BIODIVERSITY JOURNAL

2014,5 (4): 445-558

Quaternly scientific journal

edited by Edizioni Danaus,

viaV. Di Marco 43, 90143 Palermo, Italy

www.biodiversityjournal.com

biodiversityjournal@gmail.com

Official authorization no. 40 (28. 1 2.20 1 0)

ISSN 2039-0394 (Print Edition)

ISSN 2039-0408 (Online Edition)

Nature Reserve of Vendicari (Italy, Sicily),

landscape (photo by G. Iuvara).

Pendolino, Remiz pendulums (Linnaeus,

1758) (Seidlitz, 1 896) on the nest (photo by

G. 1 uvara). Cover: photo by Iuvara.

The Vendicari Nature Reserve (Italy, Sicily). The Oriented Natural Reserve (O.N.R.) “Oasi

faunistica di Vendicari”, in the territory of Noto (Sicily, Italy), UNESCO World Heritage City, was

established in March 1 4 ,h 1 984. Despite its small size (total of 1 335.62 acres), within the reserve there is

a concentration of environments hardly observable in other parts of Sicily. In particular, there have

been identified as habitats of interest to the European Community: Intermittently flowing

Mediterranean rivers of the Paspalo-Agrostidion (Habitat code 3290); Vegetated sea cliffs of the

Mediterranean coasts with endemic Limonium spp. (code 1240); Endemic phryganas of the

Euphorbio-Verbascion (code 5430); Thermo-Mediterranean and pre-desert scrubs (code 5330);

embryonic shifting dunes (code 2110); Shifting dunes along the shoreline with Ammophila arenaria

(white dunes) (code 2120); Coastal dunes with Juniperus spp. (code 2250, priority habitat); Coastal

lagoons (code 1150, priority habitat); Mediterranean and thermo-Atlantic halophilous scrubs

(Sarcocornetiea fruticosi ) (code 1420); Salicornia and other annuals colonizing mud and sand

(code 1310); Mediterranean salt meadows ( Juncetalia maritimi ) (code 1 4 1 0). A highly rich biodiversity

was therefore already reported for the reserve: data are contained in a compendium published in 20 10

[Petralia A. ( a cum di) 2010. L'area protetta di Vendicari. ©Ente Fauna Siciliana, Noto, Italy

(www.entefaunasiciliana.it)]. The plant list includes 486 species (48.4% therophytes, 22.0%

hemicryptophytes, 13.7% geophytes, 6.2% chamaephytes, 6.0% phanerophytes, 2.7% nano-

phanerophytes, 0.8% hydrophytes). There are 7 species of mammals, 25 1 bird species (79 of which are

included in the Directive 2009/147/EEC), 4 species of Amphibians, and 10 of Reptiles; moreover,

after decades of absence, in 20 1 3 and 20 1 4, Caretta caretta returned to the reserve for nesting. 221 are

the species of Macrolepidoptera present (24.0% of the species known for Sicily, 10.82% for Italy).

Among orthopteroids there are 32 species (including the Ensifer Brachytrupes megacephalus, species

of Community interest). As concerns the fauna of the marshes of the reserve, 22 species of molluscs, 3

of crustaceans, 2 of bristle worms (Polychaetes) and 7 of fish have been reported. More generally,

further faunistic data may be derived from a larger survey [Pi l a to et al., 2007. La fauna della regione

iblea. In "L'uomo negli Iblei" (a cura di A. Petr alia). ©Ente Fauna Siciliana, Noto, Italy

(www.entefaunasiciliana.it)] that lists 2914 species and subspecies referring to the entire iblean area

including Vendicari; of course the knowledge of fauna is periodically refreshed by new acquisitions

such as the recent discovery of the presence of the relevant beetle Buprestis cupressi (Buprestidae).

Finally, a project for the establishment of the Protected Marine Area of Vendicari aims to extend

protection also to the sea off the reserve, with its seabed equally rich in biodiversity.

Alfredo Petralia. Ente Fauna Siciliana Onlus, Noto, Italy; e-mail: alfredo.petralia@yahoo.it

Biodiversity Journal, 2014, 5 (4): 447-452

Global biodiversity gain is concurrent with declining popula

tion sizes

John C. Briggs

Oregon State University, Department of Fisheries and Wildlife, Corvallis, OR 97333, U.S.A; e-mail: clingfishes@yahoo.com

Current address: 2320 Guerneville Rd., Santa Rosa, CA 95403, U.S.A.

ABSTRACT Many authorities believe that the world’s foremost conservation problem is biodiversity loss

caused by the extinctions of thousands of species per year. Estimates of huge losses are based

on indirect evidence such as the amount of habitat destroyed, pollution, or overexploitation.

But, we now have documented records of species extinctions that provide direct instead of

indirect information about diversity loss. By using extinction records for well-known animal

groups plus surrogate data, I show there is no evidence for an unusually high rate of extinction,

a mass extinction is not yet underway, and there are indications of a continued biodiversity

gain. On the other hand, there is ample evidence to demonstrate the persistence of numerous

small populations that are the remnants of once widespread and productive species. These

populations represent an extinction debt that will be paid unless they are rescued through

present day conservation activity. They constitute the world’s true biodiversity problem.

KEY WORDS biodiversity gain; biodiversity loss; conservation; extinction debt; speciation.

Received 22.08.2014; accepted 02.11.2014; printed 30.12.2014

INTRODUCTION

As new portions of terrestrial wilderness con-

tinue to be utilized or modified by human activity,

wildlife has less territory, individual species are

crowded into smaller spaces, and many of them lose

population size until their existence becomes pre-

carious. Overexploitation by hunting and trapping

directly affect populations of birds and mammals.

In the oceans, there is loss of natural habitat over

large areas of sea bottom through the action of com-

mercial trawlers, and by the degradation of coral

reefs by human use and global warming. Along

shorelines, construction and pollution have im-

pacted much of the shallow marine habitat. The di-

rect effect of overfishing has resulted in hundreds

of species being reduced to remnants of their origi-

nal population sizes. These kinds of impacts are as-

sumed to have contributed to a global biodiversity

loss of several thousand species each year, an

apparent crisis that has been called the world’s

greatest conservation problem.

The reactions of conservation societies and gov-

ernment agencies to the foregoing problems have

tended in two directions: (1) trying to stem the per-

ceived loss of biodiversity due to species extinction,

and (2) paying attention to the plight of species that

are threatened by extinction. This brings up the

question, should we continue to concentrate on

overall biodiversity loss or should we devote more

resources to the needs of individual species? One

might say that both conservation approaches are im-

448

John C. Briggs

portant, but is this really true? Let us first consider

biodiversity loss.

BIODIVERSITY LOSS?

Global and local losses of biodiversity have

been a major focus of conservation action for 40

years. Anguish over the apparent, continuing ex-

tinction of large numbers of species has been ex-

pressed in numerous scientific papers, newspaper

and magazine articles, and on the internet. As

E.O. Wilson (1993) has noted, biodiversity, as a

term and a concept, has been a remarkable event

in recent cultural history. It was born as “BioDi-

versity” during the National Forum on BioDiver-

sity held in Washington, D.C., in September, 1986.

Prior to that time, Norman Myer’s (1979) book

had caused considerable excitement when it pre-

dicted the extinction of one million species be-

tween 1975 and 2000.

By the 1990s, numerous books and articles had

described biodiversity loss in terms of thousands of

species that disappeared each year. Among the most

notable, were A1 Gore’s (1992) book which esti-

mated that 40,000 species were disappearing each

year, and E.O. Wilson’s (1993) prediction of about

27,000 rain forest extinctions per year. Other huge

species loss estimations (Briggs, 2014) were soon

followed by declarations that the Earth had started

to undergo its sixth great mass extinction (Ceballos

et al., 2010; Kolbert, 2014).

In retrospect, biodiversity loss became rapidly

established as a scientific revelation and there

were few questions about sources of the informa-

tion. But, such concepts or theories need to be sup-

ported by facts and, in this case, the facts were few

and the theory was so captivating that it survived

even with little support for 40 years. The begin-

ning can be traced back to an influential work on

island biogeography by MacArthur & Wilson

(1967). The authors found that on small islands,

species diversity was determined by island size,

i.e., the larger the size, the greater the diversity.

Also, they found a constant turnover whereby the

numbers of invading species were balanced by the

native species that were lost. In subsequent years,

more research was done on islands and other small

habitats and these two discoveries were generally

substantiated.

The relationship between area size and species

diversity became important to many ecologists who

were convinced that, if a given amount of habitat

was destroyed, a certain number of species must be

lost. That idea was converted to a “rule of thumb”

which stated that when a habitat is reduced to one

tenth its original size, the number of species even-

tually drops to one half (Wilson, 1993). This species-

area rule (SAR) become well accepted and began

to be applied to locations ranging from small

islands to large continental areas. However, prohib-

itive difficulties became apparent when the SAR

was applied to areas larger than small, isolated

islands. As noted by Whittaker et al. (2001), the

problem with such data is one of scale. When small

scale data are applied to very large scale areas, the

results are apt to become meaningless. Furthermore,

there has been constructive criticism about the use-

fulness of the SAR (He & Hubbell, 2011). To avoid

the SAR problem, as well as to depend on direct

instead of theoretical data, it is preferable to utilize

information from documented extinctions. More

recently, various statistical methods have been used

to manipulate the theoretical extinction data in order

to prove large annual losses (for example Pimm et

al., 2014), but they unnecessarily complicate what

is actually a simple problem. By utilizing informa-

tion from recorded extinctions, together with data

from well-known surrogate taxa, I show that rate of

recent extinctions has been very low.

Documented extinctions

Until recent years, there had not been sufficient

data on species extinctions to provide an overall

estimate of biodiversity loss over the past 500 years

or more. But now, the availability of more data,

based on contemporary and fossil extinctions, has

made possible a new analysis. It is important to note

that previous estimates were made primarily on life

in the terrestrial and freshwater environments.

Obviously, global predictions should also depend

on information from the sea which covers about

71% of the Earth’s surface. There is one significant

difference between the data from land and sea. In

the first instance, there have been, in the early years

of island explorations by humans, thousands of

extinctions of endemic species that were confined

to very small spaces. But in the second case, recorded

extinctions have been remarkably few.

Global biodiversity gain is concurrent with declining population sizes

449

Although attention has been called to marine

biodiversity losses by Worm et al. (2006), that arti-

cle was referring to decreases in population size

rather than species extinction. The Holocene began

about 12,000 years ago and a total of 20 marine

extinctions were recorded by Dulvy et al. (2009).

When the losses of the 20 marine species (4 mam-

mals, 8 birds, 4 molluscs, 3 fishes, 1 alga) are com-

pared to a total marine diversity of about 2.21

million eukaryotic species (Mora et al., 2011), the

rate of extinction becomes vanishingly small.

Although it is often assumed that invasive species

are responsible for native extinctions, none of the

20 marine extinctions have been due to competition

from exotic invaders (Briggs, 2007).

In fact, there is now good evidence that invasive

species function to increase rather than decrease

biodiversity. In locations where large numbers of

exotic species are being introduced, such as the

eastern Mediterranean Sea (Galil, 2007) and in

many harbors and estuaries (Briggs, 2012), the

invaders are accommodated by the native species

resulting in local biodiversity increases. Informa-

tion from Pliocene invasions demonstrates that a

large fraction of invaders eventually speciate

(Vermeij, 1991; 2005) thus adding to global bio

diversity. It has been concluded that in the marine

environment, invader species are a dynamic diver-

sity-creation force with a circumglobal influence

(Briggs & Bowen, 2013).

In the terrestrial environment, the birds and

mammals are the best known vertebrates and their

extinction rates have been recorded. The records

and geographical locations of the extinctions, based

on evidence in the IUCN Red List and the CREO

List at the American Museum of Natural History,

have been analyzed by Loehle & Eschenbach

(2012). Extinctions during the past 500 years

demonstrate an enormous difference between

islands and continents. On all continents, only three

mammals are recorded as having gone extinct. The

remaining mammal extinctions (58 or 95%) took

place on islands (Australia, due to its history of iso-

lation, was classified as an island). Of 128 extinct

bird species, 122 (95.3%) were island extinctions

and only six were on continents. It has been ob-

served that well-known surrogate taxa can be used

as biodiversity indicators (Caro & O’ Doherty,

1999). If we use the birds and mammals as surro-

gates for all the vertebrates, this suggests that

extinction rates among the vertebrate animals of the

world’s continents have been very low. Another

discovery (Loehle & Eschenbach, 2012) was that

none of the bird and mammal extinctions were

known to have occurred solely because of habitat

reduction. For many years, habitat reduction, espe-

cially tropical deforestation, had been regarded as

the primary cause of species loss. A recent study of

the vertebrate species in the Brazilian Amazon by

Weam et al. (2012) demonstrated that extinctions

have been minimal (1%) and that 80% of the losses

predicted by habitat decline were yet to come.

For invertebrates, the Zoological Society of

London has published the world’s first study of

global invertebrate biodiversity (Collen et al.,

2012). This report, produced in conjunction with

the IUCN and its Species Survival Commission,

concluded that about 80% of the world’s species

were invertebrates and about 20% of them were

threatened with extinction. Of the world’s terrestrial

invertebrates, about 90% are insects. This suggests

if dependable information on insect extinction rates

were available, it might yield an approximate rate

for terrestrial invertebrates as a whole. Three orders

of insects: butterflies, tiger beetles, and Odonata

(dragonflies and damselflies), have been studied to

the extent that almost all the species are well

known. The world total of butterfly species is about

17,280 (Shields, 1989). Although three species are

often listed as extinct (two in South Africa and one

in the USA), the records are doubtful. Ehrlich

(1995) found that there was no documented extinc-

tion of a continental butterfly species anywhere in

the world. No island butterfly species has been

recorded to be extinct.

There are about 2,300 species of tiger beetles

(Pearson, 2001) and, although several are listed as

endangered, none has become extinct. For the

Odonata, a random sample of 1,500 of the 5,680

described species was assessed (Clausnitzer et al.,

2009). Ten percent were found to be threatened but

none of them had become extinct. In fact, there are

only two documented extinctions, one from Maui

in the Hawaiian Islands and the other from St.

Helena, an isolated island in the South Atlantic. If

the three insect orders can constitute a surrogate

group for all insects, and if the lack of extinction

among the insects (two out of 25,260) is indicative

of the terrestrial invertebrates, the extinction rate

has been exceedingly low.

450

John C. Briggs

The foregoing indications of very low extinction

rates may be compared to data that show continuing

gains in species diversity.

Biodiversity gains

While global losses were evidently minimal dur-

ing the past 400 to 500 years, there is evidence that

concurrent gains have taken place. As noted for the

marine environment, invasive species add to local

biodiversity and many of them eventually speciate,

thus increasing global diversity. Other paths to spe-

ciation have also become apparent. Molecular re-

search has revealed numerous cases of rapid

adaptive divergence resulting in ecological specia-

tion. Such cases have been demonstrated in plants,

invertebrates, and vertebrates (Hendry et al., 2007).

Specific examples have been reported in mammals

(Rowe et al., 2011), echinoderms (Puritz et al.,

2012), and plants (Foxe et al., 2009). Within the

past few centuries, species diversity has increased

on oceanic islands and in many continental regions;

furthermore, no general decreases in diversity have

been known to occur at regional scales (Sax &

Gaines, 2003).

In fact, human introductions for agricultural and

ornamental purposes, along with natural invasions,

have produced substantial gains in continental plant

biodiversity (Ellis et al., 2012). These positive

indications of biodiversity increase indicate that the

Earth is still gaining biodiversity, just as it has been

for the past 65 million years (MacLeod, 2013).

DISCUSSION

It is now possible to make a realistic assessment

of recent global biodiversity trends without having

to depend on estimates of habitat destruction,

species invasions or other abstract and possibly sub-

jective factors. For the past 500 years, there have

been few documented extinctions in the oceans or

on the continents, with the exceptions of some

restricted freshwater habitats. In using these data, I

do not imply an absence of unobserved extinctions

among groups of lesser known organisms. Even

when estimates of such extinctions are included, it

has been found that contemporary extinctions could

not have been as high as generally predicted

(Costello et al., 2013), and that less than 1% of all

organisms could have become extinct within the

past 400 years (Stork, 2010). Global projections of

biodiversity loss have generally included estimates

of extinction due to invasive species (McGeoch et

al., 2010). But, detailed studies have found no evi-

dence that invasive species are implicated in the

extinction of continental natives (Gurevitch &

Padilla, 2004; Davis, 2009).

The losses of endemic species on islands and in

freshwater lakes, while regrettable, took place on

very small spots on the Earth’s surface and their ex-

tinctions had little effect on the ecology of the main-

land biotas. Those endemics are generally

short-lived and tend to appear and disappear along

with their habitats (Whittaker et al., 2008). Of

course, there are the exceptions of a few ancient

islands and lakes that demonstrate the effects of

evolution and extinction over long time periods.

Why do small places lose species to invaders while

mainland habitats do not? The demise of almost all

island/lake endemics has been due to humans and

species they introduced (Blackburn et al., 2004).

Extinctions resulting from natural (non-human)

invaders have seldom been recorded. Despite the

early losses of endemic species, oceanic islands

have shown biodiversity gains in recent years (Sax

& Gaines, 2003).

The world’s greatest conservation problem is

exemplified by the thousands of species that were

once widespread but are now represented only by

very small populations. They are the remnants of

species that were almost destroyed by human over-

exploitation, habitat destruction and pollution.

These populations are threatened because they have

suffered genetic loss due to their reduced size,

inbreeding, and depensation (Allee effect). Genetic

loss reduces the ability to respond to environmental

change such as continued global warming. Further-

more, small populations are often confined to re-

stricted habitats, from which they would be unable

to migrate in response to climatic change. Formerly

abundant species that now exist in small numbers

are considered to be evidence of an extinction debt,

one that will be paid when environmental change

proves too difficult for them to adapt (Kuussaari et

al., 2009). If governments and conservation soci-

eties could be convinced to spend less effort on myth-

i-cal global biodiversity loss, and more on the needs

of species that are at risk, the world would have a

consolidated conservation goal that could produce

Global biodiversity gain is concurrent with declining population sizes

451

better results. The conservation plan, initiated by

the World Wildlife Fund, and supported by the Zoo-

logical Society of London, the Global Footprint

Network, and the European Space Agency, is

promising. Their Living Planet Index (2012) pro-

vided information on the status of 9,014 vertebrate

populations belonging to 2,688 species. The Index

reported that the population sizes had undergone a

28% global loss since 1970; the greatest decline

was in the tropics where the loss was 60%. The

Living Planet Index needs to be expanded to cover

invertebrates and plants.

CONCLUSIONS

In regard to the question about the need for con-

servation measures to be applied to global biodiver-

sity loss or to the precarious condition of species

that have been reduced to small populations, there

is no longer cause to be concerned about biodiver-

sity loss because it is apparently not true. For the

past 40 years, estimates of global loss, based on the

extinction of thousands of species per year, have

been a primary concern of ecologists and conserva-

tionists. These estimates, mainly due to belief in the

utility of the SAR, are shown to be erroneous and

the SAR is found to be applicable only to small

islands, lakes, and other restricted habitats. On the

other hand, we now have substantial evidence of

gains in global species diversity. This should permit

conservation societies, government entities, and

interested individuals to concentrate on species that

are at risk on the continents and in the oceans, as

well as species confined to islands and smaller

habitats. Species at risk comprise an extinction debt

that will be paid unless they are rescued before

global warming or other environmental change

takes their toll. A conservation emphasis on criti-

cally endangered species does not mean that

projects to preserve rain forests, coral reefs, and

other natural habitats should be abandoned.

On the contrary, such high diversity areas are

sources of biodiversity and are significant in an

evolutionary sense. Flowever, each species that is

at risk must be considered in view of its own con-

servation problems that are often unrelated to

habitat area. The current (2014) IUCN Red List

identifies 4,286 species that are critically endan-

gered and likely to become extinct due to global

warming or the inherent risks of small population

size. We need to be aware that many of those

species can be rescued prior to the anticipated rise

in extinctions.

ACKNOWLEDGEMENTS

I wish to thank M.A. Davis, E.A. Hanni, C.

Mora, and D.F. Sax for their help in reading and

improving the manuscript.

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Biodiversity Journal, 2014, 5 (4): 453-458

New records of sea stars (Echinodermata Asteroidea) from

Malaysia with notes on their association with seagrass beds

Woo Sau Pinn 1 *, Amelia Ng Phei Fang 2 , Norhanis Mohd Razalli 2 , Nithiyaa Nilamani 2 , Teh Chiew Peng 2 ,

ZulfigarYasin 2 , Tan Shau Hwai 2 &Toshihiko Fujita 3

'Department of Biological Science, Graduate School of Science, The University of Tokyo 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-

0033 Japan.

2 Universiti Sains Malaysia, School of Biological Sciences, Marine Science Lab, 11800 Minden, Penang, Malaysia

department of Zoology, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, Ibaraki 305-0005 Japan

Corresponding author, e-mail: abe_woo@hotmail.com

ABSTRACT A survey of sea stars (Echinodermata Asteroidea) was done on a seagrass habitat at the south-

ern coast of Peninsular Malaysia. A total of five species of sea stars from four families (Luidi-

idae, Archasteridae, Goniasteridae and Oreasteridae) and two orders (Paxillosida and

Valvatida) were observed where three of the species were first records for Malaysia. The sea

stars do not exhibit specific preference to the species of seagrass as substrate, but they were

more frequently found in the area of seagrass that have low canopy heights.

KEY WORDS Biodiversity; seagrass; sea stars; Straits of Malacca.

Received 15.09.2014; accepted 02.12.2014; printed 30.12.2014

INTRODUCTION

The knowledge of diversity and distribution of

asteroids in Malaysia is very limited. There are only

three accounts of sea stars (Echinodermata Aster-

oidea) previously reported in Malaysia where all of

the surveys are mainly done in shallow coral reefs

(George & George, 1987; Zulfigar et al., 2008; Sim

et al., 2009).

Seagrass beds are another important marine

environment in Malaysian waters. There are a

total of 14 species of seagrasses recorded (Bujang

et al., 2006), and apart from the common inshore

lagoons, seagrass meadows are also found in the

offshore islands with fringing reefs (Bujangand &

Zakaria, 2003). This study presents the first

record of asteroids associated with a seagrass bed

in Malaysia.

MATERIAL AND METHODS

A survey of sea stars was done in the seagrass

bed of Merambong shoal (N 1°19 , 58.01”; E 103°

36’ 08.30”) southern tip of Peninsular Malaysia

(Fig. 1). Wandering transect was done by walking at

seagrass bed when it was exposed extensively

during the best low spring tide of the year from 25th

to 27th of May 2013 (07:30-09:30 h). The exposure

of the seagrass bed only allowed a window of two

hours of sampling per day for three days. Asteroids

were collected using labelled sampling bags and

brought to the laboratory for further identifications.

Asteroid specimens were anaesthetized using sea-

water mixed with menthol crystals. Colour photo-

graphs of live specimens were taken before being

fixed using 70% ethanol. All specimens were

preserved by drying and deposited in Marine

454

Woo Sau Pinn et alii

Science Lab, Universiti Sains Malaysia, Penang,

Malaysia (MSL/MS).

RESULTS AND DISCUSSION

Five species of asteroids from four families and

two orders were found in the Merambong shoal sea-

grass bed: Luidia maculata of the family Luidiidae

(Fig. 9, voucher specimen MSL/MS/AST001),

Archaster typicus of Archasteridae (Figs. 2, 3 -

voucher specimen MSL/MS/AST002), Stellaster

equestris from the family Goniasteridae (Figs. 4, 5

- voucher specimen MSL/MS/AST003) and two

from family Oreasteridae: Protoreaster nodosus

(Fig. 8, voucher speciemen MSL/MS/AST004),

Goniodiscaster scaber (Figs. 6, 7 - voucher speci-

men MSL/MS/AST005).

All species of asteroids occurring in Malaysian

waters are listed in Table 1 . Previous records were

based on George & George (1987), Zulfigar et al.

(2008), and Sim et al. (2009). The areas surveyed

and covered by these three previous publications

were larger and centered at coral reefs which con-

tribute to the higher number of species of asteroids.

Zulfigar et al. (2008) and Sim et al. (2009) listed

asteroids found in shallow reefs throughout the

entire coast of Malaysia and George & George

(1987) at the lagoons and coral reefs of east coast

of Sabah. All five species were widely distributed

in Indo-West Pacific region (Clark & Rowe, 1971).

Besides their wide distribution, the present records

of Stellaster equestris , Luidia maculata and Go-

niodiscaster scaber were new state records in

Malaysian waters filling the gap in the species

distribution along the transition waters of Straits of

Malacca and South China Sea, consequently in-

creasing the total number of asteroids recorded in

Malaysian waters to 34 species. The recurring

species were Archaster typicus and Protoreaster no-

dosus , which had been both recorded in the central

of South China Sea and the East Coast of Sabah.

Protoreaster nodosus is known to prefer sub-

strates of seagrass and sand (Zulfigar et al., 2008)

even though it has been rarely found on corals and

rocks (Bos et al., 2008). Archaster typicus is found

in a wide range of sediment types which include

seagrass beds (Huang et al., 2006), and Mukai et al.

(1986) noted that the distribution of A. typicus was

independent of the specific grain size. Other species

S. equestris , L. maculata and G. scaber were com-

monly reported throughout the Indo-Pacific region

but were not specifically mentioned to be associated

with the seagrass except L. maculata on the sea-

grass of the western Arabian Gulf (Price, 1981).

Seagrass plays many important ecological func-

tions in the marine environment such as food,

1.38

Malaysia

/ 1.37

Straits of Johor

Tanjung Pelepas Port

5 km

Singapore

1.36

1.35

1.34

1.33

1.32

1.31

103.56 103.57 103.58 103.59 103.6 103.61 103.62 103.63 103.64

Figure 1. Study area in Merambong shoal, southern tip of Peninsular Malaysia in the Straits of Johor.

New records of sea stars (Asteroidea) from Malaysia with notes on their association with seagrass beds

455

Figures 2, 3. Archaester typicus : dorsal view (Fig. 2) and ventral view (Fig. 3). Figures 4, 5. Stellaster equestris : dorsal

view (Fig. 4) and ventral view (Fig. 5). Figures 6, 7. Goniodiscaster scaber. dorsal view (fig. 6) and ventral view (Fig. 7).

456

Woo Sau Pinn et alii

List of Species

George &

George, 1987

Zulfigar

et al., 2008

Sim et al., 2009

This study

ACANTHASTERIDAE

Acanthaster planci (Linnaeus, 1758)

ARHCASTERIDAE

Archasterty picus Muller et Troschel, 1 840

ASTEROPSE1DAE

Asteropsis carinifera (Lamarck, 1816)

ECHINASTERIDAE

Echinaster callosus Marenzeller, 1895

Echinaster luzonicus (Gray, 1840)

Echinaster sp.

Metrodira subulata Gray, 1 840

GONIASTERIDAE

Stellaster equestris (Retzius, 1805)

LUIDIIDAE

Luidia maculata Muller et Troschel, 1840

MITHORODIIDAE

Mithorodia fisheri Holly, 1932

OPHID1ASTER1DAE

Celerina heffernani (Livingstone, 1936)

Fromia elegans H.L. Clark, 1921

Fromia milleporella (Lamarck, 1816)

Fromia monilis (Perrier, 1869)

Fromia indica (Perrier, 1869)

Fromia sp.

Linckia guildingi Gray, 1 840

Linckia laevigata (Linnaeus, 1758)

Linkia cf. multifora (Lamarck, 1816)

Linckia multifora (Lamarck, 1816)

Nardoa cf. gomophia (Perrier, 1875)

Nardoa galathea (Liitken, 1865)

Nardoa gomophia (Perrier, 1875)

Nardoa tuberculata (Gray, 1 840)

Nardoa novaecaledoniae (Perrier, 1875)

Leiaster speciosus von Martens, 1866

Leiaster sp.

Ophidia sterhemprichi Muller et Troschel, 1842

OREASTER1DAE

Choriaster granulatus Liitken, 1869

Culcita novaeguineae Muller et Troschel, 1 842

Culcita cf. coriacea Muller et Troschel, 1 842

Goniodiscaster scaber (Moebius, 1 859)

Neoferdina off red (Koehler, 1910)

Protoreaster nodosus (Linnaeus, 1758)

Pentaster obtusatus (Bory de St. Vincent, 1827)

Total number of species

Table 1. Records of asteroids in Malaysian (* new records found in Malaysian waters).

New records of sea stars (Asteroidea) from Malaysia with notes on their association with seagrass beds

457

refuge and habitat for numerous other associated

organisms, improving water quality and as natural

barrier for protection of coasts against wave actions,

and sea stars are one important organism associated

to the seagrass bed (Gullstrom et al., 2002). The

seagrass of Merambong shoal is composed of ten

different species of seagrasses: Enhalus acroides,

Halodule uninervis, Halodule pinifolia , Cymodocea

serrulata, Cymodocea rotundata , Thalassia

hemprichii , Halophila spinulosa, Halophila ovalis,

Halophila minor and S yringodium isoetifolium

(Bujang et al., 2006).

Field observation did not reveal any particular

association of these asteroids to any specific species

of seagrass nor percentage area coverage of sea-

grass as they were observed throughout the seagrass

area. In terms of canopy heights of seagrass and

abundance of asteroids, areas with lower canopy

heights (in particular from the genera Halodule ,

Cymodocea and Halophila) have higher abundance

in composition of asteroids compared to areas

dominated by high canopy of seagrass ( Enhalus

acroides ) no asteroids where observed.

Vonk et al. (2010) proposed that macrobenthic

organisms including P. nodosus generally prefer

area with high seagrass biomass due to increased

habitat complexity and shelter from predation.

Scheibling (1980) and Scheibling & Metaxes

(2008) found that Oreaster reticulatus and Pro-

toreaster nodosus on seagrass bed feed on microbial

and microalgal films, detritus on the surface of sea-

grass and macroalgae. Scheibling & Metaxes

(2008) also noted the presence of detritus mainly

made out of decomposing seagrass blades and also

epiphytes on the seagrass in the stomach contents

of P nodosus in Palau. Some sea stars also utilize

the seagrass as a transition habitat in juvenile period

as exhibited by A. typicus (Bos et al., 2011), where

the juveniles migrate from mangrove to sandy and

seagrass areas before proceeding to shores. This in-

dicates that seagrass beds are important habitats that

are closely linked to asteroids.

The present study suggests the association of

asteroids to sea grass habiat. There are many other

seagrass beds in the Peninsular Malaysia, yet to be

surveyed, that possibly harbor other species of sea

stars. Future studies in this region should be done

to reveal new records of species and to fill in the

gap of species list as well as geographical distribu-

tion of sea stars.

Figure 8. Dorsal view of Protoreaster nodosus.

Figure 3. Field photograph of Luidia maculata.

ACKNOWLEDGEMENTS

We are especially grateful to members of the

Marine Science Lab, Universiti Sains Malaysia and

Dr. Yuji Ise from University of Tokyo for their kind

assistance during the field and laboratory work. We

also want to mention the contribution from Univer-

sity Putra Malaysia for sampling and logistic ar-

rangements. This study was in collaboration with

the Japan Society for the Promotion of Science for

the Asian CORE Program (Coastal Marine Science

in Southeast Asia: COMSEA). We are also grateful

for the financial support from the Ministry of

458

Woo Sau Pinn et alii

Higher Education Malaysia (MOHE) provided

through the grant: 304/PB/650630/U137.

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B., Saceda M.M. & Tejada L.P., 2011. Ontogenetic

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Okinawa. Bulletin of Marine Science, 38: 366-383.

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and size structure of populations of Oreaster reticu-

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Marine Biology, 57: 95-105.

Scheibling R.E. & Metaxas A., 2008. Abundance, spatial

distribution and size structure of the sea star Portore-

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production. Bulletin of Marine Science, 82: 221—235.

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Biodiversity Journal, 2014, 5 (4): 459-470

Contribution to the knowledge of the Cicindelidae of Benin

with collecting notes (Coleoptera Cicindelidae)

Arnost Kudrna 1 & Philippe Le Gall 2,3

1 Faculty of Science, University of South Bohemia, Branisovska 31, CZ-370 05, Ceske Budejovice, Czech Republic

2 IRD, Institut de Recherche pour le Developpement, BP 1857 Yaounde, Cameroon. UR 072

3 Laboratoire Evolution, Genomes et Speciation, UPR, 9034, Centre National de la Recherche Scientifique (CNRS), 91198 Gif, sur

Yvette Cedex, France et Universite Paris-Sud 11, 91405 Orsay, Cedex, France

^Corresponding author, e-mail: kudmaa@seznam.cz

ABSTRACT A checklist of Coleoptera Cicindelidae presently known from Benin is given. Nine taxa are

recorded for the first time from this country. Collecting data, habitat and behaviour observations

of adults made by the first author during two expeditions are given along with collecting data

provided by the second author.

KEY WORDS Cicindelidae; new records; collecting notes; West Africa; Benin.

Received 18.09.2014; accepted 05.11.2014; printed 30.12.2014

INTRODUCTION

Benin is a small country (about 700 km long and

from 120 to 200 km wide) bordering Togo in the

west, Nigeria in the east and Niger and Burkina

Faso in the north. Benin has several rivers, in

particular two of them that are restricted to the

country: the Oueme River going throughout a large

part of the territory from the north to the south and

the Mono. Semi-deciduous forests probably cov-

ered the southern part of Benin in the past, however

long presence of humans in these areas resulted in

extensive deforestation. Nevertheless, still remain

few small patches of forests, such as Niaouli and

Pobe which are of particular interest. At present the

central part of Benin is largely covered by Guinean

savannas, as result of deforestation. The north part

of Benin is composed of Guineo-sudanian and

sudanian savannas.

The country is situated in a very special eco-

logical area known as the Dahomey-gap (Dahomey

was the former name of Benin). Dahomey gap is

generally considered as an area where the savannas

descend to the Atlantic coast and where forests are

completely absent. This area displays a high biodi-

versity of insects. The high biodiversity and the

relatively a few published data treating Cicindelidae

from Benin motivated our research and this paper.

MATERIAL AND METHODS

Taxonomic classification used here follows the

last complex work on Cicindelidae of Africa (Wer-

ner, 2000a; 2000b) and the only work exclusively

studying Cicindelidae of Benin (Cassola, 2007).

Most of the data and observations resulted from the

first author's two collecting expeditions and the

additional valuable informations came from long-

term residence of the second author.

All specimens considered in this study are in the

first author's collection except for specimens with

abbreviation PLC belonging to the collection of the

second author.

460

Arnost Kudrna & Philippe Le Gall

RESULTS

List of species presently known from Benin

Family Cicindelidae Latreille, 1806

Subfamily Cicindelinae Csiki, 1906

Tribus Megacephalini Csiki, 1906

Subtribus Megacephalina W. Horn, 1910

Genus Megacephala Latreille, 1802

M. (M) quadrisignata quadrisignata Dejean,

1829

M. (M.) quadrisignata rivalieri Basilewsky,

1966

M. (M) bocandei bocandei Guerin, 1848

M. (M) denticollis schultzeorum W. Horn, 1904

M. (M) megacephala (Olivier, 1790) new coun-

try record

Tribus Cicindelini Sloane, 1906

Subtribus Prothymina W. Horn, 1910

Genus Prothyma Hope, 1838

P. (P.) concinna concinna (Dejean, 1831) new

countiy record

P. (P) concinna anosignata Bates, 1878

P. (P) leprieuri leprieuri (Dejean, 1831) new

country record

Genus Euryarthron Guerin, 1 849

E. dromicarium (Kolbe, 1 894) new countiy record

E. walterhorni Cassola, 1983 new country record

E. saginatum (W. Horn, 1912)

E. gibbosum (W. Horn, 1894)

E. planatoflavum (W. Horn, 1 922) new country

record

Subtribus Cicindelina W. Horn, 1908

Genus Elliptica Fairmaire, 1884

E. lugubris (Dejean, 1825)

E. longestriata longestriata (W. Horn, 1912)

Genus Ropaloteres Guerin, 1 849

R. vittatus (Fabricius, 1801)

R. congoensis congoensis (Fleutiaux, 1893)

R. feisthamelii (Guerin, 1 849) new country re-

cord

R. nysa nysa (Guerin, 1 849)

R. cinctus (Olivier, 1790)

Genus Hipparidium Jeannel, 1946

H. interruptum (Fabricius, 1775)

Genus Calochroa Hope, 1838

C. flavomaculata sexsignata (Mandl, 1954) new

country record

Genus Calomera Motschulsky, 1862

C. fimbriata fimbriata (Dejean, 1831)

Genus Lophyra Motschulsky, 1859

Subgenus Lophyra Motschulsky, 1859

L. neglecta neglecta (Dejean, 1825)

L. senegalensis (Dejean, 1825)

Subgenus Stenolophyra Rivalier, 1958

L. (S'.) luxerii (Dejean, 1831)

L. (S'.) saraliensis saraliesis (Guerin, 1849)

Genus Habrodera Motschulsky, 1862

H. nilotica nilotica (Dejean, 1825)

H. nitidula nitidula (Dejean, 1825)

Genus Chaetodera Jeannel, 1946

Ch. regalis regalis (Dejean, 1831)

Genus Cylindera Westwood, 1831

Subgenus Ifasina Jeannel, 1946

C. (/.) lutaria (Guerin, 1849) new country record

C. (/.) decellei Basilewsky, 1968

C. (/.) octoguttata octoguttata (Fabricius, 1787)

Genus Myriochila Motschulsky, 1862

Subgenus Myriochila Motschulsky, 1862

M. peringueyi peringueyi (W. Horn, 1895)

M. plurinotata (Audoin et Brulle, 1839)

M. melancholica melancholica (Fabricius, 1798)

Subgenus Monelica Rivalier, 1950

M. (M) flavidens flavidens (Guerin, 1849)

M. (M) vicina vicina (Dejean, 1831)

M. (M) dumolinii (Dejean, 1831)

M. (M) legalli Kudrna, 2008

Genus Cratohaerea Chaudoir, 1850

C. chrysopyga (W. Horn, 1 892)

Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)

461

Species with listed examined material col-

lected by both authors supplemented with re-

marks (if available)

Genus Megacephala Latreille, 1802

Megacephala quadrisignata quadrisignata

Dejean, 1829

Examined material. N. Benin, Kosso, V.1996,

several specimens in PLC; Tanguieta V- VI. 1998,

several specimens in PLC; Nanebou, VII.2001,

several specimens in PLC; C. Benin, Ekpa V.1996,

5 males, 4 females in PLC.

Megacephala quadrisignata rivalieri Basilewsky,

1966

Examined material. N. Benin, Kosso, 1 male

in PLC; Benin, Nanebou, 1 male in PLC; Benin,

Serou (Djougou), 1 female in PLC.

Megacephala bocandei Guerin, 1848 (Pig. 1)

Examined material. NE Benin, E of Kandi, 4

km W of Bensekou, 24-25.VI.2001, A. Kudma jr.

legit, 1 male; NW Benin, 15 km N of Kouarfa,

Bouyagnindi village, 27-28.VI.2001, A. Kudrna jr.

legit, 1 female.

Remarks. The cited pair are the only specimens

of M. bocandei captured during both first author's

trips. The male run quickly in night on black soil

path, just where the path left grassy area reach in

trees and entered in the field. The female was

observed in the late morning of a sunny day in

wooded area with high grass and neighbouring

field, moving quickly, probably searching for a prey.

Megacephala denticollis schultzeorum W.

Horn, 1904 (Pig. 2)

Examined material. Benin, village Akongbere,

near Save, 19-26.IV.2000, A. Kudrna jr. legit, 2

males, 2 females; Kosso : V-VI. 1997- 1999, numer-

ous specimens in PLC; Serou, V-VI. 1997- 1999, nu-

merous specimens in PLC; Guinlerou, 15 km west

of Parakou, IV- VII. 1996- 1998, numerous speci-

mens in PLC.

Remarks. Specimens were found in night stand-

ing on dark paths through dense woodland area with

high grass. One female came to light. A torso of a

dead adult was found at the same locality in June

2001 .

Megacephala megacephala (Olivier, 1790)

Examined material. NE Benin, E of Kandi,

around Saa, 21-23.VI.2001, A. Kudrna jr. legit, 1

male, 4 female.

Remarks. According to Basilewsky (1966), this

species is widespread from Senegal and Mauritania

to Chad and occurs in sahelian zone or neighbour-

ing areas only. The cited population here reported

was discovered in northern area of Benin, where

the countryside seems to be more dry and hotter.

Specimens were captured during night on sandy

roads and occasionally came to light. One speci-

men was found quickly running through grasses in

the end of about two hours lasting hard storm

accompanied with intensive rain. New country

record.

Genus Prothyma Hope, 1838

Prothyma concinna concinna (Dejean, 1831)

Examined material. NE Benin, E of Kandi, 7

km E of Bensekou, 23-24. VI. 2001, A. Kudma jr.

legit, 2 males.

Remarks. The first author observed four adults,

but managed to catch only two of them due to their

very rapid movement from small bare places where

discovered, into grass or other hiding-places. These

adults didn't fly. New country record.

Prothyma concinna anosignata Bates, 1878

Examined material. S Benin, Niaouli,

20.X. 1996, 1 female in PLC; S Benin, Niaouli, 10.

VII. 2002, 1 male in PLC; 1 female; S Benin,

Niaouli, 20. XI. 2003, 1 female in PLC; Benin,

Attogon, V.2001, 1 female in PLC; N Benin,

Tanguieta, 20.VII.1998, 1 female in PLC; Benin,

Penessoulou, VI. 1997, 1 male in PLC.

Prothyma leprieuri leprieuri (Dejean, 1831)

Examined material. Penessoulou, 55 km S

Djougou, Atakora Benin, Loko/P.Le Gall

Remarks. A single female specimen without

date record, collected by the second author most

probably at the light. The discovery of this species

462

Arnost Kudrna & Philippe Le Gall

Figure 1. Megacephala ( Megacephala ) bocandei, E of Kandi, 21.3 mm

Figure 2. Megacephala ( Megacephala ) denticollis schultzeorum, near Save, 31.5 mm

in Benin is not surprising due to its wide distribu-

tion from Senegal to Ethiopia. New country record.

Genus Euryarthron Guerin, 1 849

Euryarthron dromicarium (Kolbe, 1894) (Fig. 3)

Examined material. Benin, Bembereke, 2 km

W of Gando, 02-03.VII.2001, A. Kudrna jr. legit, 1

female; NW Benin, 5 km N of Tanguieta, direction

Tanougou, 28-29.VI.2001, A. Kudrna jr. legit, 3

males.

Remarks. A very beautiful wingless species of

Euryarthron which is extremely difficult to find in

Benin. It seems, that this species prefers meadows

or grassy places at the edges of forested areas.

Adults were discovered on bare places, trying to

escape into the grass, when disturbed. One male

specimen came to light. New country record.

Euryarthron walterhorni Cassola, 1983

Examined material. Benin, Tanguieta,

10.V.1997, 1 female; Kosso, VI. 1998, 2 males, 2

females; Benin, Serou VI.2000, 1 male, 1 female;

Benin, Serou, VII. 1998, 1 female. All specimens in

PLC.

Remarks. New country record.

Euryarthron saginatum (W. Horn, 1912) (Fig. 4)

Examined material. NE Benin, E of Kandi, 4

km W of Bensekou, 24-25.VI.2001, A. Kudrna jr.

legit, 2 females; NE Benin, E of Kandi, around Saa,

21-23.VI.2001, A. Kudrna jr. legit, numerous spec-

imens.

Remarks. This species was found on white-

grey soil road through dry woodland with lot of aca-

cia trees. When discovered, it tried to escape flying

Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)

463

Figure 3. Euryarthron dromicarium, S ofKerou, 13 mm

Figure 4. Euryarthron saginatum, E of Kandi, 13.3 mm

away and sit down into the nearby grass. On this

road it lived together with Myriochila plurinotata

and M. ( Monelica ) vicina vicina. In another occa-

sion it was also found in sparse acacia wood.

Euryarthron gibbosum (W. Horn, 1894)

Examined material. Benin, village Alcongbere,

near Save, 19.IV-26.IV.2000, A. Kudma jr. legit, 6

males, 3 females; NE Benin, E of Kandi, 4 km W

of Bensekou, 24-25. VI. 2001, A. Kudma jr. legit, 2

males; NE Benin, E of Kandi, 7 km E of Bensekou,

23-24.VI.2001, A. Kudma jr. legit, 1 male; NW

Benin, 5 km N of Tanguieta, direction Tanougou,

28-29.VI.2001, A. Kudma jr. legit, 1 female.

Remarks. In May 2000 this species appeared

suddenly in the dense woodland area around

Alcongbere village, near Save. Whilst first week of

intensive collecting there was unproductive, during

four next days about 15 adults, at the same, for-

merly empty places, were caught. Few more speci-

mens were found in northern parts of country. This

species prefers shaded places with sparse grass,

paths or roads inside woods.

Euryarthron planatoflavum (W. Horn, 1922)

Examined material. Penessoulou IV. 1998, 1

male in PLC.

Remarks. New country record.

Genus Elliptica Fairmaire, 1884

Elliptica lugubris (Dejean, 1825)

Examined material. NE Benin, E of Kandi, 4

km W of Bensekou, 24-25. VI.2001, A. Kudrna jr.

legit, 1 male; N Benin, S of Kerou, 7 km W

Yakrigourou, 25-26. VI. 2001, A. Kudrna jr. legit, 2

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Arnost Kudrna & Philippe Le Gall

females; NW Benin, 5 km N of Tanguieta, direc-

tion Tanougou, 28-29.VI.2001, A. Kudrna jr. legit

3 females, 1 male; NW Benin, 15 kmN ofKouarfa,

Bouyagnindi village, 27-28.VI.2001, A. Kudrna jr.

legit, 4 males, 3 females; NE Benin, E of Kandi, 7

km E of Bensekou, 23-24. VE2001, A. Kudrna jr.

legit, 1 male; Benin, Bemberelce, 7 km W of

Gando, 03 -04. VII. 2001, A.Kudrna jr. legit, 2

males; Benin, Bembereke, 2 km W of Gando, 02-

03. VII. 2001, A. Kudrna jr. legit, 1 male; Penes-

soulou, VI.1998-VI.1999, numerous specimens in

PLC; Serou.

Remarks. This very beautiful large species was

present at most of the localities, but usually in few

specimens only. Horn (1915) described subspecies

E. lugubris anthrax, based on the black coloura-

tion. However, the black specimens represent

merely a variation without any taxonomic value.

Interesting is the proportion between this black

form and the common black-yellow specimens:

first author observed only one anthrax variation

along tens of individuals on all of the collecting

spots except locality 5 km N of Tanguieta, where

six from eight caught specimens were black. This

locality, near Atacora Mountains with very sparse

wood with dominance of acacia trees was very hot

and dry place. Elliptica lugubris is generally

silvicolous dwelling species preferring shaded

grassy places.

Elliptica longestriata longestriata (W. Horn, 1912)

Examined material. NW Benin, N of Natitin-

gou, 5 kmNE ofKouarfa, 26-27.VI.2001, A. Ku-

drna jr. legit, 1 female, 1 male; NE Benin, E of

Kandi, 4 km W of Bensekou, 24-25. VI. 2001, A.

Kudrna jr. legit, 1 male, 1 female; NW Benin, 30

km SE of Natitingou, 5 km E of Sina Issire,

30.VI-01.VII.2001, A. Kudrna jr. legit, 2 females;

NW Benin, 15 km N of Kouarfa, Bouyagnindi

village, 27-28. VI. 2001, A. Kudrna jr. legit, 1

male.

Remarks. A very surprising discovery of the

species in Benin, as it was in the time of collecting

known from north of former Zaire and Central

African Republic only. This indicates a much

wider distribution than supposed. Adults were

found always on dark soil with sparse grass,

usually on the edges of fields or directly inside

when uncultivated.

Genus Ropaloteres Guerin, 1849

Ropaloteres vittatus (Fabricius, 1801)

Examined material. NW Benin, 30 km SE

Natitingou, 5 km E of Sina Issire, 30.VI-

01.VII.2001, A. Kudrna jr. legit, 1 female; Benin,

village Akongbere, near Save, 19-26.IV.2000, A.

Kudma jr. legit, 6 males, 3 females.

Remarks. R. vittatus was very rare to find in

Benin during both expeditions. Only few specimens

on very few localities were discovered. It prefers

dark soil paths and clearings in shaded woodland

areas.

Ropaloteres congoensis congoensis (Fleutiaux,

1893)

Examined material. NW Benin, N of Natitin-

gou, 5 kmNE ofKouarfa, 26-27.VI.2001, A. Ku-

drna jr. legit, 7 females, 4 males; NW Benin, 30

km SE Natitingou, 5 km E of Sina Issire, 30.VI-

01. VII. 2001, A. Kudrna jr. legit, 2 males, 2 fe-

males; N. Benin, Ekpa, VI. 1996, 2 males, 1 female

in PLC.

Remarks. This beautiful species was found on

the three cited localities only. On one occasion four

specimens were collected on the edge of a sandy

road and nearby meadow, another time it was

discovered on red soil with turfs of high grass.

Adults were usually a little bit lazy to fly and

preferred rapid run into the shadow of the turfs.

Only when disturbed repeatedly, they flew a few

meters and sat down again near to turfs. After

settling they often disappeared by running through

grasses somewhere on the reverse side, and there-

fore they were hardly found again. This beetle

seems to be generally very rare, however, when a

spot with its occurrence is found, it is usually pos-

sible to collect numerous specimens.

Ropaloteres feisthamelii (Guerin, 1849)

Examined material. NW Benin, 30 km SE

Natitingou, 5 km E of Sina Issire, 30. VI-

01.VII.2001, A. Kudrna jr. legit, 1 female; NW

Benin, N of Natitingou, 5 km NE ofKouarfa, 26-

27.VI.2001, A. Kudma jr. legit, 1 female; N Benin,

S of Kerou, 7 km W Yakrigourou, 25-26.VI.2001,

A. Kudrna jr. legit, 1 female, 2 males; NW Benin,

15 km N of Kouarfa, Bouyagnindi village, 27-

Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)

465

28.VI.2001, A. Kudrna jr. legit, 1 male; NW

Benin, 5 km N of Tanguieta, direction Tanougou,

28-29.VI.2001, A. Kudrna jr. legit, 1 male; Benin,

Bembereke, 7 km W of Gando, 03-04.VII.2001,

A. Kudrna jr. legit, 1 male, 1 female; Serou, V.

2000, 1 female in PLC.

Remarks. Relatively common species occurring

in grassy places in woodland areas, regularly at-

tracted to light. New country record.

Ropaloteres nysa nysa (Guerin, 1849)

Examined material. Benin, village Alcongbere,

near Save, 19.IV-26.IV.2000, A. Kudrna jr. legit,

numerous specimens; NW Benin, 15 1cm N of

Kouarfa, Bouyagnindi village, 27-28. VI.2001, A.

Kudrna jr. legit, 1 male, 2 females; NE Benin, E of

Kandi, 7 km E of Bensekou, 23-24. VL2001, A.

Kudrna jr. legit, 1 male; NW Benin, 5 km N of

Tanguieta, direction Tanougou, 28-29.VI.2001, A.

Kudrna jr. legit, 3 males, 1 female; Benin, Bembe-

reke, 2 km W of Gando, 02-03.VII.2001, A. Ku-

drna jr. legit, 1 male, 1 female; Penessoulou,

V-VI. 1999-2000, numerous specimens in PLC.

Remarks. Very common species with the

same habitat and behaviour as the previous R.

feisthamelii , often coming to light.

Ropaloteres cinctus (Olivier, 1790)

Examined material. Benin, village Alcongbere,

near Save, 19.IV-26.IV.2000, A. Kudrna jr. legit

numerous specimens; NE Benin, E of Kandi, 4 km

W of Bensekou, 14-25.VI.2001, A. Kudmajr. legit,

2 males, 2 females; N Benin, S of Kerou, 7 km W

Yakrigourou, 25-26. VL2001, A. Kudmajr. legit,

numerous specimens; NW Benin, 15 km N of

Kouarfa, Bouyagnindi village, 27-28.VI.2001, A.

Kudmajr. legit, 2 males, 1 female; NE Benin, E of

Kandi, 7 km E of Bensekou, 23-24. VI. 2001, A. Ku-

dmajr. legit, 2 males, 1 female; Benin, Bembereke,

2 km W of Gando, 02-03 .VII. 2001, A. Kudmajr.

legit, numerous specimens.

Remarks. Probably the commonest species of

those, which prefer grassy, shadowed places in

woodlands. This species, in contrast to Elliptica

lugubris, occurred only on a few of the visited

localities, but there it was abundant.

Genus Hipparidium Jeannel, 1946

Hipparidium interruptum (Fabricius, 1775)

Examined material. Benin, near Cove, E of

Abomey, 16.IV.2000, A. Kudmajr. legit, 1 female;

Pobe, Aguigadji, V.1998, 1 female in PLC.

Remarks. Female from E of Abomey was found

on shaded dark soil path inside palm plantation.

Genus Calochroa Hope, 1838

Calochroa flavomaculata sexsignata (Mandl, 1954)

Examined material. Africa/Benin, W-Nat.

Park, X.2002, Mekrou river, Triple Point, 1 male;

Benin, Penessoulou, 12.XI.2000, at light, 1 male, 1

female in PLC.

Remarks. New country record.

Genus Calomera Motschulsky, 1862

Calomera fimbriata fimbriata (Dejean, 1831)

Examined material. Benin, Banks of river

Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.

Kudrna jr. legit, numerous specimens; Benin,

Cove: 20. VI. 2000, numerous specimens in PLC;

Benin, Cove: 27. VI. 2000, numerous specimens in

PLC; Benin, Cove: 5. VI. 2001, numerous speci-

mens in PLC.

Remarks. Adults of this species were present in

huge masses on yellowish sand around river

Oueme, where also Lophyra neglecta neglecta, L.

senegalensis, Cylindera ( Ifasina ) octoguttata oc-

toguttata and Habrodera nilotica nilotica occurred.

Occasionally, beautiful blueish specimens (in

proportion about 1 : 1 00) were caught.

Genus Lophyra Motschulsky, 1859

Subgenus Lophyra s.str.

Lophyra {Lophyra) neglecta neglecta (Dejean,

1825)

Examined material. Benin, Banks of river

Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.

Kudrna jr. legit, numerous specimens; Benin,

Cove, VI.2000, numerous specimens in PLC;

Toffo, IIII.2001, numerous specimens in PLC.

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Figure 5. Cylindera ( Ifasina ) lutaria, W of Gando, 7.8 mm

Figure 6. Myriochila ( Myriochila ) peringueyi, Ndali, 10.1 mm

Remarks. Very common species found on sand

or sandy road near water.

Lophyra {Lophyra) senegalensis (Dejean, 1825)

Examined material. Benin, banks of river

Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.

Kudrna jr. legit, numerous specimens; Benin, vil-

lage Akongbere, near Save, 19-26.IV.2000, A. Ku-

dma jr. legit, numerous specimens; NE Benin, E of

Kandi, 7 1cm E of Bensekou, 23-24. VI. 2001, A.

Kudrna jr. legit, 1 male, 1 female.

Remarks. This species does obviously not

prefer places near water, but was found on many

localities on sandy roads. Even on the river banks

it lives further to water. A common species in

Benin.

Subgenus Stenolophyra Rivalier, 1958

Lophyra ( Stenolophyra ) luxerii (Dejean, 1831)

Examined material. Benin, village Akongbere,

near Save, 19.IV-26.IV.2000, A. Kudrna jr. legit,

numerous specimens; NW Benin, 15 km N of

Kouarfa, Bouyagnindi village, 27-28. VI. 2001, A.

Kudma jr. legit, 1 male, 1 female; NE Benin, E of

Kandi, 7 1cm E of Bensekou, 23-24.VI.2001, A. Ku-

drna jr. legit, numerous specimens; Benin, Niaouli,

VI. 1997-2002, numerous specimens inPLC; Serou,

VI. 1999, 11 males, 12 females in PLC.

Remarks. Occurs in woodland areas and

prefers dark soil roads and paths. A relatively

common species.

Genus Habrodera Motschulsky, 1862

Habrodera nilotica nilotica (Dejean, 1825)

Examined material. Benin, banks of river

Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)

467

Figure 7. Myriochila ( Monelica ) vicina, N of Natitingou, 9.2 mm

Figure 8. Myriochila ( Monelica ) legalli, N of Natitingou, 9.75 mm

Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.

Kudmajr. legit, numerous specimens.

Remarks. This species was found on yellowish

sand of river banks.

Habrodera nitidula nitidula (Dejean, 1825)

Examined material. Benin south, Grand-Popo,

ocean coast, 17.04.2000, A. Kudmajr. legit, 14

males, 2 females.

Remarks. A seashore species. The specimens

were caught on a huge long sandy beach under

windy conditions, always in a large distance from

a water line. Uncommon on this beach.

Genus Cylinder a westwood, 1831

Subgenus Ifasin a Jeannel, 1946

Cylindera ( Ifasina ) lutaria (Guerin, 1849) (Fig. 5)

Examined material. NE Benin, E of Kandi, 4

km W ofBensekou, 24-25. VI. 2001, A. Kudmajr.

legit, 1 female; NE Benin, E of Kandi, 7 km E of

Bensekou, 23-24. VI. 2001, A. Kudmajr. legit, 7

males, 1 female; Benin, Bembereke, 7 km W of

Gando, 03-04. VII. 2001, A. Kudrna jr. legit, 1

male, 1 female; Benin, Bembereke, 2 km W of

Gando, 02 -03. VII. 2001, A. Kudmajr. legit, 2

males.

Remarks. C. (/.) lutaria was found on various

localities, but always near puddles or in muddy or

moist places, usually in few specimens only. A rare

species in Benin. New record for this country.

Cylindera {Ifasina) octoguttata octoguttata

(Fabricius, 1787)

Examined material. Benin, banks of river

Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.

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Kudma jr. legit, numerous specimens; NE Benin, E

of Kandi, 7 km E of Bensekou, 23-24.VI.2001, A.

Kudma jr. legit, 1 male.

Remarks. This very common species was

present in swarms around puddles just next to river.

On several occasions it was captured near brooks

and small rivers.

Genus Myriochila Motschulsky, 1862

Subgenus Myriochila Motschulsky, 1862

Myriochila {M.) peringueyi peringueyi (W.

Horn, 1895) (Fig. 6)

Examined material. Benin, village Akong-

bere, near Save, 19.IV.-26.IV.2000, A. Kudma jr.

legit, 1 female; Benin, Ndali, 3 km W of Sontou,

04-05. VIE2001, A. Kudrna jr. legit, numerous

specimens.

Remarks. The species was abundant west of

Sontou inside a forest area on a flat volcanic rock,

partly covered with a thin layer of dark soil. No

water was present in the vicinity. This species with

unusual red-green body reflexions seems to prefer

rocks or stony places, as also the only female

collected near village Akongbere was discovered in

slightly muddy situation on dark soil road, just

where the road cross a big flat rock.

Myriochila (M.) plurinotata (Audoin et Brulle,

1839)

Examined material. NE Benin, E of Kandi, 7

km E of Bensekou, 23-24. VE2001, A. Kudrna jr.

legit, numerous specimens; NW Benin, 5 km N of

Tanguieta, direction Tanougou, 28-29.VI.2001, A.

Kudma jr. legit, numerous specimens; NW Benin,

N of Natitingou, 5 km NE of Kouarfa, 26-

27.VE2001, A. Kudrna jr. legit, numerous speci-

mens; NW Benin, 15 km N of Kouarfa,

Bouyagnindi village, 27-28.VI.2001, A. Kudma jr.

legit, 2 males, 3 females.

Remarks. This species was present on several

localities, usually sitting on soil roads or other bare

places in sunny situation. On the locality situated 5

km NE of Kouarfa it occured together with another

nine species: Elliptica lugubris, E. longestriata

longestriata, Myriochila ( Monelica ) dumolinii, M.

(M.) vicina, M. (M.) legalli, Lophyra ( Stenolo -

phyra ) luxerii, Ropaloteres cintus, R. congoensis

congoensis, R. feisthamelii. Regularly came to light.

Not rare in Benin.

Myriochila (M.) melancholica melancholica

(Fabricius, 1798)

Examined material. Benin, banks of river

Oueme, E of Zangnanado, 14.IV-15.IV.2000, A.

Kudma jr. legit, numerous specimens; Benin,

village Akongbere, near Save, 19.IV-26.IV.2000, A.

Kudma jr. legit, numerous specimens; Toffo, 12.11.

2001, several specimens in PLC; Serou, VI. 1998,

several specimens in PLC.

Remarks. This very common species was

present at most of the collecting places always near

water.

Subgenus Monelica Rivalier, 1950

Myriochila ( Monelica ) flavidens flavidens

(Guerin, 1849)

Examined material. NE Benin, E of Kandi,

around Saa, 2 1-23. VI. 2001, A. Kudrna jr. legit,

numerous specimens; NE Benin, E of Kandi, 7 km

E of Bensekou, 23-24.VI.2001, A. Kudma jr. legit,

numerous specimens; Benin, Bembereke, 7 km W

of Gando, 03-04.VII.2001, A. Kudrna jr. legit, 2

males, 3 females.

Remarks. Although considered to be a very rare

species (Werner, 2000), it was observed on many

localities in northern parts of Benin. Adults were

present in masses on laterite soils, always in muddy

or moist places or near puddles, and surely repre-

sented one of the commonest species during the

second collecting trip of the first author.

Myriochila (Monelica) vicina vicina (Dejean,

1831) (Fig. 7)

Examined material. NW Benin, 5 km N of

Tanguieta, direction Tanougou, 28-29. VI.2001, A.

Kudma jr. legit, numerous specimens; N Benin, S

of Kerou, 7 km W Yakrigourou, 25-26. VI.2001, A.

Kudma jr. legit, numerous specimens; NE Benin, E

of Kandi, 7 km E of Bensekou, 23-24. VI.2001, A.

Kudma jr. legit, numerous specimens; NW Benin,

15 km N of Kouarfa, Bouyagnindi village, 27-

28.VI.2001, A. Kudma jr. legit, 1 male, 2 females;

Penessoulou, V.1998 numerous specimens in PLC;

Penessoulou, V.1999 numerous specimens in PLC.

Contribution to the knowledge of the Cicindelidae of Benin with collecting notes (Coleoptera Cicindelidae)

469

Remarks. During second collecting trip of the

first author, this species was abundantly found in

the northern parts of the country. Specimens were

collected on bare places, paths or roads through

grass or fields.

Myriochila ( Monelica ) dumolinii (Dejean, 1831)

Examined material. Benin, Bembereke, 7 km

W of Gando, 03-04.VII.2001, A. Kudmajr. legit, 2

males; N Benin, S of Kerou, 7 km W Yakrigourou,

A. Kudma jr. legit, 2 females; NW Benin, N of

Natitingou, 5 km NE of Kouarfa, 26-27.VI.2001,

A. Kudrna jr. legit, 1 male ; NW Benin, 30 km SE

Natitingou, 5 km E of Sina Issire, 30. VI-

01.VIE2001, A. Kudmajr. legit, 1 female; Serou,

VI. 1997, several specimens in PLC; Serou,

VIE 1998, several specimens in PLC.

Remarks. Adults came regularly to light. Two

specimens were found on laterite soil road in a

sunny day. Uncommon.

Myriochila (Monelica) legalli Kudrna, 2008

(Fig. 8)

Examined material.NW Benin, N of Natitin-

gou, 5 km NE of Kouarfa, 26-27. VI.2001, A. Ku-

dma jr. legit, 5 males, 2 females; NE Benin, E of

Kandi, 7 km E Bensekou, 23-24. VL2001, A. Ku-

dmajr. legit, 1 male, 1 female; NW Benin, 15 km

N of Kouarfa, Bouyagnindi village, 27-28. VI.2001,

A. Kudmajr. legit, 1 female; S Benin, vill. Akong-

bere, near Save, 16-20.VI.2001, A. Kudmajr. legit,

1 female.

Remarks. Specimens of this recently described

species (Kudma, 2008) were found during sunny

day on dark soil road through dense wood in

forested area and also on laterite soil of a wide field

road in the agricultural area.

Genus Cvatohaerea Chaudoir, 1850

Cratohaerea chrysopyga (W. Horn, 1892)

Examined material. Benin , village Akongbere,

near Save, 19.IV-26.IV.2000, A. Kudmajr. legit, 15

males, 5 females; NE Benin, E of Kandi, around

Saa, 2 1-23. VI.2001, A. Kudmajr. legit, 3 males, 3

females; Benin, Bembereke, 7 km W of Gando, 03-

04.VII.2001, A. Kudmajr. legit, 2 males, 1 female;

Ouidah, 20.V.1996, 1 female in PLC; Benin, Pobe,

X.2001, 1 male in PLC; Niaouli IV-VI.1996 several

specimens in PLC; Niaouli VI. 1998 several speci-

mens in PLC; Niaouli V-VI.1999 several specimens

in PLC; Benin, Parakou, V.1996, several specimens

in PLC; Benin, Kosso, V-VII. 1998-2000, several

specimens in PLC.

Remarks. All specimens of C. chrysopyga were

found on termitaries. They prefer bigger ones,

situated entirely or at least partly in shaded places

and with more or less preserved structure. When

disturbed, they tried to hide themselves by mnning

constantly on the reverse side of the termitaries and

with care it was even possible to catch them by

hand. When adult successfully escaped from behind

the net, then settled on the opposite side of the

termitaries, in the nearby grass or flew away and

disappeared somewhere in the forest. But after

some time, the beetle was back. It was usually

necessary to visit several termitaries to find one in-

habited. Generally one or two specimens together

were found on one termitarium, but in one occasion

even four were present. Relatively rare in Benin.

DISCUSSION

Werner (2000a, b), in his monographic review

of African tiger beetle fauna listed 1 7 species and

subspecies from Benin. Recently Cassola (2007),

in the only so far existing publication devoted

solely to Cicindelidae of Benin reported 31 taxa

(30 species and one subspecies) from this country.

In this contribution we add another nine species as

new for Benin thus the total number is 41. Most

of the species added in this contribution were

expectable to occur in Benin. We suppose that new

records will follow and the number of tiger beetles

taxa known from this beautiful country can exceed

50 or even 55.

ACKNOWLEDGMENTS

We would like to express our thanks to Dr.

Georg Goergen. Moreover the first author thanks to

all of his companions during the two Benin's trips:

Mrs. Libena Kantnerova and Mr. Frantisek Kantner

(Lipi), Mr. Zdenek Andrs (Cemosin), Mr. Borivoj

Vorisek (Ceske Budejovice), Mr. Jin Halada (Ceske

Budejovice), first author’ s father Amost Kudma sr.

470

Arnost Kudrna & Philippe Le Gall

(Rudofov), driver Wirgile Adingni and Mr. and Mrs.

Ahanhanzo.

REFERENCES

Basilewsky P., 1966. Revision des Megacephala d'

Afrique (Coleoptera Carabidae Cicindelinae), Anna-

les Musee Royal de T Afrique Centrale, Serie IN-°8,

n°152, 1-149.

Cassola R, 2007. Studies of tiger beetles. CLXV. New

data from Benin (Coleoptera: Cicindelidae), Rivista

Piemontese di Storia Naturale, 28: 157-164.

Kudrna A., 2008. Myriochila ( Monelica ) legalli sp. n.

from Benin and Senegal (Coleoptera, Cicindelidae),

Entomologia Africana, 13: 33-37.

Werner K., 2000a. The tiger beetles of Africa (Coleoptera:

Cicindelidae), Volume 1, Taita publishers, 191 pp.

Werner K., 2000b. The tiger beetles of Africa (Coleoptera:

Cicindelidae), Volume 2, Taita publishers, 207 pp.

Biodiversity Journal, 2014, 5 (4): 471-474

The first record of Trigonostigma somphongsi (Meinken, 1 958),

a critically endangered species, in its natural habitat of Thai-

land (Cypriniformes Cyprinidae)

Nidsaraporn Petsut',Nonn Panitvong 2 , Sitthi Kulabtong 3 ,Jirawaeth Petsut 1 & Chirachai Nonpayom 4

'Department of Agricultural Technology, Faculty of Science, Ramkhamhaeng University, Bangkok 10240, Thailand; e-mail:

nidsarapom@ni.ac.th (Nidsaraporn Petsut); e-mail: jira3800@sanook.com (Jirawaeth Petsut)

2 Siamensis Biodiversity Conservation Group, 408/144 Phaholyothin Place Bldg 34FL, Phaholyothin Rd., Phayathai, Bangkok

10400, Thailand; e-mail: npanitvong@gmail.com

fisheries Program, Faculty of Agro-Industrial Technology, Rajamangala University of Technology Tawan-ok Chantaburi Campus

Chantaburi 22210, Thailand; e-mail: kulabtong2011@hotmail.com

4 534/26 Soi Phaholyothin 58 Phaholyothin Rd. Sai Mai, Bangkok, Thailand; e-mail: sornl33@hotmail.com

^Corresponding author

ABSTRACT A population of a critically endangered Trigonostigma somphongsi (Meinken, 1958) has been

discovered in a deepwater rice field, floodplain of Bangpakong Basin, Nakhomnayok Province,

central Thailand. The population was the first record of this species in its natural habitat since

its description by Meinken in 1958. The species appeared to be a seasonal horizontal migration

species, since it migrates to breed in the floodplain during the rainy season between July and

November and migrates back into the main channel during the dry season.

KEY WORDS Trigonostigma somphongsi ; Cyprinidae; Bangpakong; Thailand.

Received 19.09.2014; accepted 12.11.2014; printed 30.12.2014

INTRODUCTION

Trigonostigma somphongsi (Meinken, 1958)

was placed in the genus Rasbora (Bleeker, 1859)

(Meinken, 1958) and, subsequently, in the genus

Trigonostigma Kottelat et Witte, 1999 described by

Kottelat & Witte (1999).

The genus Trigonostigma is a well defined

group comprising 4 species: T. heteromorpha

(Duncker, 1904), as type species, with its distribu-

tion in Malay Peninsula, T. espei (Meinken, 1967)

found in south eastern and southern part of Thai-

land, and T. hengeli (Meinken, 1956) reported from

Sumatra; the fourth species, T. somphongsi, differs

from the rest of the genus in its dark pattern which

occurs as a strait horizontal line that extends from

the base of the caudal fin and ends just after it

passed the posterior part of the dorsal fin instead of

showing the wedge-like marking of other species in

the genus.

Apart from external characters of the body

shape and marking, this genus also differs from

other Rasborins in its breeding strategy since

parents deposit eggs under broad leaves of aquatic

plants instead of scattering eggs like most others.

In this regard, it is interesting to note the sex ratio

screwed towards males in this species observed in

this survey.

The type series of T. somphongsi was said to

come from aquarium trade, sent to Meinken by

Somphongs Aquarium, an ornamental fish exporter

run by Mr. Somphongs Lekaree with its base in

472

Nidsaraporn Petsut et alii

Thailand. The fish was thus, named after Somphong

in honor of his contribution of the type series.

No detail of its habitat was given in the paper;

Meinken only mentioned that it was from Southern

Thailand (Meinken, 1958). The fish appeared in

various hobby publishing during the 70s in both

Europe and Asia before completely disappearing for

some 20 years. It wasn’t until 2006 when three T.

somphongsi were found among a batch of Boraras

urophthalmoides (Kottelat, 1991) by Uta Hanel

(Germany). They happened to be one male and two

females thus forming the core for a captive breeding

population which is still going on in Europe, mainly

Germany and England, as well as in Thailand.

However, to date, no fish has ever been ob-

served in its natural habitat, which prompted IUCN

to list it as Critically Endangered (Vidthayanon,

2013) and listed it as world’s 100 most threaten

species (Baillie & Butcher, 2012). Upon our survey

of a flood plain in deepwater rice field, flood plains

of Bangpakong Basin, Nakhornnayok Province,

central Thailand, a population of T. somphongsi was

discovered. Its habitat and population demography

will be described here.

MATERIAL AND METHODS

Surveys were conducted by dragging fine mesh

sein, along marginal area of floodplain as well as

along the road and rice field. We also snorkeled to

observe its habitat and behavior under water. All

other species were released on site as quickly as

possible after identification.

All T. somphongsi (Fig. 1) were kept alive for

further study in captivity. Surveys were conducted

from September 2012 to November 2013. Locals

were interviewed for further information and water

quality parameters were measured with methods by

APHA et al. (2009).

Study area

Trigonostigma somphongsi was found in a

deepwater rice field, in the flood plains of Nakhom-

nayok River, Bangpakong Basin, Nakhornnayok

Province, central Thailand (Fig. 2), one of the main

tributaries of Bangpagong River, which empties

into the Gulf of Thailand. The head water, to the

north, originated in KhaoYai National Park, which

is a part of Dong Phayayen-KhaoYai Forest Com-

plex - UNESCO World Heritage site. The area is

characterized by flat land, with numerous water

ways. Majority of the land has been turned into

agricultural land. The main crop is rice ( Oryza sp.).

Our survey plot was in Pak Phli District, Nakom-

nayok Province.

The fish was found in the rice field and in a

densely vegetated ditch, which was flooded by a

nearby river. The water quality parameters are

shown in Table 1 . It is interesting to note the drop

of the water’s pH from 7.98, when it first enters the

floodplain, to 3.8 1 after a few months of inundation.

The field was planted with a variety of rice called

“Banna 423”, developed by the Rice Department of

Thailand. This variety is said to be able to grow as

fast as 1 0 centimeters in 24 hours and can grow as

long as 5 meters, thus being immune to the flood

and forming a dense under- water jungle.

In the same area, the other fish species were sur-

veyed and reported by Petsut et al. (2013a) and Pet-

sut et al. (2013b). A total of 23 species, 8 families

and 4 orders of freshwater fishes were recorded.

The natural aquatic plants in this area was

reported by Petsut et al. (2012) with Poaceae as

WATER QUALITY

PARAMETERS

RESULT

Water temperture (°C) at 1.00

p.m.

31.0-33.5

Transparency (cm)

80 - bottom soil (tran-

sparent)

Water depth (cm) in flood season

300 - 30

Water pH

3.81-7.98

Soil pH

3.85-4.70

Alkalinity (ml/L as CaCCb)

6.37-47.00

Ammonia (ml/L Nitrogen)

0.042 - 0.450

Nitrite (ml/L Nitrogen)

0.076-0.160

Nitrate (ml/L Nitrogen)

0.461 -0.680

Hardness (ml/L as CaCCb)

35-202

Orthophosphate (ml/L Phospho-

rus)

0.020 - 0.022

Table 1 . Water quality parameters in a deepwater rice

field, flood plain of Bangpakong Basin, central Thailand.

The first record of Trigonostigma somphongsi, an critically endangered species, in Thailand (Cypriniformes Cyprinidae) 473

dominant family. The change of benthic fauna com-

position and ecological structure of plankton com-

munities in theses area was reported by Petsut et al.

(2013c) and Petsut et al. (2013d).

RESULTS

During the dry season, i.e. when water has com-

pletely receded into the river, in the area where we

would have found, later, T. somphongsi during the

flooding, only Boraras urophthalmoides and

Trichopsis vittatus (Cuvier, 1831) were observed.

July represented the first month of inundation.

Many species of fishes were found in the floodplain

in abundance. In this period we only caught one T.

somphongsi gravid female.

From September to November, the peak of flood-

ing period, we caught many semi-adult (probably

young of the year), but failed to find any full grown

adults. We believe that the adults only migrate to

breed and then leave the flood plain, back to the

main channel. T. somphongsi is weakly sexual

dimorphic. Females can be distinguished from

males by larger size, plumper belly and less intense

orange coloration on the body. Twelve semi-adults

grew up to be 7 males and 5 females, such a

screwed sex ratio towards males was also reported

in a captive-bred population, although our sample

size is definitely too smail to be conclusive.

Trigonostigma somphongsi were found in a

mixed school with many other small cyprinids,

especially Rasbora borapetensis Smith, 1934,

Amblypharyngodon chulabhornae Vidthayanon et

Kottelat, 1990 and Boraras urophthalmoides

which often form large schools (Fig. 3), some-

times of more than a hundred specimens. These

fishes were found swimming in margin of the

deepwater rice field and in an area with not so

dense aquatic plants. T. somphongsi were found to

be minority in the school with only a few individ-

uals observed. The school was often led by R.

borapetensis (the strongest swimmer), then fol-

lowed by A. chulabhornae with B. urophthalmoi-

des (smallest species) and T. somphongsi at the tail

of the school.

Sometimes the school could be observed eat-

ing suspended food particles stirred up by re-

searchers from the bottom of the floodplain. At

one point, a small crab accidentally stepped on

Figure 1. The female of T. somphongsi is larger (left), the

male (right) shows more intense colors (in breeding tank).

Figure 2. Habitat of T. somphongsi in a deepwater rice

field, flood plains of Bangpakong Basin, central Thailand.

Figure 3. Trigonostigma somphongsi in its natural habitat can

be found in mixed school with many other small cyprinids.

474

Nidsaraporn Petsut et alii

which attracted many of the fish in the area in-

cluding T. somphongsi to come and eat the fresh

prey. Surveys by sein mostly yielded only one T.

somphongsi , if any, among many other individ-

uals of other species; only once during our survey

three individuals turned up.

DISCUSSION

Given that the other 3 species in the genus live

in peat swamps or lowland streams, it is interesting

to find T. somphongsi living in a large river and

migrating to breed in floodplain during the rainy

season. It is highly possible that the range of this

species once occupied most of the central plain of

Chao Phraya River as well as the floodplain of Mae

Klong River, in the west. However, flood control

and lost of habitat have reduced its distribution to

current area. The species appeared to be naturally

low in density in the study area, however the flood-

plain appears to be large enough to support a

healthy population.

Our study showed that the floodplain formed an

integral part to the live cycle of this rare species, it

is thus recommended that the flooding in this area

should be managed so that both human and fishes

can both benefit from it.

ACKNOWLEDGEMENTS

We are grateful to the Research and Develop-

ment Institute Ramkhamhaeng University for finan-

cial support. We also wish to thank the reviewers

for the invaluable editorial advice. We would like

to thank Mr. Thanachai Pangkhamraeng, Mr. Ji-

rawat Polpermpul, Mr. Zhou Hang, Mr. Koji Ya-

mazaki, and Mr. Pavaphon Supanantananont their

for assistance in the fieldwork.

REFERENCES

APHA, AWWA & WEE, 2009. Standard Methods for the

Examination of Water and Wastewater. 18th ed. USA:

American Public Health Association, Washington

D.C., 83 pp.

Baillie J.E.M. & Butcher E.R., 2012. Priceless or

Worthless ? The world’s most threatened species.

Zoological Society of London, 112 pp.

Kottelat M. & Witte K.E., 1999. Two new species of

Microrasbora from Thailand and Myanmar, with two

new generic names for small southeast Asian cyprinid

fishes (Teleostei: Cyprinidae). Journal of South Asian

Natural History, 4: 49-56.

Meinken H., 1958. Mitteilungen der fischbestim-

mungsstelle des VDA. XXIX. Rasbora somphongsi

eine neue Zwergrasbora. Die Aquarien- und Terrarien

Zeitschrift, 11: 67-69.

Petsut N., Kulabtong S. & Petsut R, 2012. Preliminary

survey of biodiversity of aquatic plants in rice field

ecosystem at Upper Bangpakong Basin. Journal of

Faculty of Animal Science and Agricultural Technol-

ogy Silpakorn University, 3: 1-16.

Petsut N., Kulabtong S. & Petsut R, 2013a. Preliminary

survey of freshwater fishes from acid soil area in

upstream of Bangpakong River, Nakhon Nayok

Province, Thailand. Journal of Biodiversity and En-

vironmental Sciences, 3: 33-36.

Petsut N., Kulabtong S. & Petsut R, 2013b. Two new

records of cyprinid fish (Cypriniformes Cyprinidae)

from Thailand. Biodiversity Journal, 4: 411-414.

Petsut N., Kulabtong S. & Petsut R, 2013c. Change of

benthic fauna composition in deepwater rice field

ecosystem. Veridian e-Journal Silpakorn University,

6: 1010-1024.

Petsut N., Kulabtong S. & Petsut R, 2013d. Ecological

structure of plankton communities in acid soil area:

Case study in deep water ricefield ecosystem. The

6th National conference on algae and plankton,

Chiangmai.

Vidthayanon C., 2013. Trigonostigma somphongsi. In:

IUCN 2014. IUCN Red List of Threatened Species.

Version 2014.2. <www.iucnredlist.org>. Downloaded

on 19 September 2013.

Biodiversity Journal, 2014, 5 (4): 475-480

First record of the Caucasus field mouse Apodemus ponticus

Sviridenko, 1936 (Rodentia Muridae) from Iran

Zeinolabedin Mohammadi'*,Jamshid Darvish 1,2 , Fatemeh Ghorbani 1 & Ehsan Mostafavi 3,4

'Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran

2 Rodentology Research Department (RRD), Applied Animal Institute (AAI), Ferdowsi University of Mashhad, Mashhad, Iran

department of Epidemiology, Pasteur Institute of Iran, Tehran, Iran

4 Research Centre for Emerging and Reemerging infectious diseases, Pasteur Institute of Iran, Akanlu, Kabudar Ahang, Hamadan,

Iran

’Corresponding author, e-mail: Mohammadi.zeinal@gmail.com

ABSTRACT This study is the first record of six specimens of Apodemus ponticus Sviridenko, 1936 (Rodentia

Muridae) from the Zagros Mountains, north western Iran. Four external features besides 13

linear measurements of the skull and 14 dental characters were measured. This species was

identified by its extensive and well-marked boundary throat spot. In addition, A. ponticus shows

morphometric characters including head and body length (mean= 90.86±2.54), length of bullae

(mean = 6.34=1=0. 1 1), breadth of bullae (mean = 4.77±0. 12) and dental characters consisting of

maxillary tooth row (mean = 3.85±0.06) and mandibular tooth row (mean = 3.90±0.05) which

are different from the sympatric species A. witherbyi Thomas, 1902. Based on our results, the

distributional range of A. pon ticus extends to oak forests of the Zagros Mountains, west Iran

which is considered to be the easternmost boundary of its range.

KEY WORDS Apodemus ponticus ; sympatric; Zagros Mountains; Iran.

Received 22.09.2014; accepted 18.11.2014; printed 30.12.2014

INTRODUCTION

Caucasus field mouse Apodemus ponticus

Sviridenko, 1936 (Rodentia Muridae) is one of the

most ambiguous members of the genus Apodemus

Kaup, 1829. It was first described from Olginka

Village, northwest Caucasus and supposed to be

endemic to southern Caucasus region (Azerbaijan

and Georgia; Ellerman & Morrison-Scott, 1951;

Musser & Carleton, 2005). Its limit expansion

reaches up to south Russia.

Initially, it had been considered intermediate

hybrid between A. sylvaticus (Linnaeus, 1758) and

A. flavicollis (Melchior, 1834) or included in a

superspecies namely A. flavicollis (Heptner, 1940;

Neithammer, 1978). Vereshchagin (1959) misclas-

sified A. ponticus as a form of A. fulvipectus

(Ognev, 1924). However, subsequent studies in-

dicated that Caucasus field mouse is a separate

species.

Differences between Allozyme-electroforetic

patterns of A. ponticus from A. uralensis (Pallas,

1811) (as A. ciscaucasicus Ognev, 1 924), A. wither-

byi (Thomas, 1902) (as A. fulvipectus) and A. flavi-

collis were described by some authors (Mezhzherin,

1990; Mezhzherin et al., 1992; Lavrenchenlco &

Likhnova, 1995). In addition, some diagnostic

karyological features of A. ponticus were identified

(Kozlovsky et al., 1990; Orlov et al., 1996a, b). The

Caucasus field mouse can be diagnosed from A.

witherbyi by multivariate analysis (Lavrenchenko

& Likhnova, 1995).

476

Zeinolabedin Mohammadi etalii

Although, based on mt DNA cytb gene sequen-

ces, Balakirev et al. (2007) proposed unity between

A. ponticus and A. flavicollis. Suzuki et al. (2008)

clustered it as a sister clade of A. flavicollis based

on trees constructed applying four nuclear and one

mitochondrial genes but with weak support for the

formers.

Until recently five species of wood mice of the

genus Apodemus including the following species:

A. witherbyi, A. uralensis, A. hyrcanicus

Vorontsov, Boyeskorov et Mezhzherin, 1992, A.

flavicollis and A. mystacinus were recorded

(Javidkar et al., 2005; Krystufek & Hutterer, 2006;

Darvish et al., 2010; Darvish et al., 2014) and A.

avicennicus has been described by Darvish et al.

(2006) from Iran.

In this study, the first record of A. ponticus as a

member of murine rodents would be added to the

checklist of rodent fauna of Iran.

MATERIAL AND METHODS

The study was done in Kordestan Province, west

Iran from June 2013 to July 2013, using live-traps

and snack baits (Fig. 1).

Specimens were captured and determined based

on cranial and external morphological features,

using keys including: Mezhzherin et al. (1992) and

Vorontsov et al. (1992). Standard vouchers of spec-

imens (skins, skulls, tissues) were deposited in the

Zoology Museum of Ferdowsi University of

Mashhad (ZMFUM).

Specimens were weighted, sexed and four

external characters were measured; besides, 13

linear measurements of the skull were taken using

a vernier calliper accurate to the nearest 0.05 mm

(Table 1). 14 dental measurements were per-

formed with a measuring microscope to 0.001

mm (Table 1).

Figure 1. Location of the study areas: Zagros Mountains, northwestern Iran.

First records of the Caucasus feld mouse Apodemus ponticus Sviridenko, 1 936 (Rodentia Muridae) from Iran 477

Variables A. ponticus n=6 A. witherbyi n=38

Mean ± SE

Min

Max

Mean ± SE

Min

Max

HBL

89.86±2.54

103

90.40il.18

103

101.33±1.09

104

99.56il.17

117

HFL

22.71±0.47

21.37i0.24

17.43i0.33

15.79i0.28

CBL

24.14i0.34

23.28

25.24

23.31i0.10

21.24

24.72

12.51i0.14

11.94

13.20

12.28i0.05

11.32

12.90

PAL

4.88i0.08

4.58

5.34

4.79i0.05

4.12

5.46

ZYGB

13.18i0.18

12.64

14.02

12.72i0.08

11.40

13.88

4.28i0.082

4.00

4.52

4.43i0.04

3.66

4.84

IOC

4.30i0.07

3.92

4.52

4.33i0.02

4.10

4.66

BCW

11.97i0.11

11.56

12.38

11.70i0.04

11.23

12.32

IBW

11.40i0.13

10.94

11.98

10.98i0.50

10.44

6.21i.09

5.72

6.54

5.94i0.04

5.40

6.38

BCBH

9.42i0.15

8.54

9.88

8.93i0.04

8.34

9.46

TBL

6.34i0.11

5.76

6.78

5.91i0.05

5.32

6.82

TBW

4.77i0.12

4.28

5.22

4.40i0.02

4.08

4.76

11.98i0.33

10.82

13.44

11.57i0.07

10.34

12.52

Ml.L

1.86i.05

1.55

2.08

1.85i.01

1.69

1.96

Ml.W

1.17i0.04

0.92

1.27

1.16i.01

1.02

1.26

M2.L

1.15i0.02

1.06

1.21

1.13i.01

1.03

1.20

M2.W

1.10i0.03

0.94

1.17

l.lli.01

1.01

1.22

M3.L

0.87i0.02

0.82

1.04

0.84i0.01

0.76

0.98

M3.W

0.82i0.03

0.63

0.95

0.81i.01

0.67

0.93

M.1L

1.77i0.02

1.63

1.89

1.66i0.01

1.17

1.78

M.1W

1.04i0.03

0.84

1.13

1.03i0.01

0.88

1.12

M.2L

1.18i0.01

1.11

1.25

1.14i0.01

1.04

1.25

M.2W

1.06i0.03

0.89

1.18

1.04i0.01

0.90

1.19

M.3L

0.96i0.03

0.79

1.05

0.97i.01

0.88

1.06

M.3W

0.89i0.07

0.74

0.96

0.89i0.04

0.80

MxTR

3.83i0.06

3.54

4.14

3.78i0.01

3.54

3.95

MnTR

3.90i0.05

3.68

4.14

3.76i0.01

3.37

3.94

Table 1. External, cranial and dental measurements (in mm) of A. mystacinus and A. witherbyi from northwest of Iran.

478

Zeinolabedin Mohammadi etalii

ABBREVIATIONS. Abbreviations of charac-

ters are as follows (for descriptions of characters

see Frynta et al., 2001; Javidkar et al., 2005, 2007

and Krystufek & Vohralik, 2009): HBL: head and

body length; TL: tail length; HFL: hind foot length;

EF: ear length; CBF: condylobasal length; FF: fa-

cial length; PAF: palatal length; ZYGB: zygomatic

breadth; RW: rostrum width; IOC: interorbital con-

striction; BCW: braincase width; IBW: interbulla

width; RH: height of rostrum; BCBH: height of

braincase with tympanic bulla; TBF: tympanic

bulla length; TBW: tympanic bulla width; ME:

mandible length; Ml.F: length of first upper molar;

Ml.W: width of first upper molar; M2.F: length of

second upper molar; M2.W: width of second upper

molar; M3.F: length of third upper molar; M3.W:

width of third upper molar;M.lF: length of first

lower molar; M.1W: width of first lower molar;

M.2F: length of second lower molar; M.2W: width

of second lower molar;M.3F: length of third lower

molar; M.3W: width of third lower molar; MxTR:

length of maxillary tooth row; MnTR: length of

mandibular tooth row.

RESULTS

Apodemus ponticus is sympatric and syntopic

with A. witherbyi at 1545 m (a.s. 1.) in the western

slopes of the Zagros Mountains. This species was

identified by its extensive and well-marked bound-

ary throat spot.

The length of sole is more than 2 1 mm. A. pon-

ticus shows morphometric characters including

head and body length (mean= 90.86±2.54), length

of bullae (mean = 6.34±0.11), breadth of bullae

(mean = 4.77±0.12) and dental characters consis-

ting of maxillary tooth row (mean = 3.85±0.06) and

mandibular tooth row (mean = 3.90±0.05) which

are different from the sympatric species A. wither-

byi (Table 1).

DISCUSSION

The Zagros Mountains is a part of the Irano-

Anatolian hotspot, one of the richest biodiversity

and endemicity hotspot regions in the world (Mit-

termeier et al., 2012). Irano- Anatolian hotspot also

encompasses the Ponto-Caspian realm including

the regions between Black and Caspian Sea and

southern coast of Caspian Sea proposed the

refugial area for evolution of some endemic lin-

eages of rodents such as Glis glis (Finnaeus, 1766)

(Naderi et al., 2013) and some insectivores (Dubey

et al., 2007a; Dubey et al., 2007b).

In addition, terrestrial exchange is partially con-

ceivable via some corridors (i.e. Aras River valley;

Missone, 1959) between the region and the Cauca-

sus hotspot where the Caucasus field mice were

supposed to be endemic.

The Caucasus field mice are sympatric with

congener species A. witherbyi and A. mystacinus in

Kordestan province. A. ponticus is syntopic with

A. witherbyi in bushy foothills of the Zagros Moun-

tains in 1545 m (a.s.l.) however; it has not been

collected with A. mystacinus at the same altitude.

So, the Caucasus field mice could pass the Aras

valley and establish the populations in the Zagros

Mountains.

Moreover, the Zagros Mountains are the south-

ernmost boundary of the distributional range of the

species. Finally, the Caucasus field mice from Iran

show lower average in size (i.e. CBF =24.14;

MxTR=3.83) comparing to that of specimens re-

ported from Caucasus (CBF =25.53;MxTR=3.98)

and the minimum of the foot length (21 vs 22.5);

based on measurements published by Vorontsov et

al. (1992).

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Biodiversity Journal, 2014, 5 (4): 481-498

Little effect of ecological factors and symbiotic specificity on

the distribution of Medicago subsect. Intertextae (Urban) Heyn

(Fabales Fabaceae) in the Mediterranean Basin

Meriem Laouar & A'l'ssa Abdelguerfi

Ecole Nationale Superieure Agronomique, Belfort, El Harrach 16200 Alger, Algerie; e-mail: laouar_m@yahoo.fr

■"Corresponding author

ABSTRACT In the Mediterranean region, Medicago granadensis Willd. and M. muricoleptis Tineo (Fabales

Fabaceae) of the Intertextae subsection are rare and present, each one in well defined areas,

whereas the others taxa, in the same subsection, M. ciliaris (L.) All. and M. intertexta (L.)

Mill., are more frequent with large distribution. This kind of geographical distribution is not a

coincidence; certainly different factors are the origin of this distribution. In 125 sites of different

Mediterranean countries, the ecology of the four taxa was studied, 34 trapped strains in one

site of Intertextae rhizobiums were characterized by rep-PCR and some symbiotic tests were

carried out. The results confirm that M. muricoleptis and M. granadensis are endemic in the

north and east of the Mediterranean, respectively; whereas, M. ciliaris and M. intertexta are

widespread. Although their geographic specificity, the four taxa showed no important differ-

ences in ecological conditions. M. muricoleptis, given its presence in the north of the Mediter-

ranean only, is distinguished by its precipitation requirement. By inference, the absence of M.

muricoleptis and M. granadensis in some regions is not due to the absence of the symbiont.

We confirm the symbiotic specificity of Sinorhizobium medicae (Rome, 1996) for the

Intertextae subsection and the existence of coevolution between taxa (widespread and endemic)

and rhizobia. We suppose that endemic taxa are in the process of allopatric speciation, which

explains their narrow distribution in the Mediterranean Basin.

KEY WORDS Distribution; diversity; ecology; Intertextae', Medicago', Mediterranean; symbiosis.

Received 15.10.2014; accepted 18.11.2014; printed 30.12.2014

INTRODUCTION

Legumes hold an important economic and social

place and have a definite environmental benefit in

the Mediterranean Basin, which is the area of dis-

tribution of several genera of this family, including

the Medicago L. genus. This genus includes 86

species (Small & Jomphe, 1989) and comprises sev-

eral sections and subsections, including the Inter-

textae (Urban) Heyn subsection (Small, 2011;

Coulot & Rabaute, 2013). Some taxa of the Inter-

textae show a morphological ambiguity, which

reflected in different classifications. Indeed, some

authors ascribe to the subsection 4 species, namely,

Medicago ciliaris (L.) Kroclc., M. intertexta (L.)

Mill., M. muricoleptis Tineo and M. granadensis

Willd. (Quezel & Santa, 1962; Lesins & Lesins,

1979; Small & Jomphe, 1989; Coulot & Rabaute,

2013) and others mention only 3 species, M. inter-

texta, M. muricoleptis and M. granadensis (Heyn,

1963; Ponert, 1973; Jauzein, 1995; Dobignard &

Chatelain, 2012; Tison et al., 2014). According to

482

Meriem Laouar & Aissa Abdelguerfi

the latter authors M. ciliaris is either a subspecies,

M. intertexta subsp. ciliaris (L.), Ponert, or a botan-

ical variety [M. intertexta var. ciliaris (L.) Camb,

Heyn] of M. intertexta.

The early observations on the distribution of

annual Medicago in relation with soil factors were

made by Trumble & Donald (1938) and Aitken &

Davidson (1954). Besides, the first work on autoe-

cology was carried out in Australia by Andrew &

Hely (1960). Thereafter, several studies were

performed, particularly in the regions of origins of

Medicago , which allowed the definition of the eco-

logical requirements of various species (Ab-

delguerfi et al., 1988; Ehrman & Cocks, 1988; Pros-

peri et al., 1989; Ehrman & Cocks, 1990; Abdelkefi

et al., 1992; Bounejmate, 1992; Bounejmate et al.,

1992a; 1992b).

For the most common taxa of the Intertextae

subsection, M. ciliaris and M. intertexta , autoe-

cology research was carried out, but most of that

research did not allow comparisons between the

two taxa since they were included in a single

species as indicated by Heyn (1963). The most spe-

cific study on these two taxa was carried out in Al-

geria (Abdelguerfi-Laouar et al., 2003) on 179 sites.

Besides, M. muricoleptis and M. granadensis are

poorly distributed and are reported in the literature

as rare taxa. Although they belong to the same sub-

section as M. ciliaris and M. intertexta , they are not

found in Algeria, Morocco, and Tunisia. The eco-

logical requirements of the two taxa are not yet

determined; they have only been reported in various

regions (Table 1).

Other factors, besides ecological ones, symbio-

sis for example, may affect the distribution of

legumes species. The species of rhizobia that nodu-

late the Medicago ssp. belong to the Ensifer (for-

merly Sinorhizobium ) genus and are S. meliloti

(Dangeart, 1926) and S. medicae (Rome, 1996).

One of the major characteristics of the rhizobium-

legume association is their host specificity. In gen-

eral, a given rhizobium species can only establish

an efficient symbiotic relationship with a limited

number of plant partners. Similarly, legumes

species can only be specific to a certain number of

rhizobium species. This coevolution is often ig-

nored in studies on the distribution and evolution of

legumes taxa. The Intertextae subsection taxa were

described as specific to S. medicae (Bena et al.,

1998; 2005). Bena et al. (1998) suggest, for this

subsection, a recurrent loss of the capacity to form

an efficient symbiosis with strains of the S. meliloti

species; they hypothesize a punctual mutation

inducing a modification of the mechanisms of

recognition such as the flavonoid structure.

The rather particular geographical distribution

of the four Intertextae subsection taxa, namely

those with a wide distribution and those with a

narrow distribution, needs clarification as to

whether this is due to an ecological adaptation

and/or to a specific taxon-rhizobium interactions;

this is the objectives of this work.

MATERIAL AND METHODS

Given the taxonomic ambiguity that exists

within the subsection of the Intertextae , we will use

the term taxon instead of species for M. ciliaris ;

synonym: M. intertexta subsp. ciliaris and M. inter-

texta var. ciliaris, M. intertexta, M. muricoleptis and

M. granadensis throughout the document.

Ecological data and origin of sites

The study is focused on taxa M. ciliaris, M.

intertexta, M. muricoleptis and M. granadensis. The

collected ecological data come from the Australian

Medicago Genetic Resource Centre (South Austra-

lian Research and Development Institute: SARDI),

a total number of 125 sites were surveyed in 17

Mediterranean countries and islands (Table 2). 13

sites of 125 are sympatric (sci and sig), one of

which is sympatric to M. intertexta and M. granaden-

sis (sig; Israel) and the other (12) are for M. ciliaris

and M. intertexta (sci). All the other sites are al-

lopatric (sc, si, sm and sg) and correspond only to a

species per site among the four (Table 3).

Ecological data analysis

Nine (9) ecological characters were studied;

they correspond to orographic (altitude and slope),

climatic (annual rainfall) and edaphic characters

(pH, soil texture, soil depth, soil reaction, type of

drainage and land use). Analyses of variance

(ANOVA) with a single factor (sites) were carried

out on 76 sites whose data on rainfall, altitude, and

pH were available; the 'site' factor was considered

as random effect. The software used is STAT-ITCF

Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 483

Species

Regions

M. Lilians (L.) All.

- Macaronesia

Madeira Island (Portugal), Canary Island

(Spain)

- North Africa

Algeria, Egypt, Morocco, Tunisia

- Western Asia

Cyprus, Iraq, Israel, Lebanon, Western

Syria, Western Turkey

- South-Eastern Europe

Greece (including Crete), Italy (including

Sardinia and SicilvJ

- South-Western Europe

France (including Corsica), Portugal and

Spain (including the Balearic Islands)

- Macaronesia

Canary Island (Spain)

- North Africa

Northern Algeria, Morocco, Tunisia

M. intertexta (L.)

- South-Eastern Europe

Mill.

Greece, Italy (including Sardinia and

Sicily)

- South-Western Europe

France (including Corsica), Portugal and

the South of Spain

M. granadensis

Willd.

- North Africa

Northern Egypt

- Western Asia

Israel, Lebanon, Jordan, Western Syria,

Turkey

- South-Eastern Europe

M. muricoleptis

Southern Italy (including Sicily)

Tineo

- South-Western Europe

Southeast of the France near Toulon

References

Coulot & Rabaute, 2013

Davis, 1965-1988

Dobignard & Chatelain,

2012

Heyn, 1963

Jahandiez & Maire, 1931-1 941

Lesins & Lesins, 1 979

Meikle, 1977-1985

Mouterde, 1966

Pignatti, 1982

Pottier-Alapetite, 1979-1981

Quezel & Santa, 1962

Small & Jomphe, 1989

Small, 1981

Small et al., 1 98 1

Smyth ies, 1984-1986

Tackholm, 1974

Townsend & Guest, 1966

Tutin et al., 1 964- 1980

Zohary & Feinbrun- Dothan,

1966

GRIN, 2014

Table 1 . Geographical distribution of the Intertextae subsection taxa.

(Gouet & Philippeau, 2002). For each quantitative

variable, two analyses of variance were carried

out; the first analysis comprised 4 levels corre-

sponding to the presence of the taxon: (i) site of

M. ciliaris (sc+sci), (ii) site of M. intertexta

(si+sci), (iii) site of M. muricoleptis (sm) and (iv)

site of M. granadensis (sg+sig); the second analy-

sis (5 levels) differed from the first by the distinc-

tion of allopatric sites (12) from sympatric sites

for M. ciliaris and M. intertexta. For only those

where the null hypothesis is rejected a Fisher's

LSD test was calculated. The hypothesis is null

when the F test (MS A/MSE) of ANO VA is greater

than 1 (p <0.05).

For the qualitative variables, environmental pro-

files were established for each taxon having more

than five sites; the classes of each variable are rep-

resented in Table 4.

484

Meriem Laouar & Aissa Abdelguerfi

M.ciliaris : Algeria: 5.776 - 10.464 - 10.465 - 10.642 - 10.643 - 10.644 - 10.645 -

10.648 - 10.792 - 10.932- 10.933 - 10.934 - 10.935 - 10.936 - 11.571 - 11.574 -

11.575 - 11.576 - 12.547 - 12.551 . Crete : 2.081. Cyprus: 23 .627 - 23.629 - 23.635 -

23.636. Greece: 2.239. Israel: 2 .004 - 7.687 - 7.688. Italy: 2.075 - 5.782 - 22.419 -

22.420. Morocco: 25 .506 - 25.506 - 29.024. Portugal: 7.826 - 24.554 - Sardinia

26.016. Sicily: 2.067 - 2.186 -24.831 -24.844 - 24.847 - 24.849 - 24.852 - 24.853.

Spain: 7.721 - 28.255 - 28.256. Syria: 22 .206 - 24.022 - 24.023. Tunisia: 5.785 -

5.786 - 7.714 - 7.723 -10.637 - 18.460 - 18.463 - 18.464 - 20.104 - 21.802 - 21.803 -

21.804. Turkey: 23.932.

M intertexta : Algeria: 4.010 - 10.647 - 10.649 - 10.650 - 10.651 - 10.652 - 10.659 -

10.788 - 10.791 - 11.579 - 11.580 - 11.909 - 11.910 - 11.911 - 11.912 - 15.748.

Cyprus: 2.367 - 2.370 - 5.777. Egypt: 13.797 - 13.799. France: 2.044 - 2.045. Israel:

1.589 - 2.363 - 2.364 - 2.366 - 5.779. Italy: 2.071 - 2.375. Jordan: 18.084 - 19.002.

Morocco: 10.662. Portugal: 2.372 - 2,377 - 5.783 -8,323. Sardinia: 12.302 - 26.021.

Sicily: 24 .816 - 24.819 - 24.821 - 24.823 - 24.824. Spain: 1.590 - 2.361 - 2.362 -

28.257. Syria: 13.795 - 13.796. Tunisia : 4 .008 - 4.011 - 5.489 - 7.724 - 18.465

18.466.

M. granadensis : Israel: 2.359 - 5.778 - 5.822. Syria: 13.818 - 13.819 - 22.207.

Turkey: 23.928 -23.931 -26.380.

M. muricoleptis: Greece: 22.423. Italy: 15.343 - 22.422. Sicily: 24.825 - 25.026 -

25.027 -25.002.

Table 2. Collec-

tion of S ARDI.

Country

Allopatric sites

Sympatric sites

Total

M. ci liar is

(sc)

M. intertexta

(si)

M. muricoleptis

(sm)

M. granadensis

(sg)

M. ciliaris-

M. intertexta

(sci)

M. intertexta -

M. granadensis

(sig)

Algeria

Crete

Cyprus

Egypt

Spain

France

Greece

Israel

Italy

J ord an

Morocco

Portugal

Sardinia

Sicily

Syria

Tunisia

Turkey

Total

125

Table 3. Num-

ber of allopatric

and sympatric

sites by coun-

try.

Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 485

Collection of rhizobium strains

In a homogeneous site in Algiers (sub-humid,

soil with loamy texture and slightly alkaline pH),

8 populations, two by taxon, were planted. The pop-

ulations of M. granadensis and M. muricoleptis

originate from the Mediterranean collection

(SARDI) and those ofM ciliaris and M. intertexta

originate from an Algerian collection (ENS Ad’ Al-

ger). Populations ofM ciliaris (C58) and M. inter-

texta (158) from a sympatric site were taken into

account. On the generated seedlings, nodules were

collected from which a collection of 34 strains of

rhizobia was obtained (Table 5). Bacterial isolates

were obtained using the crushed-nodule method

(Vincent, 1970) from nodules removed from 60

days old plants. The various strains were stored in

glycerol at -80 °C, after having been identified by

a symbiotic test on M. polymorpha, in addition to

the analysis of 16S rRNA sequences (Rome et al.,

1996).

Extraction of DNA, Amplification by REP-

PCR and method of analysis

The DNA extraction was conducted following

the protocol of Abdelguerfi-Laouar (2005). The rep-

PCR and BOX-PCR was completed according to

the protocol of Rademaker et al. (1998). A primer

for BOX-PCR (BOX AIR: 5’-CTACGGCA-

AGGCGACGCTGACG-3’) and two primers for

REP-PCR (REP 1R: 5 MIIICGICGICATCIGGC-3 ’

and REP 21: 5MCGICTTATCIGGCCTAC-3’) were

used (Versalovic et al., 1994). The visualization of

bands was made by UV on long agarose gels at 1 .5

% (0.5X TBE) at 90 V voltage.

The binary data were established on the basis

of the presence (1) absence (0) of bands of REP

and BOX markers. From these data, a tree of

genetic distance was obtained by groupings of

plant from a comprehensive comparison of charac-

ters, then by calculating the mean distances of

grouped plants (NJ method: Neighbour Joining).

Support for clustering was determined by bootstrap

procedure applied on binary REP-BOX data (1000

replications). The software used is Dissimilarity

Analysis and Representation for Windows (DAR-

win) (Perrier et al., 2003; Perrier & Jaquemoud-

Collet, 2006).

Symbiotic Test

The two species S. meliloti and S. medicae rep-

resented by a 2011 strain and two ABS7 strains

(Bekki et al., 1987) and USDA1827, respectively,

were inoculated on the populations of the four taxa

of the Intertextae subsection. For symbiotic tests we

kept the same host populations that served to obtain

the collection of rhizobium. The seeds were disin-

fected with sulphuric acid for 30 minutes and then

germinated after flushing. After germination, each

seed was transferred, in sterile conditions, in tubes

containing the FAHRAEUS agar medium (1.5 %)

and placed in a culture chamber (20 °C, 60 % rela-

tive humidity and a photoperiod of 1 6 h light and 8

h darkness). The inoculation was carried out after

48 h of development of the roots (0.3 ml/seedling).

The notations begin after a week and end after 90

days. The experimental protocol used for the sym-

biotic tests is total randomization with three plants

per population.

RESULTS

Frequencies and geographical distribution

of taxa

The most frequent taxon of the Intertextae sub-

section in the Mediterranean region is M. ciliaris

with a frequency of 47.8 % followed by M. inter-

texta (40.6 %) and, finally, M. granadensis (6.5 %)

and M. muricoleptis (5.1 %). Of 17 Mediterranean

countries and islands, Algeria has the highest

frequency for M. ciliaris and M. intertexta. From

figure 1, which represents the distribution of 121

sites (longitude and latitude data available), M.

muricoleptis and M. granadensis are confined in

two restricted and different regions: the North and

the East of the Mediterranean, respectively. These

two taxa are included in the area of distribution of

M. ciliaris and M. intertexta.

By comparing the presence of taxa by countiy

between the bibliographic data (Table 1) and the

collection studied (Table 2, Fig. 1) similarities and

differences can be noted. In the Collection SARDI,

M. ciliaris was not collected in Egypt, Iraq, France,

and Lebanon; the same is true for M. intertexta in

Crete, Greece and Turkey. M. muricoleptis was not

collected in France and M. granadensis was not col-

486

Meriem Laouar & Aissa Abdelguerfi

lected in Egypt, Jordan, and Lebanon. Contrarily to

the literature, M. ciliaris andM intertexta were col-

lected in Israel; M. intertexta was collected in

Egypt, Cyprus, and Jordan; these two taxa therefore

exist in these countries.

Inter-taxa ecological variability

Rainfall, altitude and pH

The comparison among M. ciliaris, M. inter-

texta, M. muricoleptis and M. granadensis shows

that, with regard to altitude and pH, few differ-

ences exist (Table 6). Only rainfall allows differ-

entiating between the sites of M. ciliaris, M.

intertexta, sympatric sites (M. ciliaris and M.

intertexta ) (Table 7), M. granadensis and the sites

of M. muricoleptis. This latter taxon prefers the

highest rainfalls that exceed 800 mm. M. granaden-

sis has the lowest rainfall average of all the sub-

section.

To have an idea about the limits of adaptation

of each taxon, minimum and maximum values of

each character and each taxon were taken into con-

siderations. M. intertexta shows very broad adap-

tation for its precipitation needs; it shows the

biggest amplitude with 850 mm (Fig 2). It manages

to grow in dry conditions (150 mm, a single site in

Jordan) as well as in very wet conditions (1000

mm), but given the average for this character, it is

more frequent in the rainy areas. M. granadensis

and M. ciliaris are the least demanding in terms of

precipitation. M. muricoleptis is water demanding

as it is only found in sites with more than 700 mm

of rainfall (Fig 2). In altitude, minimum and maxi-

mum values are very close in the four taxa; they

vary from 5 to 10 m for low altitudes and from 900

to 1000 m for higher values. Sympatric sites of M.

ciliaris and M. intertexta show an average rainfall

closer to the average for M. intertexta than to the

average for M. ciliaris.

Edaphic characters (Texture, drainage,

depth of soil and soil reaction)

The soil textures in the sites of the four taxa are

fine; they are clayey or clay-loam. The loamy tex-

ture is specific only to M. ciliaris, M. intertexta and

M. granadensis (Fig. 3). The Intertextae taxa are

found both in soils with good water drainage and

soils where water stagnates on the surface. Only M.

intertexta shows 100%, in relative frequency, for

the class of submerged soil (waterlogged) (Fig. 4)

it is the only taxon that was not mentioned in the

W1C

N43

8 6 4 2 0 2 4 6 8 10 12 14 16 18 20 21 22 24 26 28 30 32 34 36 38E

c i

c m

c i

cig

•g

Figure 1. Geographical distribution of Intertextae subsection taxa (121 sites) by longitude and latitude. The rectangle is 1 x

2 degrees [1 line: North Latitude (N: 3 1 to 42); 2 column: East Longitude (E: 0 to 38) and West (W: 0 to 10)]. Abbreviations

: c, M. ciliaris ; i, M. intertexta', g, M. granadensis', m, M. muricoleptis.

Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 487

Figure 2. Minimum, average, and maximum values of annual average rainfalls by taxon.

class with more than 40 cm of depth (Fig. 5). M.

ciliaris and M. intertexta can develop in soils that

are not very deep (10 cm). M. muricoleptis and M.

granadensis prefer deep soils.

M. granadensis does not seem to withstand

soil salinity considering its total absence in this

type of soil (Fig. 6). Owing to the absence of data

on soil reaction, M. muricoleptis was not studied.

Although this data is qualitative, ecological pro-

files confirm the resistance of M. ciliaris and M.

intertexta to salts as they are present in various

sites qualified as salty. Although the variance anal-

ysis did not highlight significant differences for

the pH, from ecological profiles of the soil reac-

tion character (Fig. 6) there are preferences de-

pending on the taxon. All of the three taxa M.

ciliaris , M. intertexta and M. granadensis grow

on alkaline soils. M. granadensis is the only one

present in sites with neutral soils and M. intertexta

confirms its presence on acid soils. Acid soils,

with a pH of 5, characterize only a few sites of M.

ciliaris and M. intertexta. By contrast, neutral and

alkaline soils are suitable for the four taxa of the

subsection.

Slope and Land Use

M. ciliaris and M. intertexta prefer flat grounds

in contrast to M. granadensis , which prefers slop-

ing grounds (16-30%). M. muricoleptis is interme-

diary with a preference for flat to undulating

ground (Fig. 7). The four taxa of the Intertextae

subsection are found in cultivated and grazed soils

and only M. ciliaris, M. intertexta andM granaden-

sis are found on roadsides (Fig. 8). M. ciliaris and

M. granadensis are more frequent on roadsides and

M. intertexta is more frequent in cultivated lands.

Unlike other taxa, M. muricoleptis is found more

often in pastures.

Symbiotic responses

The endemic taxa, M. muricoleptis and M.

granadensis, just as the taxa of M. intertexta and M.

ciliaris, are exclusively nodulated, in Algeria. The

inoculation of 34 trapped strains of rhizobia on M.

polymorpha showed an efficient nodulation

Nod+/Fix+ on all tested plants. This result confirms

that all collection of rhizobium is S. medicae.

488

Meriem Laouar & Aissa Abdelguerfi

Figures 3-8. Ecological profiles indicate the relative frequency of the taxon in the different classes (for class limits see

Table 4). Figure 3: soil texture. Figure 4: soil drainage. Figure 5: depth. Figure 6: soil reaction. Figure 7: slope. Figure

8: land use.

Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 489

The inoculation of the reference strain 2011 S.

meliloti shows that onM truncatula (A17) all the

plants nodulate and are efficient. No taxon of the

Intertextae nodulated efficiently with this strain. M.

ciliaris and M. intertexta do not show any nodule.

M. ciliaris offers the highest percentage of bumps

and M. granadensis shows the highest percentage

of Nod-. In M. granadensis and M. muricoleptis

non efficient nodules were formed on a small num-

ber of plants (Fig. 9). The strain ABS7, obtained

from M. ciliaris, nodulates efficiently, without ex-

ception, all the plants of the Intertextae subsection.

Variables

Abbreviation

Class codes

Classes

Texture

Tex

Texl-Tex3

Clay, loamy, loamy -clay

Drainage

Drn

Drnl-Drn4

Good soil drainage, free flow, Stagnation in

surface. Submersion

Depth (cm)

Dpth

Dpthl -Dpth3

0-1 0, 20-40 and +40 cm

Soil Reaction

Ret

Rctl -Rct4

Acidic, Neutral, Alkaline, Saline

Slope (%)

Sip

Sip 1-Slp3

0-3 % Flat, 3-8 % hilly, 16-30 % sloping

Land Use

LU1-LU3

Crops, grazing, roadside

Table 4. Upper Limits of qualitative variable classes used for ecological profiles.

Taxon

Population

Code

Altitude

(m)

Rainfall

(mm)

Origin

Rhizobia Strains

M. ciliaris

DZ.C242

242

980

450

Algeria

3 Strains: DZ.c242.G3.1 ; DZ.c242.G3.2 ;

DZ.c242.G3. 3

M. ciliaris

DZ.C58

860

649

Algeria

3 Strains: DZ.c58.G1.2, DZ.c58.G1.4,

DZ.c58.G 1.5

M. intertexta

DZ.I331

331

880

1053

Algeria

5 Strains: DZ.i331 .G2.1 ; DZ.i33 1.G2.2;

DZ.i33 1.G2.3 ; DZ.i33 1.G2.4 ; DZ.i331.G2.5

M. intertexta

DZ.I58

860

649

Algeria

5 Strains: DZ.i58,G2.1, DZ.i58.G2.2,

DZ.i58.G2.3, DZ.i58.G2.4 DZ.i58.G2.5

M. granadensis

DZ.GAUS98

5.822

200

550

Israel

5 Strains: DZ.GAUS98.1.1, DZ.GAUS98. 1.2,

DZ.GAUS98.1.3, DZ.GAUS98.1 .4,

DZ.GAUS98.1.5,

M, granadensis

DZ.GAUS105

23.928

950

600

Turkey

5 Strains: DZ.GAUS 105. 1. 1, DZ.GAUS 105. 1.2,

DZ.GAUS 1 05. 1 .3, DZ.GAUS 1 05. 1 .4,

DZ.GAUS 105. 1. 5

M. muricoleptis

DZ.MAUS.l 10

24.825

630

800

Sicily

5 Strains: DZ.MAUS.l 10. 1 .1 , DZ.MAUS. 1 10. 1.2,

DZ.MAUS.l 10.1 .3, DZ.MAUS.l 10.1.4,

DZ.MAUS.l 10.1.5

M. muricoleptis

DZ.MAUS.107

25.028

700

Italy

3 Strains: DZ.MAUS.107. 1 .1 DZ.MAUS.107,1.3,

DZ.MAUS. 107. 1.4

Table 5. Collection of 34 rhizobia of Intertextae obtained by trapping.

490

Meriem Laouar & Aissa Abdelguerfi

Factors

Rainfall

Altitude

Sites

Number

of sites

Average

(mm)

Number

of sites

Average

(m)

Number of

sites

Average

M. ciliaris

(sc+sci)

585.88 b

278.24

7.98

M. intertexta

(si+sei)

621.83 b

249.50

7.73

M. granadensis

(sg)

530.00 b

398.00

7.90

M. muricoleptis

(sm)

835.71 a

333.57

7.17

Meaning

* *

LSD = 1.996

Table 6. Comparison between environmental factors of the sites of Medicago ciliaris, M. intertexta, M. granadensis andM

muricoleptis. The letters a and b: indicate average groups. P(t), t-test on the groups of average [ * * * : p < 0.001; * * : P <

0.01; * : P< 0.05 ;n.s:P> 0.05 ].

Factors

Rainfall

Altitude

Sites

Number

of sites

Average

(mm)

Number

of sites

Average

(m)

Number,

of sites

Average

M. ciliaris (sc)

571.82 b

288.41

7.84

M. intertexta (si)

628.61 b

242.78

7.20

M. granadensis (sg)

530.00 b

398.00

7.90

M. muricoleptis

(sm)

835.71 a

333.57

7.17

Mixed M. ci-M. ini

(sm)

611.67 b

259.58

8.60

Meaning

* *

LSD = 1.98

Table 7. Comparison between environmental factors (3) of sites with Medicago ciliaris alone, M. intertexta alone, M.

granadensis , M. muricoleptis and mixed sites withM ciliaris and M. intertexta. The letters a and b: indicate average groups.

P(t), t-test on the groups of average [ * * * : p < 0.001; * * : P < 0.01; * : P < 0.05 ; n.s: P > 0.05 ].

By contrast, USDA1827 (obtained from M. trunca-

tula) nodulates neither M. muricoleptis nor M.

granadensis. It nodulates one population of each

taxon of M. intertexta and M. ciliaris. Indeed, the

USDA1827 is specific within the species M. trun-

catula, for it nodulates some populations and not

others.

Genetic diversity of the trapped rhizobia

The electrophoresis of rep-PCR and BOX-PCR

revealed 114 bands (we only took intense bands) of

which 45 are monomorphic and the remainder is

made up of polymorphic bands. Polymorphism is

more frequent in M. granadensis strains with 55.5%

Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 491

of polymorphic bands, followed by M. intertexta

strains (50%); it is less than 25% in the other taxa.

We did not find specific bands that differentiate the

strains of the 4 taxa. Genetic distances (Fig. 10)

show a structuring of the strains of S. medicae by

forming 2 different groups. The first group (Gl)

corresponds to the strains that nodulate M. ciliaris

and M. intertexta and the second group (G2) is the

one trapped in M. granadensis and M. muricolep-

tis. There are 2 strains of M. granadensis of the

population DZ.GAUS98, which come together

with those of M. intertexta. Symbiotic specificity

is clearly established among widespread taxa and

endemic ones.

DISCUSSION

Geographic distribution

In the Mediterranean Basin, the four taxa, which

have a close relationship (Rose et al. 1988), show

different types of distributions: (i) endemic and rare

represented by M. granadensis and M. muricoleptis,

(ii) widespread and common represented by M.

ciliaris and M. intertexta. These results confirm

those obtained by several authors (Table 1). The

new data is that M. ciliaris and M. intertexta are

present in other countries that were never men-

tioned before in the literature. M. ciliaris is present

in Israel and M. intertexta in Israel, Egypt, Cyprus,

and Jordan. M. ciliaris is the most frequent in the

Mediterranean basin and particularly in Algeria. In

this country, this taxon is ranked fifth (163

sites/564) (Abdelguerfi, 2002).

Contrary to M. ciliaris, in the south west of the

Mediterranean M. intertexta is rare; it is absent in

the Northwest of Algeria and in the arid areas

(Abdelguerfi-Laouar et al., 2003). M. muricoleptis

is present in very restricted areas, Toulon in France

and Sicily in Italy. Nevertheless (according to

Coulot & Rabaute, 2013), the presence ofM muri-

coleptis in Toulon (France) is accidental, endemic

in the north Mediterranean, from the south of Italy

to Greece and M. granadensis is more confined to

western Asia, endemic in the East of the Mediter-

ranean and only adventitious in Europe and Chile.

Contrary to what mentioned by Small et al. (1999),

M. granadensis coexists with M. intertexta as the

two taxa were found together on a site.

Ecological requirements

M. muricoleptis is the most demanding water of

the Intertextae. Its geographic distribution corre-

sponds perfectly with this need. In Morocco, M.

intertexta and M. ciliaris were found only in the

areas with high rainfall and are confined to the areas

with mild winter and summer (Bounejmate et al.,

1992a, 1992b; Bounejmate, 1996). This does not re-

flect their requirement in the Mediterranean basin.

The Intertextae is known for its preference for

heavy and humid soils (Small et al., 1999). In

Algeria, M. ciliaris, M. intertexta, M. rigidula and

M. scutellata prefer heavy soils and M. ciliaris

grows particularly on marly soils (Abdelguerfi,

2002). Considering the specificity of the texture of

the Intertextae, the taxa should withstand soils with

poor water drainage. Indeed, the results show that

the taxa are found both in soils with good water

drainage and soils where water stagnates on the sur-

face. M. intertexta is the most adapted to hydromor-

phic soils, is considered one of the most tolerant to

waterlogging of the Annual Medicago genus (Fran-

cis & Poole, 1973). The waterlogging and salinity

are associated characters in the Mediterranean basin

(Kepner et al., 2005). The tolerance of plants to this

condition is due to a combination of anatomical,

physiological and morphological adaptations

(Predeepa-Javahar, 2012). OnlyM ciliaris and M.

intertexta are present in salt soil. Therefore we may

conclude that these two taxa are adapted to salinity.

Indeed, genotypes originating from salty soils are

often considered as tolerant, that is the conclusion

of Ben Salah et al. (2010) when they compared

under saline conditions (100 mmol of NaCl) two

pure lines originating from two different sites, one

rich in salt, and the other poor.

In Morocco, Bounejmate et al. (1992a; 1992b;

1994) and Bounejmate (1996) found the two taxa

in soils low in phosphorous, hydromorphic and

salty. According to Abdelkrim (1995), M. ciliaris is

found in fallows and idle lands with soils that are

colluvial, heavy, mostly marly and clayey, poorly

drained and more or less salty. M. ciliaris is classi-

fied as glycophyte and found in association with

halophyte species (Abdelly et al, 2006; Merabet et

al., 2006; Barret-Lennard & Setter, 2010). Other

research confirmed the adaptation of these taxa to

salinity (Greenway & Andrew, 1962; Lachaal et al.,

1995; Cherifiet al., 2011).

492

Meriem Laouar & Aissa Abdelguerfi

M. truncotulo

M. granodensis

M. muricoleptis

M. intertexta

M. ciliaris

0 % 20 % 40 % 60 % 80 % 100 %

■ Nod+/Fix-

l Nod+/fix+

lj Nod-

B Bump

Figure 9. Symbiotic responses to the inoculation of the reference strain 2011 S. meliloti in the taxa of the Intertextae sub-

section. Abbreviations : Nod +, nodulating phenotype; Nod + /fix+, nodulating phenotype-fixer; Nod-, non nodulating

phenotype; Bump, non nodulating root bulge.

Figure 10. Un- weighted neighbour-joining tree based on the simple matching dissimilarity matrix of REP and BOX markers

across the 34 strains of rhizobia trapped in a common site to all taxa in the subsection Intertextae. The numbers on the tips

indicate bootstrap values (expressed in percentages) and are shown for all clusters with >50 % bootstrap support. Abbre-

viations: c, M. ciliaris ; i, M. intertexta', m, M. muricoleptis', g, M. granadensis .

Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 493

Furthermore, some studies have shown that the

frequency of M. intertexta diminishes when the

pressure of pasture increases (Piano, 1987). Piano

et al. (1991) noted thatM ciliaris andM intertexta

are more frequent in cultivated lands.

Symbiotic response of M. granadensis and

M. muricoleptis in an exotic site

The various populations of M. granadensis and

M. muricoleptis nodulated efficiently in the Alge-

rian common site. The fact that M. granadensis

and M. muricoleptis nodulated efficiently with

rhizobia natives of Algeria, shows that their ab-

sence is not related to a restrictive coevolution

plant-rhizobium in this region. On some species,

particularly cultivated ones, a clear evolution was

noted between the species and its symbiote and

one of the more interesting examples is the pea,

which may form an efficient symbiosis with

strains of rhizobium from its site of origin in Tur-

key, but not with strains from other parts of this

country (Lie et al., 1987).

Taxonomic determination of the trapped

collection of Rhizobia

M. muricoleptis , M. granadensis, M. intertexta

and M. ciliaris are exclusively nodulated by the

strains of S. medicae, which confirms the results of

Bena et al. (1998) on the Intertextae subsection and

the results of Zribi et al. (2007) on M. ciliaris.

Indeed, in the trapping site, there were different

species of Medicago that were only nodulated by S.

meliloti including species of the Melilotus Mill,

genus. This confirms the specificity between the

subsection of the Intertextae and S. medicae. A re-

cent study (Epstein et al., 2012), comparing the two

genomes of S. medicae and S. meliloti, showed that

horizontal exchanges were almost exclusively of

plasmid genes and that the divergence between the

two species resulted from episodes of recent selec-

tion pressures.

Maybe it is not very correct to believe that this

specificity, whether for M. polymorpha or the sub-

section of the Intertextae, is related only to the host.

Indeed, other mechanisms affect the chemical struc-

ture of the synthesized Nod factors and therefore

prevent the nodulation (Van Rhijin & Vanderleyden,

1995; Denarie et al., 1996; Long, 1996). Alfalfa, for

example, is only nodulated in the presence of

sulphated Nod factors. This specificity mechanism

is based on the presence or absence, depending on

bacterial strains, of some genes that control the

synthesis of specific substitutes or their transfer on

the common skeleton. Other than genetic factors,

exogenous factors can influence the symbiosis

either for the choice of rhizobia that nodulate the

plant or for their efficiency.

According to Garan et al. (2005), S. medicae

nodulate more the species of Medicago that are

adapted to acid soils; by contrast, M. meliloti forms

a more frequent symbiosis with those that grow on

alkaline to neutral soils. This result does not apply

to the 4 taxa of the Intertextae subsection, since

they rather prefer alkaline to neutral soils.

Symbiotic specificity

The symbiotic response is not limited to the

presence or absence of nodules. Others structures

can exist and appear visually on the roots in the

form of more or less developed protuberances. Ge-

nerally, these forms do not grow bigger in length,

in fact, their development stops quickly. The study

of the effect of the Nod factors of Rhizobium me-

liloti (equivalent to S. meliloti ) on cultivated al-

falfa revealed several structures, such as nodules

and other protuberances (Grosjean & Huguet,

1997) .

Therefore, the symbiotic response other than the

presence absence of efficient nodules cannot be

dissociated from genetic variations of the host plant.

In this sense, the Nod- of M. muricoleptis and M.

granadensis induced by S. meliloti shows the diffe-

rence of these taxa relative to M. ciliaris and M.

intertexta.

Furthermore, the strain USDA1827 shows a

specificity of inter- and intra-species host and it is

not the only one. The population ESI 03 of M.

polymorpha achieves an efficient symbiosis with

ABS7m, while the population F34003 does not

form any nodule with this same strain (Bena et al.,

1998) .

Genetic relation between rhizobium and

taxa

According to Martinez -Romero (2009), plant-

rhizobium coevolution is more oriented by the plant

494

Meriem Laouar & Aissa Abdelguerfi

than by the rhizobium; it is the plant that must con-

stantly select the strains with which it gets in sym-

biosis. This result shows that the taxa acquired

genetic differentiation. In Tunisia, the results of

molecular and enzymatic analysis did not show

strains-species specificity in indigenous strains of M.

sativa cv. Gabbes, M. scutelleta cv. Kelson, M. trun-

catiila and M. ciliaris (Jebara, 2001). Although M.

muricoleptis and M. granadensis do not share the

same areas of distribution, they select genetically

close strains of rhizobium that are different from the

ones of indigenous taxa, M. ciliaris and M. intertexta.

These results indicate cospeciation between the

rhizobia and the endemic and widespread taxa. Co-

speciation between the rhizobia and leguminous

plants is not clearly established. Some authors

indicate that there is little concordance between the

phylogeny of bacteria and the phylogeny of

legumes plants (Doyle, 1998; Bena et al., 2005);

others, on the contrary, find links between both

partners (Ueda et al., 1995; Wemegreen & Riley,

1999; Laguerre et al., 2001).

What is the effect of the two factors on the

geographical distribution of taxa?

When analyzing ecological data, it appears that

there are no conditions specific to either taxon.

Some variations were observed among taxa but are

not discriminating. Consequently, M. muricoleptis

and M. granadensis are not specific to some habi-

tats and the limit of their dispersion is not ecologi-

cal. According to Griggs (1940), climatic and

edaphic factors are not the primary causes of the

rarity of a species, but the primary cause is compet-

itiveness. Other biotic factors may come into play;

we have seen that symbiosis does not seem to be a

factor that limits the dispersion of endemic species

since they have grown and nodulated in Algeria

where they are naturally absent. Indeed, from a

study on the effect of symbiosis on the expansion

of the Medicago genus (Bena et al., 2005), it was

concluded that symbiotic specificity can influence

the distribution of the species of the Medicago

genus, but not to the point of influencing their level

of endemism.

In this case, M. muricoleptis and M. granadensis

show local endemism that generally results from

geographic and genetic isolation. The geographical

distribution of the 4 taxa may result from allopatric

speciation where the populations are first separated

geographically, which provokes a net decrease or a

stop of the genetic exchanges, and the progressive

accumulation of differences among the populations.

According to the phylogenetic results, that indi-

cate that M. ciliaris and M. intertexta evolved from

a common lineage and that M. intertexta evolved

independently and gave rise to M. muricoleptis and

M. granadensis (Rose et al., 1988), we may assume

that M. muricoleptis and M. granadensis are young

species (neoendemism) (Willis, 1922; Stebbins,

1980) compared with M. intertexta and M. ciliaris

and that over time they could extend to other areas.

As mentioned by Lamotte (1994), in allopatric spe-

ciation, populations may be confronted to different

environments allowing or provoking differential

adaptations.

CONCLUSION

Ecological factors did not explain why phylo-

genetically close taxa belonging to the same sub-

section have different geographical distributions,

one narrow and one wide. The ecological require-

ments of taxa are more or less similar demonstrat-

ing that this is not the factor limiting the

distribution of M. muricoleptis and M. granaden-

sis in the region of the Mediterranean. Either the

symbiosis is not a factor limiting the presence of

these taxa which perform an efficient symbiosis in

an area where are naturally absent. As against,

endemic and widespread taxa show selectivity in

symbiont (rhizobia strains) which confirms their

differences. Other factors, such as genetic pool of

taxa, should be investigated to clarify the distribu-

tion of the Intertextae.

ACKNOWLEDGMENTS

We thank S.J. Hughes (SARDI) for sending us

the ecological data and the collection of Intertextae ,

T. Huguet (ENSA Toulouse, now retired) for

helping us in achieving the symbiotic part, G.G.

Guittonneau (Univ. Orleans, now retired) for his

guidance and advice. This work was supported in

part by the Algerian-French cooperation (Tassili

project).

Effect of ecological factors and symbiotic specificity on Medicago subsect. Intertextae in the Mediterranean Basin 495

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Biodiversity Journal, 2014, 5 (4): 499-504

On the presence of Notodiaphana atlantica Ortea, Moro et

Espinosa, 20 1 3 in the Mediterranen Sea, with notes on Retusa

multiquadrata Oberling, 1 970 and Cylichna mongii (Audouin,

1 826) (Cephalaspidea Cylichnidae)

Pasquale Micali

viaPapiria 17, 61032 Fano, Pesaro-Urbino, Italy; e-mail: lino.micali@virgilio.it

ABSTRACT Notodiaphana atlantica Ortea, Moro et Espinosa, 2013 (Cephalaspidea Cylichnidae) is re-

ported from various localities of Western and Central Mediterranean. Records of Retusa mul-

tiquadrata Oberling, 1970 are listed and discussed, most of them are considered to be based

on N. atlantica. Possible synonymy between N. atlantica and R. multiquadrata is discussed,

but former name is preferred. Based on the study of material from Suez channel. Bulla mongii

Audouin, 1826 seems to be based on a very young specimen of the common species Liloa

curta (A. Adams in Sowerby, 1850), but as Audouin’s name is older, then Bulla curta shall be

considered synonym of Bulla mongii. Liloa mongii (Audouin, 1826) new combination is than

proposed.

KEY WORDS Bulla mongii', Notodiaphana atlantica ; Retusa multiquadrata', Mediterranean; Lessepsian.

Received 18.10.2014; accepted 23.11.2014; printed 30.12.2014

INTRODUCTION

The recently described species Notodiaphana

atlantica Ortea, Moro et Espinosa, 2013 (Cepha-

laspidea Cylichnidae) is here reported for the first

time in the Mediterranean Sea. In the Mediter-

ranean Sea have also been reported Cylichna

mongii (Audouin, 1 826) and Retusa multiquadrata

Oberling, 1970, two poorly known species, which

need to be clarified to avoid misuse of the name.

Mediterranean records of these three species, ob-

viously only those accompanied by a photo, are

discussed.

Notodiaphana atlantica Ortea, Moro et Es-

pinosa, 2013

2013. Notodiaphana atlantica - Ortea et al.: 17, fig.

4, pi. 1.

1972. Cylichnina multiquadrata - Nordsieck: 35,

pi. O XVI, fig. 18

1995. Retusa multiquadrata - Miklcelsen: 205, fig.

2001. Cylichnina multiquadrata - Cachia et al.: 125,

pi. XX, fig. 7

2008. Cylichnina multiquadrata - Cecalupo et al.:

128, pi. 75 figs. 5-7 (not fig. 4)

Examined material. Jerba (Tunisia), -2/3 m, 6

sh. (Figs. 5, 12-16); Pace, 5 km north of Messina,

Sicily, -6 m, 1 sh., 2014, legit A. Villari (Fig. 6);

Augusta, north of Syracuse, Sicily, beached in the

harbour area, 1 sh., 1990, legit A. Villari; Linosa

500

Pasquale Micali

island, Sicily Channel, -10 m, 1 sh., 2013, legit P.

Micali; Cabo Negro, Tetouan, Morocco, -30m, lsh.

Remarks. N. atlantica is described based on

specimens from a wide area ranging from Bahamas

islands to Cuba and Canary islands, type locality is

not designated.

Authors widely discuss the Mediterranean

records, bearing also a photo, of C. mongii and R.

multiquadrata, to ascertain whether this species is

present in the Mediterranean. In particular Authors

refer to the photos of three specimens in a work pub-

lished on web (http://www.naturamediterraneo.

com/forum/topic. asp?TOPIC_ID=l 00306) by the

Gmppo Malacologico Livornese and later on pub-

lished in the “Notiziario S.I.M.” (Gruppo Malaco-

logico Livornese, 2004), ignoring that the three

photos have been taken from Cecalupo & Quadri

(1996). Authors note that one of the three specimens

(they do not indicate which one, but possibly that

at photo lb) resembles N. atlantica for the profile

and the presence of spiral and axial threads. Authors

are misled by the indication that the figured speci-

men is 2.2 mm high and 1 .5 mm wide and conclude

that it is not N. atlantica for the size and the H/W

of 1 .46 against 2 in N. atlantica. Really Cecalupo

& Quadri (1996) determine the three specimens as

C. cfr. mongii and indicate that the specimen at fig.

1 is 2.2 mm high, while the other two, whose height

is not indicated, but may be calculated from the

enlargement (x 25) indicated in the legend of the

table, should be 1 .7 mm (fig. lb) and 1 .24 mm (fig.

lc) high. Ortea et al. (2013) conclude that N.

atlantica is not present in the Mediterranean.

Nordsieck (1972) describes and draws a speci-

men from Le Franqui, type locality of the species.

The Author states ”nach Foto von Oberling ”,

therefore description and drawing are taken from a

photo of C. multiquadrata that Oberling sent to

Nordsieck, and this is proved by the dimension of

the drawn specimen, that is very close to that

indicated by Oberling.

Ortea et al. (2013) do not mention the work of

Cecalupo et al. (2008) on the malacofauna of Gabes

gulf, where are figured two specimens from various

localities of Kerkennah island, as C. multiquadrata ,

having height ranging from 3.2 to 3.4 mm, therefore

well mature. Photo of a living specimen clearly

shows that soft parts are white, with a large darker

zone hardly visible inside the shell. This colour cor-

responds with N. atlantica , for which a large dark

spot, corresponding to digestive gland is indicated.

The specimen in Cecalupo et al. (2008) is

clearly different by N. atlantica , and it is currently

under study.

Cachia et al. (2001) describe and figure C. mul-

tiquadrata , stating that few empty shells have been

found at Salina Bay, Malta. From the description

and drawing of a specimen 3.9 mm high, there is no

doubt that it is N. atlantica.

Vazzana (2010) lists C. cfr. mongii at Scilla

(Strait of Messina), without figuring it. Based on

reported findings of N. atlantica in this area and the

photos on web, where this species is also on sale,

there is no doubts that the records in the Strait of

Messina shall be referred to N. atlantica.

Therefore based on studied material and con-

firmed records, N. atlantica is widespread in the

western and central Mediterranean sea, up to south

France, Sicilian coasts, Malta and south Tunisia.

N. atlantica may be easily separated from Liloa

mongii for the much finer cancellate sculpture with

more than double number of spiral grooves. The

sculture of L. mongii is not cancellate, consisting of

spiral grooves and growth folders. In specimens

about 2.2 mm high N. atlantica has a nearly

straight, instead of regularly convex lateral shell

profile. Seen from the aperture the profile shows a

wider and more squared last whorl and columellar

lip extended over the umbilical rim. Columellar

profile is inclined but almost straight in the joint to

the whorl, while in L. curta the columella is short

and there is an angle, not covered by columellar lip.

The abapical margin is more acute and by trans-

parency it is visible the external cancellate sculp-

ture, while in L. curta the margin is squared, quite

straight and only some spiral grooves may be seen

from inside (compare Figs. 1,2 and Figs. 3, 4)

R. multiquadrata was described a first time

(Oberling, 1970) with the following description:

“De rares specimens sur la plage de la Franqui

[north of Perpignan, south France]. Forme en cylin-

dre trapu, un peu comme R. mammillata. Phil.,

mais avec sommer perfore. Sculpture reticulee de

sillon spiraux et transverses, comme pour R. crebis-

culpta Mtr., mais reseau plus dense que dans cette

espece. La columelle est fortement developpee” .

In one later work (Oberling, 1971) the species

is again described with more details “Un petit (1 %

x 1 mm.) Retusa, presque cylindrique quoique avec

Notodiaphana atlantica in the Mediterranen Sea, with notes on Retusa multiquadrata and Cylichna mongii (Cylichnidae) 501

Figures 1, 2. Liloa mongii, Great Bitter Lake (Suez channel), height 2 mm. Fig. 1: front view. Fig. 2: apical view. Figures

3-5. Notodiaphana atlantica, Jerba (Tunisia), height = 2.3 mm. Fig. 3: front view for comparison with Fig. 1. Fig. 4: apical

view. Fig. 5: front view. Figure 6. N. atlantica. Pace (Messina), height = 2.3 mm. Figures 7-11. Liloa mongii, Great Bitter

Lake (Suez channel). Fig. 7: height 4.6 mm. Fig. 8: height 1.4 mm. Fig. 9: height 3.7 mm. Fig. 10: height 2 mm. Fig. 11:

height 2.3 mm (same specimen of Fig. 1). Figures 12-16. N. atlantica, Jerba (Tunisia). Fig. 12: height = 4.5 mm. Fig. 13:

height =1.7 mm. Figs. 14-16: height = 3.3 mm. Fig. 14: front view. Fig. 15: apical view. Fig. 16: lateral view.

502

Pasquale Micali

tours quelque peu convexes; spire enfoncee, proto-

conque visible au fond du trou ainsi cree, tours

autour de celui-ci-embrassants. Columelle tres

allongee (longueur pres de % de celle de la region

parietale); surface de la coquille treillissee de stries

spirales et verticales bien marquees. - Cette espece

ressemble vaguement au R. crebisculpta Mtrs.:

celui-ci est relativement deux fois plus long, sa

columelle beaucoup plus courte, sa protoconque est

cryptique, etc...”. The description fits with N. at-

lantica, but without the study of type material, even

after Nordsieck’s illustration of the species, the

name should be considered nomen dubium.

The name Cylichnina multiquadrata is used by

Mikkelsen (1995) for specimens from Azores, by

Buzzuito & Greppi (1997) in a list of shells from

Tasugu (south Turkey), without any comment or

figure and, later on, by Cecalupo et al. (2008) who

figure three specimens as C. multiquadrata , basing

the determination upon Oberling’s description. As

proved below, the specimens at figures 5-7 shall

actually be referred to N. atlantica, while specimen

at fig. 4, which is a little different, could be another

species.

It is astonishing that a species poorly described

and not figured, has met such a success. The type

material (not the holotype, which was not fixed)

seems to be lost (Oliverio in litteram, 08 Sept.

2014).

From what above seems that C. multiquadrata

and N. atlantica are synonyms, anyway as the spec-

imen figured by Nordsieck is not indicated as

belonging to type series, then C. multiquadrata is

here considered nomen dubium and N. atlantica is

the name to be used until Oberling’s type material

will be traced and studied.

Liloa mongii (Audouin, 1826) new combination

1826. Bulla mongii - Audouin: 39 (ref. to Savigny’s

figure, 1817: pi. 5, fig. 7).

1869. Cylichna mongii - Issel: 170 n° 424; 347 (ref.

to Savigny’s figure at pi. 5, fig. 7).

1926. Cylichna mongii - Pallary P.: 76, pi. 5, fig. 7.

1939. Cylichna mongei (sic) - Moazzo: 135.

1982. Bulla mongii - Bouchet & Danrigal: 14, fig.

58.

1996. Cylichnina cfr. mongii - Cecalupo & Quadri:

110, tav. Ill, fig. 1, la, lb.

2008. Liloa curta - Rusmore-Villaume: 150, fig.

2014. Liloa curta - Too et al.: 383, fig. 1 J (living),

3D, 17A-I

For further figures of L. curta see Too et al. (2014).

Examined material. Great Bitter lake, Suez

Channel, Egypt, legit G.P. Franzoni, 10 sh.

Remarks. Cylichna mongii (Audouin, 1826) is

a species of controversal determination, with many

records in literature (see below). At present not all

Authors agree on the origin or determination of

this species. Go fas & Zenetos (2003) list among

the species excluded from CIESM the C. cf.

mongii , with a “(w)” to indicate that “ citation is

considered to proceed from a misidentification of

a native species ”.

The difficulty in the determination of this

species is because Audouin (1826) assigned the

name of Bulla mongii to the species figured by

Savigny (1817) at pi. 5, fig. 7, therefore the species

was never described and Savigny’s drawing is very

small.

Issel (1869) indicates that the species is known

to him only from fossil specimens collected on

beaches above sea level (“, spiagge emerse del Golfo

Arabico”), but as the species was figured by Savi-

gny, it is then included among the recent species.

Issel (1869) gives the first description, obviously

based on his interpretation of the species: “ Conchi -

glia assai piccola, sottile, ovato-cilindrica, piii

ristretta alia parte inferiore che alia superiore,

bianca, liscia, non striata ne solcata, poco nitida;

apice incavato, non perforato. Apertura stretta, piii

allargata in basso che in alto; margine destro

regolarmente arcuato, semplice, superante l ’apice

alia parte superiore; parte visibile della columella

assai breve e non troncata. Dimensioni; Altezza

millim. 2; diametro 1 [shell very small, thin, ovate-

cylindrical, more restricted in the lower than in the

upper part, white, smooth, not striated or sulcate,

not glossy; spire sunken, not perforated. Aperture

narrow, larger in the lower than in the upper part;

right margin regularly arched, acute, protmding the

apex; visible portion of the columella very short,

not truncate. Dimensions: height 2 mm, width 1

mm]”.

Pallary (1926) does not add any comment. Lamy

(1938) reports this species for Ismailia (Suez

Notodiaphana atlantica in the Mediterranen Sea, with notes on Retusa multiquadrata and Cylichna mongii (Cylichnidae) 503

Channel), without comments. Moazzo (1939)

reports it for the bay of Suez and lake Timsah.

Bouchet & Danrigal (1982) illustrate the single spec-

imen, only 1 .6 mm high, present in Savigny collec-

tion, to be then considered the holotype. From the

photo it is possible to see the spiral lines present all

over the shell and the straight and folded outwardly

columellar lip.

From the comparison of type specimen and

Issel’s description, it is clear that Issel’s interpreta-

tion of this species is wrong, because he describes

the surface as smooth, not striated or sulcate.

Ortea et al. (2013) show the type specimen, after

metal coating, in little different position from photo

in Bouchet & Danrigal (1982), with a more realistic

view of the columellar profile and aperture.

Cecalupo & Quadri (1996) figure as C. cf. mongii

three specimens from Kyrenia (North Cyprus),

stating that this is the first Mediterranean record.

The CIESM (http://www.ciesm.otg/atlas/appendix

3bis.html, last update: December 2003) includes C.

cf. mongii (Audouin, 1 826) in the “List of excluded

species”, with the following comment: “ The taxon

reported under this name, from Cyprus by Cecalupo

and Quadri (1996), may be an undescribed

Mediterranean species. According to Van Aartsen

(pers. comm.) this species is also known from the

Island of Djerba, Tunisia, and Akkum, Turkey, and

without doubt lives in the Mediterranean”.

Cossignani & Ardovini (2011) figure the C. cf.

mongii using the photos from Cecalupo et al.

(2008), from Kerkennah (Tunisia), instead of those

from Cecalupo & Quadri (1996), showing the spec-

imens from Cyprus, to which is referred the com-

ment in CIESM (see above). In addition it is

erroneously indicated Malaga as origin of the

material.

The reduced size of the holotype (H= 1.6 mm)

let one suppose that it could be the immature stage

of a species living in the area. Studying the speci-

mens of Liloa curta (A. Adams in Sowerby, 1850)

collected in the Great Bitter Lake, it became clear

that Bidla mongii is based on an immature speci-

men of the species known as L. curta. Figures 7-

11 show a growth series from a specimen

corresponding to type of Bulla mongii, to a speci-

men corresponding to Liloa curta. The shell profile

varies with the growth, as the sculpture, which is

more evident in small specimens. As the Audouin’s

name is much older than Adams ‘s name, then the

new combination Liloa mongii (Audouin, 1 826) is

here proposed. This species shall be considered a

true Lessepsian migrant, as it is present in the Suez

Channel since long time and has entered the

Mediterranean.

L. curta, as such, has not been reported in the

Mediterranean sea, but record of C. mongii from

Cyprus by Cecalupo & Quadri (1996) shall be

considered the first in Mediterranean. Comparison

between L. mongii from Suez Channel and speci-

mens from Cyprus has been carried out with posi-

tive result.

L. mongii is a well known species with very

wide distribution covering Red Sea, Malaysia the

Philippines, China, Japan, Papua New Guinea,

Guam, New Caledonia and Hawaii (fide Too et al.,

2014). The description from Too et al. (2014) is the

following: “ Maximum height 18 mm; whitish; thin

and fragile, translucent, cylindrically oval, sides

slightly convex only, anterior end slightly rounded,

posterior end truncated; spire sunken, aperture

broad, outer lip thin, base semi-circular; spiral

grooves covering entire shell, distance between

spiral grooves almost equal, faint irregular axial

lines present”.

Moazzo (1939) reports this species as C. semisul-

cata Dunker, 1882 indicating it frequent in Lake

Timsah, less frequent in the Great Bitter Lake and

rare in Suez bay. Rusmore-Villaume (2008) in her

work on the Egyptian Red Sea, indicates L. curta

as “ infrequent in all areas. Locally common in shell

grit”, reaching a height of 12.5 mm. Studied speci-

mens from Great Bitter Lake reach about 5 mm.

Atys porcellana Gould, 1859, C. semisulcata and B.

curta A. Adams in Sowerby, 1850 are then syn-

onyms of B. mongii Audouin, 1826.

L. mongii may be easily separated from Atys

cylindricus (Hebling, 1779) for the depressed

spire, with a smaller protrusion between the spire

and lip, for the more cylindrical profile and the

spiral grooves covering the whole height of the

spire.

ACKNOWLEDGEMENTS

I thank Gian Paolo Franzoni (Tortoreto Lido,

Italy) and Alberto Villari (Messina, Italy) for the

submission of material, Marco Oliverio (Rome,

Italy) for the information on Oberling type material,

504

Pasquale Micali

Morena Tisselli (S. Zaccaria, Italy) for the biblio-

graphic support, Alberto Cecalupo (Milan, Italy) for

the comparison of specimens and Stefano Bartolini

(Florence, Italy) for the photos.

REFERENCES

Audoin V., 1826. Explication sommaire des planches de

Mollusques de F Egypte et de la Syrie publiees par

J.C. Savigny. Description de l’Egypte ou recuil des

observant et des recherches qui ont ete faites en

Egypte pendant F expedition de l’armee franqaise

publie par les ordres de sa majeste Fempereur

Napoleon le grand. Histoire Naturelle. Imprimerie

imperiale, Paris. Animaux invertebres, 1(4): 7-56.

Bouchet P. & Danrigal F., 1982. Napoleon’s Egyptian

Campaign (1798-1801) and the Savigny collection of

shells. The Nautilus, 96: 9-24.

Buzzurro G. & Greppi E., 1997. The Lessepsian mol-

lusca of Tasugu (South East Turkey). La Conchiglia,

Annuario 1996, Supplemento al n° 279: 3-22.

Cachia C., Mifsud C. & Sammut P.M., 2001. The marine

Mollusca of the Maltese Islands. Part Three.

Backhuys Publishers, Leiden, 182 pp.

Cecalupo A., Buzzurro G. & Mariani M., 2008. Con-

tribute alia conoscenza della malacofauna del Golfo

di Gabes (Tunisia). Quademi della Civica Stazione

Idrobiologica di Milano, 31: 1-175.

Cecalupo A. & Quadri P, 1996. Contributo alia

conoscenza malacologia per il nord dell’isola di

Cipro (Terza e ultima parte). Bollettino Malaco-

logico, 31: 95-118.

Cossignani T. & Ardovini R., 2011. Malacologia Mediter-

ranea. L’lnformatore Piceno, Ancona, 536 pp.

Gofas S. & Zenetos A., 2003. Exotic molluscs in the

Mediterranean basin: current status and perspectives.

Oceanography and Marine Biology: an Annual

Review, 41: 237-277.

Gruppo Malacologico Livornese, 2004. Documenti del

Gruppo Malacologico Livornese. Notiziario S.I.M.,

22: 60-76.

Issel A., 1 869. Malacologia del Mar Rosso, ricerche zoo-

logiche e paleontologiche. Biblioteca Malacologica,

Pisa, 387 pp.

Lamy E., 1938. Mission Robert Ph. Dollfuss en Egypte:

7. Mollusca testacea. Memoires de Flnstitut

d’Egypte, 37: 1-90.

Mikkelsen P.M., 1995. Cephalaspid opisthobranchs of

the Azores. In: Martins A.M.F. (Ed.), The marine

fauna and flora of the Azores. Proceedings of the

Second International Workshop of Malacology and

Marine Biology, Vila Franca do Campo, Sao Miguel,

Azores. Aqoreana, Supplement 4: 193-215.

Moazzo P.G., 1939; Mollusques testaces marins du Canal

du Suez. Memoires de Flnstitut d’Egypte, 38: 1-283.

NordsieckF., 1972. Die Europaischen Meeresschnecken.

Gustav Fischer Verlag. Stuttgart, 327 pp.

Oberling J.J., 1970. Quelques especes nouvelles de

Gasteropodes du bassin Mediterraneen. Kleine Mit-

teilungen Naturhistorisches Museum Bern, 1: 1-7.

Oberling J.J., 1971. Quelques taxa nouveaux or mal com-

pris de microgasteropodes Mediterraneen. Kleine

Mitteilungen Naturhistorisches Museum Bern, 2:

1 - 8 .

Ortea J., Moro L. & Espinosa J., 2013. Nueva especie de

Notodiaphana Thiele, 1931 del Oceano Atlantico y

nueva ubicacion generica para Atys alayoi Espinosa

& Ortea, 2004 (Gastropoda: Opisthobranchia: Cepha-

laspidea). Revista de la Academia Canaria de Cien-

cias, 25: 15-24.

Pallary P, 1926. Explication des planches de J.C. Savi-

gny. Memoires de Flnstitut d’Egypte, 11: 1-138.

Rusmore-Villaume M.L., 2008. Seashells of the Egyptian

Red Sea: the Illustrated Handbook. The America

University in Cairo Press, 307 pp.

Too C.C., Carlson C., Hoff P.J. & Malaquias M.A.E.,

2014. Diversity and systematics of Haminoeidae

gastropods (Heterobranchia: Cephalaspidea) in the

tropical West Pacific Ocean: new data on the genera

Aliculastrum, Atys, Diniatys and Liloa. Zootaxa,

3794 (3): 355-392.

Vazzana A., 2010. La malacofauna del Circalitorale di

Scilla (Stretto di Messina). Bollettino Malacologico,

46: 65-74.

Biodiversity Journal, 2014, 5 (4): 505-508

The first earthworm records from Malta (Oligochaeta Lum

bricidae)

Csaba Csuzdi 1 & Arnold Sciberras 2 *

'Department of Zoology, Eszterhazy Karoly Coollege, Eger, Hungary; e-mail: csuzdi.csaba@ektf.hu

2 1 33 'Arnesf , Arcade Str, Paola, Malta; e-mail: bioislets@gmail.com

* Corresponding author

ABSTRACT The first earthworm report from Malta lists seven species; six species from the Holarctic family

Lumbricidae and one species from the Mediterranean family Hormogastridae. Apart from the

Circum-Mediterranean Octodrilus complanatus (Duges, 1828) and the Trans-Aegean

Octodrilus transpadanus (Rosa, 1884) the other four lumbricid species recorded are widely

distributed peregrine. The unidentified hormogastrid specimen might represent an au-

tochthonous species in Malta.

KEY WORDS Earthworms; fauna; new record; Maltese Islands.

Received 23.10.2014; accepted 01.12.2014; printed 30.12.2014

INTRODUCTION

Earthworms (Oligochaeta Lumbricidae) repre-

sent one of the most important groups of the soil

fauna. Due to the earthworms’ activity not only the

structure of the soil is altered, but also the chemical

composition is substantially changed (Lee, 1985).

As members of the saprophagous guild, earth-

worm species play a paramount role in the decom-

position of dead plant material (litter, dead grass,

etc.) in temperate forests (Zicsi, 1983). Their activ-

ity is also important in the tropical regions as well,

where, together with termites, earthworms are re-

sponsible for the decomposition of 40% of dead

plant material (Lee, 1985).

This is the reason why earthworms are con-

sidered “soil ecosystem engineers” (Jones et al.,

1994; Decaens et al., 2001), which play a funda-

mental role in maintaining soil fertility and con-

sequently are indispensable for sustainable agricul-

ture (Jimenez et al., 2001). Contrary to their vital

importance in biogeochemical cycles we have de-

tailed ecological data only about two dozen species

(Zicsi et al., 2011) from the some 800 valid lum-

bricid species distributed over the Holarctic

(Csuzdi, 2012).

In addition, there are regions even in Europe

from where earthworm records are scarce or com-

pletely missing.

One of such region is Malta from where, up to

our present knowledge, there are no earthworm

records published. In the last year the second

author, a herpetologist interested in different lizard

groups investigated the available prey-population

including earthworms in Malta.

During this short-term study five earthworm

species have been recorded which, together with

some other specimens from the collection of the

Hungarian Natural History Museum, are herewith

presented.

506

Csaba Csuzdi & Arnold Sciberras

MATERIAL AND METHODS

A larger study collecting all fauna present in

sampling sites was being carried out in two pre-

vious separate studies.

One of the authors (AS) resident on Malta, was

able to monitor, dig and hand sort the mentioned

retrieved specimens along with his colleague

Patrick Vella. Along with the latter specimens from

the Hungarian Natural History Museum, all speci-

mens were studied by CC and included in the

current list.

All voucher specimens that have been collected

are now housed in the collection of one of the

authors (CC).

RESULTS

Family LUMBRICIDAE Rafmesque-Schmaltz, 1815

Allolobophora chlorotica (Savigny, 1826)

Enterion chloroticum Savigny, 1826: 182.

Allolobophora chlorotica : Csuzdi & Zicsi,

2003: 50 (for complete synonymy).

Examined material. SantaMarija bay, Comino

Island (Maltese Archipelago), 3 adult ex., 1 adult

and 1 juvenile ex., 3 adult ex., leg. A. Sciberras.

Aporrectodea trapezoides (Duges, 1828)

Lumbricus trapezoides Duges, 1828: 289.

Aporrectodea trapezoides : Blakemore, 2008:

531 (for complete synonymy).

Examined material. 23 adult ex., 1 adult ex.,

Chadwik Lakes, 1 adult ex., leg. V. Mahnert,

06.V.1974.

Aporrectodea rosea (Savigny, 1826)

Enterion roseum Savigny, 1826: 182.

Aporrectodea rosea : Csuzdi & Zicsi, 2003: 92

(for complete synonymy).

Examined material. 1 adult ex., 1 adult and 1

juvenile ex., Around St. Georges Bay under stones,

in Garrique, 1 adult ex., leg. V. Mahnert, 04.V.1974.

Eiseniella tetraedra (Savigny, 1826)

Enterion tetraedrum Savigny, 1826: 184.

Eiseniella tetraedra : Csuzdi & Zicsi, 2003: 153

(for complete synonymy).

Examined material. Chadwik Lakes, 1 adult

ex., leg. V. Mahnert, 06.V.1974.

Octodrilus complanatus (Duges, 1828)

Lumbricus complanatus Duges, 1828: 289.

Octodrilus complanatus : Blakemore, 2008: 625

(for complete synonymy).

Examined material. 6 adult and 5 1 juvenile ex.

Octodrilus transpadanus (Rosa, 1884)

Allolobophora transpadana Rosa, 1884: 45.

Octodrilus transpadanus : Csuzdi & Zicsi, 2003:

215 (for complete synonymy).

Examined material. Around St. Georges Bay

under stones, in Garrique, 1 adult ex., leg. V.

Mahnert, 04.V.1974.

Family HORMOGASTRIDAE Michaelsen, 1900

Hormogaster sp.

Examined material. 1 juvenile ex.

Remarks. We have only one juvenile specimen

representing this Mediterranean family Hormoga-

stridae, therefore, the exact species identification is

not possible.

DISCUSSION

This small sample from Malta consisted of

seven earthworm species of which four lumbricids

The first earthworm records from Malta (Oligochaeta Lumbricidae)

507

(A. chlorotica, A. rosea , A. trapezoides and E.

tetraedra ) are widely distributed, peregrines which

most probably were introduced by human activi-

ties. The other two lumbricid species ( O . com-

planatus and O. transpadanus ) possess more

restricted area (Circum-Mediterranean and Trans-

Aegean respectively) however, they are also capa-

ble for human introduction (see e.g. Mischis et al.,

2005; Blakemore, 2008).

The only species which can be endemic in the

island is the unidentified Hormogaster species.

Hormogaster are distributed over the Western

Mediterranean basin (Omodeo & Rota, 2008) and

seemingly have no tendency for human introduc-

tion. Consequently, the presence of this species in

Malta can be connected with the island’s geologi-

cal history.

The Maltese islands are situated on a shallow

shelf called Malta-Ragusa Rise extending from the

Ragusa Peninsula of Sicily toward the African

coast (Magri et al., 2008). The presence of many

Siculo-Maltese endemic species proves the close

biogeographic relationships between Malta and

Sicily which is a consequence of land connections

with Sicily either in the Quaternary or in the

Messinian stage of the Miocene Epoch (Hunt &

Schembri, 1999).

Therefore, the abundant presence of Hormo-

gaster redii Rosa, 1887 in Sicily (Omodeo & Rota,

2008) provides an apparent explanation of the ori-

gin of Hormogaster in Malta, however to draw

more specific conclusions exact species identifica-

tion is needed.

ACKNOWLEDGEMENTS

The authours wish to thank Patrick Vella,

Esther Sciberras, Jeffrey Sciberras, Romario

Sciberras for their assistance in field work and

Prof. Patrick J. Schembri for assistance in litera-

ture search.

REFERENCES

Blakemore R.B., 2008. Cosmopolitan earthworms - an

Eco-Taxonomic Guide to the Species (3rd Edition).

VermEcology, Yokohama, Japan, 757 pp.

Csuzdi Cs., 2012. Earthwonn species, a searchable data-

base. Opuscula Zoologica Budapest, 43: 97-99.

Csuzdi Cs. & Zicsi A., 2003. Earthworms of Hungary

(Annelida: Oligochaeta; Lumbricidae). In: Csuzdi Cs.

& Mahunka S. (Eds.), Pedozoologica Hungarica 1.

Hungarian Natural History Museum, Budapest, 271

pp.

Decaens T., Galvis J.H. & Amezquita E., 2001. Proper-

ties of the structures created by ecosystem engineers

on the soil surface of a Colombian savanna. In:

Jimenez J.J. & Thomas R.J. (Eds.), Nature’s Plow:

Soil macroinvertebrate communities in the neotropi-

cal savannas of Colombia. CIAT publ. No. 324.

Colombia, pp. 151-175.

Duges A., 1828. Recherche sur la circulation, la respi-

ration, et la reproduction des Annelides abranches.

Annales des Sciences Naturelles Paris, 15: 284-

336.

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ments and biogeography of the Maltese Islands. In:

Mifsud A. & Savona Ventura C. (Eds.), Facets of

maltese prehistory. The Prehistoric Society of Malta,

pp. 41-75.

Jimenez J.J., Decaens T., Thomas T., Mariani L. &

Lavelle P., 2001. General conclusions, research

highlights, and future needs. In: Jimenez J.J. &

Thomas R.J. (Eds.), Nature’s Plow: Soil macroin-

vertebrate communities in the neotropical savannas

of Colombia. CIAT publ. No. 324. Colombia, pp.

361-386.

Jones C.G., Lawton J.H. & Shachak M., 1994.

Organisms as ecosystem engineers. Oikos, 69: 373—

386.

Lee K.E., 1985. Earthworms, their ecology and relation-

ships with soils and land use. Academic Press,

Sydney, London, 411 pp.

Magri O., Mantovani M., Pasuto A. & Soldati M., 2008.

Geomorphological investigation and monitoring of

lateral spreading along the north-west coast of Malta.

Geografia Fisica e Dinammica Quatemaria, 31: 171—

180.

Mischis C.C., Csuzdi Cs., Arguello G. & Herrera J.A.D.,

2005. A contribution to the knowledge of the

earthworm fauna (Annelida, Oligochaeta) of the Ar-

gentinian Patagonia. In: Pop V. V. & Pop A. A. (Eds.),

Advances in earthworm taxonomy II. University

Press, Cluj,pp. 173-182.

Omodeo P. & Rota E., 2008. Earthworm diversity and

land evolution in three Mediterranean districts.

Proceedings of the California Academy of Sciences,

59(supplementum 1): 65-83.

Rosa D., 1884. Lumbricidi del Piemonte. Unione Ti-

pografico-Editrice, Torino, 54 pp.

Savigny J.C., 1826. Analyse des Travaux de l’Academie

royale des Sciences, pendant l’annee 1821, partie

physique. Memoires de l’Academie des Sciences de

l’lnstitut de France, Paris, 5: 176-184.

508

Csaba Csuzdi & Arnold Sciberras

Zicsi A., 1983. Earthworm ecology in deciduous forests

in central and southeast Europe. In: Satchell J.E.

(Ed.), Earthworm ecology from Darwin to vermicul-

ture. Chapman & Hall, Routledge, pp. 171-177.

Zicsi A., Szlavecz K. & Csuzdi Cs., 2011. Leaf litter

acceptance and cast deposition by peregrine and

endemic European lumbricids (Oligochaeta: Lumbri-

cidae). Pedobiologia, 54S: 145-152.

Biodiversity Journal, 2014, 5 (4): 509-514

Alvania dalmatica Buzzurro et Prkic, 2007 (Gastropoda Ris-

soidae): range extension, shell variability, habitat and relation-

ships with A. hallgassi Amati et Oliverio, 1 985

Luigi Romani

Via delle ville 79, 55013 Lammari, Lucca, Italy; e-mail: luigiromani78@gmail.com

ABSTRACT Shell samples of Alvania dalmatica Buzzurro et Prkic, 2007 (Gastropoda Rissoidae) were

obtained from Corfu. This is the first record of the species from the Ionian Sea and Greece.

The shells show a wide morphological variation not previously reported for the species.

Numerous shells of A. hallgassi Amati et Oliverio, 1985 were also found in the same localities.

Some unreported features of this species are pointed out and the relationships with A. dalmatica

are considered.

KEY WORDS Rissoidae; Alvania; variability; Mediterranean Sea; new findings.

Received 10.11.2014; accepted 01.12.2014; printed 30.12.2014

INTRODUCTION

Alvania Risso, 1826 (Gastropoda Rissoidae) is

a rissoid genus represented in the Mediterranean

Sea by more than 70 species (Gofas, 2014). Its in-

trageneric relationships are still largerly unresolved,

lacking large-scale investigations on anatomical and

molecular grounds. Some widely distributed and

polymorphic taxa are probably complex of cryptic

species while others often form quite uniform

groups of species with not clear interspecific bound-

aries. Most of the latters have been recently de-

scribed with very limited ranges.

Alvania dalmatica Buzzurro et Prkic, 2007 was

described from some Dalmatian islands (Croatia),

from bottoms rich of Corallium rubrum (Linnaeus,

1758) (Buzzurro & Prkic, 2007), no further records

are known.

It is closely related, on conchological grounds,

to A. hallgassi Amati et Oliverio, 1985 and A. di-

aniensis Oliverio, 1988. All these species occur in

central Mediterrenean and share a paucispiral pro-

toconch sculptured with spiral threads and an ovate-

conical teleoconch with a reticulated pattern,

formed by the intersection of spiral and axial sculp-

tures which are comparable in size.

Alvania hallgassi is known from Ionian coasts

of Southern Italy and Sicily (Amati & Oliverio,

1985; Oliverio et al., 1986; Giannuzzi-Savelli et al.,

1997; Trono, 2006; Cossignani & Ardovini, 2011;

Scuderi & Terlizzi, 2012) and reported from central

Tyrrhenian Sea (Scaperrotta et al., 2012). Alvania

dianiensis is distributed along Tyrrhenian coasts

from southern France to Sicily and recently found

in northern Adriatic Sea (Oliverio, 1988; Buzzurro

et al., 1999; Cossignani & Ardovini, 2011; Micali

& Siragusa, 2013; pers obs.).

Relying on published data, the three species can

be characterized by shell morphology, habitat and

distribution, as reported in Table 1 .

510

Luigi Romani

Alvania dalmatica

Alvania hallgassi

Alvania dianiensis

Total height

2. 6-3. 5 mm

2-2.3 mm

2-2.4 mm

Teleoconch whorls

3.6

3.2

Number of axial ribs on

the last whorl

16-17

15-30

14-23

Spiral cords on the last

whorl

7-9

8-11

6-7

Spiral cords above

the aperture

4-5

4-7

Denticles in the

outer lip

Yes

Protoconch whorls

1.4

1.5

Protoconch spiral

threads

6-7, running throughout

its extension

5-6, the nucleus with only

the first and last threads

5-6, running throughout its

extension

Protoconch interspaces

smooth

papillose

Colour

Background light yellow

with two small darker bands

(one sutural and one basal)

Background yellow with two

darker bands (one sutural

and one basal)

Whitish-yellowish, uniform

Habitat

Corallium rubrum

photophilic algae

Depth

60-90

down to 20

18-48

Distribution

Dalmatian coasts

Ionian Sea

Tyrrhenian and Ligurian seas

Table 1. Characters of Alvania dalmatica, A.hallgassi, A. dianiensis from literature.

MATERIAL AND METHODS

All shells were found in bottom samples col-

lected by SCUBA diving. The protoconch whorls

are counted according to the method as described

by Verduin (1977).

Examined material. A. dalmatica. 4 shs from

Lastovo Island (Croatia), 60-90 m, in CBC and

SBC; 80 shs from Skeloudi Island (Paleokastritza,

Corfu, Greece), 40-50 m, Kolowri island (Pale-

okastritza, Corfu, Greece), 53 m, Liapades reef off

Cape Agios Iliodoros (Liapades, Corfu, Greece),

45 m, in SBC and ARC.

Alvania cf. hallgassi- dalmatica. About 40 shs

from the aforementioned Corfu localities, dates

and collectors, in SBC and ARC; about 15 shs

from Lastovo Island (Croatia), 40 m, in SBC.

Alvania hallgassi : holotype (MCZR); more

than 180 shs from the aforementioned Corfu local-

ities, dates and collectors, in SBC and ARC; about

200 shs from Punta Campanella and Scoglio

Vervece (Naples, Italy), 50 m, in SBC and ARC;

about 150 shs from Lastovo Island (Croatia), 40

m, in SBC; 6 shs from Gallipoli (Lecce, Italy), 80

m, in CBC; 2 shs from Torre Suda (Lecce, Italy),

82 m, in APC; 4 shs from Cannizzaro (Catania,

Italy), 35 m, in LRC; 2 shs from Scilla (Reggio

Calabria, Italy), 50 m, in LRC.

Alvania dianiensis. some hundred shs from

Palinuro (Salerno, Italy) 30 m, in SBC and CBC; 8

shs from Giglio Island (Grosseto, Italy), in SBC and

CBC; 15 shs from Cres (Croatia), 36 m, in ESC.

Alvania oliverioi. 10 shs from Protaras (Cyprus),

25 m, in SBC and CBC; 2 shs from N Cyprus, 2-6

m, in CBC.

Alvania dalmatica (Rissoidae): range extension, shell variability, habitat and relationships with A. hallgassi

511

ABBREVIATIONS AND ACRONYMS. APC:

Attilio Pagli collection (Lari, Italy); ARC: Alessan-

dro Raveggi collection (Florence, Italy); CBC:

Cesare Bogi collection (Livorno, Italy); FSC:

Franco Siragusa collection (Livorno, Italy); LRC:

Luigi Romani collection (Lucca, Italy); SBC: Ste-

fano Bartolini collection (Florence, Italy); MCZR:

Zoological Museum Rome, Italy; shs: shells.

DISCUSSION

Alvania dalmatica original description was based

on the holotype, with no mention of the other shells’

features (except size), so the morphological vari-

ability of the species cannot be properly assessed.

It’s however supposed to be veiy limited. Despite the

low number of the examined topotypical shells, they

match very well with the original description and

show a great uniformity (Table 2, Figs. 1-8).

The greek shells share all diagnostic characters

with topotypical A. dalmatica : paucispiral proto-

conch sculptured by spiral threads and smooth in-

terspaces (Fig. 13); teleoconch with quite regular

cancellate sculpture, axial microsculpture on the

surface among spiral and axial ribs, outer lip inter-

nally lirate and thickened. While the protoconchs

are very uniform in the two samples, the teleo-

conchs show a far greater variability previously

unreported, both in size, sculpture and colour (Table

2, Figs. 1-8). Measured shells are fully developed

adult (labial lirae and varix present) but their av-

erage size is lower than topotypical ones, altough it

varies considerably.

Shells outline is more or less slender (Figs. 5,

8), while the number of labial lirae is regularly

lower, probably due to the smaller size. The genesis

of the spiral chords follows the same pattern in both

samples: two chords starting immediately after

metamorphosis, later a third chord rising between

them; finally in a few specimens a fourth and/or a

fifth chord appearing. The teleoconch sculpture is

highly variable due to the interaction between axial

and spiral elements: from coarse and sparse (Figs.

2, 5, 7) to quite delicate and close-set (Fig. 6).

The number of spiral cords is on average lower

compared to the Croatian shells but the appearance

of the 3rd one is far more variable as well as well

as the number of axial ribs. Consequently the spiral

cords above the aperture numbering from 2 (Fig. 2)

to 4 (Fig. 4) or 5 (Fig. 6), most commonly 3 with

an incipient subsutural chord (Fig. 3). The intersec-

Alvania dalmatica

Croatia (4 shs)

Alvania dalmatica

Greece (70 shs)

Total height

3.2-3. 5 mm

2.3-3. 1 mm (average 2.7 mm)

Teleoconch whorls

3.7-4

3.1-4 (average 3.5)

Number of axial ribs on the last whorl

16-17

13-22 (average 17.5)

3rd spiral cord appearance (whorl)

1.5-1. 7

1.3-2. 7 (average 1.9)

Spiral cords on the last whorl

8-9

5-9 (average 6.7)

Spiral cords above the aperture

2-5 (average 3)

Number of lirae in the outer lip

9-11

7-8

Protoconch diameter

400-410 pm

380-410 pm (average 400 pm)

Nucleus diameter

130-140 pm

Protoconch whorls

1.4-1. 5

1.3-1. 5 (average 1.5)

Protoconch spiral threads

6-7

Table 2. Shell morphological features of Alvania dalmatica.

512

Luigi Romani

tions are generally nodulous, but varying from weak

and barely raised (Fig. 6) to strong and somewhat

spinous (Figs. 2,1). The cancellation from squarish

(Figs. 2, 3) to clearly rectangular (Figs. 7, 8). The

size and sculpture features appear substantially

continuous. The colour also is also not constant:

generally it is uniform whitish to caramel (Figs. 3,

4), some specimens are brownish (Fig. 8), others

have two faint subsutural and columellar hazelnut

bands (Fig. 7), or spiral cords more marked than

background colour (Fig. 5).

Up to now A. dalmatica range was restricted to

south-central Adriatic Sea, with the present note it

is extended 400 km southward into Ionian Sea. This

suggests a wider distribution probably overlooked

due to the confusion with other Alvania species.

Concerning the habitat, A. dalmatica was reported

in exclusive association with Corallium rubrum

and with a restricted bathymetrical range (60-90

m), here it is extended to 40 m depth and corallige-

nous bottoms. Surprisingly no A. dalmatica shells

were found in Lastovo Is., the type locality of the

species. The depth 40 m is shallower than that

reported for the type material but coincide with that

of A. dalmatica from Corfu.

A large population of A. hallgassi was found

simpatrically with A. dalmatica in Corfu. The

shells fit with the original diagnosis in some

respects: paucispiral protoconch (Fig. 14); general

outline; quite delicate, reticulate sculpture with

axial ribs ranging from 20 to 40 (most commonly

around 30) and 8-10 spiral cords on the body

whorl; outer lip relatively thin with a faint external

varix. Yet some features disagree: the total height

is on average greater, spanning from 2.4 mm to 3

mm; the protoconch size and sculpture are sub-

stantially identical to A. dalmatica with spiral

threads all beginning from the nucleus, not only

the first and last ones as stated in the original

description; the outer lip (in fully developed shells,

about 15% of the samples) has inner denticles

(lirae) yet weaker than A. dalmatica. The teleo-

conch sculpture is also quite variable and in some

shells is rather coarse (Figs. 9, 10). The genesis of

the spiral chords is very similar to A. dalmatica

but fourth and/or a fifth chords are present in most

shells (Figs. 9, 11).

The colour in most cases shows typical pattern:

two brown bands (a sutural and a basal) on a yel-

lowish background, but several shells are uni-

formly whitish-yellowish sometimes with spiral

cords darker.

To better place these characters in a more gen-

eral context, A. hallgassi shells from various south-

ern Italy localities were examined: The holotype is

a slightly worn shell with a pebble occluding the

aperture, so it is not very useful in order to examine

these features. But in two large samples very near

the type locality about 20% of fully developed

shells are lirate (50 shs from Punta Faci, 36 m, and

40 shs from Torre del Serpe, 25 m, both south of

Otranto, Lecce, Italy, Macri pers. com.). Alvania

hallgassi from Naples have typical size (maximum

2.2 mm) colour pattern, shell sculpture, but the pro-

toconch is identical to A. dalmatica and a small per-

centage of shells exibit weak denticles in the

aperture. Also A. hallgassi from Sicily share the

same protoconch and denticulation features (the

size of the sample is small, yet two specimens are

weakly lirate). It seems, therefore, that a protoconch

wholly marked by spiral threads biginning from the

nucleus and the presence af labial lirae in a small

percetange of adult shells are typical of the species.

CONCLUSION

Concluding, A. hallgassi and A. dalmatica share

some key diagnostic features (protoconch size/

sculpture and inner lip denticulation). On the other

hand, examining large samples, several specimens

of A. hallgassi and A. dalmatica come close in

terms of sculpture and colour in an apparent contin-

uous spectrum, so being difficult to attribute them

with certainty to each species (Figs. 6, 12); these

latter features indeed are so variable in each indi-

vidual that it’s difficult to use them for diagnostic

purposes. Also some A. hallgassi shells from

Lastovo Is., with particularly coarse sculpture, over-

lap with delicate-sculptured A. dalmatica.

A. dianiensis has a papillose protoconch surface,

no labial denticles and seems to have more uniform

shell sculpture, but Micali & Siragusa (2013) attrib-

uted to A. dianiensis a population from N Adriatic

Sea with a very coarse teleoconch sculpture, largely

different from the typical pattern of the species. So,

in this context, extensive investigations involving

also molecular tools, are desirable to better under-

standing the boundaries within A. hallgassi-dianen-

sis-dalmatica complex of species.

Alvania dalmatica (Rissoidae): range extension, shell variability, habitat and relationships with A. hallgassi

513

Figures 1-12. Alvania spp. Fig. 1. A. dalmatica, Lastovo is., Croatia, 3.3 mm; Figs. 2-8. A. dalmatica, Corfu, Greece, 2.6 mm

(2), 3.2 mm (3), 3 mm (4), 3 mm (5), 2.8 mm (6), 2.7 mm (7), 2.9 mm (8). Figs. 9-10. A. hallgassi, Corfu, Greece, 2.8 mm

(9), 3 mm (10). Fig. 11 .A. hallgassi, Lastovo is., Croatia, 2.9 mm. Fig. 12. A. hallgassi-dalmatica, Corfu, Greece, 2.8 mm.

514

Luigi Romani

Figure 13. Protoconch of A. dalmatica.

Figure 14. Protoconch of A. hallgassi.

ACKNOWLEDGEMENTS

I thank Alessandro Raveggi and Maria Scaper-

rotta who picked and sorted the sediment samples,

Alessandro Raveggi, Stefano Bartolini, Cesare

Bogi, Franco Siragusa, Attilio Pagli for loaning

their material and Stefano Bartolini for taking digi-

tal photographs and composing the plate. I’m grate-

ful to Gabriele Macri, Danilo Scuderi and Daniele

Trono who shared useful information. Bruno Amati

and Enzo Campani for suggestions and for critical

reading of the manuscript. Leonardo Fortunato

improved the english text.

REFERENCES

Amati B. & Oliverio M., 1985. Alvania ( Alvaniello )

hallgassi sp. n. Notiziario C.I.S.Ma, 6: 28-34.

Buzzurro G., Hoarau A., Greppi E. & Pelorce J., 1999.

Contributo alia conoscenza dei molluschi marini

della Rada d’Agay (Francia sudorientale). La

Conchiglia, 31 (291), 36-43, 61-62.

Buzzurro G. & Prkic J., 2007. Anew species of Alvania

(Gastropoda: Prosobranchia: Rissoidae) from

Croatian coast of Dalmatia. Triton, 15: 5-9.

Cossignani T. & Ardovini R., 2011. Malacologia Mediter-

ranea. Atlante delle conchiglie del Mediterraneo -

7.500 foto a colori. L’lnformatore Piceno, Ancona.

537 pp.

Giannuzzi-Savelli R., Pusateri F., Palmeri A. & Ebreo

C., 1997. Atlante delle conchiglie marine del

Mediterraneo. Vol. 2 (Caenogastropoda, parte 1:

Discopoda - Heteropoda). La Conchiglia Ed.,

Roma, 258 pp.

Gofas S., 2014. Alvania Risso, 1826. Accessed through:

World Register of Marine Species at http://www.

marinespecies.org/ aphia.php?p=taxdetails&id= 1384

39 on 2014-10-30

Micali P. & Siragusa F., 2013. Segnalazione di Alvania

dianiensis Oliverio, 1988 in Adriatico settentrionale.

Notiziario S.I.M., 31: 28-29.

Oliverio M., 1988. Anew Prosobranch from the Mediter-

ranean Sea , Alvania dianensis n. sp. Bulletin, Zoolo-

gisch Museum, Universiteit van Amsterdam, 11:

117-120.

Oliverio M., Amati B. & Nofroni I., 1986. Proposta di

adeguamento sistematico dei Rissoidaea (sensu

Ponder) del Mar Mediterraneo. Parte I: famiglia

Rissoidae Gray, 1847 (Gastropoda: Prosobranchia).

Notiziario C.I.S.Ma, 7-8: 35-52.

Scaperrotta M., Bartolini S. & Bogi C., 2012. Accresci-

menti. Vol. IV. L'lnformatore Piceno, Ancona. 185

pp.

Scuderi D. & Terlizzi A., 2012. Manuale di Malacologia

dell'Alto Jonio. Ed. Grifo, Lecce, 188 pp.

Trono D., 2006. Nuovi dati sulla malacofauna del Salento

(Puglia meridionale). Bollettino Malacologico, 42:

58-84.

Verduin A., 1977. On a remarkable dimorphism of the

apices in many groups of sympatric, closely related

marine gastropod species. Basteria, 41: 91-95.

Biodiversity Journal, 2014, 5 (4): 515-520

Mediterranean Umbraculida Odhner, 1939 (Gastropoda

Opisthobranchia): diagnostic tools and new records

Luigi Romani

Via delle ville 79, 55013 Lammari, Lucca, Italy; e-mail: luigiromani78@gmail.com

ABSTRACT Some diagnostic tools are given to distinguish juvenile shells of the Mediterranean Umbra-

culida Odhner, 1939 species (Gastropoda Opisthobranchia) and some new records of rare

species are added.

KEY WORDS juveniles; Mediterranean Sea; new findings; protoconch; Umbraculida.

Received 10.11.2014; accepted 01.12.2014; printed 30.12.2014

INTRODUCTION

The Umbraculida is a small order of opistho-

branchiate molluscs represented in the Mediter-

ranean Sea by 4 species and 2 families: Umbra-

culidae Dali, 1889 comprising Spiricella unguicu-

lus Rang, 1828 and Umbraculum umbraculum

(Lightfoot, 1786) and Tylodinidae Gray, 1847 with

Tylodina perversa (Gmelin, 1791) and Anidolyta

duebenii (Loven, 1846).

Tylodinella trinchesii Mazzarelli, 1897 is an

obscure entity put in synonimy with T. perversa but

still poorly understood (Waren & Di Paco, 1996;

Gofas, 2013).

All species share an uncoiled patelliform or

shield-like shells. Aside from anatomical differences

adult specimens can be easily identified by shell

features (Vayssiere, 1885; Pruvot-Fol, 1954; Waren

& Di Paco, 1996; Valdes & Lozouet, 2000; Cachia

et al., 2001; Da Silva & Landau, 2007) (Table 1, 2

and Figs. 1-9). Juvenile shells (except S. unguicu-

lus) instead are not easily distinguishable from each

other. Flere are provide some information on the

protoconch and early teleoconch morphology to set

some characters useful for specific determination.

MATERIAL AND METHODS

Examined Material. Umbraculum umbracu-

lum : 7 shs, 0.7 mm to 4 mm, Lamaca (Cyprus), 45

m, in ARC; 3 shs, 2.2 mm to 4.7 mm Corfu

(Greece), 40 m, in SBC; 2 shs, 35-65 mm, Isola

delle Femmine (Palermo, Italy), 30 m, SBC; 1 sh,

51 mm, Gorgona is. (Livorno, Italy), 70/80 m, in

ECC; 1 sh, 11.7 mm, Palinuro (Salerno, Italy) 30

m, in CSC; 1 sh, 11.5 mm, Acitrezza (Catania, Italy)

40 m, in CBC.

Spiricella unguiculus. 1 sh, 3.6 mm, Salina

(Messina, Italy), 35 m, in PPC; 1 sh, 2.7 mm, Pal-

inuro (Salerno, Italy), 35 m, in SBC; Castelsardo

(Sassari, Italy), 50 m, 2.6 mm, in CBC; 1 sh, 2.2

mm, Tarifa (Spain), 27 m, in CSC.

Tylodina perversa. 16 shs, Palinuro (Salerno,

Italy), 35 m, in SBC and CSC; 2 shs, Protaras

(Cyprus), 35 m, in SBC; 2 shs, Campomarino

(Taranto, Italy), in SBC; 1 sh, Krk is. (Croatia), in

SBC; 22 shs, Elba is. (Livorno, Italy), in SBC; 1 sh,

Capraia is. (Livorno, Italy), 260 m, in SBC;

Gorgona is. (Livorno, Italy), 150 m, in CSC; 1 sh,

Capraia is. (Livorno, Italy), 150 m, in CSC; lsh,

Almeria (Spain), 110 m, in APC; 2 shs, Capraia is.

516

Luigi Romani

(Livorno, Italy), 180 m, in APC. Shs ranging from

l. 5 mm to 25 mm.

Anidolyta duebenii. 3 shs, 5 mm, 3.2 mm and

3.1 mm, Almeria (Spain), 110 m, in APC and SBC;

1 sh, 3.3 mm, Scoglio Vervece (Naples, Italy), 51

m, in APC; 1 sh, 8.3 mm, Capraia is. (Livorno,

Italy), 300 m, in CSC; 2 shs, 1.3 mm and 3.2 mm,

Pianosa is. (Livorno, Italy), 400 m, in RRC.

ABBREVIATIONS AND ACRONYMS. APC:

Attilio Pagli collection (Lari, Italy). ARC: Alessan-

dro Raveggi collection (Florence, Italy). CBC:

Cesare Bogi collection (Livorno, Italy). CSC: Carlo

Sbrana collection (Livorno, Italy). ECC: Enzo

Campani collection (Livorno, Italy). PPC: Paolo

Paolini collection (Livorno, Italy). RRC: Romualdo

Rocchini collection (Pistoia, Italy). SBC: Stefano

Bartolini collection (Florence, Italy). sh(s): shell(s)

DISCUSSION

Umbraculum umbraculum juveniles (Figs. 10-

1 3) can be easily recognized by the protoconch size,

by far the largest of the considered species. It is quite

variable in size ranging from 630 pm to 710 pm

(average 670 pm) in maximum diameter, composed

by 1 .3-1 .5 whorls, globose (nucleus not prominent),

quickly expanding, glossy, thin and semitransparent,

colour light brown. A shallow depression is present

beyond the protoconch-teleoconch border. Shell up

to 3-4 mm, more elevated, somehow capuliform,

quite thin, of the same color of the protoconch, then

increasingly flat, greyish and thicker.

Spiricella unguiculus juveniles are unmistak-

able, having basically the same silhouette of adut

shells with the protoconch arranged in the horizon-

tal plane, adherent to the surface of the teleoconch.

Tylodina pervert juveniles (Figs. 14, 16, 19)

are similar in outline to U. umbraculum but the pro-

toconch is smaller, ranging from 360 pm to 400 pm

(aver-age 370 pm) in maximum diameter. It is com-

posed by 0.9-1 . 1 whorls, globose (nucleus not prom-

inent), not quickly expanding. It is quite protruding,

glossy, thick, not transparent, white or yellowish

uniform in colour. Teleoconch is thickened in apical

region becoming th inn er toward the margin, its

profile is very variable, from extremely flat to rather

conical. Colour varies from white to brownish. The

muscle scar marks are obvious and often make in-

ternal surface quite uneven.

Anidolyta duebenii juveniles (Figs. 15, 17, 18)

have a protoconch ranging from 350 pm to 400 pm

(aver-age 370 pm) in maximum diameter composed

by 0. 9-1.1 whorls, substantially comparable to T.

perversa in size and form, but some slight differ-

ences can be detected: the nucleus is tinged while

the remaining of the protoconch and teleoconch are

white, the protoconch whorl increases less than T.

perversa so the apex has apparently a more promi-

nent aspect, whit a clear “neck” on the protoconch-

Shell features

Umbraculum

umbraculum

Spiricella unguiculus

Tylodina perversa

Anidolyta duebenii

Size (average)

50-70 mm

4-7 mm

15-20 mm

8-10 mm

Outline

oval

subrectangular

oval

profile

depressed

depressed, arched

Conical to depressed

regularly conical

apex

pointed, slightly

excentric

flat, strongly excentric

pointed, slightly

excentric

pointed, slightly

excentric

surface

dull, with only concen-

tric growth lines

Quite glossy, with only

concentric growth lines

glossy, with only con-

centric growth lines

glossy, with only con-

centric growth lines

colour

grey-yellowish

whitish-yellowish

white

Periostracum

Thick, felt-like, dark

brown

Thin, transparent

Thick, membranaceus,

purple-reddish, often

banded

thin, transparent

Muscle scar

Circular, discontinuous,

many strong scars

horseshoe-shaped

Circular, complete,

quite strong, with sinus

Circular, omplete, very

faint, no sinus

Table 1. Shell features of the Mediterranean Umbraculida (adult shells).

Mediterranean Umbraculida Odhner, 1 939 (Gastropoda Opisthobranchia): diagnostic tools and new records

517

Figures 1-3. Umbraculum umbraculum, isola delle Femmine, Palermo, Italy, 65 mm (Figs. 1, 2), 35 mm (Fig. 3).

Figs. 4-6. Tylodina perversa, Krk is., Croatia, 25 mm. Figs. 7-8. Anidolyta duebenii, Capraia is., Livorno, Italy, 8.3 mm.

Fig. 9. Spiricella unguiculus, Castelsardo, Sassari, Italy, 2.6 mm.

518

Luigi Romani

Figures 10-13. Umbraculum umbraculum juvenes, Corfu, Greece, 4 mm. Figures 14, 16, 19. Tylodina perversa juvenes,

Elba island, Italy, 1.8 mm (Fig. 14), 3.6 mm (Figs. 16, 19). Figures 15, 17, 18. Anidolyta duebenii juvenes, Almeria, Spain,

3.2 mm.

Mediterranean Umbraculida Odhner, 1 939 (Gastropoda Opisthobranchia): diagnostic tools and new records

519

teleoconch border. The teleoconch is more elevated,

regularly conical, uniformly thin. The muscle scar

forms a complete circle, it is very weak and almost

invisible.

Umbraculum umbraculum and T. perversa

young shells could be mistaken but protoconch size

is resolutive, also muscle scar sinus is important,

already visible in few mm specimens. T. perversa

and A. duebenii are obviously the most difficult

species to separate having the protoconch of the

same size but the colour of the nucleus and promi-

nence could be useful tools to distinguish them.

Moreover shell profile, thickness and muscle scars

help distinguishing also very small shells. Anidolyta

duebenii records are deeper than 100 m (the Naples

record is unusually shallow) but bathymetry is mis-

leading in order to separate it from T. perversa , as

dead specimens of the latter can be found at depths

greater than 250-300 m. Most A duebenii records

examined in collections are actually T. perversa orig-

inating from deep water.

Spiricella unguiculus is a very rare species, with

a lusitanian distribution, recorded in literature for

few scattered shells. It’s biology and ecology are

virtually unknown as no living specimens have

been found so far. Its systematic position in Umbra-

culidae is doubtful judging by shell characters and

only tentative lacking anatomical and molecular

data (Tringali, 1990; Da Silva & Landau, 2007 and

references therein; Cossignani & Ardovini, 2011).

With the present note its range is extended to

northern Sicily and southern Spain.

1 . Protoconch larger than 600 pm

Umbraculum umbraculum

- Protoconch smaller than 600 pm 2

2. Protoconch smaller than 350 pm, recumbent

Spiricella unguiculus

- Protoconch larger than 350 pm, raised 3

3. Protoconch color uniform, less promi-

nent Tylodina perversa

- Protoconch nucleus tinged, more promi-

nent Anidolyta duebenii

Table 2. Key of the Mediterranean Umbraculida

based on the protoconch features.

Anidolyta duebenii is an uncommon species

living in deepwaters, spanning from Norwegian Sea

to Lusitanian seamounts and Mediterranean Sea

(Waren & Di Paco, 1996; Beck et al., 2006). The few

mediterranean records are from Spain and Corsica

(Waren & Di Paco, 1996; Penas et al., 2006; Penas

et al., 2008). It’s now reported from Gulf of Naples

and confirmed from Northern Tyrrhenian Sea.

ACKNOWLEDGEMENTS

Stefano Bartolini, Cesare Bogi, Enzo Campani,

Attilio Pagli, Paolo Paolini, Alessandro Raveggi

and Carlo Sbrana are thanked for making available

material for this study. Marco Oliverio, Morena

Tisselli, Maurizio Forli and Maurizio Sosso for use-

ful discussion. A special thanks to Pasquale Micali

for his precious suggestions which clarified much

of my original doubts. I’m grateful to Stefano

Bartolini for taking digital photographs and com-

posing the plates.

REFERENCES

Beck T., Metzger T. & Freiwald A., 2006. Biodiversity

inventorial atlas of macrobenthic seamount animals.

Available online at: http://wwwl.uni-hamburg.

de/OASIS/Pages/publications/BIAS.pdf [Accessed:

30-10-2014],

Cachia C., Mifsud C. & Sammut P., 2001. The Marine

Mollusca of the Maltese Islands Part 3: Sub-class

Prosobranchia to sub-class Pulmonata, order Basom-

matophora. Backhuys Publishers, Leiden, 266 pp.

Cossignani T. & Ardovini R., 2011. Malacologia Mediter-

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7500 foto a colori. Ancona, L'informatore Piceno.

536 pp.

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tropoda, Umbraculidae) and climate change: filling

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Rubio F., Salas C., Sierra A. & Gofas S., 2006. Molus-

cos marinos de la isla de Alboran. Iberus, 24: 23-151.

Penas A., Rolan E. & Ballesteros M., 2008. Segunda

adicion a la fauna malacologica del litoral de Garraf

(NE de la Peninsula Iberica). Iberus, 26: 15-A2.

520

Luigi Romani

Pravot-Fol A., 1954. Mollusques Opisthobranches.

Faune de France. Lechevalier, Paris. 58: 1-460.

Tringali L., 1990. Breve nota sul ritrovamento di due

interessanti micromolluschi nel Mar Tirreno. No-

tiziario C.I.S.M.A., 12: 13-16.

Valdes A. & Lozouet P., 2000. Opisthobranch molluscs

from the tertiary of the Aquitaine basin (South-West-

ern France), with descriptions of seven new species

and a new genus. Palaeontology, 43: 457-479.

Vayssiere A., 1885. Recherches zoologiques et

anatomiques sur les mollusques Opisthobranches du

Golfe de Marseille. Pt. 1, Tectibranches. Annales du

Musee d'Histoire Naturelle de Marseille, Zoologie 2,

Mem. 3: 1-181, pis. 1-6.

Waren A. & Di Paco G., 1996. Redescription of

Anidolyta duebeni (Loven), a little known notap-

sidean gastropod. Bollettino Malacologico, 32: 19-

26.

Biodiversity Journal, 2014, 5 (4): 521-524

New records of Ceratocanthinae (Coleoptera Scarabaeoidea

Hybosoridae) from Arunachal Pradesh (India) with descrip-

tion of a new species of Pterorthochaetes Gestro, 1 898

Alberto Ballerio

Viale Venezia 45, 25123 Brescia, Italy; e-mail: alberto.ballerio.bs@numerica.it

ABSTRACT In order to publish data to be included in the forthcoming new edition of the Catalogue of

Palaearctic Coleoptera, Madrasostes feae (Gestro, 1898) and Pterorthochaetes dembickyi

n. sp. (Coleoptera Scarabaeoidea Hybosoridae Ceratocanthinae) are recorded from Arunachal

Pradesh (India).

KEY WORDS Palaearctic region; Pterorthochaetes ; Madrasostes', new species.

Received 25.11.2014; accepted 09.12.2014; printed 30.12.2014

INTRODUCTION

After the publication of new data on Palaearctic

Ceratocanthinae (Coleoptera, Scarabaeoidea, Hy-

bosoridae) (Ballerio, 2014) to be included in the

forthcoming second edition of the Catalogue of

Palaearctic Coleoptera by Lobl and Smetana, some

new data on Ceratocanthinae from Arunachal

Pradesh (an Indian region belonging to the Palaearc-

tic region) were obtained by examining unidentified

material kept in ZFMK collection. The purpose of

this note is therefore to describe a new species of

Pterorthochaetes Gestro, 1898 and to provide new

faunistic data on Madrasostes feae (Gestro, 1898)

based on the aforementioned new Indian material.

Poggi (2010) demonstrated that the correct date

of publication of the names contained in Gestro's

revision of Asian Ceratocanthinae (which includes

also Pterorthochaetes and M. feae) is 1898 and not

1899, as previously reported.

MATERIAL AND METHODS

I refer to Ballerio (2013) and references therein

quoted for methods and terminological conven-

tions.

Habitus photographs were taken with a Canon

Eos D5 Mil with a macro objective MP 65 mm, all

photos were then mounted with the Zerene Stacker

software and cleaned and unmasked using a photo

processing software.

ABBREVIATIONS. EL: maximum elytral

length; EW: maximum total elytral width; HL:

maximum head length; HW: maximum head width;

L: length; PL: maximum pronotal length at middle;

PW: maximum pronotal width at middle; W: width;

ZFMK: Zoologische Forschungsmuseum Alexan-

der Koenig collection, Bonn, Germany.

RESULTS

Madrasostes feae (Gestro, 1898) (Fig. 1)

Examined material. 1 male and 1 female

(ZFMK): NE India, Assam- Arunachal border,

Bhalukpong, 150 m, 27°00'48"N 92°39'08 M E, L.

Dembicky leg., 1-8.V.2012.

522

Alberto Ballerio

Remarks. First record for Arunachal Pradesh.

Madrasostes feae was previously known from

Nepal, NE India (Uttarakhand, Meghalaya and

Sikkim), Myanmar, Thailand and Kampuchea

(Ballerio, 2014).

Pterorthochaetes dembickyi n. sp.

Examined material. Holotypus, male, in coll.

ZFMK: NE India, Arunachal Pr., Etalin vicinity,

700 m, 28°36'56"N 95°53'21"E, L. Dembicky leg.,

12-25.V.2012. Allotypus in ZFMK, same data as

holotypus.

Description of holotypus (Figs. 3-6). HL: 0.9

mm; HW: 1.8 mm; PL: 1.6 mm; PW: 2.9 mm; EL:

3.3 mm; EW: 2.9 mm. Large sized Pterorthochaetes,

surface shiny, setose; volant. Dorsum black, seta-

tion yellowish-brown, sternum reddish-brown, an-

tennae and tarsi reddish-brown. Head: subpen-

tagonal, wider than long, fore margin finely ser-

rated, tip acute, interocular distance about 10 times

the maximum width of dorsal ocular area, dorsal

ocular area large, dorsal sculpturing of head distally

made of very coarse and deep transverse wrinkles

and proximally of impressed small dense mixed

comma-shaped and horseshoe-shaped punctures

centrifiigally oriented, each one having a pore in the

internal side, bearing an erect simple short seta.

Pronotum: wider than long (W/L ratio= 1.8),

fore angles normally shaped, pronotal lateral mar-

gins fringed with a row of short simple setae,

spaced out by an interval about their length or

longer, disc of pronotum covered by dense im-

pressed ocellate transverse small punctures larger

at sides of disc and becoming horseshoe-shaped

large punctures, with opening outwards, towards

pronotal base and sides, each puncture with a pore

in the middle bearing a gently clavate medium sized

erect seta; punctation relatively dense, the distance

between punctures being subequal to their diameter

on disc and inferior to their diameter at sides.

Scutellum: punctures transversely horseshoe-

shaped, sparse, thick and coarse. Elytra: shape oval,

longer than wide (W/L ratio= 0.8); elytral surface

covered by dense punctation, made of medium

sized impressed horseshoe-shaped punctures with

opening directed outwards, horseshoe branches

short, punctures spaced out by an interval larger

than their diameter, horseshoe-shaped punctures

mixed with a few simple shallow small punctures

irregularly distributed. Each horseshoe-shaped punc-

ture containing a pore bearing a gently clavate long

erect seta.

Male genitalia: spiculum gastrale as in figure 1 1 ,

parameres asymmetrical, as in figures 7-9, internal

sac with an elongate narrow sclerite, as in figure 10.

Variability. Allotypus: overall morphology as

in the description of holotypus. Sexual dimorphism

as in all other Pterorthochaetes. Bursal sclerites

slightly asymmetrical, with a dorsal sharp projec-

tion and shaped as in figure 12.

Comparative notes. Pterorthochaetes dembickyi

n. sp. is mainly characterized by the shape of bursal

sclerites, shape of parameres and of the sclerites of

internal sac of aedeagus, which isolate the new

species from all other known Pterorthochaetes. As

regards outer morphology, the size, the setation of

pronotal margins and the punctation pattern of ely-

tra and pronotum allow us to place this new species

near P. septemtrionalis Ballerio, 1999 and P. yun-

nanensis Ballerio, 2014.

The new species can be easily distinguished

from P. septemtrionalis because the latter has

much denser and larger elytral punctation, elytral

horseshoe-shaped punctures have branches longer

and the opening is directed mainly backwards

(and not outwards as in the new species), while

differences from P. yunnanensis are subtler,

consisting in the shape and density of simple ely-

tral punctures: in P. yunnanensis they are much

more impressed and denser than in P. dembickyi

n. sp., also horseshoe-shaped punctures are

slightly denser and larger in P yunnanensis. The

strong differences in the shape of bursal sclerites

and, for P. septemtrionalis and P. dembickyi n. sp.,

in the shape of parameres and of sclerites of

internal sac of aedeagus (in P. yunnanensis the

male is unknown) do not allow any confusion be-

tween the new species and P. septemtrionalis and

P. yunnanensis.

Etymology. Noun in the genitive case. Dedi-

cated to Lubos Dembicky, who collected the type

series.

Distribution and Habitat. Known only from

the type locality in NE India (Fig. 2). The type

series was collected under the bark of dead trees (L.

Dembicky, pers. comm.), in a montane broadleaf

New records of Ceratocanthinae from Arunachal Pradesh (India) with description of a new species of Pterorthochaetes 523

Figure 1. Madrasostes feae , specimen from Figure 2. Pterorthochaetes dembickyi n. sp., type locality

Bhalukpong, habitus in dorsal view. (photo by L. Dembicky, 2012).

1 mm

Figures 3-6. Pterorthochaetes dembickyn n. sp., holotypus. Fig. 3: extended, dorsal view. Fig. 4: enrolled, ventral view.

Fig. 5: enrolled, dorsal view. Fig. 6: enrolled, lateral view.

524

Alberto Ballerio

Figures 7-10. Pterorthochaetes dembickyi n. sp., holotypus,

parameres. Fig. 7. Dorsal view, Fig. 8. Lateral view. Fig. 9.

Lateral view. Fig. 10. Internal sac (arrow indicates the elon-

gate sclerite).

Figure 11 .Pterorthochaetes dembickyn n. sp., spiculum gas-

trale of holotypus. Figure 12. Pterorthochaetes dembickyn

n. sp., bursal sclerites of allotypus (arrows indicate the dorsal

sharp projection).

forest near Etalin (Mishmi Hills), an area belonging

to the Eastern Himalayan broadleaf forests ecore-

gion (Wikramanayake et al., 2002).

Remarks. I examined other four females of

Pterorthochaetes (ZMFK) from the type locality,

which have bursal sclerites somewhat similar to the

ones of P dembickyi n. sp., although with dorsal

projections stronger, blunter and longer. The outer

morphology is quite different, the length is shorter

(about 1 mm shorter), elytral horseshoe-shaped

punctures are larger and pronotum has larger

horseshoe-shaped punctures at the sides, with open-

ing wider, and a few wrinkles near fore angles.

Based on what we know about intraspecific mor-

phological variation in the genus Pterorthochaetes ,

it is more likely that those females represent a dis-

tinct new species rather than an extreme variation

of P. dembickyi n. sp. Because of this I excluded

those females from the type series.

ACKNOWLEDGEMENTS

I would like to thank Dirk Ahr ens (ZFMK) and

Lubos Dembicky (Moravske zemske muzeum,

Brno, Czech Republic) for the loan of material and

information. Special thanks to Ignazio Sparacio

(Palermo, Italy) for editorial assistance.

REFERENCES

Ballerio A., 2013. Revision of the Australian Ceratocan-

thinae (Coleoptera, Scarabaeoidea, Hybosoridae).

ZooKeys, 339: 67-91.

Ballerio A., 2014. New data on Palaearctic Ceratocanthi-

nae with description of a new species from China

(Coleoptera: Scarabaeoidea: Hybosoridae). Koleopterol-

ogische Rundschau, 84: 277-280.

Gestro R., 1898. Sopra alcune forme di Acanthocerini.

Annali del Museo Civico di Storia Naturale di

Genova, 39: 450-498.

Poggi R., 2010. Gli Annali pubblicati dal Museo Civico

di Storia Naturale “Giacomo Doria” di Genova: storia

del periodico ed indici generali dei primi cento

volumi (1870-2009). Annali Museo civico Storia

naturale “Giacomo Doria”, 101: 1-530.

Wikramanayake E., Dinerstein E., Loucks C.J., Olson D.

M., Morrison J., Lamoreux J., McKnight M. &

Hedao P., 2002. Terrestrial Ecoregions of the Indo-

Pacific. A Conservation Assessment. Island Press,

Washington, 643 pp.

Biodiversity Journal, 2014, 5 (4): 525-532

Biological diversity of the National Park of El-Kala (Algeria),

valorization and protection

Sarri Djamel 1 *, Djellouli Yamna 2 & Allatou Djamel 3

'Department of Nature and life Sciences, Faculty of Science, University of M’Sila, Algeria; e-mail: djamel_sarri@yahoo.fr

2 Social science and Faculty of Arts. University of Maine, Mans. France; e-mail: Yamna.djellouli@univ-lemans.fr

department of biology, Faculty of Science.University Constantine 1, Algeria; e-mail: djalatou@yahoo.fr

‘'Corresponding author

ABSTRACT The National Park of El-Kala (PNEK, biosphere reserve) conceals a remarkable biological

and cultural richness. The investigations carried out through its territory (1996-2010) made

it possible to count 1590 vegetable species (distributed among spontaneous vascular and

introduced plants, mushrooms, lichens, algae and phytoplankton) as well as 7 1 8 animal

species. Several of these species, vegetable and animal, are protected in Algeria and belong to

the red list of the I.U.C.N. (International Union for Conservation of Nature). The safeguarding

and valorization of this richness require the installation of a management plan in adequacy

with the International Conventions of biological diversity within the framework of the durable

development, i.e. to protect and develop the natural wealth by involving residents of the

park.The aim of this paper is to present a detailed study of the flora and fauna of the entire

ecosystem of the PNEK. We insist on the considerable importance that flora and fauna bring

to the socio-economic life of the area and to its inhabitants.

KEY WORDS durable development; National Park El-Kala; natural diversity; safeguarding; valorization.

Received 13.10.2014; accepted 09.12.2014; printed 30.12.2014

INTRODUCTION

This work is an outline of a study entitled

“Durable development in the protected area of

Algeria, the case of the National Park of El-Kala

(PNEK) and the bordering areas of important eco-

logical interest”. The principal thing before any in-

tervention of valorization or protection of the

natural resources is to make a full inventory and

analysis on the biological diversity of the PNEK.

On the basis of prospection on the ground and

examination of several works and papers realized

in the area (Aouadi, 1989; Debelair, 1990; Miri,

1996; Samraoui & de Belair, 1997; Kadid, 1999;

Rezzig, 1999; Boutabia, 2000; Benyacoube &

Chabi, 2000; Sarri, 2002) and other various docu-

ments on flora of Algeria (Battandier & Trabut

1902; Maire 1952; Quezel & Santa, 1962), we tried

to inventoiy and make an assessment on the natural

richness of the PNEK, as well as a collection of the

various national and international legislative texts

which can intervene for better management and

protection of this protected surface.

The analysis of these data allowed us to make

preliminary proposals, which concern the protection

and the rational and durable use of this wealth with

national and international interest, in order to ulti-

mately pass to the phase of inquiries (Questionnar-

526

Sarri Djamel et alii

ies concerning the biodiversity and policy directives

for the durable development).

National Park of El-Kala

Located at the extreme east of Algeria, the Na-

tional Park of El-Kala extends on a surface of

76438 ha. It has some hills, not exceeding 600 m

altitude and three lakes in North, West and East

parts. The southernmost part is strewn with djebels

which culminates with djebel El-Ghorra, 1202 m

(Fig. 1).

The bioclimat is of the soft wet type with sub-

wet heat, the annual temperatures minimal average

reachs 9°C where as the annual maximum average

is 30°C. The annual precipitations average ranges

from 800 to 900 mm, often attaining a maximum of

1300 mm (Aouadi, 1989). According to Belouaham

et al. (2009), the area’s humidity of El-Kala reaches

72.4% which is relatively significant due to the prox-

imity of the littoral and the huge forests and the

whole wetlands surface, which furrow the Park ter-

ritory. Wind, usually frequent, move the dunes,

creating entirely bare spots. This is the case of the

Lake Mellah outlet and te Messida beach.

The Park is characterized by two geological for-

mations: the quaternary one, primarily represented

by marine and river deposits, with the average

Eocene corresponding to clays and sandstones of

Numidia (mainly localized in the bottoms of val-

leys), and the Miocene corresponding to conglom-

erate sands and red clays principally localized in

Southeast. The park’s grounds are those of the

forest, brown washed with a variant of forest humus

mull acid Moder. The National park of El-Kala was

created in 1983 by decree n° 83-462 of July 23rd,

1983, classified as “Reserve of the biosphere”, by

UNESCO, on December 17th, 1990.

The essential objective of the park is the protec-

tion and conservation of the floristic and faunal

components as well as of both the natural environ-

ment and cultural-historical inheritance.

Relatively less marked by the impact of human

activities, this park consists of a mosaic ecosystems

which have great biological and ecological impor-

tance. Here we distinguish:

Mediterranean Sea

Souarekh

Tl-Aioun

Souk

Ain-ELAssel

Echatt

Lac-Des

'iseaux

Cheffia

Asfour

Zilouna

Chilian!

HaiiHiiam *B eni-Salali

/fBouhadjar

'ued%>» .

Tunisia

Algeria

Caption

sector of bougous

sector of brabtia

sector of oum-theboolm

limits of National Parc of El-Kala

lace and stoppings

kilometers

limits of communes

Projection UTM 31 N

Figure 1. Study area: chart of the administrative limits of the wilaya of El-Tarf (Algeria)

with the limits of the National Park of El-Kala.

Biological diversity of the National Park of El-Kala (Algeria), valorization and protection

527

- a marine ecosystem (length of 50 km), contain-

ing a particular flora and fauna (for example: red

coral) not very disrupted (varied submarine habitats

and absence of pollution).

- a dune ecosystem, consisting of a littoral dune

cord still stable (20 to 120 m of altitude), the maquis

of the kermes oak with some testifies of the floristic

procession such as: Quercus coccifera L., Juniperus

phoenicea L., J. oxycedrus L., Pistacia lentiscus L.,

Retama monosperma (L.) Boiss., Ephedra fragilis

Desf., etc...

- a lake ecosystem, constituted by the low marshy

plains and the lakes some of which are classified as

“Ramsar Sites”: lake Oubeira, (2200 ha), lake

Tonga (2600 ha), lake Mellah (860 ha, the only

lagoon in Algeria which communicates with the

sea), Marais of Bourdim (11 ha), Blue lake (3 ha)

and Black lake (6 ha).

These appreciated water tanks constitute a shel-

ter of biological richness and are of great interest

for the park habitats.

- As far as concerns the forest ecosystem, popu-

lating the mountainous zone, of average altitude,

intersected by interior depressions and dominated

by important relieves, the oak cork represents the

climactic forest on siliceous ground. It is replaced

in altitude (700 m) by the Zeen oak ( Quercus fagi-

nea Lam.).

The National Park of El-Kala is one of the most

prestigious protected zones of the Western Mediter-

ranean. It is characterized by the presence of truly

peculiar natural conditions which make it a place

of uncommon biological richness. For this reason,

it can be considereded as one of the highest relict-

ual places of the geological and biogeographical

history of the Mediterranean area (Benyacoube &

Chabi, 2000).

MATERIAL AND METHODS

This work is the result of a set of field and bib-

liographical investigations, including observation

on the field made by us, along with the follow up

of several actions, realized through the territory of

the park, joined to the consultation of several papers

(thesis, dissertation, reports, expertise, etc...) real-

ized in the territory of the park and its nearby, as

well as of all available data on the flora of Algeria

and North Africa.

RESULTS AND DISCUSSION

Floristic diversity of the National park of El-

Kala

The natural vegetation which we meet in dif-

ferent ecosystems of the National Park of El-Kala

is represented by the cork oak which dominates

with other tree species including Zeen oak,

Kermes oak, Pine of Alep, glutinous Alder,

Wilows, white Poplar, and other introduced

species as Eucalyptus , the Acacias, the Maritime

pine and the bald cypress. The floral diversity of

the national park of El-Kala is represented by 1590

botanical species. This figure includes the sponta-

neous botanical species, mushrooms, algae, lichens,

phytoplankton and the introduced or cultivated

vegetable species (Tables 1,2).

The vegetable kingdom is also rich and varied.

The lower plants (Algae, Foams, mushrooms,

Lichens) remain less studied. We count however

more than 175 (Sarri, 2006) species of mushrooms

including Truffles (560 for Algeria) and 117 species

of Lichens (Boutabia, 2000). The Higher Vascular

plants, more than 1050 species (3750 for the flora

of Algeria), were better inventoried including 382

rare and 27 protected species.

The region of El-Kala is itself a "biological cross-

roads", in time (since it reflects the succession of

the climates of Quaternary) and in space (it is char-

acterized by habitats overlap and biogeographic

interpenetrations). Species and their status are

reported in the Tables 1,2.

Biogeography of the vascular vegetable spe-

cies listed in the PNEK

Several authors (see for example: Paccalet,

1981; Ozenda, 1982; Guittonneau, 1982; Quezel,

1957, 1978, 1983, 1993; De Belair, 1995, 1996)

were interested in the study of the biogeography (of

plants and animals) considered by International

Conventions one of the criteria of appreciation of

biological diversity.

For example, Quezel (1978; 1983; 1993) re-

ported that septentrional Africa (Mediterranean and

Saharan) represents at the present time the part of

this continent where biological and ecological di-

versity is most significant (Belouahem et al., 2009)

(Figs. 3-6).

528

Sarri Djamel et alii

VEGETABLE SPECIES

STATUS OF SPECIES

N. of species

by details

N. of species

by groups

VASCULAR PLANTS

Species without status

674

1050 *

Species appearing in the red list (IUCN)

Protected species

Spontaneous medicinal species

Useful spontaneous species

Endemic species - endemic of North Africa

Watery and cultivated species

Fodder species

MUSHROOMS

Species without status

175

LICHENS

Species without status

117

Protected species

ALGAE

Species without status

THEPHYTOPLANKTON

Species without status

INTRODUCED SPECIES

Decorative introduced species

Medicinal cultivated species

SAILOR

Species being reported on appendices II and III of

ASP Protocol (Convention of Barcelona)

TOTAL

1590

Table 1. Floristic diversity of the National Park of El-Kala, Algeria.

*: 1050 for PNEK (3750 for Algeria) including 382 rare, 122 families (128 for Algeria) and 392 kinds (907 for Algeria)

In the present study we report several plants of

different biogeographic origins (Fig. 2). In particu-

lar, the species of Mediterranean origin are most

numerous (445 species which accounts for

42.38%) followed by 5.24% of species of tropical

origin which shows the first origin of the site. The

specific biological diversity observed wihin the

National park of El-Kala (which belongs to Alge-

rian Numidia) is related to the favorable ecological

conditions which allow the preservation of these

species.

In fact, in sub-littoral Numidia both the high

temperatures in summer and the accentuate humid-

ity, due to the dune barrier, combine together to

create a real subtropical climate. On the other hand,

wintry weather conditions (low T°C and high plu-

viometry) contribute to create a remarkable mode-

rate climate (Belouahem et al., 2009).

Note. The presence of the two protected vascu-

lar plants Euphorbia dendroies L. and Orchis

provincialis Balbis is uncertain;

- the truffle Terfezia arenaria (Moris) Trappe

(1971), reported in the littoral dunes of the territory

of the park, represents some sort of curiosity;

- the very few studies on the flora in this region

make our study very difficult;

- the document on flora of Algeria should be up-

dated as based on data by Quezel & Santa (1962-63);

- floristic list may change at any time due to the

large area and its ecological characteristics.

Fauna diversity of the National park of El-

Kala

The most important groups of animals we ob-

served in the National Park of El-Kala include

Biological diversity of the National Park of El-Kala (Algeria), valorization and protection

529

Subdivisions

biogeographic

Numbers by geo-

graphical category

Percentage

Mediterranean

species

445

42.38

Species of

transitions

280

26.66

Scandinavian

species

125

11.90

Endemic species

7.14

Cosmopolitan

species

6.10

Tropical species

5.24

Species without

indications

0.57

11,6

Scandinavian

42.66

Mediterranean

5.24 Tropical

6.1 Cosmopolitan

7.14 Endemic

0.6 without inication

26.66 transition

Table 2. Frequencies and number of species inventoried in

the PNEK by biogeographic subdivisions.

Figure 2. Biogeographic spectrum of the National

Park of El-Kala, Algeria (expressed in %).

Figure 3. Geranium atlanticum B.R., endemic ofN-Africa. Figure 4. Scolopendrium vulgare Sm., very rare species.

Figures 5, 6. Campanula alata Desf., endemic of Algeria-Tunisia, Red List-IUCN.

mammals, insects, reptiles, Amphibians, birds and

fish. We counted up to 706 animal species includ-

ing the zooplankton (Table 3). The National Park

of El-Kala is one of the last refuges for the stag

endemic to Algeria and Tunisia. Forty years ago,

there were more than 300 individuals. This number

fell considerably because of the hunting and the

forest fires. Currently, its number does not reach

30 individuals; maybe less. Several animal species

are endemic to the region, others are more widely

distributed, but they do not live any more in the

area. The faunistic list can change at any moment

seen the importance of the zone for its surface and

ecology (Figs. 7-9).

Protection and valorization of the richness

The years lived in the National Park of El-Kala,

allowed us to gather information about the needs

and the socio-economic activities of the inhabitants

as well as a considerable knowledge on its natural

and even cultural potential.

Rational and durable exploitation of the flora

Several examples can be enumerate:

- the cork oak for its cork;

- heathers for the clothes industry of pipes and

ornament;

530

Sarri Djamel et alii

- fruit trees of forest (Olive-tree, Cane-apple

bush, Myrtle, Hawthorn. . .) for food purposes;

- the medicinal plants (Bay-tree sauce, Laven-

der, Myrtle...) have great potentials (they can be

employed directly, i.e. roots, leaves, flowers, or by

extraction of essential oils and/or substances to be

used for pharmaceutical products);

- decorative plants (including ferns, and many

Liliaceae;

- mushrooms (including truffles) for food pur-

poses;

- olive oil and mastic tree oil.

All plants quoted above can become an impor-

tant source of incomes for the residents (inhabitants

of the park) and thereafter for the investors.

Within the framework of the valorization of the

flora, we also record the various scientific works in

phytochemistry done by national researchers, which

one of the Authors participated to by collecting and

identifying several samples: Genista aspalathoides

Lamk ssp. erinaceoides (Lois.) Maire, Genista

ferox Poirret, Genista ulicina Spach, Genista tricus-

pidata Desf., Serratula cichoracea (L.) DC., Hal-

imium halimifolium (L.) Willk., Matricaria

chamomilla L., etc...

The idea is to create small eco-exploitation

farms or eco-companies which cultivate, protect,

exploit, and trade local products (at the finished or

raw state) in a rational and long-lasting way through

their own territory (in the short and medium term)

and, in the future, towards abroad (in the long term).

Rational and durable exploitation of fauna

Among the animal species occurring within the

Park, the least protected and valued are water birds,

sea and freshwater fish (as the eel), mollusks (as the

clam of the Melah lake) and the deer ( Cervus ela-

phus barbarus Bennett, 1833). The extraction of the

Coral requires some precautions because it is in per-

manent reduction. To avoid the disappearance of the

stag from the National Park of El-Kala and even

from the whole Algeria, a program was set up for

breeding it in captivity and in a so-called “bilateral”

semi-captivity, between the National Park and the

hunting center of Zeralda, with the aim of ensuring

its existence, perenniality and releasing them peri-

odically. Until 2002 it produced more than 50 indi-

viduals.

These results, which are very satisfactory and

encouraging, let us think and suggest that, altough

it ensures a good protection of this animal, with a

rigorous application of legislative texts and the mul-

ANIMAL SPECIES

NUMBER OF SPECIES

OTHER DETAILS

PROTECTED

SPECIES

MAMMALS

(107 for Algeria in [6])

Terrestrial 39

Sailors 04

REPTILES

ET AMPHIBIANS

24 (82 for Algeria)

Reptiles 19

Amphibians 05

INSECTS

215

All groups 215

BIRDS NICHOR

AND MIGRATING

214

(402 for Algeria in [16])

water and forest birds 1 1 7

birds navy 12

Raptors 25

26 and 3 1

FISH

128

marine fish 104

fresh water fish 24

ZOOPLANKTON

Mollusques (clams) 55

Crustacees (crustaceans) 33

Brachinopodes (brachiopods) 03

Tuniciens (tunicates) 03

TOTAL

718

126

Table 3. Faunal diversity of the National Park of El-Kala, Algeria.

Biological diversity of the National Park of El-Kala (Algeria), valorization and protection

531

tiplication of breeding programs, in a short time we

could get to the point where we could see the meat

of the stag for sale from the butcher. Meat which,

in turn, would come from regular regulated and

paying hunting tourism.

Or, still, one can quote another economic activ-

ity practised in the territory of the park representing

a good source of job and currency, i.e., the har-

vesting of snails, which are generally sold at 200

DA for kilo to Tunisians.

The legislative arsenal protecting national parks

(protected areas)

A collection of 133 legislative texts was carried

out. This arsenal of texts reflects the importance of

the national natural inheritance of the national park

of El-Kala. These texts give a great support to the

management of the whole protected area of the

Country. In reality, these laws are constantly disre-

garded (are not met) and do not give any real indi-

cation neither to managers nor to administrations

and residents.

CONCLUSION

The originality of the National Park of El-Kala

returns especially to its biological diversity. A floris-

tic diversity of 1590 vegetable species including

1050 vascular seedlings (27 protected, 80 endemic

and 20 species appearing in the red list (IUCN)),

175 mushrooms, 117 lichens (52 protected), 70

algae, 93 species of phytoplankton, 77 species of

vascular introduced and cultivated plants as well as

eight vegetable sailors species being reported on

Appendix II and III of Protocol of the Convention

of Barcelona.

The faunal diversity is marked by 7 1 8 animal

species including 43 species of mammals (17 pro-

tected), 24 reptiles (3 protected) and Amphibians,

215 insects (13 protected), 214 species of birds

(87 protected), 104 marine fish species (9 protected),

24 fresh water fish species and 92 species of zoo-

plankton. To preserve this originality, the study rec-

ommends creating small Eco-exploitations farms or

eco-companies, which exploit and at the same time

protect this floristic and faunistic richness. One

should not forget that the flora and fauna not only

represent an important source of incomes for the in-

Figure 7. Delicious Lactaire; possibility of potential signifi-

cant culture. Figure 8. Exploitation of light for drying of the

cork. Figure 9. The Barbary stag in semi captivity.

habitants of the park but also can contribute to in the

economic development of country. The knowledge

of faunistic and floristic diversity and of the distri-

bution methods of the fauna and flora of a territory,

532

Sarri Djamel et alii

allows us to have an effective tool for control and

management of the natural habitats.

It is up to people having in charge and managing

the protected areas, and a good information helps

in directing reasoned actions of maintenance of the

Territory. The park of El-Kala is a national heritage.

Unfortunately, today we are witnessing a series of

irresponsible and irrational behaviors that demon-

strate a lack of education and environmental aware-

ness. It is important that people understand that the

peculiarities of PNEK reflect the deep meaning of

Numidia and Krumiria (Northeast Algeria) and

therefore this park is a treasure that must be pro-

tected and defended.

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organisation spatiale. Memoire Ingenieur INA El-

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Biodiversity Journal, 2014, 5 (4): 533-544

Sloth bear, Melursus ursinus Shaw, 1 79 1 (Mammalia Ursidae),

from India: conservation issues and management actions, a

case study

Vikas Kumar 1 *, AmitA. Revale 2 , Sachin K. Singh 2 , Maulik Amlani 2 & Abduladil A. Kazi 2

'College of Forestry, Kerala Agricultural University, Thrissur, Kerala - 680656 India

2 ACHF, Navsari Agricultural University, Navsari, Gujarat - 396450 India

■"Corresponding author, email: vkskumar49@gmail.com

ABSTRACT One of the 12 mega biodiversity centres of the world, India is unique in having four of the

eight bear species (Mammalia Ursidae) that are found in the world. They are brown bear

( Ursus arctos Linnaeus, 1758 s.L), Asiatic black bear ( Ursus thibetanus Cuvier, 1823), sun

bear ( Helarctos malayanus Raffles, 1821) and sloth bear (. Melursus ursinus Shaw, 1791). The

abundance of sloth bear in India, which is also present in Sry Lanka with the endemic sub-

species Sri Lankan sloth bear, M. ursinus inornatus Pucheran, 1855, is determined by its

location within the global distribution range, quantum, quality and continuity of habitat

available and the anthropogenic pressures the species faces. Bears in India are threatened due

to poaching for bear parts, retaliatory killings to reduce conflicts and habitat loss due to

degradation and fragmentation. In addition to these concerns, the rehabilitation of communi-

ties that eke out a living on dancing bears has made bear conservation a challenge in India.

Deforestation and hunting are major threats to bears in India. Unless urgent conservation mea-

sures are taken and degraded forest areas are restored, we suspect that sloth bear may soon

become endangered in India.

KEY WORDS Bear-human interactions; conservation; habitat; management; sloth bear.

Received 15.10.2014; accepted 11.12.2014; printed 30.12.2014

INTRODUCTION

In the world, there are about 5,416 species of

mammals distributed in about 1,229 genera, 153 fam-

ilies and 29 orders (Wilson & Reeder, 2005). Four

hundred and twenty species of mammals (7.75 %

of the world’s mammals) are known from India

(Nameer, 2008). Among the mammals carnivores

are the most widely distributed terrestrial animals

on earth (Schipper et al., 2008). Bears are mammals

that belong to the family Ursidae G. Fischer de Wald-

heim, 1817 and represented by seven living species

that are widely distributed in a variety of habitats

throughout the Northern Hemisphere (Table 1).

Bears are found on the continents of North America,

South America, Europe and Asia. Out of seven

known species of bears, five are seen in India which

includes Himalayan brown bear, Himalayan black

bear, Malayan sun bear, brown bear and sloth bear.

Common characteristics of modem bears include a

large body with stocky legs, a long snout, shaggy

hair, plantigrade paws with five non-retractile claws

and a short tail. The lips are free from the gums and

protrusible. Bears rely principally on their sense of

534

Vikas Kumar et alii

No.

Scientific name

Common

name

Status

1 .

Ursus americanus

Pallas, 1780

American

black bear

Least

concern

Ursus arctos

Linnaeus, 1758

Brown bear

Endangered

Ursus thibetanus

Cuvier, 1823

Asiatic black

bear

Vulnerable

Helarctos malaya-

nus Raffles, 1 82 1

Sun bear

Vulnerable

Melursus ursinus

Shaw, 1791

Sloth bear

Vulnerable

Ursus maritimus

Phipps, 1774

Polar bear

Vulnerable

Tremarctos orna-

tus (Cuvier, 1825)

Spectacled

bear

Vulnerable

Table 1 . Seven species of bears in the world

(Sourse: I.U.C.N., 2012).

smell however the eye sight and hearing are com-

paratively poor (Prater, 1971). Bears are placed in

the order Carnivores but, except for the largely car-

nivorous polar bear, bears are omnivorous, feeding

mostly on plant material, insects, fish, and mam-

mals. They are generally large, stocky, and powerful

animals. All bears are plantigrade, walking on their

entire foot. Their activities are mainly governed by

the availability of food items and directly compo-

nents within their habitat (Joshi et al., 1999b).

Sloth bear ( Melursus ursinus ) is one of the four

bear species found in India and is entirely tropical

in distribution and posses several morphological,

physiological and behavioural adoptions to the trop-

ical habitat. Most sloth bears are found in India and

Sri Lanka (in this island with the endemic sub-

species inornatus Pucheran, 1855, Sri Lankan sloth

bear) but they have also been reported from

Bangladesh, Nepal and Bhutan (Garshelis et al.,

1999a; Johnsingh, 2003; see also http://www.

bearbiology. com). In India, sloth bears are found

from the foothills of Himalayans to the Southern

end of Western Ghats (Yoganand et al., 2006). They

are also found in the Brahmaputra Valley of Assam

(Cowan, 1972; Krishnan, 1972; Brander, 1982). It

may still occur in the wet forest regions of eastern

Bangladesh (Khan, 1982; Servheen, 1990) border-

ing the Mizoram state of India, from where it has

been reported (Yoganand et al., 1999). They appar-

ently favour drier forests and have been reported to

prefer areas with rocky outcrops. In India, 90% of

sloth bear populations are confined in the dry and

moist deciduous forests of which the former

account for 50% of the sloth bear populations. Sloth

bear also occur in tropical evergreen forests, scrub

lands and rocky hills. The bear lives in a variety of

habitat such as Teak forest and Sal forest, lowland

evergreen forest and the hill countiy up to elevation

of 1700 m and riparian forests and tall grass areas

on the floodplains of Nepal (Joshi et al., 1997).

However, their relative abundance varies across

these vegetation types, as indicated by their higher

abundance in deciduous forests, followed by dry

deciduous, scrub and evergreen forests. Recent

local extirpations and population declines have also

been reported from the north-western populations

(in the state of Rajasthan), a few isolated forests in

the northern Western Ghats and adjoining areas,

along the north-western Shivalik hills (no recent

record of sloth bears to the west of the river

Ganga), the northern forested areas of the state of

West Bengal bordering Sikkim and Bhutan, and in

the north-eastern states of India (Yoganand et al.,

1999). To suit the tropics, it has no underfur;

however, it has a long coat that perhaps helps in

defending it from insect bites and also perhaps to

exaggerate its size to predators (such as tiger and

leopard) or conspecifics.

The sloth bear’s low metabolic rate and high

thermal conductance (McNab, 1992) may be advan-

tageous in the hot climates where it lives, in that it

reduces heat production and facilitates heat loss.

Sloth bears seem to also have a behavioural adap-

tation to avoid hot weather conditions in their

habitat by reducing daytime activity.

Clutton-Brock & Harvey (1983) suggested as

advantages of having large body size, we speculate

that the large body size of the sloth bear might help

it to conserve heat; to travel great distances in

search of its dispersed, seasonal food; to enhance

the ability to survive on qualitatively poorer food

of insects and fruits; to enable it to break hard ter-

mite mounds and to dig deep into social insect

colonies; or to help it store fat and live on it during

periods of shortage and during parturition denning.

The potential sloth bear distribution range in India

was estimated to be about 200,000 Km 2 (Johnsingh,

Sloth bear, Melursus ursinus (Mammalia Ursidae), from India: conservation issues and management actions, a case study 535

2003; Akhtar, 2004; Chauhan, 2006). But the recent

surveys indicate the distribution range to be

400,000 Km 2 .

Sloth bear is small bear with a shaggy coat espe-

cially over the shoulders with grey and brown hairs

mixed in with the dark black coat. It has a distinc-

tive whitish or yellowish chest patch in the shape

of a wide U, or sometimes a Y if the lower part of

the white hairs extends down the chest. The snout

is light coloured and mobile. It is thought that the

reduced hair on the muzzle may be an adaptation

for coping with the defensive secretions of termites.

Adult males weight 80-140 Kg and females weight

55-95 Kg (Prater, 1980; Garshelis et al., 1999b).

Physical adaptations for digging and eating insects

include long, slightly curved claws, a broad palate

for sucking, the absence of two front upper incisors

and large protmsible lips (Harris & Steudel, 1997).

Its vernacular name is bhalu (Hindi), Karadi (Tamil

and Malayalam). Mating generally takes place be-

tween May and July and the cubs are bom between

November and January (Jacobi, 1975; Laurie &

Seidensticker 1977; Joshi et al., 1999b).

The actual period of pregnancy is shorter, as the

fertilised egg is implanted after a period of delay

(Puschmann et al., 1977). Similar to what is ob-

served in the temperate bear species. In captivity,

mating pairs come together for only one or two days

during which time there may be considerable vocal-

izing and fighting. Gestation lasts from six to seven

months. Most litters consist of either one or two

cubs, but litters of three cubs have been reported.

Cubs are bom in earth dens and apparently do not

leave them until they are two to three months old.

The cubs stay with their mothers who carry them

on their backs until they are nearly two or more

years of age (Joshi et al., 1999b).

Bears are usually solitary with the exception of

courting individuals and mothers with their cubs.

They are generally diurnal, but may also be crepus-

cular or nocturnal, particularly in and around human

habitations. Bears have excellent sense of small and

are good climbers and swimmers. Many bears of

northern regions go into a period of dormancy dur-

ing winters colloquially called hibernation. Sloth

bears are one of the largest termite-eater among

mammals. A significant portion of then diet consists

of ants and termites (Schaller, 1969; Eisenberg &

Lockhart, 1972; Laurie & Seidensticker, 1977;

Joshi et al., 1999a) and hence the sloth bear is con-

sidered as the only myrmecophagous among Ursi-

dae. Since some Ursids disperse seeds they are con-

sidered to be important seed dispersers for many

tropical plant species where fruits form major part

of their diet (Baskaran, 1990; Willson, 1993; Parley

& Robbins, 1995; Welch et al., 1997; Auger et al.,

2002; Kitamura et al., 2002; Sreekumar & Balakr-

ishnan, 2002; Koike et al., 2008). Around the world,

bears and humans have co-existed for centuries as

evident from the references of bears in ancient art,

culture, folklore, epics, religion and literature. Bears

are good indicators of habitat quality as they occupy

the position of an apex predator in a few ecosys-

tems. They are unique in the sense that they could

feed on plants, prey on other species as well as scav-

enge dead animals.

Sloth bears feed extensively on termites and have

special adaptations for doing this. The naked lips are

capable of protruding and the inner pair of upper

incisors is missing and the inner pair of lower in-

cisors is missing, which forms a gap through which

termites can be sucked. The sucking noises made by

feeding in this manner can apparently be heard from

over 100 meters away. They also eat eggs, other

insects, honey combs, carrion and various kinds of

vegetation including fruits (Gokula et al., 1995;

Joshi et al., 1997). The sloth bears consume plant

species included Cassia fistula L., Zizyphus oenoplia

(L.) Mill., Glycosmis pentaphylla (Retz.) DC.,

Holigarna arnottiana Wall, ex Hook, f., Fins spp.,

Syzygium cumini (L.) Skeels., Grewia tilifolia Vahl,

Mangifera indicaL., Bridelia retusa (L.) A. Juss. and

Cardia dichotoma G.Porst. (Sajeev, 2013).

As a result of the continued habitat destruction

and degradation, sloth bear populations have de-

clined or become fragmented all over and as a

result, they have become locally extirpated in some

areas (Cowan, 1972; Krishnan, 1972; Servheen,

1990; Murthy & Sanlcar, 1995; Garshelis et al.,

1999a; Singh 2001; Johnsing, 2003). Sloth bear is

included in Schedule I of India Wildlife Protection

Act- 1972 and Appendix I of the Convention on In-

ternational Trade in Endangered Species of Wild

Elora and Fauna (C.I.T.E.S.).

POPULATION STATUS AND HABITAT

The Central Zoo Authority (C.Z.A.) is statuary

Ministry of Environment & Forests, Government of

536

Vikas Kumar et alii

India established in 1992 to oversee the functioning

of zoos in India and provide technical assistance.

There are 70 Zoos and five Rescue Centers housing

a total number of 795 individual (as on 3 1st March,

2012) bears in captivity for the purpose of conser-

vation, education to the public and for their lifetime

care (Table 2). The distribution and details of the

bear species housed in various Indian Zoos & Re-

scue Centers are shown in figure 1 and Table 3.

CONSERVATION ISSUES

I. Threats to the species

Sloth bear is protected by inclusion in Schedule

1 of the wildlife (Protection) Act 1972. The sloth

bear population in India is threatened largely by

poaching (Garshelis et al., 1999b). Bears have been

poached for gall bladder and other parts, which are

often exported to South-East Asian countries as an

ingredient to Traditional Chinese Medicines. In the

last five years, poaching and hunting has become

uncommon as reported by the Government of India.

Incidence of sloth bears getting killed by road and

railway hits and electrocution were also noted. In

Odisha, based on only the recorded cases by the

forest department, the total number of sloth bears

killed is over 30 in last five years.

A number of sloth bears (n=8) died in the state

due to road and train accidents in last five years as

recorded by the forest department. It is also reported

that the bears might be poached/hunted in some

areas but access to these areas is limited due to se-

curity issues. Trade of live bear cub and bear body

parts poses a direct threat to the animal and its

future survival in the state. With adjoining state like

Chhattisgarh, Maharashtra and Odisha reporting

presence of illegal trade routes, the trade is likely

to exist in Madhya Pradesh as well. Sidhi, Shivpuri

and Shahdol districts of Madhya Pradesh are con-

sidered sloth bear cub poaching hot spots. The rea-

sons for the lack of information on illegal trade can

be attributed to:

a. Infrequent poaching of sloth bears in the

region.

b. Strong networking among the defaulters that

help them got by unnoticed by the authorities.

c. Because reporting poaching is considered a

disgrace.

The sloth bear has the most widely recorded

SL. No.

Species of Bear

Male

Female

Un-

known

Sex

Total

No. in

Zoos

No. on

Rescue

Centers

No. of

Zoos

No. of

Rescue

Centers

Sloth bear

Melursus ur sinus ur sinus

Shaw, 1791

292

267

562

251

311

Himalayan black bear

Ursus thibetanus laniger

(Pocock, 1932)

106

223

211

Himalayan brown bear

Ursus arctos isabellinus

Horsfield, 1826

Malayan sun bear

Helarctos ma lay anus

malayanus Raffles, 1821

European brown bear

Ursus arctos arctos

Linnaeus, 1758

TOTAL

403

366

795

472

323

97 (70)

6(5)

Table 2. Statuses of bears in Indian Zoos (as on 31st March, 2012).

Sloth bear, Melursus ursinus (Mammalia Ursidae), from India: conservation issues and management actions, a case study 537

distribution range than any of large carnivore in

Central India (Jhala et al., 2011). The erstwhile state

of Madhya Pradesh (undivided Madhya Pradesh in-

cluding Chhattisgarh) had largest sloth bear popu-

lation in this country with the bear inhabiting an

area of 135,395 Km 2 of the forest (Rajpurohit &

Krausman, 2000).

In Central India, sloth bear is locally considered

as one of the most feared and dangerous wild ani-

mals (Bargali et al., 2005). Sloth bear seem to have

a very low tolerance toward humans. Majority of

the HBC cases have occurred either when the

human enters sloth bear habitat or when the sloth

bear enters kitchen gardens in the village home-

steades. Maximum conflict cases have occurred in

the month of March and early April, which coin-

cides with Mahua, Madhuca indica (J. Konig) J.F.

Macbr., season when both bears and human com-

pete for the same resource. The conflict intensity

may raise up to 2.23 cases per day during this

period, while in other months; it comes down to 1 .4

cases/day (Sarkar, 2006).

In Maharashtra, however, bear-human conflict

especially in district of Chandrapur, Gondia, Gad-

chiroli, Bhabdara, Akola and Amravati in the Vi-

darbha region is on the rise. In Tamil Nadu, only

one poaching case was recorded across the state dur-

ing the past five years in Gudalur Forest Division.

Apart from this, two more bears were killed possi-

bly due to conflict in 20 1 0-20 1 1 . A total of 20 cases

of conflict have been recorded in the state in the last

five years (2006-2011) including 19 cases of human

injuries and one case of human death. However,

much information on human-bear conflict is lacking

from this state.

Other edibles valued by bear as well as humans

are Jamun, Syzygium cumini (L.) Skeels., Bair,

Zizyphus spp., Tendu, Diospyros melanoxylon

Roxb, Bel, Aegle marmalos, (L.) Correa, Chironji,

Buchanania lanzan Spreng., and honey. Therefore,

when both human and bear share the same space

and depend on the same resources, the conflict

(human injuries and human death) becomes in-

evitable. Because of such negative interaction,

attrition levels among the locals rise, often leading

to considerable number of bears being persecuted

and killed in retaliation. No poaching of bear or

incident of trade in bear or bear parts has been

recorded by the forest department of Gujarat in

last five years.

II. Threats to the habitats

Implementation of Schedules Tribes and Forests

Dwellers Act, 2006 will also have an impact on bear

converted into arable land. Change in cropping pat-

tern is also harming the bear food availability in the

area. Due to fragmentation of forests, sloth bears

often enter villages to ride agriculture and forage

on wild ficus and horticultural produce being

processed (Mango, Anona, Mahua, Ground nut,

Maize and Sweet potato). Some villagers are now

resorting to alternate crops that do not attract bears.

Large source of bear food is being removed from

around villages intentionally which ultimately will

have a bearing on sloth bear population in Chhat-

tisgarh (Akhtar et al., 2006a).

Outside the protected areas, sloth bear habitat in

territorial forest divisions is facing habitat degrada-

tion due to various activities including anthropolog-

ical pressures from local communities, quarrying of

granite and sandstone, diversion of forest land for

non-forestry purposes and illegal cultivation by

local communities. Due to habitat fragmentation,

Sloth bear populations are getting encircled by agri-

culture activity around foothills of hillocks whereby

they get confined to hill portions like in Jaffarghat

Fort and Warangal District in Andhra Pradesh. The

sloth bear habitat between India and Nepal is con-

nected through northern Bihar (Terai Arc Land-

scape) and the sloth bear population in central and

eastern Indian landscape are connected through

southern Bihar. These sloth bear occupied areas

under threat due to various anthropogenic reasons,

which needs special management emphasis (Gupta

et al., 2007).

The potential sloth bear habitat range in Amnachal

Pradesh is about 1500 Km 2 . Here, sloth bear habitat

is threatened due to slash and bum or jhum cultiva-

tion, deforestation and encroachment. Construction

of roads and infrastructure development, tea plan-

tation and development of human settlements in

foothills and adjacent plains have also threatened

the potential sloth bear habitat, leading to habitat

loss and degradation (Choudhury, 2011).

The sloth bear habitat in Gujarat mostly occurs

in terminating mountain ranges of Arawalis, Sapuda

and Sahiyadri with dry deciduous to moist forest

types. Fmits and other parts of more than 35 plant

species have been reported from here, which is are

consumed by sloth bears (Mewada, 2011).

538

Vikas Kumar et alii

Figure 1. Sloth bear, Melursus ursinus ursinus, distribution in India.

The main issues with the available bear habitat

in the state are pressure on the habitats by livestock

grazing, tourism and developmental activities and

mining, which are reported as major factors leading

to habitat degradation and fragmentation of forest

patches. Out of seven forest divisions with sloth

bear population in this state, forest patches in four

divisions are unprotected and not declared as

sanctuaries.

MANAGEMENT ACTION

Stakeholder involvement in various aspects of

wildlife management can yield many benefits

(Chase et al., 2000). The specific conservation

recommendations for minimizing bear-human con-

flicts and bear habitat conservation are as fol-

lowing.

I. Protection to the species

The sloth bear is listed in Schedule I of the

Indian Wild Life (Protection) Act (Govt, of India,

1972; Govt, of India, 2003), Vulnerable (I.U.C.N.,

2012). Special powers accorded to the forest staff

in Assam have enabled them to patrol the protected

areas more effectively than other parts of the coun-

try. However, in areas outside the protected areas,

lack of and inadequately trained staff hampers

protection measures.

There is no specific strategy for protection of

sloth bear in Bihar (Govt, of Bihar, 2012), Haryana

and Gujarat. However, being found in the protected

areas of the state, the species gets the highest

degree of legal safeguard. Lack of reliable infor-

mation network restricts intelligence-based en-

forcement to control poaching and illegal trade.

Majority of bear habitats fall outside the jurisdic-

Sloth bear, Melursus ursinus (Mammalia Ursidae), from India: conservation issues and management actions, a case study 539

tion of protected area network of the state, they

lack protection equipments, trained man power and

local rescue team. In Andhra Pradesh, the sloth

bear is listed in Vulnerable (A2 cd+4cd; Cl) cate-

gory of I.U.C.N. Red List of threatened species

(Garshelis et al., 2008).

II. Habitat management

The development projects such as roads, irriga-

tion dams, hydro-electric project in the wildlife

sanctuaries are the major threats to bear habitat in

the state of Kerala, Tamil Nadu and Karnataka. The

impact of such developmental activities on sloth

bear status and distribution is not known and often

is ignored. In Gujarat, forest field staffs manage

habitats in almost all the forest divisions, which

include regular monitoring, plantation programs,

often with committee’s involvement. Eco develop-

ment committees, village development committees,

stakeholders groups are formed in each forest divi-

sion to carry out habitat restoration and improve-

ment programs. Community forestry programs,

wherein local people learn the value of planting and

protecting trees, could expand habitat for sloth

bears, and could also reduce the bear-human

interactions. The strength of this approach is that it

is instigated from the bottom up (i.e., people do it

because it benefits them, rather than because it is

mandated), but it also must be supported from the

top down (Poffenberger, 1990).

III. Management of bear-human interactions

No specific management actions have been

taken for sloth bear human interaction in many of

the states such as Arunachal Pradesh, Assam, Bihar,

Jharkhand, Gujarat, Rajasthan, Meghalaya, Naga-

land and Uttrakhand. In Chhattisgarh, there is a

policy for compensation by financial reimburse-

ment in case of human mauling or killing by wild

animals but not for crop depredation; in Mahara-

shtra, Madhya Pradesh, Uttar Pradesh, West Bengal

and Goa state there is a policy for ex-gratia for crop

damage or human causalities due to bear of Rs

1,00,000/-, and up to Rs 75,000/- for permanent dis-

ability due to bear attacks. In addition to the reim-

bursement of medical expenses, forest department

also provides compensation for the loss of man days

incurred by the victim as a welfare scheme.

In Maharashtra, sloth bear is known for its ag-

gressiveness, both towards humans and towards

other large mammals. The survey conducted by

Wildlife Trust of India indicates that between 2006

to 201 1, Gondia has reported the maximum number

of human sloth bear conflict cases (65) followed by

Chadrapur (36) and Bhandara (26). Desai et al.

(1997) reported that bear-human interactions are

very common issue in all districts of Gujarat except

Panchmahal district. The Gujarat states recorded

127 human sloth bear interaction cases in the last

five years, of which 95 were cases of human in-

juries with one casualty (Mewada, 2011). Se-

shamani & Satyanarayan (1997) have reported that

Jharkhand has a long history of the human-bear

conflict but the State does not have effective strat-

egy to deal with the human-bear conflict. According

to Karnataka Forest Department records, the bear-

human conflicts are severe in five districts namely

Chamrajnagar, Chickmagalur, Tumkur (maximum),

Chitradurga and Bellary. In Kerala the forest depart-

ment has provided proper guidance to villagers liv-

ing aroung bear-bearing areas such as Periyar Tiger

Reserve and Parambikulam Tiger Reserve on how

to avoid interaction with sloth bear. The question-

naire survey results shows that in only five out of

34 forest divisions recorded sloth bear-human con-

flict namely Kannur, Wayanad, Palghat, Emakulam

and Kollam. Incident of poaching, confiscation and

retaliatory killings seem to be few in the Odisha and

Tamil Nadu states (Baslcaran et al., 1997). Other

measures to mitigate human bear conflict include

promotion of awareness through various awareness

programmes and hoarding on sloth bear conserva-

tion. In addition in few states forest departments

have provided drums and crackers to villagers to

chase bears away from villages. Andhra Pradesh

Forest Department has made a provision to have a

Conflict Management Team at the Circle level. In

the recent years remote drug delivery devices (tran-

quilizing equipments) have been purchased in

Valmiki Tiger Reserve (Govt, of Bihar).

IV. Research and Information

Scientific information on sloth bear is restricted

to a few status surveys, conflict surveys and short

studies (Gopal, 1991; Johnsingh, 2003; Chauhan &

Rajpurohit, 2006; Dharaiya & Ratnayeke, 2009;

Dharaiya, 2010; Choudhury, 2011).

540

Vikas Kumar et alii

SL.

NO.

ZOO NAME

MALE

FEMALE

UNSEX

TOTAL

Agra Bear Rescue Facility, Agra

139

129

268

Alipore Zoological Garden, Kolkata

Amtes Animal Ark, Wardha

Arignar Anna Zoological Park, Vandalur,

Chennai

Aurangabad Municipal Zoo, Aurangabad

Bhagwan Birsa Biological Park, Ranchi

Bondla Zoo, Usgao

Children Park & Zoo, Gadag

Dr. K. Shivarma Karanth Pililcula

Biological Park, Mangalore

Dr. Shyamaprasad Mukharjee Zoological

Garden, Surat

Gandhi Zoological Park, Gwalior

Indira Gandhi Park Zoo, Rourkela

Indira Gandhi Zoological Park,

Visakhapatnam

Indira Priyadarshini Sangrahalaya,

Anagodu, Davangere Taluk

Jaipur Zoo, Jaipur

Jhargram Zoo, Jhargram

Kamla Nehru Prani Sanghrahalaya Zoo,

Indore

Kamla Nehru Zoological Garden,

Ahmedabad

Kanan Pandari Zoo, Bilaspur

Kanpur Zoological Park, Kanpur

Karuna Society For Animals and Nature-

Rescue Centre, Dist. Anantapuram

Lucknow zoological Park, Lucknow

Maharajbag Zoo, Nagpur

Mahendra Chaudhury Zoological Park,

Chhatbir, Chandigarh

Maitri Baagh Zoo, Bhilai

Mini Zoo A. M. Gudi Balvana,

Chitradurga

Nandankanan Biological Park,

Bhubaneshwar

National Park, Bannerghatta Zoological

Garden, Bangalore

104

Table 3. Records of sloth bear, Melursus ursinus ursinus, in India zoos (continued).

Sloth bear, Melursus ursinus (Mammalia Ursidae), from India: conservation issues and management actions, a case study 541

SL.

NO.

ZOO NAME

MALE

FEMALE

UNSEX

TOTAL

National Zoological Park, Delhi

Nehru Zoological Park, Hyderabad

Pt. Govind Ballabh Pant High

Altitude Zoo, Nainital

Rajiv Gandhi Zoological Park and

Wildlife Research Center, Pune

Ramnabagan Mini Zoo, Burdwan

Sakkarbaug Zoo, Junagarh

Sanjay Gandhi Biological Park, Patna

Sri Chamarajendra Zoological

Gardens, Mysore

Sri Venkateswara Zoological Park,

Tirupati

Tata Steel Zoological Park, Jamshedpur

Thiruvananthapuram Zoo,

Thiruvananthapuram

Tiger & Lion Safari, Shimoga

Van Vihar National Park, Bhopal

Vanavigyan Kendra, Hunter Road,

Hanamkonda, Warangal

Wild Animal Conservation Centre,

Mothijharan, Sambalpur

TOTAL

292

267

562

Table 3 (continued). Records of sloth bear, Melursus ursinus ursinus, in India zoos.

A few intensive studies on sloth bear ecology

were carried out in Panna National Parks (Yo-

ganand et al., 2005) and North Bilaspur Forest Di-

vision (Akhtar & Chauhan, 2000; Akhtar, 2004;

Bargali, 2004; Akhtar, 2006; Akhtar et al., 2008;

Mewada, 2011). However, there is lack of even

basic information on sloth bear presence/ absence

for many areas in North-Eastern states. Information

on population estimates, relative abundance and

monitoring are wanting.

V. Capacity Building

Apart from some wildlife managers and front-

line staff, most of the field managers and staff

require capacity building. Other stakeholders

require sensitization and training in order to help

protection on sloth bear, its habitat and reducing

sloth bear-human conflict.

VI. Awareness Campaign

The majority of the local people are uneducated

as they are primitive tribes of the region and still at-

tached with their ancient culture. Education should

be provides not only for the necessity of protecting

forest habitats in order to ensure the survival of

sloth bear, but also for highlighting the benefits to

people in protecting and managing valuable re-

sources. Sloth bear must be included as a key species

in ongoing awareness campaigns. Local people,

Joint Forest Management Committees, Eco-Devel-

opment Committees, Eco-Clubs and school chil-

dren should be sensitized about sloth bear

542

Vikas Kumar et alii

conservation. Policy makers, judiciary and enforce-

ment agencies may be sensitized on Wildlife crime

and law enforcement. Good quality audio-visual

materials and collaterals (posters, brochures, stick-

ers, etc.) in local language may be produced and dis-

tributed. Awareness campaign should focus on

highlighting damagers in collecting the minor forest

produce from the areas where bears have their dens.

VII. Legislation and Policy

Apart from the awareness and involvement of

local people, the administrative reforms are also

required for effective conservation of bears and

habitat. Despite an array of Policies and Legislation,

conservation efforts for sloth bear and its habitat

have faced limitations due to want of site specific

policies or flexibility in adaptation of existing

policies.

CONCLUSION

Some of the recommendations proposed by

stake holders to control poaching/hunting of bears

included: (i) creating awareness and using local

communities to cub bear hunting/poaching for the

illegal trade in bear parts or live cub trade; and (ii)

strengthening existing network of informers, and

various law enforcing agencies, including monitor-

ing of wildlife crimes at Inter-State check posts and

international borders. To reduce bear-human inter-

actions, the following were recommended: (i)

awareness creation on bear behaviour and the phi-

losophy of co-existence in addition to strengthening

of indigenous conflict reduction measures to reduce

crop and livestock depredation by bears; and (ii)

strengthening the conflict management teams with

equipment, training, and capacity building and im-

provement in the current mechanism of assessment

of economic losses of crop /livestock depredation

by bear and other wildlife. For bear habitat man-

agement the recommendations were to: (i) continue

protection to bear habitats and prevent habitat loss

due to conversion for agriculture/ horticulture and

developmental projects; (ii) restore degraded bear

habitats through existing government programmes

using local communities; and (iii) identify critical

bear habitats and corridors outside PA network and

manage them as Community or Conservation

Reserves with approval and support from local

communities. Similarly, recommendations for re-

search, capacity building, conservation educate and

legislation and policy have been made.

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Biodiversity Journal, 2014, 5 (4): 545-555

Biodiversity of Sudan: between the harsh conditions, political

instability and civil wars

Ahmed A.H. Siddig

PhD candidate, University of Massachusetts Amherst - Dept. Environmental Conservation, 160 Holdsworth Way/ Amherst, MA

01003-9285 U.S.A.; email: asiddig@eco.umass.edu

ABSTRACT More than 90% of the area of Sudan is classified as desert and semi-desert ecosystems, and

desertification is spreading with global climatic changes. Also the country is suffering from

60 years of chronic civil wars and instability. Consequently these situations have severely

affected the status and trend of biological diversity of the country to critical thresholds (i.e.

extinction) as many reports show. Improved knowledge of the current status of biodiversity in

response to such conservation challenges is critically important. In this review, my aim is to

highlight the recent conservation challenges of Sudan as they relate to desertification and civil

wars, and to look at the big picture of the impacts of these challenges to biodiversity conser-

vation in Africa. I then present examples of urgent management interventions and research

needs for better biodiversity conservation. The primary message of this paper is to confirm the

possibility of making conservation actions in these vulnerable areas. It is never too late as long

as there is peace and willingness. This framework could be a model to tackle and analyses bio-

diversity conservation issues in similar cases in the region.

KEY WORDS Africa; Biodiversity conservation; desertification; dry-lands; political instability; Sudan.

Received 17.10.2014; accepted 11.12.2014; printed 30.12.2014

INTRODUCTION

The news coming from Sudan is always about

civil war, political conflicts, awful statistics about

the refugees and displaced people and rarely opti-

mistic. In addition to the political instability, envi-

ronmentally the country is one of the most fragile,

dry and desertified areas in Sub-Saharan Africa,

which leads to high vulnerability to global climatic

changes and extreme events such as drought and

flooding (I.P.C.C., 2013). The United Nations Con-

vention on Combating Desertification (U.N.C.C.D.)

defined dry lands (arid, semi-arid and diy sub-humid

zones) as areas other than polar and sub-polar

regions in which the aridity index (i.e. the ratio of

annual precipitation to potential evapo-transpiration)

falls within the range of 0.05-0.65 (U.N.C.C.D.,

1994). According to this definition, about 93% of

the area of the country is classified as dryland (Table

1), which extends from hyper arid and arid zones in

the north to the semi-deserts in the middle to low

rainfall woodlands savanna in the deep south and

south east (Goda, 2007; Mustafa, 2007).

In addition to the dominant harsh conditions

there are some areas with unique ecological condi-

tions such as mountains, the Nile strip and wetlands

depressions. These areas support vegetation com-

munities and natural habitats that are critical to

maintaining biological diversity, particularly

wildlife and forest resources (Mukhtar & El

546

Ahmed A. H. Siddig

Wakeel, 2002). The forest resources in Sudan were

estimated by F.A.O. in 1990 to be about 19% of the

total area of the northern part of the countiy, but the

current report of U.S.A.I.D. in 2012 showed the

total forested areas of the country have been re-

duced substantially to about 11.6 % (Fig. 1).

Despite the habitat loss and degradation, these

forests are still playing vital enviromnental roles in

biodiversity conservation and combating desertifi-

cation as well as supporting the livelihood of local

communities. For instance the forest products con-

sumption survey conducted by the Forest National

Aridity Zone

Ecosystem type

Area

(Square Km)

% (Area of

the Sudan)

Annual

Rainfall (mm)

Aridity Index

(R=P/PET)

Hyper-arid

Desert

776000

<20

<0.05

Arid

Semi-desert

630000

20 - 100

0.05-0.20

Semi-arid

Grassland Savanna

340000

100-300

0.21-0.50

Dry sub -humid

Low rainfall

woodland Savanna

65000

300 - 500

0.51-0.65

Sub-tropic

High rainfall

woodland Savanna

70000

500 - 800

>0.65

Total

1881000

100

Table 1. Classification and extent of dry lands in Sudan adapted from Ayoub (1998), Mustafa (2007) and Badri (2012).

Figure 1 . The location of Sudan in Africa (left). The map of land cover showing the ecological gradients from the desert in the

north to rainy savannah in the deep south (right). The area of the country divided between 50.7% as desert, 13 % agricultural

lands, 12.6 % grass lands, 10% forests cover, 1 % Water resources. ~ 1% others (i.e. urban areas). Adapted from F.A.O. (2012).

Biodiversity of Sudan: between the harsh conditions, political instability and civil wars

547

Corporation (F.N.C.) in 1995 showed that forests

are the main sources of sawn timber, round poles,

building materials and 87.5% of energy (fuel wood)

to the country. Also about 100 indigenous trees

species provide direct food, oil, honey, fruit, fodder,

gum, fiber, medicine, and tannin agents to the peo-

ple (Badi, 2004). Takona (1999) and Siddig &

Abdellhameed (2013) emphasized the great socioe-

conomic, cultural and heritage values of biodiver-

sity of Sudan, and the value of local markets based

on wildlife products, forest products and fibers craft-

ing materials as an employment opportunity for

many people, especially in rural areas.

Although there are a few efforts by local govern-

mental agencies and NGOs, there are many critical

challenges facing biodiversity of Sudan. First, po-

litical instability and civil wars led the country to

lose about 70% of its biodiversity that was concen-

trated in the southern part, as it became independent

state in 2011 as republic of South Sudan. Severe

wars continue in about 50% of the rest of the coun-

try (8 states out of 15). Second, the combination of

socio-economic (e.g. food insecurity and refugees)

and global environmental factors (e.g. climate

change, drought and desertification) plus the lack

of integrated plans exacerbate the decline of biolog-

ical diversity of the country to critical thresholds

(i.e. extinction). The need to know the current status

of biodiversity in response to such complex politi-

cal and environmental challenges is critically

important. Nimir, (1995), Takona, (1999), Funk et

al. (2011) and Badri (2012) pose many logical

questions on this topic. I suggest that the most im-

portant questions include: What is the current state

of biodiversity of the country in the light of these

wars and harsh conditions? What and where are the

hot spots of conservation? What are the subsequent

challenges facing biodiversity? And most impor-

tantly, how can these challenges will be solved?

This review comes to bring attention to the

impacts of wars combined with harsh conditions on

biodiversity as regional theme with a particular case

of Sudan after July 2011 based on recent govern-

mental and international agencies reports working

in Sudan as well as the domestic literature. The spe-

cific aims of this paper are two-fold. First, I display

and diagnose the most serious challenges of biodi-

versity conservation in the country based on my

point of view. Second, I present a vision of solutions

as a suggested framework for biodiversity conser-

vation, including a top ten management strategies

and urgent research needs.

CONSERVATION CHALLENGES

The critical challenges facing biodiversity in

Sudan are similar to elsewhere in the continent, and

have been listed in Takona (1999), Goda (2000),

Abdelhameed & Nimir (2007), Nur (2007), U.N.E.P.

(2007), and Badri (2012). Although I generally agree

with these previous studies about these problems, I

argue that political conflicts and civil wars is a chal-

lenge that substantially affects everything in the

country including biodiversity. In the following

points I show how continuous conflicts and unrest

directly impact biodiversity conservation:

Species loss and mass extinctions

Almost 60 years of violence led the country to

lose its southern part, and continues in more than

50% of the rest of the rest of the country (9 states

out of 17). In addition, there are intermittent mili-

tary tensions in the border between Sudan and

South Sudan from time to time. Consequently, hun-

dreds of individuals of many taxa have been killed

as a direct effect of shootings and fire set by fight-

ers. Also, several species (e.g. Gazelles and Ostrich)

have declined due to overhunting by the militants

who use them as a primary food source in the

woods. Recent IUCN (2013, e.g. Tables 5) Tables

of endangered species indicate the absence of infor-

mation for about 114 animals’ species (i.e. data

deficit) and 127 species reported as threatened,

including 19 plants and 108 animals (16 mammals,

18 birds, 3 reptiles, 21 fishes and 50 invertebrates).

Many ecologically important species went extinct

since 1980s or are thought to be extirpated from

their natural territories in Blue Nile, South Darfur

and the Nuba mountains regions. Species endan-

gered because of these conflicts and other stressors

(e.g. drought) include top predators: cheetah,

Acinonyx jubatus Schreber, 1775; African lion,

Panthera leo Linnaeus, 1758; greater spotted eagle,

Aquila clanga Pallas, 1811; imperial eagle, Aquila

heliaca Savigny, 1809; houbara bustard, Chlamy-

dotis undulata (Jacquin, 1784); and lesser kestrel,

Falco naumanni J.G. Fleischer, 1818. Herbivorous

on the endangered list are Hippopotamus, Hip-

548

Ahmed A. H. Siddig

popotamus amphibius Linnaeus, 1758; Barbary

sheep, Ammotragus lervia Pallas, 1777; Dorcas

gazelle, Gazella dorcas Linnaeus, 1758; red-

fronted gazelle, Gazella rufifrons Gray, 1846;

Soemmerring’s gazelle, Gazella soemmerringei

Cretzschmar, 1826; African elephant, Loxodonta

africana Blumenbach, 1797; and African spurred

tortoise, Geo chel one sulcata (Miller, 1779), as well

as several bats like Trevor’s free-tailed bat, Mops

trevori (Allen, 1917); horn-skinned bat, Eptesicus

floweri (de Winton, 1901)', and lappet-faced vulture,

Torgos tracheliotos (Forster, 1791) (Badri, 2012).

Habitat loss and fragmentation

Habitat loss and fragmentation due to excessive

deforestation and agricultural expansion in forest

lands. The Sudanese Forest National Corporation

(F.N.C.) estimated that vast forested areas of the

sub-humid zones in southern Darfur and Kordofan

have been cleared by refugees and displaced people

for use as fuel wood and building poles. Approxi-

mately 1 million hectares was cut down during

2005-2010 in both Sudan and South Sudan (F.A.O.,

2005; Gaafar, 2011). Also according to the U.N.

mission in Sudan, millions of people from both Su-

dans have become internally displaced and refugees

as a direct impact war, surviving hard conditions

and depending largely on the already poor forests

for shelter and livelihood.

Insufficient governmental support

For decades, the government’s major concern

always is to deal with wars. There is not enough

government effort or budget allocated to develop

conservation programs. It is no secret in Sudan that

for decades, the budget of the ministries of defense

and interior is about 50-60% of the total, with the

rest divided among more than 25 ministries.

Furthermore, the latest trends in international arms

transfers showed that Sudan is classified among the

top three African countries in weapons imports,

after Algeria and Morocco, receiving 9% of the total

continent’s imports (Wezeman & Wezeman, 2014).

These numbers show the priorities of the govern-

ment, and why ministries like environment and

physical development, higher education, and

science and technology receive less than 1% of the

total budget annually.

Redundant and weak institutions

Redundant and weak institutions are responsi-

ble for managing natural resources and enforcing

conservation policies. It is surprising that many

ministries are formed to accommodate opposition

and former militia leaders who agree to partici-

pate in the government and not because of the

technical need for these ministries. Thus the is-

sues of biodiversity are divided among at least 5

ministries and unfortunately none of them is fully

functional. For example it is primarily follow to

Ministry of the Environment and Physical Devel-

opment, but it has redundancies with the Ministry

of Agriculture (especially at the state level),

Forest National Corporation, the Higher Council

of the Environment and Natural Resource and

Wildlife Protection Administration in the Ministry

of Interior.

Data deficits

A general problem in Sudan is information

gaps in almost all sectors, particularly the current

biodiversity status and geographical distribution

(What is where? What are the trends?). For exam-

ple, there are no current detailed studies about the

state of biodiversity of some important ecosystems

such as Blue Nile state (e.g. Al-Angesena area)

and South and West Darfur states (e.g. Radom

National park). Because of the unsecure condi-

tions, it is not surprising that the data collection

(e.g. species diversity) for conservation (e.g.

habitat restoration) is extremely rare and some-

times impossible. This shortage of information

makes conservation planning haphazard and inter-

ventions cannot even begin.

Accelerating natural disturbances

Desertification is a familiar scenario in almost

70% of the country and one of the biggest chal-

lenges not only because of its fast annual creeping

rate but also because it is encroaching on vast

habitat areas (Table 1). The high rate of deforesta-

tion, soil erosion, forest fires and few reforestation

efforts are primary drivers of this phenomenon. In

addition, the I.P.C.C. 5th report classified Sudan as

one of the most vulnerable spots to climatic changes

since the country is at the defense line of the sub-

Biodiversity of Sudan: between the harsh conditions, political instability and civil wars

549

Saharan region and has high deforestation rates.

Consequently extreme events such as drought,

flooding and fire are likely to increase severely

(Badri, 2012). Conflicts result in more stochastic

deforestations and unplanned use of natural re-

sources which ultimately increase the risk of ero-

sion and desertification.

Absence of local communities in establishing

Absence of local communities in establishin-

gand adopting participatory conservation projects.

Community involvement varies from place to

another, but for the time being the general public,

is concerned more about safety, peace, poverty

alleviation, and food security rather than conserving

biodiversity.

Political restrictions

Political restrictions from the government over

the NGOs working in environmental fields. Due to

these tensions some NGOs are having difficulties

implementing their conservation projects because

the government wants them to do it according to its

agenda which is not necessarily the same as the

NGO’s plans.

THE BIG PICTURE OF BIODIVERSITY

CHALLENGES IN AFRICA

The truth is that the circumstances (i.e. civil

wars and instability) threatening the biodiversity of

Sudan occur elsewhere, not only in neighboring

countries (e.g. South Sudan, Libya and Central

Republic of Africa) but also in the majority of the

African countries (e.g. Mali and Somalia). Unfor-

tunately, political instability, spreading wars and

chronic conflicts, millions of refugees and displaced

people, severe levels of poverty and low education

are the largest common denominator among most

countries of the region (Swatuk, 2007; Nur, 2007).

Furthermore, these countries have weak conserva-

tion institutions with no clear plans aggravated by

budget issues. Because conservation in general

needs committed governments, people living in a

safe and healthy environment, and available re-

sources, it is not surprising that issues of biodiver-

sity conservation are a low priority in Africa.

The other dimension of this dilemma is that we

do not know when these decades of unrest and

conflicts are going to stop (though the reasons

behind them are well known) so that development

can begin. Meanwhile, the consequences of such

deterioration of biodiversity in African countries

on the global environment and biodiversity

become more severe and uncertain. For instance,

U.N.E.P. (2013) reported that the globally impor-

tant and richest tropical areas in Africa such as

Lake Victoria, Congo basin and the Nile fall in

regions where conflicts have raged for decades

and consequently no detailed biodiversity updates

or related environmental data are available. The

ecological significance of this area is not limited

to global water budget and winter habitat for

several western migratory birds. The region is also

considered an important sink for carbon dioxide,

thus significant to the global carbon budget and all

global climate change (U.N.E.P., 2006).

While the governments and the oppositions in

countries like Mali, Libya, Egypt, Somalia and

Sudan are so busy in fighting each other and allo-

cating most resources and efforts to this, appar-

ently they have forgotten to be united against

drought and desertification as the biggest enemy

these countries and their people have ever faced.

The region has the most severe deforestation

worldwide, since vast areas being cleared by

millions from local communities who were forced

by wars, poverty and lack of development to use

forests as their only source for shelter, livelihood,

energy, and building materials. There is much to

lose: more than 70% of the African tropical forests

are located in Democratic Republic of Congo,

Rwanda, Burundi, Central African Republic,

Sudan and South Sudan, where deforestation re-

lated to conflicts is happening every day (Mon-

tagnini & Jordan, 2005).

It is important to mention the influences of this

continental unrest on the ability of international

partners (e.g. U.N.E.P., U.N.D.P., W.W.F., World

Bank, U.S.A.I.D., Conservation International, and

WCS) to continue funding biodiversity and envi-

ronmental conservation projects in Africa. Not only

is there the direct risks of performing field work or

wasting money, but part of this discouragement is

because it is very unlikely that conservation plans

will achieve the goals of the projects in a sustain-

able manner.

550

Ahmed A. H. Siddig

Despite this dark picture of biodiversity in

Africa, there are a couple of bright spots. There is

tremendous progress in some countries such as

South Africa, Kenya and Tanzania whom just

passed through a long history of similar political

tragedies but ended up as successful stories. South

Africa, after years and years of violence, is a good

example of how stability can make development

possible. Among several paths of reforms, biodiver-

sity conservation was launched following simple

principles based on strong governmental authority

and involvement of universities and research

centers, local communities and NGOs in planning

and management of natural resources. By 2012,

official South African reports stated that 9.3 million

people come to the country from all over the world

for wildlife and ecotourism, which is a great achieve-

ment in biodiversity conservation.

My second example is Kenya that came a long

way from crises to become the largest center of

international and regional environmental organiza-

tions in the continent. ‘Those trees make Kenya,

Kenya!’ is a familiar slogan to Kenyans and peo-

ple who visit Kenya. It represents the vision of the

country regarding the environment and indicates

awareness and adoption by local communities.

Establishing community based-ecotourism orga-

nizations is an impressive and creative example

that shows what can be done when a committed

government works together with responsible

NGOs and engaged citizens.

Let me conclude by mentioning the interesting

lesson of Tanzania in biodiversity conservation and

its significance in stabilizing the economy of the

country. There is no doubt that Tanzanian govern-

ment, with local and international partners, has

worked very hard to develop the current working

plan for managing protected areas and positioning

them as a primary source of income to the country.

This wonderful model of managing natural re-

sources is not only a plan for biodiversity conser-

vation, but also made Serengeti, Arusha and other

12 national parks among top tourism areas in the

world. The Tanzanian government announced in

2013 that the country has joined the club of 1-

million wildlife tourists per year, which is a big

achievement. There are also other encouraging

attempts by few countries including Zimbabwe,

Botswana, Namibia, and Zambia who are relatively

stable with well-developed biodiversity plans.

TOP TEN PROPOSALS FOR BETTER

BIODIVERSITY CONSERVATION

The big message I want to convey by this paper

is that conservation action is still possible. It is

never too late as long as there are peace, stability,

willingness, and overall the governmental commit-

ments and engaged citizens and NGOs, no matter

how few the resources. Countries can maximize the

use of land resources for the benefit of people at the

same time as aiming towards sustainable biodiver-

sity conservation. Consistent with this belief and

drawing from success stories mentioned above and

call by recent reports e.g. U.N.E.P. & I.E.S. (2007)

and Badri (2012), I suggest some strategies (Fig. 2)

to improve the existed efforts. These would be a

great start towards better biodiversity conservation

in Sudan as well as elsewhere in the region where

conflicts and unrest continue.

Management strategies

1. Governance and Government commitment

towards natural resources conservation by support-

ing annual budgets and strengthening the institu-

tions that formulate and implement the conservation

plans with systematic monitoring and evaluation

protocols.

2. Improving environmental educational

programs especially at secondary and higher

education levels by addressing the recent globally

important issues (e.g. climate change, endangered

species) as annual updates in the curriculum. More

broadly, major needs of the education system of

Sudan are strengthened polices, curriculum

reforms to match international trends (e. g. millen-

nium goals), training of faculty (teachers) and

assistant staff, and improved government commit-

ment and funding. I urge adoption of some inter-

national (similar educational models) standards

such as quality assurance systems that include

strict monitoring and evaluation system of the edu-

cational process.

3. Adoption of research and scientific methods

to identify conservation priority areas (e.g. ecosys-

tem level vs. population level) but also select

among many adaptation strategies (e.g. water har-

vesting vs. enclosures for habitat restoration).

Biodiversity of Sudan: between the harsh conditions, political instability and civil wars

551

A proposed framework for environmental conservation in Sudan

Stakeholders Inputs

Stakeholders

Gov. agencies

Universities

Research centers

N*GOs

Local communities ... etc.

Management

strategies

Assess needs/ vulnerabilities

(Existing + expected)

Develop working plans

Evaluate strategies

• Ecological

• Human

• Management

Recommended

Action(s)

Implementation

Monitoring

Figure 2. A proposed framework for environmental conservation in Sudan based on the role of the government

in initiating research and management plans with consideration of environmental stakeholders.

4. Use of technology in management planning

such as remote sensing, GIS, radio collars, camera

traps, and acoustic monitoring to improve manage-

ment and inform decision makers.

5. Adoption of long-term monitoring programs

by focusing on specific focal ecosystem indicators

(e.g. abundances, composition and richness) and

key climatic variables (e.g. amount and length of

rainy season) at pennanent plots across the country.

These monitoring data will be good indications not

only for detecting current conditions and trends, but

also could alert managers to early warning signals

of ecosystem change.

6. Involvement of indigenous communities and

nongovernmental stakeholders in conservation

planning and implementation. This community

involvement could be achieved by using a citizen

science approach that can play two roles at once.

While involvements of local communities will

likely increase the awareness about certain environ-

mental issues (e.g. risk of deforestation) it could be

a cost-effective way to collect biodiversity data

such as species occupancy information.

7. Capacity building, especially for natural re-

sources mangers, focuses on improving awareness

for the reasons to protect biodiversity, identifying

hot spots, and building monitoring skills and a

documentation system for conservation projects.

8. Enforcing and updating legislation so that

conservation efforts are based on the power of law.

One sad example though is that National park like

Radom is the biggest protected area in the country

552

Ahmed A. H. Siddig

but most of its area is dominated by drug cartels

farming activates; furthermore there is no gover-

nment authority inside the park to take actions.

9. Strengthen networking and international part-

nerships with powerful agencies such as Wildlife

Conservation Society (W.C.S.), World Wildlife

Fund (W. W.F.), and Nature Conservancy and others

to take advantage of their experience in conserva-

tion elsewhere.

10. Activating the commitments of Sudan in in-

ternational environmental conventions (e.g. United

Nations Convention on Environment and Develop-

ment, U.N.C.E.D., United Nations Framework

Convention on Climate Change, U.N.F.C.C.C.,

Convention of Biological Diversity, C.B.D., Con-

vention on international Trade in Endangered

Species of Wild Fauna and Flora (C.I.T.E.S.) and

protocols (e.g. Kyoto and Ramsar) and following

national action guidelines.

Urgent research needs

My suggestions for management interventions

emphasize the adoption of research and scientific

approaches. I believe that research must play a key

role in the next era of conservation biology in

Sudan. Research would diagnose major causes of

the deterioration of biodiversity and reveals the hot

spots of decline during the past. In addition, re-

search will establish baseline information, identify

priorities, and inform future management and in-

vestment of resources.

Although the importance of research and

science-based decisions has been urged by many

authors and reports previously (e.g. Abdelhameed,

2007; Zakialdeen, 2009; Funk et al., 2011), like all

things in Sudan, research has encountered many

obstacles ranging from funding, to weak institu-

tions and facilities, to absence of master plans, to

research capacity (e.g. training). Identifying the

most pressing research questions will help to focus

limited resources. Based on the work of Sutherland

et al. (2009) regarding the top hundred most

important questions to conservation of global bio-

diversity, I scaled down to Sudan and adapted a list

of top ten research questions about biodiversity of

the country.

The questions are:

1. Desertification and drought

Studies on the causes of desertification are rela-

tively better and more focused than studies of strate-

gies of control. Despite these efforts there are many

research gaps at the country level such as: Where

do the greatest effects of desertification occur?

What is the encroachment rate of the desert and

where does mostly occur (i.e. how many km/yr.)?

Also, important related questions remain unan-

swered, for example: What is the frequency and du-

ration of drought periods? Are there socioeconomic

impacts of desertification and drought? What are

these impacts and where?

2. Climate change

The concern with climate change in dry lands is

how to adapt to it in the context of the myriad

problems already facing these areas. For instance,

how to allocate limited resources among many

urgent needs - for example, choosing between water

harvesting techniques or establishing refiigia in pro-

tected areas - needs to be studied and choices based

on objective (i.e. quantitative) criteria. To design

effective studies, it is important that to determine

the methods of evaluating the vulnerabilities and

effectiveness of adaptations and mitigation mea-

sures at any ecosystem.

3. Biodiversity , population dynamics and

conservation hot spots

There is an absence of biodiversity information

in Sudan; the I.U.C.N. (2013) reported zeros for

many taxa to indicate a data deficit. Therefore, to as-

sess the conservation status of species and to make

a baseline for any further questions, we need to know

who is where and how many of them are there, par-

ticularly at the protected areas. For endangered

species, we need to assess the status and likelihood

of extinction by conducting a population viability

analysis (PVA), a widely adopted technique in con-

servation biology (Lindenmayer et al., 1993; Vie et

al., 2009). Additional key studies that relate conser-

vation and populations dynamics include studies of

population characteristics other than abundance. For

example, fecundity, age classes and sex ratio data,

especially for threatened species, are keys to under-

standing the population dynamics.

Biodiversity of Sudan: between the harsh conditions, political instability and civil wars

553

Understanding how human activities (e.g. defor-

estation by refugees), environmental (e.g., fire) and

biological (e.g., disease) disturbances impact popu-

lations, communities and metapopulation process

are also important.

4. Forest ecology , wetlands and habitat as-

sessment

Issues like seed germination and natural regen-

eration of some threatened trees species such as

a desert date (. Balanites aegyptiaca Del.) and

Boswellia papyrifera Del. are of great concern and

should be a priority area of research. Also there is

an absence of studies in important areas like the

temporary wetlands and flood plains of the Nile.

These are thought to be rich ecosystems supporting

several fauna and flora species as well as an essen-

tial source of livelihood to millions of people living

at the Nile strip and tributaries.

5. Ecological modeling and forecasting

Modeling, simulations and other statistical tech-

niques can be employed to craft very sophisticated

ecological questions (e.g. what if) and to improve our

understanding about possible future scenarios. Mod-

eling techniques can also integrate data and predic-

tions over large spatial scales (i.e. landscape level).

6. Environmental education

I believe that education is the right way to start

making real changes in biodiversity conservation in

the country. However, the current education system

is broken and needs to be reformed on scientific

basis starting by asking questions like: Does our

education meet standards at the levels of internatio-

nal criteria (e.g. international education polices of

the U.N.E.S.C.O.)? How could we develop a

quality assurance system for higher education

institutions generally in Sudan in a cost-effective

way? I think by answering these questions we can

make sure our environmental education meets the

international quality standards in higher education

with a monitoring and evaluation system.

7. Environmental risk assessments

Despite the political instability and unrest,

Sudan has witnessed some developmental projects

such new dams, highways and establishment of

urban centers. The call here is that biodiversity and

risk assessments studies should be considered when-

ever similar projects are being planned (El-

Meghraby, 2009). As violence and conflicts continue

in many parts of the country, there is a need to know

what exactly the effect of these wars is on biodiver-

sity. I suggest that knowing the effect of a particular

civil war that has a certain number of refuges on the

surrounding forest cover would be useful to predict

the future dynamics of the habitat affected by war.

CONCLUSIONS

Biodiversity is of critical importance to the

livelihood of people and is also of high ecological

value. Despite its importance, biodiversity in

Sudan, as many other resources, has been a victim

of political instability and continuous civil wars

since the 1950s. Absence of strong governance and

polices, and socioeconomic factors have contrib-

uted to this substantial deterioration. In addition, the

harsh setting, drought, desertification, flooding,

fire, habitat destruction and recent climate change

have played a great role in reducing habitats and

populations.

Despite these stressors on biodiversity and the

lack of current information about the ecosystems,

communities and populations, conservation efforts

must proceed with effective management actions.

Urgent management actions at this point should in-

clude governance and governmental commitment

(e.g. funding, facilities, policies), adoption of re-

search and improving environmental education,

adoption of technology and long-term monitoring

programs, and involving local communities and

NGOs in planning and enforcement of legislations.

The government must also stay committed to inter-

national environmental conventions and protocols

(i.e. U.N.C.E.D., U.N.F.C.C.C., C.B.D., C.I.T.E.S.),

Finally, I recommend capacity building and training

of conservation practitioners. This would have great

value especially if it is conducted in the context of

international partnerships with other prominent

conservation agencies (e.g. U.S.A.I.D., W.C.S.,

W.W.F., and The Nature Conservancy).

The research need at this point is to create the

bench marks to build upon. Not only questions

concerning species richness and abundance are

554

Ahmed A. H. Siddig

important. It is also critical to know the effects of

different disturbance factors (e.g. desertification

and human aspects) on the ecosystems, habitats and

populations. Studies investigating the role of biodi-

versity in the livelihood of local communities as

well as the role of communities in conservation

should be a priority. The Nile needs more in-depth

investigations about its faunal and floral diversity,

biogeochemistry, water chemistry and the effects of

heavy agricultural and urbanization activities on the

environment of the both banks of the Nile. Also

areas affected by the conflicts, especially where the

effects of refugees and internally displaced people

could affect the resources must be a priority of

research.

In conclusion, I believe that all researchers and

conservation biologists in Sudan share with me the

same positive feelings and responsibility about the

country’s biodiversity and resources. I hope this

work to lead to new initiatives from both the gov-

ernment agencies and conservation biologists. I

truly want this report to motivate in-depth work and

collaborative efforts that will substantially improve

the status of biodiversity in Sudan as well as be a

model for conservation in the region.

ACKNOWLEDGEMENTS

This paper came after the invitation from Har-

vard Forest (H.F.), Harvard University to give a talk

about biodiversity of Sudan - status, conservation

challenges, research needs. I do gratefully offer my

acknowledgment to Audrey Barker Plotkin - the re-

search and seminar coordinator in HF for the request

and discussion of the initial idea. Also I would like

to warmly thank Professor Aaron M. Ellison, Har-

vard Forest for his valuable comments and encoura-

gement to write this paper. Also I extend my thanks

to Islamic Development Bank (I.D.B.) for funding

my PhD research in US as well as to Harvard Forest

for providing host and space to my research.

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