-

clusions or irregular electron dense deposits (Fig.

84) occurring subcutaneously or in pseudocoelom,

have been observed in many fresh water (e.g., Mon-

hystera Bastian, 1865; Ironus Bastian, 1865; Tobri-

lus Andrassy, 1959; Tripyla Bastian, 1865) sensu

Aleksey ev and Dizendorf, 1981; Andrassy 1958,

1981, 1984; Juget, 1969; Micoletzky, 1922, 1925;

Riemann, 1970; Jacobs & Heyns, 1990) and marine

nematodes e.g., Sabatieria Rouville, 1903; Sphae-

rolaimus Bastian, 1865; Terschellingia de Man,

1888 (Nicholas et al., 1987). The ultrastructural,

ecophysiological and physical microanalysis further

revealed high sulphur content of the osmiophilic

and homogeneous crystalloids (Nuss & Trimkow-

ski, 1984). Other reports suggested their role in de-

toxification or preventing harmful accumulation of

QudsiaTahseen

metal sulphides in the tissues (Nuss, 1984; Nicholas

et al., 1987) or in storing food during adverse con-

ditions (Bird et al., 1991).

Body pores (Figs. 85, 86) are common among

many Enoplea. Generally a body pore leads through

a canal to a unicellular, merocrine hypodermal

gland (Fig. 87) and an associated bipolar neurocyte

e.g., Chromadorina germanica (Butschli, 1874).

However, Electron Microscopy revealed multivesi-

cular complexes similar to Golgi bodies (Lippens,

1974). Some marine worms e.g., Ptycholaimellus

ponticus (Filipjev, 1922) Gerlach, 1955 with a sy-

stem of body pores and hypodermal glands mo-

dify the sedimentary microenvironments by

building tubes (Hope & Murphy, 1969).

The diversity in nematodes revolves mostly

around the evolution of stoma and one or more

pharyngeal bulbs. The stoma or buccal cavity,

usually a triradiate structure bounded by three or

six lips, exhibits variations reflecting the different

feeding modes (Wieser, 1953; Jensen, 1987b;

Moens & Vincx, 1997; Traunspurger, 1997.

The buccal cavity may be absent or minute

(Figs. 48-51) to spacious, unarmed type (Figs. 33,

34) in non selective deposit feeder species. The ne-

matodes feeding on diatoms possess a buccal cavity

armed with small to moderate-sized teeth (Jensen,

1982; Romeyn & Bouwman, 1983; Romeyn et al,

1983; Moens & Vincx, 1997). The buccal cavities

of powerful predators may further be armed with

immoveable armature/teeth (Figs. 37-40, 52-59),

rows of small denticles or moveable structures ter-

med mandibles or jaws (Figs. 60, 63).

Pharynx, the anterior muscular part of the gut

with a tri-radiate lumen does not show habitat- wise

specificity but largely varies according to the fee-

ding modes. In marine nematodes the pharynx is

largely cylindrical with posterior part gradually

expanding, occasionally forming a muscular bulb.

The dorsal gland orifice usually opens through the

stegostom while pharyngeal gland nuclei are lo-

cated in basal part. The pharyngeo-intestinal jun-

ction (cardia) and intestine do not show aquatic

adaptations.

The secretory-excretory cell (renette cell =

ventral gland, cervical gland or excretory cell)

opens through a ventral pore between mid pharynx

to anterior intestine (Bird & Bird, 1991) except

Monhystera disjuncta Bastian, 1 865 and some Iro-

nidae having a labial location (Van de Velde &

Coomans, 1987). In marine nematodes, the well de-

veloped renette cell has secretory role in tube-buil-

ding e.g., Ptycholaimellus Cobb, 1920 (Jensen,

1988). The secretory role has been also verified in

Sphaerolaimus gracilis de Man, 1876 (Turpeen-

niemi & Hyvarinen, 1996) and Monhystera disjun-

cta (Van De Velde & Coomans, 1987).

The number and structure of ovaries along with

other genital components though taxonomically im-

portant, do not show much difference from those of

terrestrial nematodes and are largely specific of higher

taxa (Lorenzen, 1981, 1994). Ovaries in aquatic ne-

matodes generally tend to be long and well develo-

ped reflecting high fecundity. Likewise the position

of vulva usually varies from middle (e.g., members

of Tobrilidae, Plectidae etc.) to posterior (e.g., mon-

hysterids) in aquatic nematodes.

The females are usually didelphic-amphidelphic

with antidromously reflexed (outstretched in Cyto-

laimium exile Cobb, 1920) ovaries. However, mon-

hysterids represent mono-prodelphic females while

the gonad can be mono-opisthodelphic in most spe-

cies of Alaimidae. There is a connection between

the reproductive and digestive systems in some On-

cholaimidae through demanian system (Figs. 97-

101), which varies from simple (e.g., Viscosia de

Man, 1890) to highly-developed one (e.g., Adon-

cholaimus Filipjev, 1918 and Oncholaimus).

The demanian system serves the functions of

maintaining viability of spermatozoa, releasing a

sex attractant, facilitating egg deposition and tran-

sfer of sperm to the intestine, and elimination of ex-

cess sperms deposited in females through the

digestive system (Eyualem et al., 2006). The aqua-

tic male nematodes may possess one (monorchic)

or two (diorchic) testes largely depending on the ta-

xonomic group they belong to. Typically, the cuti-

cularised spicules and gubemaculum and the genital

supplements/papillae are also not habitat-specific.

Most aquatic nematodes possess long filamen-

tous tails and propel themselves faster by its whipping

action (Gerlach, 1953, 1971; Wieser, 1959; Warwick,

1971; Riemann, 1974). Nevertheless, the tail shape can

be variable from round, conical, cylindroid-clavate to

elongated-filiform (Figs. 102-112). In most marine ne-

matodes it may be provided with caudal setae, speci-

fically confined to terminus as terminal setae (Fig.

111). Often the bluntly-rounded tail terminus bears a

spinneret- the outlet for caudal glands’ (Figs. 113-117)

sticky secretion (Distem) that helps in anchorage to an

object or substratum. This phenomenon of nictation is

a foraging adaptation in aquatic nematodes.

Nematodes in aquatic environments: adaptations and survival strategies

30 31 32

Figures 19-32. Modifications in anterior sensilla.

Fig. 19: Chronogaster sp. Fig. 20: Monhystera sp. Fig. 21: Mononchus aquaticus. Fig. 22: Hoffmanneria sp. Fig. 23: Pri-

smatolaimus sp. Fig. 24: Sabatieria lyonessa. Fig. 25: Xiphinema sp. Fig. 26: Goezia leporini after Martins & Yoshitoshi,

2003. Fig. 27: Rhaptothyreus sp. Fig. 28: Epsilonema pustulatum after Karssen et al., 2000. Fig. 29: Theristus sp.

www.nem.wur.nl/UK/ln+the+picture/Gallery/. Fig. 30: Camallanus tridentatus after Santos & Moravec, 2009. Fig. 31:

Cephalobus sp. Fig. 32: Myctolaimus kishtwarensis Hussain, Tahseen, Khan & Jairajpuri, 2004(Scale bar =10 pm).

QudsiaTahseen

34 35

Figures 33-47. Modifications in anterior sensilla.

Fig. 33: Paramesonchium sp. Fig. 34: Cervonema sp. Fig. 35: Prodesmodora sp. Fig. 36: Rhabdocoma sp. Fig. 37: Apha-

nolaimus sp. Fig. 38: Amphimonhystera sp. Fig. 39: Platycoma sp. Fig. 40: Wieseria sp. Fig. 41: Ceramonema sp.;

Fig. 42: Diplopeltoides sp. Fig. 43: Paramesaccmthion sp. Fig. 44: Pheronous sp. Fig. 45: Cyatholaimium sp. Fig. 46: 7b-

brilus sp. Fig. 47: Coninckia sp.

Nematodes in aquatic environments: adaptations and survival strategies

Reproduction and development

Reproductive mechanisms do differ among ne-

matodes in different habitats. Mostly marine nema-

todes are dioecious and amphimictic with obligate

bisexuality thus enhancing the chances of fertiliza-

tion and promoting high genetic variation. Howe-

ver, sex ratio is significantly influenced by

temperature in Pellioditis marina Bastian, 1865

(Rhabditidae) and Diplolaimelloides meyli Timm,

1961 (Monhysteridae), with more males at higher

temperatures (dos Santos et al., 2008).

Amictic reproduction is mostly common in the

spatially and temporally variable environments

(Townsend et al., 2003) thus conforming well to the

large proportions of species without males in varia-

ble marine habitats or in occasionally stressed ha-

bitats (Nicholas, 1975). The sex ratio in some

marine forms lean towards femaleness to reproduce

more in order to sustain in the unstable environ-

ment. The changes in growth rate as well as the du-

ration of life cycle are further indicative of the

volatility of environment (Palacin et al., 1993).

The fresh water species inhabiting shallow

water bodies or those subject to repeated drying

and wetting, tend to be without males (Grootaert,

1976; Wharton, 1986; Ocana, 1991a) thus opting

for parthenogenesis e.g., Enmonhystera Andrassy,

1981; Plectus Bastian, 1865; Rhabdolaimns de

Man, 1880. Organisms living in isolated and un-

stable habitats have evolved cryptobiosis, self-fer-

tilization, and passive dispersal, benefiting them in

the challenging conditions.

Life cycle stages often provide a means of sur-

viving changes in the environment. The laid eggs,

with their sticky/complex rugose/spinose shell

(Figs. 90, 91) surface, adhere to sediment particles.

The eggs may further be provided with entangling

devices such as byssi or polar filaments to resist

water current in fresh water habitats. Experimen-

tally a 5°C increase in temperature produces up to

a six-fold increase in the number of eggs laid (War-

wick, 1981c). The sperms of some aquatic nemato-

des may possess a pseudoflagellum (a protoplasmic

hair) unlike the typically round or amoeboid (cra-

wling) sperms of terrestrial forms. Retention of the

nuclear envelope in mature spermatozoa has also

been reported (Lee, 2002). One unique feature

found in some marine species is traumatic insemi-

nation (Maertens & Coomans, 1979; Chabaud et al.,

1983; Coomans et al., 1988), a type of copulation

not occurring through vulva, but through punctu-

ring of the cuticle followed by the formation of ter-

minal ducts as a part of the demanian system. The

excess sperms are thus discharged into the intestine

(Coomans et al., 1988).

The aquatic habitats with high wave action also

led to conditions of ovoviviparity in nematodes.

Monhystera paludicola de Man, 1880 shows intra-

uterine hatching thus avoiding the risk of loosing

the eggs in fast- flowing waters (Hofmanner, 1913;

Hofmanner & Menzel, 1915; Juget, 1967). Al-

though facultative ovoviviparity has been also ob-

served in the shallow water populations, this

characteristic was frequently expressed in toxic en-

vironments (Van Gaever et al., 2006). Some spe-

cies of Monhystera are characterised by a

specialized uterus with associated cells and glands

(Figs. 88, 89) and a spermatheca.

The uterus is elongated and its length increases

with age ( Jacobs & Heyns, 1990) so as to hold and

protect greater number of developing juveniles in

stressed conditions (Otto, 1936; Schiemer et al.,

1969; Otto & Schiemer et al., 1973). The highly in-

determinate mode of cell division (Justine, 2002) in

some aquatic enoplids contrary to normal determi-

nate/ mosaic cell division tends to regulate the de-

velopment in stressed environments.

In some marine nematodes, such as Pellioditis

marina the cell lineage with polyclonal cell fate di-

stribution allows a faster embryonic development

by reducing the need for cell migrations (Houtho-

ofd et al., 2003) resulting in extremely short gene-

ration time (Moens et al., 1996). Many small

species have short generation times of usually

about one month or less (Gerlach, 1971; He ip et

al., 1985). However, the period of development va-

ries from 3 days in Rhabditidae to 12 months in

some Chromadoridae and Enoplidae (Houthoofd et

al., 2003). Faster development shortens the vulne-

rable period of embryo to disturbances thus pre-

venting embryonic deformities and/or arrest.

Nevertheless, the generation time and fecundity are

markedly temperature dependent.

Another aquatic bacterivore Rhabdolaimns is

stated to survive as dauer stage in warm dry and

acidic soils (Dmowska, 2000; Beier & Traunspur-

ger, 2001). It has been reported that marine nema-

todes from oligotrophic regions of ocean are

smaller in size than those from sites showing hi-

gher level of organic matter flux (Udalov et al.,

2005). Such smaller nematodes produce fewer eggs

than larger nematodes.

QudsiaTahseen

This leads to the lower rate of reproduction

and therefore, to the lower proportion of juveni-

les. The “male: female” ratio tends to be 0.7 while

a ratio of 0.4-0. 6 has been found in nematode

communities from deep-sea hydrothermal vents

(Zekely et al., 2006).

Ecological adaptations

Tight reaches only in the upper layers of the

water column; hence photosynthesis is limited to a

few 100 meters water depth. The main energy

source for deep bottom dwellers, therefore, comes

from the primary production at the surface. The or-

ganisms inhabiting this niche are mostly extremo-

philes, tolerant of extremely low temperatures

(<0°C) and have an adaptation to high pressure as

well. Aquatic nematodes, like their terrestrial coun-

terparts, serve as food for small invertebrates or

fungi and can be categorized as herbivores, carni-

vores, omnivores, predators, bacterivores and fun-

givores with a range of food sources viz., algae,

diatoms, aquatic vegetation, bacteria, fungi, other

small invertebrates including nematodes.

Tittoral macrophytes, their associated periphy-

tons and free-floating biofilms also provide limited

in situ resources for nematodes (Peters & Traun-

spurger, 2005). The nature of the organic substrate

in the environment changes with time. Different

food supplies influence species compositions and

their succession (Ferris & Matute, 2003; Ruess,

2003; Ruess & Ferris, 2004; Michiels & Traun-

spurger, 2005; Ferris & Bongers, 2006) directly as

well as indirectly.

During the settling of food resources from sur-

face to deep floor, much of the photo synthetic deri-

ved material is mineralized. Larval forms of

soft-bodied marine invertebrates including nemato-

des are adapted to take advantage (Manahan, 1990)

of the organic carbon as dissolved organic material

(DOM). In marine environments, the meiofauna

builds the trophic linkage between bacteria and ma-

crobenthos (Kuipers et al., 1981) and constitute an

energy sink (McIntyre, 1969).

Besides the direct consumption of detritus, ne-

matodes carry out double remineralization and

cycle in carbon twenty times their mass annually

(Platt & Warwick, 1980). Thus nematodes facilitate

the detrital conversion by mechanical breakdown

of the detritus, excretion of limiting nutrients to

bacteria, producing films conducive to bacterial

growth and by bioturbating sediments around detri-

tus (Riemann & Schrage, 1978; Meadows & Tufail,

1986) hence increasing porosity and light penetra-

tion. Thus the meiofaunal nematodes affect mat

communities through bioturbation and grazing

(Hdckelmann et al., 2004).

The habitat preference has been observed in

some marine nematode families (Tietjen, 1977) e.g.,

muds: Comesomatidae, Linhomoeidae; muddy

sands: Comesomatidae, Monhysteridae, Desmodo-

ridae, Linhomoeidae; fine sands: Monhysteridae,

Comesomatidae, Desmodoridae, Axonolaimidae;

medium-coarse sands: Monhysteridae, Desmodori-

dae, Chromadoridae; clean, coarse sands: Epsilone-

matidae and families of Draconematoidea. Current

transport apparently plays a significant role in the

dispersal of certain meiobenthic nematodes.

However, the nematodes occurring in the surfa-

cial layers of the sediments seem to be the most af-

fected (Witthoft-Muhlmann et al., 2007). Some

species like Sabatieria pukhra (Schneider, 1906)

and Odontophora setosa (Allgen, 1929) found in

the deeper sediment layers are rarely suspended

(Eskin & Palmer, 1985). The species diversity and

the occurrence of the nematodes are influenced

mainly by wind speed and river discharge. In calm

weather and low discharge, species diversity is re-

duced and deposit feeders dominate.

The feeding habits can be inferred from the phy-

siognomic characters of buccal cavities (Wieser,

1960; Wieser & Kanwisher, 1961; Boucher, 1973;

Platt, 1977; Romeyn & Bouwman, 1983; Jensen,

1987b) and associated structures (Bouwman et al.,

1984) in aquatic species. The epistrate feeders e.g.,

Eudiplogaster paramatus ( Schneider, 1938); Chro-

madorita tennis (Schneider, 1906) etc. are toothless

or possess a small tooth in buccal cavity to break

open cell membranes and suck out the cell contents

(juice feeders); deposit feeders (particulate feeders)

with or without tooth, swallow the whole food item

and prevent its escape e.g., Daptonema biggi (Ger-

lach, 1965) Lorenzen, 1977 (swallowing diatoms),

Linhomoens gittingsi Jensen, 1986 (engulfing sul-

phide-oxidising bacteria.

Sediments with high silt content generally show

abundance of deposit- feeders (Heip et al., 1985)

usually scoring 2 or 3 on the coloniser-persister

scale (Bongers et al., 1991, 1995), characterised by

short life cycles and a high colonisation ability

(Schratzberger et al., 2007). Predators with buccal

cavities armed with movable/protrusible mandibles

Nematodes in aquatic environments: adaptations and survival strategies

Figures 48-63. Modifications in stoma.

Fig. 48: Bujaurdia sp. Fig. 49: Plectus sp. Fig. 50: Onyx sp. Fig. 51: Tripylina sp. Fig. 52: Odontophora sp. Fig. 53:

Udonchus sp. Fig. 54: DiplogastreJlus sp. Fig. 55: Achromadora sp. Fig. 56: Enoplolaimus sp. Fig. 57: Mononchoides

sp. Fig. 58: Odontopharynx sp. Fig. 59: Fictor sp. Fig. 60: Prismatolaimus sp.; Fig. 61: Onchulus sp. Fig. 62: Ioton-

chus sp. Fig. 63: Odontophora sp. www.nem.wur.nl/UK/In+the+picture/Gallery/ (Scale bar = 10 pm).

QudsiaTahseen

Figures 64-80. Modifications in stoma.

Fig. 64: Oxystomina sp. Fig. 65: Ceramonema sp. Fig. 66: Pseudocella sp. Fig. 67: Barbonema sp. Fig. 68: Odontanti-

coma sp. Fig. 69: Neochromadora sp. Fig. 70: Cobbia sp. Fig. 71: Gammarinenia sp. Fig. 72: Gomphionema sp. Fig. 73:

Parodontophora sp. Fig. 74: Bathylaimus sp. Fig. 75: Ptycholainiellus sp. Fig. 76: Synonchium sp. Fig. 77: Octonchus sp.

Fig. 78: Calyptronema sp. Fig. 79: Filipjevia sp. Fig. 80: Ditlevsenella sp.

Nematodes in aquatic environments: adaptations and survival strategies

for swallowing the whole prey (e.g., members of

Thoracostomopsidae, Enoplidae, Selachinematidae)

can be largely classified as persisters; and the sca-

vengers with buccal cavity provided with a lumened

onchium (tooth-like structure) to feed on dead ani-

mals or suck the cell contents of injured animals

e.g., oncholaimids and enchelidiids.

Bonger’s (1990) colonizer-persister classifica-

tion of nematodes holds good for terrestrial and fre-

shwater habitats, however, it has less application

in marine habitat (Bongers et al., 1991; Fraschetti

et al., 2006), partly due to a lack of empirical sup-

port for the classification of some marine genera

and the absence of extreme colonisers and persi-

sters in most marine habitats. Nevertheless, Saba-

tieria has been found to be a good colonizer

showing dominance in anthropogenically disturbed

sediments (Tietjen, 1980).

The individuals have evolved life-history cha-

racteristics (e.g. rapid growth rate, ability to adapt

to a wide range of environmental conditions) that

allow them to quickly establish in newly exposed

habitats or disturbed sediments in high densities

(Thistle, 1981; Moore & Bett, 1989; Somerfield et

al., 1995). The environmental constraints restrict

species establishment and mediate interactions bet-

ween successful colonists (Schratzberger et al.,

2008) Leptolaimus de Man, 1876 found at physi-

cally disturbed sites, is not classified as truly oppor-

tunistic species (Modig & Olafsson, 1998).

Ullberg & Olafsson (2003) hypothesised that

the agility of such small, surface-dwelling nema-

tode species with high dispersal potential (Lee et

al., 2001; Commito & Tita, 2002) might be an

evolutionary response towards higher levels of

competence for coping with disturbance (Schratz-

berger et al., 2009).

Adaptations to stress

Many aquatic nematodes can adapt physiologi-

cally to environmental challenges (Samoiloff et al.,

1980, 1983; Mutwakil et al., 1997; Doroszuk et al.,

2006). Fresh water as well as deep sea environ-

ments offer much hostile and extreme conditions

compared to other aquatic habitat types. Therefore,

the physiological challenges faced by nematodes

are greater in these ecosystems.

A variety of environmental stresses may trigger

quiescence viz., desiccation or high temperature

(anhydrobiosis), low temperature (cryobiosis),

osmotic stress (osmobiosis) and low oxygen (ano-

xybiosis); in extreme cases of prolonged quie-

scence, the metabolic rate may fall below detec-

table levels and appear to cease. This extreme

dormant condition is referred to as anabiosis

(Wharton, 1986) or alternatively as cryptobiosis

(Cooper & van Gundy, 1971). Unlike diapause,

the dormant state ends when the environmental

stress is relieved.

Temperature. Many biological structures, such

as enzymes and lipid bilayer membranes may show

molecular instability or fluidity due to temperature

extremes. Increasing temperatures can increase re-

action rates and can cause protein denaturation, re-

sulting in complete and often irreversible loss of

function (Hochachka & Somero, 1984). In fresh

water ecosystems such as springs, nematodes gene-

rally tend to avoid high temperatures above 43 °C

and high ionic concentrations (Ocana, 1991a, b) ex-

cept Rhabditis terrestris (Stephenson, 1942). At hy-

drothermal vents, however, temperature can range

from 2°C to 400°C and animals may have occasio-

nal brief contact with temperature difference of

100°C (Chevaldonne et al., 1992; Delaney et al.,

1992; Cary et al., 1998; Desbruyeres et al., 1998).

The deep sea is a relatively inhospitable envi-

ronment for metazoans with constantly low (~2 °C)

ambient temperature, high pressure, absence of

light and scarce organic carbon. Adaptation to the

deep sea includes presence of more “fluid” proteins

and lipids to counter the high pressure and low tem-

perature (Hochachka & Somero, 1984). Low tem-

peratures may slow or impede many biochemical

reactions and decrease the fluidity of lipids, a factor

of primary importance to cell membrane function

(McMullin et al., 2000).

Most of the adaptations that enable polar inter-

tidal invertebrates to survive freezing, are associa-

ted with their ability to withstand aerial exposure.

Nematodes surviving the freezing, exhibit low

metabolic rate and slow growth rate and the ina-

bility to survive at temperatures above 3-8°C. The

bacterial-feeder, Plectus murrayi Yeates, 1970

(Timm, 1971) inhabiting semi-aquatic and terre-

strial biotopes in the Antarctic McMurdo Dry Val-

leys, has its distribution limited by organic carbon

and soil moisture and survives extreme desicca-

tion, freezing conditions, and other types of stres-

ses (Adhikari et al., 2010).

The Antarctic nematode, Panagrolaimus davidi

Timm, 1971 shows both freeze-avoidance and

freeze-tolerance strategies thus experiencing free-

zing temperatures over nine months of the year and

QudsiaTahseen

facing regular cycles of freezing and thawing in

spring; the nematode thus undergoes cryoprotective

dehydration instead of freezing when held at its nu-

cleation temperature for a longer period, or when

cooled at a slower rate (Wharton et al., 2003).

P. davidi is the only animal known to survive ice

crystallization within its cells (Wharton et al.,

2005). With slower cooling rates, the water inside

the worm is super cooled, thereby creating a

vapor pressure difference between the ice in the

medium and the nematode. Besides synthesizing

trehalose, P. davidi produces a protein that inhi-

bits the activity of organic ice nucleators though

the sequence of this protein has no homology with

any other anti-freeze or ice-nucleating proteins

(Wharton et al., 2005).

Oxygen. Many meiobenthic species persist

over extensive periods under hypoxic and anoxic

conditions (Wetzel et al., 2002). Nematodes are

the most tolerant organisms as their species ri-

chness does not change in hypoxic-anoxic condi-

tions though their species composition and

trophic structure display significant changes

(Gambi et al., 2009).

Jensen (1987a) found that species, living in dee-

per sediment layers were significantly more slender

than their oxybiotic, surface-dwelling congeners,

however, nematodes of the genera Desmoscolex

Claparede, 1863; Tricoma Cobb, 1894 and Cobbio-

nema Filipjev, 1922 have been reported mostly from

the anoxic depths (> 300 m) of the Black Sea (Zait-

sev et al., 1987). At some places even Desmoscolex

and Bolbolaimus Cobb, 1920 are replaced by the

species ( Chromadorella Filipjev, 1918, Sabatiera

Rouville 1903 and Poly sigma Cobb 1920) more to-

lerant to the extreme conditions (Gambi et al., 2009).

Oxygen stress is successfully tackled by the

fresh water genera of Monhysteridae and Tobrili-

dae (Triplonchida) having prevalence in the habi-

tats with limited or no oxygen (Nuss, 1984;

Jacobs, 1987). Low oxygen concentrations are to-

lerated well by most Rhabditida (Ocana, 1993).

Such species survive anaerobic sediments by anae-

robic metabolism, facultative anaerobic metabo-

lism or quiescence (Bryant et al., 1983). Few

species can cope with changing oxygen levels by

alternating between aerobic and anaerobic meta-

bolism similar to the mechanism found in the in-

sect parasite Steinernema carpocapsae Weiser,

1955 (Shih et al., 1996).

Likewise a species Allodorylaimns andrassyi

(Meyl, 1955) Andrassy, 1986 (Dorylaimida) found

to survive in oxygen-free sediments of Lake Tibe-

rias (Israel) for 8 months of a year (Por & Masry,

1968). High salinity and high temperature are less

common physiological stresses for aquatic nemato-

des than low oxygen. In springs, Udonchus Cobb,

1913 and Rhabdolaimus have been reported to to-

lerate high salinity and temperature (Ocana, 1991a,

b). However, the genus Mesodorylaimus macrospi-

culum Zullini, 1988 seems to withstand stress (Tu-

dorancea & Zullini, 1989) in intermittent lakes that

are subject to high salinity and temperature.

The ability to survive under anaerobic condi-

tions may thus be quite widespread among nema-

todes, although different mechanisms may be

involved (Schiemer & Duncan, 1974; Biyant et al.,

1983). The presence of Theristns anoxybioticus Jen-

sen, 1995 at the oxygenated sediment surface of

muddy sediment suggested that even this facultative

anaerobe nematode needs to reach oxygen for its

reproduction (Jensen, 1995).

Thus, survival under anoxia would be possible

only under critical conditions. For reproduction on

the other hand, especially for the development of

eggs, there must be another more efficient pa-

thway of energy production (Riess et al., 1999) al-

though nitrate respiration has never been reported

in nematodes so far.

In shallow beaches drifting macroalgal mats in

the summer months induce anoxic and sulfidic con-

ditions with devastating effects on members of the

benthic fauna. Other disturbances like eutrophica-

tion in conjunction with density- stratified water

masses frequently results in severe oxygen deple-

tion of bottom waters, especially during the sum-

mer months, leading to hypoxic (dissolved oxygen

concentration <2 mg f 1 ) or even anoxic (dissolved

oxygen concentration of 0 mg l 1 ) conditions (Ro-

senberg et al., 1992). While most hypoxic events

affect the fauna in deeper sublittoral regions below

a thermo- or halocline; eutrophication has also

been attributed to the increase in benthic macroal-

gae (Rosenberg, 1985; Hull, 1987; Raffaelli et al.,

1991; Kolbe etal., 1995).

There is induction of Hb synthesis in many in-

vertebrates under stressful conditions (hypoxia,

temperature increase and CO poisoning). The

mud-dwelling nematode Enoplus brevis Bastian,

1865 with a pharyngeal haemoglobin (Hb) shows

feeding rates under hypoxia than the related, E.

communis Bastian, 1 865 that lacks Hb (Atkinson,

1977). Hb may be associated with vital functions

in euryhaline invertebrates living in widely dif-

ferent salinities and pH and lacking significant

osmotic, ionic, and acid-base regulatory capaci-

ties (Weber & Vinogradov, 2001).

Nematodes in aquatic environments: adaptations and survival strategies

Figures 81-91. Fig. 81: Pigment spot in Enoplus sp. Fig. 82, 83: Crystalloids in pseudocoelom of Tobrilus sp.

and Ironus sp. Fig. 84: Ultra structure showing longitudinal section of muscle fibres with crystalloids and electron-dense

bodies. Fig. 85, 86: Body pores in Cryptonchus sp. and Ptycholaimellus sp. Fig. 87: Flypodermal gland openings. Fig. 88,

89: glands associated with uterus and vagina. Fig. 90, 91: Egg shells with rugose or spinose surface

[Scale bar: 81-83, 85-89, 90, 91 = 10 pm; 84 = 1 pm).

QudsiaTahseen

Figure 92: Metaneme (AF: anterior filament, PF: posterior

filament, Sc: Scapulus, SC: sensory cell). Fig. 93: pigment

spot. Fig. 94: Ocellus. Fig. 95: Ocellus surrounded by pig-

ments. Fig. 96: Anterior end of nematode with cephalic

organ (CO). Figures 97-101: Demanian system (Os: Osmo-

sium; Uv: Uvette; MD: Main duct; DE: Ductus entericus;

DU: Ductus uterinus).

Water. The aquatic nematodes face two basic

problems of water gain or water loss depending

upon the type of surrounding environment.

Marine nematodes the osmoconformers, often

live in water that has a very stable composition and,

hence, they have a very constant internal osmola-

rity. Many invertebrates that osmoconform achieve

tissue tolerance by increasing intracellular osmola-

rity by mobilization of amino acids, thereby balan-

cing extracellular fluid.

This reduces the osmotic gradient across cell

membranes and maintains constant cell volume

(Schmidt-Nielsen, 1997; Kirk et al., 2002).

Panagrolaimus davidi, an Antarctic nematode, is

associated with ornithogenic soils (Porazinska et al.,

2002) in coastal areas that are ice-free during spring

and summer with sufficient meltwater from adja-

cent snowbanks. The water content of these sites

varies from saturated to completely dry (Wharton,

1998) and the nematode faces changes in external

osmotic concentration (Wharton, 2003). Panagro-

laimus davidi maintains its internal osmotic con-

centration above that of the external medium and is

thus an hyperosmotic regulator.

The nematode achieves regulation under hypo-

smotic stress more rapidly than under hyperosmotic

stress (Wharton, 2010). The nematodes found in

coastal zones are exposed to conditions of rapid de-

and rehydration similar to the mosses and lichens.

Drying initially decreases rates of anaerobic micro-

bial processes in sediments due to reduced oxygen

penetration (Baldwin & Mitchell, 2000). Differen-

ces among aquatic and terrestrial species in resi-

stance to desiccation and inundation cause shifts in

community composition along hydro-period gra-

dients (Larned et al., 2007).

The ability to enter anhydrobiosis may be one

of the most important and widespread adaptations

in evolutionary terms amongst nematodes but not

expressed in species of stable habitats. Freshwater

nematodes of temporary ponds commonly enter

quiescence in response to water stress (Wharton,

1986; Womersley & Ching, 1989). The phenome-

non is also common in nematodes of polar regions

(Pickup & Rothery, 1991; Wharton & Barclay,

1993; Wharton, 2004). Important information on

anhydrobiosis has been provided by several wor-

kers (Cooper & van Gundy, 1971; Demeure &

Freckman, 1981; Wharton, 1986; Womersley, 1987;

Barrett, 1991; McSorley, 2003).

The onset of anhydrobiosis marks a gradual water

loss from 75-80% to 2-5% in anhydrobiotic forms

(Demeure & Freckman, 1981). The fresh water ne-

matodes Actinolaimus hintoni Lee 1961 and Dorylai-

mus keilini Lee, 1961 were revived from cryptobiotic

(anabiotic) stage in dried mud (Lee, 1961).

Anhydrobiotic nematodes contain large amounts

of sugars, especially the disaccharide trehalose, a

dimer of glucose that protects cells by replacing

water associated with membranes and proteins.

However, most species are killed if drying oc-

curs too quickly whereas repeated events of drying

and rehydration decrease viability of nematodes

(Demeure & Freckman, 1981; Barrett, 1991). An-

hydrobiotic nematodes rehydrate in water, but there

is an average lag time (from less than an hour to se-

veral days) between immersion and their return to

Nematodes in aquatic environments: adaptations and survival strategies

normal activity (Cooper & Van Gundy, 1971; Whar-

ton, 1986; Barrett, 1991). Recovery is improved if

rehydration is slow, and nematodes are exposed to

high relative humidity before being immersed in

water. Anhydrobiosis involves decreased cuticular

permeability and the condensation or packing toge-

ther of tissues with increased levels of trehalose or

glycerol (Demeure & Freckman, 1981; Wharton,

1986; Womersley, 1987; Barrett, 1991). Coiling is

a typical behavioral response observed in anhydro-

biotic nematodes.

Pollutants. Environmental pollution is an im-

portant cause of stress in natural populations. Besi-

des affecting the population dynamics, it can also

lead to genetic changes (mutations) and adaptations.

The nematode bioassays lead to detection of a wide

range of chemical concentrations with distinct toxic

effects of lethality, developmental inhibition and

mutagenicity. Most studies have been undertaken

using the continental species Panagrellus redivivus

Goodey, 1945 against few studies carried out on

aquatic nematodes to determine pollution and toxi-

city in marine environments (Warwick, 1981b; Sa-

moiloff & Wells, 1984; Bogaert et al., 1984;

Vranken et al., 1991).

Aller & Aller (1992) showed that meiofauna ac-

tivity stimulated solute fluxes and reaction rates,

particularly aerobic decomposition and associated

processes such as nitrification in the oxic zone of

the marine sediments. Among toxicants, sulfide is

perhaps the most abundant with its impacts on bio-

logical systems well documented (Somero et al.,

1989; Grieshaber & Volkel, 1998).

Sulfide, in just micromolar amounts, is capable

of impairing biological processes and may seve-

rely inhibit aerobic metabolism by interfering with

cellular respiration and oxygen transport in diffe-

rent metazoan (Somero et al., 1989; Vismann,

1991; Grieshaber & Volkel, 1998; Szabo, 2007).

In the mitochondria, sulfide may poison the respi-

ratory enzyme cytochrome c oxidase, thus inhibi-

ting ATP production by the electron transport

chain and is capable of inhibiting muscular con-

traction independent of its effects on aerobic me-

tabolism (Julian et al., 1998).

Thus an organism adopts the strategies to avoid

sulfide, switch to anaerobic metabolism (Grieshaber

& Volkel, 1998), exclude sulfide from sensitive tis-

sues, or oxidize sulfide to less toxic forms. Most in-

habitants of vent and seep environments do not

realistically have the option of avoiding sulfide

altogether. Some marine nematodes e.g., Oncholai-

mus campylocercoides De Coninck & Stekhoven,

1933; Sabatier ia wieseri Platt, 1985; Terschellingia

longicaudata de Man, 1907; Sphaerolaimus pcipil-

latus Kreis, 1929; Siphonolaimus ewensis Warwick

& Platt, 1973; Pontonema vulgare Bastian, 1865,

while living in sulphidic transition zones convert

hydrogen sulphide to elemental sulphur which tem-

porarily reduces the concentration and toxic effect

of H 2 S and also provides an energetic 'deposit' for

latter oxidation to thiosulphate, sulphite or sulphate

under oxic conditions (Thiermann et al., 2000).

Many nematodes (Stilbonematinae, Desmodo-

ridae) harbour symbiont chemoautotrophic bacteria

(Hentschel et al., 2000; Ott et al., 2008; Bayer et al.,

2009) that oxidize sulfide and fix CO 2 . The ITbs of

these organisms bind sulfide without covalent mo-

dification of the heme groups and facilitates its tran-

sport or diffusion thus protecting the tissues from

sulfide poisoning.

These symbionts, in turn, constitute the worms'

major food source and are acquired from the envi-

ronment and shed off at every moult but reacquired

from the environment. The mechanisms of sym-

biont recruitment from the environment (Bulghe-

resi et al., 2006) have shown that Ca 2 +-dependent

lectin Mermaid mediates symbiont-symbiont and

worm-symbiont attachment in Laxus oneistus

(Ott et al., 1995).

Thick tubes or cuticles reduce or prevent expo-

sure of some external tissues to sulfide with Pty-

cholaimellus serving a good example (Nehring et

al., 1990). The effect of mercury contamination was

rather confusing as low doses of mercury appeared

to have much more drastic effects than the medium

and high doses.

Austen and McEvoy (1997) observed that low

doses of copper and zinc seem too toxic to kill all

the bacteria and meiofauna in the samples so that

complete decomposition of nematodes did not

occur (Hermi et al., 2009). Schratzberger et al.

(2009) found Araeolaimus bioculatus (de Man,

1876) to be intolerant to mercury contamination,

with effects observed even at the low concentration

used (0.084 ppm dw).

Mcnylynnia stekhoveni (Wieser, 1954) was cate-

gorized as “opportunistic” at low and medium mer-

cury doses with Hg(L) and Hg(M) concentrations

whereas Prochromadorella neapolitana (de Man,

1876) Micoletzky, 1924 was found to be a “mercury-

resistant” species (Schratzberger et al., 2009).

QudsiaTahseen

Pollutants also modify the distribution and

abundances of nematodes through indirect ecologi-

cal interactions (Johnston & Keough, 2003). If pol-

lution decreases abundance of a competitively

dominant species, inferior competitors may increase

in abundance not as a direct result of the contami-

nant but due to altered competition. Copper causes

decrease in recruitment and abundance of a number

of organisms (Johnston & Keough, 2000, 2003;

Mayer-Pinto et al., 2010). Thus metazoans largely

detoxify absorbed or ingested metals by using

metal-binding proteins (metallothioneins) and for-

ming subcellular inclusions.

These mechanisms often act jointly to consoli-

date and enclose excess metals, which then accu-

mulate within tissues and/or skeletal structures over

time (Beeby, 1991; Luoma & Carter, 1991). The

metal detoxification strategies used by nematodes

are not very different from those used by other or-

ganisms (McMullin et al., 2000) for example the

existence of phytochelatins, the heavy metal-bin-

ding peptides, in nematodes that are synthesized

by plants and fungi when exposed to metals

(Monserrat et al., 2003).

Phylogenetic implications

Assuming that all life originated in the sea and

that metazoan phyla evolved more than 550 million

years ago (mya) during the Precambrian period

(Conway, 1993; Valentine et al., 1996, 1999; Fe-

donkin & Waggoner, 1997; Peterson & Davidson,

2000), it can be assumed that the ancestral nema-

tode was also marine.

Nematodes also lack an informative fossil re-

cord (the oldest known fossil, Cretacimermis libani

Poinar et al., 1994 (Poinar, 2003) dates to around

135 mya). Filipjev (1929, 1934) and Lambshead &

Schalk (2001) have accepted the marine ancestry of

Nematoda while De Ley & Blaxter (2002, 2004)

considered a terrestrial origin for the Nematoda.

As highly productive terrestrial ecosystems exi-

sted in the Precambrian there might have been

chances of supporting the evolution of a new phy-

lum (Kenny & Knauth, 2001). Nevertheless, a ma-

rine origin of the Nematoda can be traced as some

terrestrial taxa of current phylogeny have been

found nested within marine clades.

The strongest evidence for a marine ancestry of

the Nematoda comes from the Chromadorea: the

basal clades are all predominantly marine (Micro-

laimoidea, Chromadorida, Desmodorida, Monhy-

sterida, and Araeolaimida) whereas the almost ex-

clusively non-marine Rhabditida are derived from

the ancestor of the Monhysterida or Araeolaimida

(Meldal et al., 2007).

The similarity in cuticular structure of Acan-

thonchus Cobb, 1920 (Wright & Hope, 1968),

Chromadorina Filipjev, 1918 (Lippens, 1974),

and Caenorhabditis (Epstein et al., 1971; Zuc-

kerman et al., 1973) lends circumstantial evi-

dence to the hypothesis that the Secernentea

arose from chromadorid-like ancestors. Howe-

ver, a reinterpretation of the cuticular structure

by Decraemer et al. (2003) suggested that this is

a homoplasic character that has appeared inde-

pendently in several clades.

Though aquatic nematodes can not be treated

separately as far as the phylogenetic grouping is

concerned. Nevertheless, one of these lineages in-

cludes marine, freshwater and terrestrial taxa, sug-

gesting that early Enoplia were characterised by

much greater osmotic tolerance than early Dory-

laimia (De Ley, 2006).

Most enoplids include large predators with big

hooks or teeth in more or less complex arrangements

as well as some additional sensory structures such

as eyespots and the stretch receptors (metanemes).

They are interesting phylogenetically because of

possessing some features, presumably ancestral wi-

thin Nematoda viz., a highly indeterminate mode of

development (Justine, 2002) and retention of the nu-

clear envelope in mature spermatozoa (Lee, 2002).

The ventrally spiral amphid was considered

plesiomorhic by Lorenzen (1981), yet the non-spi-

ral form seemed to be a secondary character loss.

Likewise, the presence of ocelli is usually conside-

red to be a primitive character though these struc-

tures are the most complex photoreceptors that the

nematodes possess.

Coomans (1979) suggested that the pigment

spots and their associated amphid ial photoreceptors

are less elaborate and may represent a stage that ori-

ginated later in the evolution and so have not yet

achieved great complexity.

Nevertheless, the occurrence in nematodes with

both types of photoreceptors: rhabdomeric and ci-

liary, supports Vanfleteren & Coomans ’s (1976) and

Sharma et al.’s (2006) conclusion that morphologi-

cal characters used in the classification are not

enough to recognize phyla along the main lines of

evolution.

Nematodes in aquatic environments: adaptations and survival strategies

Figures 102-112. Modifications at posterior body end.

Fig. 102: Anaplectus sp. Fig. 103: Panagrellus sp. Fig. 104: Rhabdolaimus sp. Fig. 105: Tripylina sp. Fig. 106: Chrono-

gaster sp. Fig. 107: Plectus sp.; Fig. 108: Tobrilus sp. Fig. 109: Philometra sp. Fig. 110: Epsilonema pustulatum after

Karssen et al., 2000. Fig. Ill: Desmoscolex sp. Fig. 112: Cryptonchus sp. Figures 113-117. Modifications at tail terminus.

Fig. 113: Plectus sp. Fig. 114: Chronogaster sp. Fig. 115: Epsilonema pustulatum after Karssen et al., 2000. Fig. 116: Do-

rylaimopsis variabilis Muthumbi et al., 1997. Fig. 117: Tobrilus sp. (Scale bar: 102-112 =10 pm; 11 3- 117 = 1 pm).

QudsiaTahseen

CONCLUSION

Aquatic nematodes are of vital importance as a

very significant portion of the energy flow in the

benthic system passes through these nematodes.

However, one of the main reasons for the aquatic

nematodes being ignored is that they are not of di-

rect benefit or nuisance to man. Their role in stimu-

lating bacterial metabolism is now well documented

(Tenore et al., 1977; Tietjen, 1980) and they have

an important and direct influence on the producti-

vity of shallow waters by enhancing nutrient rege-

neration in the sediments.

They also affect the texture (Cullen, 1973) and

the physical characteristics of sediments by mu-

cous secretion, which are significant for dredging

and dumping operations. It can be further said that

the story of their adaptations to a particular envi-

ronment type is far more complex than could be in-

ferred. Despite the recent information gained,

studies are required on the plesiomorphous forms,

the mutants and the apomorphs to reveal how far

deviations exist.

Future researches should further consider the

detailed structure and anatomy of the receptors as

modification in them are reflected in changes in be-

haviour. Although the nematode nervous system is

considered to be a conservative system with a rather

small number of cells, different behavioural pat-

terns exist according to the different environments

and ecological niches occupied by the species.

ACKNOWLEDGEMENTS

The financial assistance provided by Ministry

of Environment, Department of Science and Te-

chnology, New Delhi and Third World Academy

of Science, Italy is being acknowledged here

with thanks.

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Biodiversity Journal, 2012, 3 (1): 41-48

Reproductive biology and growth of Lesser Spotted Dogfish

Scyliorhinus canicula (Linnaeus, 1758) in Western Algerian

coasts (Chondrichthyes, Scyliorhinidae)

Ahlem Amina Taleb Bendiab, Salim Mouffok* & Zitouni Boutiba

Laboratoire Reseau de Surveillance Environnementale, Department of Biology, Faculty of Sciences, Oran University, BP 1524 El

Menaouar, Algeria.

^Corresponding author, email: halieutsalim@yahoo.fr.

ABSTRACT Elasmobranch fishes have a large distribution. At the level of the Mediterranean fisheries, a

low density of elasmobranchs is noted at the assemblages, these fisheries appearing near to

the point of best efficiency or even to over-exploitation. Indeed, a general decline of shark

populations was observed over the last decade on the Mediterranean coast. The aim of this

work was to evaluate different biological characteristics of the species Scyliorhinus canicula

(Linnaeus, 1758). A sampling of 461 specimens was realized between September 2009 and

August 2010 from the western coast of Algeria. The oviduco-somatic index OSI, the hepato-

somatic index (HSI) and the condition factor (Kn) were estimated monthly for 249 females

to identify the reproduction period. Obtained results show a rapid maturation from September

to November and from February to April when the Kn values are very low.

KEY WORDS biology; fishery; western Algerian coasts; Scyliorhinus canicula ; sentinel species.

Received 02.03.2012; accepted 20.03.2012; printed 30.03.2012

INTRODUCTION

The Lesser Spotted Dogfish Scyliorhinus cani-

cula (Linnaeus, 1758), a species of Chondri-

chthyens fish studied in several areas of the globe,

oviparous, abundant and frequently observed along

the coasts of Europe in the Atlantic and Mediterra-

nean (Halit & Ta§kavak, 2006), is very abundant on

the Algerian coast.

Recently, S. canicula was shown to be a good

indicator to evaluate the level of exploitation of the

marine ecosystem by its vulnerability to the fishing

impact due to its slow growth, late reproduction and

very low fertility rates (Rodriguez-Cabello et al.,

1997; Massuti & Moranta, 2003) and by its asso-

ciation with other noble species frequenting the

same habitat.

Taking into account that length at maturity, fe-

cundity and sex-ratio are some of the most impor-

tant parameters in studying reproductive dynamics

of elasmobranch population, this study was carried

out by examination of annual changes of the ovi-

duco-somatic index (OSI), hepatosomatic index

(HSI) and condition factor (Kn) in order to evaluate

the level of the exploitation in the Algerian coasts.

In fact, on southern Mediterranean coast, the

knowledge on S. canicula is still fragmentary, being

limited to some remarks about Algerian waters.

Therefore, the aim of the present paper was to

study the population dynamics, reproduction, con-

dition, age and growth of this species. This is the

first paper with a complete analysis of the biology

of S. canicula in south-western Mediterranean.

MATERIAL AND METHODS

A-Reproduction study

A series of biological samples was conducted on

specimens of S. canicula caught by the commercial

AATaleb Bendiab, S. Mouffok & Z. Boutiba

trawlers in the sampling area of Oran and

Arzew (Fig. 1). Specimens’ total length was mea-

sured and both sex and maturity were reported for

females which represent the focus of our study.

Three different maturity stages were defined (Table

1) according to Rodriguez-Cabello et al. (2007) and

Capape et al. (2008).

Stage

Microscopic aspect

(color and eggs’ texture)

I immature

No eggs and no Capsules

II Beginning of

maturation

Ovaries small, light brown,

egg-capsules rigid

III Advanced maturation

Ovaries enlarged, dark

brown, egg-capsules rigid

Finally, to monitor morphological variations, the

condition index was calculated to assess the degree

of overweight consecutive to genital development

and repletion state of the target species. Condition

factor was studied in females in order to show dif-

ferences of Kn (Le Cren, 1951) related to time, ac-

cording to the formula: Kn = W/W lh with W th = aL b

where “W” is the total weight, “W th ” is the theore-

tical weight, “a” and “b” are coefficients of the re-

lative growth between weight and length and “L”

is total length.

B-Growth Study

The objective of this part of the study was to de-

fine several biological characteristics, such as struc-

ture of population size, growth and age of S.

canicula in the study area.

Table 1. Different stages of maturity of Scyliorhinus

canicula females.

Sex-ratio analysis was performed studying glo-

bal sex-ratio, sex-ratio by length classes and sex-

ratio by seasons using the logistic model

STATISTICA Software (StatSoft Inc., 2001) and

calculating the heterogeneity testy with one degree

of freedom, p <0.05. The value of the reduced di-

stance (Schwartz, 1983) was also estimated; it is a ho-

mogeneity test which compares the average sizes of

males and females, in case of large samples, by the fol-

lowing equation:

£ =

Xx-Xi

With reference to the work of Capape et al.,

(2008) and to define the beginning and the extent

of spawning period, oviduco-somatic index (OSI)

was calculated using the following equation OSI=

(OW/TW)*100, where OW is capsules’ weight and

TW is total weight of the specimens.

Flepato somatic index (HSI) was calculated

using the following equation: HSI= (LW/TW)* 100,

where LW is liver weight and TW is total weight of

the specimens. Variation of OSI and HSI related to

sexual maturity stages and seasons was examined

in S. canicula females.

Basic principle of the growth equation of Von

Bertalanffy.

There are several mathematical models to ex-

press the growth in elasmobranchs. A detailed re-

view was made by Beverton & Holt (1957), Ursin

(1967), Gulland (1983), Sparre & Venema (1996)

and Pauly & Moreau (1997). The most popular

model is Von Bertalanffy (1938) growth equation:

Lt = Loo [1-e k(t t0) ].

ELEFAN method (ELECTRONIC LENGTH FREN-

OUENCY ANALYSIS).

In this study, we used a numerical method, the

method ELEFAN (Pauly & Moreau, 1997). For ma-

thematical modeling, the LFDA software (Kir-

kwood et al., 2001) was used. Analyses were made

for males and females, separately.

RESULTS

A-Study of reproduction

1) Sex-ratio

After sexing of 461 specimens we found a sam-

pling rate of 54.01% of femininity significantly

more important than males sex ratio (45.99%).

These results are consistent with other studies car-

ried out in different parts of the Mediterranean at

depths ranging between 200 and 500 m (Rodriguez-

Cabello et al., 1998; Capape et al., 2008) (Table 2).

Reproductive biology and growth of Lesser Spotted Dogfish Scyliorhinus canicula (L., 1 758) in Western Algerian coasts

The length abundance curve is shown in figure 2.

Figure 3 shows a variation of the percentage of fema-

les per month. The females percentage is still domi-

nant during the end of summer and at the beginning

of autumn up to winter, declining in the spring period.

Results were compared with theoretical 8 (1.96)

at a rate of 95% confidence (Table 3). The calculated

value of s = 0.33 is less than the value (1.96) given

by the table of the z-score; this finding indicates that

males are, on average, significantly larger than fe-

males. As regards the sexual maturation of females,

different stages of maturation of the gonads during

different months of the year are shown in figure 4.

Sex

Total

Percentage

Females

249

54.01%

Males

212

45.99%

Total

461

* 100%

Table 2. Percentage of sexes in Scyliorhinus canicula

(*p<0,05).

Sex

Males

Females

Total

212

249

X (cm)

37.02

35.10

a 2 (cm) 2

1943.02

1965.25

8 0.33

Difference significant

Table 3. Different size parameters of males and females of

Scyliorhinus canicula.

2 ) Indices of fish condition

In our study we have used three indeces to determi-

nate the spawning period of the species in the study

area: the oviduco-somatic index (OSI) specific to

Elasmobranchs, hepatosomatic index (HSI) and

condition index (Kn). These allowed to quantify

morphological changes of the specimens and to

identify reproduction period by studying the evolu-

tion of maturity stages of the ovary.

Hepato-Somatic Index (HSI) and Oviduco-Somatic

Index (OSI) and condition factor (Kn).

Monthly averages of OSI and HSI calculated

from 249 females are plotted in figure 5. Three

peaks were observed corresponding to the maxi-

mum annual spawning period of the population.

The highest values of OSI were found in December,

February, June and August and the lowest values in

October, January, April, May and July.

The highest values of the HSI occurred in Decem-

ber, February, March, the lowest fall in October, Ja-

nuary and April (Fig. 5). Figure 6 shows the condition

factor Kn by seasons in both sexes. The values of Kn

resulted overweight, thus revealing breeding events and

confirming a rapid maturation occurring from Septem-

ber to November and from February to April when the

values of Kn are very low with irregular variations.

3) Length at maturity

For the statistical method, the L50 point esti-

mated the body size at sexual maturity at 36 cm

(Fig. 7). All data are combined in Table 4. Our re-

sults confirmed values reported for Mediterranean

Author

Area

Males (cm)

Females

(cm)

Ford (1921)

English

Channel

50-60

57-60

Faure-Fremiet

(1942)

Atlantic

52-60

Leloup & Oli-

vereau (1951)

Atlantic

52-60

Leloup & Oli-

vereau (1951)

Mediterra-

nean Sea

37-44

Zupanovic,

1961

Adriatic Sea

Collenot,1966

English

Channel

60-68

Capape and

al., 1991

Mediterra-

nean

41-47

Present work

Algeria (west)

—

Table 4. Summary of first sexual maturity length (L50) of

S.cyliorhinus canicula females and males from different

areas (* only females were studied to determine the size at

maturity).

AATaleb Bendiab, S. Mouffok & Z. Boutiba

fisheries which differ from those from the North

Atlantic where specimens length at maturity is lon-

ger than that found in the Mediterranean Sea. Total

individuals’ length of the monthly samples ranged

from a minimum of 20 centimeters to a maximum

of 50 cm. Minimum sizes correspond to females

and maximum sizes correspond to males (Table 5).

B- Growth study

The values of growth parameters were calcula-

ted using the software LFD A (subroutine ELEFAN)

(Kirkwood et al., 2001). Tables 6 and 7 report va-

lues of Loo (asymptotic length), K (coefficient of

growth), to (the theoretical age at which the size is

zero), also for O (growth index). These values, once

estimated for S. canicula specimens, were then re-

placed in the equation of Von Bertalanfify. Parame-

ters obtained from the equation of Von Bertalanfify

did not differ significantly between the two sexes;

but asymptotic length, growth rate and growth

index resulted slightly different in males.

Biometric relations observed by analysis of re-

lative growth are shown in Table 8. This relation-

ship indicates an upper bound of allometry (b

greater than 3) for females in all months of the year.

We can say that the weight of the species grows

faster than the cube of length. Such an allometric

relationship was observed also in males. In fact, the

upper bound also appeared in the allometry of

males, except for males sampled in December and

February when the values of allometry were redu-

ced. The fitting of a and b (W th = aL b ) was employed

as input data in stock assessment models.

DISCUSSION

In our study (covering 12 months) a sample of

461 individuals of Scyliorhinus canicula was obser-

ved, resulting that females were more important

than males. More information were obtained

through the study of sex ratio based on different pa-

rameters and specimens size during the year.

We noted a fluctuation in the rate of femininity

with a significant dominance during autumn and

winter, which seems to correspond to a strong and

early maturation period of the ovaries.

We also observed a clear statistically significant

decrease in the rate of femininity tending to reach a

numerical equality with males at the beginning of

Sex

Females

Males

specimens caught

249

212

Maximum size

(cm)

47.4

Minimum size

(cm)

20.1

_22.2

Table 5. Size of Scyliorhinus canicula females and males

analysed in the present study.

Sex

Females

Males

Parameters

K Fco to ({)

K Foo to (j)

Result

0.57 47.70-0.76 3.39

Table 6: Growth parameters for Scyliorhinus canicula fe-

males and males.

Sex

Von Bertalanffy Equation

Females

Ft- 47.7 [1-e -° 57 (t+o.76)]

Males

Ft =49.23 [1-e -051 (t+a39) ]

Table 7. Von Bertalanffy Equation.

Sex

w th= a L b

Females

w th = 0.00578 F 3 176

Males

W th = 0.01675 L 3 0215

Table 8. Biometric relation in Scyliorhinus canicula.

spring, i.e. in March and April, which could corre-

spond to sexual rest or post-spawning periods; re-

garding the correlation between sex and body size,

one can observe that size classes between 20 and

43 cm of total length are almost significantly domi-

nated by females.

Large individuals are represented by males with

a total length of 44-50 cm. This difference in size

in favor of males was also reported by other authors

in the Mediterranean, including Capape et al.

(1991) in the Gulf of Lions, De La Gandara et al.

Reproductive biology and growth of Lesser Spotted Dogfish Scyliorhinus canicula (L., 1 758) in Western Algerian coasts

Length class (cm)

■ STAGE III %

" STAGE II %

STAGE l %

Figure 1: Study area.

Figure 2: Abundance curve. Results of jf test show a predominance of one sex over the other by length of specimens

(* p<0.05).

Figure 3: Distribution of males and females of Scyliorhinus canicula by season, yy test results show a prevalence of one

sex over the other per sampling month.

Figure 4: Percentages of different stages of sexual maturity in Scyliorhinus canicula females per month.

Figure 5: Monthly trend of OS1 and HS1 with standard errors in Scyliorhinus canicula.

Figure 6: Condition index (Kn) with standard error according to the season in Scyliorhinus canicula females.

Figure 7: Size of first maturity in Scyliorhinus canicula.

AATaleb Bendiab, S. Mouffok & Z. Boutiba

(1994) and Rodriguez-Cabello et al. (1998) along

the Spanish coast; they all pointed out the size dif-

ference between females and males, which could

be explained by the fact that large females are li-

kely to be less accessible to fishing gear as they

move to specific reproduction areas (Rodriguez-

Cabello et al., 1998).

From the three indexes studied (OSI, HSI and

Kn) we determined the spawning period of the spe-

cies. Moreover, by a macroscopic approach we

studied the sexual cycle of the species, the bree-

ding of which appears to be annual (see also Ca-

pape et al., 2008) with maximum phases of

maturation occurring in December, February and

March (during the laying period) and interruptions

in October, January and April, corresponding to a

state of sexual rest or repletion.

Similar observations were reported by Capape

(1977) however, we found periods of high ovarian

maturation that differ from those reported in that

paper, probably due to changes in environmental

conditions as fluctuations in ocean water masses

(Harris, 1952; D'Onghia et al., 1995; Mouffok et

al., 2008). Ford (1921) reported that, in southern

England, there were a peak in August and a mini-

mum in September and October. While in the paper

of Faure-Fremiet (1942) these peaks were in June

and January. Lo Bianco (1909), Leloup & Olive-

rau, (1951) and Capape et al., (1991, 2008), main-

tained that this period can last all year round,

without interruptions. In line with further studies

on endocrine control of reproductive cycle by

Sumpter & Dodd (1979), we support the idea that,

although the spawning period of S. canicula could

be quite long, it should have a maximum peak of

spawning in spring and winter.

To accurately determine the period of breeding

and spawning of benthic or demersal species, seve-

ral indicators are generally used. Referring to

ISRA-IRD (1979), it is recommended to use at least

two indices when studying the reproduction of a tar-

get species. Please note that, in the present study,

OSI and HSI vary in parallel and the evolution of

these values is opposite to that of Kn.

We estimated the size at first maturity (L50) at

36 cm. According to Rodriguez-Cabello et al.,

(1998) the size at first maturity of females in the

Mediterranean is smaller than that found in North

Atlantic; this difference (also found in males) was

explained by suggesting a possible relationship bet-

ween maturity of the species and latitude (Lam,

1983). Our results confirm and support findings ob-

tained by different authors mentioned above sugge-

sting that reproductive parameters of Scyliorhinus

canicula differ from one region to another, probably

under the influence of various environmental and

geographic parameters (Leloup & Oliverau, 1951;

Relini & Orsi-Relini, 1987; Capape et al., 1991; De-

mestre & Martin, 1993; Guijarro et al., 2007) such

as the passage of the Atlantic currents entering the

Mediterranean through the Strait of Gibraltar rich

in organic matter providing an ideal enrichment of

Algerian deep waters (Cartes et al., 2002).

Finally, our results for growth curves (in line

with those reported by Rodriguez-Cabello et al.,

1997), strongly suggest a slow growth rate and an

important longevity, up to 10-20 years, for S. ca-

nicula specimens.

ACKNOWLEDGEMENTS

The authors thank the Algerian Ministry of Hi-

gher Education and Scientific Research (MESRS)

which funded this experimental study within the

framework of CNEPRU project No F0 1820090008.

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Biodiversity Journal, 2012, 3 (1): 49-54

Ecological features of Tundra Cranes in North-Eastern

Siberia (Aves, Gruidae)

M ar i a V I ad i m i rtseva

Institute for biological problems of criolithozone. Siberian Branch of Russian Academy for Science 677980, Yakutsk, Lenin pro-

spect, 41, Russia; e-mail: sib-ykt@mail.ru.

ABSTRACT In sub-arctic tundra of North-Eastern Siberia (Yakutia region) the breeding areas of Siberian

Crane, Grus leucogeranus (Pallas, 1773) and Lesser Sandhill Crane, Grus canadensis cana-

densis (Linnaeus, 1758), overlap. In the present paper ecological interrelations between these

two crane species are reported. Siberian Crane is the dominant species and occupies more pro-

ductive ecological niche such as damp lowlands. Sandhill Cranes have to content themselves

with less productive but more extensive habitats such as drier and higher levels of tundra. Ge-

nerally speaking, Sandhill Cranes prefer to feed in damp lowlands, as can be observed in areas

where Siberian Cranes are absent. Such a displacement toward another ecological niche has

not a significant impact on Sandhill Crane thanks to the plasticity and tolerance of this species.

KEY WORDS Siberian crane; Sandhill crane; breeding area; ecological niche; chick-raising period.

Received 19.01.2012; accepted 20.03.2012; printed 30.03.2012

INTRODUCTION

In tundra of North-Eastern Siberia (Yakutia region)

Siberian Crane, Grus leucogeranus (Pallas, 1773)

and Lesser Sandhill Crane, Grus canadensis cana-

densis (Linnaeus, 1758), share the same breeding

area. Siberian Cranes inhabiting areas from Yana-

Kolyma watershed to Kolyma River represent the

eastern population of the species.

The welfare of Siberian Crane eastern population

strongly influences the conservation of the species

all around the world since western population now

counts just a few pairs of specimens. By the present,

Siberian Crane eastern population numbers up to

4004 individuals, as it was shown by the counts on

the main wintering ground of the species in Poyang

Lake Natural Reserve, South-Western China (Qian,

2003). Lor the western population, only one Siberian

Crane was registered in the wintering ground in Iran

during 2010-2011 (Tavakoli, 2011).

Sandhill Crane in Yakutia is represented by one

from six subspecies. In the Old World, Lesser Sandhill

Crane is present in North-Eastern Russia from

Kamchatka peninsula and North-Western Chukotka

to subarctic tundra of north-eastern Yakutia. During

the censuses of the 1980’s, the number of Sandhill

Cranes on breeding ground in Yakutia was estima-

ted at 370 individuals (Labutin & Degtyarev, 1988).

Several authors reported a significant increase

in SandhillCranes number along with the expan-

sion of its breeding range westwards beginning

from the second half of the 20 th century (Portenko,

1972; Kischinski, 1988; Labutin & Degtyarev,

1988; Labutin et al., 1990; Poyarkov et al., 2000;

Degtyarev, 2009).

Perhaps this phenomenon is associated with

hunting on the Sandhill Crane in North America

(Meine & Archibald, 1996). In particular, speci-

mens number noticeably increased near-Kolyma

tundra (Table 1). During this study, in 1998, a

Sandhill Crane pair with two chicks was observed

for the first time on the left bank of Indigirka River,

200 m west from the species breeding area limit;

this finding seems to prove that Sandhill Cranes

Maria Vladimirtseva

breed near-Indigirka tundra and indicates the suc-

cess of this species in its further expansion we-

stwards (Vladimirtseva, 2002; Germogenov et al.,

2003; Vladimirtseva et al., 2009).

In Indigirka basin, where their breeding ranges

overlap, the two Tundra Crane species use different

ecological niches (Watanabe, 2006). Siberian Cranes

occupy damp lowlands near or between big lakes

extending up to 15 km in length, whereas Sandhill

Cranes can be often seen on higher and drier habi-

tats. Over the last decade, in the studied area (1314

km 2 near-Indigirka tundra) the population of Sibe-

rian Cranes grew by four pairs and, in 2009, the po-

pulation density was estimated as 0.71 ind/10 km 2 .

In Indigirka basin, where Sandhill Cranes show

a lower population density in the peripheral zone of

the breeding area and share their breeding territory

with Siberian Cranes, it was very difficult to carry

out chronometrical observations, especially for

pairs with chicks due to their constant movement

resulting in short-term watching.

Chronometrical observations were made near-Indi-

girka tundra during summer seasons from 1998 to

2009. The highest recorded duration of continuous

observations of the Sandhill Crane brood in the In-

digirka basin was of 1 1 hours and 3 min. These data

were compared with those obtained during the pe-

riod 2010-2011 from a population with a high po-

pulation density inhabiting near-Kolyma tundra

(see Table 1).

Siberian Cranes are rare in Kolyma river basin and

mostly do not breed there. The main objectives of

this study were to provide data on Sandhill Crane

population density, habitat conditions, breeding pair

time budget and species behavior in the study area

and to compare these results with those obtained for

the population of Indigirka basin.

MATERIALS AND METHODS

Counts of the Crane pair numbers and observa-

tions were made from the highest points of local

hills (called “edoms”) using a telescope with sixty-

fold magnification, as well by hiking and boating.

Observations were recorded by the methods of con-

tinuous and regular (every 15 sec) recording (with

mention of all details) (Dolnik, 1980; 1995).

Sandhill Crane social structure and population

size were estimated within the study-area consisting

of 402 km 2 near-Kolyma tundra, River Bolshaya

Chukochya mouth (Table 2) by a total of 256.15

hours of chronometrical observations. A pair of Si-

berian Cranes between lakes Bolshoye Morskoye

E^OLSHAYA

CHUKOjCHYA ^r 1

INDIGIRKA

KOLYMA

1:1000000

Figure 1. Research areas: 1, near-Indigirka tundra (from 1998 to 2009); 2, near-Kolyma tundra, Bolshaya Chukochya

mouth (in 2010); and 3, Kolyma Delta, locality Pokhodskaya Edoma (in 2011).

Ecological features ofTundra Cranes in North-Eastern Siberia (Aves, Gruidae)

Figure 2. Sandhill Crane chick, Bolshaya Chukochya River basin, and (in the small box on the right) an adult bird.

(18.2 km in length) and Maloye Morskoye (11.1

km) was registered from the watching point on the

lake Vankhmat. Considerable distance from the ob-

ject (15 km) did not let to see if they had any

chicks. Local people registered this pair of birds

for over 10 years.

RESULTS

As revealed during the chick-raising period.

Sandhill cranes do not show pronounced intra-spe-

cific territorialism. Although pairs had individual

breeding territories, their boundaries could easily

be violated. Representatives of all social groups,

pairs with chicks, pairs without chicks and single

birds moved freely over a wide area and could

meet and connect in groups of up to seven birds

for a short time.

A comparison of time budgets between the two

crane species showed that Sandhill Crane chicks

are more independent than Siberian Cranes at the

same age: i.e. they can feed almost without the

help of their parents (Table 3). In addition, the Si-

berian Crane chick is given more time to rest du-

ring daylight hours.

A distinctive feature of Sandhill Cranes occur-

ring near-Indigirka tundra was the constant move-

ment associated with gathering food items, such as

sedge shoots, small invertebrates, mammals (lem-

mings and voles) and small bird chicks, from the

ground surface never showing feeding connected

with digging. On the contrary, Sandhill Cranes near-

Kolyma tundra spent 68% of their feeding time at

the lowest elevation areas, so-called "pits", where

they dig out roots of sedge using their beaks, which

is typical of Siberian Cranes.

Moreover, Sandhill Cranes near-Indigirka area

spent significantly more time in a state of alertness

and anxiety than Sandhill Cranes inhabiting near-

Kolyma tundra (where there are no Siberian cranes)

and than Siberian Cranes (Table 4).

In general, time dedicated to brood care indicates

that the rate of activities of Sandhill Cranes is a little

more accelerated than that of Siberian Cranes. When

considering the results reported in Table 4 it should

be taken into account that some activities (alertness,

movement and feeding) overlap in time, so that the

sum of all activities during the day is over 100%.

DISCUSSION

Siberian Crane and Sandhill Crane share the

same breeding area near-Indigirka tundra. Never-

theless, these species have the possibility to realize

Maria Vladimirtseva

Near-Indigirka

tundra

Near-Kolyma tundra

Banks island,

1965, Yukon-Ku-

skokwim Delta,

1976

Ust-Chaun lo-

wland, Chukotka,

2002

Left bank of

Indigirka, 2009

Bolshaya Chuko-

chya mouth, 20 1 0

Pokhods-kaya

Edoma, 2011

Pokhods-kaya

Edoma, 2007

0.85 ind./lO km 2

2.7 pairs /1 0 km 2 ,

5.9 ind./lO km 2

. 4.5 ind./ km 2

4.8 md./lO km 2 , AAAm

(Degtyarev, 2009)

5.4-17.8 pairs /I U

km 2 (Boise, 1976;

Walkinshaw, 1965)

6. 5-7. 4 pairs /1 0

km 2 (Winter, 2002)

Table 1. Sandhill Crane population density in different years and in different parts of its range.

Adult cranes number

Breeding

success

Including

umcKS numoer

Ind.

Singles

Pairs

Groups of

3-7

Broods

number

In 17

broods

In 21

broods

239

216

35.2

Table 2. Sandhill Crane population structure and reproduction in the study-area during 2010.

Activities

Sandhill Cranes

Siberian Cranes

(n=5)

Indigirka basin (n=2)

Kolyma basin (n=12)

Absolute rest

116.09±0.02 (16.00-16.19)

16.64±0.85

14.96±0.30

Incomplete rest

8.32±0.12 (8.11-8.53)

13.71±0.08

30.46±0.51

Self feeding

1.71±0.01 (1.70-1.72)

2.05±0.92

0.71±0.82

Alarm

3.59±0.71 (3.09-4.10)

Table 3. Time (expressed in %) dedicated to daily activities by crane chicks in the study areas.

Sandhill Cranes

Siberian Cranes

(n=5)

Activities

Indigirka basin (n=2)

Kolyma basin (n=12)

Feeding

49.86±0.59 (50.80-50.92)

50.05±0.6

32.66±0.21

Movement (no feed ing )

8.41±0.4 (9.00-9.82)

2.8±0.31

2.6±0.12

Alert

6.0±0. 19(5.8-6.2)

0.9±0.55

0.1±0.60

Anxiety

14.0±0.39 (14.6-15.4)

1.0±0.09

7.5±0.21

Cleaning of feathers

0.8±0.01 (0.09-0.12)

1.2±0.41

3.8±0.32

Night's sleep

14.99±0.08 (15.90-16.08)

15.6±0.26

14.9±0.52

Feeding the chicks

32.8±0.2 (34.7-34.9)

34.9±0.14

38.4±0.19

Table 4. Time (expressed in %) dedicated to daily activities by adult cranes within the study areas.

Ecological features of Tundra Cranes in North-Eastern Siberia (Aves, Gruidae)

their potential in population growth because they

use two different ecological niches; Siberian Cranes

occupy damp lowlands near or between big lakes,

whereas Sandhill Cranes can be often seen on hi-

gher and drier habitats.

Siberian Cranes are absent in Kolyma River

basin, probably because of lack of big lakes which

constitute an optimal habitat for their breeding.

Observations near-Kolyma River tundra showed

that Sandhill Cranes with chicks spent most of their

feeding time in damp and low wetlands. In the area

at the mouth of Bolshaya Chukochya River, San-

dhill Cranes do not compete for territories in chick-

raising periods, as in Chukotka (Winter, 2002) or

Alaska (Boise, 1976), thus suggesting that their

food resources should be abundant enough.

Near Kolyma River tundra Sandhill Cranes feed

in the Siberian Crane way: during the day, they pe-

riodically dig out parts of sedges staying in the same

place. On the contrary, near-Indigirka River tundra

Sandhill Cranes gather food (i.e. sedge sprouts, in-

sects, small animals and small bird clutches or

chicks) mostly from the surface, which makes them

covering great distances during feeding activities.

Near Indigirka River (= the co-habitation area

of the two species) Siberian Crane appears to be do-

minant and is replaced by Sandhill Crane in the less

productive ecological niche, that is, the higher and

drier areas of the tundra; while in northern-eastern

tundra of Yakutia (where Siberian crane is absent)

Sandhill Crane broods clearly prefer damp and low

wetlands.

Sandhill Cranes are capable to use a wide range

of habitats, since they are not so highly specialized

and hence result more adaptable to environmental

conditions than Siberian Crane. Using a less pro-

ductive but more extensive habitat. Sandhill Cranes

occurring in Indigirka tundra continue to expand

their breeding range westwards increasing in den-

sity and number (Vladimirtseva et al., 2009).

Taking into account both growth of Sandhill Cra-

nes number and the extension of their breeding

range in Yakutia, in order to examin inter- and intra-

specific relationships between Siberian Cranes and

Sandhill Cranes within the co-habitation area as well

as in Kolyma tundra, further studies are certainly

needed. Global warming, one of the most serious

threats to Siberian Crane, may lead to reduction and

loss of nesting habitat for this vulnerable crane spe-

cies breeding in wet lowlands close to big lakes.

At the present time, Siberian Crane and Sandhill

Crane can coexist by using different ecological niches

but, on the other hand, in the next decade ecological

and ethological observations regarding these species

will probably show the degree of danger of emerging

and evolving threats menacing their existence.

CONCLUSION

1. In the tundra near Indigirka River Siberian

Crane and Sandhill Crane occupy different ecolo-

gical niches which strongly reduces the competitive

relationship between these species and allows them

to realize, at best, potential growth in their respec-

tive populations.

2. In Kolyma basin, where Siberian Cranes are

absent. Sandhill Crane broods prefer to feed in wet

habitats. On the contrary, in Indigirka River basin,

where breeding ranges of these two crane species

overlap, the dominant Siberian Crane is replaced

by Sandhill Crane in the higher and dryer zones of

the tundra. Such a displacement toward another

ecological niche has not a significant impact on

Sandhill Crane thanks to the plasticity and tole-

rance of this species.

3. Large-scale movement of Sandhill Crane

broods in Indigirka River tundra may be due firstly

to the tolerance of these organisms which, unlike

Siberian Crane, are not strongly dependent on we-

tlands; and, secondly, to their habit of gathering

food items from terrain surface which allows them

to exploit more elevated terrains and explore much

larger areas.

ACKNOWLEDGEMENTS

This research was funded by the Grant for

Young Scientists, Siberian Branch of Russian Aca-

demy for Science. Grateful thanks go to Yakov and

Ivan Berezkin, Niznekolymsky Nature Protection

Inspection, who were very helpful guides for this

research.

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near the western boundary of their range: distribu-

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USSR Ornithological Society, Vladivostok, 161-164.

Labutin Y.V., Degtyaryev A.G. & Perfiliev V.I., 1990.

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ber and social structure crane and swan popula-

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Yakutia Science Center. Yakutsk, 99 pp.

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Survey and Conservation Action Plan. Gland, 294 pp.

Portenko L.A., 1972. Birds of Chukotka Peninsula and

Vrangel Island. Nauka, 1, 42 pp.

Poyarkov N.D., Hoggies J. & Eldrige V., 2000. Atlas

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Watanabe T., 2006. Comparative breeding ecology of

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Biodiversity Journal, 2012, 3 (1): 55-58

irst record of the Giant House Bat Scotophilus nigrita

'Schreber, 1 774} in Cameroon (Mammalia, Chiroptera

Eric Moise Bakwo Fils 1 *, Alima Bol AAnong 1 & Fernand-NestorTchuenguem Fohouo 2

’Department of Life and Earth Science; Higher Teachers’ training School, University of Maroua, P.O. Box 46, Maroua, Cameroon,

department of Biological Sciences; Faculty of Sciences, University of Ngaoundere; Cameroon.

* Corresponding author, e-mail: filsbkw27@gmail.com.

ABSTRACT We report the first record of the Giant House Bat Scotophilus nigrita (Schreber, 1774) (Mam-

malia, Chiroptera), from Cameroon where this species was never documented before. Scoto-

philus nigrita is one of the biggest species of Microchiropterans. Some mis identifications

were noted before 1978 with S. dingani (A. Smith, 1833) being identified as S. nigrita.

KEY WORDS Chiroptera; Scotophilus nigrita, Cameroon; new record.

Received 24.01.2012; accepted 23.02.2012; printed 30.03.2012

INTRODUCTION

As with many animal taxa, detailed scientific in-

formation about bats and their distribution in west-

central Africa is currently often lacking. Thus, most

African species are only known from a scattered

portion of their geographic ranges. Hence the ta-

xonomical and distributional status of many species

in this area remains enigmatic.

This is one of the principal problems facing

those who want to develop conservation or recovery

plans in this area (Fenton & Rautenbach, 1998).

The new record of a species in an area can be ex-

plained by two hypotheses: firstly the lack of inven-

tory in this area and secondly a low sampling effort

on this area. The main problem in central Africa is

the lack of bat studies.

Recent studies in this area have demonstrated

that some species, which were previously conside-

red to be absent or rare, have been regularly caught

(Cosson, 1995, Sedlacek et al., 2006).

This work can be useful for better understanding

of this important field of zoology and promote the

necessary guidelines for the protection of bats in

different geographical areas of the world; we must.

indeed, discuss further research on these special

mammals for a better understanding of their biolo-

gical behavior.

MATERIALS AND METHODS

On 13 April 2011, during a survey in the Sa-

helian zone of northern Cameroon, Bakwo (with

Bol) captured a single reproductive adult male in

Mokolo (10°43' 943”N; 13°46' 806”E; eleva-

tion: 849 m).

The specimen is deposited in the collection of

the Laboratory of Zoology of the University of

Maroua under the number BFEM 072.

The individual was caught in a mist net (9x2.8

m) set under water across a river at 21:21 hours.

This zone is characterized by a Sudano-Sahelian

climate with low savannah (Suchel, 1988). The

climate in the area is characterized by two seasons,

with major rainfall peaks generally occurring in

October (Suchel, 1988).

In our specimen, the belly is whitish with no

clear boundary (Fig. l).The predominant colour of

the pelage of the back is deep chestnut (Fig. 2).

E. M. Bakwo Fils, A. Bol A Anong & F.-N.Tchuenguem Fohouogiorno

Figures 1, 2. Scotophilus nigiita , male collected at Mokolo, on 13 April 2011 and currently in the collection of the Laboratory of

Zoology of the University of Maroua.

Figure 3. Records of Scotophilus nigrita (red) based on published data (African Chiropteran Report, 2011) including the recent re-

cord from Cameroon (indicated by star).

First record of the Gant House Bat Scotophilus nigrita in Cameroon (Mammalia, Chiroptera)

The external measurements of the specimen

were measured with a dial calliper (Mitutoyo) and

are as follows: FA: 84.8 mm; tibia: 34.2; ear: 19.3

mm; tail: 75.7 mm.

DISCUSSION

Based on our external measurements, we assign

this specimen to the taxon Scotophilus nigrita

(Schreber, 1774), which was not previously known

from Cameroon (African Chiroptera Report, 2011).

The measurements of the specimen do not exceed

the variation range reported for this species given

by Robbins (1978): FA: 86; and Robbins et al.

(1985): FA 82.3 (77.5-88.0), tail: 78 (76-80).

The Giant House Bat, Scotophilus nigrita

(Schreber, 1774), ranks as Near Threatened (NT) in

the IUCN redlist (Monadjem et al. 2010); Scotophi-

lus nigrita has been recorded as scattered records

from west, east, and south-east Africa (African Chi-

roptera Report, 2011).

It has been reported from Senegal, Cote

d'Ivoire, Ghana, Togo and Nigeria in west Africa,

from central Sudan, and from western Democratic

Republic of the Congo, western Kenya and Tanza-

nia, south to Mozambique, Malawi, eastern Zim-

babwe and north-eastern South Africa (Fig. 3).

This species ranks among the rarest bats in

Africa (Rosevear, 1965) and most information

on this species is based on casual records (Hap-

pold, 1987). Most of the few records of this spe-

cies in Africa have been from dry savannah sites

(Happold, 1987).

The present record also comes from a savannah

region and corroborates published data. However,

Happold (1987) mentioned an unusual presence of

this species near Lagos (Nigeria) in rainforest zone.

CONCLUSION

Scotophilus nigrita is one of the biggest species

of Microchiropterans. It was originally described

by Schreber in 1774 from a specimen collected in

Senegal (Robbins, 1978). Some misidentifications

were noted before 1978 with S. dingani (A. Smith,

1833) being identified as S. nigrita.

The new record bridges the gap between the

west African and the northeast and central African

distribution areas of this species (Fig. 3) and in-

creases the number of bat species known to occur

in Cameroon.

According to its previous known range, the nea-

rest record of this species was in Lagos (Happold,

1987) i.e. about 1250 km far from Cameroon.

Further survey is needed to specify the extend

of the range of this species and to determinate its

conservation status.

ACKNOWLEDGMENTS

Financial and logistical support was generously

provided by the International Foundation for

Science (D/4983-1).

We gratefully acknowledge valuable contribu-

tion of Mang Yannick Dimitry during the field

work.

REFERENCES

African Chiroptera Report, 2011. African Chiroptera Pro-

ject. Pretoria, i - xviii, 1- 4474.

Cosson J.-F., 1995. Captures of Myonycteris torquata

(Chiroptera: Pteropodidae) in forest canopy in south

Cameroon. Biotropica, 27: 395-396.

Fenton M.B. & Rautenbach I.L., 1998. Impacts of igno-

rance and human and elephant populations on the

conservation of bats in African woodlands. In: Kunz

T.H. and Racey PA. (eds.): Bat Biology and Conser-

vation. Smithsonian Institution Press, Washington,

D C., 261-270.

Happold D.C.D., 1987. The mammals of Nigeria. Cla-

rendon Press, Oxford, 402 pp.

Monadjem A., Raabe T., Dickerson B., Silvy N. &

McCleery R., 2010. Roost use by two sympatric spe-

cies of Scotophilus in a natural environment. South

African Journal of Wildlife Research, 40: 73-76.

Robbins C.B., 1978. Taxonomic identification and

history of Scotophilus nigrita (Schreber) (Chi-

roptera: Vespertilionidae). Journal of Mamma-

logy, 59: 212-213.

Robbins C.B., De Vree F. & Van Cakenberghe V., 1985.

A systematic revision of the African bat genus {{Sco-

tophilus)} (Vespertilionidae). Annales du Museum

Royal d'Afrique Centrale, Sciences Zoologiques,

246: 51-84.

Rosevear D.R., 1965. The Bats of West Africa, Trustees

of the British Museum (Natural History), London,

401 pp.

E. M. Bakwo Fils, A. Bol A Anong & F.-N.Tchuenguem Fohouogiorno

Sedlacek O., Horak D., Riegert J., Reif J., & Horacek I.,

2006. Comments on Welwitsch's mouse-eared bat

(. Myotis wehvitschii ) with the first record from Came-

roon. Mammalian Biology, 71: 120-123.

Suchel J.-B., 1988. Les climats du Cameroun. Tome

3: Les regions climatiques du Cameroun. These de

Doctorat d’Etat, Universite de St Etienne, France,

1177 pp.

Biodiversity Journal, 2012, 3 (1): 59-68

Cerambycidae (Coleoptera) richness in Mediterranean land-

scapes of Spain: diversity and community structure analysis

Francisco Javier Peris-Felipo & Ricardo Jimenez-Peydro

Laboratorio de Entomologia y Control de Plagas, Instituto Cavanilles de Biodiversidad y Biologla Evolutiva, Universitat de Valencia

(Estudi General), P. O. Box 22085, 46071 Valencia, Spain.

' Con-esponding author, e-mail: francisco.peris@uv.es.

ABSTRACT The aim of the present work was to analyse the diversity of Cerambycidae (Coleoptera) in 3

Spanish protected Mediterranean natural parks affected by bioclimatic conditions: La Font

Roja, Las Lagunas de la Mata-Torrevieja and La Tinenga de Benifassa. Sampling was conduc-

ted by direct and indirect collection (light and Malaise traps) between 2004 and 2009. During

this period, 1 ,102 specimens, belonging to 61 different species, were captured. Alpha, beta and

gamma diversities, as well as the structure of the communities were subsequently analysed.

Our results indicate that Tinen9a de Benifassa has higher diversity than Font Roja and Las La-

gunas de la Mata-Torrevieja. Based on analysis of structural models, these communities were

observed to be unstable and are composed of only a few abundant species and a large number

of rare species. All 3 parks conform to log-series and log-normal distributions. These results

demonstrate that it is not possible consider the habitat influence in community structure, since

each habitat displays very different botanical and faunal compositions, and climate conditions.

KEY WORDS Cerambycidae; Diversity; Community; Mediterranean landscape.

Received 15.02.2012; accepted 20.03.2012; printed 30.03.2012

INTRODUCTION

Mediterranean ecosystems are very important in

biodiversity terms, and are thus considered hotspot

areas (Myers et al., 2000). Landscapes and habitats

grow in complexity over time, as a consequence of

ecological processes. For example, Mediterranean

forest landscapes rich in evergreen species frequen-

tly intersect with brushwood, pasture, farming and

ranching areas.

In close proximity to these areas, however, it is

often possible to identify zones which have been re-

claimed by highly diverse natural communities after

the cessation of human intervention. Despite the

huge resistance displayed by Mediterranean bioto-

pes to human pressure, isolation and fragmentation

are unavoidable (Pungetti, 2003), resulting in the

emergence of isolated patches in the landscape.

Saproxylic beetles play an essential role in these

ecosystems, by taking part in decomposition pro-

cesses essential for the nutrient cycle, and by inte-

racting with other groups of organisms which are

also important for the well-being and economy of

the ecosystem, such as mites, nematodes, bacteria

and fungi (Speight, 1989; Alexander, 2008).

Beetles carry these organisms from tree to tree,

aiding their dissemination throughout the habitat

and are also involved in pollination (Nieto &

Alexander, 2010).

Significant long-term effects to Saproxylic

beetles which have been identified include loss of

habitat due to logging and wood harvesting and

the decline of older, old-growth trees throughout

the landscape, as well as the lack of land manage-

ment strategies aimed at recruiting new tree gene-

rations (Buckland & Dinnin, 1993; Nieto &

Alexander, 2010).

More short-term and localised threats arise from

sanitation works and the removal of old trees due

to safety concerns, in places subject to intense

Francisco Javier Peris-Felipo & Ricardo Jimenez-Peydro

human use (Hill et al., 1995; Johns, 1989; Grove &

Stork, 1999).

Raising awareness among conservation profes-

sionals and resource managers about the needs of

saproxylic organisms, who depend on tree aging dy-

namics and wood decay processes, is crucial, since

their role in the ecosystem has far-reaching impli-

cations for land management (Kaila et al., 1997;

Reid & Kirby, 1996).

A lack of intervention or minimal intervention

in formerly wooded pasture areas can deter the re-

newal of old trees, with very damaging results,

whereas livestock grazing may actually be very be-

neficial for the maintenance of adequate habitats

(Nieto & Alexander, 2010).

The death and decay of wood offers a broad

range of potential microhabitats for the spatial se-

gregation of different saproxylic insects, according

to tree species, tissue type and position within the

trees. In addition to this spatial segregation, a tem-

poral segregation follows degradation phases du-

ring wood decay. During this process, many stages

can be recognised along with their specific sapro-

xylic fauna. Saproxylic insect richness depends on

the quantity and quality of dead wood available in

the forest, as well as on forest size, fragmentation

and management (Mendez Iglesias, 2009).

The Cerambycidae family is one of the richest

in saproxylic beetles, with approximately 35,000

catalogued species (Grimaldi & Engel, 2005). Some

of these species have frequently been found to be

significant for the declaration of internationally im-

portant forests (Speight, 1989).

However, despite the large number of studies

on this family of beetles, very few studies have

been conducted on their diversity and community

structure in natural areas, to improve our under-

standing of this coleoptera community.

In this context, the current work aimed to ana-

lyse Cerambycidae community patterns and di-

versity in three natural parks in the Comunidad

Valenciana (Eastern Spain): La Font Roja, Las

Lagunas de la Mata-Torrevieja and La Tinen^a de

Benifassa.

These parks enjoy an outstanding position in

terms of biodiversity, emphasising their environ-

mental significance due to their particular biocli-

matic conditions. To analyse Cerambycidae

communities, weekly samples were collected, and

abundance, alpha, beta and gamma diversity, as well

as community structure were analysed for each park.

MATERIALS AND METHODS

Three natural parks in Comunidad Valenciana

were selected for Cerambycidae beetle collection

(Figs. 1-3): La Font Roja, Las Lagunas de la Mata-

Torrevieja and La Tinen^a de Benifassa, each of

which features peculiar microclimate conditions.

La Font Roja Natural Park is located to the

north of Alicante province, and is known for its

low level of anthropogenic disturbance. The park

extends over 2,298 ha, with a maximum elevation

of 1,356 m. The orientation of the hill range fa-

vours cool, moist winds from the northeast, resul-

ting in rainfall retention.

This fact, along with the steep slopes and the

predominance of limestone, fosters the existence

of different landscape units. Among these, deci-

duous forests, brushwood, scrub rock vegetation,

pine forests and agricultural areas can be differen-

tiated. In addition, each face experiences different

climate conditions: the north face is classified as

upper sub-humid, with annual rainfall between

600-1,000 mm; while the south face is dry, with an-

nual rainfall between 350-600 mm. Due to high

average temperatures throughout the year (15-

20°C), and the low average rainfall, the park is

classified as dry and thermo-Mediterranean.

Las Lagunas de la Mata-Torrevieja Natural Park

is located to the south of Alicante province, and ex-

tends over 3,700 ha, 2,100 of which are covered by

water. The park is notable for its saline soils, exten-

sive wild orchid population ( Orchis collina Banks

& Sol. ex Russell), differentiated areas of Senecio

auricula Bourgeau ex Coss and salt marsh plants of

the genus Limonium , reed and bulrush areas with

abundant grass plants such as Arthrocnemum sp.

and Juncus sp., and Mediterranean areas populated

by Ouercus coccifera L., Finns halepensis Mill, and

Thymus sp. The climate is arid with an annual rain-

fall below 300 mm and high temperatures.

La Tinenga de Benifassa Natural Park is located

to the north of Castellon province, and extends over

approximately 25,814 ha. The park covers an ex-

tensive and well-preserved mountainous area,

encompassing numerous and widely varied lan-

dscapes associated with medium and high-altitude

Mediterranean regimes and hosting a high biodiver-

sity of fauna and flora. It is possible to differentiate

forests of Finns sylvestris L., Finns uncinata Mill,

and Fagus sylvatica L., Juniperus communis L., and

Ouercus ilex L., alternating with crops of Primus sp.,

Cerambycidae (Coleoptera) richness in Mediterranean landscapes of Spain: diversity and community structure analysis

Figure 1 . Natural Park of La Tinen^a de Benifassa. Figure 2. Natural Park of Font Roja. Figure 3. Natural Park of Las

Lagunas de la Mata-Torrevieja. Figure 4. Arhopalus ferus. Figure 5. Stenurella melanura.

Francisco Javier Peris-Felipo & Ricardo Jimenez-Peydro

Corylus sp., etc. Climate conditions are continen-

tal humid, with annual average temperatures

below 12°C: freezing conditions are possible

throughout most of the year. Rainfall varies in dif-

ferent zones according to topographical features

and the annual precipitation ranges from 600 to

1,000 1/m 2 . The park is contained within the supra-

mediterranean bioclimate.

Samples were collected via direct capture on

plants located in the sampling areas and indirect

capture with light traps and Malaise traps (Tow-

nes model), which complement each other in the

capture of specimens.

Specimens were collected between 2004 and

2009 (Figs. 4-11). During this time, each natural

park was visited weekly, with a few exceptions due

to unforeseeable circumstances. Specimens captu-

red via direct and light trap were kept frozen and

specimens captured with Malaise traps were preser-

ved in 70% ethanol until final preparation. Speci-

mens were identified in the lab following criteria

established by Vives (2000) and Sama (2002).

Specimens were deposited in the UVEG ento-

mological collection.To analyse diversity and com-

munity structure, data were separately organised

according to taxa presence in each park, which has

been reported to be the most efficient method of in-

terspecific comparisons (Tavares et al., 2001).

Using this data, alpha, beta and gamma diversities

of each park were calculated.

Alpha diversity was calculated according to taxa

richness, abundance and dominance. Taxa richness

was used to evaluate richness in each sampling area,

and was measured using the Margalef index (Mo-

reno, 2001). Abundance refers to faunal composi-

tion in each area (Magurran, 1991), and was

measured using the Shannon index, which evaluates

equity and indicates the degree of uniformity in spe-

cies representation (in abundance), taking all data

into consideration (Moreno, 2001; Magurran, 1991;

Villarreal et al., 2004). Dominance was calculated

by measuring genera and species occurrence using

the Simpson index, which is often used to measure

species dominance values in a given community;

negative values represent equity (Magurran, 1991).

The following indexes were used to measure

beta diversity: the Jaccard index, which relates the

total amount of shared species with the total amount

of exclusive species (Moreno, 2001; Villarreal et

al., 2004); the complementarity index, which indi-

cates the degree of similarity in species composition

and abundance between two or more communities

(Moreno, 2001; Villarreal et al., 2004); and cluster

analysis, which is used to calculate the degree of

correlation based on similarity/dissimilarity. The

statistics-processing software PAST was used for

calculation of these values. (Hammer et al., 2001).

Finally, gamma diversity, which indicates the

degree of diversity of all involved environments, is

determined from the richness index of each area

(alpha diversity) and the beta diversity (Schluter &

Ricklefs, 1993; Villarreal et al., 2004).

In order to complete the diversity analyses and

investigate the community structure, log-series, log-

normal and broken-stick models were also applied

(Magurran, 1991). The log-series model represents

an unstable community, composed of a few abun-

dant species and a high number of rare species. The

broken-stick model refers to maximum occupation

of an environment with equitable sharing of resour-

ces between species. Finally, the log-normal reflects

an intermediate situation between the previous two

models (Soares et al., 2010).

Using the data obtained from the 3 parks, each

of these models was applied to calculate the expec-

ted number of species - log2, grouping species ac-

cording to abundance (Magurran, 1991; Tokeshi,

1993; Krebs, 1999). To test the significance of the

models, expected species values were compared

with those from observed species by chi-square

analysis (Zar, 1999).

RESULTS

During the sampling period, a total of 1,102

specimens of Cerambycidae, representing 61 spe-

cies, were collected (Table 1). Tinenga Natural

Park (NP) displayed the most abundance and spe-

cific richness, with 534 collected specimens and 56

species. Especially abundant were Agapanthia

cardui (14.55%), Stennrella melanura (46.93%)

and Pseudovadonia livida (10.45%).

La Font Roja NP was second in abundance and

specific richness, with 390 specimens and 27 spe-

cies. The most abundant were Stenurella melanura

(46.93%) and Chlorophorus trifasciatus (16.53%).

Finally, Las lagunas de la Mata-Torrevieja NP had

193 specimens and 13 species, of which Agapanthia

cardui , with 62.69%, was the most abundant. In

terms of alpha diversity, Tinen^a NP showed the

most specific richness, with a value of D ^ = 8.91 1,

Cerambycidae (Coleoptera) richness in Mediterranean landscapes of Spain: diversity and community structure analysis

Figure 6. Pseudovadonia livida. Figure 7. Stenopterus ater. Figure 8. Chlorophorus trifasciatus. Figure 9. Monochamus

galloprovincialis. Figure 10. Agapanthia cardui. Figure 11. Agapanthia asphodeli.

Francisco Javier Peris-Felipo & Ricardo Jimenez-Peydro

Species

Tinenga

FontRoja

Lagunas

Acanthocinus aedilis (Linnaeus 1758)

“2“

0.37

“0“

Agapanthia annularis (Olivier 1795)

“U”

3.11

Agapanthia asphodel i (Latreille 1804)

~nr

3.36

~TT

3.46

2 6

2.59

Agapanthia cardui (Linnaeus 1767)

14.55

~TT

5.60

121

62.65

Agapanthia dahli (Richter 1 §20)

0.55

Agapanthia villosoviridescens (De Geer 1775)

0.75

Albcma m-griseum Mulsant 1 846

~U~

~r~

1.06

AnastrangaUa sanguinolenta (Linnaeus 1761)

~r~

0.75

“U”

Arhopahts ferns (Mulsant 1 839)

0.37

2.13

1.04

Arhopalus rusticus (Linnaeus 1758)

0.56

~T~

1.6

Arhopalus syriacus (Reitter 1 895)

“2“

0.37

Aromia moschata (Steven 1 809)

~T~

0.15

“U”

Calamobius Jilum (Rossi 1790)

4.85

1.6

3.63

Cerambyx cerdo (Lucas 1842)

0.56

o.§

Cerambyx scopolii (Fuessiy 1775)

0.75

“U”

Certalhim ebulinum (Linnaeus 1767)

1.68

~TT~

3.11

Chlorophorus pilosus (Forster 1771)

~TT~

3.54

~1T~

3.46

Chlorophorus rujicornis (Olivier 1790)

”2”

0.37

Chlorophorus sartor (Muller 1766)

~T~

0.19

“2“

0.53

Chlorophorus trijasciatus (Fabricius 1781)

~~W~

5.60

16.53

Chlorophorus varius (Muller 1766)

~2 r

0.37

Clytiis arietis (Linnaeus 1758)

~1T~

2.43

Clytus rhamni Germar 1817

“2“

0.37

Clytiis tropicus (Panzer 1795)

~T~

0.15

“0“

Ergates faber (Linnaeus 1761)

”2”

0.37

~T~

0.26

Hesperophcines sericeus (Fabricius 1787)

0.19

Hylotnipes bajulus (Linnaeus 1758)

“2“

0.37

“2“

0.53

~U~

Iberodorcadion fuentei (Pic 1 §55)

~T~

0.15

~T~

0.52

Iberodorcadion sutural e (Chevrolat 1862)

0.52

Monochamus gall opr ovincialis (Olivier 1795)

~T~

1.12

“2“

0.53

“2“

1.04

Opsilia caerulescens (Scopoh 1763)

~TT~

4.25

4.26

~TT~

13.47

Pachitodes cerambiciformis (Schrank 1781)

0.56

Paracorymbia fulva (De Geer 1775)

“2“

0.37

~U~

Paracorymbia otini (PeyenmhotF 1949)

“0“

~u~

~T~

0.26

~U~

“0“

Penichroa fasciata (Stephens 1831)

”2”

0.37

”2”

0.53

Phymatodes testaceus (Linnaeus 1758)

0.53

Phytoecia pustulata (Schrank 1776)

— T~

0.75

~U~

Phytoecia virgula (Charpentier 1825)

2.80

~~r~

1.06

Plcigionotus arcuatus (Linnaeus 1758)

0.19

Pogonocherus perroudi Mulsant 1839

~T~

0.15

Prionus coriarius (Linnaeus 1758)

~T~

0.15

Pseudovadonia livida (Fabricius 1777)

10.45

Purpuricenus budensis (Goeze 1783)

~1T~

2.61

Rutpelci maculata (Poda 1761)

“2 ”

0.37

Saperda carcharias (Linnaeus 1758)

“2“

0.37

Stenopterus ater (Linnaeus 1767)

3.92

~12~

3.2

Stenopterus mauritanicus (Lucas 1846)

~T~

1.12

Stenopterus rufus (Linnaeus 1767)

~r~

0.75

Stenurella bifasciata (Muller 1776)

0.56

Stenurella melanura (Linnaeus 1758)

~TT~

11.75

176

46.53

Stenurella nigra (Linnaeus 1 75§)

~W~

6.72

“U”

Stictoleptura cordigera (Fuessiy 1775)

0.56

0.26

Stictoleptura fontenayi (Mulsant 1839)

~T~

0.37

Stictoleptura rubra (Linnaeus 1758)

~r~

0.56

“U”

Stictoleptura scutellata (Fabricius 1781)

0.19

0.26

Stromatium unicolor (Olivier 1795)

~~T~

1.31

~T~

0.26

~T~

0.52

Trichoferus fasciculatus (Faldermann 1837)

0.56

~T~

0.53

~~T~

6.74

Trichoferus griseus (Fabricius 1792)

0.53

“U”

Vesper us xatarti Dufour 1 839

0.75

2.4

“ 2 “

1.04

Xylotrechus antilope (Schonherr 1817)

“ 2 “

0.37

Xvlotrechus arvicola (Olivier 1795)

“ 2 “

0.37

“0“

TOTAL

534

375

193

Table 1. Cerambycidae abundance and average for each Natural Park.

Cerambycidae (Coleoptera) richness in Mediterranean landscapes of Spain: diversity and community structure analysis

followed by La Font Roja, with 4.218; while Lagu-

nas de Torrevieja showed the least specific richness

with a score of 2.28 (Table 2). In addition, accor-

ding to the Shannon index, proportional abundance

was also highest for Tinenga (3.212) and lowest for

Lagunas (1.399). Furthermore, results obtained with

the Simpson index are in agreement with these ran-

kings (0.9346 for Tinenga, 0.7417 for Font Roja and

0.5799 for Lagunas) (Table 2).

In order to calculate beta diversity (similarity/dis-

similarity), data from the different sampling areas

Tinenga

Font Roja

Lagunas

Species

Specimens

534

375

193

Shannon

3.212

2.032

1.399

Simpson

0.9346

0.7417

0.5799

Margalef

8.911

4.218

2.28

Table 2. Diversity and abundance of Cerambycidae captured.

were compared using the Jaccard index (Table 3).

The results show a low level of comparability bet-

ween species inhabiting each park; the highest

value was found for the combination

Tinenga/Font Roja (0.383), followed by Font

Roja/Lagunas (0.344).

The comparability between Tinenga and La-

gunas was even lower, with a value of only 0. 186

(Table 3). This increased similarity between Ti-

nenga and Font Roja is due to the fact that the

predominant botanical composition is similar in

both forests.

On the other hand, the relationship between

Font Roja and Lagunas is due to the fact that both

natural parks have a high abundance of Pinus ha-

lepensis, which have an associated fauna of sapro-

xylic insects. Finally, the low comparability value

obtained between Tinenga and Lagunas is due to

significant differences in the botanical composi-

tion of these 2 parks.

With respect to the Complementarity Index (C),

Tinenga/Lagunas showed the highest value (0.813),

again indicating the dissimilarity between species

captured in each park; while Tinenga/Font Roja

showed lower complementarity (0.45), indicating a

stronger similarity in the specific composition of

these parks (Table 3).

These results were subjected to cluster analy-

sis using a Jaccard cluster (Fig. 12). Gamma di-

versity grouped all 3 parks, yielding a value of 62.

Tinenga

Font Roja

Lagunas

Tinenga

0.383

0.186

Font Roja

0.45

0.344

Lagunas

0.813

0.655

Complementarity

Table 3. Comparative of Complementarity and Jaccard

indexes values for Cerambycidae in each park.

0 , 95 -

0 , 9 -

0 . 85 -

0,8

| 0 , 75 -|

0 . 7 -

0 . 65 -

0 , 6 -

0 , 55 -

Figure 12. Cluster of Cerambycidae per NP.

Tinenga, with 57 captured species, displayed

the most diversity, followed by Font Roja (26) and

Lagunas (13).

Finally, analysis of the community structure of

Cerambycidae in each park revealed agreement

with log-series and log-normal models, with p-va-

lues greater than 0.05, while no parks matched the

broken-stick model (resulting p-values were below

0.05) (Table 4).

Francisco Javier Peris-Felipo & Ricardo Jimenez-Peydro

Log-series Log-normal Broken-stick

FontRoja Tinenqa Torrevieja FontRoja Tinenga Torrevieja FontRoja Tinenga Torrevieja

Class exp f obs f exp f obs f exp f obs f exp f obs f exp f obs f exp f obs f exp f obs f exp f obs f exp f obs f

2.75

3.75

1,16

9.66

23.26

4.69

7.40

17.71

3,51

3,27

10,22

1,48

3.62

8.50

1.76

3.41

9.01

1,5

2,87

8,31

1,32

3.76

8.49

1.83

3.54

9.17

1,53

4,74

12,25

2,22

3.57

7.49

1.74

2.89

6.91

1,24

6,44

13,38

3,12

3.01

5.47

1.48

2.01

3.94

0,87

5,96

8,17

3,02

2.09

2.87

1.04

1.11

1.72

0,49

2,56

1,67

1,32

1.00

0.81

0.51

0.50

0.56

0,23

0,24

0,04

0,09

0.24

0.07

0.10

0.19

0,14

0,00

0.01

0.08

0,00

X 2 = 7.24 X 2 = 5.67 X 2 = 6.77 X 2 = 9.57 X 2 = 10.23 X 2 = 7.91 X 2 = 1271.1 X 2 = 57.64 X 2 = 28.85

p = 0.5106 p = 0.4607 p = 0.4522 p = 0.2961 p = 0.1152 p = 0.3402 p = 0.0000 p = 0.0000 p = 0.0001

Table 4. Expected specific frequencies for each of the models used and statistical comparison with observed frequencies.

DISCUSSION

Alpha diversity results show that Tinenqa de Be-

nifassa NP has higher diversity and specific ri-

chness than the other 2 parks. In addition, a

comparison of the results for each park reveals no-

tably disparate values, due to wide differences in

the number of identified species. This is corrobora-

ted by the dissimilar values of the Shannon and

Simpson indexes, indicating a lack of similarity in

the distribution of dominant species.

Beta diversity results suggest that the three parks

under consideration in the present study are marke-

dly different in specific composition. Despite this

low similarity, the Complementarity index shows

that Tinenqa NP and Font Roja NP do have some

similarities in their specific composition.

Taken together, these data suggest that Tinenqa

NP has the highest biodiversity among the three

parks, each of which contains a specific Ceramby-

cidae faunal composition. This correlates with the

different botanical compositions and habitats pre-

sent in each park, since the cycle of each Ceramby-

cidae species (with the exception of a few, less

specialised ones) is associated with certain plant

species (Linsley, 1959; Vives, 2000). In contrast,

analysis of the structural models of these commu-

nities indicates that Cerambycidae communities in

all of these parks fit log-series and log-normal mo-

dels, which means that they include a few abundant

species and a number of rare species.

Thus, community structure is not determined by

habitat, because all three parks display very diffe-

rent faunal and botanical compositions and biocli-

mates. Community structure also appears to be

unaffected by human action, because while Lagunas

de la Mata-TorreviejaNP is fully encircled by roads

and housing, Tinenqa NP has remained virtually

free from anthropogenic pressure. To conclude, stu-

dies on biological diversity and community struc-

ture are vital for the development of a better

understanding of ecosystems, and for the correct

adoption of measures for the conservation and

maintenance of biodiversity (Pyle et al., 1981; Pe-

arson & Cassola, 1992; Kremen et al., 1993).

ACKNOWLEDGMENTS

We wish to thank the staff of Parque Natural de

la Font Roja, Parque Natural de las Lagunas de la

Ceram bycidae (Coleoptera) richness in Mediterranean landscapes of Spain: diversity and community structure analysis

Mata-Torrevieja and Parque Natural de la Tinenga

de Benifassa for their help during this study. Also,

we would like to thank all of those who have offe-

red their support, time and advice.

This work was funded by the research project

CGL-2004-027 1 1 and co-funded by the Ministry of

Science and Technology and the European Union

(European Regional Development Fund).

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Biodiversity Journal, 2012, 3 (1): 69-78

Can a simple Pelagic-Demersal ratio explain ecosystem

tinctioning?

Maria Grazia Pennino 1, & Jose Maria Bellido 1,2

1 Instituto Espanol de Oceanografia. Centro Oceanografico de Murcia. C/ Varadero 1. San Pedro del Pinatar. 30740. Murcia. Spain.

2 School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, AB24 2TZ Aberdeen, Scotland, UK.

’Corresponding author, e-mail: grazia.pennino@mu.ieo.es.

ABSTRACT In quantity terms, the proportion of the total marine fish landings which is accounted for by

pelagic fish has increased continuously, with large oscillations reflecting natural variations

of resources productivity and fishing strategies. The aim of the present work is to assess this

trend in different Mediterranean fishing areas from 1970 to 2005 using the Pelagic/Demersal

ratio (P/D). The P/D ratio is a simple ecosystem indicator based on commercial landings and

provides a measure of the status of the fish community also in data-poor fisheries situations.

Simple statistical techniques were used to study fishery ecosystem through the collection and

comparison of geographical parameters as chlorophyll-^ (Chl-a) pigmentation intensity and

rainfall. In all the Mediterranean the P/D ratio appears to be correlated with the mean Chl-a

value and increased with time, this may depend both on a better availability of nutrients in

the water column and the overexploitation of resources. The areas where there is a greater

presence of zones of upwelling and nutrient inputs are the ones with the highest values of the

index. Additionally, comparison with the analysis of the multispecies landings shows that the

trend of the index is influenced by the landings of Clupeidae and Engraulidae, a fact showing

that fisheries in these areas are increasingly relying on the smaller, short-lived fishes from the

lower part of marine food webs.

KEY WORDS Pelagic-Demersal ratio; Mediterranean Sea; Chlorophyll-^; Rainfall.

Received 16.02.2012; accepted 18.03.2012; printed 30.03.2012

INTRODUCTION

There is a growing understanding that exploited

fish populations must be considered as integral

components of ecosystem function, rather than units

operating independently of their environment (Cury

& Christensen, 2005). Internationally, there has

been wide recognition of the need to move towards

an ecosystem approach to fisheries, a development

spearheaded by FAO through their Code of Conduct

for Responsible Fisheries (Garcia, 2000), and sup-

ported by many regional and national institutions.

A special attention has been focused on fishing

in the Mediterranean Sea, where significant eco-

system changes have become evident in recent de-

cades (Zaitsev, 1994; Caddy et al., 1995; Pauly &

Watson, 2004).

FAO data show that landings from marine fish

species (about 400,000 tonnes) has increased con-

tinuously, with large oscillations reflecting natural

variations of resources productivity as well as pro-

bably boom and bust fishing strategies.

The modernisation of small- and large-scale fi-

shing fleets (i.e., larger boats, higher tonnage and

engine horsepower, improved fishing gears, use

of high-technology equipment) led to the expan-

sion of fishing in areas previously inaccessible

(Stergiou et al., 1997).

As a result, new ‘resources’ started to be exploi-

ted, mostly at high trophic levels. Moreover, while

Maria Grazia Pennino & Jose Maria Bellido

earlier studies suggest that the Mediterranean was

originally very nutrient-limited (Murdoch &

Onuf, 1972), recent researches show that the eco-

system is significantly affected by nutrient run-

off over the last years.

Pelagic fishes are generally influenced by nu-

trient enrichment when it stimulates the plankton

production (Caddy, 1993), while demersal fishes

are influenced by the dynamics of benthic commu-

nity, which generally responds negatively to the

conditions of excessive enrichment (De Leiva Mo-

reno et al., 2000).

The aim of the present work is to assess this

trend in the Mediterranean Sea with the use of the

ecosystem indicators. These indicators are to be

estimated by fishery, environmental data and simple

statistical techniques.

The Pelagic/Demersal index is a simple indi-

cator that can be derived from commercial stati-

stics. This ratio synthesizes the structure and

functioning of the ecosystem in time and space

and, in turn, how fisheries and eutrophication in-

fluence them (Libralato et al., 2004).

In fact, an increase in the P/D ratio of landings

would seem to imply either an increase in forage

fish abundance due to predatory release or environ-

mental change. The decline of top predators stocks

due overfishing leads to expansion in biomass of

pelagic fishes. A similar result may occur with eu-

trophication, because the demersal resources are ad-

versely affected by hypoxia resulting from excess

primary production, which has less negative effects

(or may even be positive) for pelagic species.

For this reason, the trend of the P/D index

was compared with multispecies landings, with

an independent index of primary production, na-

mely the surface concentration of Chlorophyll-a

(Chi -a), and with an index of potential land run-

off impacts on marine fisheries such as precipi-

tation to the sea surface.

The present study shows the potential of the

Large Marine Ecosystem approach to examine

these phenomena in the whole Mediterranean fi-

shery ecosystem, in order to obtain an integrated in-

sight of environmental and fishery issues.

The innovativeness of this approach is the con-

sideration of the ecosystem as a whole including all

the geographical, biological and ecological interac-

tions, allowing the acquisition of new knowledge of

coastal and marine ecosystems (Pennino et al., 2011).

MATERIALS AND METHODS

Fishery data was achieved from the GFCM (Ge-

neral Fisheries Commission for the Mediterranean)

database (www.fishbase.org) that presents annual

statistics allocated by countries, species items and

statistical divisions, of capture production in the

Mediterranean and Black Sea region for the period

1970-2005. For statistical purposes the Mediterra-

nean GFCM region, which coincides with the FAO

fishing “Area 37- Mediterranean and Black Sea",

has been split into seven divisions (Fig. 1).

We have only analyzed the data of Mediterra-

nean Sea, excluding those of the Black Sea. Lan-

dings data refer to nominal catches of 25 1 different

species, not biomasses, and refer legal and reported

large- and small-scale fisheries, excluding recrea-

tional or sport fishing.

These are collected by the national institution

and reported to FAO by Member Countries. The

data exclude production from marine aquaculture

practices and statistics for marine mammals and

seaweeds. The P/D index is estimated as the ratio

between pelagic species and demersal species, that

were defined by trophic information that classify

the diet of adults of each commercial species, and

were extracted from Stergiou & Vasiliki (2002) and

fishbase website (http://www.fishbase.org). The

P/D ratio was calculated for all 35 years of time se-

ries and for each division.

Subsequently, the index trend was compared

with their multispecies landings grouped in 15

groups according to trophic level. The trophic

level of each group is a mean of the different va-

lues that exist for a given species, obtained from

Fishbase (www.fishbase.org) and from Stergiou

& Vasiliki (2002). The environmental data used in

this study were acquired using the “GES-DISC

Interactive Online Visualization ANd aNalysis In-

frastructure (Giovanni), as part of the NASA's

Goddard Earth Sciences (GES) Data and

Information Services Center (DISC)” (http://ocean-

color.gsfc.nasa.gov/).

An independent index of primary production,

namely the surface concentration of Chlorophyll-#

(Chi-#) was used based on remote sensing imagery

from 1998 to 2005. Obviously primary production

depends on a range of factors, including light, light

penetration, temperature, which could not be taken

into account here for the absence of comparable

Can a simple Pelagic-Demersal ratio explain ecosystem functioning?

quantitative data with a broad temporal and geo-

graphical coverage.

Nevertheless, the mean annual value of Chl-a is

an index of primary production that represents the

seasonal production of the marine area considered.

To extract and analyze the Chi -a data we used the

function “Lat-Lon Map, Time-averaged” that pro-

vides a time-averaged colour data plot for a speci-

fied area. The values plotted are the mean value of

the data product calculated for year. After adjusting

for different grid referencing systems, maps of the

GFCM subdivisions were superimposed on images

of mean Chl-a values, in order to obtain specific in-

formation for each fisheries subdivision.

We analyzed the data of rainfall to the sea sur-

face to assess a nutrient input for every division and

year of the series. The annual mean data are extrac-

ted with the same function “Lat-Lon Map, Time-

averaged”, as mm/hr for rain rate for mm for

accumulated rainfall. The source is TRMM and

Other Satellite Monthly 0.25° x 0.25° Rainfall Data

Product (3B43 Version 6).

RESULTS

Balearic

The area of Mediterranean Sea that has the hi-

ghest values of P/D ratio is Balearic with a mean of

3.15 (Table 1). The trend of the index reaches the

highest values in 1988 with 4.32 and in 1994 with

3.97 (Fig. 1). Comparing this P/D trend with the

landings it can be seen that in those same years

there have been increases in the landings of the

class Clupeidae with respectively 146,704 and

Divisions

Chl-tf

(mg/mm 3 )

Rainfall

(nun/Km 2 )

P/D index

Balearic

0.45

583

3.15

Gulf of Lions

0.79

618

2.80

Sardinia

0.31

624

0.45

Adriatic

0.95

911

0.90

Ionian

0.39

454

0.80

Aegean

0.27

559

1.23

Levant

0.68

356

0.80

Table 1 . Mean of Chlorophyll-a, Rainfall and Pelagic/De-

mersal index for all Mediterranean divisions (1998-2005).

172,747 tonnes (Fig. 2). In the first half of the 80s

landings of this class suffered a decline, while in-

creasing those of the class Engraulidae (Fig. 2).

The analysis of the time series shows a negative

relationship between these classes, i.e. any decrease

in landings of Clupeidae is offset by an increase of

landings of Engraulidae. These two categories are

respectively 55% and 10% of total landings of Ba-

learic. The most representative species in the class

Clupeidae is the European sardine ( Sardina pilchar-

dus ), while in the class Engraulidae is the European

anchovy ( Engraulis encrasicolus).

The index of primary production, calculated by

the time series of 1998-2005, shows constant trend

Balearic

: o » -

200000

180000

ISOOOQ

UO00D

129000

100000

80000

£0000

40000

20000

Qfiiv&i/a B Crustacea □Cepnjlopocj □ C entracanthldae

Be rgraui da* □ Haiti slits ■ Clupeidae □ l.lulliflje

Qspardae Qscorpaenifomies jMertucciiaae Q •- eormjndoe

□GaOdae QRajlfcimes □ S tiarfc*

1975

>985

1995

2005

19T0

‘■990

1990

yti'tit

2000

Figure 1. Pelagic/Demersal ratio of Balearic. Figure 2. Group's landings of Balearic.

Maria Grazia Pennino & Jose Maria Bellido

with a minimum value of 0.41 (mg/mm 3 ) in the first

year of the series, and a maximum of 0.48 (mg/mm 3 )

in 2001. The peak of Chl-a in 2001 is also found in

the values of P/D index and corresponds to an in-

crease in Clupeidae landings (Fig. 15).

The increased intake of nutrients in these years

is not found in the trend of Chi -a, but the trend is

reflected in the P/D ratio. In fact in 2003 the index

recorded a value of 3.63, the highest in the last years

series. At the species level in the same year class

Scombridae landings increased of 11,000 tonnes.

The precipitation levels remain fairly constant

across the years with values around 500 mm, except

in 2002 and 2003, which recorded an average of 700

mm (Fig. 16). Another factor to take into account is

that Balearic receives inflows of Atlantic water with

significant inputs of nutrients with important upwel-

ling occurring in the Alboran Sea and along the Al-

gerian coast (Estrada, 1996; Caddy & Oliver, 1996).

Gulf of Lions

After the Balearic, the Gulf of Lions is the area

with the highest average P/D, with a value of 2.80

(Table 1). The higher values of the time series are

recorded in the early years, matching the biggest

landings of the class Clupeidae and Engraulidae.

The two classes are the 45% and 16% of the total lan-

dings. The minimum values are found in 1986 and

1982 (1.2 and 1.13) corresponding to an increase in

the landings of the Bivalvia (Figs. 3 and 4). In 2003

there was a further decline in the P/D index, given

the increased Merluccidae landings (Fig. 4).

In the same year the index of primary production

shows its lowest value (0.69 mg/mm 3 ). The year

2001 shows the highest peak in the trend of Chl-a,

as in Balearic, and corresponds to an increase in the

P/D index and in the Engraulidae landings (Fig. 15).

The index P/D shows a declining trend in 2005

correlated with a decrease in landings of small pe-

lagic species, but not with the concentration of

Chl-a. The average rainfall is one of the highest in

the Mediterranean, taking into consideration that it

is the smallest division, and also the area receives

considerable inputs from the river Rhone.

In 2001, when the trend of Chl-a and the P/D

ratio record the maximum value, the level of rainfall

in the area is minimal (Fig. 16). The maximum

value of precipitation is recorded in 2002 (834 mm),

year when the landings of the class Engraulidae in-

crease of 4,000 tonnes, while those of class Clupei-

dae decrease by 3,000 tonnes.

Sardinia

The lowest P/D index occurs in the Sardinia di-

vision and remains below unity for the entire time

series, with a mean the 0.45 (Table 1). Only in its

first decade in which landings of Engraulidae and

Clupeidae are high, the values exceed the unit (Figs.

5 and 6). In recent decades they have been repre-

sented mainly by the class Bivalvia. Until 1986 the

landings of small pelagic fish are between 20,000

and 30,000 tonnes.

In these years a negative relationship is apparent

between the landings of Engraulidae and Clupeidae,

i.e. a rise in landings of one group reflects a de-

crease in the other group. Since 1987 the landings

show a sharp drop of 20,000 tonnes. Only in 1993

the Engraulidae class has a peak of 10,000 tonnes,

while Clupeidae in 1999, 2003 and 2005.

The P/D index shows an increase only in 1999

and 2005. This is because the index is heavily in-

fluenced by the landings of Bivalvia starting in the

mid 80s; when landings of this fall in 2005, the

index increases up to a value of 0.82. Values of P/D

index less than 1 indicate a prevalence of demersal

fishes compared to pelagic species.

The landings of this area, unlike others that have a

high prevalence in the total landings of pelagic species,

have a uniform distribution in all classes (Fig. 6).

Furthermore, in this area most of the fishing

boats are mainly of small-scale fishing, which cor-

responds to a different environmental impact. The

index of primary production shows a constant trend

with a maximum 0.36 (mg/mm 3 ) in 2005, coinci-

ding with the increase of the Clupeidae landings

and the P/D ratio (Figs. 15 and 5).

The minimum value is recorded in 2001 (0.27

mg/mm 3 ). It is surprising that maximum and mini-

mum values are close in time, configuring a quite

erratic trend in last years. The decrease of Chl-a in

2001 also finds its counterpart in the trend of rain-

fall. Indeed, the trend remains constant throughout

the series with an average of 624 mm and records

the minimum value in 2001 with 520 mm (Fig. 16).

Adriatic

De Leiva Moreno et al. (2000) found a mean

value of P/D equal to 3.76 in the Adriatic for the hi-

storical series 1978-88. From our analysis, the mean

P/D is 0.90; years from 1978-88 show the highest va-

lues of the index, but always less than 3 (Fig. 7).

Can a simple Pelagic-Demersal ratio explain ecosystem functioning?

Gulf of Lions

□ Bivalvia

■ : ngrauiidae

■>:> pantfae

H’3adidae

H 'lustacea

OnaWshes

□?i cgrpaeniromi

i tonnes

□ Cephalopoda

■ cuipr sae

■ MpducciKise

□ Shams

O - erWracanlhidae

pMuiiiane

□ 5 com tadae

1975

1985

(995

2005

1970

1980

1990

2000

years

tDones

85000

30000

25000

20000

15000

10000

5000

Sardinia

□ Bivaiuia Qemstacea □ Cephalopoda QcemracaniniEae

■ Emjraundae ElHatflsIies ■ Ctupedae □ Muniaae

■ 5 paodae □scctpaefiifornies Pwpimceiidae Qscomofldiae

OGadiflae QRajitofmes □ s narks

1975

1985

1995

20D5

1970

I960

1990

2000

Wanes

100000

90000

80000

70000

60000

50000

40000

80000

20000

10OQ0

Adriatic

HBivalMa Hemstacea □ Cephalopoda ■C entracanmaae

■Enorauncae Daatnsties ■ Oiupeicae □i.iuiMiae

■spanoae Qscoipoentiormes ■ Metiucciidae Qscombr'dae

HOadidae PRajifomies P Sltaite

1975

1970

1980

1985

vears

1995

2005

1990

2080

Figure 3. Pelagic/Demersal ratio of Gulf of Lions. Figure 4. Group's landings of Gulf of Lions.

Figure 5. Pelagic/Demersal ratio of Sardinia. Figure 6. Group's landings of Sardinia.

Figure 7. Pelagic/Demersal ratio of Adriatic. Figure 8. Group's landings of Adriatic.

It is known that the Adriatic is under the in-

fluence of the rather polluted river Po which brings

in around 330,000 1 of nitrogen and 28,000 1 of pho-

sphorus annually (Degobbis, 1989), and seasonally

intense hypoxia of the upper Adriatic is caused by

phytoplankton blooms (Legovic & Justic, 1997).

Moreover, the analysis of the level of rainfall

throughout the Mediterranean shows that the Adria-

tic has the highest average (911 mm), confirming

the major nutrient input from this area. According

with these reasons we would expect high values in

the index; the analysis by species notes that large

quantities of landings of Bivalvia affect strongly the

index (Fig. 8). This class represents 23% of the lan-

dings of the area and it is an important local fishery

resources, especially in the lagoon of Venice, where

the species of the genus Tapes are heavily exploited

(Granzotto et al., 2003).

Indeed the index P/D, calculated without the

landings of the Bivalvia reaches values equal to 4.

The index records the highest values in 1979 (2.3 1),

at the peak in landings of Engraulidae (90,000 ton-

nes), and in 1981 (2.32), at the peak landings in the

class Clupeidae (62,000 tonnes).

Maria Grazia Pennino & Jose Maria Bellido

Over the years 1986-1995 the class Clupeidae

undergoes a sharp collapse in the landings and the

index P/D shows a declining trend reaching a mi-

nimum value of 0.63 in 1992. Comparing the values

of Chi-# with the other areas, it is clear that the

Adriatic is the area with the highest mean (0.95

mg/mm 3 ). Analyzing the time series in the primary

production is noted that the minimum value was re-

corded in 2003 (0.64 mg/mm 3 ) (Fig. 15).

The index P/D shows a positive relationship

with the trend by highlighting the minimum value

of 0.68 in the same year, reported probably with the

highest peak of the whole series of class Bivalvia.

In the same year the trend of rainfall records the mi-

nimum value (720 mm) (Fig. 16).

In 2002 and 2004 the level of rainfall and Chi-#

reached the maximum value and the P/D ratio

seems to follow these maximums, presenting P/D a

slightly increase (Figs. 7 and 8). Landings by spe-

cies show in 2002 a decrease of 7,000 tonnes in the

Engraulidae class, while in 2004 increase of 16,000

tonnes. In 2002 also landings of Bivalvia suffered

a collapse and, after a recovery in 2003, continue

to decline (Fig. 8).

Ionian

The Ionian has a mean P/D ratio of 0.80, with

values of less than 1 for the entire series (Table 1).

The 19% of total landings is the Cephalopoda class

with a sharp increase in 1988 of 20,000 tonnes. In

this area the values of the index and the analysis of

the landings do not seem to support that there is a

clear predominance of pelagic fish on groundfish

(Figs. 9 and 10). In fact, 12% of the landings be-

longs to the class Merluccidae that significantly re-

duces the value of the index (Fig. 10).

The Chi-# index in this area is generally in the

range 0.20-0.30 mg/mm 3 and remains constant for

the entire time series. After Levant, Ionian shows the

lowest average (454 mm) in the level of rainfall, de-

spite being the largest division of the Mediterranean.

The trend of rainfall remains constant over the years

with values ranging between 500 and 400 mm, ex-

cept in 2000 where it reached 300 mm (Fig. 16). In

the same year also the Chi -# registered its lowest

value (0.37 mg/mm 3 ) (Fig. 15). In 2003, the values

of Chi-# and rainfall reach the maximum, while the

P/D ratio decreases and the trend of landings by spe-

cies shows a joint decline in the landings of the class

Clupeidae, Sparidae and Scombridae.

Aegean

The Aegean shows a mean P/D ratio of 1.23.

The values are higher in the first four years and bet-

ween 1979 and 1985, reflecting high landings of

classes Clupeidae and Engraulidae (Fig. 11). The

two categories account for 22% and 15% of the

total landings. In correspondence of the years in

which values of the index are rising, nutrient inputs

increased under the influence of river run-off and

Sea of Marmara inflows (Friligos, 1989). Although

in recent decades the landings of Clupeidae and En-

graulidae classes are significantly increased, values

of P/D are less than 2, because there is also a large

increase in landings of the class Bivalvia and Cru-

stacea (Fig. 12). The Aegean is considered an oli-

gotrophic area with biological production

significantly nutrient-limited. Low levels of surface

Chi -# pigmentation seem to confirm this feature. In

fact the trend of Chi-# is constant with values ran-

ging from 0.30 and 0.20 mg/mm 3 (Fig. 15).

As far as concerns level of precipitation, the va-

lues fluctuate between 500 and 700 mm, with a mi-

nimum of 405 mm in 2000 (Fig. 16). In the same

year the Chi-# shows a minimum value of 0.26

mg/mm 3 , and the P/D ratio declines. In this year

landings of Engraulidae suffer a decline of 4,000

tonnes, while the class Clupeidae increase landings

of 6,000 tonnes.

The level of rainfall reaches its peak in 1998 and

2002, respectively with 700 and 600 mm.

During those same years, landings of Clupeidae

show an increasing trend, while the Chi-# does not

show values relatively high.

Levant

The P/D ratio for Levant is generally in the

range 0-1 and has remained relatively constant, with

a mean of 0.80 (Fig. 13). The highest values of the

P/D index are between 1993 and 1997 (Fig. 13).

Over the same period the landings of the class Clu-

peidae have suffered an increase of 30,000 tonnes

(Fig. 14), and in fact is the category which repre-

sents the 30% of the total landings. The values of

Chi-# in the Levant area are in the range between

0.63 and 0.74 mg/mm 3 (Fig. 15).

The maximum value is recorded in 2002. In the

same year P/D index reaches the minimum value,

presumably due to an increase in landings of the

Bivalvia, Mullidae and Crustacea.

Can a simple Pelagic-Demersal ratio explain ecosystem functioning?

Ionian

33DOO

30000

29000

20000

1970

1975

1980

1985

years

1990

1995

2000

2005

tonnes

50000 —

45000

40000

Os valvia Dcwsracea OCepfialopoda □ c entraeanttiidae

BeJigraulidae O Ratfishes Bciupeiciae n '.lullicat

QspailiJae □Scorpaen-.tomies BMemiccndae Qscamlxidae

BGadidae OR-anformes □ £ n iiVi

I SOM

6000

1DOOO

iannes

50000

450DO

40000

■35000

30 000

25000

20000

15000

10000

5000

Aegean

np. ivaluia HCruslacea Q Cephalopoda BCentraranthidae

■Engrauitdae DFiattisnes Bciupedae

BSpandae □Scot»aen ulermes Q [.'rduccr.dat QScombodae

■Gadidae ciRoirttirmes nstiaite

1970

1979

1980

1985 1995 2005

1990 2000

years

tonnes

50000

Levant

DB ivalua QCmstacea Q Cephalopoda QCentracanthiOoa

■Engraulidae ORatfshes B Clupeidae DMuilidae

1670

I960

1660

2000

years

Figure 9. Pelagic/Demersal ratio of Ionian. Figure 10. Group's landings of Gulf of Ionian.

Figure 11. Pelagic/Demersal ratio of Aegean. Figure 12. Group's landings of Aegean.

Figure 13. Pelagic/Demersal ratio of Levant; Figure 14. Group's landings of Levant.

The class Clupeidae undergoes an increase in

landings of 30,000 tonnes between 1993 and 1999.

Later in 2001 show a decline of 20,000 tonnes, with

a minimum of 16,000 tonnes in 2003. Only in 2005

the landings increased another time; the Levant is

the area with the lowest average rainfall (356 mm).

In 2001 alone, the trend peak was at 400 mm.

The minimum value is recorded in 1999 (251 mm)

(Fig. 16). In the same year landings of Clupeidae in-

crease of 15,000 tonnes and the P/D index recorded

the highest value (1.26).

DISCUSSION

This study supports the idea that analyses of the

relationships between landings of pelagic and de-

mersal marine fish are useful indicators of overall

trends in fisheries; for example, since the demersal

fish stocks are generally in higher demand, a rise in

P/D ratio may be caused by a decline in demersal

stocks due to overexploitation.

Hence, a positive trend over time in the P/D

index may depend both on eutrophication and

Maria Grazia Pennino & Jose Maria Bellido

overexploitation of resources (Libralato et al.,

2004). Nutrient enrichment and overfishing have si-

milar and synergistic effects: a decline in diversity,

an initial increase in productivity of benthic/demer-

sal and pelagic food webs, then the progressive do-

minance of the production system by short-lived,

especially pelagic species (Caddy, 1993). In all the

areas the ratio between the landings of pelagic and

demersal species increased with time, a fact sho-

wing that fisheries in these areas are increasingly

relying on the smaller, short-lived fishes from the

lower part of marine food webs.

It is clear that the small pelagic fish are essen-

tial elements of marine ecosystems due to their si-

gnificant biomass at intermediate levels of the

food web, playing a considerable role in connec-

ting the lower and upper trophic levels. Small pe-

lagics are usually considered as forage fish (Tacon

& Metian, 2009).

Therefore, fluctuations in small pelagic popula-

tions can modify ecosystem structure and functio-

ning and have a major impact on the whole

ecosystem. The data show a gradual transition in

landings from long-lived, high trophic level, pisci-

vorous bottom fish toward short-lived, low trophic

level invertebrates and planktivorous pelagic fish.

High exploitation rates have been applied to demer-

sal stocks over the last few decades and particulary

in the western Mediterranean. Comparison with the

analysis of the multispecies landings shows that the

trend of the index is influenced more by the lan-

dings of Clupeidae and Engraulidae, which in fact

represent more than 60% of the total landings of the

Mediterranean area. The analysis also revealed a di-

vergent trend between species most representative

of these classes ( Sardina pilchardns and Engraulis

encrasicolus ); when the first declines, the latter in-

creases significantly and viceversa. In the last de-

cade the increase in landings of small pelagic fish

is probably compounded by increasing competition

from the fish meal market due to increasing de-

mands from the aquaculture industry for the pro-

duction of carnivore fish and shrimps for the high

value markets (Tacon & Metian, 2009).

The species considered demersals (although

some of them show a pelagic behaviour) represent

around 40% of total reported landings in the Medi-

terranean. In those areas there is an identifiable se-

ries of target species as hake ( Merluccius

merluccius ), red mullets ( Mullus spp.), blue whiting

(Micromesistius poutassou), whiting ( Merlangius

merlangus ), anglerfishes (Lophius spp.), Pagellus

spp., bogue ( Boops hoops), picarels ( Spicara spp.)

striped venus ( Chamelea gal Una), Octopus spp.,

cuttlefish {Sepia officinalis) and the red shrimp

( Aristens antennatus).

Analysis shows that the two environmental va-

riables examined influence the P/D ratio but does

not fully explain its trend. The Chi -a and rainfall le-

vels may be at least partly associated with nutrient

run-off of the areas. In particular, the associations

pointed out between the P/D ratio and the Chi -a

index, suggest that the P/D ratio may be a useful in-

direct index of the level of nutrients available.

The Mediterranean has been globally considered

as an oligotrophic sea (Margalef, 1985; Estrada,

1996; Stergiou et al., 1997). The satellite imagery

of Chi -a shows a gradual decrease in nutrient which

would result in a west to east decrease in producti-

vity, with local exceptions resulting from a north to

south productivity gradient due to incoming nutrients

Figure 15. Mean Chlorophylla-a (1970-2005). Figure 16. Mean precipitation (1970-2005).

Can a simple Pelagic-Demersal ratio explain ecosystem functioning?

from rivers as the Rhone in the Gulf of Lions, the

Po in Adriatic division and different inflows into

the Aegean. In Sardinia division nutrient inputs

from land are low and, in the south and east, Me-

diterranean nutrients have been severely depleted

during the eastward flow of surface waters from

the Straits of Gibraltar (Murdoch & Onuf, 1972;

Caddy & Oliver, 1996).

In Ionian area there is a restricted water ex-

change across the shallow sill between the Adriatic

basins, and this seems to reflect a trophodynamic re-

gime efficiently removing nutrients from the coastal

current moving southward from the northern Adria-

tic (Civitarese et al., 1998). Nutrient levels in the Le-

vant are very low and Chi -a concentrations off the

coast of Israel are between 1/2 and 1/10 of those for

the Sargasso Sea, an area of very low primary pro-

ductivity ( Azov, 1990). Also, river run-off has been

substantially reduced since blockage of Nile outflow

by the Aswan Dam (Halim et al., 1995).

The lowest P/D ratios occur in the Sardinia, Io-

nian and Levant divisions and remain below unity

for the entire time series. In these areas the fisheries

are characterised by fragmented fleets, usually com-

posed by relatively small vessels, use of a large

number of landing sites and multi-species landings.

The positive index indicates a dominance of pelagic

on demersal fish, but values less than 1 suggest that

the demersal stocks in these areas are not yet fully

exhausted. Also areas where there is a greater pre-

sence of zones of upwelling and nutrient inputs, as

Balearic and Gulf of Lions, are the ones with the

highest values, except for the Adriatic where lan-

dings of the class Bivalvia greatly influence the

trend of the P/D ratio.

ACKNOWLEDGMENTS

This research was supported by NASA's Gio-

vanni, an online data visualization and analysis tool

maintained by the Goddard Earth Sciences (GES)

Data and Information Services Center (DISC), a

part of the NASA Earth-Sun System Division.

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Biodiversity Journal, 2012, 3 (1): 79-84

Diversity and distribution of seaweeds in the Kudankulam

coastal waters, South-Eastern coast of India

Sathianeson Satheesh* & Samuel Godwin Wesley

Department of Zoology, Scott Christian College, Nagercoil - 629003, Tamil Nadu, India.

* Corresponding author, present address: Department of Marine Biology, Faculty of Marine Sciences, King Abdulaziz University,

Jeddah - 21589, Saudi Arabia; e-mail: satheesh_s2005@yahoo.co.in.

ABSTRACT The macroalgal resources of inter-tidal region of Kudankulam coastal waters are presented

in this paper. A total of 32 taxa were recorded in the Kudankulam region: 15 belonging to

Chlorophyta, 8 to Phaeophyta and 9 to Rhodophyta. Ulva fasciata Delil, Sargassum wightii

Greville, Chaetomorphci linum (O.F. Muller) Ktitzing, Hydropuntia edulis (Gmelin) Gurgel

et Fredericq, Dictyota dichotoma (Hudson) Lamouroux, Caulerpa sertulariodes (Gmelin)

Howe, Acanthophora muscoides (Linnaeus) Bory de Saint- Vincent and Ulva compressa Lin-

naeus were the commonly occurring seaweeds in the rocky shores and other submerged hard

surfaces. The seasonal abundance of seaweeds was studied by submerging wooden test panels

in the coastal waters. The seaweed abundance on test panels was high during pre-monsoon

and monsoon periods and low in post-monsoon season. In general, an updated checklist and

distribution of seaweeds from Kudankulam region of Southeast coast of India is described.

KEY WORDS macroalgae; benthic community; coastal biodiversity; rocky shores; Indian Ocean.

Received 23.02.2012; accepted 08.03.2012; printed 30.03.2012

INTRODUCTION

Seaweeds are considered as ecologically and

biologically important component in the marine

ecosystems. Seaweeds make a substantial contribu-

tion to marine primary production and provide ha-

bitat for nearshore benthic communities (Mann,

1973; Williams & Smith, 2007).

Seaweeds are key space occupiers of rocky sho-

res and interact with other organisms and hence

play a key role in overall coastal biodiversity. They

are found on rocks in the intertidal zone as a giant

underwater forest. It was estimated that about 200

seaweed species support an international economy

in primarily phycocolloid (algins, agars, and carra-

geenans) and food products valued at over billions

of U.S. S 6.2 (Zemke- White & Ohno, 1999).

Seaweeds grow abundantly along the Indian

coastline particularly in rocky shore regions; rich

seaweed beds occur around Visakhapatnam in the

eastern coast, Mahabalipuram, Gulf of Mannar, Ti-

ruchendur, Tuticorin and Kerala in the southern

coast; Veraval and Gulf of Kutch in the western

coast; Andaman and Nicobar Islands and Lakshad-

weep (Umamaheswara Rao, 1967; Silva et al.,

1996; Sahoo, 2001).

The seaweed resources are also abundant around

Mumbai, Ratnagiri, Goa, Karwar, Varkala, Vizhin-

jam and Pulicat in Tamil Nadu and Chilka in Orissa.

About 841 taxa of marine algae were found in both

inter-tidal and deep water regions of the Indian

coast (Oza & Zaidi, 2001).

Seaweeds are under threat in developing coun-

tries, where they are being disturbed by a variety of

human activities. Increasing concern on destruction

of seaweed resources and alterations in the diversity

of various life forms makes it necessary the studies

on the taxonomy and species diversity for a better

management of marine algae. Although systematic

studies on marine algae and their distribution are

Sathianeson Satheesh & Samuel Godwin Wesley

known from different coastal parts of India, not

much published informations are available about

the seaweeds of Kudankulam coastal waters, hence

the distribution and diversity of seaweed species of

Kudankulam coast is presented in this paper. Such

a study in this region can be of great importance due

to the emerging mega Nuclear Power Project.

Ecological survey of water bodies around a

power plant is an important endeavour both from

the environmental and the operational point of view.

The release of warm water to the receiving water

body is of concern due to the long and short-term

impact on the flora and fauna.

MATERIALS AND METHODS

The investigation was carried out at Kudanku-

lam (8° 9’ 5” N and 77° 39’ 59” E), Gulf of Mannar

in the southeast coast of India (Fig. 1). The study

area is situated on the distal end of Gulf of Mannar

Biosphere Reserve. The rocky shore of Kudanku-

lam inhabits an astonishing biodiversity, represen-

ting nearly almost all the invertebrate phyla and

urochordates. Hard rocky bottom of this area grea-

tly supports the algal diversity and provide suitable

shelter and feeding ground for grazers. Seasons at

Kudankulam may be classified into pre-monsoon

(June- September), monsoon (October-January), and

post-monsoon (February-May).

Field surveys were undertaken to the selected

sampling stations of the Kudankulam region over a

period of three years from 2003 to 2006. The algal

samples were collected in every season during the

study period by detaching a portion from the sea-

weed bed, kept in polythene bags with fresh seawa-

ter, transported to the laboratory and fixed in 4%

formaldeyde for further studies.

The seaweeds were identified using the taxono-

mic keys provided by Umamaheswara Rao (1987),

Desikachary et al. (1990, 1998) and Krishnamurthy

(1999), and the nomenclature was updated using

Appeltans etal. (2012).

The seasonal distribution of seaweeds was studied

by submerging test panels for a period of one year

from June 2003 to May 2004. Test panels made

from teak wood with a size oflOx 10x2 cm were

vertically placed in a suitably designed wooden raft

with grooves in such a way so as to keep a 10 cm

distance between panels.

The raft with panels (in replicate, n = 6) was su-

spended at 2 m depth in the coastal waters using flo-

ats and sinkers. Panels were suspended during the

first week of a season and retrieved during the last

week of that season so as to keep the panels for 1 10

days in coastal waters. Each panel was studied for

the seaweed species composition and biomass. The

total and the differential biomass (wet weight) of

the seaweeds were estimated after carefully scrap-

ping them from the panels and weighing them.

Figure 1. Map sho-

wing the study area:

Kudankulam, Gulf

of Mannar in the

southeast coast of

India.

■■■I

KERALA

TAMIL NADU

BAY

BENGAL

PALK STRAIT

GULF

MANNAR

SRI

LANKA

KAN YAKLI MARI • KUDANKULAM

Diversity and distribution of seaweeds in the Kudankulam coastal waters, South-Eastern coast of India

RESULTS

A total of 32 seaweed taxa were collected

from the Kudankulam region (Table 1). The Chlo-

rophyta prevailed with 15 taxa followed by Rho-

dophyta (9 taxa) and Phaeophyta (8 taxa).

Ulva fasciata Delile, Sargassum wightii Gre-

ville, Chaetomorpha linum (O.F.Miiller) Kiitzing,

Gracilaria ednlis (Gmelin) Gurgel et Fredericq,

Dictyota dichotoma (Hudson) Lamouroux, Cau-

lerpa sertulariodes (Gmelin) Howe, Acanthophora

muscoides (Linnaeus) Bory de Saint-Vincent and

Ulva compressa Linnaeus were the commonly

found seaweeds in the rocky shores and other sub-

merged hard surfaces.

Ulva fasciata is the common green alga inha-

biting the rocky shores of this region. During the

monsoon season (October-January), Ulva fasciata

forms thick mats covering the entire rocky sub-

stratum (Fig. 2).

CHLOROPHYTA

Stoechospermum polypodioides (Lamouroux)

Agardh, 1848

Order Ulvales

Family Ulvaceae

Order Ectocarpales

Ulva compressa Linnaeus, 1753

Family Scytosiphonaceae

Ulva intestinal is L i n n ae u s , 1753

Colpomenia sinuosa (Mertens ex Roth) Derbes

Ulva fasciata Delile, 1813

et Sober, 1851

Ulva lactuca Linnaeus, 1753

Ulva reticulata Forsskal, 1775

Order Fucales

Order Cladophorales

Family Sargassaceae

Sargassum ilicifolium (Turner) Agardh, 1 820

Family Cladophoraceae

Sargassum wightii Greville, 1848

Chaetomorpha antennina (Bory de Saint-Vincent)

Kiitzing , 1 847

RHODOPHYTA

Chaetomorpha linoides Kiitzing, 1 847

Chaetomorpha linum (O.F. Muller) Kiitzing, 1845

Order Gracilariales

Order Bryopsidales

Family Gracilariaceae

Hydropuntia edulis (Gmelin) Gurgel et Frdricq, 2004

Family Caulerpaceae

Gracilaria corticata (Agardh) Agardh, 1852

Caulerpa peltata Lamouroux, 1 809

Gracilaria debit is (Forsskal) Borgesen, 1932

Caulerpa scalpelliformis (Brown ex Turner)

Agardh, 1817

Order Gigartinales

Caulerpa sertularioides (Gmelin) Howe, 1 905

Family Solieriaceae

Caulerpa racemosa (Forsskal) Agardh ,1873

Sarconema filiforme (Sonder) Kylin, 1932

Family Halimedaceae

Family Cystocloniaceae

Halimeda macroloba Decaisne, 1 84 1

Hypnea valentiae (Turner) Montagne, 1841

Halimeda opuntia (Linnaeus) Lamouroux, 1816

Order Siphonocladales

Family Phyllophoraceae

Ahnfeltiopsis densa (J. Agardh) Silva et De Cew,1992

Family Valoniaceae

Valoniopsis pachynema (Martens) Borgesen, 1 934

Order Ceramiales

PHAEOPHYTA

Family Rhodomelaceae

Acanthophora muscoides (Linnaeus) Bory de

Order Dictyotales

Saint-Vincent, 1828

Palisandra perforata (Bory de Saint-Vincent)

Family Dictyotaceae

Nam, 2007

Dictyota dichotoma (Hudson) Lamouroux, 1 809

Padina pavonica (Linnaeus) Thivy, 1 960

Order Corallinales

Padinia antillarum (Kiitzing) Picone, 1886

Family Corallinaceae

Padina gymnospora (Kiitzing) Sonder, 1871

Amphiroa sp.

Table 1. Checklist of seaweed taxa found in Kudankulam coastal waters.

Sathianeson Satheesh & Samuel Godwin Wesley

Figure 2. Intertidal rocky reef covered by Ulva fasciata in

Kudankulam coastal waters.

Chaetomorpha linum , and Caulerpa sertulario-

des are the other dominant green seaweeds taxa ob-

served during this period of study.

The brown seaweeds (Phaeophyta) are represen-

ted by 8 taxa and Sargassum wightii is the domi-

nant one. Dictyota dichotoma and Padina antillarum

(Ktitzing) Picone are also abundantly observed on

the intertidal rocky reefs. A rich growth of Sargassum

sp.pl. was observed during pre-monsoon and monsoon

months (Fig. 3). Sargassum sp. pi. was harvested du-

ring October-December period by the local people.

Colpomenia sinuosa (Mertens ex Roth) Derbes et

Sober was commonly observed on the artificial sub-

strata submerged in the seawater.

Rhodophyta of the Kudankulam coastal waters

consisted of 9 taxa. Gracilaria corticata (Ag.)

Agardh, Hydropuntia edulis (Gmelin) Gurgel et

Fredericq, and Acanthophora muscoides (Linnaeus)

Bory de Saint- Vincent were the dominant red sea-

weeds observed during this study period. Amphiroa

sp. and Hypnea valentiae (Turner) Montagne were

also commonly observed on the rocks. Gracilaria

sp.pl. were abundantly observed during May-Octo-

ber period. Acanthophora muscoides and Hypnea

valentiae were abundant during November-January

period on the rocky shores.

The test panels immersed during June 2003 and

examined at the end of September 2003 (pre-mon-

soon) showed a total algal biomass value of

13.14±2.9 g/dm 2 (Table 2). The macro-algal com-

munity of the panels submerged during this period

was dominated by Ulva fasciata (5.3±1.7 g/dm 2 )

and Ulva compressa (3.18±0.9 g/dm 2 ) (Table 2).

Hydropuntia edulis (2.5± 0.78 g/dm 2 ) was also ob-

served as one of the dominant groups in this panel

Figure 3. Growth of Ulva fasciata , Caulerpa racemosa, Scagassum

wightii and Gracilaria corticata in the rocky shores of stydy area.

series. Sargassum wightii , Padina antillarum and

Hypnea valentiae were also observed. The panels

exposed during the monsoon season (October-Ja-

nuary) showed a biomass value of 19±2.3 g/dm 2 ,

dominated by Ulva compressa (4.7±0.9 g/dm 2 ) and

Acanthophora muscoides (3.8±0.71 g/dm 2 ).

The biomass of Ulva fasciata Delil on this panel

series was 1.92±0.72 g/dm 2 , while Hypnea valen-

tiae recorded a very low biomass value of 0.6±0.09

g/dm 2 . Sargassum wightii was also observed on the

panels with a biomass of 0.81 ±0.12 g/dm 2 .

The panels submerged during the post-monsoon

season (February-May 2004) showed a seaweed bio-

mass of 6.3±1.2 g/dm 2 . Hydropuntia edulis , showed

a biomass value of 1.87±0.087 g/dm 2 followed by

Acanthophora muscoides (1.71±0.48 g/dm 2 ). The

biomass of Ulva compressa on post-monsoon panels

was 1.6±0.2 g/dm 2 (Table 2). Ulva fasciata and Hyp-

nea valentiae were also observed on the panels sub-

merged during post-monsoon season.

DISCUSSION

Studies on the diversity and distribution of sea-

weeds in Indian waters were carried out by several

authors (Untawale et al., 1989; Kalimuthu et al.,

1995; Jayachandran & Ramaswamy 1997; Kaliape-

rumal & Kalimuthu, 1997; Stella Roslin et al.,

1997; Selvaraj & Selvaraj, 1997; Mohammed et

al., 1999; James et al., 2004; Krekar, 2004; Rath

& Adhikary, 2006). Southeast coast of India is a

unique marine habitat characterized by a high

biodiversity. Results of the present study indicate

the occurrence of 32 seaweed taxa in the Kudanku-

Diversity and distribution of seaweeds in the Kudankulam coastal waters, South-Eastern coast of India

Pre-monsoon season

Monsoon season

Post-monsoon season

Total algal biomass

13.14±2.90

19.00±2.30

6.30± 1.20

Ulva fasciata

5.30±1.70

1.92±0.72

0.70±0.04

Ulva compressa

3.18±0.90

4.70±0.90

1.60±0.20

Hydropuntia edulis

2.50± 0.78

4.70±0.90

1.87±0.09

Acanthophora muscoides

—

3.80±0.71

1.71±0.48

Sargassum wightii

—

0.81±0.12

—

Hypnea valentiae

—

0.60±0.090

—

Table 2. Biomass of seaweeds settled on the wooden test panels submerged in pre-monsoon, monsoon and

post-monsoon season period at Kudankulam coast. The wet biomass values are expressed as g/dm 2 . Mis-

sing values ( — ) indicates very low biomass values in that season.

lam coastal waters; most of the seaweeds such as

Sargassum wightii, Ulva fasciata , Gracilaria cor-

ticata and Chaetomorpha linum , are abundantly

observed on the rocks during the pre-monsoon

(June- September) and monsoon months (October-

January). The richness of seaweed resources is due

to the intertidal rocky reefs available in the Kudan-

kulam region. The seaweed flora observed in the

present study is similar to that reported from the ne-

arby Tiruchendur coast (Chennubhotla et ah, 1991).

Marine ecologists have a long history of using

artificial substrate and habitats to test hypothesis

about sessile plants and animals (Osman, 1977; Su-

therland & Karlson, 1977). In this study, settlement

panels were used to analyse the seasonal distribu-

tion of macroalgal communities. The seaweed bio-

mass on test panels was high during pre-monsoon

and monsoon seasons. In an earlier study (Satheesh

& Wesley, 2007), we have reported that Gracilaria

sp., Enteromorpha sp., and Ulva sp., showed dense

settlement during pre-monsoon and post monsoon

months on test panels.

The observed pattern of seasonal distribution is

likely to be related to the life history of the alga,

particularly the dispersal abilities of its spores. The

supply from macroalgal propagule may influence

the abundance of algae in littoral habitats (Worm et

al., 2001). As the test panels provide limited space

for the settlement of marine organisms including

seaweeds, the seasonal biomass of only a few spe-

cies could be observed in this study.

Gradual rise in the anthropogenic influence, im-

pact of the possible thermal discharge from the

emerging nuclear power station and the indiscrimi-

nate collection of algae (mostly Sargassum sp.) may

be the cause of concern for the biodiversity of algal

species at Kudankulam coast. Both frond bleaching

and cell plasmolysis of algae were observed in ther-

mal effluent discharge areas (North, 1969; Lobban

et al., 1985).

These negative effects may reduce the survival

and growth of seaweeds, resulting in extensive re-

ductions in the number of species of marine algae

(Wood &Zieman, 1969).

The present study could be useful as new base-

line record for future biomonitoring studies in this

coast. Further systematic studies on the seaweed re-

sources may provide useful data for the conserva-

tion of marine algal resources in this region.

ACKNOWLEDGMENTS

We thank Ministry of Earth Sciences, Govt, of

India for providing financial assistance through

DOD-OSTC.

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Biodiversity Journal, 2012, 3 (1): 85-90

Carabus ( Eurycarabus ) faminii Dejean, 1826 (Coleoptera,

Carabidae) in Sicily: distribution and taxonomic considera-

tions with description of a new taxon

Ivan Rapuzzi 1 & Ignazio Sparacio 2

’Via Cialla n. 47, 33040 Prepotto (UD), Italy; e-mail: info@ronchidicialla.it.

2 Via E. Notarbartolo n. 54 int. 13, 90145 Palermo, Italy; e-mail: isparacio@inwind.it.

ABSTRACT The study of large series from many localities from all over Sicily of Carabus (Eurycarabus)

faminii Dejean, 1 826 confirmed that in Sicily live two different subspecies. After examination

of the holotypus of C. faminii we found that C. faminii sabellai Sparacio, 2007 is a synonym

of the nominal form widespread in south-east part of Sicily. The western subspecies is de-

scribed in this paper.

KEY WORDS Carabidae; Carabus faminii ; new subspecies; new synonym; Sicily.

Received 24.01.2012; accepted 02.03.2012; printed 30.03.2012

INTRODUCTION

Two subspecies of Carabus (Eurycarabus) fa-

minii Dejean, 1826 are reported to Sicily: the no-

minal subspecies, widespread in the western

provinces (Turin et al., 1993, 2003; Taglianti Vigna,

1993; Lorenz, 1998; Brezina, 1999; Bousquet et al.,

2003; Vigna Taglianti et al., 2002, Deuve, 2004;

Sparacio, 2007) and the ssp. sabellai Sparacio, 2007

reported to the south-eastern ones (Erei Mountains).

Two other subspecies are widespread in the Ma-

ghreb: ssp. lucasi Gaubil, 1849 and ssp. numidicus

Castelnau, 1835 (Casale et al., 1982; Culot, 1985;

Ghiretti, 1996).

As part of a larger study on Carabus faminii in

Sicily we examined the holotypus of the species de-

scribed by Dejean in 1826 observing that it is pre-

cisely identified with the recently described

subspecies from Erei Mountains. Taking into ac-

count this consideration the form collected since

XIX Century in the western provinces of Palermo,

Trapani and West Agrigento, would result without

a name and is described in the present paper. Mo-

reover we also review the distribution of the two

Carabus faminii populations in Sicily in the light of

some recent findings.

ACRONYMS. The materials used for this study

are deposited in the following Museums and private

collections: Vittorio Aliquo, Palermo, Italy (CA);

Marcello Arnone, Palermo, Italy (CMA); Michele

Bellavista, Palermo, Italy (CB); Museum National

d’Histoire Naturelle, Paris (MNHN); Museo di Sto-

ria Naturale di Niscemi, Caltanissetta, Italy (CMN);

Ivan Rapuzzi, Prepotto, Udine, Italy (CR); Marcello

Romano, Capaci, Palermo, Italy (CMR); Ignazio

Sparacio, Palermo, Italy (CS); Roberto Torrisi,

Motta Sant’ Anastasia, Catania, Italy (CT).

Carabus (Eurycarabus) faminii faminii Dejean, 1826

Examined material. Holotypus (MNHN);

Monti Erei (Enna): Monte Rossomanno, 4 males

and 3 females (CS; CR); Sughereta di Niscemi

(Caltanissetta), 1 male (CMN); Licodia Eubea (Ca-

tania), Bosco Vaito (CT); Agrigento, 4 males and 3

females (CR; CS); Agrigento, Valle dei Templi, 1

female (CMA); Piazza Armerina, Aidone (Enna),

1 male and 2 females (CR).

Holotypus of C. faminii Dejean, 1826. The ho-

lotypus (Figs. 1, 4) is a pinned specimen, length of

21.5 mm, with the following original labels: red

Ivan Rapuzzi & Ignazio Sparacio

label with the written "HOLOTYPE"; label with the

written EC42; label with the symbol label with

the written “Ex Musaeo Chaudoir”; label with the

written “Carabus famini Dejean”.

Body black, polished, lateral margins of pro-

notum and elytra slightly red-purple. Head of nor-

mal shape, smooth front, neck faintly punctulate

and rugulose; convex eyes, frontal furrows narrow,

extended to the anterior border of eyes, clypeus

small, labrum bilobed; antennae thin and short,

surpassing with three segments the base of elytra.

Apical segment of palpi strongly widened, the ma-

xillary ones are axe-shaped.

Pronotum transverse, sides regularly rounded,

maximum width in the anterior third, rounded

front margins, hind angles of pronotum rounded

and large, thin and complete median sulcus, sur-

face finely punctured.

Elytra short, oval, very convex; rough surface

with irregular sculpture; primary intervals forming

rows of short tubercles interrupted by foveae; se-

condary and tertiary intervals confused in a large,

smooth and flat area. Legs short and robust, femurs

wrinkles on both surfaces.

Variability. The examined specimens from

South-Eastern Sicily are morphologically related to

the holotype of C. faminii Dejean, 1826 described

above, size ranges from 20 mm to 23 mm, the late-

ral margins of elytra and pronotum are sligthly co-

lored, completely absent in some specimens.

The aedeagus of a specimen from Rossomanno

Mount (it was not possible to extract the aedeagus

from the holotype) was described and figured by

Sparacio (Sparacio, 2007).

Females are more convex with rounded elytra,

length ranges from 21 mm to 23 mm.

Biology and Distribution. C. faminii faminii

was collected under stones and debris of Pinus and

Eucalyptus reforestation and oak bushes.

The nominal subspecies is distributed in south-

eastern provinces (Fig. 7). In the map are reported

the following localities: Licodia Eubea (Torrisi,

2010), Agrigento, Pachino (Magistretti, 1962, 1965)

in addition to Erei Mountains (Rossomanno Mount

and Aidone) and Sughereta di Niscemi.

Comparative notes. The holotypus of C. fa-

minii Dejean, 1826 is identified to the spp. sabellai

(see Sparacio, 2007). Under this consideration it is

necessary to establish the following synonymy:

Carabus (Eurycarabus) faminii faminii

Dejean, 1826

= Carabus (Eurycarabus) faminii sabellai

Sparacio, 2007 n. syn.

Carabus (Eurycarabus) faminii romanoi n.ssp.

Examined material. Holotypus male, Godrano

(PA), 25.XI.1978, legit I. Sparacio (CR); Paratypi:

Bosco Ficuzza (PA), loc. Valle Maria, 7.1.1973, 1

male (CMR); Triscina (TP), 23. IV. 1973, 1 male and

1 female (CMR); Mazara del Vallo (TP),

17. XI. 1974, 1 female (CMR); Piana degli Albanesi

(PA), Monte Maganoce, 4.1.1974, 1 female (CMR);

idem, 1 l.XII. 1974, 1 male and 1 female (CMR);

idem, 11.1.1976, 1 female (CMR); Godrano (PA),

3.1.1975, 1 male and 1 female (CMR); idem,

11.1.1976, 1 male (CMR); idem, XL 1976, 1 male

and 2 females (CMR); idem, 3.1.1979, 1 male and

1 female (CMR); idem, 23. XI. 1979, 1 male and 2

females (CMR); idem, 16.1.1980, 1 female (CMR);

idem, 23.1.1980, 1 male and 2 females (CMR);

idem, 1. II. 1981, 2 males (CMR); idem, 30.XI.1980,

1 male and 3 females (CMR); idem, 4.1.1989, 1

male and 2 females (CMR); idem, 20. XII. 1992, 1

female (CMR); Lago Rubino (TP), 6.II.1980, 2

males (CMR); Godrano (PA), 25.XI.1978, 1 male

and 1 female (CA); idem, 2 l.X. 1979, 2 males (CA);

idem, 9. XII. 1979, 3 males (CA); idem, 16.1.1980,

2 females (CA); idem, 20.1.1980, 1 male (CA);

idem, 2.III.1980, 1 female (CA); idem, 2. III. 1980,

1 male (CA); idem, 10.1.1993, 1 female (CA);

idem, 12. X. 1996, 2 females (CA); idem,

23.11.2003, 1 female (CA); Campobello di Mazara

(TP), Cave di Cusa, 3 l.XII. 1989, 1 male and 1 fe-

male (CA); Bosco Ficuzza (PA), 28.1.1989, 2 males

(CA); Foce Fiume Belice (TP), 17.IV. 1988, 1 fe-

male (CA); idem, 21. XI. 1992, 1 male and 1 female

(CA); idem, 16.XII.1992, 1 male (CA); Lago Scan-

zano (PA), 20.III.2005, 1 male and 1 female (CA);

Godrano (PA), 25. XI. 1978, 1 male and 1 female

(Coll. IS); idem, 30.XI.1996, 2 males and 1 female

(CS); Foce Fiume Belice (TP), 10.VI.1981, 2 fe-

males (CS); idem, 17. IV. 1993, 2 males (CS); Bosco

Ficuzza (PA), 28.1.1989, 2 males and 2 females

(CS); idem, 31.XII.1989, 1 female (CS); idem,

28. XI. 1993, 2 males (CS); idem, 5.XII.1993, 1

male and 1 female (CS); idem, 30. XI. 1996, 1 male

(CS); idem, 13. XI. 2001, 1 male and 4 females

Carabus (E.) faminii (Coleoptera, Carabidae) in Sicily: distribution and taxonomic considerations with description of a new taxon 87

Figure 1. C. faminii faminii holotypus. Figure 2. C. faminii romanoi n. ssp. holotypus. Figure 3. C. faminii romanoi n. ssp.

paratype female, Sicilia, Bosco Ficuzza (PA), XIF2010, F Rapuzzi & L. Caldon leg. (CR), lenght 26 mm.

(CS); Campobello di Mazara (TP), Cave di Cusa,

31. XII. 1988, 1 male and 2 females (CS); Bosco Fi-

cuzza (PA), 8.II.2009, 2 males and 2 females (CS);

Bosco Ficuzza (PA) 8.XII.1978, 1 male and 1 fe-

male (CB); idem, 23.XI.1979, 1 male (CB); idem,

27.XII.2008, 1 male and 1 female (CB); Piana Al-

banesi (PA), 1.1975, 1 female (CR); Bosco Ficuzza

(PA), XII. 1980, 1 male (CR); idem, 11.11.1989, 1

female (CR); idem, 6.XII.1992, 1 male (CR); idem,

XII. 2009, 1 male and 1 female (CR); idem,

XII. 20 10, 7 males and 8 females (CR); Corleone

(PA), 30.XI.1988, 1 female (CR); Foce Fiume Be-

lice (TP), 21. XI. 1992, 1 female (CR); Campobello

di Mazara (TP), 20.X.1985, 1 female (CR); Go-

drano (PA), XII. 2009, 7 males and 5 females (CR);

idem, XI. 20 10, 3 males and 8 females (CR); Go-

drano, 25. XI. 1978, 1 males (CMA); idem,

21.X.1979, 2 males (CMA); idem, 9.XII.1979, 3

males (CMA); idem, 16.1.1980, 2 males (CMA);

idem, 20.1.1980, 1 male (CMA); idem, 25.XI.1992,

1 male (CMA); idem, 10.1.1993, 1 female (CMA);

idem, 12.X.1996, 2 females (CMA); idem,

23.11.2003, 1 female (CMA); Bosco Ficuzza,

28.1. 1989, 2 males (CMA); Campobello di Mazara,

Cave di Cusa, 31. XII. 1988, 1 male and 1 female

(CMA); Foce F. Belice, 17.IV. 1988, 1 female

(CMA); idem, 21. XI. 1992, 1 male and 1 female

(CMA); idem, 16. XII. 1992, 1 male (CMA); Bosco

Ficuzza, Lago Scanzano, 20. III. 2005, 1 male and 1

female (CMA).

Description of Holotypus male. Length in-

cluding mandibles: 24 mm, maximum width of

elytra: 10 mm. Body black, the margins of prono-

tum and of the edge of elytra with purple. Shiny

above (Fig. 2).

Head of normal size, surface with punctures

more evident at the base and sides, front and disc

almost perfectly smooth; supra-antennary ridge

deep and split. Eyes very salient, perfectly hemi-

spherical. Short antennae extending with 2.5 anten-

nomeres beyond pronotal base. Apical segment of

palpi strongly widened, axe-shaped; labial palp bi-

setose. Pronotum very transverse as wide as elytra,

slightly convex, very wide at base, maximum width

at the middle; sides regularly rounded and bent up-

wards at the basal angles. Hind angles of pronotum

Ivan Rapuzzi & Ignazio Sparacio

very long and widely rounded; basal depression

broad and deep. Pronotal disc slightly rough, sides

and base with irregular punctures.

Elytra oval elongated, convex, maximum width

beyond the half, shoulders angulate, sides regularly

rounded. Heterodynamic elytral sculpture: primary in-

tervals in form of short catenate rows, interrupted by

foveae with metallic lustre; secondary and tertiary in-

tervals fused in a single intermediate zone raised as or

more than primary intervals. Legs short of normal size.

Aedeagus (Figs. 5, 6) characteristic of the spe-

cies but a little more developed and with shorter

apex than C.faminii faminii.

Variability. The length of the body ranges

from 23 mm to 28 mm. The color of the margins

of the pronotum and the edge of the elytra is more

frequently red-violet or purple, rarely green or gol-

den green. Labial palp are disetose or trisetose.

Shape of pronotum and elytral sculpture are very

little variable.

Figure 4. C.faminii faminii holotypus, head and pronotum.

Figure 5. C.faminii romanoi n. ssp. aedeagus frontal view.

Figure 6. idem, lateral view.

Etimology. We are honoured to dedicate this

new subspecies to our friend Marcello Romano

(Capaci, Palermo, Italy) entomologist and connois-

seur of Sicilian biodiversity.

Biology and Distribution. C.faminii romanoi

n.ssp. was found under stones and debris in various

types of environments: i.e. dune system, stony

ground, undergrowth of woodlands or natural refo-

restation, even degraded, generally down to 800 m

above sea level.

The species survives with small population very

isolated and endangered by the loss of original ve-

getation due to urbanisation and agriculture (au-

thors' observations, Ragusa, 1883; Aliquo, 1970;

Aliquo & Castelli, 1991). According to Palumbo

(1892) the species was common in Selinunte area.

In Sicily C. faminii romanoi n. ssp. is known only

from the Western provinces: Palermo, Trapani and

Western part of Agrigento (Fig. 7). It is reported

for several localities.

C. faminii romanoi n.ssp. (C. faminii sensu

Auctores) is reported from: Monte Pellegrino, Pa-

lermo (Ghiliani, 1839), Termini Imerese (Calcara,

1842), Palermo, Agrigento (Rottenberg, 1870-71),

Favorita near Palermo (Ragusa, 1874), Santa

Ninfa and Prizzi (De Stefani & Riggio, 1882), Se-

gesta, Castelvetrano and Favorita near Palermo

(Ragusa, 1883), Castelvetrano, Selinunte (Pa-

lumbo, 1890, 1892), Palermo, Prizzi and Castel-

vetrano (Vitale, 1912; Luigioni, 1929), Palermo:

Passo di Rigano (Luigioni & Tirelli, 1912), Pa-

lermo, Castelvetrano (Magistretti, 1962), Marsala

(Magistretti, 1965), Monte Pellegrino (Aliquo,

1970), Piana degli Albanesi, Bosco Ficuzza and

Rocca Busambra (Riggio & Massa, 1974), provin-

cie di Agrigento, Trapani and Palermo (Casale et

al., 1982; Du Chatenet, 1986, 2005; Sparacio,

1995), contrada Tonnarella and borgata Costiera

(Mazara del Vallo), Capo Granitola, Cave di Cusa,

Partanna (Aliquo & Castelli, 1991), Prizzi, Castel-

vetrano, Salemi (Facchini & Baviera, 2004),

Agrigento, Realmonte (Casale et al., 2005).

Comparative notes. C. faminii romanoi differs

from C.faminii faminii for the following characters:

larger body size; wider and livelier coloration on la-

teral margins of elytra and pronotum; stronger head;

eyes more prominent; antennae shorter and stron-

ger; larger pronotum with a wider base; longer and

less convex elytra; elytral intervals strongly convex,

raised and regular; stronger legs.

Carabus (E.) faminii (Coleoptera, Carabidae) in Sicily: distribution and taxonomic considerations with description of a new taxon 89

Figure 7. Geographic distribution of C. faminii in Sicily: circles=C. faminii faminii; squares =C. faminii romanoi n. ssp.

CONCLUSION

In a recent paper one of the authors (Sparacio,

2007) correctly pointed out that C. faminii in Sicily

includes two different subspecies.

The study of new C. faminii populations and the

examination of the holotypus, described generically

of “Sicily”, allowed us to better understand the

spread of this species in Sicily. The populations in-

habiting the south-east of Sicily (the provinces of

Enna, Caltanissetta, Siracusa, Ragusa, southern Ca-

tania and the eastern part of Agrigento) belong to the

nominative subspecies, whereas the western popu-

lations (Province of Trapani, Palermo and Agrigento

West) are attributed to C. faminii romanoi n. ssp.

ACKNOWLEDGMENTS

We wish to thank Dr. Thierry Deuve and Dr.

Azadeh Taghavian (Museum National d'Histoire

Naturelle, Paris, France) for the loan of typus of C.

faminii Dejean, 1826.

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fauna coleotterologica della regione sicula (Col. Ci-

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Calcara P., 1842. Cenno Topografico dei dintorni di

Termini. Tipografia e Legatoria Roberti. Palermo,

31 pp.

Ivan Rapuzzi & Ignazio Sparacio

Casale A., Sturani M. & Vigna Taglianti A., 1982. Co-

leoptera Carabidae I. Fauna d’ltalia, 18. Calderini,

Bologna, 499 pp.

Casale A., Vigna Taglianti A., Brandmayr P. & Colom-

betta G., 2005. Insecta Coleoptera Carabidae (Cara-

bini, Cychrini, Trachini, Abacetini, Stomini,

Pterostichini). In: Ruffo S., Stoch F. (eds), Checklist e

distribuzione della fauna italiana. Memorie Museo ci-

vico di Storia naturale di Verona, 16: 159-163.

Culot J., 1985. Memento des faunes carabologiques du

monde. Systematique du dr. Breuning. Bruxelles,

126 pp.

Dejean P, 1826. Species general des Coleopteres de la

Collection de M. le Baron Dejean, I-V. Crenot, Paris.

II: 62.

De Stefani Perez T. & Riggio G., 1882. Catalogo dei Co-

leotteri siciliani raccolti ed ordinati da Teodosio De

Stefani Perez e Giuseppe Riggio ed esistenti nella

collezione entomologica del Museo Zoologico-zoo-

tomico della R. Universita di Palermo. Tipografia

Giornale di Sicilia, Palermo, 27 pp.

Deuve T., 2004. Illustrated Catalogue of the Genus Ca-

rabus of the World (Coleoptera, Carabidae). Pensoft

Publishers, Sofia-Moscow, 461 pp.

Du Chatenet G., 1986. Guide des Coleopteres d’ Europe.

Delachaux & Niestle, Paris, 480 pp.

Du Chatenet G., 2005. Coleopteres d’ Europe. Carabes,

Carabiques et Dytiques. Volume I Adephaga. N.A.P.

Editions, Verrieres le Buisson, 640 pp.

Facchini S. & Baviera C., 2004. II contributo alia revi-

sione della collezione coleotterologica di Francesco

Vitale: Coleoptera Carabidae. II Naturalista siciliano,

28: 1005-1050.

Ghiliani V., 1 839. Insetti di Sicilia determinati dal Sig. F.

Ghiliani nel suo viaggio in quest’isola anno 1839.

Atti della Accademia Gioenia di Scienze Naturali in

Catania, 19: 19.

Ghiretti D., 1996. Photographic Catalogue of the genus

Carabus. Conte Ed. Lecce, 404 pp.

Lorenz W., 1998. Systematic list of the extant ground

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Luigioni P, 1929. 1 Coleotteri d’ltalia. Catalogo sinoni-

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Accademia delle Scienze di Roma, 13: 1-1160.

Luigioni P. & Tirelli A., 1912. Una settimana in Sicilia.

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Magistretti M., 1962. Cicindelidi e Carabidi della Re-

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Carabidi di Sicilia ed il loro significato biogeogra-

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cademia Gioenia di Scienze Naturali in Catania,

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Turin H., Casale A., Kryzhanovskij O.L., Makarov K.V.

& Penev L.D., 1993. Check List and Atlas of the

genus Carabus Linnaeus in Europe (Coleoptera, Ca-

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Biodiversity Journal, 2012, 3 (1): 91-92

Lurifax vitreus Waren & Bouchet, 200 1 (Gastropoda, Orbite-

stellidae), a new record for deep waters of the Tuscan

Archipelago (Tyrrhenian Sea, Italy)

Francesco Giusti 1 & Carlo Sbrana 2 *

1 Via S. Giuseppe n. 24, 53100 Viareggio (LU), Italy.

2 Via Sette Santi n. 1, 57126 Livorno, Italy.

*Corrisponding author, e-mail: carletto.nicchi@tiscali.it.

ABSTRACT We record a finding of one perfect adult, one young specimen, and other two no-well conser-

ved adults of Lurifax vitreus Waren & Bouchet, 2001 (Gastropoda, Orbitestellidae) coming

from deep waters of Tuscan Archipelago.

KEY WORDS Orbitestellidae; Lurifax vitreus ; Hydrotel vent; Cold Seeps.

Received 24.01.2012; accepted 23.02.2012; printed 30.03.2012

INTRODUCTION

Lurifax vitreus Waren & Bouchet, 2001 was de-

scribed as a species belonging to the fauna of the

resurgence of hot and cold deep sea waters.

The several specimens found came from a very

wide distribution area, ranging from the Atlantic

ocean ridge hydrothermal vents to the cool "seeps"

off New Zealand, with a bathymetry between 850

and 1800 meters (Waren & Bouchet, 2001).

The "cold seep" and "hydrotermal vent" are

structures present on the ocean seabeds, supporting

biomes completely independent from solar energy.

They form as a result of volcanic activity on the

ocean floor: the water seeps through cracks in the

crust becoming super-heated in contact with

magma, being able to reach temperatures of 400 ° C,

and then goes back getting into the ocean floor

(Peres & Picard, 1964).

In addition to the discoveries that led to the de-

scription of Lurifax vitreus , we include the fin-

dings of a specimen from the coast of Lazio (-600

Terracina: Ardovini & Cossignani (1999, sub An-

timargarita sp.) and another adult of the same re-

gion of Lazio (Smiriglio & Mariottini, 2002)

probably coming from the facies CB at a depth of

450-600 meters.

MATERIALS AND METHODS

The shells reported by this note come from the

cleaning of commercial fishing nets of trawlers ope-

rating in waters off Tuscany in September 2003.

The debris was collected at a depth of 470 m.

Examined Material.

Family Orbitestellidae Iredale, 1917

Genus Lurifax Waren & Bouchet, 2001

Lurifax vitreus Waren & Bouchet, 2001

Tuscan Archipelago, Capraia Island, 1 adult

shell devoid of soft parts, 1 juvenile shell devoid

of soft parts, 2 remnants of adult shells.

DISCUSSION AND CONCLUSIONS

In addition to what already reported by the au-

thors on the occurrence of Lurifax vitreus in the

"Hydrotermal vents and cold seeps" facies and in

the White Coral facies (reported as facies CB), we

report the discovery of the species in question for

the biocenosis of bathyal sludge (reported as bio-

Francesco Giusti & Carlo Sbrana

Figure 1. Lurifax vitreus , adult specimen, height 4 mm.

Figure 2. Lurifax vitreus, juvenile specimen, height 2.5 mm.

cenosis VB); this assertion is further reflected in

the discovery, in the same debris, of species ty-

pical of the biocenosis "VB", viz. Addisonia ex-

centrica (Tiberi, 1855), Aporrhais serresianus

(Michaud, 1828), Dentalium agile (M. Sars in

GO Sars, 1872), Benthonella tenella (Jeffreys,

1869), Abra longicallus (Chess, 1835).

ACKNOWLEDGMENTS

We thank our friend Stefano Bartolini for his pa-

tience and superb skill demonstrated in the execu-

tion of the photos accompanying this note, Mrs.

Gika Zamosteanu for the passion in the search of

the debris that led to the discovery of the specimens,

and Mr. Zaccaria Frimi for providing us with the

debris. Finally we express our gratitude to prof.

Enzo Campani (Malacological Livornese group) for

critical reading of the manuscript.

REFERENCES

Ardovini R. & Cossignani T., 1999. Atlante delle con-

chiglie di profondita del Mediterraneo. L’ informa-

tore Piceno Ed., Ancona, 111 pp.

Peres J.M. & Picard 1., 1964. Nouveau manuel de

Bionomie Bentique de la Mer Mediterranee. Re-

cuil des Travaux de la Station Marine d’Endoume,

31: 1-137.

Waren A. & Bouchet P, 2001 . Gastropoda and Monopla-

cophora from hydrotermal vents and seeps; new taxa

and records. The Veliger, 44: 116-23 1 .

Smiriglio C. & Mariottini P, 2002. Lurifax vitreus

Waren & Bouchet, 2001 (Gastropoda, Orbitestelli-

dae), first report from Western Mediterranean Sea.

Bollettino Malacologico, 38: 45-47.

Biodiversity Journal, 2012, 3 (1): 93-95

A new species of genus Laubuca Bleeker, I860 cyprinid

fish from Bangladesh (Cypriniformes, Cyprinidae)

Sitthi Kulabtong 1 , Siriwan Suksri 2 & Chirachai Nonpayom 3

’Department of Fishery Management, Faculty of Fisheries, Kasetsart University, Bangkok, Thailand 10900; e-mail: kulab-

tong2011@gmail.com.

Reference Collection Room, Inland Fisheries Resources Research and Development Institute, Department of Fisheries, Thailand

10900; e-mail: Siriwan.suksri@gmail.com.

3 534/26 Soi Phaholyothin 58 Phaholyothin Rd. Sai Mai, Bangkok, Thailand; e-mail: sornl33@hotmail.com.

ABSTRACT A new species of cyprinid fish (Cypriniformes, Cyprinidae), Laubuca brahmaputraensis n.

sp. from Brahmaputra River, Bangladesh, is described. This species is distinguished from

other species of genus Laubuca Bleeker, 1 860 by the combination of the following characters:

lateral line scales comprising 31-32 + 1-2 scales, transverse line scales of 146- 147/ 1 / 214 -

314 scales, body depth ranging from 25. 1 to 29.3 % Standard length (SL), pelvic fin not rea-

ching beyond the anus, anal fin with 3 unbranched rays and 1914-2014 branched rays, black

blotch above the pectoral fin base and no tubercles on lower jaw.

KEY WORDS Laubuca ; Cyprinidae; Brahmaputra River; Bangladesh; new species.

Received 02.03.2012; accepted 20.03.2012; printed 30.03.2012

INTRODUCTION

Freshwater fishes genus Laubuca Bleeker,

1860 (Pisces, Cypriniformes, Cyprinidae) has

been reported for Indian subcontinent and Indo-

Australian archipelago (Hamilton, 1822; Weber

& de Beaufort, 1916; Smith, 1931; Menon, 1952;

Silas, 1958; Deraniyagala, 1960; Pethiyagoda et

al., 2008).

Currently the genus Laubuca comprises eight

valid species: L. caeruleostigmata Smith, 1931

from Thailand; L. laubuca (Hamilton, 1822) wi-

dely distributed in Indian subcontinent and Indo-

Australian archipelago; L. dadyburjori Menon,

1952 and L. fasciata Silas, 1958 from India; L.

lankensis Deraniyagala, 1960 from Sri Lanka; and

L. insularis, L. ruhuna and L. varuna described

by Pethiyagoda et al. (2008) from Sri Lanka.

In Bangladesh, Ataur Rahman (2003) reported

that L. laubuca is the only species of genus Laubuca

found in the country area.

In October 1995, the inland aquarium fish

collector who caught all the specimens of Lau-

buca employed in this study (collection site:

Brahmaputra River, Bangladesh), sent these spe-

cimens to the Inland Fisheries Resources Rese-

arch and Development Institute, Department of

Fisheries, Thailand [NIFI] under the name L.

laubuca [NIFI 2799].

In 2012 after having reviewed all the speci-

mens sent by Mr. Kittipong Jaruthanin, we con-

cluded that these fish are significantly different

not only from specimens belonging to L. laubuca

as described by Ataur Rahman (2003 ) from Ban-

gladesh, but also from all other species of Lau-

buca hitherto known, by the combination of the

following characters: lateral line scales, tran-

sverse line scales, body depth, caudal peduncle

depth, fin rays and the absence of tubercles on

lower jaw.

Hence, the population collected from Brahma-

putra River is described herein as a new species.

S. Kulabtong, S. Suksri & C. Nonpayom

Laubuca brahmaputraensis n. sp.

Examined material. Holotypus, NIFI 4532: Brah-

maputra River, Bangladesh, 12. X. 1995, legit Kit-

tipong Jaruthani, (Fig. 1); Paratypi, NIFI 2799: 2

specimens, same data of holotypus.

Description of holotypus (sexual external charac-

ters cannot be specified). L. brahmaputraensis n.

sp. is slender, body depth is 26.1%SF. The fish is

very compress, body width is 8.7 %SF. Scales in

lateral series are medium to large, lateral line scales

include 31 + 1-2 scales, transverse line scales on

body comprises 46 - V 2 II 1 / 24 -34 scales and pre-

dorsal scales are 16. Head length (HF) is 24.1 %SF,

head depth (HD) is more than half of body depth

(BD) and head length (66.6 %BD or 72.2 %HF or

17.4 %SF). The eye is large, eye diameter is

36.1 %HF (50.0 %HD or 8.7 %SF). Post orbital

length is 38.9 %HF (10.7 %SF), snout length is

short, with 18.1 %HF (4.3 %SF) and interorbital

width is 5 1 .4 % HF ( 12.4 % SF) longer than postor-

bital width (44.4 %HF or 10.7 %SF).

Dorsal fin origin is posterior behind anal fin ori-

gin, predorsal fin length is 66.9 %SF, prepectoral

fin length is 31.4 %SF, prepelvic fin length is

48.2 %SF and preanal fin length is 66.9 %SF. Cau-

dal peduncle depth is 9.8 %SF. Pectoral fin is long

but not reaching beyond the anus, the pectoral fin

length is 31.4 %SF and 9 branched fin rays.

Pelvic fin is short not reaching beyond anus, the

pelvic fin length is 20.1 %SF and 5 branched fin

rays. Anal fin base is longer than dorsal fin base,

the anal fin base length is 28.4 %SF, dorsal fin with

3 unbranched rays and 8 branched rays and anal fin

with 3 unbranched rays and 19 A branched rays. The

dorsal fin base length is 12.7 %SF.

Variability. 30.7-33.9 mm SF. Variation of male

and female are unknown.

Etymology, from Brahmaputra River, Bangladesh,

where this species was collected.

Distribution. This species is known only from

Brahmaputra River, Bangladesh.

Comparative notes. L. brahmaputraensis n. sp. is

distinguished from other species of genus Laubuca

by the combination of the following characters:

lateral line scales complete, with 31-32 + 1-2 scales;

transverse line scales on body showing 46 - V 2 H 1 /

2 V 2 - 34 scales; body is slender, body depth is

25.1-29.3 %SF; caudal peduncle depth is 8.9-

9.8 %SF; anal fin with 3 unbranched rays and 1 9 4-

20 V 2 branched rays; pelvic fin is short (43.2-

83.3 %HF) not reaching beyond the anus; a black

blotch above the pectoral fin base; lower jaw smo-

oth, lacking tubercles on skin.

Particularly, L. brahmaputraensis n. sp. is

clearly different from L. caeruleostigmata of Thai-

land in many characters: body depth is 3. 4-4.0 times

SF (in L. caeruleostigmata is 2.25), lateral line sca-

les includes 31-32 scales (vs 34-35 scales in L. cae-

ruleostigmata).

Moreover, L. brahmaputraensis n.sp. has one

black blotch above the pectoral fin base (vs. 4-5

dark vertical stripes above pectoral fin base on sides

of body in L. caeruleostigmata) (Smith, 1931;

Smith, 1945; Silas, 1958).

L. brahmaputraensis n.sp. is different from

other species of genus Laubuca of Sri Fanka by the

combination of the following characters: lower jaw

smooth, lacking tubercles on skin (vs. some densely

tubercles in L. insularis and L. lankensis ); pelvic fin

is short not reaching beyond the anus (vs. a long

pelvic fin reaching beyond posterior anal fin origin

in L. insularis ); body depth is 25.1-29.3 %SF (vs.

32.8-34.6 %SF in L. ruhuna, 27.9-32.4 %SF in

L. varuna , 27.2-29.8 %SF in L. lankensis , and 26.0-

28.8 %SF in L. insularis ); anal fin is 1 9 1/2-20 A

branched rays (vs. 1514 -171/2 in L. varuna , 17-18/2

in L. ruhuna , 174 -1914 in L. insularis , and 164-

20/2 in L. lankensis ) (Pethiyagoda et al., 2008).

L. brahmaputraensis n.sp. is distinguished from L.

dadyburjori of India by a complete lateral line sca-

les (vs. an incomplete one in L. dadyburjori).

L. dadyburjori has a black stripe on lateral se-

ries, with 2-5 black circular spots on it, the stripe is

extend from the anterior of eye to caudal peduncle

whereas L. brahmaputraensis n. sp. does not show

any black stripe along the body (Menon, 1952;

Silas, 1958). L. brahmaputraensis n. sp. is distin-

guished from L.fasciata of India by short pelvic fin

not reaching beyond the anus (vs. a long pelvic fin

reaching beyond the anus in L.fasciata), lower jaw

smooth (vs. scattered tubercles in L. fasciata), a

black blotch above the pectoral fin base (vs. a black

longitudinal stripe in L. fasciata)', anal fin shows

19/2 - 20/2 branched rays (vs. 14 '4 - I6/2 in L. fa-

sciata) (Pethiyagoda et al., 2008; Silas, 1958).

A new species of genus Laubuca Bleeker, 1 860, cyprinid fish from Bangladesh (Cypriniformes, Cyprinidae) 95

Figure 1. Laubuca brahmaputraensis n. sp. from Brahmaputra River, Bangladesh.

L. brahmaputraensis n. sp. is distinguished from

L. laubuca of Bangladesh by body depth which is

3. 4-4.0 times SL (vs. 2. 7-3. 3 times SL or 3. 5-4. 2

times total length, TL, in L. laubuca ), lateral line

scales comprises 31-32 scales (vs. 34-36 in L. lau-

buca ), branched anal fin rays include 19 1 /2-20 1 /2

branched rays (vs. 18-19 in L. laubuca ), predorsal

scales are 16-17 (vs. 20-21 in L. laubuca) (Ataur

Rahman, 2003).

ACKNOWLEDGEMENTS

The authors are grateful to reviewers for revie-

wing this manuscript. A special thank to Mr. Kitti-

pong Jaruthanin, who collected all the specimens of

L. brahmaputraensis n. sp. employed in this study.

We wish to thank Dr. Rohan Pethiyagoda,

Wildlife Heritage Trust in Sri Lanka and Dr. Sorin

Stefanut, Institute of Biology Bucharest, Romanian

Academy, Romania for providing the original de-

scription of many species of genus Laubuca.

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