FEEDING ECOLOGY OF THE COMMON chamaeleon (Linnaeus, 1758) AND THE Chamaeleo africanus Laurenti, 1768.

DIMAKI M.1, LEGAKIS A.², CHONDROPOULOS B.³ & VALAKOS E.D. 4

1. The Goulandris Natural History Museum, 13, Levidou St., 145 62 Kifissia, Greece. 2. Zoological Museum, Dept. of Biology, Univ. of Athens, 157 84 Athens, Greece. 3. Section of Biology, Dept. of Biology, Univ. of Patra, 260 01 Patra, Greece 4. Section of Animal & Human Physiology, Dept. of Biology, Univ. of Athens, 157 84 Athens, Greece. INTRODUCTION In this work the results of the comparative food analysis of the Common Chameleon Chamaeleo chamaeleon (Linnaeus, 1758) and the African Chameleon Chamaeleo africanus Laurenti, 1768 are presented. This is the first time that information on the diet of Greek specimens of the Common Chameleon are presented. The distribution of the Common Chameleon in RESULTS Greece includes the Aegean islands of Samos, Chios, and . The African Chameleon is found in Greece only at Gialova near Pylos (Böhme et al., 1998; Dimaki et al., 2001). A comparison of the two species, among seasons and between sexes is presented, also a comparison Comparison between seasons of our results with those on the literature is made. Chamaeleo africanus Chamaeleo chamaeleon

N spring=13 N spring=13 N summer=31 N summer=31 N autumn=21 N autumn=21 N autumn=19 N autumn=19 45 18 28 24

40 16 24 20 35 14 20 30 12 16 16 25 10 12 12 C. africanus 20 8 8 15 6 8

F

10 F 4

% N % 4 4

% N % 5 2 0 0 0 0

crabs

snails

crabs

snails

hairs hairs

spiders

Diptera

spiders

snails snails

pebbles

Diptera

pebbles

Odonata

spiders spiders

Diptera Diptera

Odonata

pebbles feathers pebbles feathers

Phasmida

Hemiptera Chilopoda

Orthoptera

Odonata Odonata

Phasmida

Neuroptera Coleoptera

Hemiptera Chilopoda

Dictyoptera

Orthoptera

Dermaptera Embioptera

Neuroptera Coleoptera

Dictyoptera

Lepidoptera

Hemiptera Hemiptera

Dermaptera Embioptera

Orthoptera Orthoptera

Lepidoptera

Coleoptera Coleoptera

Dictyoptera Dictyoptera

Hymenoptera

plant remains plant

Lepidoptera Lepidoptera

Hymenoptera

plant remains plant

lizards' sloughs lizards'

Hymenoptera Hymenoptera Summer

plant remains plant remains plant Spring Spring sloughs lizards' Summer

larvae (Coleoptera) larvae Autumn

Autumn Autumn (Coleoptera) larvae Autumn

Isoptera (Diplopoda) Isoptera

Isoptera (Diplopoda) Isoptera

larvae (Coleoptera) larvae (Coleoptera) larvae

In autumn more Lepidoptera and pebbles were found in the stomachs of C. chamaeleon, while in the spring more plant remains and spiders. In autumn more pebbles were found in the stomachs but the arthropod diet of C. africanus does not seem to change significantly between summer and autumn. However, there is no difference between the number of each prey category items in the two examined seasons (t-test, p>0.05). MATERIALS & METHODS The niche breadth does not seem to change between the examined seasons (H' autumn= 0.859, H' spring=0.787 for C. chamaeleon and H' summer= 0.875, H' autumn=0.944 for C. africanus).

The stomach and faecal contents of 136 specimens were examined: 71 of the Common Chameleon (36 males and 34 females) and 65 of the African Chameleon (29 males and 29 females). Τhe remaining specimens are of unidentified sex. Most of the specimens were from A comparison of the two studied Greece and had been found killed by cars. We also had some museum species specimens from Africa, Asia, and the . Thirteen of the specimens of the Common Chameleon were found in N C.africanus=65 the spring, 4 in the summer, and 21 in the autumn. One specimen of the N C.chamaeleon=71 DISCUSSION 28

African Chameleon was found in the spring, 31 in the summer, 19 in the 24 autumn, and 2 in the winter. The rest were of unknown season. 20 The composition of the diet of the two examined species tends to differ. Differences in the prey composition among The stomach and faecal items of each specimen were counted and 16 different chameleon species have been reported {C. pumilus and C. namaquensis (Burrage, 1973), C. chamaeleon (Blasco et examined under a dissecting microscope provided with a micrometer 12 scale in the objective lens. We identified whole prey items and 8 al., 1985)}. However, it is not certain whether these differences are due to the preference of the species, the composition and

%N 4 recognizable body parts to order level. Each lizard’s sex was recorded 0 availability of the local prey fauna or the season. on the basis of the presence of hemipenes in males or ovaries in

hairs

crabs

snails

spiders

Diptera Stomach content is a measure of the food amount which has been ingested at the time of a lizard’s capture (Jameson et al.,

pebbles feathers females. Odonata

Phasmida

Hemiptera Chilopoda

Orthoptera

Neuroptera Coleoptera

Dictyoptera

Dermaptera Embioptera

Lepidoptera

Hymenoptera plant remains plant 1980). The mean and range of item number found in each examined stomach (13 items, 0-50 ) in C. africanus and (12 items, Diet was summarized in two ways: a) as a proportion of the total sloughs lizards' C.africanus

larvae (Coleoptera) larvae C.chamaeleon number of prey items in all the stomachs examined (%N) and b) as a (Diplopoda) Isoptera 0-210) in C. chamaeleon, falls within the range of other chameleon species {C. pardalis (Bourgat, 1971), C. namaquensis proportion of individuals eating a certain prey category (F).  (Burrage, 1973), C. chamaeleon (Blasco et al., 1985), and Pleguezuelos et al. (1999)}. Feeding niche breadth (H') was calculated using the Shannon-Wiener The composition of the diet of the two species tends to differ. However there is no statistically significant difference between the index: H' = -Σp log p (where p is the proportion of individuals using Many plant remains were found in the stomach and feces of C. africanus and C. chamaeleon which is in accordance with j j j total number of prey items of the two species (t-test, p>0.05). The prey category j) niche breadth does not seem to change between the two species (H' the presence of plant material in the stomach contents of other chameleon species {C. namaquensis (Burrage, 1973) and C. C. chamaeleon = 0.902, H' C. africanus = 0.921). These values pardalis (Bourgat, 1972)} and of C. chamaeleon (Burmeister, 1989) in northern but not in (Blasco et al., 1985), indicate that both species use a wide variety of prey. The most frequent category taken by C. chamaeleon was and Pleguezuelos et al. (1999), also in C. calyptratus, C. parsoni, C. dilepis, C. senegalensis and C. jacksoni (Sullivan & Hymenoptera (24.07%) followed by plant remains (18.72%), and Tremper 1991; Abate, 2002) . We presume that plant material is a regular dietary component of C. africanus and Diptera (12.67%). The most important prey taxa for C. africanus C.chamaeleon . were plant remains (21.61%), Coleoptera (19.43%), and Hemiptera (15.40%). The diet varies slightly with the season in both the studied species and this is in accordance with Blasco et al. (1985), Proportion of each prey category in the examined stomachs (% N) and proportion of Pleguezuelos et al. (1999), and Dimaki et al.(2001). chameleon individuals having eaten the same prey category (F) during spring and autumn According to our results the most frequent category taken by C. chamaeleon was Hymenoptera, plant remains, Diptera and Coleoptera. In Spanish population of C. chamaeleon the dominant prey taxa during all year are Orthoptera, Lepidoptera, Chamaeleo africanus Hymenoptera, Diptera and Hemiptera (Blasco et al., 1985), while according to Pleguezuelos et al. (1999) are Diptera, Chamaeleo chamaeleon Hymenoptera, Orthoptera and Heteroptera. In Northern Libya the dominant taxa of prey items for C. chamaeleon are summer autumn spring autumn Hymenoptera, Coleoptera and Diptera (Burmeister, 1989) and in are Orthoptera, Cicadidae and Cimicomorpha N=13, n=353 N=21, n=211 N=31, n=471 N=19, n=209 45 45 28 28 (Luiselli and Rugiero, 1996). 40 40 24 24 35 35 20 20 The presence of food items such as crab legs, snails, bird feathers, and lizard sloughs is not uncommon in {C. 30 30 16 16 25 25 namaquensis (Burrage, 1973)}. 20 20 12 12 15 15 8 8 Many worms (Cestoda, Nematoda and Trematoda) were found and is likely to have been parasites. 10 10

% % % 4 % 4 5 5 The composition of the diet of C. chamaeleon tends to differ between the two sexes, however this is not the case for 0 0 0 0

crabs crabs

hairs hairs

snails snails specimens from Spain (Pleguezuelos et al., 1999).

snails snails

spiders spiders

spiders spiders

Diptera Diptera

Diptera Diptera

pebbles pebbles

pebbles feathers pebbles feathers

Odonata Odonata

Odonata Odonata

Phasmida Phasmida

Hemiptera Chilopoda Hemiptera Chilopoda

Orthoptera Orthoptera

Hemiptera Hemiptera

Orthoptera Orthoptera

Neuroptera Coleoptera Neuroptera Coleoptera

Dictyoptera Dictyoptera

Coleoptera Coleoptera

Dictyoptera Dictyoptera

Dermaptera Embioptera Dermaptera Embioptera

Lepidoptera Lepidoptera Lepidoptera Lepidoptera We found pebbles and sand at a noticeable percentage for both examined species. This seems to be common for a

Hymenoptera Hymenoptera

Hymenoptera Hymenoptera

plant remains plant remains plant plant remains plant F remains plant F lizards' sloughs lizards' F sloughs lizards' F %N %N

larvae (Coleoptera) larvae (Coleoptera) larvae larvae (Coleoptera) larvae %N (Coleoptera) larvae %N chameleon, as C. namaquensis has been observed having ingested small stones, gravel and sand (Burrage, 1973). Johnson

Isoptera (Diplopoda) Isoptera (Diplopoda) Isoptera (1966) and Sokol (1971) suggest that deliberate lithophagy is common in lizards because it hastens the penetration of digestive juices into the bodies of the ingested insect prey and plant materials. Faecal analysis of 3 chameleon individuals that N: number of examined specimens were kept in terraria revealed the presence of a leaf piece and two small stones, not present in their food container but in the n: number of prey items terraria.

REFERENCES Prey composition of the two sexes

Abate, A. 2002. Cultivating Acacia Trees for Veiled Chameleons. Chameleon Information Network 43: 1. during the examined seasons Blasco, M., Romero, J., Sanchez, J.M. & Crespillo, E. 1985. La biología alimentaria y reproductora del Camaleón común, Chamaeleo chamaeleon (L.) (Reptilia, Chamaeleonidae) de la Peninsula Iberica. Monografias I.CO.NA., 43: 121-148. Böhme, W., Bonetti, A. & Chiras, G. 1998. The chameleons of the Greek mainland: taxonomic C. africanus C. chamaeleon N males=29 N males=36 allocation and conservation needs of a second European species (: Sauria: Chamaeleonidae). N females=29 N females=34 Herpetozoa 11 (1/2): 87-91. 28 30 24 Bourgat, R. 1971. Vie en captivité des Caméleons malgasches. Aquarama. 5(16): 41-44. 24 Bourgat, R. 1972. Nouriture du Caméleon: Regimen alimentaire et capture des Proies. Ceyl. J. Sci. 20 18 10(1):1-15. 16 12 12 Burmeister, E.G. 1989. Eine Walzenspinne (Solifugae, Galeondidae) als Nahrung des Gemeinen 8

Chamaleons (Chamaeleo chamaeleon Linnaeus, 1758). Herpetofauna 11 (58): 32-34. 4 6

% N % N % 0 Burrage, B.R. 1973. Comparative ecology and behaviour of Chamaeleo pumilus pumilus (Gmelin) and 0 C. namaquensis A. Smith (Sauria: Chamaeleonidae). Ann. S. Afr. Mus. 61: 1-158.

crabs

snails

hairs

snails

spiders

Diptera

pebbles spiders

Diptera

Odonata Dimaki, M., Valakos, E. D., Legakis, A., Chondropoulos, B. & Bonetti, A. 2001. Preliminary results on pebbles feathers

Odonata

Phasmida

Hemiptera Chilopoda

Orthoptera

Neuroptera Coleoptera

Dictyoptera

Hemiptera

Dermaptera Embioptera Orthoptera

Lepidoptera Coleoptera

Dictyoptera

Lepidoptera

Hymenoptera the feeding ecology of the African Chameleon Chamaeleo africanus Laurenti, 1768 from the southwestern remains plant

Hymenoptera

plant remains plant lizards' sloughs lizards' Males Males Peloponnese, Greece. Herpetologia Candiana Lymberakis, P., Valakos, E., Pafilis, P. & Mylonas M. (eds) larvae (Coleoptera) larvae Females Females Pp: 57-63. (Diplopoda) Isoptera (Coleoptera) larvae Jameson, Jr.E.W., Heusner, A.A. & Lem, D. 1980. Seasonal, sexual and altitudinal variations in stomach content and ingested fat in Sceloporus occidentalis. J. Herp. 14(3): 255-261. The composition of the diet of C. chamaeleon tends to differ between the two Johnson, D.R. 1966. Diet and estimated energy assimilation of three Colorado lizards. Amer. Midl. Nat. sexes. However, this is not the case for C. africanus. There is no statistically 76 (2): 504-509. significant difference between the total number of each prey category items of the Pleguezuelos, J. M., Poveda, J.C., Monterrubio, R & Ontiveros, D. 1999. Feeding habits of the Common two sexes for both the examined species (t-test, p>0.05). Chameleon, Chamaeleo chamaeleon (Linnaeus, 1758) in the Southeastern Iberian Peninsula. The niche breadth does not seem to change between the two sexes (H' male=0.917, Journal of Zoology. 45 (1): 267-276. H' female=0.923for C. africanus and H' male=0.921, H' female=0.840 for C. Sokol, O. M. 1971. Lithophagy and geophagy in . J. Herp. 5: 69-71. chamaeleon). Sullivan, M. & Tremper, R. 1991. Omnivorous Chameleons? Chameleon Information Network 5: 7. The most frequent category taken by both sexes of C. africanus were plant remains (21.62% in males and 23.62% in females) followed by Coleoptera (18.18% in males Acknowledgments and 17.09% in females) then Hymenoptera in males (13.51%), Hemiptera in females (16.58%) and Hemiptera in males (13.27%), Hymenoptera in females (11.81%). C. chamaeleon Many thanks to Mr. L. van Tuijl for his help during my visit to Zoological Museum of Amsterdam. This The most important prey taxa taken by males of C. chamaeleon was Hymenoptera visit was realized through a grant from LSF/ZMA project. Many thanks also to E. Zimalis and the Museum (15.32%) followed by Diptera (13.31%) and Coleoptera (12.50%). The most frequent of Natural History of Samos for the financial support during my field work in Samos island during 2000. food category for females were Hymenoptera (27.68%), plant remains (23.72%) and Diptera (12.52%).

9th International Congress on the Zoogeography and Ecology of Greece and Adjacent Regions, Thessaloniki, Greece, 22-25/5/2002