1 Julodis armeniaca

Marseul, 1865,

Turkey, Bingol

Yayla, 20. VII.2007.

2 .J.aristidis,

Tunisia, Tozeur,

8.IV.2004.

3. J. lucasi , Tunisia,

Gafsa, 11.IV.2006.

Cover: J. andreae,

Turkey, Adiyaman -

Nemrut Dagi,

12.VI.2007 (photos-

collectionM. Gigli).

The genus Julodis Eschscholtz, 1829 (Coleoptera Bupreslidae). The genus Julodis is the type genus of the Subfamily Julodinae Lacordaire, 1857.

Species in this group are quite unusual Buprestidae for their general appearance, but especially for the larval biology. They don't live in wood or other plant

tissues like other larvae of this family, but they dig into the soil and feed on the roots of various plants. In contrast to larvae of other Buprestidae, they are

covered by long bristles directed obliquely backwards, helping in the movement in the ground, just like in the larvae of Coleoptera Cetonidae. The genus

Julodis is currently divided into two groups. One in South Africa (especially Cape Region) and Namibia, represented by 34 taxa (species and subspecies),

and another group primarily Palaearctic, spread from Spain and North Africa to the steppes of Central Asia (up to the Chinese province of Gansu), with

some species in the Oriental Region (Pakistan and India) and other taxa in Kenya (92 species and subspecies). Many species are extremely variable. The

widespread polymorphism and the existence of many similar species has led to the description of many species, then failed into synonymy, and probably

others will follow the same fate, especially in certain groups of Palaearctic species. The European Fauna includes six species and subspecies, in the Iberian

Peninsula, South France, Italy (Lampedusa Is.) and Balkans. Julodis onopordi s.l. is one of the most polymorphic species. It, according to actual

conception, is widespread in the range of Mediterranean climate in Spain and southern France, and in North Africa, from Morocco to Sinai, with many

different populations, some of which are considered subspecies. It is the only species in the genus in the Italian Fauna (Lampedusa Is., only). Another very

variable species, spread over extensive territories, is Julodis andreae s.l., who lives in all the lands between Turkey, Iran and Azerbaijan. On the contrary,

there are species very localized, limited to areas with well-defined characteristics of the soil and climatic conditions. Among these, three species live in the

vast steppe and pre-desert around the large salt lakes of Northern Africa: Julodis aristidis Lucas, 1860, Julodis chrysesthes Chevrolat, 1860, Julodis

kerimi Fairmaire, 1875. They are differently distributed over the territory in consequence of the type of soil, the presence of salt, gypsum, and its

granulometry, of great importance for the needs of the larvae. Adults mostly feed on leaves and young twigs of shrubs and small trees, but also on

herbaceous plants. Maurizio Gigli. Via Monte Macereton. 13-00141 Roma, Italy; email: gigli.maurizio@alice.it

Biodiversity Journal, 2012, 3 (3): 159-164

New data of the freshwater fish genera Laubuca Bleeker, 1 860

(Cypriniformes Cyprinidae) and Phenacostethus Myers, 1 928

(Atheriniformes Phallostethidae) in Thailand

Sitthi Kulabtong 1 *, Siriwan Suksri 2 & Chirachai Nonpayom 3

'Save wild life volunteer Thailand, Wangnoi District, Ayuttaya Province 13170, Thailand; email: kulabtong201 l@hotmail.com

Reference Collection Room, Inland Fisheries Resources Research and Development Institute, Department of Fisheries, Thailand

10900; email: Siriwan. suksri@gmail.com

3 534/26 Soi Phaholyothin 58 Phaholyothin Rd. Sai Mai, Bangkok, Thailand; email : sornl33@hotmail.com

* Corresponding author

ABSTRACT In the present paper are reported, for Thailand, additional records of the cyprinid fish Lau-

buca siamensis Fowler, 1939 and priapium fish Phenacostethus smithi Myers, 1928 re-

spectively from Mekong Basin, Meklong Basin, Southeast Basin and from upstream of

Bangpakong Basin and Yom Basin. Description and distribution data of the two freshwater

fishes are also provided.

KEY WORDS Laubuca ; Phenacostethus ; Cyprinidae; Phallostethidae; Thailand.

Received 02.03.2012; accepted 26.06.2012; printed 30.09.2012

INTRODUCTION

Freshwater fishes of the genera Laubuca Blee-

ker, 1860 and Phenacostethus Myers, 1928 are po-

orly known in Thailand.

Currently, for Laubuca genus two valid species

have been recorded in Thailand, namely L. caeru-

leostigmata and L. laubuca (Smith, 1931; 1945;

Banarescu, 1971).

The cyprinid fish Laubuca siamensis was de-

scripted by Fowler (1939) and the distribution of

this species is known only in waterfall at Trang Pro-

vince, peninsular Thailand.

In Thailand, Laubuca species taxonomic status

is still unclear, especially as far as concerns L. lau-

buca'. in 1971, L. siamensis was reported as a junior

synonym of Chela laubuca by Banarescu (1971)

and in 2009, the genus Chela Hamilton, 1822 in

Thailand was considered a junior synonym of genus

Laubuca based on a molecular study of phylogene-

tic interrelationships (Fang et al., 2009).

Phenacostethus are small priapium fishes,

found in large rivers and river estuaries in Sou-

theastern Asia.

The genus is separated into three valid species,

namely P. trewavasae Parenti, 1986 from Sarawak,

Malaysia, P. posthon Roberts, 1971 from peninsu-

lar Thailand (Satul Province, Pungah Province),

Malaysia and Sumatra, Indonesia and P. smithi

Myers 1928 widely distributed: Mekong Basin

(Thailand and Cambodia); Chantaburi River, Sou-

theast Basin; Lower Chaophaya Basin (Bangkok);

Malay Peninsula, Sarawak, Borneo, Malaysia

(Myers, 1928; Roberts, 1971; Parenti, 1986; Rain-

both, 1996; Parenti & Lim, 2005).

In the present paper, the authors re-examine all

specimens of the cyprinid fishes Laubuca stored in

Inland Fisheries Resources Research and Develop-

ment Institute, Department of Fisheries, Thailand

[NIFI]. The authors found that the specimens

named as L. laubuca from Thailand are clearly dif-

ferent from the original description of Hamilton

160

S. Kulabtong, S. Suksri & C. Nonpayom

(1822) of L. laubuca by the combination of the fol-

lowing characters: lateral line scales, body depth,

number of anal fin rays, pelvic fin length, pectoral

fin length and absence of tubercles on lower jaw.

The authors suggest the valid name of these speci-

mens to be L. siamensis Fowler, 1939. In addition,

the authors report additional records on the distribu-

tion of L. siamensis in Mekong Basin, Meklong

Basin and Southeast Basin, Thailand.

As far as concerns the project at Yom River and

upstream of Bangpakong Basin, Kabin Buri District,

Prachin Buri Province and Nakhon Nayok Province,

Central Thailand, we found many specimens of P.

smithi in both areas, an additional record of this spe-

cies in Thailand.

ACRONYMS. Standard length (SL); Head

length (HL).

RESULTS

Order Cypriniformes Bleeker, 1859

Family Cyprinidae Cuvier, 1817

Laubuca siamensis Fowler, 193 9

Chela laubuca. Smith, 1945: Peninsular Thai-

land); Sontirat et al., 2006: Southeast Basin,

Thailand.

Examined material. NIFI 0079, 2 specimens,

Aun River, Sakon Nakhon Province, Northeast

Thailand, 1.1967, legit Sopa Trirat. NIFI 1227, 1

specimen, Klong Sang, Chav Raan Reservoir, Surat

Thani Province, South Thailand, IV. 1983, legit Kar-

nasuta, J. NIFI 1968, 1 specimen, Tapi River Basin,

Phrasaeng Suratthani Province, South Thailand,

IV. 1985, legit Sonkphan, L. (Fig. 1). NIFI 1969, 4

specimens, same data of NIFI 1968. NIFI 2527, 2

specimens, Tanow Sri River, Sune Pung Distric,

Ratchaburi Province, West Thailand, XII. 1993, legit

Chavalit Vidthayanon (Fig. 2). NIFI 2966, 4 speci-

mens, Klong Phraya W.S. Krabi Province, South

Thailand, 1970, legit J.N.

Description. L. siamensis is distinguished

from other species of Laubuca genus by the com-

bination of the following characters: lateral line

scales complete, with 31-33 + 2 scales; transverse

line scales on body with 6-7/ 1 / 2-4 A scales; body

depth is 28.6-33.0%SL. Pectoral fin is short not

extending to the anus; anal fin with 3 unbranched

rays and 1 8 A - 2 HA branched rays; pelvic fin is

long (93. 8-136. 6%HL) reaching beyond the anus;

pectoral fin length is 34.6-39.4%SL; a clearly

black blotch above the pectoral fin base; thin black

longitudinal stripe along the body; caudal pedun-

cle with clearly dark blotch; lower jaw smooth, no

tubercles on skin.

Particularly, L. siamensis is compressed, body

depth is 28.6-33.0%SL. Body width is 9.6-

13.2%SL. Scales in lateral series are medium to

large, lateral line scales complete, with 31-33 +2

scales, transverse line scales on body with 6-7/ 1 /

2- 4 A scales and 16-18 predorsal scales. Head

length is 21.2-26.8%SL. Eye is large, eye diameter

is 25.5-37.9%HL (6.5-8.6%SL). Post orbital length

is 39.0-43.8 %HL (8.6-10. 1%SL), snout length is

short, 25.9-3 1.9%HL (6.0-7. 1 %SL) and interorbital

width is 46.9-50.4 % HL (10.9-11.8 % SL), shorter

than postorbital width (48.3-54.9 %HL or 12.0-12.5

%SL). Dorsal fin origin coincides with posterior

anal fin origin, predorsal fin length is 62.8-

71.8%SL, prepectoral fin length is 25.4-30.6 %SL,

prepelvic fin length is 43.0-46.5 %SL and preanal

fin length is 64.1-68.9 %SL.

Caudal peduncle depth is 9.2-10.9 %SL; pec-

toral fin is long but not reaching beyond the anus,

the pectoral fin length is 34.6-3 9. 4%SL showing

11-12 branched fin rays. Pelvic fin is long rea-

ching beyond the anus, the pelvic fin length is

93. 8-136. 6%HL or 20. 8-36. 6%SL with 5 branched

fin rays. Anal fin base is longer than dorsal fin

base, the anal fin base length is 26.0-28.5%SL,

dorsal fin with 3 unbranched rays and 8 branched

rays and anal fin with 3 unbranched rays and ISA-

21 A branched rays. The dorsal fin base length is

10.5-14.0 %SL.

Distribution. This species is distributed in Me-

kong Basin, Meklong Basin, Southeast Basin and

peninsular Thailand.

Comparative notes. Other examined material.

L. caeruleo stigmata: NIFI 0041, 1 specimen, Poung

Klong Nong Moa, Ayuttaya Province, Central Thai-

land, XII. 1966, legit Theachareon, p. NIFI 2602, 23

specimens, Pasak, Lopburi Province, Central Thai-

land, 1.1994, legit Chukajom T. (Fig. 3).

L. siamensis was descripted by Fowler (1931)

from waterfall at Trang Province, peninsular Thai-

land, and “ siamensis ” is referring to Siam, the old

name of Thailand, the type locality of this species;

this species has been considered unit now a junior

New data of the freshwater fish genera Laubuca and Phenacostethus in Thailand

161

Figure 1. Laubuca siamensis , 48 mm SL, Tapi River Basin, Phrasaeng, Suratthani Province, South Thailand. Figure 2.

L. siamensis , 51 mm SL, NIFI 2527 , Tanow Sri River, Ratchaburi Province, West Thailand. Figure 3. L. caeruleostigmata ,

61 mm SL, N1F1 2602, Pasak River, Lopburi Province, Central Thailand. Figures 4, 5. Phenacostethus smithi , 15-17 mm

SL, male (above) and female (below), N1F1 4545, Yom Basin, VIII. 2011, Siriwan Suksri leg., Thailand.

162

S. Kulabtong, S. Suksri & C. Nonpayom

synonym of Chela laubuca (Banarescu, 1971) and

genus Chela in Thailand has been considered a ju-

nior synonym of Laubuca (Fang et al., 2009).

The current status of L. siamensis is L. lau-

buca. L. laubuca was descripted by Hamilton

(1822) from Northern parts of Bengal (NorthEast

India; Bangladesh). From a comparison with docu-

ments and specimens from Thailand, we strongly

believe that, in Thailand, the valid name of L. lau-

buca is L. siamensis.

L. siamensis from Thailand is distinguished

from the original description of Hamilton (1822)

and the report of Gunther (1868), who re-examined

the C. laubuca specimens of Dr. Bleeker’s Collec-

tion from Bengal, by the combination of the follo-

wing characters: lateral line scales are 31-33 + 2 (in

L. laubuca they are 37), body depth is 3.00-3.50

times greater than SL (in L. laubuca is 2.75-2.80

times); transverse line scales is 6-7/ 1 / 2-4 Vt. scales

(in L. laubuca is 71/2/1/4); pelvic fin shows 5 rays

(in L. laubuca 7); pectoral fin is short not extending

to the anus (in. L. laubuca it reaches the anus); pel-

vic fin is long extending beyond the anus (in L. lau-

buca is shorter, not reaching beyond the anus); first

ray of pelvic fin appears like a filament (in L. lau-

buca it is undivided from the other branched rays);

a thin black longitudinal stripe along the body and

a clearly dark blotch on caudal peduncle (which are

absent in L. laubuca).

L. siamensis is clearly different from L. cae-

ruleostigmata of Thailand by many characters

such as: body depth is 3. 0-3. 5 times greater than

SL (in L. caeruleostigmata is 2.25 times), lateral

line scales includes 31-33 scales (in L. caeruleo-

stigmata 34-35). L. siamensis has one black blotch

above the pectoral fin base, a thin black longitudi-

nal stripe along the body and a clearly dark blotch

on caudal peduncle (L. caeruleostigmata shows 4-

5 dark vertical stripes above pectoral fin base on

both sides of the body) (Smith, 1931; Smith, 1945).

Order Atheriniformes Rosen, 1966

Family Phallostethidae Regan, 1913

Phenacostethus smithi Myers 1928

Examined material. NIFI 4545, 8 specimens,

Yom Basin, Pakpot Subdistrict, Moung District, Su-

Figure 6. Collection area, floodplain of Yom Basin in Sukhothai Province, Thailand.

New data of the freshwater fish genera Laubuca and Phenacostethus inThailand

163

khothai Province, Thailand, 25.VIII.2011, legit Si-

riwan Suksri (Figs. 4-5). NIFI 4548, 3 specimens,

upstream of Bangpakong Basin, Kabin Buri Di-

strict, Prachin Buri Province, Thailand, 5.II.2011,

legit Sitthi Kulabtong.

Description. P. smithi has a slender and cylin-

drical body. Body depth is 16.5-19.9%SL. Head is

short, head length is 18.2-19.1 %SL. Eye is big, eye

diameter is 33.5-37.6 %HL. Post orbital length is

33.5-37.7%HL, snout short (23.5-24.3 %HL) and

mouth is upward. First dorsal fin is very small, but

second dorsal fin is large. Pre-second dorsal fin

length is 70.6-70.7 %SL and the second dorsal

shows 6-7 rays.

Dorsal fin origin is clearly posterior the anal fin

origin. Pre-anal fin length is 52.3-52.9%SL and the

anal fin comprises 14-17 rays. Second dorsal fin

base is shorter (12.4-14.4%SL) than anal fin base

(23.5-25. 1%SL). The body is translucent, with tiny

scales. Head with membranous dome. Males have

a priapium (reproductive organ) below the head at

the base of pectoral fin.

The priapium of P. smithi is ruffled and hence

distinguished from that (i.e. smooth) of other Phe-

nacostethus occurring in Thailand.

Variability. Priapium, the reproductive organ

is found in males only.

Biology and Distribution. Phenacostethus

smithi were found in several habitats of Yom Basin

(Fig. 6); floodplain canal and mainstream, charac-

terized by slow and turbid waters and muddy bot-

tom. In each habitat, submerged or marginal plants,

such as green algae, papyrus and grass, were found.

Specimens from upstream of Bangpakong Basin

were found in a small stream nearly the mountain,

with shallow, turbid and slow waters.

This species is known from Yom Basin, Ban-

gpakong Basin, Lower Chaophaya Basin and Sou-

theast Basin in Thailand; Mekong Basin in

Thailand and Cambodia; Malay Peninsula, Sara-

wak, Borneo in Malaysia.

ACKNOWLEDGEMENTS

A special thanks to reviewers for reviewing this

manuscript. Authors wish to thank Dr. Rohan Pe-

thiyagoda. Wildlife Heritage Trust in Sri Lanka and

Dr. Sorin Stefanut, Institute of Biology Bucharest,

Romanian Academy, Romania for providing the

original description of many species of Laabuca

genus. Finally we are grateful to all partners for

their support.

REFERENCES

Banarescu P., 1971. Further studies on the systematics of

Cultrinae with reidentification of 44 type specimens

(Pisces, Cyprinidae). Revue Roumaine de Biologie,

Serie de Zoologie, 16: 9-20.

Fang F., Noren M., Liao T.-Y, Kallersjo M. & Kullander

S.O., 2009. Molecular phylogenetic interrelationships

of the south Asian cyprinid genera Dcmio, Devario

and Microrasbora (Teleostei, Cyprinidae, Danioni-

nae). Zoologica Scripta, 38: 237-256.

Fowler H.W., 1939. Zoological results of the third De

Schauensee Siamese Expedition. Part IX. Additional

fishes obtained in 1936. Proceedings of the Academy

of Natural Sciences of Philadelphia, 91: 39-76.

Gunther A., 1868. Catalogue of the fishes in the British

Museum, v. 7. Catalogue of the Physostomi, contai-

ning the families Heteropygii, Cyprinidae, Gonor-

hynchidae, Hyodontidae, Osteoglossidae, Clupeidae,

Chirocetridae, Alepocephalidae, Notopteridae, Halo-

sauridae, in the Collection of the British Museum.

Taylor & Francis, London, 512 pp.

Hamilton F., 1 822. An account of the fishes found in the

river Ganges and its branches. A. Constable e Co.,

Edinburgh, 405 pp.

Myers G.S., 1928. The systematic position of the phal-

lostethid fishes, with diagnosis of a new genus from

Siam. American Museum Novitates, 295: 1-12.

Parenti L.R., 1986. Bilateral asymmetry in phallostethid

fishes (Atherinomorpha) with description of a new

species from Sarawak. Proceedings of the California

Academy of Sciences (Series 4), 44: 225-236.

Parenti L.R. & Lim K.K.P, 2005. Fishes of the Rajang

Basin, Sarawak, Malaysia. The Raffles Bulletin of

Zoology Suppl. 13: 175-208.

Rainboth W.J., 1996. FAO species identification field

guide for fishery purposes. Fishes of the Cambodian

Mekong. Rome, 265 pp.

Roberts T.R., 1971. The fishes of the Malaysian family

Phallostethidae (Atheriniformes). Breviora, 374: 1-27.

Smith H.M., 1931. Descriptions of new genera and spe-

cies of Siamese fishes. Proceedings of the United

States National Museum, 79: 1-48.

Smith H.M., 1945. The freshwater fishes of Siam, or

Thailand. Bulletin of the United States National Mu-

seum, 188: 1-622.

164

S. Kulabtong, S. Suksri & C. Nonpayom

Sontirat S., Tunchareon S. & Soothornkit Y., 2006. Fish

species diversity in the areas of National Parks and

Wildlife Sanctuaries in the five eastern provinces of

Thailand. Proceedings of 44th Kasetsart University

Annual Conference: Fisheries, Bangkok (Thailand),

p. 60-67.

Biodiversity Journal, 2012, 3 (3): 165-172

Evaluation of the toxicity of metal pollutants on embryonic

development of the sea urchin Paracentrotus lividus (Lamarck,

1816) (Echinodermata Echinoidea)

Saliha Dermeche *, Fa/gal Chahrour & Zitouni Boutiba

Laboratoire Reseau de Surveillance Environnementale (LRSE), Departement de Biologie, Faculte des Sciences ,Universite d'Oran,

Algerie; e-mail: salidermeche@yahoo.fr

' Corresponding author

ABSTRACT Bioassays are frequently used to evaluate biological effects of pollutants on marine orga-

nisms. The objective of such tests is the detection of toxic effects on populations that are

representative of a given ecosystem. Sea urchin is a model organism employed in the field

of environmental toxicology due to its sensitivity towards various pollutants, particularly

heavy metals. Preliminary bioassay tests on embryos and/or larvae of Paracentrotus lividus

(Lamark, 1816) from Madagh (Oran, Algeria) were used to assess the potential toxicity

and determine the LC$q of four metal pollutants, Cadmium, Copper, Lead and Zinc.

KEY WORDS Bioassays; LCyp; Madagh; Heavy metals; Paracentrotus lividus.

Received 22.05.2012; accepted 06.07.2012; printed 30.09.2012

INTRODUCTION

Inland aquatic and marine systems represent

containers for virtually all contaminants, via direct

and indirect contributions (Peijnenburg et al.,

1997). Research on the action of heavy metals on

the development of the sea urchin eggs represent an

important contribution to the progress of kno-

wledge in the field of embryonic determination.

Sea urchin is a preferred model in such a rese-

arch, due to a number of reasons including external

growth of embryos, rapid cell division rate and cell

transparency, thus being commonly employed in

the field of Environmental Toxicology (Guillou &

Michel, 1993; Quiniou et al., 1997). Bioassays or

bio-tests frequently use several techniques to mea-

sure, predict and control the effect of the release of

toxic substances on marine organisms.

Present study examines the impact of four

heavy metals, Cadmium, Copper, Lead and Zinc,

on the embryonic development of the sea urchin

Paracentrotus lividus (Lamarck, 1816) (Echinoder-

mata Echinoidea).

MATERIALS AND METHODS

We investigated the site of Madagh bay (Oran,

Algeria: 35°37'952" N; 000°104'243" W) (Fig. 1),

a non-impacted area, closed at its ends by two

small caps reducing the action of winds. Moreo-

ver, the proximity of the Habibas island, which is

considered a marine protected area, could make

this site a reference station for comparative stu-

dies regarding the monitoring of pollution impacts

in the coastal marine ecosystem of western Alge-

ria, a site rich in algae and Posidonia meadows

(Benghali, 2006).

Collection of sea urchins was carried out during

the period March- June 2010, when spawning is at

its peak in this echinoid species. Spawning was in-

duced by injection of 0.5 ml of 0.5 M KC1 into the

166

S. Dermeche, F. Chahrour & Z. Boutiba

MAROC

ALGERIE

A T L A S

OKm 100 Km

Figure 1. Sampling site: Madagh bay, Oran, Algeria.

coelomic cavity of the sea urchin (Harvey, 1940);

the male sex products were recovered "dried" and

stored in melting ice. Moreover, sperms of several

males were pooled. Females were placed in a 250

ml Erlenmeyer flask containing filtered seawater

(FSW) so that the genital pore was in contact with

the surface of the water. After spawning, eggs were

sieved with a 160 micron sieve and collected in a

test tube. Volume was adjusted to 500 ml using

FSW and homogenized. Subsequently, the first 100

ml of the solution (containing eggs) was removed

and replaced by FSW. This operation was repeated

a second time (Dinnel et al., 1988; Quiniou et al.,

1999; Guillou et al., 2000).

Once suspensions of gametes were obtained,

eggs and sperms were recovered separately in 2 ml

of FSW. Fertilization was performed in beakers

containing 1500 to 2000 oocytes to which 250 pi

of sperm was added. After one hour of contact, we

checked the fertilization success under a light mi-

croscope. Bioassays were carried out according to

Coteur et al. (2003). A 15 well plate was used for

each metal pollutant (Cd, Pb, Cu and Zn).

Four different increasing concentrations (10

gg/1; 50 jLig/1; 100 gg/1; 200 gg/1) and a control so-

lution (FSW), employed as blank, were used. Each

well contained 10 ml of each solution, then 250-300

embryos were transferred to each well and incuba-

ted for 72 hours at 21 ± 1 °C.

At the end, larval development was stopped by

adding neutral formalin (35%) and the percentage

of anomalies was determined according to the cri-

teria of Klockner et al. (1985). Number of mal-

formed eggs/larvae, expressed in percentage, was

assessed under the optical microscope by scan-

ning slides containing about 100 eggs each. The

number of dead cells was adjusted by the formula:

% mortalities corrected = (Po - Pt)/( 100 - Pt),

where Po is the percentage of mortalities observed

and Pt is the percentage of mortalities in controls

(Abbott, 1975).

Five replicates were performed for each concen-

tration and each metal. The statistical treatment of

experimental data was performed by the probit me-

thod (Bliss, 1935), which is useful for experiments

with reduced number of animals and particularly

suitable for research on marine invertebrates, as con-

firmed by Bendimerad (2000).

RESULTS

The mean percentages of embryonic abnorma-

lities observed in each heavy metal solution ± stan-

dard deviation are shown in Table 1 .

As shown in Table 1, concentrations of 10 gg/1

and 50 gg/1 determined minor negative effects on

larval development. At 100 gg/1, the malformation

percentage is about double or more (respect to 50

Evaluation of the toxicity of metal pollutants on embryonic development of the sea urchin Paracentrotus lividus

167

[pg /l]

Metals

100

200

7.31 ± 1.84

18.26 ±2.97

79.32 ± 15.38

88.00 ± 14.60

5.00 ± 1.68

12.20 ±7.85

22.40 ±7.97

40.33 ±4.04

5.93 ± 1.76

28.93 ±4.52

41.91 ±4.13

52.66 ±24.61

10.60 ±2.70

17 ±3.98

36.73 ± 10.32

40.5 ±24.02

Table 1 . Mean percentages of abnormal embryos ± standard deviation observed in the sea urchin P. lividus from Ma-

dagh bay (Oran, Algeria) treated with four heavy metal solutions at different concentrations.

jug/1) depending on the metal, in particular, it resul-

ted 79.32% for Cd, 41.91% for Cu, 22.40% for Pb

and finally 36.73% for Zn (Figs. 2-5).

Graphs show results we partly expected: the

more the concentration increases, the more the per-

centage of malformations is important, although,

surprisingly, percentage of malformations observed

after treatment with Cadmium at 200 pg/1 is higher

(88%) (Fig. 2) than that detected with the other me-

tals: 52.66% (Copper, Fig. 3), 40.33% (Lead, Fig.

4) and 40.50 % (Zinc, Fig. 5).

LCjp, calculated according to the method of

Bliss (1935), resulted 61.65 pg/1 for Cd, 158.48 pg/1

for Cu, 389.04 pg/1 for Zn and 446.68 pg/1 for Pb.

DISCUSSION

Geffard (2001), using Pb solutions at 10 pg/1

and 50 pg/1, obtained, as percentages of malforma-

tions, 14.8 ± 6.7% and 17.2 ± 3.9%, respectively;

whereas, 100% of larvae with abnormalities were

observed at 1200 pg/1. The LCjp was 482.0 ±

101.0 pg/1. The LC$o value we found for Pb is

446.68 pg/1. When comparing the two values, they

appear to be very similar.

In a previous study, carried out on the same spe-

cies and in the same biotope, Dermeche (2010) re-

ported, for Cd and Pb solutions at 10 pg/1,

percentages of malformations of 8.33 ± 0.47% and

10.66 ± 0.47%, respectively. At 200 pg/1 the per-

centages passed to 82.33 ± 0.94% and 40.67 ±

0.94% with a LC$g of 69. 1 8 pg/1 for Cadmium and

436.51 pg/1 for Lead. Once again, these values are

close to the values discussed in the present paper

(61.65 pg/1 for Cd and 446.68 pg/1 for Pb). Many

authors use Zinc and Copper to determine the LC$q

by using the sea urchin larvae. According to Hall

& Golding (1998), Ghirardini et al. (2005) reported

that a concentration of 30 pg/1 of Copper shows a

negligible effect, while it takes a concentration of

50 pg/1 to observe the first malformed larvae. These

results are consistent with those obtained by His et

al. (1999) who observed developmental defects

after treatment with a Copper solution at 60 pg/1.

Our study gives a percentage of 28.93 of mal-

formations at a concentration of 50 pg/1, a result that

remains consistent with results obtained by different

authors. Bougis & Corre (1974) suggested that the

effect of Copper varies depending on the quality of

brood stock. This would explain different results

obtained. It is likely that gametes of poor quality

are more sensitive to a toxic agent.

Although echinoderms are capable of removing

accumulated contaminants, the residence time in the

body and the principal mode of elimination appear

to depend on the metal (Warnau et al., 1997; Man-

naerts, 2007). According to Basuyaux et al. (2009)

and Petinay et al. (2009), larvae can develop up to

a Copper concentration of 90 pg/1 but malforma-

tions start appearing at 50 pg/1. Copper leads to a

significant reduction in growth at 30 pg/1 with lar-

vae showing spicules reaching 464 ± 7 microns

while normal ones generally are up to 495 ± 9 pm.

Bielmyer et al. (2005) noted that abnormalities in

larval development and, above all, the stop at plu-

teus stage were manifested at concentrations ran-

ging from 40 to 80 pg/1.

According to Fernandez & Beiras (2001), Cd

causes 100% of arrest of development of the

168

S. Dermeche, F. Chahrour & Z. Boutiba

°q Mnlfm ittaHcins

■ taNonaal

Development

: %Ma|fonnnliO[is

■ ^Normal

DevdopninJt

Figure 2. Percentage of deformed and normal larvae of

Paracentrosus Jividus observed after tretament with Cad-

mium solutions.

Figure 3. Percentage of deformed and normal larvae of

Paracentrosus Jividus observed after tretament with Cop-

per solutions.

Figure 4. Percentage of deformed and normal larvae of

Paracentrosus Jividus observed after treatment with Lead

solutions.

Figure 5. Percentage of deformed and normal larvae of

Paracentrosus Jividus observed after treatment with Zinc

solutions.

pluteus at 16 jLtg/1 and the stop at blastula and ga-

strula stage at concentrations from 32 to 64 jng/1, re-

spectively. Several studies demonstrated sensitivity

of sea urchin embryos to heavy metals solutions in

the range of 0.01-0.1 mg/1 for Hg and Cu, and 0.1-

10 mg/1 for Cd and Pb (Waterman, 1937; Kobaya-

shi, 1981; Carr, 1996; Warnau et al., 1996).

In a Cu solution at 64 pg/1, embryonic develop-

ment was arrested at gastrula stage, and at morula

stage at 128 jug/1. The toxic effects of Zinc on the

larval development of sea urchin were as follows:

the highest concentration used, 480 pg/1, completely

inhibited the embryonic development; at very low

concentrations (7.2 jng/1) no inhibitory effects were

observed at first cleavage or at pluteus formation;

exogastrula and Apollo-like gastrula were observed

at concentrations ranging from 14 to 58 jug/1. At hi-

gher concentrations (120 to 240 jng/1 ), embryonic de-

velopment and the elevation of the fertilization

membrane showed signs of delay and even malfor-

mations, as well as polyspermies, permanent bla-

stula, or exogastrula (Kobayashi & Okamura, 2006).

Other metals known to cause exogastrulation in

echinoids are: sodium selenite, cobalt chloride, zinc

chloride or acetate, nickel, mercury chloride or ace-

tate, the trivalent chromium and manganese chlo-

ride (Rulon, 1952; 1956; Timourian, 1968;

Timourian & Watchmaker, 1970; Kobayashi, 1971;

1990; Murakami et al., 1976; Pagano et al., 1982;

Evaluation of the toxicity of metal pollutants on embryonic development of the sea urchin Paracentrotus lividus

169

Species

References

Paracentrotus lividus

<32 pg/1

> 11 pg/1

—

Pagano et al., 1986

—

> 3 3 pg/1

Ramachandra et al.,1997

—

0.21-0.26 pg/1

—

Warnau & Pagano, 1994

—

482.68 pg/1

—

Geffard, 2001

158.48 pg/1

61.65 pg/1

446.68 pg/1

389.04 pg/1

present study

Strongylocentrorus pur-

puratus

6.3 pg/1

—

<9.7 pg/1

—

Dinnel, 1990

—

0.5 pg/1

—

23 pg/1

Ramachandra et al.,1997

Strongylocentror us

inter me dius

—

0.5 to 2.5 pg/1

—

Gnezdilova et al., 1985

Arbacia Iixula

—

10-100 pg/1

Castagna et al., 1981

Table 2. Toxicity (ZCjp) of heavy metal (Cd, Cu, Pb, Zn) solutions at different concentrations for different sea urchin

species from the Mediterranean.

Mitsunaga & Yasumasu, 1984; Vaschenko et al.,

1994); according to Lallier (1955) and Timourian

(1968), skeletal malformations of pluteus were

caused by Zinc whereas delay in skeletal develop-

ment was always caused by Cadmium and Cobalt

(Kobayashi, 1990; Mannaerts, 2007).

King & Riddle (2001) showed that exposure

of Sterechinus neumayeri embryos to various con-

centrations of Copper caused significant damages

to the development at different stages and, parti-

cularly, at the stage of blastula; moreover, signi-

ficant abnormalities were observed at a

concentration of 4-5 pg/1. High mortality of em-

bryos was estimated at a concentration of 16 pg/1,

and abnormalities were observed at a concentra-

tion of 32 pg/1; a Copper concentration of 11.4

pg/1 caused 50% of developmental abnormalities

after 6 to 8 days of exposure.

Radenac et al. (2001) reported, for Cu solutions

at 50 pg/1, about 36.9% of malformations which

approximates the results (28.93%) observed, for

the same concentration, in this study; however, at

100 pg/1 this rate reached 99.80% which exceeds

our result (41.91%); 100% of larval malformations

were obtained at 250 pg/1 while our study showed

52.66% of malformations at 200 pg/1. For Pb so-

lutions, at 250 pg/1, a high percentage (96.6%) of

malformation was reported. On the contrary, in

our study, at 200 pg/1, we obtained only 40.33%

of malformations. These results seem to suggest

a different sensitivity of different species to

heavy pollutants; concerning Zn, our results are

coherent with those of Radenac et al. (2001).

CONCLUSIONS

Considering different stages of development of

P. lividus , embryos and larvae were found to be

the most sensitive and best suited to study heavy

metal toxicity. Moreover, they can be used when

testing short (embryotoxicity) and long-term (lar-

val growth) issues. Information reported in this

study show that responses are indicative of embryo

sensitivity. P. lividus fulfills the characteristics of

a good indicator species as accumulative bio-indi-

cator of the health of a given environment.

Cadmium, Copper, Lead and Zinc are consi-

dered among the most toxic and persistent pollu-

tants, with a very long biological half-life (16 to

33 years) leading to accumulation in organs (Gu-

thrie & Perry, 1980). It is therefore an urgent need

for further research and adequate scientific-envi-

ronmental strategies to encourage studies of this

type and use the results for the management of

harmful polluting sources.

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Biodiversity Journal, 2012, 3 (3): 173-178

Metoncholaimus sp.(Nematoda Oncholaimidae) pseudopara-

site of Mullus surmuletus (Linnaeus, 1 758) (Perciniformes Mul-

lidae) in the western Algerian Sea

Maya Meriem Hassani',S. Ahmed Kerfouf '* & Nawel Amel BrahimTazi 2

‘Laboratoire d'eco-developpement des espaces, Universite Djilali Liabes, Sidi Bel Abbes, Algerie; e-mails: mayahassani@live.com;

kerfoufahmed@yahoo.fr

2 Laboratoire Reseau de Surveillance Environnementale, Universite Es-Senia Oran, Algerie; e-mail: meltazi@hotmail.com

jjj

' Corresponding author

ABSTRACT This study was carried out between October 2009 and July 2010 to determine nematode pa-

rasites of the red stripped mullet, Mullus surmuletus (Linnaeus, 1758), in the gulf of Oran

(western Algeria), located at 35°43’ N - 0°37’ W. A total of 100 fishes caught from the local

fishermen by gill-net were investigated. Our investigation revealed the presence of three ne-

matodes (one female and two males) located in the intestine of two infected fishes, these ne-

matodes were alive and not attached to the mucosa of the fish host. The examination of the

nematodes recovered showed that they belong to the genus Metoncholaimus Filipjew 1918

(Oncholaimidae Oncholaiminae). These nematodes are free living mostly in the coastal marine

sediment; Mullus surmuletus might acquire them accidentally while either feeding on them

or along with other food items taken from the bottom.

KEY WORDS Mullus surmuletus ; Nematode; Pseudoparasites; Oran; Western Algeria.

Received 04.05.2012; accepted 26.07.2012; printed 30.09.2012

INTRODUCTION

The striped red mullet Mullus surmuletus (Lin-

naeus, 1758) (Perciniformes Mullidae), a benthic

perciform fish with a widely known distribution, is

very common in the Algerian coasts and is a com-

mercially important species (Figs. 1-3).

On the other hand, its nematode parasites in the

western Mediterranean sea are poorly known al-

though having been studied since more than one

century by numerous authors who considered the

system Helminthes-Mw//ws as the richest one and

the most diversified of the Mediterr anean sea (Ba-

youmy et al., 2008; Ferrer et al., 2005; Neifar et al.,

2007; Ternengo et al., 2009). In this regard, we

began a helminthological study during which we

faced the problem posed by pseudoparasitism by

known species of free-living nematodes.

MATERIALS AND METHODS

Fish were collected by means of a trammel net

at a mean depth of 15 m, according to the traditio-

nal local small-scale fishery techniques. Individual

body weight and size (total length), sex, and matu-

rity stage were recorded. The range of fish size

(total length) was 10.5-22 cm.

The whole gastro-intestinal tract was removed

immediately after capture and all portions (sto-

mach, pyloric caeca and intestine) were opened

by a longitudinal incision. Removal of contents

was obtained by successive washes with a wash

bottle in a Petri dish, the food material collected

was examined under a dissecting microscope

Zeiss Stemi 2000.

Only helminthes infesting this tract were exami-

ned. The parasites were hand sorted and placed ini-

174

M.M. Hassani, S.A. Kerfouf & N.A. BrahimTazi

Figures 1, 2. Sampling site: Madagh bay, Oran, Algeria. Figure 3. Mullus surmuletus (Linnaeus, 1758).

tially in 2% NaCl saline solution and then stored in

75% ethanol. The nematodes specimens were stai-

ned in Acetic-Carmin, dehydrated and mounted in

Canada balsam.

The collected nematodes were cleared in glyce-

rin for examination. Drawings were made with the

aid of a Camera Lucida connected to a Wild bright

field microscope.

For the identification of nematodes, drawings

were compared with those of specialists in parasitic

nematodes of fishes (Anderson, 1992; Moravec,

1998). Identification of nematode pseudoparasites

did require the consultation of specialist works on

free-living nematodes (i.e. Hope & Murphy, 1972;

Tarjan, 1980; Platt & Warwick, 1983).

RESULTS

Systematic position

Phylum Nematoda Rudolphi, 1808

Class Adenophorea Linstow,1905

Order Enoplida Filipjev, 1929

Family Oncholaimidae Filipjev, 1916

Genus Metoncholaimus Filipjew, 1918

Metoncholaimus sp.

Description (Figs. 4-7). Body elongated, somewhat

tapering to both cephalic and caudal regions.

Metoncholaimus sp. (Nematoda, Oncholaimidae) pseudoparasite of Mullus surmuletus in the western Algerian sea

175

Cuticle. Smooth without transverse striations,

thick, particularly in the cervical and the caudal

regions.

Anterior extremity. The head bears a crown of

tubular and non-segmented sensilla; mouth opening

is spacious, roughly hexagonal, with narrow mem-

branous margin provided with small papillae; lips

are very distinct and developed; buccal capsule

large, with well sclerotized walls, sub-terminal next

to a simple muscular esophagus very long and so-

mewhat expanded at its posterior part. Nerve ring

encircling esophagus anteriorly, excretory pore not

located. Outer sensory organs represented by a

crown of well developed tubular and non-segmen-

ted bristles, never seen beyond the nerve ring.

Caudal region: the tail of males and females is

conical, tapered and curved, short bristled mainly

located in both preanal regions in both sexes.

Genital equipment, males: testes initiating at

a short distance below the end of the muscular

esophagus; strong spicules, regularly pairs are ar-

ched without individualized capitulum and the di-

stal end is flared into two points. Solid

gubernaculum, consisting of two distinct parts,

central bulging and curved ventral apophysis. Nu-

merous short bristles (8 to 10) are present in the

cloacal opening region.

Genital equipment, females: only one female was

found, it was non-gravid with monodelphic uterus.

Ovary anteriorly starting below esophagus end. Ge-

nital opening situated in posterior end of the body.

DISCUSSION

The examination of stomach contents of Mullus

surmuletus revealed the presence of several preys

difficult to identify because of their advanced state

of digestion. Generally, they are mainly composed

of fragments of polychaetes, small fish or crustace-

ans (N'Da, 1992).

The stomach content analysis of Mullus surmu-

letus revealed a wide food range that can explain

the observed parasite richness (Klimpel et al.,

2008). Only parasites resist to digestion which led

us to believe that the three Metoncholaimus speci-

mens found alive and intact were nematode parasi-

tes of the fish. More precisely, these nematodes are

pseudoparasites, i.e. Mullus surmuletus may acci-

dentally ingest them from marine sediments, the

diet of the latter being composed largely of benthic

prey (Quero & Vayne, 1997) that the mullet har-

vests from the sediment through its burrowing and

tactile barbells (Bougis, 1949).

Pseudoparasitism is a fairly rare phenomenon,

but was nevertheless described; indeed, pseudopa-

rasites were found alive and in perfect condition in

the fish Haemulon sciurus (Shaw, 1803) in Brazil.

On a total of 50 fish examined, 13 contained nema-

tode pseudoparasites at the rate of 2 to 50 speci-

mens per fish.

These nematodes were identified as Metoncho-

laimus amplus Filipjev, 1918, Oncholaimidae (Mo-

ravec et al., 1990) that is a species of free living

nematodes described for the first time by Hopper

(1967). There are small differences between Meton-

cholaimus amplus specimens which may be consi-

dered to be within the limits of intraspecific

variability.

This species was recorded in the coast of Flo-

rida, Bermuda Islands and also from the Suez canal

(Riemann & Rachor, 1972). Comparison of our de-

signs with those of Hopper (1967) did not allow us

to assign our specimens to this species, however,

we can assign it to the genus Metoncholaimus

whose identification keys according to Keppner &

Tarjan (1989) are:

• Cuticle smooth without transverse striations.

• Non-segmented cephalic setae located in one

to three crowns before the nerve ring.

• Simply muscular and cylindrical esophagus

without vesicular cells.

• Well-developed buccal capsule.

• Tapered shank short and curved.

• Spicules paired, fronted a gubernaculum.

• Presence or no of ventral apophysis.

• Short caudal setae concentrated primarily on

the preanal region of male.

From a comparison of Metoncholaimus amplus

Hopper, 1967 with our specimens, a few differences

came to our attention: (i) M. amplus has two crowns

of cephalic setae, Metoncholaimus sp. just one; (ii)

as far as concerns shape and size of the copulatory

apparatus, M. amplus shows thin and slender spi-

cules and lacks of a ventral apophysis, our speci-

mens - on the contrary- had stronger spicules and a

ventral apophysis; (iii) in M. amplus the nerve ring

of esophagus is situated at the mid-length of eso-

phagus while in Metoncholaimus sp. is located

more anteriorly.

176

M.M. Hassani, S.A. Kerfouf & N.A. BrahimTazi

bucai capsule

muscular esophagus

cephalic seta

esophagus

spicules

gubernaculum

- apophysis

anus

Figures 4-7. Metoncholaimus sp. pseudoparasite of Mullus surmuletus. Fig. 4: anterior end; Fig. 5: detail of the anterior

end; Fig. 6: posterior end of male; Fig. 7: posterior end of female.

Metoncholaimus sp. (Nematoda, Oncholaimidae) pseudoparasite of Mullus surmuletus in the western Algerian sea

177

It should be noted that M. ampins approximates

our specimens particularly by the appearance of

the head region, the esophageal structure, the

shape of the buccal capsule, the measurements of

the body and the implementation of the bristles in

the caudal region.

The genus Metoncholaimus has twelve species

and, in the Mediterranean Sea, is mainly represen-

ted by the species Metoncholaimus pristiurus Zur

Strassen, 1894 (Gerlach & Riemann, 1973), with an

abundance of 68.54% of the total population of

free-living nematodes (Hedfi et al., 2010).

CONCLUSIONS

It is clear that Metoncholaimus sp. is not a real

parasite of Mullus surmuletus. Indeed, setae on its

cephalic and caudal regions indicate a free-living

mode of life. Nevertheless, the mode of survival

of pseudoparasites into the digestive tract and

their resistance to digestive enzymes remain un-

known although they are known to be biomonito-

ring tools in coastal ecosystems due to their

extreme sensibility to any environmental stress

(Mahmoudi et al., 2002).

Pseudoparasitism by known species of free li-

ving nematodes is rare, however it is interesting to

report it in order to attract the attention of some

ichtyoparasitologists who would easily confuse

free living nematodes with parasitic nematodes of

fishes because, despite nematodes are the most fre-

quent and the most important parasites of fishes

constituting a significant part of the parasite fauna

of these hosts in freshwater, brackish-water or even

marine environments throughout the world, there

is a world-wide shortage of specialists capable of

identifying unknown helminthological materials

(Moravec, 2007).

REFERENCES

Anderson R.C., 1992. Nematode Parasites of Vertebrates.

Their development and transmission. C.A.B. Interna-

tional, Walligford, 578 pp.

Bayoumy E.M., Abd El-Monem S. & Ammar K.A.,

2008. Ultrastructural study of some helminth parasi-

tes infecting the Goatfish, Mullus surmuletus (Ostei-

chthyes: Mullidae) from Syrt coast, Libya. Nature

and Sciences, 6: 51-63.

Bougis P., 1949. Recherches biometriques sur les rougets

{Mullus barbatus L. et Mullus surmuletus L.). These,

Universite de Paris, 174 pp.

Ferrer E., Aznar F.J., Balbuena J.A., Kostadinova A. &

Moravec F., 2005. Anew cystidicolid nematode from

Mullus surmuletus (Perciformes: Mullidae) from the

western Mediterranean. Journal of Parasitology, 91:

335-344.

Gerlach S.A. & Riemann F., 1973. Checklist of Aquatic

Nematodes: a catalogue of Nematoda Adenophorea

excluding the Dorylaimida. Veroffentlichungen des

Instituts fur Meeresforschung in Bremerhaven, Sup-

plement 4, pp. 1-734.

Hedfi A., Boufahja F., Mahmoudi M., Essid N., Hamouda

B., Aissa P & Mahmoudi E., 2010. Restructuration

des communautes nematologiques, du vieux port de

Bizerte apres son amenagement, p. 15-16. In Azzo-

ciation Tunisienne de Taxonomie, lere conference in-

ternationale, Taxonomie et Biodiversite, 23 Avril

2012, Cite des Sciences de Tunis, Tunis, 35 pp.

Hope W.D. & Murphy D.G., 1972. A taxonomic hierar-

chy and checklist of the genera and higher taxa of

marine nematodes. Smithsonian Contribution to Zoo-

logy, 137: 1-101.

Hopper B.E., 1967. Free-living marine nematodes from

Biscayne Bay, Florida, II. Oncholaimidae; descrip-

tion of five new species and one new genus ( Meyer -

sia). Marine Biology, 1: 145-151.

Keppner E.J. & Tarjan A.C., 1989. Illustrated Key to the

Genera of Free-Living Marine Nematodes of the Order

Enoplida. NO AA Technical Report NMFS, 77: 1-26.

Klimpel S., Kleinertz S. & Palm H.W. 2008. Distribution

of parasites from red mullets {Mullus surmuletus L.,

Mullidae) in the North Sea and Mediterranean Sea.

Bulletin of Fish Biology, 10: 25-38.

Mahmoudi E., Baccar E. & Aissa P, 2002. Response of

free-living nematodes. Bulletin de Zoologie, 132:

111-123.

Moravec F., 1998. Nematodes of freshwater fishes of the

Neotropical Region, Academy of Sciences of the

Czech Republic, Praha, 464 pp.

Moravec F., Kohn A. & Santos C.P, 1990. Metoncholai-

mus ampins Hooper, 1967 (Nematoda: Oncholaimi-

dae), a pseudoparasite of the fish Haemulon sciurus

(Shaw) in Brazil. Folia Parasitologica, 37: 363-365

Moravec F., 2007. Nematode parasites of fishes: recent

advances and problems of their research. Parassito-

logia, 49: 155-160.

N'Da K., 1992. Regime alimentaire du rouget de roche

Mullus surmuletus (Mullidae) dans le nord du Golfe

de Gascogne. Cybium, 16:159-167.

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Neifar I., Ferrer E. & Gastello D., 2007. Parasite fauna

of red striped mullet, Mullus surmuletus, in Tunisia

and the Spanish Mediterranean: a geographical

comparison. Parasitologica, 49: 351-356.

Platt H.M. & Warwick R.M, 1983. Free-living marine

nematodes. Part I. British Enoplids, Cambridge Uni-

versity, Cambridge, 307 pp.

Quero J.C. & Vayne J.J., 1997. Les poissons de mer des

peches francaises. Delachaux etNiestle, Lausanne-

Paris, 304 pp.

Riemann T & Rachor P, 1972. Geographical distribu-

tion of species of the genus Metoncholaimus (Filip-

jew, 1918). Journal of Zoology, 21: 167-187.

Tarjan A.C., 1980. An Illustrated guide to the marine ne-

matodes. Institute of Food and Agricultural Sciences

University of Florida, Gainesville, 135 pp.

Temengo S., Levron C., Mouillot D. & Marchand B., 2009.

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terranean Sea). Parasitology Research, 104: 1279-1287.

Biodiversity Journal, 2012, 3 (3): 179-188

Biodiversity and conservation of Wildlife at the Wafra area

n Kuwait

Hanan AI-Khalifa'^Afaf Al-Nasser 1 , Mohammad Safar Abbas 2 &Jamal Dashti 1

'Kuwait Institute for Scientific Research, RO. Box 24885, 13109 Safat, Kuwait; email: hkhahfa@kisr.edu. kw

2 Joint Operation (JO)- Wafra, Kuwait Oil Company, Kuwait

’Corresponding author

ABSTRACT In response to the increasing needs to conserve wildlife and to enhance biodiversity, the

Joint Operations-Wafra (JO- Wafra) protected their natural environment by fencing and de-

dicating areas for conservation of biological diversity. The main objective of this study is

to conduct a wildlife baseline assessment in the oilfields of JO-Wafra and to identify po-

tential habitats of endangered or threatened species that could occur on site. The wildlife

survey covered the winter and early spring seasons. Although short and insufficient to pro-

vide a detailed assessment, the field data collected indicated significant differences in the

number of individuals and wildlife fauna species within the fenced and unfenced oilfields.

It also showed that the fenced JO-Wafra has rich and diverse wildlife fauna species, an in-

dication of ecological health. In addition to JO-Wafra oilfield, it is recommended to protect

the South Umm Guddair (SUG) oilfields from livestock grazing and wildlife hunters. The

protected area could, therefore, increase wildlife habitats and might harbor some endan-

gered wildlife species. It is also recommended to connect the two oilfields with native

shrubs and trees planted along the road, to serve as “green corridor”, shelter and additional

source of food for the animals of both oilfields.

KEY WORDS Endangered wildlife; Oil fields; Wildlife fauna; Wildlife habitat; Wildlife monitoring.

Received 07.06.2012; accepted 02.08.2012; printed 30.09.2012

INTRODUCTION

Biological diversity refers to the variety of life

forms including the genes they contain, and the eco-

systems they form.

There are three different levels of biodiversity:

genetic diversity which refers to the variety of ge-

netic material contained in all the individuals, spe-

cies diversity which refers to the variety of living

species and ecosystem diversity which refers to the

variety of habitats and ecological processes. In

other words, it is reflected by the variety of all

forms of life on earth, which provides the building

blocks for human existence.

The total number of species (defined as a popu-

lation of organisms which are able to interbreed

freely under natural conditions) is estimated to

range from 5 million to 100 million globally;

though less than 1.7 million have actually been de-

scribed (BUDEST, 1993; FEPA, 2003; Maffi, 2005;

Sarkar, 2006).

Biodiversity conservation is of a major impor-

tance internationally because humans derive their

food, medicines and industrial products from bio-

logical diversity of the wild and its domesticated

components. It also gives future generations the op-

portunity to enjoy nature. In addition, biodiversity

is important for the recycling of essential elements,

such as carbon, oxygen, and nitrogen.

It is also responsible for mitigating pollution,

protecting watersheds and combating soil erosion;

accordingly, experiencing and increasing our kno-

180

H.Al-Khalifa,A.Al-Nasser, M.S. Abbas &J.Dashti

wledge about biodiversity transforms our values

and beliefs (McGregor, 1994; FEPA, 2003; Boro-

kini et al., 2010).

The state of Kuwait covers an area of about

17600 Km 2 at the north-eastern corner of the Ara-

bian peninsula, between 28° 30’ N and 30° 05’ N in

latitude and between 46° 33’ E and 48° 35’ E longi-

tude. Kuwait's environment is characterized by

scarcity of rainfall (100 mm/yr) and extreme tem-

perature variations throughout the year.

The summer temperature is very hot (over 40-

50°C), while the winter is cool to mild with a mean

temperature of 12.7°C. The water resources are

very limited in Kuwait. There is no fresh surface

water supply and very limited renewable groun-

dwater. The adverse climate conditions of the state

of Kuwait affected its biological diversity and en-

vironmental ecosystems (Omar et al., 2001). The

desert of Kuwait has long been known as an im-

portant source of food, livestock grazing and wil-

dlife hunting. Desert plants were used for fuel and

medication purposes.

Urbanization, rapid increase in population, over-

grazing, recreation usage, environmental factors,

and destruction due to Iraqi invasion in 1990 are

main contributing factors to the ecological degra-

dation of the country (McGregor, 1994; Omar,

2000; Selby, 2005). Biodiversity conservation has

become one of the challenging priorities for many

countries, including the state of Kuwait, to combat

species extinction. The State of Kuwait ratified the

International Convention on Biodiversity and the

National Strategy for Biodiversity Conservation

was adopted in order to conserve and enhance bio-

logical diversity in the country. Numerous wildlife

research studies were conducted in the State of Ku-

wait. From all these studies, information on flora

and fauna of Kuwait has been collected.

A list of desert animals has been prepared. Also,

threatened desert animals and those to be extinct

were identified such as Houbara Bustard ( Chlamy -

dotis undulata macquennii ), Desert Monitor ( Vara -

nus griseus). Ostrich ( Struthio camelus ) and

Arabian Oryx ( Oryx leucoiyx ) (KISR., 1999; De-

lima et al., 2005; Zaman et al., 2005).

In December 1922, a partitioned neutral zone

(PNZ) was established by agreement between the

Kingdom of Saudi Arabia and the State of Kuwait,

in order to allow tribesmen from both countries to

use this favorite grazing ground (Chichester, 2000).

In 1938-1940, oil was discovered from the Al-

Burgan area, near PNZ. In 1948, a 60 year conces-

sion was granted by the Kuwait government to the

Aminoil, a small group of oil companies to ex-

plore and exploit the Kuwait side of the PNZ. Si-

milarly in 1949, the Getty Oil Company (formerly

Pacific Western Oil Corporation) gained grants

from the Kingdom of Saudi Arabia (KSA) to ex-

plore the PNZ (KSA side).

The Joint Operations (JO) was born in 1960

when the two oil companies formed a joint commit-

tee to oversee and supervise their operations with

the resultant productions divided equally to both

parties: the Kuwait Oil Company (KOC), which

operates the Kuwaiti concession and the Texaco In-

corporated, Saudi Arabian Texaco (SAT) that ope-

rates the Saudi Arabian concession.

The 3,600 Km 2 partitioned neutral zone oil-

fields were not spared during the Iraqi invasion of

Kuwait in 1990. The oil wells were destroyed and

burned contributing to the environmental catastro-

phe man had ever known. In 1999-2002, the peri-

meter fence around the JO-Wafra main oilfield was

constructed to prevent livestock grazing and wil-

dlife hunters from the area.

This resulted to the gradual rehabilitation of the

flora and fauna in the oilfield. Literature on the

wildlife fauna of the Wafra area is very limited.

Example is the “Insect Fauna of Kuwait” by Al-

Houty (1989), when some insect samples were

collected in the Wafra area.

An environmental impact review prepared by

Chichester (2000) described the fauna of the

upland deserts and sabkha of the Partitioned Neu-

tral Zone (PNZ) as “Over 220 species of birds

have been observed in the PNZ in recent years...

fauna of the upland deserts and sabkha includes

common insects; ants and beetles; lizards and sna-

kes; such as Sand Boa, Rat Snake, Blue-throated

Agamid, Desert Monitor, and Dhub. Small, noc-

turnal mammals include Jerboa, Jirds, Desert Fox,

and Long-eared Hedgehog”.

The current study involves fauna baseline asses-

sment within the JO-Wafra territories with the fol-

lowing main objectives: assess the wildlife fauna in

JO-Wafra main area; and compare the quality of ha-

bitat inside and outside the JO-Wafra main area.

The work has been implemented between Kuwait

Institute for Scientific Research (KISR) and Kuwait

Gulf Oil Company (KGOC).

Biodiversity and conservation of Wildlife at the Wafra area in Kuwait

181

MATERIALS AND METHODS RESULTS

The wildlife fauna study commenced in De-

cember 2005 and terminated in March 2006. This

report covers only the study period (i.e. from Ja-

nuary to March, 2006), wherein 15 field data col-

lection exercises were performed with a total of

345 field data collected from 11 selected wildlife

(fauna) study sites, within the fenced JO- Wafra

main oilfield and the unfenced SUG (South Umm

Guddair) oilfield. Selections of wildlife study sites

at the JO- Wafra oilfield were performed during re-

connaissance surveys. The criteria used in selecting

the possible wildlife study sites were: (1) type of

habitat that include soil and vegetation cover; and

(2) location within the oilfield, disturbed or undi-

sturbed (see Table 1).

Several wildlife survey methodologies were im-

plemented to study the wildlife biodiversity, na-

Types of habitat

Wildlife study sites number

1 .Habitat with good vegeta-

tion cover

2, 3, 4, 8, 9 and 10

2. Habitat with poor vegeta

tion cover

1 and 5

3. Windblown sand covered

habitat

6 and 7

4. Overgrazed and unprotec

ted habitat

Table 1. Different Wildlife study sites according to

types of habitat.

mely: 1) Line Transects (LT): of 5 km to record

animals within a specific habitat type. 2) Pitfall

Trapping (PFT): to catch ground crawling animals

such as reptiles and invertebrates. 3) Baited Mam-

mal Trap Line: is usually a one kilometer long trap

line. The large mammal trap (MTL) is placed bet-

ween two small mammal traps (MTS) at a distance

of 250 meters. 4) Mark-Release-Recapture (MRR):

to estimate the population dynamics of an area.

MRR models were developed for field studies in

which the count statistics are numbers of marked

and unmarked animals caught (Nichols, 1992;

Grenwood, 2000).

From December 2005 to March 2006, 17 trips

were made to the JO- Wafra main (fenced) and the

unfenced South Umm Guddair (SUG) oilfields. A

total of 15 field data collecting exercises were

performed. This included line transects, baited

mammal trappings and pitfall trappings, conduc-

ted over at least three consecutive days (Table 2;

Figs. 1-2).

Line Transects (LT): a total of 49 LT exercises

were performed, covering the winter and early

spring periods of the country. It was noticeable that

during the last days of line transect exercises, more

birds were observed and even the shy Red fox ( Vul-

pes vulpes) was recorded. This may be due to the

rise in temperature and the pleasant spring weather

in the air. More than 34 species of wildlife fauna

were recorded from the line transects performed.

These included 27 species of birds, one species

of mammal, one species of reptile and more than

six species of invertebrates (butterflies, dragonflies,

flies and ground hoppers). Table 3 lists the species

recorded during line transect exercises at the JO-

Wafra oilfields. The list is not conclusive, as it was

taken during winter and early spring seasons.

No. of

Field Trips

Type of Trips

Location of Trips

Field orientations, recon-

naissance, site selections

and installation of field JO-Wafra main and

2 study equipment e.g., SUG oiltield

mammal traps and pitfall (south Um Gud-

traps with drift fences dair)

Field data collection resul-

ting to the following field

data collected:

49 from line transects (LT) 11 wildlife (fauna)

148 from two (x2) small study sites within

15 mammal traps at each the fenced JO-

study site Wafra and the un-

74 from one (xl) large fenced

mammal trapping at each SUG oilfields

study site

74 from pitfall traps in as-

sociation with drift fences

(1x5) at each study site

Table 2. Trips made by Wildlife Survey Team to JO-

Wafra Oilfields.

182

H.Al-Khalifa,A.Al-Nasser, M.S. Abbas &J.Dashti

Wildlife fauna recorded during LT

(January 2006 to March 2006)

® m 20

■g S 15

C Q.

= W10

Inside JO Outside JO

Location of LT

Figure 1. Wildlife species recorded during line transect in-

side and outside JO-Wafra oilfields

Wildlife fauna recorded at JO-Wafra

(January - March 2006)

Herbivores

Fruitivores

6 %

Granivores

24%

Consumers

Predators

15%

Insectivores

43%

Figure 2. Different trophic levels in the wildlife fauna re-

corded at JO-Wafra oilfields from January to March 2006.

Ground crawlers trapped in PFT at JO-Wafra oilfields

(January 2006 - March 2006)

S 15

Lizards

Insects

Beetles

Arachnids

■ Number of species 5

Class of Animals

Animal Species Trapped in PFT at JO-Wafra

(January 2006 -March 2006)

Figure 3. Classes of animal species trapped in PFT at JO-

Wafra oilfields.

Figure 4. Animals recorded from PFT at JO-Wafra are

shown according to their trophic levels.

More animal species are expected to be recor-

ded if the survey covers the four seasons, especially

the two migration periods of the country. Except for

the residents, such as the Black-crowned finch lark.

Crested lark, House sparrow and the Feral pigeon,

the birds might only be over wintering in the coun-

try e.g., Tawny pipit, Short-eared owl, Blue rock

thrush. Pied wheatear, Woodchat shrike, Great grey

shrike, and Hoopoe lark among others.

The list is only 7.7% from the total number of

bird species recorded in the country. The Black-

crowned finch larks ( Eremopterix nigriceps ) were

recorded breeding at study area, while both the Cre-

sted larks ( Galerida cristata) and the Isabelline

wheatears ( Oe nan the isabellina) were also obser-

ved displaying courting behaviors.

Pitfall trappings: there were 64 pitfall trapping

exercises performed at the fenced main JO-Wafra

and the unfenced SUG oilfields. More than 46 ani-

mal species were recorded during these exercises,

including 10 species of arachnids; lizards (5 spe-

cies); beetles (15 species); and 16 species of insects

(Figs. 3-4 and Table 4). Baited mammal trappings:

there were seven (x7) mammal trapping exercises

performed at the JO-Wafra study sites, for the du-

ration of the study period.

Biodiversity and conservation of Wildlife at the Wafra area in Kuwait

183

Study Site

Animal Species

SLT

NLT

SUG

Black-crowned Finch Lark, Eremopterix nigriceps (Gould, 1839)

Barn swallow, Hirundo rustica (Linnaeus, 1758)

Blue Rock-Thrush, Monticola solitaries (Linnaeus, 1758)

Lepidoptera sp. 1

Chiffchaff, Phylloscopus collybita (Vieillot, 1817)

Cream-coloured courser, Cursorius cursor (Latham, 1787)

Crested lark, Galerida cristata (Linnaeus, 1758)

Arabian babbler, Turdoides squamiceps (Cretzschmar, 1 827)

Desert wheatear, Oenanthe deserti (Temminck, 1825)

Dhub, llromastyx microlepis (Blanford, 1874)

European roller, Coracias garrulous (Linnaeus, 1758)

Feral pigeon, Columba livia (J.F. Gmelin, 1789)

Great grey shrike, Lanius excubitor (Linnaeus, 1758)

Ground hopper, Tetri x undulata (Sowerby, 1 806)

Floopoe, Up upa epops (Linnaeus, 1758)

Greater Hoopoe lark, Alaemon alaudipes (Desfontaines, 1789)

House sparrow, Passer domesticus (Linnaeus, 1758)

Isabelline wheatear, Oenanthe isabellina (Temminck, 1829)

Kestrel, Falco tinnunculus (C.L. Brehm, 1855)

Northern wheatear, Oenanthe oenanthe (Linnaeus, 1758)

Olivaceous warbler, Iduna pallida (Hemprich et Ehrenberg, 1833)

Pallid harrier, Circus macrourus (S.G. Gmelin, 1770)

Pied wheatear, Oenanthe pleschanka (Lepechin, 1770)

Red-backed shrike, Lanius collurio (Linnaeus, 1758)

Red fox, Amphicoma vulpes vulpes (Fabricius, 1792)

Sand martin, Riparia riparia (Linnaeus, 1758)

Short-eared owl, Asio flammeus (Pontoppidan, 1763)

Short-toed eagle, Circaetus gallicus (Gmelin, 1788)

Short-toed lark, Calandrella br achy dactyl al longipennis (Eversmann, 1848)

Stable flies, Stomoxys calcitrans (Linnaeus, 1758)

Sundevall jird, Meriones crassus (Sundevall, 1842)

Swift, Apus barbatus (Sclater, 1866)

Tawny pipit, Anthus campestris (Linnaeus, 1758)

Turtle dove, Steptopelia turtur (Linnaeus, 1758)

Table 3. Animal species recorded during line transect at the JO-Wafra Oilfield. Legend: G=General line transect.

SLT=South LT. NLT=North LT. SUG= Unfenced JO-Wafra oilfield LT.

184

H.Al-Khalifa,A.Al-Nasser, M.S. Abbas &J.Dashti

Study Site

Animal species

Arabian darkling beetle, Pemelia arabica (Kaszab 1982)

Brilliant ground weevil, Bembidion sp.

Camel spider, GaJeodis arabs (Koch, 1842)

Capsid bug, Eurydema ornatum (Linnaeus, 1758)

Centipede, Craterostigma sp.

Churchyard beetle, BJaps kollari (Seidlitz G von, 1896)

Desert runner, Cataglyphis niger (Andre, 1981)

Domino beetle, Anthia duodecimguttata (Bonelli, 1813)

Elevated stalker, Adesmia stoeckleini (Koch, 1940)

Giant black ant, Camponotus xerxes (Forel, 1904)

Golden-tipped ant, Camponotus sericeus (Forel, 1904)

Ground mantis, Eremiaphila braueri (Krauss, 1902)

Hairy capsid bug, Tropinota squalida (Scopoli, 1763)

Joker bee, Parachistus pulchellus (Greathead, 1980)

Jumping spider, Salticidae

Fesser scarab, Mnematium sp.

Fesser yellow scorpion, Uroplectes alstoni (Purcell, 1901)

Fong-legged spider, Pholcidae

Mesopotamian beetle, Sepidium mesopotamicum (R.,1904)

Mosquito, Anopheles pharoensis (Theobald, 1901)

Opossum beetle, Mesostena puncticollis (Sober, 1835)

Orb-weaver spider, Araneidae

Pill bug, Armadillidium vulgare (Fatreille, 1804)

Pinstripped ground weevil, Ammoc/eonus aschabadensis (Ft., 1884)

Pitted beetle, Adesmia cancell ata (Klug, 1830)

Meloe "Queen", Meloe omanicus (Kaszab, 1983)

Rack beetle, Tentyrina palmeri (Crotch, 1872)

Rock gecko, Bunopus tuberculatus (Blanford, 1874)

Sand gecko, Stenodactylus doriae (Blanford, 1874)

Saber-toothed beetle, Scarites guineensis (Dejean, 1831)

Scorpion (Black), Androctonus crassicauda (Olivier, 1807)

Seville row beetle, Paraplatyope arabica (Koch, 1965)

Short-nosed lizard, Mesalina brevirostris (Blanford, 1874)

Silverfish, Thermobia domestica ( Packard, 1837)

Small black ant, Monomorium gracillimum (Smith, 1861)

Biodiversity and conservation of Wildlife at the Wafra area in Kuwait

185

Study Site

Animal species

Small red ant, Monomorium pharaonis (Linnaeus, 1758)

Scutte lizard, Acanthodactylus scutellatus (Audouin, 1827)

Schmidt lizard, Acanthodactylus schmidti (Haas, 1957)

Tiger moth, Utetheisa pulchella (Linnaeus, 1758)

Ugly trox, Scleron sulcatum (Kulzer, 1956)

Variable stalker, Adesmia cothurnata (Forskal, 1775)

Winged ant, Podalonia sp.

Wolf spider, Lycosidae

unidentified moth

unidentified larva

Lepidoptera sp. 2

Table 4. List of animal species trapped at different PFT in JO-Wafra Oilfields.

The twenty two (x22) MTS trapped 15 rodents

from one species ( Meriones crassus). Whereas the

collapsible Tomahawk traps (MTL) trapped one

species (feral dog). There were seven rodent recap-

tures and three of the feral dog, which is ‘trap

happy’ because it was recaptured every trapping

exercises. Table 5 shows the animal species trapped

and caught during mammal trapping exercises at

the JO-Wafra oilfields.

Mark-release-recapture (MRR): the field data

collection exercises were performed during the win-

ter, when the temperature ranged from 3°C to 8°C

and during early spring, when the temperatures star-

ted to rise (14°C to 18°C). Therefore, the field data

collected is not representative of the entire popula-

tion of each study site but indicative only for the

duration of the study period.

There were 32 trapping exercises performed at

the JO-Wafra oilfields. This includes eight exercises

each for the PFT; baited MTS1; MTS2; and MTL.

These trapping exercises caught a total of 74 wil-

dlife fauna (including recaptures) from different

study sites at JO-Wafra. Five (5) species of lizards

were caught in the PFT, namely: Mesalina breviro-

stris (27 individuals); Acanthodactylus scutellatus

(x8); A. schmidtii (x2); and 22 geckos ( Stenodacty -

lus slevini and B unopus tuberculatus).

Nine recaptures were recorded for the lizards

during pitfall trappings; the first three species of the

above-mentioned lizards were recorded to be active

in winter, while the two species of geckos were

trapped only when the ambient temperature at the

study sites were higher at around 20°C.

The fringed-toed lizards i.e. A. scutellatus and

A. schmidtii seemed to be concentrated only at the

low lying soot covered habitat, with good vegeta-

tion cover. The two species of geckos: S. slevini

and B. tuberculatus were trapped in the PFT only

at the start of spring, when the temperatures at the

study sites were higher. These species were recor-

ded during the last two exercises. Two (2) species

of mammals (Meriones crassus and Canis dome-

sticus ) were trapped during baited mammal trap-

ping exercises.

There were 19 Sundevall jirds ( Meriones cras-

sus) captured by the small mammal traps from eight

study sites within the JO-Wafra main oilfield. Seven

re-captures were recorded.

DISCUSSION AND CONCLUSIONS

The current study was conducted to assess the

wildlife fauna in JO-Wafra main area; and to com-

pare the quality of habitat inside and outside the JO-

Wafra main area. The work has been implemented

between Kuwait Institute for Scientific Research

(KISR) and Kuwait Gulf Oil Company (KGOC).

186

H.Al-Khalifa,A.Al-Nasser, M.S. Abbas &J.Dashti

Seventeen field visits to the JO-Wafra oilfields

were undertaken by the wildlife team, to perform

15 field data collection exercises that resulted in

444 field data collected. The oil fires that occurred

during the Iraqi invasion of Kuwait were the main

cause of diversity loss in the country. It had signi-

ficant effect on species and ecosystem, this effect

shifted species distribution and caused reductions

in population size that could be due to reduction

in survival and fecundate rates.

This negative effect is well documented in

other studies that investigated similar items (Da

Fonseca et al., 2005; Parmesan, 2006; Fischlin et

al., 2007). Conserving wildlife and biodiversity is

increasingly recognized as an essential element of

life. Its importance involves production of plants

and animals for food, providing recreational re-

sources, flood and pest control, providing chemi-

cals for treatments. Accordingly, biodiversity

conservation is strongly related to finance, eco-

nomy and poverty degree in a society.

Petts & Platt (1990) demonstrated that most of

the benefits derived from wildlife and biodiversity

conservation are potentially quantifiable and can

significantly add to the economy of a society.

Many worldwide studies in the literature relate

biodiversity to social poverty (Adams et al., 2004;

Treves et al., 2005; Fisher & Christopher, 2007).

Consequently, wildlife and biodiversity conserva-

tion became a priority in the world.

The approach of protecting natural resources

and increasing extent of protected areas has been

described and used in other worldwide studies to

conserve wildlife and biodiversity (McNeely &

Schutyser, 2003; UNEP, 2006). In addition to re-

source protection, the current study also applied

the technique of monitoring wildlife populations.

It involves collecting, analyzing, and interpreting

ecosystem information. Such techniques develop

wildlife and natural resource management ap-

proaches. Monitoring wildlife and ecosystems

provide information that managers and compa-

nies such as Kuwait Oil Company can use to ad-

just or modify their commercial activities so that

they minimize negative effect on natural resour-

ces. These techniques have been used worldwide

to conserve wildlife and biodiversity (Adger et

al., 2003; Fischlin et al., 2007).

The field data collected showed that the fenced

JO-Wafra main oilfield has rich and diverse wil-

dlife fauna species, which suggests that ecological

health in this area is significantly better than the

unfenced and unprotected SUG oilfields.

Although short and insufficient to provide a de-

tailed assessment of the studied areas, the field

data collected showed that the fenced JO-Wafra

main area is rich and diverse in wildlife fauna, in-

dicating significant ecological health compared to

the unfenced and overgrazed South Umm Guddair

oilfield, which is located approximately 29 kilo-

meters northwest of the main oilfield. The field

data collected also indicated that additional sur-

veys and monitoring activities for the wildlife at

the JO oilfields are necessary and conducted to

cover the different climatic seasons and migration

periods of the country.

The field data collected showed that there are

at least four types of wildlife habitats at the JO-

Wafra oilfields: high and low lying habitat with

good vegetation cover; high and low lying habitat

with poor vegetation cover; windblown sand co-

vered habitat; and over-grazed and unprotected ha-

bitat. The first three types of habitats are located

inside the fenced oilfield, while the latter is at the

unfenced South Umm Guddair (SUG) oilfield. Be-

cause of the perimeter fence constructed in 2000,

the JO-Wafra main oilfield enjoyed protection

from livestock grazing and wildlife hunters.

This has brought to the gradual rehabilitation

of the flora and fauna within the perimeter fence.

There were more than 78 wildlife fauna species

recorded at the JO-Wafra main oilfield. This in-

cludes the 19 species (24.36%) of wildlife fauna

recorded at the unfenced SUG oilfield. The ti-

ming of the field data collection might have im-

pact on the numbers of individuals and fauna

species recorded from both study areas because

desert animals tend to hibernate during winter

and only come out during spring. It is suggested

and recommended that the SUG oilfield be fen-

ced and protected from livestock overgrazing

and wildlife hunters. The two oilfields then could

be connected with native shrubs and trees plan-

ted along the road.

The fenced SUG and the additional plants will

augment and increase the possible areas for re-

sting, feeding and even breeding of some threate-

ned and endangered migrating fauna that pass

through the country during their migration move-

ments (examples are the Houbara bustard, Chla-

Biodiversity and conservation of Wildlife at the Wafra area in Kuwait

187

mydotis undulata macquennii and the Imperial

eagle, Aquila heliaca). The Houbara bustard be-

cause of the size of its habitat requirement may be-

come the "umbrella" species in the wildlife

conservation program. In other words, the pre-

sence of Houbara bustard bird in any habitat re-

flects richness in biodiversity in that habitat

(Gregory, 2005). Accordingly, it is important that

wildlife conservation programs are oriented speci-

fically at particular species of most concern such

as Houbara bustard. Such programs should be im-

plemented based on regional, national and interna-

tional scope (Young, 1997; Mawdsley et al., 2009).

The weather during the field data collection

exercises (occurrences of rains and low tempera-

ture) might have impact on the animals’ availabi-

lity. Ectothermic (cold blooded) animals tend to

hibernate during cold weather (winter) and come

out only from hibernation when the temperature is

favorable (spring). This could be true because the

Sand gecko (, Stenodactylus s lev ini ) and the Rock

gecko ( Bunopus tuberculatus) were trapped only

during the PFT trapping exercises in March, when

the temperature in the oilfields had risen to above

20°C, whereas most of the beetles, ants and the

fringe-toed lizards, such as Acanthodactylus scu-

tellatus ; A. schmidtif, and Mesalina brevirostris

were trapped when the temperatures in the field

ranged from 3° to 8°C.

The large percentage of predators (51%) of ani-

mals recorded from the PFT indicated good supply

of prey or food resources i.e. consumers 47% and

scavengers 2%. The low numbers of captures in

the baited mammal trappings were expected be-

cause of the timing of the field exercises, winter.

Desert animals tend to hibernate during winter and

come out during spring and summer (examples are

hedgehog, gerbil, jerboa, etc.). More animal spe-

cies are expected to be recorded if the survey was

to cover the four seasons, especially the two di-

stinct migration periods of Kuwait.

Expanding the survey period and applying more

conservation strategies and programs is recommen-

ded in future work. No conservation program or

strategy is optimal, some strategies have to be

oriented to a specific target. Development of a set

of strategies or approaches that complement each

other is sometimes important to create useful con-

servation tools and to fulfill requirements needed

for an appropriate wildlife conservation approach.

ACKNOWLEDGEMENTS

The authors would like to thank Joint Opera-

tion management for facilitating the research as-

sessment in Al Wafra fenced area. Thanks are also

extended to KISR staff for their effort in executing

field work.

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Chichester M.O., 2000. Environmental Profile and En-

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Da Fonseca GAB., Sechrest W. & Ogelthorpe J., 2005.

Managing the matrix. In: Lovejoy T.E. & Hannah

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Haven, Connecticut, Yale University Press.

Delima E., Al-Mutairi M., Dashti J., Al-Dossery S.,

Loughland R., Gregory G., Khalil F., Pandi P, Oli-

varez E. & Siddiqui K, 2005. Boubyan Island En-

vironmental Assessment and Preparation of a

Master Plan: Wildlife Survey. Final Report. KISR

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FEPA (Federal Environmental Protection Agency),

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Fischlin A., Midgley G.F., Price J.T., Leemans R., Gopal

B., Turley C., Rounsevell M.D.A., Dube O.P, Tara-

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of the Intergovernmental Panel on Climate

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Fisher B. & Christopher T., 2007. Poverty and biodiver-

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the biodiversity hotspots. Ecological Economics, 62:

93-101.

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W.J. (ed.), Cambridge University Press.

Gregory G., 2005. The birds of the state of Kuwait.

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On the presence of the Caddisflie Stenopsyche siamensis Marty-

nov, 1 93 1 from Central Thailand (Trichoptera Stenopsychidae)

Nidsaraporn Petsut 1 *, Sitthi Kulabtong 2 & Patinya Sreesamran 3

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

nidsaraporn@ru.ac.th

2 Save wild life volunteer Thailand, Wangnoi District, Ayuttaya Province 13170, Thailand; e-mail: kulabtong2011@hotmail.com

3 53 Moo 3, Banyang Subdistrict, Muang District, Nakronpatom Province 73000, Thailand; e-mail: man_evo@hotmail.com

■"Corresponding author

ABSTRACT In the present paper, caddisflie larvae and pupae of Stenopsyche siamensis Martynov, 193 1

(Trichoptera Stenopsychidae) are recorded from upstream of Maewong Basin, Central

Thailand.

KEY WORDS Caddisflies; Stenopsyche siamensis ; Stenopsychidae; Trichoptera.

Received 08.07.2012; accepted 26.07.2012; printed 30.09.2012

INTRODUCTION

Caddisflies are aquatic insects of the order Tri-

choptera Kirby, 1813. This order of aquatic insects

is a very large one comprising more than 10,000 spe-

cies in the world (Sangpradub & BoonSoong, 2006).

In tropical Asia, Caddisflies include about 28 fa-

milies (Dudgeon, 1999) and, more particularly, 491

species were recorded in Thailand (Malicky &

Chantaramongkol, 1999). In natural freshwater eco-

systems Caddisflies are important and fundamental

components.

Caddisflies of the family Stenopsychidae Mar-

tynov, 1924 are different from other families of Tri-

choptera by the combination of the following

morphological and ecological characters: a) head

longer than 2 times as long as wide; b) mesopleuron

not extended anteriorly; c) dorsum of abdominal

segment 9 without sclerotized plate; d) larvae of the

family building nests between large stones (San-

gpradub & BoonSoong, 2006).

In Thailand, Stenopsychidae comprise one

genus, Stenopsyche McLachlan, 1868, and six spe-

cies (Malicky & Chantaramongkol, 1999) including

Stenopsyche siamensis Martynov, 1931; life cycle

and feeding habits of S. siamensis in Thailand were

studied by Laudee & Chantaramongkol (2003).

Stenopsyche siamensis Martynov, 1931

This species is widely distributed in Thailand

and Malaysia (Laudee & Chantaramongkol, 2003).

In a survey project of aquatic ecology at upstream

of Maewong Basin, Pangsira Thong District, Kam-

phaeng Phet Province, Central Thailand, carried out

in May 2012, we found many specimens of S. sia-

mensis at larvae and pupae stage.

This report is important for faunistic and eco-

logical aspects, considering that all the Trichop-

tera are good ecological indicators. Particularly,

larvae and pupae of S. siamensis (Laudee &

Chantaramongkol, 2003), were found in upstream

mountainous areas or islets of Maewong Basin,

where water is of high-quality, the stream is tran-

sparent and running fast, on average about less

than 1 m deep and the stream ground is made of

rough sand and large stones.

These larvae make protective cases by fibers

between large stones and/or under stones, stay in-

190

N. Petsut, S. Kulabtong & P. Sreesamran

Figures 1-4. Residence constructions under stones (Fig. 1), larva (Fig. 2) and pupa (Fig. 3, 4) of Stenopsyche siamensis

from Maewong Basin, Thailand.

side the construction and live in the stream since

they get to pupa stage when, the small sticky

fiber, reinforced by rough sand from the stream

ground, is wrapped around the body of the insect

(Figs. 1-4).

Present paper reports on an additional record

of the species from Central Thailand confirming

indirectly the good water quality of upstream of

Maewong Basin.

ACKNOWLEDGEMENTS

The authors are grateful to reviewers for revie-

wing this manuscript. A special thank to Mr. Tha-

napol Saranark and Mr. Wathunyu Kalumpuk, for

supporting the field survey.

REFERENCES

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benthos, Ecology and Conservation. Hong Kong Uni-

versity Press. Hong Kong.

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274 pp.

Biodiversity Journal, 2012, 3 (3): 191-200

A contribution to the knowledge of the terrestrial Mammalian

fauna of Comino and its satellite islets (Maltese Archipelago)

Arnold Sciberras 1 *, Jeffrey Sciberras 2 , Michael Sammut 3 & Gaetano Aloise 4

'33 ‘Arnest’, Arcade Str, Paola, Malta; email: bioislets@gmail.com

2 24 ‘Camilleri Court’ flat 5, il-Marlozz Str, Mellieha (Ghadira), Malta; email: wildalienplanet@gmail.com

3 11, Sqaq Rigu, Birkirkara, Malta; email: aquilarus@gmail.com

4 Museo di Storia Naturale della Calabria e Orto Botanico, University of Calabria, Via P. Bucci, s.n., 87036 Rende, Italy; email:

aloise@unical.it

’Corresponding author

ABSTRACT The present work aims to contribute to existing knowledge on Mammalia species occurring

on Comino and its satellite islets and to provide additional records collected between the

years 1 998-20 1 2. At the present state of knowledge, on the islands of the Maltese Archipelago

there are 19 different species of terrestrial mammals (Erinaceomorpha: AteJerix olgirus. So-

ricomorpha: Suncus etruscus, Crocidura sicula. Chiroptera: Rhinolophus ferrum-equinum, R.

hipposideros, Miniopterus schreibersii, Myotis purlieus, Eptesicus serotinus, Nyctalus noctula,

PipistreUus pygmaeus , P. kulii, Plecotus austriacus, Tadarida teniotis. Lagomorpha: Oricto-

Jagus cuniculus. Rodentia: Apodemus sylvaticus, Rattus rattus, R. norvegicus, Mus musculus.

Carnivora: Mustela nivalis), more than half of which are bats. Out of 1 3 species listed here,

8 species are represented as new to the islands while 3 species are confirmed and 2 species

are listed as unlikely occurring.

KEY WORDS Mammalia; Comino; Satellite islets; Maltese Islands.

Received 08.07.2012; accepted 18.08.2012; printed 30.09.2012

INTRODUCTION

Very little work is directed to Maltese Mam-

malia, and even less is known about their distri-

bution, especially with respect to the smaller

islands. Some scattered notes provide some lite-

rature of past records.

The first data on the mammalian fauna of the

Maltese Archipelago were reported by Gulia

(1890). Busuttil & Borg (1925) were the first to

attempt to list the mammalian fauna present on

Comino Island.

Unfortunately their list only constitutes of Mal-

tese vernacular names and this often causes diffi-

culty in determining the precise species as local

names change through time and may refer to a num-

ber of closely related species.

Lanfranco (1969) repeats these records in his

work; Savona- Ventura (1982) focuses on giving

new data on the mammals living on Comino and

Cominotto. Baldacchino & Schembri (2002) along

with the life history of mammalia and herpeto fauna

of the Maltese Islands, give also some localities

where the latter species were recorded.

Recently Aloise et al. (2011) represented the

possibility that Crocidura sicula (Miller, 1900) is

present also on Comino. This latter record is con-

firmed in the present work.

What follows is the current mammalian fauna

known to occur or have occurred on the latter is-

lands. In addition to bibliographic data available,

data were collected through direct observations, by

collection of dead specimens and through discus-

sion with local people.

192

A. SCIBERRAS, J. SCIBERRAS, M. SAMMUT & G.ALOISE

All non-flying mammals of the Maltese Archi-

pelago, however, are thought to have been introdu-

ced, at different times, by Men.

MATERIALS AND METHODS

Study area

The Maltese Archipelago consists of three main

islands, which are Malta, Gozo (Ghawdex) and Co-

mino (Kemuna) and a number of minor islands,

islets and rocks. Comino, the third largest island of

the Archipelago, is surrounded by following satel-

lite islands: Cominotto, Old Battery's Rock, Lan-

tern Point Rock, Comino Cliff Face Rock/ Pigeon

Rock, Small Blue Lagoon Rock, Large Blue La-

goon Rock, Ghemieri Rocks (Fig. 1; Table 1).

Comino (Kemuna)

Comino is the third largest island of the Maltese

Islands, with an area of 2.7 km 2 . Comino is also

considered to be the smallest of the three main is-

lands, but it can be referred as the mainland with

respect to its satellite islets. However, due to its

mono-geological component of Upper Coralline

Limestone above sea-level, it has much less habi-

tats than Gozo and Malta. Moreover with its small

size, the range in topography is also limited, with

a genaral tilt from South to North, identical incli-

nation to the one of Marfa Ridge.

Cliffs are only dominant on the eastern and sou-

thwestern perimeters of the island, while only two

considerably long valleys exist there. Sand-dunes

are minimal and localised. With respect to vegeta-

tion communites. Thyme garigue and Anthyllis-

Teucrium and Euphorbia melitensis phryganas are

most common, with dense Hypericum aegyptium

garigues along the coast, followed by Pistacia len-

tiscus pseudomaquis further inland and few Pinus

halepensis woodland patches.

Other phryganas are rare on Comino, but a con-

siderable large population of Senecio bicolor exists

on Comino, in some areas it is dense enough to

contribute to its own phrygana. Elsewhere in Mal-

tese Islands, this species seems common in Malta

and Gozo, and rare on the islets, but always scatte-

Name of the

lslet/rock

Code

(fig-1 )

Rank by

area

Height

(m)

Width (m)

W-E

orientation

Length

(m) N-S

orientation

Distance from

the mainland

(m)

Topogra-

phical in-

clination

Surface

Geology

Soils

Cominotto

>20

500

-200

125

South to

North

Upper Co-

ralline

Terra

Rossa

Large Blue La-

goon Rock

170

South to

North

Upper Co-

ralline

Terra

Rossa

Small Blue La-

goon Rock

110

West to

East

Upper Co-

ralline

Terra

Rossa

Pigeon Rock

East to

West

Upper Co-

ralline

Inglin

complex

Battery Rock

6-7

East to

West

Upper Co-

ralline

Terra

Rossa

Lantern Rock

Upper Co-

ralline

Ghemieri

Rocks

(3 rocks)

6,1,2

14,14,10

19, 20,38

10,82, 30

Upper Co-

ralline

Table 1. Characteristics of the Satellite islets of Comino (Maltese Archipelago).

A contribution to the knowledge of the terrestrial Mammalian fauna of Comino and its satellite islets (Maltese Archipelago) 1 93

Comino

Figure 1. Satellite islets of Comino (Maltese Archipelago): Old Battery's Rock (J), Lantern Point Rock (K), Comino Cliff

Face Rock/ Pigeon Rock (L), Small Blue Lagoon Rock (M), Large Blue Lagoon Rock (N), Ghemieri Rocks (X), Comi-

notto (O).

red (not in dense clumps). Sub endemic rare plants

have been noticed occuring sporadically on the is-

land, such as the Pelagian-Maltese endemics Lina-

ria pseudolaxiflora Lojacono and Daucus

lopadusanus Tineo, while the other is Senecio pyg-

maeus D.C, a Sicilian-Maltese endemic.

Cominotto (Kemunett)

By far, Cominotto is the largest islet near Co-

mino, with 9.9 ha; it is the second largest uninhabi-

ted island of Malta. The island has an S -shaped

topographical orientation.

Cominotto also has a similar altitude of the other

nearby islets on the south east of the island. Cliffs

dominate the south coast, while a peninsula, larger

than Small Blue Lagoon Rock, is connected on the

south east of Cominotto.

Cominotto has three slopes, east to west from

its highest point to its sandy beach and nearby

coast, south to north and west to east from the hi-

ghest point too.

Thymbra cap data. Convolvulus oleifolius ,

Teucr turn fruticans , Br achy podium retusum and

Anthyllis hermanniae are dominant species on the

eastern side of the island, especially facing Co-

mino. Euphorbia melitensis , and Pistacia lenti-

scus are dominant on the highest point of the

island. Darniella melitensis is dominant on the

south cliffs.

Euphorbia melitensis is also dominant on the

northwest of the island. In winter, several annual

species dominate the island, such as Convolvulus

althaeoides , Anthyllis vulneraria, Linum strictum ,

Linum trigynum, and Galactites tomentosa in the

disturbed patches of the island. Phagnalon graecum

194

A. SCIBERRAS, J. SCIBERAS, M. SAMMUT & G.ALOISE

subsp. ginzbergeri is only present in the peninsula

of the island (Sciberras & Sciberras, 2010).

Large Blue Lagoon Rock (Il-Hagra Ta’

Bejn il-Kmiemen il-Kbira)

Large Blue Lagoon Rock is the second largest

islet of Comino. The islet has one slope, which is

slightly steeper than that of Small Blue Lagoon

Rock. The south perimeter is dominated by cliffs,

except for a sizeable sea cave on its eastern side,

which goes right through the islet. Its topographic

landscape shows that it used to form part of the col-

lapsed western valley of Comino.

The upper half is inhabited by vegetation. Hy-

pericium aegypticum is the dominant species all

over the islet, while Daucus carota is dominant on

the west side of the islet. Some patches are domi-

nated by Convolvulus oleifolius (Sciberras & Sci-

berras, 2010).

Small Blue Lagoon Rock (Il-Hagra Ta’Bejn

il-Kmiemen iz-Zghira)

Situated between Large Blue Lagoon and Co-

minotto, the Small Blue Lagoon Rock is the third

largest islet of Comino. Most vegetation also oc-

curs on its upper half. Arthrocnemum macro sta-

chyum and Daucus carota are the dominant species

all over the islet.

Lygeum spartum entirely covers a small patch

of soil. Lavatera arborea ( Malva dendromorpha ),

with only four specimens, barely survives near the

Lygeum spartum and is only present on this islet in

Comino' s Archipelago (Sciberras & Sciberras,

2010).

Comino Cliff Face Rock/Pigeon Rock/Ta’

Taht sl-Mazz Rock(ll-Gebla ta’ Taht il-Mazz)

Ta’ Taht il-Mazz rock is the fourth largest islet

near Comino. The islet is very steep, with vertical

sheer cliffs on its east side facing the western cliffs

of Comino, while its western is slightly less steep,

but still sheer.

The majority of species of plants occur on its

west side and upper half of it, while only one spe-

cies inhabits its east side. Inula crithmoides is a do-

minant species on the eastern face of the islet,

while Darniella melitensis is dominant on the we-

stern cliff face of the islet. Daucus carota and Li-

monium melitensis are also dominant, but on a les-

ser extent. Anthyllis hermanniae and Pistacia

lentiscus are rare on the islet.

No soil exists on the rock, vegetation is gro-

wing on the debris (the accumulating debris) and

in rough weather the lower area is inundated by

wave action (Sciberras & Sciberras, 2010).

Old Battery’s Rock (Gebla ta' taht il -Bat-

terija)

This small rock is situated on the southeast of

Comino under the old battery it is the second smal-

lest rock of Comino. Remnant soil exists on the

islet which is inundated by water wave action du-

ring rough weather. Till 2010 the flora of the islet

consisted of 22 individuals of Inula crithmoides

(Sciberras & Sciberras, 2010).

Lantern Point Rock (Gebla Tal-Ponta

Rqiqa)

Lantern Rock it is slightly smaller than Old Bat-

tery’s Rock, it supports very little vegetation, only

two species, Limonium melitense and Inula cri-

thmoides. It is a large boulder of no more than 7 m

high, with another small boulder lying on top of it

(Sciberras & Sciberras, 2010).

RESULTS

Erinaceomorpha Gregory, 1910

Erinaceidae G. Fischer, 1814

Atelerix algirus (Lereboullet, 1842)

Algerian Hedgehog

Taxonomy of Hedgehog of Maltese Islands was

uncertain for a long time. The Hedgehog was first

recorded for the Malese Islands by Gulia (1858),

which, however, erroneously considers this popu-

lation belonging to Erinaceus europaeus. After the

taxonomic revision of the Maltese specimens (Lan-

franco, 1969), currently all the populations occur-

ring in the Maltese Archipelago belong to the

species Atelerix algirus.

Busuttil & Borg (1925) mention that a species

of hedgehog was imported to Comino from the nei-

A contribution to the knowledge of the terrestrial Mammalian fauna of Comino and its satellite islets (Maltese Archipelago) 1 95

ghbouring islands of Malta or Gozo probably by

the ornithologist A. Schembri, in the 19th Century,

to control infestations of Blattaria sp. Lanfranco

(1969) and Savona- Ventura (1982) seem not to re-

spond to the presence of this species to the island

while Baldacchino & Schembri (2002) state that

this species is not present.

Two of the authors (A. Sciberras and J. Sci-

berras) have recorded this species 8 times over a

time span of 14 years and in one occasion

(23. XI. 2005) a nest was found containing 5

young. Specimens were encountered mostly in

the centre of Comino Island, particularly in a lo-

cation known as Ta' Caruana. Several naturalists

informed the authors however that during the

1990's several specimens saved from Maltese

roads, especially from Mgarr to Mizieb area,

were released on the island for safety reasons.

Both white and dark forms were encountered

on the island. The status of the population present

in Comino is unknown. The Algerian Hedgehog is

present in Comino, Malta and Gozo, but is absent

from all the other smaller islands.

Soricomorpha Gregory, 1910

Soricidae G. Fischer, 1814

Crocidura sicula (Miller, 1900)

Sicilian shrew

In the Maltese Archipelago is confirmed the

presence of two species of Soricidae: Suncus etru-

scus (Savi, 1822) and Crocidura sicula. On the

basis of current knowledge S. etruscus occurs only

in Malta, and C. sicula , classified as C. suaveolens,

is recorded only from the island of Gozo (Schem-

bri & Schembri, 1979). Only recently has advan-

ced the possibility that this species is present on

Comino (Aloise et al., 2011).

Two specimens were obtained from the analy-

sis of Asio otus (Linnaeus, 1758) pellets found

from beneath the nest of the latter. Although most

likely the latter specimens were caught from Co-

mino, there is also the possibility that the speci-

mens were caught from Gozo by the predator and

then expelled on the nesting site. Similar pellets

were collected by A. Sciberras containing Rattus

sp. remains and were retrieved where Asio flam-

meus (Pontoppidan, 1763) was occasionally si-

ghted; presumably these remains belong to the lat-

ter species. On 18. III. 2012 a dead specimen of

Crocidura sicula was found drowned in a bucket

presumably full of rain water close to the Northern

Coast, confirming the presence of a population of

this species on the island.

On 19.X.2011 a lower jaw bone of Crocidura

sp. was found on Cominotto (A. Sciberras, J. Sci-

berras and L. Pisani, unpublished data) but the pre-

sence of a population of Crocidura Wagler, 1832

on this islet is not confirmed. The Sicilian shrew

is absent from all the other smaller islands.

Chiroptera Blumenbach, 1774

Rhinolophidae Gray, 1825

Rhinolophus hipposideros minimus (Heu-

glin, 1861) Lesser Horseshoe Bat

This species was already more commonly

known in Gozo and less in Malta, which is repor-

ted by the early work on the Maltese Islands (see

Borg et al., 1997 and references therein).

On 12. III. 2004 a dead specimen was found in

a location known as Il-Hazina on Comino Island

by one of the authors (A. Sciberras). This species

t is a new record for this island.

Vespertilionidae Gray, 1821

My otis punicus Felten, Spitzenberger &

Storch, 1977 Mediterranean Mouse-eared Bat

Taxonomy and distribution of the Mouse-eared

bat of the Maltese Islands have been debated for

a long time, because of its morphometric peculia-

rities. In the past reported as M. oxignatus (Lanza,

1959; Van den Brink, 1967; Lanfranco, 1969),

was then reported to M. blyti punicus and studied

in detail (Felten et al., 1977; Savona- Ventura,

1984a, 1984b; Borg, 1998; Borg & Cachia-Zam-

mit, 1988, 1994; Borg et al., 1990; 1997; Borg,

1998). M. punicus actually up to now is found on

Malta and Gozo.

On 12.III.2004 and 22.XI.2005 a specimen of

this species was found in a subterranean area close

to the Comino tower. This is the first record for the

island. On the Maltese Archipelago, this species

was formerly common but has suffered immense

196

A. SCIBERRAS, J. SCIBERRAS, M. SAMMUT & G.ALOISE

decrease in the 1980's and according to Baldac-

chino & Schembri (2002) the current population

consists of only around 250-300 specimens.

Pipistrellus kuhli (Kuhl, 1817)

Kuhl’s Pipistrelle

This species was presumed rare in the Maltese

Archipelago before 1969 (Gulia, 1890; Lanfranco,

1969) but according to a 1990 study (Borg et al.,

1990, 1997) the latter was found to be more fre-

quent and it had a distribution all over the three

main islands: Malta, Gozo and Comino.

Pipistrellus pygmaeus (Schreber, 1774)

Soprano Pipistrelle

Busuttil & Borg (1925) record the presence of

two species of bats, noting that one preferred roo-

sting in cracks while the other in caves. Lanfranco

(1969) repeats this record. Savona- Ventura (1982)

observed several specimens in flight and entering

crevices at Santa Marija bay on VIII. 1977. None

were captured, and so the records are only from di-

rect observations. It was suggested to be similar to

Pipistrellus pipistrellus (Schreber, 1774). Nowa-

days it is being considered that Pipistrellus pyg-

maeus (Leach, 1825) is the likely species to exist

in the Maltese Archipelago (Baldacchino &

Schembri, 2002).

Several specimens were noted in flight by the

three of the authors ( A. and J. Sciberras, M. Sam-

mut) and from field observations they look to be a

Pipistrellus sp., but none were ever recovered for

taxonomic identification. Several specimens were

also observed flying over Cominotto and landing

in crevices of Comino Cliff Face Rock.

Plecotus austriacus (Fischer, 1829)

Grey Long-eared Bat

Present on Malta, Gozo and Comino, the spe-

cies was reported already by Gulia (1890, 1914),

Lanza (1959) and Van den Brink (1967) as P. au-

ritus (Linnaeus, 1758). Baldacchino & Schembri

(2002) state that this species had a distribution all

over the three main islands. Although the authors

never observed this species on Comino a dead spe-

cimen was found on Cominotto Beach by one of

the authors (A. Sciberras) on 6.VII.2001. This is

the first record for Cominotto island.

Tadarida teniotis (Rafinesque, 1814)

European free-tailed bat

A skull of this species was retrieved from

Larus sp. pellet from Large Blue Lagoon Rock

(13.6.2011 A. and J. Sciberras leg.). Although the

shape and size of the island suggest that, probably,

the animal was preyed on a different site than

where the remains were found, this is an intere-

sting record because besides being new to the

islet, this species is extremely rare and was repor-

ted from the Maltese Islands twice before the di-

scovery of this skull.

The first time was in 1993 in a locality known

as Cittadella on the island of Gozo where 2 speci-

mens were observed hunting insects under street

lights. The same specimens were noted till mid -

May in the same locality. Another specimen was

recorded flying close to the cliffs of Had - Dingli

in Malta in November of 1996 (Baldacchino &

Schembri, 2002). To add to the interest on the

same islet where the skull was located, on

8. VIII. 20 10 the same authors observed gulls,

identified as Larus michahellis (Naumann, 1884)

by M. Sammut, hunting bat specimens that approa-

ched the vicinity of a colony of 7 gulls that were

resting on the islet.

This was just before sunset. It could be that this

species does occasionally predate on bats as it was

noted to predate on other terrestrial species such

as Podarcis filfolensis (Bedriaga, 1876). It could

also be that the bat was caught away from this site

even offshore and it was regurgitated locally.

Carnivora Bowdich, 1821

Mustelidae Fischer, 1817

Mustela nivalis (Linnaeus, 1766) Weasel

Baldacchino & Schembri (2002) state that this

species locally is restricted in the Maltese Islands

to the island of Malta. It is very scarce on the main

island but it is widespread and observations of

this species range from the North to the South of

the main island of Malta.

A contribution to the knowledge of the terrestrial Mammalian fauna of Comino and its satellite islets (Maltese Archipelago) 1 97

Whilst most observations of this species are of

single individuals, a den with cubs was observed

in Balluta area (Wardija Limits) (A. Sciberras,

5.IV.2002, unpublished data) and an adult with

five cubs was observed at Mtahleb (M. Sammut

& C. Cachia Zammit, 13. XI. 2010, unpublished

data), although illegal, most of the specimens

(from Qammieh and Ahrax headlands in

Mellieha) have been killed for taxidermal purpo-

ses. On 23.IV.2012, one of the authors (M. Sam-

mut) saw an adult specimen of this species at a

location known as Il-Hazina (Comino island) mo-

ving swiftly from behind a rubble patch.

Following that it climbed from behind a rub-

ble wall and popped up on the rubble wall where

it was seen very well and could be identified wi-

thout any doubt. It disappeared again as swiftly as

it had appeared. It was seen in the afternoon and

though the author remained in the area for over an

hour it was not seen again.

An indication of the presence of species on

the island is the finding of 3 dead specimens of

Rattus norvegicus and a young specimen of Oryc-

tolagus cuniculus near Comino' s pig farm

(6.V.2004, A. Sciberras, unpublished data). These

carcasses showed signs that they had been killed

and dragged from the neck, and less than 50 cm

away a den similar to the one observed at Balluta

was discovered.

No cubs or adults were observed despite the

constant monitoring. Interestingly, people who

have lived all their lives and constantly patrol the

island of Comino have never seen the species on

the island (S. Vella, pers. comm.). It is also worth

noting that Mustela putorius furo (Linnaeus, 1758)

was once observed on Comino in the 1970's (M.

Psaila, pers. comm.).

In the past feral specimens have escaped from

rabbit hunters which visited the island (S. Vella,

pers. comm.). One of the authors (A. Sciberras)

also has reports on Mustela sp. being present in

Gozo but after checking the site (an area known

as Munxar) 3 feral specimens of M. putorius furo

were noted roaming free. One of the authors (J.

Sciberras) received reports by locals of Mustela

sp. at San Bias Bay.

After observing the site and description of the

locals it was confirmed that a few specimens of M.

putorius furo were present at the site. Lanfranco

(1969) also records the latter feral species in Malta

and it is suggested that these must be escapees

from O. cuniculus hunting parties.

Rodentia Bowdich, 1821

Muridae Illiger, 1815

Rattus norvegicus (Berkenhout, 1769)

Brown rat

The Brown Rat is considered common, but can

be very common and, under certain conditions, can

become particularly problematic.

Its presence has been detected on all the major

islands, Cominotto and many other smaller islands.

The presence of rats on the Comino and Cominotto

Islands is referred by Busuttil & Borg (1925),

while Lanfranco (1969) mentions this species and

Rattus rattus , Savona- Ventura (1982) observed a

specimen of the species on Cominotto in IX. 1975.

Baldacchino & Schembri (2002) also record the

presence of the species on Comino.

Presently including the period of observations

stipulated above, this species is numerous on the

islands and was recorded on the following islets

(A. Sciberras, unpublished data): Manoel Island,

Qawra Point or Ta’ Fra Ben islet, Selmunett Is-

land, Large Blue Lagoon Rock, Haifa Rock, and

Tac-Cawl Rock. On Fungus rock and Selmunett

Island, it is known of its devastating impact on the

Insular biodiversity (Baldacchino & Schembri,

2002; Sciberras, 2007; Sciberras & Schembri,

2008).

Rattus rattus (Linnaeus, 1758) Black Rat

The Black Rat is reported as present and

common on Malta, Gozo, Comino and some of

the satellite islets. Busuttil & Borg (1925) record

the presence of rats on the Comino and Comi-

notto Island while Lanfranco (1969); Savona-

Ventura (1982) states in III. 1978 he found a dead

specimen of this species.

Baldacchino & Schembri (2002) and Aloise et

al. (2011) also record the presence of this species

on Comino including Malta and Gozo and state

that it is common. The species is also known for

Fungus rock (Borg & Sultana, 2003).

From experience with data also collected from

a local Pest control company, this species is nu-

merous where it is present but it does have a re-

198

A. SCIBERRAS, J. SCIBERRAS, M. SAMMUT & G.ALOISE

stricted distribution. Most records of specimens

come from Valletta and neighbouring harbour ci-

ties. In all the years of observations and data col-

lection, this species was never encountered on

Comino or its satellite islets.

Mus musculus (Linnaeus, 1758)

House mouse

Widespread and very common, the House

Mouse is abundand throughout. Present on all

major islands, although not proven, its presence

can be regarded as likely also on the islands of

smaller size, because of its unique ecological

characteristics.

Busuttil & Borg (1925) reported the presence

of a mouse on Comino and so did Savona- Ven-

tura (1982) when he noted a specimen at Santa

Marija Bay in 1977. Since it was not caught, it

could not be certain whether it was this species

or Apodemus syfvaticus (Linnaeus, 1758). Seve-

ral specimens were caught annually on the north

Coast of Comino as a part of pest control treat-

ment. From 34 studied samples all specimens re-

sulted in being M. musculus.

Lagomorpha Brandt, 1855

Leporidae Fischer, 1817

Oryctolagus cuniculus (Linnaeus, 1758)

Wild Rabbit

Busuttil & Borg (1925) reported the presence

of a rabbit on Comino and this was repeated by

Lanfranco (1969). This species was very common

at their time and it is presumed that this species

was introduced around 1890' s on the latter Island.

Prisoners and soldiers during 1914-1918 did short

work on the rabbit population on Comino.

In 1969 Comino was declared a protected area

from hunters and the rabbit population must have

benefited, however Savona- Ventura (1982) assu-

med the survival of the animal through its scattered

dropping and not so much on the sightings. He also

recorded the species on Cominotto by finding

droppings of the latter in IX. 1975. In the 1980's,

Myxomatosis was introduced and the Maltese po-

pulation was virtually wiped out as happened with

the Comino population.

A local resident introduced this species from

Gozo again in several occasions as he did with

other species (Sciberras, 2009). Today the Comino

population is the largest in density when compared

to the size with other Maltese Islands.

The populations recorded in past literature on

Cominotto and Selmunett are extinct (Sciberras

unpublished data). It is interesting to note that in

the Maltese Archipelago, two colour morphs

occur: the brown form and the yellow form. The

Maltese population consists of almost entirely the

brown form with occasional yellow and hybrids

with domestic rabbits. Domestic rabbits are gene-

rally set free because of some kind of illness such

as VHD (Viral Hemorrhagic Disease), Myxoma-

tosis and the most commonly found Ear Cancer. If

these survive they sometimes interbreed with the

wild stock (Sciberras, 2006).

The Gozo population has both forms in equal

numbers, whilst the Comino population constitutes

entirely of the yellow form and only on very rare

occasions, slightly darker specimens are noted.

CONCLUSIONS

At the present state of knowledge, on the is-

lands of the Maltese Archipelago are 19 different

species of terrestrial mammals (Erinaceomorpha:

Atelerix algirus ; Soricomorpha: Suncus etruscus ,

Crocidura sicula ; Rhinolophus ferrum-equinum ,

R. hipposideros , Miniopterus schreibersii, Myo-

tis purlieus , Eptesicus serotinus , Nyctalus noc-

tula , Pipistrellus pygmaeus , P. kulii , Plecotus

austriacus , Tadarida teniotis', Lagomorpha:

Orictolagus cuniculus ; Rodentia: Apodemus syl-

vaticus , Rat t us rattus, R. norvegicus , Mus mu-

sculus ; Carnivora: Mustela nivalis ), more than

half of which are bats.

As regards the island of Comino and its satel-

lite islands, most of these species are present

(68,4%), not being up to now verified the presence

of S. etruscus and A. sylvaticus , among the non-

flying, and R. ferrum-equinum, M. schreibersii , E.

serotinus and N. noctula among the bats.

With the species listed above, Busuttil & Borg

(1925) reported that a certain Captain Stivala re-

leased on the island of Comino a pair of Gazella

sp. These bred successfully but were eradicated by

prisoners during the First World War.

A contribution to the knowledge of the terrestrial Mammalian fauna of Comino and its satellite islets (Maltese Archipelago) 1 99

A population of Felis silvestris catus (Schreber,

1777) introduced in the 1980' s was exceeding over

20 specimens around Comino hotel (Northern

Coast) in the late 1990's and it was eradicated by

environmentalists for the protection of the native

wildlife of Comino. This update on the mammalian

fauna was a result of observations, made indirectly

while the authors were conducting other studies or

surveys mostly entomological, herpetological or or-

nithological.

Upon further investigation, especially on spe-

cies most critical (eg. Crocidura sicida and Chi-

roptera), would be necessary to verily the status of

the population, to guarantee their conservation in

the Archipelago.

ACKNOWLEDGEMENTS

A. and J. Sciberras are in debt to Esther Sciber-

ras, Romario Sciberras and Luca Pisani for their

constant assistance in the field. Special thanks go

to Professor Patrick J. Schembri, Alfred. E. Baldac-

chino and Pietro Lo Cascio for providing useful

contacts and some literature. Thanks also go to

Mario Gauci for his hospitality during Gozo visits.

Mark Psaila and Salvu Vella are acknowledged for

sharing their observations.

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Biodiversity Journal, 2012, 3 (3): 201-228

New and little known land snails from Sicily (Mollusca

Gastropoda)

Fabio Liberto 1 , Salvatore Giglio 2 , Maria Stella Colomba 3 * & Ignazio Sparacio 4

'Strada Provinciale Cefalu-Gibilmanna n. 93, 90015 Cefalu, Italy; email: fabioliberto@alice.it

2 Contrada Settefrati, 90015 Cefalu, Italy; email: hallucigenia@tiscali.it

TJniversita di Urbino, Dept, of Biomolecular Sciences, via Maggetti n. 22, 61029 Urbino, Italy; email: mariastella.colomba@uniurb.it

4 Via E. Notarbartolo n.54 int. 13, 90145 Palermo, Italy; e-mail: isparacio@inwind.it

’Corresponding author

ABSTRACT In the present paper are reported new and little known land snails from Sicily (Mollusca

Gastropoda). Particularly, Platyla similis (Reinhardt, 1880) (Aciculidae) and Rumina sa-

harica Pallary, 1901 (Subulinidae) are first recorded in the island; new taxonomic data,

useful for a better systematic classification, are provided on two little-known taxa, Lam-

pedusa lopadusae nodulosa Monterosato, 1892 (Clausiliidae) and Cernuella (Cernuella)

tineana (Benoit, 1862) (Hygromiidae); and finally, a new species of slug, Tandonia mari-

nellii n. sp. (Milacidae), currently known from North-Western Sicily, is described.

KEY WORDS Mollusca; land snails; Sicily; taxonomy; new species.

Received 10.07.2012; accepted 26.08.2012; printed 30.09.2012

INTRODUCTION

During 19 th century several taxa of terrestrial

molluscs of Sicily were established, many of

which are still little known and of uncertain taxo-

nomic status, nevertheless some genera or families

of molluscs, including slugs, have been neglected

for a long time. The study of terrestrial molluscs

of Sicily undertaken by present authors in the last

decade, despite the complexity of the subject, con-

tinues with this further contribution in which some

new faunal reports are provided, little known taxa

are examined and, in addition, a new species of

slug is described.

ACRONYMS. APP = anterior portion of palatal

plica; BC = bursa copulatrix; BCD = diverticulum of

bursa copulatrix; CL = columellar lamella; DE = distal

epiphallus; DG = digitiform glands; DSC = dart sac

complex; DBC = duct of the bursa copulatrix;

DCP = distal caviti of the penis; DGS = dart gun;

DG = digitiform glands; DSC = dart sac complex;

DSO = dart sac opening; E = epiphallus; F = flagel-

lum; FO = free ovidutto; FR = frenula; G = penial pa-

pilla; GA = genital atrium; ISO = inner stylophore

opening; F = lunella; OSO = outer stylophore opening;

P = penis; PCP = proximal caviti of the penis;

PD = penial diverticulum; PE = proximal epiphallus;

PE = parietal lamella; PEE = parallel lamella;

PP = principal plica; PPP = posterior portion of (upper)

palatal plica; PR = penial retractor muscle; SCL = sub-

columellar lamella; SL = spiral lamella; SP = sutural

plica/plicae; V= vagina; VAG = vaginal accessory

gland; VC = vaginal chambre; VD = vas deferens;

VP = vaginal pleats.

The materials used for this study are deposited

in the following Museums and private collections:

M. Bodon collection, Italy, Genova (CB); D.P Cilia

collection, Santa Venera, Malta (CC); S. Giglio col-

lection, Cefalu, Italy (CG); Laboratory of Cytoge-

netics and Molecular Biology, University of Urbino,

Italy (LCMBU); F. Liberto collection, Cefalu, Italy

(CL); Museo Civico di Storia naturale di Comiso,

202

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

Italy (MCSNC); Museo Civico di Storia Naturale

di Genova “G. Doria”, Italy (MSNG); G. Nardi col-

lection, Nuvolera, Italy (CN), A. Reitano collection,

Tremestieri Etneo, Italy (CR); I. Sparacio collection,

Palermo, Italy (CS); The Steinhardt National Col-

lections of Natural History, Zoological department,

Tel- Aviv University, Israel (TAU).

MATERIALS AND METHODS

All specimens were collected by sight on the

soil and under the rocks or by sieving litter and soil.

Observations on ecology of these organisms and

their feeding behavior were made directly in the

field. Dry shells have been studied as regards size,

colour, morphology, sculpture, aperture, plicae and

lamellae, lunella and clausilium. Photographs were

taken with a digital camera. In order to study and

illustrate genital organs, the specimens were drow-

ned in water and fixed in 75% ethanol.

Reproductive apparatus was extracted by means

of scalpel, scissors and needles. Illustrations of ge-

nitalia were sketched using a camera lucida. Height

and maximum diameter of the shell along with

some parts of genitalia were measured (in millime-

ters) by a digital gauge. Voucher specimens were

stored in collections indicated below. Toponyms

(place-names) are reported following the Portale

Cartografico Nazionale (PCN, http://www.pcn.mi-

nambiente.it /PCN/), Map IGM 1:25000. Each lo-

cality and/or collection site is named in the original

language (italian). The material used for the mole-

cular analysis was collected on the field during Fe-

bruary 2012. All the specimens were studied and

observed at the steromicroscope (Leica MZ 7.5).

Genetic study described in the present study was

based on a comparative analysis of COI partial se-

quences which are frequently used as markers in the

investigation of evolutionary processes at the specific

level. Briefly, the study was conducted by DNA iso-

lation, PCR amplification, sequencing, alignment of

the sequences and phylogenetic reconstructions

using the Maximum Likelihood algorithm. For a de-

tailed description see below.

RESULTS

Class Gastropoda Cuvier, 1795

Ordo Architaenioglossa Haller 1890

Family Aciculidae J.E.Gray, 1850

Platyla similis (Reinhardt, 1880)

Examined material. Italy, Sicily, Cefalu, Rocca

di San Nicola, 37°59 , 07”N 14°02’42”E, 600 m,

01.VI.2008, 6 specimens (CG); Cefalu, Cozzo Carca-

rello, 37°59 , 29” N, 14°03’05”E; 320 m, 15.VI.2008,

8 specimens (CL); idem, 23.VIII.2009, 22 specimens

(CL); idem, 23.IV.2012, 12 specimens (CL).

Figures 1,2. Shell of Platyla similis from Cefalu, Cozzo Calcarello, h: 2.32 - D: 0.89. Figure 3. Geographic distribution

of Platyla similis (circles) and P. subdiaphana (squares) in Sicily (personal data).

New and little known land snails from Sicily (Mollusca Gastropoda)

203

Description. Morphologically, this Sicilian po-

pulation of P. similis has typical characters of the

species: shell conical (Figs. 1-2), slender, colorless,

height 2.16-2.58 mm, width 0.80-0.98 mm, with 4-

5 whorls slightly convex, last portion of last whorl

slightly ascending in relation to the penultimate,

aperture slightly oblique, sinulus little depth, exter-

nal peristomal rib consists of a weak thickening, not

clearly defined anteriorly and posteriorly.

Biology and Distribution. P. similis lives in

woodland litter, on the soil, in the cracks and at the

base of the calcareous rocks. P. similis has South-

Oriental European distribution including Bulgaria,

Croatia, Serbia, Greece, Romania, Kosovo, and

Central and Southern Italy (Boeters et al., 1989;

Bodon et al., 1995; Bodon & Cianfanelli, 2008;

Bank, 2012).

Remarks. We report the presence of P. similis

for the first time in Sicily, from Nothern Madonie

mountains, on the calcareous rocks named “Rocca

di San Nicola” and “Cozzo Calcarello”. Shells were

collected by sieving litter and soil, sampled in

cracks of the calcareous rock, at the base of rocky

walls or under boulders in the woods of oaks.

In Sicily it was known until now only the en-

demic species: P. subdiaphana (Bivona, 1839)

(Boeters et al., 1989; Bodon et al., 1995; Bodon

6 Cianfanelli, 2008; Bank 2012) (Fig. 3). Boeters

et al. (1989) distinguish all species of Platyla Mo-

quin-Tandon, 1856 into three groups on the basis

of the presence or absence and conformation of

the external peristomal rib (see also Bodon &

Cianfanelli, 2008).

P. similis is inserted into the second group cha-

racterized by an external peristomal rib not robust

and not clearly delimited posteriorly. P. subdia-

phana belongs to the third group characterized by

a robust external peristomal rib bounded by a

sharp line or by a large groove. P. subdiaphana ,

also, is distinguished from P. similis for bigger

size (height 3.5-4.45 mm).

Ordo Stylommatophora A. Schmidt, 1855

Family Milacidae Germain, 1930

Tandonia marinellii n. sp.

Examined material. Holotypus: Italy, Sicily,

Custonaci, Monte Sparagio, Pizzo Giacolamaro,

38°03 , 18”N 12°44’35”E, 665 m, 08.1.2012 (MSNG

56989). Paratypi: Italy, Sicily, Custonaci, Monte Co-

fano, 38°06’H”N 12°40 , 39”E, 255 m, 14.IV.1991,

2 specimens (CS); San Vito lo Capo, Macari, Pizzo

Castelluzzo, 38°07’28”N 12°44 , 41”E, 364 m,

11.2007, 3 specimens (CR); Erice, 38°02’24”N

12°35 , 34”E, 500 m, 03.X.2011, 1 specimen (CN);

Calatafimi, Cozzo Gessi, 37°54’44”N 12 o 50’41”E,

264 m, 20.XI.20 11, 3 specimens (CL); idem, 2 spe-

cimens (CG); Calatafimi, Monte Bernarco,

37°54’56”N 12°49’45”E, 370 m, 20.XI.2011, 6 spe-

cimens (CL); Castellammare del Golfo, Fraginesi,

38°0r06”N 12°50 , 08”E, 180 m, 4.XII.2011, 1 spe-

cimen (CS); Custonaci, Monte Sparagio, Pizzo Gia-

colamaro, 38°03’18”N 12°44’35”E, 665 m, 8.1.2012,

1 specimen (CL); idem, 1 specimen (TAU 76575);

idem, 1 specimen (MCSNC 4411); Custonaci,

Monte Sparagio, Pizzo Giacolamaro, 38°03’17”N

12°44 , 57”E, 716 m, 4. II. 20 12, 8 specimens (CL);

Trapani, contrada Chinea, near the Lago Rubino,

37°53’49”N 12°44 , 05”E, 260 m, 18.11.2012, 2 spe-

cimens (CS); Custonaci, Muciara, 38°03 , 27”N

12°43’64”E, 542 m, 4.III.2012, 11 specimens (CS);

idem, 2 specimens (MSNG 56990; MSNG 56991).

Description of Holotypus. Slug medium-

sized, length 55 mm after preservation (the speci-

men is contracted). Clypeus about 1/3 of body

length, superficially granulated, with horseshoe-

shaped groove, and a hollow near keel; evident Ca-

rina running from clypeus to posterior apex of

body. Body and mantle brownish-yellow with blac-

kish pigment forming irregular reticulation and

dots which disappear toward the sole, keel orange.

Foot sole tripartite, creamy-coloured, mucus thick,

viscous, white-yellowish. Shell (limacella) nail-

like, oval, well calcified, white, with apex posterior

and situated on major axis, at the highest point,

convex above, slightly concave ventrally (Figs. 18-

20); length: 7.5 mm; diameter: 4.9 mm.

Genitalia (Figs. 4-7, 11). Vas deferens thin, en-

ding laterally at proximal epiphallus tip. Epiphallus

very long (20 mm), divided by a slight constriction

in a narrow cylindrical proximal portion with thin

walls (proximal epiphallus) and in an ample conic

distal portion with thick walls (distal epiphallus).

Internally, the proximal epiphallus is crossed by

around 15 anular crests more evident in the central

zone, and 5-6 longitudinal folds in the slight broa-

dening apical knob, while the distal epiphallus has

a very narrow duct; penial retractor muscle ending

204

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

Figures 4-7. Genitalia of T. marinellii n. sp., holotypus: whole genitalia (Fig. 4), internal structure of vagina (Fig. 5), in-

ternal structure of penis (Fig. 6), internal structure of penis and epiphallus (Fig. 7).

New and little known land snails from Sicily (Mollusca Gastropoda)

205

Figure 8. Spermatophore of the holotypus of T. marinellii n. sp. Figure 9. Anterior portion of spermatophore of T. ma-

rinellii from Calatafimi. Figure 10. Spermatophore of T. sowerbyi from Novara di Sicilia, Rocca Novara, Sicily. Figures

11, 12. Scheme of genitalia of T. marinellii n.sp., (Fig. 11) and of T. sowerbyi by Wiktor (1987), modified (Fig. 12).

206

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

laterally on penial complex where slight constric-

tion separates distal epiphallus from proximal epi-

phallus. Border between epiphallus and penis

externally evident, inside the epiphallus protrudes

into the penis with a semispheric extension, bearing

at its apex a small cylindrical papilla. Penis irregu-

lar, cylindrical, 1 1 mm long, approximately X A of

length of epiphallus, with thin walls, inside with

some striations and divided by a constriction in two

cavities: a narrower, oblong proximal cavity (8 mm)

and a short, wide distal cavity (2.2 mm). A thin she-

ath envelopes the penial complex, keeping proximal

epiphallus bent on the distal epiphallus and the

penis contracted; wide and short genital atrium,

with fine folds around the genital opening.

Vagina long (9.8 mm), inside there are some di-

scontinuous longitudinal folds. Vaginal accessory

gland enters by means of thin canaliculi at about

midway along vagina. An annular pad separates the

real vagina from a small chamber (vaginal cham-

ber) with thick, smooth wall, where the duct of

bursa copulatrix and the free oviduct end. Duct of

bursa copulatrix short and slender. Bursa copulatrix

elongate with a narrow apical prolungation. Long

and slender free oviduct, slightly wider near vagina.

Spermatophore (Fig. 8) worm-like, glossy, gol-

den. Anterior apex lacking (broken), the remaining

anterior portion is regularly tubular and bare, only

on the distal part there are some short spines (with

4-5 apexes), the posterior portion is covered with

some short spines with bifurcate point (two apexes)

or simple (one apex); posterior apex of the sperma-

tophora, bigger, completely covered of bifurcate or

simple spines. The spermatofore was found in the

channel of the bursa copulatrix with the posterior

apex contained into "vaginal chamber".

Variability. Body colour variable (Figs. 13-16)

from uniform orange with some spots hardly visible

to orange-brown speckled with darker patches; keel

clear, orange or cream; clypeus with blackish hor-

seshoe-shaped groove and sometimes with a dark

central line; genitalia: proximal epiphallus and di-

stal epiphallus generally have the same length, but

in some specimens the proximal portion is slightly

shorter; the epiphallus protrudes into the penis with

a semispheric or conic extension, penis length va-

rying from 6 mm to 10 mm; vagina length varies

from 2 mm to 9 mm. Spermatophore variable in

size (Fig. 9) and color from red to yellow-gold;

these were found in the channel of bursa copulatrix

with the big apex contained into "vaginal chamber".

Etimology. The new species is dedicated to

Aldo Marinelli (Roma), as sign of appreciation for

creating the forum “Natura Mediterraneo” (availa-

ble at: http://www.naturamediterraneo.com/forum/).

Biology and Distribution. Species rather

common in natural environments with forests, me-

diterranean maquis or garrigue, nocturnal, during

the day specimens shelter under rocks and logs;

sexual maturity occurs in winter. T. marinellii n.

sp., at present, is known only from North-Western

Sicily (Fig. 21).

Comparative notes. T. sowerbyi (Ferussac,

1823) was the only known species in Sicily (Wa-

gner, 1931, Giusti, 1973; Manganelli et al., 1995;

Bank 2012) (Fig. 21). In this region it seems to be

native as widely widespread, especially in natural

environments, and having been reported since 1800

(Lessona & Pollonera, 1882 sub Amalia carinata

and A. carinata var. oretea\ Mina Palumbo, 1883

sub Amalia carinata ; Pollonera, 1891 sub Amalia

carinata). The populations of eastern Sicily exami-

ned by us show the typical morphological charac-

ters of T. sowerbyi (Wiktor, 1987, Giusti et al.,

1995) (Figs. 10, 12). The epiphallus in T. sowerbyi

is of medium length and cone-shaped, while in T.

marinellii n. sp. the epiphallus is very long and

equipped with an evident proximal portion comple-

tely absent in I sowerbyi ; the penis retractor mu-

scle in T. sowerbyi ends at about 2/3 of the length

of the epiphallus, while in T. marinellii n. sp. ends

at half the length of the epiphallus exactly where

the distal portion ends and the proximal one begins;

a pair of short supplementary muscles inserted at

the distal end of epiphallus observed in T. sowerbyi ,

lack in the new species.

The penis in T. sowerbyi is divided by a con-

striction in a short distal portion followed by a lon-

ger proximal chamber, while in T. marinellii a

proximal long portion is followed by a short distal

one, wide and sac-shaped; penial papilla in I so-

werbyi is squished, of vestigial type, while in T. ma-

rinellii is of cylindrical shape; the fold-like

thickening (reduced "stimulator") present in T. so-

werbyi , lacks in T. marinellii ; the spermatophore in

T. sowerbyi has a posterior portion covered with

very branched spines (Fig. 10), whereas in I mari-

nellii is covered by scattered spines not branched or

New and little known land snails from Sicily (Mollusca Gastropoda)

207

Figures 13-16. T. maninellii n.sp., Custonaci, Monte Sparagio, Giacolamaro, 08.1.2012: variability of the body colour. In

a specimen (Fig. 16) is visible the white-yellowish mucus.

208

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

O p^n-orm li ;an i im

16800 D panOrrililanum'

16933 D panomnilanumi

10935' O p^normilfinum,

16801 D punorm it an unv

16822 D panormiilsniirn.

16802 D panormilanum

16934 D panormiiamjm

— 10980 D panormiitanurn

16799 D panormilanifm

16797 D gdclv&ri

0795 D golcheri

6796 D gplcheri

d_r ie '

Gil — 1C

I 2 D laews

TOO L D taciwc

05944 D irtvodena

16920 D lnw4«n«

- 1 5984 D iniAidcnr:

16927 D invadens

L 1 0026 D inid^Kjpns

•pg * 15035 D irtvatlusTs

I 16919 D I modems

■ 1-403-8 D inwirirnr,

■ 16924 D irivadtuis

16925 O invadens

1 1692G O mwsdons

3 D reticulatum

O reticuialumi

2 O rc-ticulutum

4 D reticulatum

top

tOO

□e

2 T budepest

3 T budapcsl

1 t buGapest

TCUS2 COi LCO 1490. scf

TCUS4 COI LCO 1490. scf

TCUS 1 COI LCO 1490 scf

TMAD2 COI LCO 1490. scf

1 TMAD4 COI LCO 1490.6CT

. TMAD3 COI LCO 1490 . scf

90 * TM ADS COI LCO 1490. scf

— 506 Loh marginals

14 10 L flatAJs

flavus

flaws

A L flaws

fioj 1A1C

LM 2 L fit

I— 896 L

IOC L 3 L flt

4 iL c L 1

fluws

. flaws

— W0O2 L wnlilPorcidli

m p 1162 L clfiaiwsnlg«r

I* 14/8 L cmcreciciigcr

1 S44 L cinereoniger

1125 L cinsreoniger

B6 < 1 178 L ci acrconigcir

p 1379 L cinttre’omger

|i 734 L cineraoniger

55 1 701 L cinerconigcr

Li 365 L Bamansis

L5O0 L sarnensis

L979 L samcnsis

L 984 L aamoosis

L644 L sarpenrsis

70 1 L965 L sarnertsis

■ L890 L samensis

-I L053 L sarncnsis

* L970 L sarne-nsis

068 L woltsrstorffl

100

too

143 L minimus

126 L cf cewsfcu*

169 L corslcus

1 70 L corsicus

129 L cf. eofslcus

1010 L sancsrrsiij

■ 301 L cimineansis

— 81 1 L lanninfi

70S I Prandstcticri

991 L maxiniua

i — 1 185 L maximum

f- 903 L maxrmus

671 L maxlmus

16308 L max

&44 L mnxiimus

992 L maxlmus

Li 109 I maximurs

Figure 17. Maximum Likelihood consensus tree (rooted with respect to the genus Limax) inferred from a dataset of 83

(seven sequences obtained in the present paper and 76 retrieved from GenBank database) mitochondrial COI gene partial

sequences. Numbers above branches represent bootstrap values.

New and little known land snails from Sicily (Mollusca Gastropoda)

209

at most bifurcate with wider base, and the posterior

apex is bigger.

Examined material of Tandonia sowerbvi. Italy,

Emilia Romagna, Castiglione dei Pepoli, Roncobi-

laccio, 44°06 , 59 ,, N 11°13 , 42 ,, E, 593 m,

5. XE2011, 2 specimens (CS). Italy, Sicily: Castel-

buono, Cozzo Luminario, Piano Sempria,

37°54 , 18”N 14°03’59”E, 1192 m, X.1990, 4 spe-

cimens (CS); Palermo, Parco della Favorita, Val-

lone del Porco, 38°10 , 07”N 13°20 , 39 ,, E, 243 m,

13. XI. 1990, 4 specimens (CS); Monreale, Bosco

Ficuzza, Diga Scanzano, 37°55 , 14”N 13°22 , 25”E,

536 m, l.XII. 1990, 6 specimens (CS); Palermo,

Fiume Oreto, Ponte delle Grazie, 38°04’4”N

13°19 , 25”E, 95 m, 19.XI.1990, 5 specimens (CS);

idem, 3.XII.1990, 2 specimens (CS); Isnello, Con-

trada Montaspro, 37°54 , 42 ,, N 13°59’30”E, 857 m,

5. III. 1991, 1 specimen (CS); Collesano, Contrada

Croce, 37°55’23”N 13°55’20”E, 511 m, 5.III.1991,

6 specimens (CS); Cammarata, Monte Cammarata,

Cozzo Panepinto, 37°38 , 16”N 13°36 , 34”E, 984 m,

III. 1992, 4 specimens (CS); idem, 2 specimens

(CL); Petralia Sottana, Fiume Imera Meridionale,

37°48 , 26”N 14°05’01”E, 808 m, 2.XI. 1992, 3 spe-

cimens (CS); San fratello, Monte Soro, Pizzo

Muto, 37°56 , 16”N 14°38’16”E, 1410 m, X.2001,

1 specimen (CS); idem, 1 specimen (CL); Melilli,

Riserva Naturale Integrale Grotta Palombara, 2008

(CR); Monreale, Ponte Arcera, 37°55’42”N

13°23 , 01”E, 470 m, 14.XI.2008, 2 specimens,

(CL); Melilli, Riserva Naturale Integrale Grotta Pa-

lombara, 2008 (CR); Vizzini, Contrada Rubala,

near the F. Vizzini, 37°08 , 28 ,, N 14°44 , 15”E, 376

m, 11.1.2009, 5 specimens (CL); Prizzi, Fontana

Grande, 37°42 , 53”N 13°25 , 43”E, 800 m, 15.XI.2009,

4 specimens (CL); Torrenova, Rocca Scovoni,

Piano Scodoni, 38°05’38”N 14°41’26”E, 25 m,

06. XII.2009, 1 specimen (CL); Castelbuono, S. Gu-

glielmo, near the creek San Calogero, 37°55’04”N

14°04 , 22”E, 670 m, 1.2010, 3 specimens (CL); No-

vara di Sicilia, Rocca Novara, 37°59’35”N

15°08’25”E, 1000 m, 07.XI.2010, 4 specimens

(CL); Itala, Piano Fattaredda, 38°02’48”N

15 o 25’09”E, 612 m, 12.XII.2010, 2 specimens

(CL); Isnello, Vallone Montaspro, 37 0 54’18”N

13°58’55”E, 783 m, 26.11.2012, 2 specimens (CL).

Tandonia rustica (Millet, 1843) has an Euro-

pean central and southern distribution and is found

in the northern regions of Italy and along the Apen-

nines up to the central regions. This species is cha-

racterized by a very long epiphallus externally si-

milar to that of T. marinellii. However, T. rustica

is characterized by its whitish or creamy colora-

tion, somewhat violetish, with numerous, small

black dots; the penial complex (epiphallus+penis)

is smaller (around 10 mm) compared to T. mari-

nellii (20-31 mm), and has a different structure:

penis proportionally shorter and epiphallus sho-

wing internally long longitudinal rows of papillae,

penial papilla proportionally larger and much more

ornate; the place where musculus retractor inserts

is not constricted; atrium is narrow and tube-sha-

ped while in T. marinellii is short and very broad.

Examined material of Tandonia rustica. Italy,

Emilia Romagna, Castiglione dei Pepoli, Ronco-

bilaccio, 5.XI.2011, 1 specimen (CS); Italy, Lom-

bardia, Brescia, Valvestino, Armo, 45°46’N

10 o 35’E, 666 m, 22.X.2000, 1 specimen (CN);

idem, Anfo, S. Petronilla, 45°46’N 10 o 29’E, 524

m, 4.V.2008, 1 specimen (CN); idem, Ghedi,

45°24’N 10°16’E, 85 m, 20.IX.1996, 1 specimen

(CN), idem, Marone, Velio, 45°45’N 10 o 05’E, 200

m, 01.V.2007, 1 specimen (CN).

Molecular analysis. Seven Tandonia speci-

mens, three from Custonaci (TP) and four from

Madonie mountains (PA), labelled as TCUS and

TMAD respectively, were analyzed. Samples were

stored in 75% Ethanol at -20 °C in test tubes. For

each individual, a piece of about 40-50 mg was

used for total DNA extraction. Pieces of each spe-

cimen were deposited as vouchers at University of

Urbino, Lab. of cytogenetics and molecular bio-

logy. COI amplicons (654 bp) were obtained by

LCO1490/HCO2198 universal primers (5’-

GGTC AAC AAATC ATAAAGATATTGG-3 75 ’ -

TAAACTTC AGGGT GACC AAAAAAT C A-3 ’ )

as in Folmer et al. (1994) with a PCR cycle of 95

°C for 5 min; 95 °C for 1 min, 42 °C for 1 min, 72

°C for 1 min (37 cycles); 72 °C for 10 min. Se-

quencing of the purified PCR products was carried

out using automated DNA sequencers at Eurofins

MWG Operon (Germany). Finally, sequence chro-

matograms of each amplified fragment were brow-

sed visually. Sequences generated in this study

were analysed with additional seventy-six Lima-

cidae COI sequences retrieved from GenBank (IDs:

AF239733-34, AM259702-06, AM259712-14,

EF128217, FJ481179, FJ481181, FJ606455-71,

FJ606481, FJ606483, FJ606485, FJ606487,

FJ606489, FJ606491, FJ606493, FJ606495,

210

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

FJ606497, FJ606499, GQ145509, GQ145523,

GQ145525, GQ145527, GQ145538-39, GQ145553,

GQ145572-75, JN248291-99, JN248300-15; see also

Reise et al., 2011). Sequences were visualized with

BioEdit Sequence Alignment Editor 7 (Hall, 1999),

aligned with the ClustalW option included in this

software and double checked by eye. Standard mea-

sures of nucleotide polymorphism and phylogenetic

analyses were conducted in MEGA 5.0.3 (Tamura

et al., 2011). The best-fit evolution model of nucleo-

tide substitution resulted GTR+G (General Time

Reversible+Gamma). The evolutionary history was

inferred by using the Maximum Likelihood me-

thod; the bootstrap consensus tree was inferred

from 500 replicates; a discrete Gamma distribution

was used to model evolutionary rate differences

among sites (5 categories; +G, parameter = 0.4467).

Codon positions included were lst+2nd+3rd. All

positions containing gaps and missing data were eli-

minated. Divergence among TCUS and TMAD

groups (Dxy), assessed as p distance, was 5.9%.

Although genetic differences (p distance) are

only indicative when assigning a group to a given

taxonomic rank, the distance we assessed (5.9%)

between COI sequences obtained from specimens

collected in Madonie mountains and Custonaci not

only is in line with values considered discrimina-

tory at the specific level in Mollusca (i.e. Herbert

et al., 2003; Pfenninger et al., 2006), but it is even

greater than estimated distances separating entities

accepted as distinct species ( L . corsicus/L. senensis,

2.3%; L. ciminensis/L. senensis , 4.2%; L. mini-

mus/L. wolterstorffi , 4.4%).

In conclusion, phylogenetic tree (Fig. 17) and

genetic distance between TCUS and TMAD groups

firmly support the hypothesis that specimens from

Custonaci and Madonie mountains belong to two

distinct Tandonia species.

Remarks. The genus Tandonia Lessona & Pol-

lonera, 1882 has European-Mediterranean distribu-

tion extended to the Black Sea coasts (Wiktor, 1987,

Giusti et al., 1995). In Italy it’s verified the presence

of six species (Bank, 2012): T. nigra (C. Pfeiffer,

1849), T. bndapestensis (Hazay, 1880), T. robici

(Simroth, 1884), T. rustica , T. simrothi (Hesse,

1923), T. sowerbyi. Among them, T. sower by i and

T. rustica are morphologically the more similar to

T. marinellii n. sp. that, on the other hand, sharply

differs from these taxa for all the characters descri-

bed above. Noteworthy, in bibliography about Si-

cilian and surrounding geographical areas a few

taxa of uncertain taxonomic value are reported.

These taxa are examined below. Amalia marginata

var. oretea Lessona & Pollonera, 1882 is a taxon

described for Sicily (locus typicus: “Palermo presso

il fiume Oreto”) only on external morphological

characters: “Typica, clipeo tantum zonula nigra lon-

gitudinali mediana instructo” (Lessona & Pollonera,

1882). The body coloration in Tandonia ( =Amalia

Moquin-Tandon, 1855) is quite variable and topo-

typic specimens studied by us can be traced back,

due to the shape of genitalia, to T. sowerbyi (Figs.

10-12). A. marginata var. oretea is then confirmed

as a synonym of T. sowerbyi (Giusti, 1973; Bank,

2012). It would have been critical examination of

typical material, but the specimens described by

Lessona & Pollonera (1882) are no longer available

in their collection housed at the Museo Regionale

di Scienze Naturali di Torino (E. Gavetti in litteris).

Bourguignat (1877) established a new genus and

a new species, Palizzolia monterosati, on a single

Milacidae shell from Calatafimi with the following

description: “Limacelle ovalaire, epaisse, tres-bom-

bee (comme spherique) en dessous, caracterisee en

dessus: 1° Par une surface plane, sur laquelle on di-

stingue un cucleus median, circonscrit par une pro-

fonde depression; 2° par une forte echancrure a sa

partie mediane superieure”

Lessona & Pollonera (1882) recognise in Paliz-

zolia diagnostic characters of the shell of Milacidae

(oval, medial nucleus) and put Palizzolia in homo-

nymy with the genus Milax Gray, 1855 (sub Ama-

lia). This choise was followed by Cockerell (1991),

Kennard & Woodward (1926), Wiktor (1987) al-

though with a question mark, Alzona (1971) and

Barker (1999). However, the shell of Milacidae of-

fers no morphological characters useful for a relia-

ble classification at both genus and species level

and therefore it is possible that Palizzolia could be

an older synonym of Tandonia.

The taxon monterosati was usually treated as

doubtful species (Lessona & Pollonera, 1882; Mina

Palumbo, 1883; Cockerell & Collinge, 1893; Wik-

tor, 1987; Cockerell, 1991;) because the rear hol-

low, the considerable thickening of the lower part

of the shell and the groove around the apex are ab-

normalities detectable in different species of both

Milax and Tandonia genera; only Kennard & Wo-

odward (1926) pose the taxon monterosati in syno-

nymy with Milax gagates (Draparnaud, 1801).

New and little known land snails from Sicily (Mollusca Gastropoda)

211

Figures 18-20. Shell (limacella) of T. marinellii n.sp., holotypus, h: 7.65 mm - D: 5.05 mm. Figure 21. Geographic

distribution of Tandonia marinellii n. sp (circles) and T. sowerbyi (squares) in Sicily (personal data). Figures 22-24.

Typus of Palizzolia monterosati (MHNG BGT 2385), h: 4.5 mm - D: 3.8 mm, thickness 2.2 mm. Figure 25. Original

label of P. monterosati (MHNG BGT 2385). Figure 26. Four sequential visions of the ampoule rotated progressively so

that to allow the overall vision of the label of P. monterosati (MHNG BGT 2385).

Giusti et al. (1995) note that Tandonia shells are

generally thicker and oval, however examination of

the Palizzolia monterosati type (MHNG BGT

2385) (Figs. 22-26) does not provide indications

for univocal taxonomic attribution. At Calatafimi,

locus typicus of P. monterosati , we surveyed M. ni-

gticans (Philippi, 1851) and T. marinellii n. sp., but

the presence of M. gagates and T. sowerbyi cannot

212

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

be definitely ruled out. Hence, it appears that the

taxon/binomial Palizzolia monterosati Bourgui-

gnat 1877 is a nomen dubium, attributable with

certainty at neither genus nor species level. In

these cases, on the basis of article 75.5 of ICZN,

the Commission may be asked, in order to settle

all taxonomic doubts, to set up a neotype which,

in our opinion, should be Milax gagates since Pa-

lizzolia , as prevalent use, has been considered a sy-

nonym of the genus Milax , and monterosati

synonym of Milax gagates.

For North Africa, particularly Tunisia and

North Eastern Algeria, no species of the genus

Tandonia was ever reported (Cockerell, 1891;

Wiktor, 1987; Abbes et al., 2010). Milax gasulli

Altena, 1974 and Amalia ater Collinge, 1895 are

well known morphologically (genitalia) and con-

sidered as valid species of the genus Milax. Wiktor

(1987) based on specimens of Algeria (without ad-

ditional indications) puts Umax scaptobius Bour-

guignat, 1861 in synonymy with Milax gagates

and both Amalia cabiliana (Pollonera, 1891) and

A. gagates (var. or subsp.) mediterrana Cockerell,

1891 in synonymy with Milax nigricans.

Amalia maculata Collinge, 1895, described for

the surroundings of Algiers, was considered by

Wiktor (1987) synonymy of T. sowerbyi, but the

original description does not allow per se a certain

assignment to the genus Tandonia. The taxon ma-

culata Collinge 1895, however, is pre-occupied by

Amalia maculata Koch & Heynemann, 1874 =Ly-

topelte maculate (Koch & Heynemann, 1874) of

the family Agriolimacidae (see Wiktor, 1987) and,

for this reason, Hesse (1926) published, in its

place, the new taxon Milax collingei. Limax ere-

miophilus Bourguignat 1861 (locus typicus Al-

giers, Algeria) was described only based on color

and remains a taxon of uncertain allocation at both

genus and species level. T. sowerbyi is reported for

the regions of Southern Italy, attested with cer-

tainty up to Basilicata (Ferreri et al., 2005).

For Calabria two little-known taxa were de-

scribed by Paulucci (1879), unreported even by

Alzona (1971): Amalia mongianensis (locus ty-

picus: Monte Pecoraro, Mongiana, Catanzaro)

and A. fulva (locus typicus: “Monte Sant'Elia,

Palmi”). The specimens from Calabria we could

examine are to be considered as T. sowerbyi , al-

though there are some morphological features

that require further study.

Family Subulinidae Thiele, 1931

Rumina saharica Pallary, 1901

Examined material. Rumina saharica. Italy,

Sicily, Egadi Islands, Marettimo, admist Case

Romane and Buccerie 200-250 m, 37°58’N,

12°03’E, 30.V.2010, 6 specimens, 1 shell (CL);

idem, 18 shells (CS); idem VIII. 20 12, 2 speci-

mens, 10 shells (CC).

Description. Shell dextral (Figs. 27-30), whi-

tish, truncated, height 30.5 mm, maximum dia-

meter 10 mm, slender, sub-cylindrical, with

slightly convex sides, the last whorl is wider than

the penultimate whorl. Animal white. Genitalia

(Figs. 31-32) characterized by vagina internally

with longitudinal pleats and penis internally with

some sparsely distributed papillae towards the

proximal end.

Biology and Distribution. R. saharica is a

thermophilic and xeroresistant species. The genus

Rumina Risso, 1826 has Mediterranean distribu-

tion extending to Macaronesia, but it was disper-

sed by man in some extra-Mediterranean countries

(United States, Mexico, Cuba, Bermudas, China,

Japan). Currently, R. saharica seems to prevail in

the north African-East European area (Carr, 2002;

Prevot et al, 2007).

Remarks. Prevot et al. (2007) with molecular

analyses demonstrated the presence in the Mediter-

ranean area of two groups of species: R. decollata

and R. saharica. They also showed the presence in

R. decollata of two clades genetically distinct but

morphologically similar. In addition, Mienis (2002)

re-evaluates the validity of R. paviae (Lowe 1861)

from Morocco, Algeria, and Tunisia. In Sicily, ac-

tually, is known only R. decollata (Manganelli et

al., 1995; Bank, 2012) (Figs. 23-24).

Carr (2002) signals, in the collection of Na-

tural History Museum of London, the presence

of three shells similar to R. saharica collected in

Sicily, however he points out that without data

on the genitalia the classification of Rumina spe-

cies is not certain. The population of Rumina

from Marettimo Island (Western Sicily) which

we examined shows the typical morphological

characters of R. saharica (sensu Carr, 2002) with

the exception of the duct of bursa copulatrix

which is slightly longer.

New and little known land snails from Sicily (Mollusca Gastropoda)

213

Figures 27, 28. Shell of Rumina saharica , Marettimo, h: 31.9 mm - D: 10.2 mm. Figures 29, 30. Idem, h: 26.4 mm - D:

9.8 mm. Figure 31. Genitalia of R. saharica, Marettimo. Figure 32. Idem, internal structure of penis and vagina.

214

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

Family Clausiliidae Morch, 1864

Lampedusa lopadusae nodulosa Montero-

sato, 1892

Clausilia (Lopadusaria) nodulosa - Monterosato,

1892: 29

Clausilia (Lopedusaria) nodulosa - Kobelt, 1893: 303

Clausilia (Lopedusaria) nodulosa - Kobelt, 1897: 292

Clausilia lopadusae var. nodulosa - Westerlund,

1901: 105

Clausilia lampedusae var. - Giglioli, 1912: 217

Lampedusa lopadusae nodulosa - Alzona in Zavat-

tari, 1961: 427

Delima (Lmpedusa) lopedusae - Alzona, 1971: 92

Lampedusa lopadusae , (synonym) nodidosa - Ho-

lyoak, 1986: 217

Lampedusa lopadusae , (synonym) nodulosa -

Beckmann, 1992: 22

Lampedusa lopadusae , (synonym) nodulosa - Cian-

fanelli, 2002: 61, T. 9, f. 29

Lampedusa lopadusae , (synonym) nodulosa -

Bank, 2012

Examined material. Italy, Sicily, Pelagian Is-

lands, Lampione, 31.VIII.2009, 12 specimens, legit

T. La Mantia (CS); idem, 09.IX.2009, 23 speci-

mens, legit A. Corso (CL); idem, 23. VII. 2010, 5

specimens, legit T. La Mantia and S. Pasta (CS).

Description. Shell sinistral (Figs. 33-36), me-

dium-sized (height 13-18.7 mm; maximun diameter

3. 6-4.4 mm), fusiform, apex obtuse, elongated and

inflated at half of its height, rather thick and robust,

yellowish-brown in colour when fresh; external sur-

face with oblique, thin and close ribs, 54-81 ribs on

penultimate whorl. Spire with 9-10 convex whorls

slowly and regularly growing, last whorl distinctly

narrower than penultimate whorl and tapering dow-

nwards, rather gibbous near umbilicus. Sutures

deep, subcrenulated; umbilicus slit-like, internally

closed; aperture about % of shell height (height 3.5-

4.4 mm; maximun diameter 2. 9-3. 7 mm), irregu-

larly ovalar or sub-squared, peristome continuous,

reflected, little thickenek. Aperture with 5 lamellae

on parietum and columellar side and 3 or 4 plicae

and lunella on palatum. On parietum (Figs. 41-42),

starting from suture, there are: parallel lamella in

the form of small relief, spiral lamella at centre of

parietum, columellar lamella, a little subcolumellar

lamella, and a tooth like parietal lamella (upper la-

mella); only columellar lamella and parietal lamella

are visible trough the opening (in apertural view).

On the palatum (Fig. 43) there is a lateral lunella

and, starting from suture: a long, well developed

sutural plica; a second sutural plica variable in

length: as long as the first one, shorter, or someti-

mes absent; principal plica thin and raised; palatal

plica showing a rear portion merged with the upper

part of lunella, a central indistinct part and an an-

terior part in the form of relief just visible. Clausi-

lium elongated, plough-like (Fig. 44).

Body. Animal oval-elongate, narrow, posteriorly

pointed, white-yellowish; upper tentacles short, cy-

lindro-conical, apically widened, with small black

eyes; lower tentacle very short (Fig. 51; see also

Cianfanelli, 2002 fig. 29).

Genitalia. Anatomical organization of the geni-

talia (Fig. 49) is similar to L. lopadusae (Soos, 1933;

Pinter & Varga, 1984; Holy oak, 1986; Giusti et al.,

1995) with penial complex consisting of flagellum,

epiphallus, penis and penial diverticulum; flagellum

short and slender; epiphallus divided by insertion of

penial retractor muscle into proximal (1.5- 1.6 mm)

and distal (1.2- 1.9 mm) portions; long, hook-like pe-

nial diverticulum (1.5-1.88 mm) arising on border

between epiphallus and penis; penis long (2. 6-3. 6

mm); on the inner wall there are 5 longitudinal crests

which are parallel in the distal portion and rather in-

distinct towards the penial diverticulum. Vagina

long; short, wide copulatory duct branched in a short

and slender duct of bursa copulatrix with small oval

bursa copulatrix, and a short diverticulum of bursa

copulatrix; short free oviduct.

Biology and Distribution. At the base of ve-

getation, at the soil, under stones (T. La Mantia in

verbis). L. lopaduse nodidosa is endemic of the lit-

tle isle of Lampione (Fig. 52), Pelagian Islands, bet-

ween Sicily and Tunisia.

Remarks. Monterosato (1892) described "Clau-

silia (Lopadusaria) nodulosa" from the island of

Lampione, with the following words: ”Conchiglia

solida, striata quasi obliquamente (nella C. Lopa-

dusae le coste sono perpendicolari ed esattamente

lamellate); apertura a bordi ben rivoltati, porcella-

niosi; colorazione bianchiccia; anfratti cochleae-

formi, apice piu ottuso. Dimensione quasi la

stessa.” [“Solid shell, ribbed almost sideways (in C.

lopadusae the ribs are perpendicular and exactly la-

mellated); opening with edges well turned, porce-

lain-like; whitish colour; cochlea-shaped whorls,

apex more obtuse. Almost the same size"].

New and little known land snails from Sicily (Mollusca Gastropoda)

215

Figures 33-36. Shell of L. lopadusae nodulosa , Lampione, h: 16.94 mm - D: 4.16 mm. Figures 37-40. Shell of L. lo-

padusae lopadusae , Lampedusa, h: 17.11 mm - D: 4 mm.

216

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

Figures 41-44. L. lopadusae nodulosa , Lampione: palatum of two specimens (Figs. 41-42), parietum (Fig. 43) and clausi-

lium (Fig. 44). Figures 45-48. L. lopadusae lopadusae , Lampedusa, palatum of two specimens (Figs. 45-46), parietum

(Fig. 47) and clausilium (Fig. 48).

New and little known land snails from Sicily (Mollusca Gastropoda)

217

Subsequently, this taxon is reported by Kobelt

(1893; 1897) while Westerlund (1901) and Alzona

(1961) consider it respectively as variety and sub-

species of L. lopadusae. Alzona (1971), Holyoak

(1986) and Beckmann (1992) put L. nodulosa in sy-

nonymy with L. lopadusae. No news of this taxon

is reported by Manganelli et al. (1995) and Cossi-

gnani & Cossignani (1995). Cianfanelli (2002), de-

spite considering it a synonym of L. lopadusae ,

reports that the population of the island of Lam-

pione “. . . presenta dei caratteri piuttosto distinti sia

nella conchiglia che nell’animale” ["... shows pretty

distinct characters both in the shell and in animal"].

Nordsieck (2007) did not mention it in his catalog

on the Clausiliidae of the world, Bank (2012) still

considers it a synonym of L. lopadusae. L. nodulosa

differs from L. lopadusae (Figs. 37-40. Figs. 45-48.

Fig. 5 1) for shell less robust, darker in color i.e. yel-

lowish-brown (yellowish-grey in L. lopadusae ),

with deeper sutures, and whorls more convex so

that the shell profile, in frontal view, appears less

linear than L. lopadusae ; peristome is less develo-

Figure 49. Genitalia of L. lopadusae nodulosa. Figure 50, 51. Body colour in L. lopadusae lopadusae (Fig. 50) and L. lo-

padusae nodulosa (Fig. 51). Figure 52. Lampione island (photo P. Lo Cascio).

218

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

ped and calcified; ribs are more oblique, more nu-

merous and less robust; in the internal structure of

the shell, L. nodulosa mostly shows a second sutu-

ral plica (rarely present in L. lopadusae). Genitalia

of L. nodulosa differ from L. lopadusae for penial

diverticulum slightly longer; the animal is lighter in

color. As reported in the original description of

Monterosato (1892), highlighted by Cianfanelli

(2002) and confirmed by our observations, L. no-

dulosa presents some morphological differentia-

tions with respect to L. lopadusae and therefore we

believe it is worthy of taxonomic reconsideration,

at least at the sub-specific level, also in view of its

peculiar geographical isolation. Indeed, the island

of Lampione, where L. nodidosa lives, reaches its

maximum altitude at 36 m above sea level and is

approximately 17.5 Km far from Lampedusa, from

which is separated by a stretch of sea -80 m deep.

Despite its very little size, this islet harbours a very

rich pool of plant and animal species, particularly

some local endemics of high biogeographic interest

(Lo Cascio & Pasta, in press.)

Family Hygromiidae Tryon, 1866

Cernuella (Cernuella) tineana (Benoit 1862)

Helix tineana - Benoit, 1862: 185-187, t. 4, fig. 24

(Calatafimi)

Helix tineana - Pfeiffer, 1868: 487 (Sicilia, Cala-

tafimi)

Helix tineana - Benoit, 1875: 14 (Calatafimini)

Helix Xerophila tineana - Kobelt, 1875: 18 (Ca-

latafimi)

Helix (Xerophila) Jacosta tineana -Westerlund,

1876: 104 (Sicilia)

Helix (Xerophila) Jacosta tineana var. kobeltiana -

Westerlund, 1876: 104

Helix tineana - Kobelt in Rossmassler, 1877: 103-

104, fig. 1452 (Sicilia, Calatafimi)

Xerophila (Jacosta) tineana - Kobelt, 1881: 47

(Sicilien)

Xerophila (Jacosta) tineana kobeltiana - Kobelt,

1881:47 (Sicilien)

Helix tineana - Benoit, 1882: 37 (Calatafimini)

Helix (Helicella) Jacosta tineana - Tryon, 1887:

253 pi. 62 fig. 92-94 (Sicily)

Helix (Xerophila) Jacosta tineana - Westerlund,

1889: 318 (Sicilien, Calatafimini)

Helix (Xerophila) Jacosta var. mista - Westerlund,

1889: 318-319 (Sicilien)

Helix (Xerophila) Jacosta tineana var. kobeltiana -

Westerlund, 1889: 319 (Sicilien)

Helix (Xerophila) Jacosta tineana var. mista -We-

sterlund, 1890: 61 (Sicilien)

Helix (Xerophila) Jacosta tineana var. kobeltiana -

Westerlund, 1890: 61 (Sicilien)

Helicella Jacosta tineana - Pilsbry, 1894: 260

Helicella Jacosta tineana var. mista - Pylsbry, 1894:

260

Helicella Jacosta tineana var. kobeltiana - Pylsbry,

1894: 260

Helicella (Xerotropis) tineana - Alzona, 1971: 174

Helicella (Xerotropis) tineana mixta - Alzona,

1971: 174

Helicella (Xerotropis) tineana kobeltiana - Alzona,

1971: 174

Examined material. Italy, Sicily, Monte Cofano,

Gorgo Cofano, 38°06’07”N 12°40’31”E, 228 m,

14.X. 1984, numerous specimens (CS); Italy, Sicily,

Sciacca, Torre Macauda, 37°28 , 58”N 13°10’59”E,

59 m, l.VII/3 l.VII. 1986, numerous specimens (CS);

Italy, Sicily, Monte Cofano, Gorgo Cofano,

38°06’07”N 12°40’31”E, 228 m, 14.IV. 1991, nume-

rous specimens (CS); Italy, Sicily, Ribera, Contrada

Castello, 37°30 , 18”N 13°15 , 04”E, 153 m, IX.2005,

3 specimens, 10 shells (CR); idem, 37°30’23”N

13°14’12”E, 144 m, IX.2005, 2 specimens, 12 shells

(CR) ; Italy, Sicily, Cava a Nord di Ribera,

30.XII.2007, 3 specimens, M. and E. Bodon (CB);

Italy, Sicily, Sciacca, Torre Macauda, 37°28 , 58”N

13 o 10’59”E, 59 m, 24.V.2008, numerous specimens

(CS) ; idem 22.11.2009, 23 shells (CL); Italy, Sicily,

Sciacca, Torre Macauda, 37°28 , 58” N 13°10 , 59” E,

60 m, 22.XI.2009, 1 specimen, 8 shells (CL); Italy,

Sicily, Custonaci, Rio Forgia, 38 o 03’42”N

12°39 , 32”E, 56 m, 6.II.2011, 3 subfossil shells (Figs.

70-72); Italy, Sicily, Monte Cofano, Gorgo Cofano,

38°06 , 07”N 12°40’31”E, 228 m, 20.XI.2011, nume-

rous specimens (CS); Italy, Sicily, Monte Cofano,

Gorgo Cofano, 38°06 , 07”N 12°40’31”E, 228 m,

4.III.2012, numerous specimens (CS); Italy, Sicily,

Custonaci, Baglio Cofano, 38°06 , 11”N 12°40’40”E;

250 m, 05.VIII.2012, 29 shells (CL).

Description. Shell dextral (Figs. 53-55, 57-75),

medium-sized (height: 7.2 mm, maximum diameter

17 mm), depressed, robust, whitish or greyish-yel-

low in colour with brown band and dark apex; ex-

ternal surface finely and regularly ribbed, opaque.

New and little known land snails from Sicily (Mollusca Gastropoda)

219

Figures 53-56. “Helix” tineana , Calatafimi, Paulucci collection (MZUF GC/10825) (Figs. 53-55) and original label (Fig.

56), photos Saulo Bambi. Figures 57-60. C. tineana , Custonaci, Monte Cofano, Baglio Cofano, h: 5.55 mm - D: mm

11.10 mm.

220

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

Figures 61-63. CernueUa tineana , Sciacca, Torre Macauda, h: 6.90 mm - D: 12.92 mm. Figures. 64-66. Idem, h: 6.30

mm - D: 12.46 mm. Figures 67-69. C. tineana , Sciacca, Monte San Calogero, coll. Paulucci (MZUF GC/41419), foto

Saulo Bambi. Figures 70-72. C. tineana , Custonaci, Rio Forgia, subfossil.

New and little known land snails from Sicily (Mollusca Gastropoda)

221

Figures 73-75. Cernuella tineana, Sciacca, Torre Macauda, h: 7.07 mm - D: 12.42 mm. Figures. 76-78. C. amanda, San

Vito lo Capo, Salinelle, h: 12.18 mm - D: 7.12 mm. Figures 79-81. C. rugosa , Castelluzzo, Calette degli Agliarelli, h:

6.30 mm - D: 11.95 mm. Figures 82-84. C. cisafpina, Castellammare del Golfo, Fraginesi, h: 6.90 mm xD: 10.80 mm.

222

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

Figures 85-87. Genitalia of Cernuella tineana , Custonaci, M. Cofano, Gorgo Cofano (Fig. 85), C. cisalpina, Castellam-

mare del Golfo, Fraginesi (Fig. 86) and C. rugosa , Castelluzzo, Golfo di Cofano (Fig. 87).

New and little known land snails from Sicily (Mollusca Gastropoda)

223

l mm

Figure 88. Genitalia of Cernuella tineana, Sciacca, Torre Macauda. Figure 89. Idem, internal structure of penis, dart

sac and vagina.

224

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

spire more or less flat, with 5 regularly growing

whorls, slightly convex; marked sutures; last whorl

very convex below and keeled at its periphery; um-

bilicus deep and wide, about 1/3 of maximum shell

diameter; aperture oval and slightly angled, peri-

stome simple, interrupted, with internal rib.

Body. Animal whitish; dorsal region provided,

more or less extensively, of dark spots.

Genitalia. Short free oviduct, duct of bursa co-

pulatrix of medium length, with large base, ending

in a sac-like bursa copulatrix; vagina short (1-1.6

mm), 2 tufts of digitiform glands with 4-5 slender

lobes and 8-12 apexes, disposed on opposite sides

of proximal vagina. Dart-sac complex consisting

of a pair of stylophores located on one side of va-

gina; large outer stylophore containing dart. Penial

complex composed of flagellum, epiphallus and

penis; flagellum long (2-2.4 mm), ending where

vas deferens enters penial complex; epiphallus

long 3-5 times the length of the penis (4. 5-5. 5

mm), ending where penial retractor muscle con-

tacts penial complex wall; penis short (1.5-2. 2

mm); penial papilla cylindrical, elongate, with api-

cal opening, and base connected to penial walls by

three small muscles (frenula).

Biology and Distribution. C. tineana is found

on the ground, usually on grass often under stones.

It is endemic to Sicily, distributed with point popu-

lations in coastal and low-hill territories ranging from

Custonaci (Monte Cofano) in the province of Trapani

to Ribera in the province of Agrigento (Fig. 90).

Comparative notes. Anatomical character of

"Helix" tineana suggest to ascribe this species to

the genus Cernuella Schluter, 1838 sensu stricto:

penial papilla with three basal frenula, two groups

of digitiform glands on opposite sides of the vagina,

proximal vagina short or absent, proximal portion

of the duct of bursa copulatrix wide (Manganelli &

Giusti, 1987; Manganelli et al., 1996a, b, 2001).

Currently, five species of Cernuella s. str. are reco-

gnized in Sicily (Bank, 2012): C. aradasi (Pirajno,

1842), C. metabola (Westerlund, 1889), C. cisal-

pina (Rossmassler, 1837), C. virgata (Da Costa,

1778), C. rugosa (Lamark, 1822).

C. aradasi is a dune-species with limited distri-

bution to the dunes near the lighthouse in Messina

(North-east Sicily) and neighbouring sandy soils.

It’s distinguished from C. tineana for shell smaller,

smooth, globose and without keel; genitalia cha-

racterised by relatively large penis and by epiphal-

lus twice as long as penis.

C. metabola is an endemic species from Lam-

pedusa island; it is distinguished from C. tineana

by the shell with the globose shell with disconti-

nuous, thick ribs and narrow umbilicus. A prelimi-

nary study on the genitalia of this species seems to

highlight significant differences from the other Cer-

nuella species (unpublished data).

C. cisalpina is a polymorphic species, with a

Mediterranean distribution, for which several taxa

of still difficult taxonomic interpretation were

established. Shell of small-medium size, “small

sized Cernuella ” sensu Manganelli & Giusti

(1987), subglobose, with thin ribs, sometimes well

raised, last whorl usually rounded or angled at its

periphery (keel-like) (Figs. 82-84). Some popula-

tions of C. cisalpina present a shell similar to that

of C. tineana , but in addition to the morphological

characteristics of C. tineana pointed out above,

they are always distinguishable by their genitalia

with epiphallus 2-3 times longer than penis, fla-

gellum and penis proportionally shorter and digi-

tiform glands lower, i.e. between the vagina and

the inner dart sac (Fig. 86).

C. virgata is a polymorphic species showing a

European-wide distribution. In Sicily it is common

at low and medium altitudes where specimens can

be found on grass and shrubs. C. virgata is distin-

guished from C. tineana for the shell which is smo-

oth or with faint wrinkles, without keel and larger,

"large sized Cernuella " sensu Manganelli & Giusti

(1987); genitalia resembling those of C. cisalpina

but with epiphallus longer and more numerous di-

gitiform glands.

C. rugosa , endemic of Western Sicily known

only for two locations (Figs. 79-81, 90), is an ex-

tremely vulnerable species deserving of protection.

From the morphological point of view C. rugosa is

distinguished from C. tineana for the shell with rai-

sed, irregularly spaced ribs and a cordlike, crenula-

ted keel at its periphery, and for the penial complex

(Figure 87; Manganelli at al., 1996b, Fig. 16) with

penis longer, epiphallus and flagellum shorter.

C. tineana is morphologically well distinguisha-

ble from other Cernuella species sensu stricto. Dif-

ferential diagnosis problems may arise with the shell

of Cernuella (Xeroamanda) amanda Rossmassler,

1838 (see also Benoit, 1862-1857) (Figs. 76-78).

In the latter species the shell is as convex infe-

riorly as in the upper part, the keel is less obtuse

than C. tineana , opening more angled and the um-

New and little known land snails from Sicily (Mollusca Gastropoda)

225

bilicus markedly funnel- shaped. However, an exa-

mination of genitalia can easily allow to distinguish

the two species that belong to distinct subgenera

(Manganelli etal., 1996).

Remarks. Helix tineana was described by Be-

noit (1862) for the surroundings of Calatafimi,

"Pizzo di grasso " and dedicated to the then Director

of the Orto Botanico of Palermo, Vincenzo Tineo.

Benoit (1857) provides, in addition to the detailed

description of the shell, also a comparative analysis

of “Helix” rugosa Lamark, 1822 and “Helix”

amanda Rossmassler, 1838, and draws the three

species in table IV, figs. 24, 25, 29. In his later

works, Benoit (1875, 1882) reported this species ci-

ting only the locus typicus. Other authors cited this

species: Pfeiffer (1868), Kobelt (1875), Kobelt in

Rossmassler (1877), Tryon (1887). Westerlund

( 1876) reports it indicating the locality "Sicilia" and

describes the variety kobeltiana on the basis of spe-

cimens received by Kobelt under the name " H.

tinei Ben.". Subsequently, Westerlund (1889) re-de-

scribes H. tineana from " Sicilien bei Calatafimi "

and adds to the variety kobeltiana the new var.

mista with "Sicilien" as locus typicus.

Alzona (1971) ascribes “tineana” to the genus

Helicella Ferussac, 1821 subgenus Xerotropis Mon-

te rosa to, 1892 and considers the two varieties de-

scribed by Westerlund (1889) as valid subspecies.

Neither Cossignani & Cossignani (1995) and Man-

ganelli et al. (1995) nor Bank (2012) report "Helix"

tineana for, respectively, the Italian fauna and the

European fauna.

Despite repeated searches, we have not found

this species in the locus typicus, Calatafimi. Howe-

ver, in Paulucci collection we saw a shell determi-

ned as “Helix tineana” (MZUF GC/10825),

collected in Calatafimi by a Sicilian naturalist De

Stefani, in 1868 (Figs. 53-56). This topopypic sam-

ple corresponds with Benoit’s original description

and even with the specimens we have sampled and

studied on Monte Cofano. The more southerly po-

Figure 90. Geographic distribution of C. tineana (circles) and C. rugosa (squares) in Sicily.

226

F. Liberto, S. Giglio, M.S. Colomba & I. Sparacio

pulations (Sciacca, Ribera) have slightly larger di-

mensions. To these populations we attribute, by

comparison, also one sample from Paulucci collec-

tion sub H. caficiniana (MZUF GC/41419) picked

up at Sciacca, Monte San Calogero (South-Western

Sicily) (Figs. 67-69).

“Helix” caficii , described by Westerlund (1876)

with locus typicus Sciacca, corresponds, in our

view, with the populations of C. tineana of Sciacca.

If the examination of the type in the Westerlund col-

lection will confirm this assumption "Helix" caficii

may be a synonym of C. tineana.

ACKNOWLEDGEMENTS

We wish to thank Luigi Barraco (Valderice, Tra-

pani, Italy), Marco Bodon (Italy, Genova), Saulo

Bambi and Simone Cianfanelli (Museo di Storia

Naturale delFUniversita di Firenze sezione di zoo-

logia de “La Specola”), David R Cilia (Santa Ve-

nera, Malta), Andrea Corso (Siracusa, Italy), Giulio

Cuccodoro and Yves Finet (Museum d’Histoire na-

turelle, Geneve, Switzerland), Elena Gavetti

(Museo Regionale di Scienze Naturali di Torino,

Italy), Alessandro Hallgass (Roma, Italy), Tommaso

la Mantia (Palermo, Italy), Pietro Lo Cascio (Lipari,

Messina, Italy), Giuseppe Maraventano (Lampe-

dusa, Agrigento, Italy), Gianbattista Nardi (Nuvo-

lera, Brescia, Italy), Roberto Poggi (Museo Civico

di Storia Naturale di Genova “G. Doria”, Italy),

Agatino Reitano (Tremestieri Etneo, Catania, Italy),

Andras Varga (Andras Varga, Matra Muzeum

Gyongyos, Hungary), Francisco Welter-Schultes

(Zoologisches Institut, Berliner, Germany).

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Biodiversity Journal, 2012 , 3 ( 3 ): 229-236

A stability assessment on seasonal variation of seaweed beds

n theTrat peninsula of Thailand

Nidsaraporn Petsut'jAnong Chirapart 2 & Methee Keawnern 1

’Department of Fishery Management, Faculty of Fisheries, Kasetsart University, Bangkok 10900, Thailand; email: nidsarapom@ru.ac.th

department of Fishery Biology, Faculty of Fisheries, Kasetsart University, Bangkok 10900, Thailand

’Corresponding author

ABSTRACT Species diversity, biomass and distribution pattern of seaweed beds in the Trat peninsula,

east coast of Thailand, were investigated in relation to environmental conditions from Ja-

nuary to December 2011. The macroalgal samples and environmental factors were collec-

ted monthly; covering cool-dry (January-February, November-December), hot-dry

(March-April) and rainy (May-October) seasons at four sampling stations; Ao Cho, Ao

Lane, Laem Tien and Laem Sok. A total of 26 taxa of marine benthic algae were recorded,

of which 16 species of red marine algae were the most diverse group. It was found that

Ccitenella nipae , Gracilaria salicornia, Gelidium pusillum , Hydropuntia changii, Hypnea

hamulosa, Kyrtutrix maculans, Laurencia decumbents, Lyngbya majuscula , Peyssonnelia

rubra and Ulva clathrata were the most abundant throughout the sampling period. The hi-

ghest number of marine flora species was obtained in March (25 species), whereas the lo-

west in June (12 species). Algal biomass had a maximum value in April (59.50 g/m 2 dry

weight) and minimum value in July (20. 14 g/m 2 dry weight).

KEY WORDS Seasonal variation; benthic algae; seaweed beds; Conservation; Trat peninsula.

Received 12.07.2012; accepted 03.09.2012; printed 30.09.2012

INTRODUCTION

The seaweed or marine macrophytic algae,

which are a large and diverse group of eukaryotic

photo synthetic organisms occurring in marine en-

vironment, are one of the major marine fishery re-

sources in Thailand (Edwards et al., 1982).

Seaweed beds are a common habitat in coastal in-

shore communities consisting of large benthic ve-

getation and distributed widely along coastline of

Thailand (Lewmanomont, 1998; Prathep, 2005).

They are highly valuable ecologically and eco-

nomically and perform a variety of functions within

marine coastal ecosystems (Lobban & Harrison,

1994; Stachowicz et al., 2008). Most seaweed beds

are served as a vitally important food sources for

fish and aquatic invertebrates and provide breeding

area for several species of marine animals (Zhang

et al., 2008). Additionally, seaweeds are used

around the world as food and fertilizers and for the

extraction of valuable commercial products (Sam-

bamurty, 2006, Graham et al., 2009).

Trat is one of the provinces located in the east

of Thailand, and encloses the upper Gulf of Thai-

land adjacent to the border between Thailand and

Cambodia. Along the coastline of Trat peninsula,

there are many different types of coastal ecosystems

including estuaries, mangrove areas, sandy shores

and mudflats. In addition to coastal environment,

there is a considerable amount of nutrient supply

variation in the response of wave exposure gradient.

Because of the properties of coastal area features

and environmental diversity, Trat peninsula has re-

markably diverse marine fishery resource, espe-

230

N. Petsut, A. Chirapart & M. Keawnern

cially macroalgal flora; wild populations of macro-

algae are widely distributed in the intertidal and

subtidal zones of Trat peninsula (Pirompug, 1976)

and used as human food and for agar extraction

(Edwards & Tam, 1984; Chirapart et al., 1992).

Currently, the abundance and diversity of Thai

seaweed has been vulnerable to decline because of

over-harvesting of natural populations and the eco-

logical deterioration of several inshore and estuary

ecosystems (Lewmanomont, 1998).

In Trat costal areas and adjacent waters, the

rapid extension and development of fisheries acti-

vities by local fishermen and conversion of man-

grove areas into shrimp farms and urban areas

threaten aquatic organisms (Menasveta, 1997) and

this situation has a potentially negative impact on

the coastal ecosystem (Doydee, 2005). Accordingly,

the change in ecosystem and environmental condi-

tions, mangrove deterioration and costal land-use

activities would result in a decrease of macroalgal

biodiversity and biomass in Trat peninsula.

The need to promote a scenario of seaweed re-

source management is therefore important for su-

stainable conservation and restoration of coastal

ecosystem. However, information and knowledge

regarding to macroalgal assemblages and their

ecology is very limited in this coastal region. In

order to provide useful data for a possible preli-

minary management strategy for conservation of

seaweed resources in Trat peninsula we determi-

ned seasonal variation in the species diversity,

biomass and distribution pattern of macroalgae

with reference to some environmental variables

for better understanding of the recent situation in

algal communities.

MATERIALS AND METHODS

Study area

The study site is located at the coastal area of

Trat province, east of Thailand. Four coastal areas

of intertidal habitat, which are different in shape and

environmental condition, were chosen as research

station: Ao Cho (site 1), Ao Lane (site 2) Laem Tien

(site 3) and Laem Sok (site 4).

Among the stations, Ao Clio and Ao Lane are

semi-exposed areas. Ao Cho is characterized by the

formation of sandy beaches alternated with rocky

shores and partly surrounded by mangroves, while

natural habitat of Ao Lane is composed mainly by

mudflat and this area is moderately occupied by in-

digenous fisheries community.

Laem Tien is a non-exposed area with muddy

sand bottom fringed by mangroves, and some parts

of this area are heavily exploited for aquaculture

and shrimp farms. Additionally, Laem Sok, a fully

exposed area with rocky shore habitat, is partially

converted for commercial and industrial activities.

Sample collection and laboratory analysis

Species diversity, biomass and distribution

Field sampling was carried out once a month at

four stations for a year (from January to December

2011). Benthic marine macroalgae were sampled

thoroughly by wading or snorkeling. Complete

thalli of live specimens were uprooted by hand or

with paint-scraper, placed in plastic bags, labeled

by location and date of collection, and transported

to laboratory.

Algal samples were rinsed to remove sediment

and debris, photographed, preserved as herbarium

vouchers, or, on some occasions, preserved in 4%

formalin-seawater solution, and deposited at the

Algal Bioresources Research Center, Faculty of Fi-

sheries, Kasetsart University. The species identifi-

cation was based on gross morphology and internal

features following Lewmanomont & Ogawa

(1995); Huisman (2000) and Litter & Litter (2000;

2003). In order to determine algal biomass and di-

stribution pattern, a quadrat method along a vertical

transect line set across the intertidal zone perpendi-

cularly to the coastal line was performed monthly

throughout the study period.

Once a month 25 replicates of sampling quadrat

(50x50 cm) from research stations were collected

for determination of algal biomass. Algal samples

from each quadrat were carefully cleaned with fre-

shwater to remove sand, silt, epiphytes and other de-

bris before weighting. Dry weight of algal biomass

was obtained by drying the samples in the oven at

105°C for 48 hours (Wong & Phang, 2004).

Environmental parameters

Environmental parameters, including physical

and chemical factors, were recorded seasonally at

the moment of each sampling. For physical varia-

bles, seawater temperature, salinity, pH, turbidity

and dissolved oxygen (DO) were measured in the

A stability assessment on seasonal variation of seaweed beds in the Trat peninsula ofThailand

231

field. Seawater temperature and DO were determi-

ned using a salinity compensated dissolved oxygen

meter (YSI Model 57).

Salinity was determined by hand refractome-

ter; pH was measured using a pH meter (YSI

Model 60) and water transparency was estimated

by a turbidimeter (LaMotte Model 2020). Total

rainfall of Trat peninsula was obtained from the

Meteorological Department ofThailand. For che-

mical variables, nutrient concentration in the sea-

water was evaluated.

Water quality was sampled from each study site

and fixed in ice chests to examine alkalinity, har-

dness, ammonia, nitrate, nitrite and phosphate,

using the methods of Sasaki & Sawada (1980) and

Strickland & Parsons (1972).

Statistical analysis

Data for statistical analysis were tested initially

for normality and homogeneity (Zar, 1984). One-

way analysis of variance (ANOVA) was employed

to search for any significant difference among

month, site and biomass data of each species.

Statistical significance was set at p<0.05 and the

stability of the estimate reflected by 95% confident

intervals. All tests and analyses were performed

with SPSS version 12.0 (SPSS, Inc., Chicago, IL).

RESULTS

Species diversity

A total of 26 taxa were identified including 3

species of Cyanobacteria, 3 species of Chlorophyta,

4 species of Phaeophyta and 16 species of Rliodo-

phyta (Tables 1,2).

The number of species varied during the study

period and ranged from 25 (March 2011) to 12

(June 2011). Catenella nipae , Gracilaria salicor-

nia , Gelidium pusillum , Hydropuntia chang 'd. Hyp-

nea hamulosa , Kyrtutrix maculans , Laurencia

decumbents , Lyngbya majnscula , Peyssonnelia

rubra and Ulva clathrata were found throughout

the sampling period.

On the other hand, Brachytrichia quoyi, Chae-

tomorpha crassa , Cladophora sp., Dictyota dicho-

toma, Hydroclathrus clathratus , Padina australis ,

P. sanctae-crucis, Acanthophora spicifera , Bostry-

cia tenella , Centroceras clavulatum , Ceramium

flaccidum , Erythrotrichia sp ., Gelidiopsis intrica-

tum , Gracilariopsis irregularis, Neosiphonia sava-

tieri and Palisada papillosa had only single

occurrences in time.

Biomass and distribution pattern of marine

benthic algae in each season and site

Total marine macroalgal biomass gradually

increased from January to March, reached to the

peak in April (hot-dry season) with 59.50 g/m 2

dry weight and dramatically decreased in July

(rainy season) with 20.14 g/m 2 dry weight, and

then steadily increased from August to Decem-

ber, reaching to the peak again in November

(cool-dry season) with 55.46 g/m 2 dry weight.

The seasonality of macroalgae biomass at the site

was less uniform. During both dry and wet sea-

sons, Gracilaria salicornia and Hydropuntia

changii attained the maximum biomass mean

value at 29.51 g/m 2 dry weight and 14.82 g/m 2

dry weight, respectively.

Acanthophora spicifera , Hydroclathrus clathra-

tus and Padina sanctae-crucis had greatest biomass

during the cool-dry season, and less biomass during

the wet season. In contrast, Gracilariopsis irregu-

ralis , Hypnea hamulosa, and Padina australis exhi-

bited higher biomass during the hot-dry season than

in the wet season.

Most seaweed biomass exhibited greatest abun-

dance in Ao Clio e.g. Gracilaria salicornia, Graci-

lariopsis irreguralis, Hypnea hamulosa,

Hydropuntia changii, Palisada papillosa and Pa-

dina sanctae-crucis. Some species, e.g. Acantho-

phora spicifera, Hydroclathrus clathratus , Hypnea

hamulosa, Hydropuntia changii, Palisada papillosa

and Padina australis, were common in Ao Lane.

The brown algae, Padina australis and P. san-

ctae-crucis, however, were common in Laem Tien.

Some species, e.g., Gracilaria salicornia, Hypnea

hamulosa, and Palisada papillosa were common in

Laem Sok. In general, there were no patterns found

in biomass of algae among different sites.

Ten species were found throughout the entire

study period. These included two species of cyano-

bacteria, Kyrtutrix maculans, Lyngbya majnscula,

one species of green algae, Ulva clathrata, seven

species of red algae, Catenella nipae, Gracilaria

salicornia, Gelidium pusillum, Hydropuntia chan-

gii, Hypnea hamulosa, Laurencia decumbents and

Peyssonnelia rubra.

232

N. Petsut, A. Chirapart & M. Keawnern

Ao Cho

Ao Lane

TAXA

CYANOBACTERIA

Brachytrichia quoyi (Agardh) Bomet

et Flahault

Kyrtutrix maculans (Gomont) Ume

zaki

Lyngbya majuscula (Dillwyn) Harvey

CHLOROPHYTA

Chaetomorpha crassa (C. Agardh)

Kiitzing

Cladophora sp. Kiitzing

Ulva clathrata (Roth) C. Agardh

-i-

PHAEOPHYTA

Dictyota dichotoma (Hudson)

Lamouroux

Hydroclathrus clathratus (C.Agardh)

M. A. Ho we

Padina australis Hauck

Padina sanctae-crucis Borgesen

RHODOPHYTA

Acanthophora spicifera (M. Vahl)

Borgesen

Bostrycia tenella (J.V. Lamouroux)

C.Agardh

Catenella nipae Zanardini

Centroceras clavulatum (C.Agardh)

Montagne

-i-

Ceramium flaccidum (Harvey ex

Kiitzing) Ardissone

Erythro trichi a sp. Areschoug

Gelidiopsis intricatum (C.Agardh)

Vickers

Gelidium pusillum (Stackhouse)

Le Jolis

Gracilaria salicornia (C.Agardh)

E.Y. Dawson

Gracilariopsis irregularis Abbott

Hydropuntia changii (Xia et

Abbott)Wynne

Hypnea hamulosa (Esper)

J.V. Lamouroux

Laurencia decumbents Kiitzing

Neosiphonia savatieri (Hariot)

M.S.Kim

-!-

-h

Palisada papillosa (C.Agardh)

K.W.Nam

Peyssonnelia rubra (Greville)

J. Agardh

Table 1. Seasonality of macroalgae at Trat Peninsula January (=1)/December (=12) 2011: Ao Cho and Ao Lane.

A stability assessment on seasonal variation of seaweed beds in the Trat peninsula ofThailand

233

Laem Tien

Laem Sok

TAXA

1 2 3 4 5 6 7 8 9 10 11 12

CYANOBACTERIA

Brachytrichia quoyi (Agardh) Bomet

et Flahault

Kyrtutrix maculans (Gomont) Ume

zaki

Lyngbya majuscula (Dillwyn) Harvey

CHLOROPHYTA

Chaetomorpha crassa (C.Agardh)

Kiitzing

Cladophora sp. Kiitzing

Viva clathrata (Roth) C.Agardh

PHAEOPHYTA

Dictyota dichotorna (Hudson)

Lamouroux

Hydroclathrus clathratus (C Agardh)

M. A. Howe

Padina australis Hauck

Padina sanctae-crucis Borgesen

RHODOPHYTA

Acanthophora spicifera (M. Vahl)

Borgesen

Bostry’cia tenella (J.V. Lamouroux)

C.Agardh

Catenella nipae Zanardini

Centroceras clavulatum (C.Agardh)

Montagne

Ceramium flaccidum (Harvey ex

Kiitzing) Ardissone

Erythrotrichia sp. Areschoug

Gelidiopsis intricatum (C.Agardh)

Vickers

Gelidium pusillum (Stackhouse)

Le Jolis

Gracilaria salicornia (C.Agardh)

E.Y.Dawson

Gracilariopsis irregularis Abbott

Hydropuntia changii (Xia et

Abbott)Wynne

Hypnea hamulosa (Esper)

J. V. Lamouroux

Laurencia decumbents Kiitzing

Neosiphonia savatieri (Hariot)

MS. Kim

Palisada papillosa (C.Agardh)

K. W.Nam

Peyssonnelia rubra (Greville)

J.Agardh

+ +

+ + +

”h

+ +

+ + + + + + + + + + + +

+ + + +

+ + + + +

4 - +

+ + + +

+ + + + + + +

+ +

+ + +

+ + + + + + +

+ +

+ + + + + +

+ + + + + + + + + + + +

Table 2. Seasonality of macroalgae at Trat Peninsula January (=1)/December (=12) 2011: Laem Tien and Laem Sok.

234

N. Petsut, A. Chirapart & M. Keawnern

Physical and chemical factors study

There were insignificant variations in water

temperature (p>0.05) among sites but significant

variations in water temperature (p<0.05) among

months. The water temperature was 27.5-33.5°C

during the dry season and 25.5-3 1.5°C during the

rainy season. The range was rather wide and was

likely to influence the species diversity, biomass

and distribution pattern of seaweed beds. In addi-

tion, there were insignificant differences in salinity

(p>0.05) among sites but significant differences in

salinity (p<0.05) among months. The salinity du-

ring the dry season was 32-37 %o and 15-27 %o du-

ring the rainy season.

Such a rather wide range was likely to in-

fluence the marine macroalgae. There were insi-

gnificant differences in turbidity (p>0.05) among

sites but significant variations in turbidity (p<0.05)

among months. The turbidity was 4.70-346.67

NTU during the dry season and 10.33-983.33 NTU

during the rainy season. These differences could

influence the species diversity, biomass and distri-

bution pattern of marine algae

ANOVA revealed that there were insignificant

variations in P0 4 3 ' (p>0.05) and TIN (total inor-

ganic nitrogen: NH 4 + + N0 3 ~ + N0 2 ) (p>0.05)

among sites but significant variations in P0 4 3 '

(p<0.05) and TIN (p<0.05) among months. The

phosphate during the dry season was 0.0004-

0.0391 mg/1 and 0.0030-0.0670 mg/1 during the

rainy season. And the TIN was 0.0134-0.2642

mg/1 during the dry season and 0.0343-0.2800

mg/1 during the rainy season. These ranges were

rather wide, and were likely to influence the ma-

rine macroalgae.

DISCUSSION

Species diversity study

A total of 25 genera and 26 species of marine

benthic algae were recorded, of which 16 species

of red marine algae (a characteristically abundant

and diverse group in the tropics) were the most as-

sorted. Red algae occupy a wide range of irra-

diance environments, including high-latitude and

high- intertidal habitats subjected to long periods

of full sunlight (Graham et al., 2009).

Twenty-four percent higher species richness of

marine algae was found at our study site compared

to the study of Laehyeb (2011), in which only 21

species were reported throughout Trat peninsula;

only three field collections were made in that pre-

vious study as compared to the four field collec-

tions in this study. Thus, the number of visits for

field collection as well as the collection efforts

could be important for appraising species diversity

more accurately. In addition, the differences we

observed suggested that there was temporal varia-

tion in species diversity of marine algae.

Many marine macroalgae have posed ecologi-

cal problems in some marine ecosystems, which is

probably due to environmental changes linked to

decreasing of mangrove forest, sewage discharges,

shrimp culture, tourism and factories activities

(Doydee, 2005; Thongroy et al., 2007; Laehyeb,

2011). These activities have had serious impact on

coastal environments.

Biomass and distribution pattern study

Among all four study areas of Trat peninsula,

marine macroalgal biomass and diversity were

the highest at Ao Cho during the dry season. This

area is semi-exposed, sandy bottom with rocks

and partly surrounded by mangroves. This same

phenomenon was observed in macroalgae at Si-

rinart Marine National Park by Prathep (2005) in

Thailand. Water motion is one of the most impor-

tant variables influencing marine macroalgae, be-

cause it regulates turbidity, light penetration and

nutrient availability (Nishihara & Terada, 2010;

Kang et al., 2011).

At Ao Cho, marine macroalgae were exposed

to intermediate levels of water motion, which al-

lows the exchange of gases and uptake of nutrients

(Lobban & Harrison, 1994; Kang et al., 2011). Ao

Lane is a semi-exposed area as same as Ao Cho

but is characterized by large mudflats and harbours

a lot of fishery communities. This place is very

sensitive to environmental changes due to human

activity stressing the natural environment, such as

sewage discharges of fishery communities, which

can cause the decrease of the species diversity and

of seaweed abundance. Laem Tien is a wave-shel-

tered area covered by mangroves with a large

muddy sand bottom. Some parts of this place are

used for aquaculture.

A stability assessment on seasonal variation of seaweed beds in the Trat peninsula ofThailand

235

This site showed the lowest biomass and spe-

cies diversity. Taking into account that the area is

rather sheltered from wave action, marine macro-

algae may be exposed to some physiological

stress due to limited circulation of nutrients and

gas exchange (Prathep & Tantiprapas, 2006;

Thongroy et al., 2007).

In addition, this site is subjected to environ-

mental changes because of water pollution from

the shrimp farms. Laem Sok is a wave-exposed

area with a large rocky shore habitat and many re-

staurants nearby the harbor. This place shows a

high level of water motion, which is likely to affect

species diversity and abundance of macroalgae

(Prathep, 2005; Kang et al., 2011). In addition, in

this area mangrove forests decreased in the last

few years (Doydee, 2005; Laehyeb, 2011).

Generally speaking, mangroves are really im-

portant since these plants indirectly participate to

habitat complexity and diversity of fauna and

flora, particularly marine macroalgae (Ashton et

al., 2003; Ellison, 2008, Doydee & Buot, 2011).

In fact by trapping nutrients and sediments

from river runoffs from the uplands and transpor-

ting them to coastal waters (Anongponyoskun &

Doydee, 2006; Ellison, 2008; Doydee, 2009) they

contribute to improve shoreline stability and

water quality. Therefore, the decrease of man-

grove forests is certainly another reason affecting

negative changes in species diversity and abun-

dance of seaweed.

ACKNOWLEDGEMENTS

We thank the Japan International Research

Center for Agricultural Sciences for partial finan-

cial support. Mr. Narongrit Muangmai for the in-

valuable editorial advice and Mr. Jiraweath Petsut

for assistance with the field work.

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Biodiversity Journal, 2012, 3 (3): 237-242

Freshwater and brackish “oasis” fauna in the deep Black

Igor P. Bondarev

Benthos Ecology Department, Institute of Biology of the Southern Seas (IBSS), Ukrainian National Academy of Sciences

(NASU), Nakhimov av., 2, Sevastopol, 99011, Ukraine; email: igor.p.bondarev@gmail.com

ABSTRACT Present paper reports on the possible existence of recent freshwater fauna in the Black

Sea. Based on information available from malacology, ecology, paleontology, stratigraphy,

hydrogeology and observations in situ, the presence of freshwater biota on the shelf and

continental slope is discussed, including the existence of aerobic life forms in the Black

sea deep-water cavity.

KEY WORDS Aerobic; Biodiversity; Ecosystem; freshwater; submarine springs.

Received 03.08.2012; accepted 03.09.2012; printed 30.09.2012

INTRODUCTION

The Black Sea is a very specific marine basin

with anaerobic water mass spreading from the ma-

ximal bottom depth (more than -2200 m) to about -

200 m. This water thickness is valuated as about

85% of the whole Black Sea water volume (Zaitsev,

2006) and suggested as absolutely unfit for euka-

ryotic life (Vinogradov, 1997).

The Black Sea water salinity varies from about

17-18%o on the inner shelf till 23%o in the deepest

basins’ parts (Sorokin, 1982) which excludes any

possibilities for freshwater biota inhabitance. Any-

way, the possibility of existence of aerobic life

"oases" related to fresh groundwater springs in sul-

fured hydrogen zone was hypothesized, taking into

account a few unusual faunistic findings, signs "of

island" speciation (Zaika, 2008).

Additionally, on the Black Sea continental shelf

bottom surface were repeatedly found out the shells

of several gastropod mollusk species typical of fre-

shwaters or brackish complexes (ITina, 1966; Go-

likov & Starobogatov, 1972; Chukhchin, 1984).

Most of these species - met nowhere else and de-

scribed as extinct - supposedly re-deposited from

ancient (Neoeuxinian) sediment layers formed in

much more freshwater environmental conditions

(Golikov & Starobogatov, 1972). However, among

the above-mentioned gastropods, only one ( Theo -

doxus pallasi Lindholm, 1924) is known for certain

from Neoeuxinian sediment deposits.

During the R/V «Maria S. Merian» (Leibniz In-

stitute for Baltic Sea Research, Germany) expedi-

tion, which was conducted in the Black Sea within

the framework of the European project HYPOX in

2010, a live gastropod mollusk was sampled at the

depth of 250 m (Sergeeva et al., 2011). If one be-

lieves that its presence in anoxic zone may be not

casual, then it is necessary to admit the existence of

oxygen input into the sulfiired hydrogen water layer

by sources which serve as freshwater springs.

The finding of meiobenthic crustaceans in the

deep Black Sea (around -2000 m) and at a depth

of 174 m (Korovchinsky & Sergeeva, 2008) may

be considered as one of the biological and ecolo-

gical proofs of the existence of aerobic fauna in

anaerobic zone. In 1986, during a test diving on

the submarine inhabited vehicle of the USSR

Navy at a depth of 600-640 m in the Yalta canyon

at bottom, one "oasis" of aerobic life was found

238

Igor P. Bondarev

out (Prof. Gevorkyan V.Kh. personal report); this

information was under secret for a long time and

therefore never published. The most credible reason

for the existence of such an "oasis" is the occur-

rence of a zone of stable and powerful submarine

unloading of oxygen-rich groundwaters.

Oceanological and geological researches confir-

med the presence of submarine discharge of fresh

water zones on the Black Sea continental shelf and

slope (Trotsyuk et af, 1988; Shnyukov & Ziborov,

2004). Actually, these zones can create proper con-

ditions for the existence of freshwater or brackish

biota, both in aerobic and in anaerobic water masses

of the Black Sea.

The aim of the present research, based on geo-

logical, biological and ecological data, is to investi-

gate the existence of specific biocenoses in the

Black Sea, related to the zones of the submarine un-

loading of freshwaters. A discovery and description

of such a biocenosis would extend knowledge about

the Black Sea biodiversity and give new ideas about

possible ways of the “oasis” fauna evolution.

DISCUSSION

Geological and oceanological evidence

Submarine freshwater springs are known from

many regions. Very recently, a Max Plank Institute

science troop found rich bacterial life connected

with freshwater springs even in the Dead Sea (Io-

nescu et af, 2012). Black Sea is also suitable for se-

arching submarine sources of freshwater. On

geological terms it is possible to distinguish three

basic types of submarine sources of groundwater

unloading: artesian, karstic and waters of subriver-

bed flow (Shnyukov & Ziborov, 2004).

Data on the dynamics of the artesian pools’

groundwater opened toward the Black Sea, testily

movements of different hydrogeological floors. Ac-

tually these pools embrace all coastline of the Black

Sea (Shnyukov & Ziborov, 2004). Submarine

springs issued from the limestone massifs or other

kinds of karsting rocks are widely spread in the

Black Sea.

Researches, managing with submarine inhabited

vehicles, showed the presence of numerous rocky

outcrops from the bottom silty-mud sediments

cover on a narrow and steep continental shelf and

slope of south Crimea (Bondarev, 2008; 2009).

Oceanological researches in 37 th voyage R/V

“Academician Vernadsky” showed submarine un-

loading of karsting-crack waters in head parts of

many Crimean submarine canyons. The hydroche-

mical tests of near- bottom water allowed to set

that in canyons salinity is lowered notably up to

12, 14, 15, 17%o (with reference to base-line va-

lues of 21-22%o). Particularly, the desaltation of

salt waters on the canyons bottom was found out

on the continental slope of Turkey, north of Kef-

ken Island and on the extreme north-west of the

Turkish shelf (at 300-500 m below the sea

level;13-17%o). Signs of desaltation were found

also in the canyons of north-west Black Sea

(Shnyukov & Ziborov, 2004).

Use of impermeable water samplers, vacuum

degassing and chromatographic analysis allowed to

set the presence of solved oxygen in the benthic

layer of deep-water part of the Black Sea. In the

area adherent to the estuarine part of Danube, oxy-

gen in benthic water decreases from 4.2 ml/1 in an

off-shore zone practically to zero on the shelf edge.

As recorded in eight near-bottom samples taken at

different depths on the bottom and on the sides of a

deep canyon up to 1340 m of depth, below the

slope, up to the distal part of canyon fan, oxygen

amount ranges from 0.3 to 1.6 ml/1. On the Anato-

lian side (the cone of dejection of Kyzil-Irmak

river) water-solved oxygen was found out in two

deep-water stations with bathymetric marks -2064

m and -2003 m, respectively. Measured oxygen

concentrations were 0.5 and 0.7 ml-1. At depths of

over 2000 m, near-bottom waters contained oxygen,

as revealed by tests from the districts of western ha-

listaza zone, interhalistaza zone and the east hollow

of the Black Sea (Trotsyuk et af, 1988).

Major part of water samples containing oxygen

was collected in submarine canyons or in the sur-

roundings where the underground source of aerobic

freshwaters binds to the submarine unloading. All

these features do suggest the presence of specific

freshwater aerobic biocenoses in the Black Sea is

to be considered highly probable.

Biological and ecological evidence

Shells of gastropod molluscs of freshwater or

brackish habitats were discovered on continental

shelf and slope of the Black Sea (Golikov & Staro-

Freshwater and brackish “oasis” fauna in the deep Black Sea

239

bogatov, 1972), where water salinity is 19-21%o.

Their list (Table 1) was recently filled up by one

specimen of living gastropod from the near-Bospo-

rus region, where background water salinity exce-

eds 22%o. Neritidae and Hydrobiidae mostly

consist of marine species.

ditions, these shells should be absent. In addition,

these shells are found in the middle and external

part of shelf and are absent in littoral zone.

These circumstances and the sub-fossil state of

seashells allowed to suppose they to origin from

more ancient layers, maybe formed in a freshwater-

Taxa

Locality / inhabitance (after Kantor & Sysoev, 2006, others

indicated)

Fam. Neritidae:

Theodoxus milachevitchi Golikov

et Starobogatov, 1966

Theodoxus pallasi Lindholm, 1924

Crimea offshore/ recent mud, depth 20-60 m Black Sea Ne

oeuxinian, Vityazean & Kalamitian layers, recent muds on

the depth 18-158 m (Author’s data)/Aral & Caspian Seas,

very freshened littoral spots in the Azov Sea (Golikov &

Starobogatov, 1972); rivers of Ural Mountains and Armenia

Fam. Flydrobiidae, Subfam. Pyrgulinae:

Caspia valkanovi (Golikov et Starobogatov, 1966)

Crimea offshore, silt on the 20 m depth

Caspiohydrobia sp.

Near-Bosporus region, mud on the depth of 250m (Author’s

data)

Turricaspia crimeana (Golikov et Starobogatov, 1966)

Crimea, 15 m

Turricaspia iljinae (Golikov et Starobogatov, 1966)

Crimea offshore, mud on the 80- 180 m depth

Turricaspia lirata marisnigri Starobogatov, in Alexeenko

et Starobogatov, 1987

Crimea, Modiolula phaseolina (Philippi, 1844) contained

mud.

Turricaspia nevesskae (Golikov et Starobogatov, 1 966)

Crimea offshore, mud on the 80- 180 m depth

Table 1. List of freshwater and brackish water gastropods found on the shelf and continental slope of the Black Sea.

However the genus Theodoxus Monfort, 1810

comprises species dwelling exceptionally in fresh

or strongly refreshing (up to 5%o) waters of Eura-

sia. This characteristic allows to use them as bioin-

dicators of freshwater environments (Goodwin,

2006). The Subfamilia Pyrgulinae Brusina, 1882

also includes genera and species from freshwaters

(springs, rivers and lakes) of Europe and front Asia

(Anistratenko, 1998).

A considerable part of these species inhabits

brackish seas - Aral and Caspian. In the Azove-

Black Sea basin the subfamily is represented by

three genera whose species are usually encountered

in the brackish zones of estuaries and rivers (Goli-

kov & Starobogatov, 1972; Kantor & Sysoev,

2006). Hence, substantial differences in water sali-

nity of sampling locations and in typical habitats of

mollusk species led to hypothesize a possible intro-

duced origin of shells from a freshwater environ-

ment. But, in that case, in the southern part of

Crimea littoral, where there are special habitat con-

like environment (Golikov & Starobogatov, 1972).

Such environmental conditions existed in a Neoeu-

xinian period of the Black Sea evolution (IEina,

1966); Neoeuxinian layers on the shelf of Crimea

are covered by more young ground sedimentations,

from 1 to 4 m thick (Shcherbakov et al., 1978).

Moving of shells through such a thick layer by

means of natural processes is hardly plausible. But

even if we assume such a possibility, then in Neo-

euxinian deposits these species should be much

more abundant than in recent sediments. However,

species reported in Table 1 were found only in re-

cent bottom deposits, with the exception of Theo-

doxus pallasi.

This species is the only one that is really cha-

racteristic for Neoeuxinian layers whereas in later

deposits is quite rare. It is has been reported that

shells of T. pallasi from recent bottom deposits have

better saved surface and color pattern compared to

those from Neoeuxinian sediments (IEina, 1966;

Golikov & Starobogatov, 1972).

240

Igor P. Bondarev

In our samples there is one T. pallasi subfossil

specimen from a depth of 158 m from the recent

bottom sediment of near-Bosporus region (Fig. 1).

Maintenance of colouring of the shell testifies its

relatively recent fossilization. Available data allow

to suppose that the shells of the freshwater species

complex discovered on Black Sea shelf belong to

recent living species inhabiting within the limits of

the freshwaters biotopes.

In 2010, during the Black Sea international ex-

pedition of R/V "Maria S. Merian" (Leibniz Institute

for Baltic Sea Research, Germany) in a near-Bospo-

rus region on a depth of 250 m, a live specimen, be-

longing to the genus Caspiohydrobia Starobogatov,

1970, was collected (Fig. 2). As at this depth in the

Black Sea there are anoxic conditions, it was hypo-

thesized that the animal had been rescued only by

chance (Sergeeva et al., 2011). However if we admit

the existence of specific aerobic freshwater fauna in

Figure 1. Subfossil of Theodoxus pallasi , shell height: 5.8

mm, width: 7 mm, Bosporus region, depth 158 m, R/V

"Maria S. Merian", 2010.

Figure 2. Live-collected Caspiohydrobia sp. (soft parts co-

lored with “Bengal rose”), shell height: 3.4 mm, Bosporus

region, depth 250 m, R/V "Maria S. Merian", 2010.

the depths of the Black Sea, then the location of this

mollusk corresponds to the biotope formed by a sub-

marine unloading of freshwaters.

In 1986, during test dive of submarine inhabited

vehicle of the USSR Navy in the Yalta canyon at a

depth of 600-640 m. Dr. Gevorkyan (personal

comm.) looked at one "oasis" of eukaryotic suppo-

sedly aerobic life. The biotope was characterized by

unusually clear (for the Black Sea) water because

of the absence, in the water column, of the charac-

teristic particles of organic suspended debris

(known as "marine snow"). On the outcropped

rocks macrobenthos forms did remind hydroids.

The most notable detail of the biota was the occur-

rence of fishes, exceeding 20 cm in size. The most

likely hypothesis for the presence of such a biotope

and a biocenosis is the possible existence of a po-

werful submarine spring of aerobic waters, stably

existing since a long time.

Notably, generally speaking, strategy of repro-

duction [laying eggs attached to the substratum

and non pelagic development, (see Chukhchin,

1984; Anistratenko, 1998,] and early ontogenesis

peculiarities of these mollusks allow them to exist

within the limits of localized biotopes showing pa-

rameters contrasting with those of surrounding en-

vironments. Another important ecological

characteristic for allowing species to inhabit the

deep Black Sea is the resistance to hypoxia. Hy-

drobiidae comprise mollusks adapted to the lack

of oxygen (Chukhchin, 1984), and the specimen

of Caspiohydrobia sp. discovered at a -250 m of

depth belongs to this family. In 2002, during the

international expedition on R/V Meteor (Ger-

many) to two stations in the north-western part of

the Black Sea at the depths of 1900 m and 2190

m, respectively, it was discovered a meiobenthic

crustacean species unknown to science. The same

species was found out in 2003 in an expedition on

R/V “Yantar” (Russia) in north-eastern part of the

Black Sea at a 171 m of depth. The specimen (Cla-

docera: Ctenopoda) allowed to describe a new spe-

cies, Pseudopenilia bathyalis Sergeeva, 2004 and

a new respective genus taxon. Consequently, also

the Pseudopenilidae family Korovchinsky & Ser-

geeva, 2008 was described.

Hydrochemical analyses of near-bottom water

in a deep-water place of sampling of Pseudopenilia

bathyalis showed the presence of sulfiired hydrogen

in an amount of 4-12 ml/1 at a salinity of 22-23%o.

Freshwater and brackish “oasis” fauna in the deep Black Sea

241

However, finding out this crustacean species at a

depth of 171 m in the hypoxia zone allows to sup-

pose that we deal with an aerobic organism adap-

ted to oxygen-deficit conditions.

Places of submarine water unloading are local

phenomena in the Black Sea. Their spatial charac-

teristics and stability in time could be substantially

differentiated depending on sources regime. For

example, water supplement varies seasonally and

may lead to a temporary stop of unloading.

Characters of water springs related to the arte-

sian layers are more stable. In addition, salt and sol-

ved gases composition may be different. Spatial

structure of freshwater biotope can change as a re-

sult of dynamic influences of the surrounding water

masses. The innate structure of such biotopes can

be non-homogeneous, thus including several biota

that differently react to presence/absence of oxygen

and of refreshing/salting waters. Hence biotopes

and biocenoses of submarine unloading zones may

be extremely heterogeneous, various and very vul-

nerable ecosystems.

CONCLUSIONS

The existence of aerobic life in the deepest part

of the Black Sea is traditionally contested and even

denied (see Vinogradov, 1997). On the contrary,

the present paper strongly supports the hypothesis

reporting several evidence on the issue, including

the occurrence of the endemic Pseudopenilidae fa-

mily (Korovchinsky & Sergeeva, 2008) which

suggests the evolutionally-long existence of spe-

cific fauna in the deep Black Sea. Probably, a fre-

shwater relict fauna could have existed not only

from Neoeuxinian time (27-10 thousand years

ago) but also earlier.

In fact, the existence of submarine freshwaters

springs is independent from the change of sea sa-

linity levels and quantitative and quality composi-

tion of this fauna may have undergone

transformation during time, depending also on the

changes of sea salinity. Oceanological and hydro-

geological researches (Shnyukov & Ziborov, 2004;

Trotsyuk et af, 1988) reported on desalted waters

in near-bottom layers from tide-mark to deep-

water cavity bottom of the Black Sea. The general

volume of the submarine discharge in the Black

Sea is only approximately estimated. However, di-

scharge volumes calculated for single areas show

that this volume is ecologically significant. For

example, only for the Crimean coast from Bala-

klava to Simheiz (less than 50 km), karst submarine

springs were appraised as about 700 thousand

m 3 /day (Shnyukov & Ziborov, 2004). The same au-

thors assessed the volume of subriver-bed flow as

1/3 of the volume of river flow. At the moment,

water unloading in submarine canyons, although

being demonstrated as a fact (Shnyukov & Ziborov,

2004), has not been calculated yet (not even preli-

minarily). The process of the submarine unloading

can and must have ecological consequences.

This paper aims at not only discussing and con-

tributing to a deeper knowledge of the refinement

of the Black Sea biodiversity and of the recent

state of the ecosystem, but also encourages the re-

vision (by several colleagues) of some other

aspects of the natural history of this ecosystem.

ACKNOWLEDGEMENTS

The Author is thankful to the Dr Gevorkyan

V.Kh. (Institute of Geological Sciences NASU,

Kyiv) for his personal communications and to Dr.

Sergeeva N.G. (IBSS, NASU, Sevastopol) for ha-

ving allowed the examination of macrobenthos

samples collected in the expedition of R/V "Maria

S. Merian"(Leibniz Institute for Baltic Sea Rese-

arch, Germany) in 2010.

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Biodiversity Journal, 2012 , 3 ( 3 ): 243-246

Description of two new species of Carabus Linnaeus, 1 758

from China (Coleoptera Carabidae)

Ivan Rapuzzi

Via Cialla n. 47 - 33040 Prepotto (UD), Italy; email: info@ronchidicialla.it

ABSTRACT In the present paper two new species of Carabus Linnaeus, 1 758, subgenus Apotomopterus

Hope, 1838, are described and figured: Carabus (Apotomopterus) francottei n. sp. and Ca-

rabus (Apotomopterus) eccoptopteroides n. sp., comparative notes with the related taxa

are provided.

KEY WORDS Coleoptera; Carabidae; Carabus ; Apotomopterus , new species; China.

Received 28.08.2012; accepted 14.09.2012; printed 30.09.2012

INTRODUCTION

In terms of number of species the subgenus Apo-

tomopterus Hope, 1838 is the largest subgenus of

the genus Carabus L., 1758. The subgenus is wide-

spread in Southeast China and adjacent Countries,

in many places several species are sympatric

(Deuve, 1997a, 1997b; Kleinfeld, 2009).

In the last decades thanks to the investigation

of new or less known areas a large number of new

species and subspecies was described (Kraatz,

1894; Boileau, 1896; Breuning, 1931, 1932-1936,

1950; Hauser, 1932; Deuve, 1991, 1995, 1997a,

1997b, 2001, 2002; Brezina, 2003; Deuve, 2004;

Lassalle, 2006; Deuve & Li, 2009; Kleinfeld, 2009;

Deuve, 2012a, 2012b).

The examination of some Apotomopterus speci-

mens from North Guangdong and South Sichuan

provinces in Southern China allowed to identify

two new species described herein.

Carabus (Apotomopterus) francottei n. sp.

Examined material. Holotypus male (Fig. 1),

China, North Guangdong province, Mts. Nanling

Shan, VI. 2009. The holotypus is deposited in the

author’s collection. Paratypus: 1 male, same data as

holotypus. The paratypus is deposited in the au-

thor’s collection.

Description of Holotypus male. Length inclu-

ding mandibles: 33 mm, elytral width: 10.7 mm.

Color black with very few metallic luster brownish-

copper on dorsum and pronotum, mat.

Head moderately thickened. Frontal impres-

sions deep and rugose, exceeding anterior margin

of eyes; vertex slightly convex, surface of the ver-

tex slightly punctured and rugulose; short neck.

Surface faintly punctulate and rugulose. Mandi-

bles moderately long, strong, and regularly cur-

ved. Palpi long, penultimate segment of labial

palp multisetose (3-4). Eyes very convex and pro-

minent. Antennae very long extending of 5 V 2 an-

tennomeres pronotal base and extending the

second half of elytra. Pronotum very large and si-

nuate, transverse, about 1.34 times as broad as

long, slightly convex; sides of pronotum narrow

margined, slightly bent upwards; hind angles sli-

ghtly protruding behind its base; surface of pro-

notum uniformly punctured; basal depressions

large, roughly punctured.

Elytra elongate, sub-parallel sides, slightly

emarginated at apex, moderately convex, maximum

width behind middle; shoulders rather large and

244

Ivan Rapuzzi

rounded; sculpture triploid homodyname, intervals

uniformly convex, only the primary interrupted in

the row in quite long links by small foveae, not

punctured striae. Male aedeagus (Figs. 2, 3) small,

regular curved; apical half slightly thickened, a

little sinuate on the ventral side; apex a little nar-

rowed spatulate.

Variability. No variability of paratypus. Body

length 3 1 mm.

Etimology. The new species is cordially dedi-

cated to Dr. Auguste Francotte (Liege, Belgium) na-

turalist and specialist of Coleoptera Cerambycidae,

my friend from many years.

Comparative notes. The new species is closely

related with the sympatric C. (Apotomopterus) sau-

teri nanlingensis Deuve et Tian, 1999, but easy to

be distinguished by the following characteristics

(Deuve & Tian, 1999): larger and more sinuate pro-

notum; homodyname triploid sculpture of elytra

with very regular intervals; larger and flat elytra;

different color of elytra and pronotum; larger and

curved median lobe of aedeagus.

Carabus (Apotomopterus) eccoptopteroides n. sp.

Examined material. Holotypus male (Fig. 4),

China, South Sichuan province, Pu-Ge County,

Lianxiang, Kakaliangzi, 1/11. VI. 2012. The holoty-

pus is deposited in the author’s collection. Paratypi:

18 females, same data as holotypus. The paratypi

are deposited in the author’s collection.

Description of Holotype male. Length inclu-

ding mandibles: 36 mm, elytral width: 11 mm.

Color black with very faint cupper luster on dorsum

and pronotum, mat. Legs, antennae and palpi black.

Head of normal shape, neck quite narrow, eyes

small and slightly prominent. Flat vertex with a

raised polish trilobate plate, the rest of the surface

of the vertex rugulose. Mandibles short and stout.

Palpi thin and very long, labial palp bi or three se-

tose. Antennae long and thin, extending with 5 A

antennomeres beyond pronotal base and extending

the apical half of elytra. Pronotum rounded, sli-

ghtly transverse, about 1.18 times as broad as

long; disc of pronotum slightly convex; sides of

pronotum very narrow margined, not bent up-

wards; hind angles very short, slightly protruding

behind its base; surface of pronotum thin punctu-

red; basal depressions small and not deep. Elytra

very elongate, narrow, oval, moderately convex,

maximum width just behind the middle; shoul-

ders very narrow and rounded; sculpture triploid

homodyname, intervals uniformly convex, with

the primaries cut into quite long segments by

small fovea; not punctured striae. Male aedeagus

(Figs. 5, 6) very elongate, basal and median por-

tion rectilinear and sub-cylindrical, apical portion

strongly curved and very elongated; apex large

and rounded.

Variability. Only females: the length of the

body ranges from 36 mm to 43 mm. Pronotum more

or less transverse: from 1.16 to 1.26 times as broad

as long. Elytra very long, very narrow, rather con-

vex, with very strong preapical emargination, the

posterior angles are acuminate and very protruding,

forming a sharp tooth. The apical half of elytra is

marginated and bent upwards.

Etimology. The given name wants to indicate

the morphological vicinity of the present new

species with C. (Apotomopterus) eccoptopterus

Kraatz, 1894.

Comparative notes. C. (Apotomopterus) ec-

coptopteroides n. sp. is related with several Apo-

tomopterus species: C. (A.) aeneocupreus

Hauser, 1932; C. (A.) benardi^QxQxxmng, 1931; C.

(A.) eccoptopterus Kraatz, 1894; C. (A.) keithi

Deuve, 1995; C. (A.) piriformis Deuve, 1997 but

easy separable by the following characters (Kra-

atz, 1894; Breuning, 1931; Hauser, 1932; Deuve,

1995, 1997b):

eccoptopterus : the new species is similar by the

very elongate shape of body but differs by the stron-

gly punctured pronotum, stronger preapical emar-

gination of females elytra and by the shape of

aedeagus strongly curved at the apical portion.

keithi'. the new species differs by the larger size,

strongly punctured pronotum, stronger preapical

emargination of females elytra and by the shape of

aedeagus strongly curved at the apical portion.

benardi : the new species is very different for

the much more elongate body, the more convex

elytra with very regular sculpture and the faintly

punctured pronotum.

piriformis', the new species differs for the more

elongate body, the more regular sculpture of elytra,

the faintly punctured pronotum and the shape of ae-

deagus more strongly curved at the apical portion.

245

Description of two new species of Carabus Linnaeus, 1 758 from China (Coleoptera, Carabidae)

Figure. 1. Carabus (Apotomopterus) francottei n. sp. holotypus. Figures. 2, 3. idem, male edeagus lateral view (Fig. 2)

and frontal view (Fig. 3). Figure. 4. C. (A.) eccoptopteroides n. sp. holotypus. Figures. 5, 6. idem, male edeagus lateral

view (Fig. 5) and frontal view (Fig. 6). Figure. 7. C. (A.) eccoptopteroides n. sp. paratypus female.

REFERENCES

Boileau H., 1896. Description d’un Carabe nouveau. Le

Naturaliste, 18: 203-204.

Breuning S., 1931. Cinq nouvelles formes de Carabini.

Buletin du Museum D’Histoire Naturelle de Paris.

(2), III: 620-623.

Breuning S., 1932-1936. Monographic der Gattung Ca-

rabus L. Bestimmungs-Tabellen der europaischen

Coleopteren. Troppau, 1610 pp.

Breuning S., 1950. Einige neue Arten und Rassen der

Gattungen Carabus und Cychrus aus Ostasien. Ento-

mologische Arbeiten aus dem Museum G Frey Tut-

zing Bei Muenchen, 1 : 198-201 .

Brezina B., 2003. World Catalogue of the Genus Carabus

L. Pensoft, Sofia-Moscow 1999: 170 pp.

246

Ivan Rapuzzi

Deuve Th., 1991. Descriptions et diagnoses de nouve-

aux Coleopteres Carabidae asiatiques. L’Entomolo-

giste, 47: 13-27.

Deuve Th., 1995. Contribution la connnaissance taxo-

nomique des Geners Carabus et Cychrus en Asie.

Revue frangaise d’Entomologie (NS), 17: 69-76.

Deuve T., 1997a. Catalogue des Carabini et Cychrini de

Chine. Memories de la Soc. Ent. France, 1 : 236 pp.

Deuve T., 1997b. Nouveaux Carabus L. et Cychrus F.

de la Chine, de l’Asie Centrale et de la Turquie

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Deuve T. & Tian M., 1999. Diagnoses preliminaries

de nouveaux Carabus L. de Chine meridionale.

Coleopteres, 5: 139-147.

Deuve T., 2001. Noveaux Carabus L. et Cychropsis

Boileau de Chine, de Birmanie et d’lran. Coleopte-

res, 7: 49-61.

Deuve T., 2002. Noveaux Carabus L. de la Chine du

Sud-Ouest, de l’lran et de la Coree. Coleopteres,

8: 219-231.

Deuve T., 2004. Illustrated Catalogue of the Genus Ca-

rabus of the World (Coleoptera, Carabidae). Pen-

soft. Sofia-Moscow, 461 pp.

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Carabus L., 1758. Liste Blumenthal 2011-2012. As-

socation Magellanes - Andresy - France.

Deuve T., 2012b. Description d’un nouvel Apotomop-

terus du Sichuan (Coleoptera, Carabidae). Coleop-

teres, 18: 13-16.

Deuve T. & Li J., 2009. Nouveaux Carabus de Chine et

de Coree et confirmation de la validite specifique de

Carabus (Carabus) cartereti Deuve, 1982 (Cole-

optera, Carabidae). Coleopteres, 15: 1-12.

Hauser G., 1932. Zwei neue Arten der Untergattung

Apotomopterus. Mitteilungen der deuthschen ento-

mologischen Gesellschaft, 3: 75-77.

Kleinfeld F., 2009. Apotomopterus . Monographische

Uberisicht ttder das Subgenus Apotomopterus

Hope, 1838 des Genus Carabus Linnee, 1758. Dr.

Frank Kleinfeld, Uhlandstrasse 15, 90768 Fiirth,

281 pp.

Kraatz G., 1894. Apotomopterus eccoptopterus Krtz n.

sp. von China. Deutsche Entomologische Zeit-

schrift, 38: 137-139.

Lassalle B., 2006. Nouveaux Carabes d’lran, et de la

Chine. Lambillionea, 106: 103-106.

Biodiversity Journal, 2012, 3 (3): 247-250

Newly reported marine red alga, Neosiphonia savatieri (Ha-

riot) M.S. Kim et I.K. Lee 1 999 (Rhodophyta Rhodomelaceae)

from Thailand

Narongrit Muangmai 1,2 , Sinchai Maneekat 2,3 , Nidsaraporn Petsut 4 & Chatcharee Keawsuralikhit 2,3 *

'School of Biological Sciences, Victoria University of Wellington, Kelburn, Wellington 6140 New Zealand

2 Biodiversity and Aquatic Environmental Research Unit, Center for Advanced Studies for Agriculture and Food, Kasetsart Uni-

versity, Phaholyothin Road, Bangkok 10900 Thailand; e-mail: ffischs@ku.ac.th

department of Fishery Biology, Faculty of Fisheries, Kasetsart University, Phaholyothin Road, Bangkok 10900 Thailand

department of Agricultural Technology, Faculty of Science, Ramkhamhaeng University, Ramkhamhaeng Road, Bangkok 10240

Thailand

■"Corresponding author

ABSTRACT Neosiphonia savatieri (Hariot) Myung Sook Kim et In Kyu Lee, 1999 is reported for the first

time from Thailand based on specimens collected from the Gulf of Thailand and Andaman

sea. We herein describe the vegetative and reproductive morphology of the specimens. Im-

portant features for species identification include the thallus configuration, number of peri-

central cells, cortication, branching pattern, origin of rhizoids, origin of branches, occurrence

of trichoblasts and reproductive characteristics. Our results expand the known geographic di-

stribution of this species and confirm its taxonomic features.

KEY WORDS Marine red alga; Morphology; Neosiphonia savatieri ; Rhodomelaceae; Thailand.

Received 01.09.2012; accepted 15.09.2012; printed 30.09.2012

INTRODUCTION

The genus Neosiphonia Myung Sook Kim et In

Kyu Lee, 1999 was segregated from Poly siphonia

Greville, 1823 based on the generitype, N. flavima-

rina M.S. Kim et I.K. Lee, 1999 from Bangpo on

the western coast of Korea (Kim & Lee, 1999).

Currently, there are 30 assigned species (Guiry &

Guiry, 2012) of which 15 species have been recor-

ded for South East Asia region (Ho, 1969; Silva et

al., 1987; Abbott et al., 2002; Kim et al., 2008).

N. savatieri (Hariot) M.S. Kim et I.K. Lee, 1999

was originally described based on collected material

from Kanagawa Prefecture, Japan and subsequently

it has been reported from Philippine, Korea, Malay-

sia, Norfolk Island, Hawaiian Island and Samoan

Archipelago (Silva et al., 1987; Abbott, 1999; Mil-

lar, 1999; Masuda et al., 2001; Kim, 2005; Skelton

& South, 2007; Kim et al., 2008).

In Thailand, only generic level of the genus

Neosiphonia has been currently reported (Coppe-

jans et al., 2010). During the collections under the

project of the biodiversity inventory and informa-

tion management in biodiversity hotspots, the tuf-

ting red alga, Neosiphonia sp. was collected in both

Andaman Sea and the Gulf of Thailand.

Eventually we identified those specimens as N.

savatieri and confirmed the taxonomic features

based on morphological and anatomical characteri-

stics of vegetative and reproductive plants.

MATERIALS AND METHODS

Specimens examined were hand-collected du-

ring October 2010 at sand dune area around the

estuary of Pak Bara, Satun province, Andaman Sea

(99°43 , 2 ,, E; 6°51’27”N).

248

N. Muangmai, S. Maneekat, N. Petsut & C. Keawsuralikhit

Additional material examined was from Ao Len,

Trat Province, Gulf of Thailand (102°32’57”E;

12°4’13”N). Algal samples for morphological in-

vestigation were fixed and stored in 5%

formalin/seawater or pressed onto herbarium sheets.

Voucher specimens were deposited in the herbarium

of Laboratory of Applied Research for Aquatic

Plant and Plankton, Biodiversity and Aquatic Envi-

ronmental Research Unit of Faculty of Fisheries,

Kasetsart University, Bangkok, Thailand.

Specimens were stained with 1% aniline blue,

acidified with IN HC1 and mounted in a 40%

Karo®corn syrup on glass microscope slides. Digi-

tal images were photographed by microscope digi-

tal camera Olympus DP20 (Olympus, Tokyo,

Japan) and eventually edited using Photoshop Ele-

ments 6 (Adobe, San Jose, CA, USA). Species iden-

tification was based on the literatures of N. savatieri

from Japan, Korea and Malaysia (Hariot, 1891; Ma-

suda et al., 2001; Kim, 2005; Kim et al., 2008).

RESULTS AND DISCUSSION

Based on diligent observations on morphologi-

cal features of gametophytic and tetrasporangial

thalli, we conclude that this is the first record of N.

savatieri (Figs. 1-13) from Thailand.

Our Thai materials are in agreement with de-

scriptions of previous studies of N. savatieri from

other localities. The description below is based on

the Thai materials.

Neosiphonia savatieri (Hariot) Myung Sook

Kim et In Kyu Lee, 1999

Basionym: Polysiphonia savatieri Hariot, 1891:

226-227.

Habitat: Plants from Andaman Sea grew epi-

phytically on Gracilaria minuta Lewmanomont,

1994 and G. salicornia (Agardh) Dawson, 1954,

which inhabited the lower intertidal on the sand

dune nearby the river mouth. The specimens from

the Gulf of Thailand were found on the thallus of

Hydropuntia changii (Xia et Abbott) Wynne, 1989

at 1 m depth (Fig. 1).

The specimens of N. savatieri are erect, grow

individually, and reach up to 5-10 mm high. Axes

with 4 pericentral cells ecorticate, 90-180 pm in

diameter (Figs. 2-3).

Specimens pseudodichotomously branched,

showing a Y-shaped ramification with an angle of

approximately 50 degrees (Fig. 2). Rhizoids aggre-

gated in tufts in the lower segment of the axes, cut

off from pericentral cells (Fig. 4), they penetrate

into the tissue of G. minuta. Trichoblasts or bran-

ches are produced on successive segments (Fig. 5).

Trichoblasts formed on every segment in a spiral

arrangement and deciduous, leaving persistent scar

cells (Fig. 6). Trichoblasts are abundant only at the

apical part (Fig. 6). Lateral branches are exogenous,

replacing trichoblasts (Fig. 5). Exogenous branches

develop at various spots on the axis and grow from

scar cells of the trichoblasts (Fig. 7).

Tetrasporangia arranged in slightly spiral series

on the upper branches (Fig. 8). A single tetraspo-

rangium is formed in each segment (Fig. 9). Mature

tetrasporangia are prominent, 60-80 pm in diameter.

Spores are tetrahedrally organized. Spermatangial

branches are formed at the first dichotomy of fertile

trichoblasts (Fig. 10). Mature spermatangial bran-

ches are lanceolate, 180-260 pm long and 60-80 pm

wide, and lack sterile apical cells (Fig. 10).

An initial of carpogonial branch is formed on

the second segment of the fertile trichoblast near

the tip of lateral branches (Fig. 11). Procarp consists

of a three-celled carpogonial branch and two sterile

cells borne on the supporting cell. After fertiliza-

tion, the gonimoblast gradually develops from the

auxiliary cell (Fig. 12). Mature cystocarps are sphe-

rical with a slightly protruding ostiole, 180-220 pm

in diameter (Fig. 13).

Based on the specimen collected from Kana-

gawa, Japan, Hariot (1891) originally assigned N.

savatieri to the genus Polysiphonia , which is cha-

racterized by its four pericentral cells, unicellular

rhizoids cut off by a cross wall from the proximal

end of the pericentral cells and spermatangial bran-

ches arising as a primary branch of a trichoblast.

Kim & Lee (1999) later assigned species with rhi-

zoids cut off from pericentral cells, spiral arrange-

ment of tetraspores, three-celled carpogonial

branches and spermatangial branches on the pri-

mary dichotomy of trichoblast filament to a new

genus, Neosiphonia.

The Thai specimens reported here agree well

with the original description of N. savatieri and

confirm the important identifying characteristics of

this genus. Our Thai specimens were morphologi-

cally very similar to N. savatieri described from the

Newly reported marine red alga, Neosiphonia savatieri (Rhodophyta Rhodomelaceae) from Thailand

249

Figures 1-13 Neosiphonia savatieri from Thailand. Fig. 1 : plants epiphytic on Hydropimtia changii (arrows), Scale bar, 1 cm.

Fig. 2: thalli pseudodichotomously branched with an angle of about 50 degree, Scale bar, 500 pm. Fig. 3: transverse section

of the middle portion of a branch with 4 pericentral cells and a axial cell, Scale bar, 50 pm. Fig. 4: rhizoid (arrow) cut off

from pericentral cells, Scale bar, 10 pm. Fig. 5: apical portion of a branch showing oblique divisions of apical cells (arrows),

Scale bar, 100 pm. Fig. 6: trichoblasts (arrows) and scar cells of deciduous trichoblast arranged in spiral manner in the apical

part of a cystocarpic plant, Scale bar, 100 pm. Fig. 7: exogenous branches (arrows) of a tetrasporic plant, Scale bar, 200 pm.

Fig. 8: tetrasporic plants showing the spiral arrangement of tetrasporangia, Scale bar, 200 pm. Fig. 9: mature tetrasporangium

bearing one per segment, Scale bar, 20 pm. Fig. 10: spermatangial branches arising on a branch of the fertile trichoblasts

(arrow), Scale bar, 100 pm. Fig. 1 1 : procarp (arrow) developing on the second segment of a fertile trichoblasts at the tip of

branches, Scale bar, 20 pm. Fig. 12: post-fertilization stage, Scale bar, 50 pm. Fig. 13: mature cystocarps, Scale bar, 70 pm.

250

N. Muangmai, S. Maneekat, N. Petsut & C. Keawsuralikhit

Philippines, Hawaii, Malaysia, and Japan and

Korea; all were relatively small epiphytic algae and

have spermatangial branches formed on a branch of

trichoblasts, spiraled tetrasporangia and an appro-

ximately 50 degree angle in the Y-shaped branching

pattern (Silva et al., 1987; Abbott, 1999; Masuda et

al., 2001; Kim, 2005; Kim et al., 2008).

Furthermore, Thai specimens of A. savatieri ap-

pear to be prevalent in river deltas surrounded by

mangroves and grow specifically on gracilarioid

algae. Our study shows that N. savatieri occur in

both marine and brackish waters and that the distri-

bution of this species extends to Thailand.

Additionally, Thai specimens of N. savatieri

showed that young lateral branches are formed by

replacing trichoblats, while Kim (2005) and Ma-

suda et al. (2001) described branches that are not

associated with trichoblasts in N. savatieri from

Korea and Malaysia. According to Stuercke & Fre-

shwater (2008), the origin of branches has been

used as one of the important characteristics to se-

parate species in Polysiphonia sensu lato.

It is important to take into account whether the

relationship of branches and trichoblasts or other

specific morphological characters are useful for

species delineation of N. savatieri. Additional mo-

lecular and morphological analyses of N. savatieri

will be needed in order to gain more insights into

the species delimitation and differentiation among

closely related species, especially in South East

Asian region.

ACKNOWLEDGEMENTS

We thank those who helped us obtaining valua-

ble specimens: Sunan Pattarajinda, Teerapong

Duangdee and Wirayut Kuisorn. Sincere thanks are

also due to Khanjanapaj Lewmanomont and John

Bower for providing many useful suggestions and

critical comments to the English. This research was

partly funded by Office of Natural Resources and

Environmental Policy and Training, Bangkok,

Thailand.

REFERENCES

Abbot LA., 1999. Marine red algae of the Hawaiian Is-

lands. Bishop Museum press, Hawaii, 465 pp.

Abbott I. A., Fisher j. & McDermid K.J., 2002. Newly

reported and revised marine algae from the vicinity

of Nha Trang, Vietnam. In: Abbott I. A. & Mcder-

mid K.J. 2002. Taxonomy of Economic Seaweeds

with reference to some Pacific species. Vol. VIII,

California Sea Grant College Program, California,

291-321.

Coppejans E., Prathep A., Leliaert F., Lewmanomont K.

& De Clerck O., 2010. Seaweeds of Mu Ko Tha Lae

Tai (SE Thailand): Methodologies and field guide to

the dominant species. Biodiversity Research and

Training Program, Bangkok, 274 pp.

Guiry M.D. & Guiry G.M., 2012. AlgaeBase. World-

wide electronic publication, National University of

Ireland, Galway, http://www.algaebase.org; searched

on 15 March 2012.

Hariot R, 1891. Liste des algues marines rapports de Yo-

koska (Japon) par M. le Dr Savatier. Memoires de la

Societe des Sciences Naturelles et Mathematiques de

Cherbourg, 27:211-230.

Ho P.H., 1969. Rong bien Vietnam - Marine algae of

South Vietnam. Saigon, 558 pp.

Kim M.S., 2005. Taxonomy of a poorly documented

alga, Neosiphonia savatieri (Rhodomelaceae, Rho-

dophyta) from Korea. Nova Hedwigia, 81: 163-175.

Kim M.S. & Lee I.K., 1999. Neosiphonia flavimarina

gen. et sp. nov. with a taxonomic reassessment of the

genus Polysiphonia (Rhodomelaceae, Rhodophyta).

Phycological Research, 47: 271-281.

Kim M.S., Lim P.E. & Phang S.M., 2008. Taxonomic

notes on Malaysian Neosiphonia and Polysiphonia

(Rhodomelaceae, Rhodophyta). In: Phang S.M.,

Lewmanomont K. & Lim P.E., (eds.), Taxonomy of

Southeast Asian Seaweeds. Monograph series 2. Uni-

versity of Malaya, Kuala Lumpur, 33-44.

Masuda M., Abe T., Kawaguchi S. & Phang S.M., 2001.

Taxonomic notes on marine algae from Malaysia. VI.

Five species of Ceramiales (Rhodophyceae). Bota-

nica Marina, 44: 467-477.

Millar A. J.K, 1999. Marine benthic algae of Norfolk Is-

land, South Pacific. Australian Systematic Botany,

12: 479-547.

Silva PC., Menez E.G. &MoeR.L., 1987. Catalog of the

benthic marine algae of the Philippines. Smithsonian

Contribution to the Marine Sciences, 27: 1-179.

Skelton PA. & South G.R., 2007. The benthic marine

algae of the Samoan Archipelago, with emphasis

on the Apia District. Nova Hedwigia Beihefte, 132:

1-350.

Stuercke B. & Freshwater D.W., 2008. Consistency of

morphological characters used to delimit Polysipho-

nia sensu lato species (Ceramiales, Florideophyceae):

analyses of North Carolina, USA specimens. Phyco-

logia, 47: 541-559.

Biodiversity Journal, 2012, 3 (3): 251-258

Additional data on the genus Muticaria L ndholm, 1 925 with de-

scription of a new species (Gastropoda Pulmonata Clausiliidae)

Maria Stella Colomba'^Agatino Reitano 2 , Fabio Li berto 3 , Salvatore Giglio 4 , Armando Gregorini 1 & Ignazio

Sparacio 5

'Umversita di Urbino, Dept, of Biomolecular Sciences, via Maggetti 22, 61029 Urbino, Italy.; email: mariastella.colomba@uniurb.it;

armando. gregorini@uniurb . it

2 Via Gravina n. 7, 95030 Tremestieri Etneo, Italy; e-mail: tinohawk@yahoo.it

3 Strada Provinciale Cefalu-Gibilmanna n° 93, 90015 Cefalu, Italy; email: fabioliberto@alice.it

4 Contrada Settefrati, 90015 Cefalu, Italy; email: hallucigenia@tiscali.it

5 Via E. Notarbartolo 54 int. 13, 90145 Palermo, Italy; e-mail: isparacio@inwind.it

’Corresponding author

ABSTRACT Morphological analysis and molecular genetic studies conducted on the genus Muticaria

Lindholm, 1925 (Pulmonata Clausiliidae) in Sicily allowed to identify a new species which

is described in the present paper.

KEY WORDS Clausiliidae; Muticaria ; Sicily, new species.

Received 01.09.2012; accepted 18.09.2012; printed 30.09.2012

INTRODUCTION

The genus Muticaria Lindholm, 1925 has a di-

stribution limited to South-East Sicily and Maltese

Islands. Currently it includes three species: Mutica-

ria syracusana (Philippi, 1836) and M. neuteboomi

Beckmann, 1990 spread in southeastern Sicily and

M. macrostoma endemic to the Maltese Islands,

where it occurs with four subspecies: M. macro-

stoma macrostoma (Cantraine, 1835), M. macro-

stoma scalaris (L. Pfeiffer, 1850), M. macrostoma

oscitans (Charpentier, 1852) and M. macro stoma

mamotica (Gulia, 1861) (Beckmann, 1992; Giusti

et al., 1995; Bank, 2012).

A preliminary molecular study on 16S rDNA

partial sequences (Gregorini et al., 2008) carried out

on Sicilian Muticaria revealed the existence of si-

gnificant genetic differences between populations

attributed either to M. syracusana or M. neute-

boomi , including the topotypic ones.

Particularly, M. neuteboomi resulted the most

widespread species with populations inhabiting

inner areas of Iblean plateau (South Eastern Sicily),

while M. syracusana resulted confined to a few coa-

stal locality of Syracuse province.

A second and more detailed molecular study

(Colomba et al., 2010) was conducted on topotypic

specimens of M. syracusana and M. neuteboomi

with a comparative analysis of mitochondrial 16S

rDNA and cytochrome oxidase I (COI) gene partial

sequences. This study, besides confirming prelimi-

nary data (Gregorini et al., 2008), strongly corrobo-

rated the validity of the two species.

As additional contribute to the research on the

genus Muticaria in South Eastern Sicily and within

the context of a wider and more detailed work, in the

present paper the population of Muticaria from Spi-

nagallo (Syracuse) is described as new species on the

grounds of morphological and molecular data.

ACRONYMS. BC = bursa copulatrix;

BCD = diverticulum of bursa copulatrix; CL = co-

lumellar lamella; DBC = duct of the bursa copula-

trix; DE= distal epiphallus; FO = free oviduct; GA

= genital atrium; L = lunella; P = penis; PD = di-

verticulum of penis; PE= proximal epiphallus;

PL = parietal lamella; PLL = parallel lamella;

252

M.S. Colomba, A. Reitano, F. Liberto, S. Giglio.A. Gregorini & I. Sparacio

PP = principal plica; PR = penial retractor muscle;

SL = spiral lamella; SP = sutural plica/plicae;

V= vagina; VD = vas deferens.

The materials used for this study are deposited

in the following Museums and private collections:

A. Brancato collection, Syracuse, Italy (CB); S. Gi-

glio collection, Cefalii, Italy (CG); Laboratory of

Cytogenetics and Molecular Biology, University of

Urbino, Italy (LCMBU); F. Liberto collection, Ce-

falu, Italy (CL); Museo Civico di Storia naturale di

Comiso, Italy (MCSNC); Museo Civico di Storia

Naturale di Genova “G. Doria”, Italy (MSNG);

Museo Naturalistico F. Mina Palumbo, Castel-

buono, Italy (MNMP ); A. Reitano collection, Tre-

mestieri Etneo, Italy (CR); I. Sparacio collection,

Palermo, Italy (CS).

Muticaria brancatoi n. sp.

Examined material. Holotypus: Italy, Sicily,

Siracusa, Cugno Lungo, 37°00 , 25”N 15°10 , 47”E,

110 m, 02.IX.20 12, legit A. Brancato (MSNG

57016). Paratypi: Italy, Sicily, Siracusa, Contrada

Spinagallo, 37°00'12”N 15°10'50 ,, E, 120 m,

12.III.2008, 5 specimens, 3 shells (CR); idem, 14

specimens, 30 shells (CR); Siracusa, V.ne Mosca-

santi, 37°00'58”N 15 o 09'53”E, 130 m, 28.XIL2010,

2 shells (CR); Siracusa, Cugno Lungo, 37°00'53”N

15°10'11”E, 135 m, 28. XII. 20 10, 2 specimens, 3

shells (CR) Siracusa, Cugno Lungo, 37°00’25”N

15°10 , 41”E, 110 m, 01.IV.2012, 16 shells (CL); Si-

racusa, Cugno Lungo, 37°00 , 27”N 15°10 , 48”E, 80

m, 01.IV.20 12, 8 specimens, 86 shells (CL); idem,

2 specimens, 2 shells, legit F. Liberto (MCSNC

4412); idem, 6 shells (CG); Siracusa, Cugno Lungo,

37°00 , 25”N 15°10 , 47”E, 110 m, 02.IX.2012, 8

shells (CB); idem, 20 specimens, 32 shells (CS);

idem, 2 specimens, legit I. Sparacio (MNMP ).

Description of holotypus. Shell sinistral (Figs.

1, 2, 9), dimensions: height: 12.30 mm; maximum

diameter: 4.20 mm, medium, cylindrical-fusiform,

decollate, rather robust, light yellowish-grey in co-

lour; external surface with minute, raised, close

ribs, 69 ribs on penultimate whorl; last whorl with

robust, evident and very spaced ribs; spire slowly

and regularly growing, with 4 whorls; last whorl ta-

pering downwards, with a very elevated and curved

cervical keel; suture moderately deep; umbilicus

slit-like, aperture about 1/3 of shell height, square.

with 5 lamellae (on parietum and columellar side)

and lunella and 4-5 plicae (on palatum); on parietum

(Figs. 7, 8), starting from suture, there are: long, well

developed, non-emerging parallel lamella; short spi-

ral lamella, deviating from centre of parietum to

adhere to parallel lamella, (upper) parietal lamella

tooth-like; non-emerging columellar lamella; subco-

lumellar lamella internal; on palatum (Figs. 5, 6) there

is an evident, lateral lunella and, starting from suture:

two sutural plicae, the principal plica with a robust

posterior portion, not fused to lunella apex, and a thin

anterior portion, basal plica small, internally fused to

base of lunella, very small sulcal lamella; clausilium

triangular and slender (Figs. 3, 4), plough-like basal

plate, apically pointed; peristome continuous, reflec-

ted, distinct from the wall of the last whorl.

Genitalia (Figs. 12-14). Genitalia are characteri-

zed by: short vagina, very short free oviduct, well de-

veloped ovispermiduct and a short copulatory duct

ending in branched bursa copulatrix complex; one

branch consisting of a short and wide diverticulum of

the bursa copulatrix; other branch consisting of very

short bursa copulatrix duct and oval and elongated

bursa copulatrix. Penial complex consisting of flagel-

lum, epiphallus, penial diverticulum and penis; epi-

phallus divided by point insertion of robust penial

retractor muscle into proximal and distal portions, the

latter very short; wide and pointed penial diverticu-

lum arising on border between distal epiphallus and

penis; penis short (2.5 mm). Internal walls of penis

show a long, wide and elevated pleat and two thin

and less evident pleats; left ommatophore long and

well developed.

Variability. Dimensions in decollate specimens

(4-5 whorls): height: 11.02-12.30 mm; maximum dia-

meter: 4. 16-4.55 mm. The number of ribs on the pe-

nultimate whorl of the shell ranges from 57 to 70 (on

average, 67); in some specimens the principal plica is

absent in its central portion.

Etimology. The new species is dedicated to Aldo

Brancato (Syracuse, Sicily), dear friend and esteemed

naturalist.

Biology and Distribution. This species lives on

calcareous rock. It is found in cavities and under stone

on stony soil. Endemic species to the South-Eastern

Sicily, at the time known only for the locality of de-

scription.

Comparative notes. M. syracusana shows slen-

der and conical-fusiform shell with ribs on penulti-

Additional data on the genus Muticaria Lindholm, 1 925 with description of new species

253

Figure 1. Shell of Muticaria brancatoi n. sp., Siracusa, Cugno Lungo, h: 11.57 mm - D: 4.33 mm. Figure 2. idem, h:

12.27 mm - D: 4.29 mm.

254

M.S. Colomba, A. Reitano, F. Liberto, S. Giglio.A. Gregorini & I. Sparacio

Figures 3-8. Muticaria brancatoi n. sp., Siracusa, Cugno Lungo, clausilium of two specimens (Figs. 3, 4), palatum (Figs.

5, 6) and parietum (Figs. 7, 8).

Additional data on the genus Muticaria Lindholm, 1 925 with description of new species

255

Figures 9-11. Cervical keel in Muticaria brancatoi n. sp., Siracusa, Cugno Lungo (Fig. 9), M. syracusana, Siracusa, Tea-

tro Romano (Fig. 10) and M. neuteboomi, Ragusa, Cava d’Ispica (Fig. 11). Figures 12-14. Genitalia of M. brancatoi n.

sp., Siracusa, Cugno Lungo (Fig. 12) internal structure of penis (Fig. 13) and ommatophore (Fig. 14).

256

M.S. Colomba, A. Reitano, F. Liberto, S. Giglio.A. Gregorini & I. Sparacio

NEU1 COI LCO LCO 1490.scf

NEU3 COI LCO LCO 1490.scf

NEU2 COI LCO LCO 1490.scf

NEU5 COI LCO LCO 1490.scf

NEU4 COI LCO LCO 1490.scf

SYR4 COI LCO LCO 1490. scf

SYR1 COI LCO LCO 1490. scf

SYR5 COI LCO LCO 1490. scf

SYR2 COI LCO LCO 1490. scf

SYR3 COI LCO LCO 1490. scf

100

M GARGANENSIS COI

Albinaria caerulea COI

100

SPI3 BIS COI LCO 1490. scf

SPI5 BIS COI LCO 1490. scf

SPI6 BIS COI LCO 1490. scf

SPI7 BIS COI LCO 1490. scf

SPI4 BIS COI LCO LCO1490.scf

0.06

Figure 15. Maximum Likelihood consensus tree inferred from 500 replicates. The tree is drawn to scale, with branch

lengths measured in the number of substitutions per site. Bootstrap values, i.e.the percentage of replicate trees in which

the associated taxa clustered together in the bootstrap test are shown next to the branches.

mate whorl more spaced and less numerous (27-

54); on palatum, the principal plica is very short and

fused to upper palatal plica. M. neuteboomi is cha-

racterized by fusiform shell, from slender to mode-

rately ventricose, with more numerous ribs on

penultimate whorl (56-97); on palatum, the principal

plica is independent of upper palatal plica. All Muti-

caria from Maltese islands are characterized for a

principal plica independent of the upper palatal plica.

Molecular Analysis. Five Muticaria speci-

mens from C.da Spinagallo (Syracuse, SE Sicily),

labelled as SPI, were analyzed. Samples were sto-

red in 75% Ethanol at -20 °C in test tubes. For

each individual, the entire animal was used for

total DNA extraction (by Wizard Genomic DNA

Purification Kit, Promega).

Para-voucher specimens, sensu Groenenberg et

al. (2011) i.e. different specimens than the ones used

for DNA analysis, but from the same sample or po-

pulation, were stored by MSC (University of Ur-

bino). COI amplicons (644 bp) were obtained by

LCO1490/HCO2198 universal primers (5’-

GGTC AAC AAATC ATAAAGATATTGG-3 75 ’-TA-

AACTT C AGGGT GACC AAAAAAT C A-3 ’ ) as in

Folmer et al. (1994) with a PCR cycle of 95 °C for

5 min; 95 °C for 1 min, 42 °C for 1 min, 72 °C for 1

min (37 cycles); 72 °C for 10 min. Sequencing of the

purified PCR products was carried out using auto-

mated DNA sequencers at Euro fins MWG Operon

(Germany). Finally, sequence chromatograms of

each amplified fragment were browsed visually. Se-

quences generated in this study were analysed with

additional Muticaria syracusana (labelled as SYR)

and M. neuteboomi (labelled as NEU) COI sequen-

ces, previously deposited by us in GenBank (IDs:

HQ696869 and HQ696867, see also Colomba et

al., 2010) Medora garganensis (ID: AY425595)

and Albinaria caerulea (ID: NC_001761) COI se-

quences were employed as outgropus.

Sequences were visualized with BioEdit Se-

quence Alignment Editor 7 (Hall, 1999), aligned

with the ClustalW option included in this software

and double checked by eye. Standard measures of

nucleotide polymorphism and phylogenetic analy-

ses were conducted in MEGA 5.0.3 (Tamura et al.,

2011). The best-fit evolution model of nucleotide

substitution resulted T92+G (Tamura 3 -parameter

+ Gamma). The evolutionary history was inferred

by using the Maximum Likelihood method; the bo-

otstrap consensus tree was inferred from 500 repli-

cates; a discrete Gamma distribution was used to

model evolutionary rate differences among sites (5

categories; +G, parameter = 2.1279). Codon posi-

tions included were lst+2nd+3rd. All positions con-

Additional data on the genus Muticaria Lindholm, 1 925 with description of new species

257

Figure 16. Geographic distribution of Muticaria species genetically analysed in SE Sicily: Muticaria brancatoi n. sp.

(star), M syracusana (square) and M. neuteboomi (dots).

taining gaps and missing data were eliminated. Di-

vergences between SPI/S YR and SPI/NEU groups

(Dxy), assessed as p distance, were 27.5% and

27%, respectively. Hence, phylogenetic tree (Fig.

15) and genetic distance between groups support

the hypothesis that specimens from Spinagallo

may be ascribed to a distinct Muticaria species.

Remarks. Muticaria brancatoi n. sp. appears

well differentiated morphologically from nearby

and strictly related species currently known. Mo-

lecular data showed a good differentiation for

Spinagallo populations already in preliminary

studies conducted on 16S rDNA partial sequences

(Gregorini et al., 2008), but with this survey, car-

ried out by the analysis of cytochrome oxidase

subunit I gene, p distance from the other species

is considerably greater.

Based on available data no evolutionary

and/or paleobiogeographic hypothesis is possible,

nevertheless, this work highlights a remarkable

complexity (Fig. 16) and differentiation within

the genus Muticaria in Sicily (Gregorini et al.,

2008; Colomba et al., 2010), much greater than

supposed until now.

ACKNOWLEDGEMENTS

We wish to thank Andrea Corso (Syracuse,

Italy)

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