North-Western Journal of Zoology Vol. 3, No. 1, 2007, pp.1-8
Food Habits of the Lycian Salamander, Lyciasalamandra fazilae (Başoğlu and Atatür, 1974): Preliminary data on Dalyan Population
Kerim ÇİÇEK1,*, Cemal Varol TOK3, Ahmet MERMER1, Murat TOSUNOĞLU3 and Dinçer AYAZ2
1Ege University, Faculty of Science, Biology Department, Zoology Section, 35100, Bornova-İzmir, Turkey 2Ege University, Faculty of Science, Biology Department, Hydrobiology Section, 35100, Bornova-İzmir, Turkey 3Çanakkale Onsekiz Mart University, Faculty of Science-Literature, Department of Biology, 17020, Çanakkale, Turkey. *Corresponding author: Kerim ÇİÇEK e-mail: [email protected]
Abstract. We analyzed stomach contents of 21 (13 ♂♂, 8 ♀♀) adult Lycian salamanders, Lyciasalamandra fazilae, inhabiting Gökbel and İztuzu, south of Dalyan (Köyceğiz, Muğla). Although various terrestrial invertebrates constitute the diet of the salamander, larvae and adult beetles (39.61%), centipedes (16.88%) are the most important food groups. Lyciasalamandra fazilae is an active predator capable of changing its feeding regime in proportion to the species richness within its habitat.
Key words: Lycian Salamander, Lyciasalamandra fazilae, Food Composition, Turkey
Introduction southern Anatolian coast, Turkey, where it is found from northeast of Distribution of genus Lycia- Fethiye to the western shore of Lake salamandra (Lyciasalamandra luschani, Köyceğiz (range= ~688 km2). L. atifi, L. antalyana, L. billae, L. fazilae, The species is listed as endangered L. flavimembris and L. helverseni) in the Red List Category and Criteria ranges from Greece to the south and of IUCN because its extent of southwest of Turkey as well as some occurrence is less than 5,000 km², its islands including Kastellorizon, distribution is severely fragmented, Meyisti, Kekova, and Carpathos and there is continuing decline in the (Veith & Steinfartz 2004). One of extent and quality of its habitat (Tok these, Lyciasalamandra fazilae, was first et al. 2006). It is potentially threatened described by Başoğlu & Atatür (1974) by habitat loss caused by forest fires in the vicinity of Gökçeovacık, Dalyan and over-collection for scientific and Üzümlü (Muğla). Lycian purposes. Salamander is restricted to the
N West J Zool, 3, 2007 Oradea, Romania 2 Çiçek, K. et al.
Lycian salamander is mainly We captured salamanders during terrestrial, inhabits rocky limestone daytime between 10.00h and 14.00h under stones. The mean temperatures were 17oC areas usually in pine forests and during the sampling conducted on March 3, marquis, and is found sometimes 2006 and 27oC on April 22, 2006. Within half under stone accumulations on an hour following capture, we anaesthetized hillsides without vegetation (Başoğlu individuals in a 1 % solution of MS-222 & Özeti 1973, Baran & Atatür 1998). It (methane tricaine sulfonate) in the field and is found at elevations between 15 and extracted their stomach contents by forced regurgitation with forceps (Hirai & Matsui 1025 m and lives in places where 2001). We preserved the contents in 70% mean annual rainfall is less than 1000 ethanol for later analysis. We measured mm. snout-vent lengths of all the individuals to Although age structure (Olgun et the nearest 0.01 mm with a dial calliper. al. 2001), breeding (Poylmeni 1994; After these procedures, we marked the Özeti 1973, 1979), feeding biology salamanders by toe-clipping and released them on the spot where they were captured. (Polymeni 1989, Düşen et al. 2004) We collected and observed potential preys of and gregarious behaviour (Gautier et the study area in order to be able to compare al. 2006) of Mediterranean and Greece stomach contents with environment. populations of Lyciasalamandra species The prey items were identified (Chinery have been documented, data on the 1992, 1993, Demirsoy 1998, Lodos 1982, 1984, 1989, Roberts 1995, Stoev 2002) to the lowest biology of Lycian salamander are still possible taxon and lengths and widths were scarce (Veith et al. 2001). measured. Approximate volumes of prey The aim of the present study is to items were calculated using the formula for present the food habits of Lycian an ellipsoid (Dunham, 1983): salamander in Gökbel and İztuzu V= 4/3π (L/2) (W/2)2, populations. In the formula above, L is length of prey and W is the width of prey.
Plant material found in the stomach
contents included mosses, seeds, and small Materials and Methods leaves, and was most likely ingested
accidentally during foraging. Unidentified The study site is located in Gökbel and arthropods in this study usually consisted of İztuzu, (36o 46' N, 28o 40' E, 105 m a.s.l.) a wing, a leg, or a body segment, which may south of Dalyan (Köyceğiz, Muğla) indicate either the salamander was unable to southwest Turkey. Dominant plant species capture the entire prey item or remaining in the biotope of individuals inhabiting portion of the prey item was not detected stony clearings in a pine forest (Pinus brutia) because it had passed through the digestive include Asphodelus aestivus and Ballota system at a different rate. The food contents acetabulosa. These species are accompanied were assessed with respect to frequency of by others such as Geranium disectum, occurrence, numeric proportion and Picnomon acarna, Scandix pecten-veneris, Crepis volumetric proportion. Since the distribution sancta, Aucalyptus cameldulensis, Euphorbia of data was significantly different from the egzugea, and Delphinium staphystagia.
N West J Zool, 3, 2007 Food Habits of Lyciasalamandra fazilae: Preliminary data on Dalyan Population 3 normal distribution (Kolmogorov-Smirnov Among the prey taxa shown in test, P<0.05), averages were compared with Table 1, coleopteran larvae (71.43%), the non parametric Mann Whitney U test. centipedes (66.67%), spiders (38.09%) The significance level was P≤0.05. and terrestrial snails (33.33%) were frequently consumed by Lycian Results Salamander (frequency of occurrence >30%). Coleopteran larvae (39.61%) During the study, 21 adult and centipedes (16.88%) (>10%) were individuals (13 ♂♂ and 8 ♀♀) were numerically the most consumed prey captured. The mean snout-vent length items. Volumetrically, larval co- (hereafter SVL) (±CI) was determined leopterans (82.01%) and centipedes as 61.12±1.30 (range= 58.03 - (16.67%) were the most important 64.97mm) at males, and as 62.38±4.07 food items among the preys. Larval (range= 50.97 - 68.53mm) at females. preys constituted 31.82% of stomach No statistically significant difference contents by number and 82.02% by was observed between sexes with volume. The most diverse orders were respect to SVL (Mann-Whitney U test, Coleoptera (larvae of Carabidae, P > 0.05). From the stomach contents Elateridae, Tenebrionidae, Cocci- of 21 individuals, 154 prey items were nellidae, and Curculionidae) and extracted with a median (±CI) number Araneae (Araneidae, Lycosidae, and of 7.00 ± 5.79. Slight differences were Salticidae). observed between sexes with respect Gastropoda was determined as the to number of prey items per stomach, only class belonging to phylum frequency of occurrence, numeric and Mollusca. It made up 6.49% of total volumetric proportion; nonetheless, preys by number, and 0.10% by these were not statistically significant volume. Regarding stomach contents, (Mann-Whitney U test, P> 0.05). the class was represented by the Diverse arthropods and molluscs families Vertiginidae (n%=3.90, along with plant material and v%=0.09) and Polygyridae (n%=2.60, minerals were also encountered. v%<0.01). Furthermore, plants (n%= Arthropoda contained six classes 3.25, v%<0.01) and minerals (n%=1.95, (Malacostraca, Diplopoda, Arachnida, v%<0.01) were also found in food Chilopoda and Insecta) and contents. Highly digested prey items constituted 93.49% of food contents accounted for 2.30% total stomach by number. Insecta included 6 orders contents. and made up 55.19% by number, Our field studies revealed pre- 82.26% by volume of stomach sence of prey animals in the biotope contents.
N West J Zool, 3, 2007 4 Çiçek, K. et al.
Table no.1 Food composition (in %) of Lyciasalamandra fazilae (154 preys from 21 stomachs, total volume 4824.58mm3). f%= frequency of occurrence, n%= numeric proportion, v%= volumetric proportion.
Prey Taxa f% n% v% Insecta 95.24 55.19 82.26 Orthophtera 4.76 1.30 <0.01 Hemiptera 4.76 1.30 <0.01 Lygaeidae 4.76 1.30 <0.01 Homoptera 4.76 2.60 <0.01 Coleoptera 85.71 39.61 82.09 larvae 71.43 28.57 82.01 Carabidae 14.29 3.25 0.02 Elateridae 4.76 1.30 <0.01 Tenebrionidae 4.76 3.25 0.05 Coccinellidae 4.76 0.65 <0.01 Curculionidae 4.76 1.30 <0.01 Diptera 19.05 5.20 0.02 larvae 4.76 1.95 <0.01 Culicidae 9.52 2.60 0.01 Lepidoptera 9.52 1.30 0.01 larvae 9.52 1.30 0.01 Hymenoptera 14.29 1.95 <0.01 Formicidae 14.29 1.95 <0.01 Arachnida 38.09 8.44 0.29 Araneae 38.09 8.44 0.29 Araneidae 14.29 1.95 0.01 Lycosidae 28.57 4.54 0.23 Salticidae 14.29 1.95 0.05 Malacostraca 23.81 5.19 0.13 Isopoda 23.81 5.19 0.13 Oniscidae 19.05 4.54 0.13 Chilopoda 66.67 16.88 16.67 Lithobiomorpha 14.29 3.25 0.10 Geophilomorpha 42.86 13.64 16.58 Diplopoda 28.57 7.79 0.55 Julida 9.52 1.95 <0.01 Gastropoda 33.33 6.49 0.10 Stylommatophora 33.33 6.49 0.10 Vertiginidae 23.81 3.90 0.09 Columella sp. 23.81 3.90 0.09 Polygyridae 14.29 2.60 <0.01 Cryptomastix sp. 14.29 2.60 <0.01 Plant 19.05 3.25 <0.01 Mineral 14.29 1.95 <0.01 Unidentified 19.05 2.30 <0.01
N West J Zool, 3, 2007 Food Habits of Lyciasalamandra fazilae: Preliminary data on Dalyan Population 5
belonging to orders such as Stylom- gastropods as food. Especially larval matophora, Chilopoda, Diplopoda, coleopterans and centipedes are the Isopoda, Arachnida, Formicidae, most important food items in its diet. Diptera, and Coleoptera. Considered The earlier studies reported that potential food in the environment, all larval and adult insects were predo- of these prey groups were en- minantly consumed preys, and the countered in the stomach contents in other groups included gastropods, varying proportions. millipedes, pill bugs and sow bugs. (Baran & Atatür 1998, Polymeni 1989). Düşen et al. (2004)’s findings Discussion suggested that adult coleopterans (33.04%) were the main prey of The present study revealed that Lyciasalamandra luschani, L. atifi, L. Lycian salamander feeds on a variety antalyana, L. billae, L. fazilae and L. of invertebrates, and particularly, flavimembris whereas gastropods terrestrial arthropods constitute an (19.59%) and spiders (10.82%) were important part of its diet. The previous other important preys. European Fire studies on other salamander species Salamander, Salamandra salamandra, showed that feeding habits of also consumes Gastropoda, Mi- individuals were strongly affected by riapoda, and Araneae most frequently habitat conditions such as soil moisture, (Covaciu-Macrov et al. 2002). season and prey availability (e.g. Considering the variety of food Gunzburger 1999, Jaeger 1972, Martof groups found in the stomach contents, & Scott 1957). Various other studies it could be stated that Lyciasalamandra related to Lyciasalamandra species also fazilae has a wide range of prey in its mentioned that the individuals in the diet. The finding that especially larval biotope consumed available prey preys have a considerable volume in (Düşen et al. 2004, Polymeni 1989), the food contents shows that the meaning that the salamanders are an individuals need to have a opportunistic feeder in that habitat. The sophisticated sense of sight in order to present study also confirms the be able to detect and catch such slow- findings of other studies on this moving prey animals. Eyes are the species, namely that the Lycian primary sensory organs for feeding salamander is an opportunistic pre- and movements of the prey trigger a dator. response for eating (Duellman & Our study indicates that Lycian Trueb 1986, Pough & Magnusson 1992, Salamander prefers beetles, spiders, Stebbins & Cohen 1995). Moreover, centipedes, millipedes and terrestrial N West J Zool, 3, 2007 6 Çiçek, K. et al. adult insects provide less energy nopterans, hemipterans, homopterans compared to larvae because their and orthopterans in the food content bodies are covered with chitin. stem from the fact that possibility of Preference of larvae by the capture by the individuals is rather individuals is most probably due to low. The predator should than choose the urge for consuming the calories its diet relative to the abundance, or they need in a shorter period of time availability, of the most profitable (Jager & Rubin, 1982). Yet another prey type (Krebs, 1978). Poor-flying or possibility could be the fact that larval non-flying prey abundant under preys can be captured much easier stones were observed in the stomach than adult insects. contents of the population we have Considering the variety of prey examined, indicating that the Lycian groups observed in the area, the per- salamander is an active predator centages of preys in the stomach (sensu Huey & Pianka 1981). contents were expected to be different Despite small differences in per- than what we determined; however, centages, no statistically significant prey groups such as coleopteran difference was found between the larvae, centipedes, spiders and iso- sexes with respect to food contents. pods were seen to be consumed more Sexual dimorphism is generally lower compared to other prey groups. This in urodeles (61%) (Shine 1979). In is probably associated with the Lycian salamander, no statistically potentiality of prey capture by the significant difference was observed individuals. The high percentage of between sexes with respect to SVL. other prey groups such as spiders, This stems from the fact that females centipedes and terrestrial gastropods and males use the same microhabitat is connected with the large possibility during foraging. In addition, Düşen et of their occurrence under stones. This al. (2004) stated that there are no largely increases the likelihood of difference stomach contents between these preys to be used as food by sexes. predators. Furthermore, a widely In conclusion, Lyciasalamandra distributed prey animal in the biotope fazilae is an active predator usually like Formicidae (ants) is rarely feeding on poor-flying or non-flying encountered in the food content, terrestrial preys, and its food indicating that the individuals could composition can change in proportion exhibit fussy behaviour during to the species richness of the habitat it foraging. The findings in limited lives in. The fact that salamanders, amount of flying Insecta groups such such as Lycian salamander, inhabiting as dipterans, lepidopterans, hyme- forest biotopes feed on terrestrial
N West J Zool, 3, 2007 Food Habits of Lyciasalamandra fazilae: Preliminary data on Dalyan Population 7 invertebrates from that particular Demirsoy, A., (1998): Omurgasızlar - böcekler biotope is a clear indication of the dışındaki omurgasızlar (yaşamın temel kuralları), Cilt II/Kısım I. Meteksan Yayınları, significant role they play in balancing Ankara. the populations of these prey groups. Duellman, W. E., Trueb, L., (1986): Biology of We firmly believe that the data we amphibians. The Johns Hopkins University have obtained will contribute to the Press, London. Dunham, A. E., (1983): Realized niche overlap, little-known biology of this species, resource abundance, and intensity of and detailed studies to be conducted interspecific competition. pp. 261-280. In: on different populations of this Huey, R. B., Pianka, E. R., Schoener, T.W. endangered species will shed light on (eds.) Lizard ecology: studies of a model organism (eds.), Harvard University Press, researchers for successful imple- Cambridge, Mass. mentation of measures to be taken. Düşen, S., Öz, M., Tunç, R., (2004): Analysis of the stomach contents of the Lycian Sala- mander Mertensiella luschani (Steindachner, 1891) (Urodela: Salamandridae), collected References from Southwest Turkey. Asiatic
Herpetological Research 10: 164-167. Baran, İ., Atatür, M. K., (1998): Turkish Gautier, P., Olgun, K., Üzüm, N., Miaud, C. Herpetofauna (amphibians and reptiles). (2006): Gregarious behavior in a salamander: Republic of Turkey Ministry of Environment, attraction to conspecific chemical cues in Ankara. burrow choice. Behavioural Ecology & Başoğlu, M., Atatür M. K., (1974): The Sociobiology 59: 836-841. subspecies division of the Lycian Sala- Gunzburger, M. S., (1999): Diet of the Red Hills mander, Mertensiella luschani (Steindachner) salamander Phaeognathus hubrichti. Copeia in Southwestern Anatolia. İstanbul 523-525 Üniversitesi, Fen Fakültesi, Mecmuası, Seri B Hirai, T., Matsui, M., (2001): Food habits of an 39: 147-155. endangered Japanese frog, Rana porosa Başoğlu, M., Özeti, N., (1973): Türkiye amfibileri brevipoda. Ecological Research 16:737-743. (The amphibians of Turkey; taxonomic list, Huey, R. B., Pianka, E. R., (1981): Ecological distrubution, key for identification pp. 127-138). consequences of foraging mode. Ecology 62: Ege Üniversitesi, Fen Fakültesi, Kitaplar Serisi 991-999. No: 151, Bornova / İzmir. Jaeger, R. G., (1972): Food as a limited resource Chinery, M., (1992): Insectes d’Europe. Bordas, in competition between two species of Paris. terrestrial salamanders. Ecology 53: 535-546. Chinery, M., (1993): Insects of Britain & Western Jaeger, R. G., Rubin, A. M., (1982): Foraging Europe. Collins Guide to the Insects, Domino tactics of a terrestrial salamander: judging Books Ltd., Hong Kong. prey profitability. Journal of Animal Ecology Covaciu-Marcov, S.D., Cupşa, D., Telcean, I., Sala, 51: 167-176. G., Cicort, A. (2002): Trophical spectrum data of Krebs, J.R., (1978): Optional foraging: decision Salamandra salamandra (Amphibia, Urodela) rule for predators. pp. 23-63. In Krebs, J.R. from Budureasa region (Bihor county, and Davis, N.B. (eds) Behavioural ecology; Romania) (in Romanian with English abstract) an evolutionary approach. Blackwell Analele Univ. Oradea, Fasc. Biologie, Tom. IX, Scientific Publications, Oxford, London. pp.109-118.
N West J Zool, 3, 2007 8 Çiçek, K. et al.
Lodos, N., (1982): Türkiye Entomolojisi (Genel Roberts, M. J., (1995): Spiders of Great Britain uygulamalı faunistik), Cilt II. Ege Üniversitesi and Northern Europe. Collins, Harley Books, Matbaası, Bornova / İzmir. Cochester. Lodos, N., (1984): Türkiye Entomolojisi (Genel Shine, R. 1979. Sexual selection and sexual uygulamalı faunistik), Cilt III. Ege Üniversitesi, dimorphism in the Amphibia. Copeia 297- Ziraat Fakültesi Ofset Basımevi, Bornova / 306. İzmir. Stebbins, R. C., Cohen, N. W., (1995): Natural Lodos, N., (1989): Türkiye Entomolojisi (Genel history of amphibians. Princeton University uygulamalı faunistik), Cilt IV. Kısım I, Ege Press, United Kingdom. Üniversitesi, Ziraat Fakültesi Ofset Basımevi, Stoev, P., (2002): A Catalogue and key to the Bornova / İzmir. centipedes (Chilopoda) of Bulgaria. Pensoft Martof, B. S., Scott, D.C., (1957): The food of the Publishers, Sofia and Moscow. Salamander Leurognathus. Ecology 38: 494- Tok, C.V., Uğurtaş, I.H., Sevinç, M., Crochet, P.- 501. A., Papenfuss, T., Sparreboom, M., Kuzmin, Olgun, K., Miaud, C., Gautier, P., (2001): Age, S., Anderson, S., Denoël, M., Eken, G., Kılıç, growth, and survivorship in the viviparous T, Gem, E., (2006): Lyciasalamandra fazilae. In: salamander Mertensiella luschani from south- IUCN 2006. 2006 IUCN Red List of western Turkey. Canadian Journal of Threatened Species.
Burggren, W. W. (eds.) Environmental physiology of the amphibians. The University of Chicago Press, Chicago and London,
N West J Zool, 3, 2007