Amphibia-Reptilia 29 (2008): 329-336
Dietary strategy of a Pyrenean lizard, Iberolacerta aurelioi, living in a poor resources alpine environment Fèlix Amat1 , Valentín Pérez-Mellado2 , José Ángel Hernández-Estévez2 , Teresa García Díez2 Abstract. We report the first study of diet composition of a Pyrenean lizard of the genus Iberolacerta, the Aurelio’s lizard, I. aurelioi, living in an alpine rocky slope at 2300 m of altitude in Andorra. Diet composition was studied during two years from 289 faecal pellets containing 966 prey items. Number of prey per pellet shows annual, seasonal and sexual differences. Diet of the species is poorly diverse, mainly dominated by insects, but we find clear evidences of opportunistic cannibalism based on the presence of toes and scales in feces. In addition, we detected minor sexual, annual and month differences in prey presence and abundance. Low amplitude of trophic niche width and prey diversity, as well as predation on clumped prey and cannibalistic behaviour suggest that Iberolacerta aurelioi has a remarkable dietary strategy in response to strong thermal and food availability constraints at high mountain habitats. Keywords: diet, Iberolacerta aurelioi, lizard ecology.
Introduction Lacertid lizards are small and primarily active foragers on small invertebrates, especially arthropods (Vitt and Pianka, 2007). Diet composition and segregation among species, sexual dietary divergence, prey recognition and its selection have been widely studied in a set of diverse environments from deserts to Mediterranean landscapes and Alpine ecosystems (see for example Díaz and Carrascal, 1990; Castilla et al., 1991; Pérez-Mellado, 1992; Pérez-Mellado and Corti, 1993; Burke and Mercurio, 2002; Bombi et al., 2005; Perera et al., 2006; Luiselli, 2008). In this context, if potential prey abundances are higher and relatively stable through the time, a specialized diet became a suitable strategy. On the other hand, with low prey availability and/or acute temporal changes or when lizard populations are very dense, involving a strong competition among individuals, a generalized trophic strategy could be the most successful
1 - Museu de Granollers – Ciències Naturals, Francesc Macià 51, 08400 Granollers, Spain e-mail:
[email protected] 2 - Departamento de Biología Animal, Facultad de Biología, Universidad de Salamanca, Campus Unamuno s/n., 37071 Salamanca, Spain e-mail:
[email protected]
option (Schoener, 1971; Sih, 1993). The Iberian lizards of the genus Iberolacerta live at high altitudes in Pyrenees, from 1900 to 2800 m of altitude and other mountain areas of the Iberian Peninsula. The three Pyrenean endemic species (I. aurelioi, I. aranica and I. bonnali) are specialized in climbing and running on sunny rock slopes and boulders (Arribas, 2000), with an annual activity period from late May to September. These high mountain areas are poor in dietary resources (see for example Pérez-Mellado et al., 1991; Roig, 1998). Hence, it is crucial for lizards to manage efficiently prey availability during their very short period of activity. To date, diet and feeding strategies of Pyrenean Iberolacerta are barely unknown and only there is a scarcely informative study from I. bonnali (Martínez-Rica, 1977), while the diet of I. cyreni, a lizard living in rocky meadows in Central Iberian Peninsula, has previously studied (Pérez-Mellado, 1982; Pérez-Mellado et al., 1991). The aim of this study is to examine the diet composition and its temporal variation in a population of the Aurelio’s lizard, Iberolacerta aurelioi. Materials and methods Field work was done in 2004 and 2005, during the activity period of the species, from June to September in an alpine
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Figure 1. A: Annual and monthly variation in the number of prey items per pellet, in females, males and juveniles (JN: June, JL: July, AU: August, S: September). B: Monthly variation of prey presence (number of feces containing the most common prey categories) in males during 2004 (AR: Araneae, OR: Orthoptera, HO: Homoptera, DI: Diptera, LE: Lepidoptera, CO: Coleoptera, HY: Hymenoptera and FO: Formicidae). rocky slope in Port del Rat (Central Pyrenees, NW Andorra, UTM 31T 375 472) at 2300 m.a.s.l. At the study site, I. aurelioi is the only lizard species. Lizards were manually caught, sexed by examination of the external cloacal morphology and snout-vent length (SVL) measured with a digital caliper (precision of ±0.1 mm). Minimum SVL of gravid females and sexually active males are above 49 mm (unpublished data), so individuals larger than this size were classified as adults. Thus, three sex and age categories were considered: adult males, adult females and juveniles. Because I. aurelioi is a vulnerable species, strictly protected by Andorran laws, we discarded the analysis of stomach contents and used fecal samples to perform the analysis. Fecal pellets were collected keeping lizards in individual cages during approximately 12 hours. Feces were analyzed through a binocular microscope. In order to study diet composition we identified, measured and classified remains in a mixed scheme combining taxonomic orders and ontogenic stages (see for example Pérez-Mellado et al., 1991). We examined sex and age categories, year and month of sampling as factors influencing the number of prey per pellet (prey richness) using an ANOVA analysis on logtransformed values. Diet composition was described by a)
relative prey presence (percentage of individuals consuming each item category) and b) prey abundance (percentage of a given prey item relative to the total number of prey items) and c) prey diversity using Shannon index (Hs ). In order to test annual, monthly and sex-age categories differences on prey presence and abundance we use Chi square test. Dietary overlap among sex or age categories (males versus females and adults versus juveniles) was estimated by means of Pianka’s index. We compare the trophic niche amplitude of Iberolacerta aurelioi with other lizard species by means of the standardized Levins’s index of niche breadth (Bs ).
Results From 203 adults (104 females and 99 males) and 86 juveniles, a sample of 289 fecal pellets was collected in 2004 and 2005. Sample size is nearly equal in both years allowing the identification of 22 item categories from a total of 966
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prey items. ANOVA analysis showed significant differences on the average number of prey per pellet among years (F1,263 = 0.574, P = 0.009), months (F3,263 = 0.243, P = 0.033) and sex-age categories (F2,263 = 0.330, P = 0.019). No interaction effects were detected among these factors (year × month, F3,263 = 0.107, P = 0.275; month × sex-age, F6,263 = 0.146, P = 0.107; year × sex-age categories, F2,263 = 0.124, P = 0.225; month × year × sex-age categories, F6,263 = 0.025, P = 0933). Thus, the number of prey items is comparatively larger in pellets collected in 2005 than in 2004, and in females, followed by males and juveniles (fig. 1). In adults, monthly variation of number of prey per pellet showed a maximum in July 2004 and August 2005 contrasting with the maximum value of juveniles obtained in August 2004. Diet composition analysis reveals that I. aurelioi is basically an insectivorous lizard (ta-
ble 1). The most common prey for all sex and age categories in both years were Araneae, Orthoptera, Homoptera, Lepidoptera, Formicidae, Hymenoptera, Diptera and Coleoptera. Flying arthropods were important, representing 30% of the overall prey items. Interestingly, lacertid remains, basically scales, but also two toes in one pellet, were relatively common (table 1). The analysis of age or sex, annual and monthly variation of the most common prey showed several differences. Considering both years and the whole activity period, more males ate Formicidae and less Coleoptera than females, while few juveniles ate a minor quan2 = 42.873, tity of large prey as Orthoptera (χ14 P < 0.001). In addition, prey presence did not differ significantly among years, but males and females showed monthly variation in 2004 2 = 43.531, P = 0.002 and and 2005 (χ21 2 χ21 = 45.44, P = 0.001). In July, a larger number of males ate more frequently large prey
Table 1. Diet of Iberolacerta aurelioi summarized by relative presence (%P) and abundance (%A) of a given prey item, percentage of flying prey and diversity index (Hs ) for each population category, pooling the samples of 2004 and 2005. Males Prey item Araneae Opilionida Acarida Isopoda Plecoptera Orthoptera Orthoptera Nymphs Dictyoptera Isoptera Homoptera Heteroptera Diptera Diptera larvae Lepidoptera Lepidoptera larvae Coleoptera Coleoptera larvae Hymenoptera Formicidae Undet. arthropods Undet. insect larvae Lacertidae No of prey items % Flying prey Hs
%P 16.1 – 4.0 1.0 – 15.1 – 2.0 1.0 14.1 2.0 24.2 1.0 22.2 2.0 27.2 1.0 30.3 42.4 4.0 17.1 27.2 337 29.0 2.278
Females %A 4.7 – 1.4 0.2 – 4.4 – 0.5 0.5 5.0 0.8 8.6 0.2 7.7 0.5 13.3 0.2 12.7 27.0 1.1 5.9 4.1
%P 29.8 – 0.9 – 0.9 19.1 0.9 – 0.9 0.1 4.8 22.1 – 18.2 – 47.1 2.8 31.7 22.1 0.9 22.1 5.7 380 32.8 2.214
Juveniles %A 8.1 – 0.2 – 1.0 5.2 0.2 – 0.2 5.2 1.5 8.9 – 6.5 – 20.2 0.7 16.8 16.5 0.2 6.0 1.8
%P 24.4 1.1 2.3 – 1.1 9.3 – 2.3 – 31.3 1.1 24.4 – 19.7 1.1 31.3 3.4 22.0 30.2 1.1 12.7 8.1 249 29.7 2.167
%A 9.6 0.4 0.8 – 0.4 3.6 – 0.8 – 13.6 0.4 13.2 – 7.6 0.3 14.8 0.4 8.4 16.8 0.4 4.4 2.8
Total %P 23.5 0.3 2.4 0.3 0.6 14.5 0.3 1.7 0.6 20.7 2.7 0.2 0.3 20.0 1.0 35.6 2.4 28.3 31.4 2.0 17.6 9.6 966 30.7 2.349
%A 7.3 0.1 0.8 0.1 0.5 4.5 0.1 0.5 0.3 7.3 10.3 9.9 0.1 7.0 0.3 16.4 0.7 13.2 20.2 0.6 5.5 2.8
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(a) Figure 2. Monthly variation of prey presence (number of feces containing the most common prey categories) in females during 2005 (abbreviations as in fig. 1).
as Coleoptera and Lepidoptera in contrast to the large number of feces containing Formicidae and Hymenoptera in September (fig. 2A). Females showed a similar pattern in 2005 sample, with more individuals eating larger prey in June and small and clustered prey in August (fig. 2B). The analysis of data considering only the most common prey: Araneae, Orthoptera, Homoptera, Lepidoptera and Diptera, showed differences of prey abundance among sex and age categories, pooling all months and years 2 (χ10 = 46.864, P < 0.001, figs 3 and 4) and monthly variation in females during both years 2 (2004: χ15 = 9433.764, P = 0.003 and 2005: 2 χ15 = 33.536, P = 0.003). Presence and abundance of lizard remains in feces are not affected by annual, monthly or sex and age factors. Overall niche breadths (by Shannon index of diversity) were slightly minor in juveniles
than adults (table 1). On the other hand, all the comparisons among sex and age categories showed a large overlap in their diets (males and females, Pianka’s index: 0.908; immatures and adults, Pianka’s index: 0.956).
Discussion According to our results, Iberolacerta aurelioi can be considered an insectivorous lizard, able to adjust its feeding strategy to a thermally and prey restrictive environment, including the observed seasonal and annual shifts. Interestingly, this dietary constraint results in occasional cannibalistic behavior. Fecal pellets from females had more prey than those from males as in Zootoca vivipara (Roig et al., 1998). Egg production is likely more energetically expensive
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(b) Figure 2. (Continued).
than spermatogenesis. Thus, females should have higher levels of annual activity to recover fat reserves, with an intense foraging, especially in habitats of low prey availability. Comparing prey richness in 2004 and 2005, we observe nearly the same pattern in all sex and age categories and months. Bigger values recorded in last year could reflect higher prey availability due to favorable climatic conditions during 2005 (personal observation). Nevertheless, both in males and females, maximum prey richness was approximately delayed one month, probably as a consequence of late snow thaw. This situation may force lizards to perform a higher rate of food intake to compensate a shorter period of prey availability in 2005. The examination of monthly variation of prey richness showed lower values in pellets from males and females during June, followed by a peak in July or August. Juveniles showed an inverse monthly cy-
cle. If prey availability was equal for the whole population of lizards, this result could suggest that adult investment in reproductive behaviour could restrict the time available for foraging. The occasional cannibalism reported in this study is a clear evidence of a strong aggressive interaction among individuals. In addition, the smaller body size of juveniles may constrains the size of consumed prey, excluding larger prey and producing a lower diet diversity in juveniles, as showed in other lacertid lizards (Carretero and Llorente, 1983; Castilla et al., 1991). I. aurelioi spends its activity time climbing on rocky surfaces in boulders and walls, mainly during the morning and afternoon, when ambient temperatures are lower. At midday, lizards remain most of the time upon rocks and mat grass to avoid too high temperatures (unpublished data). The dominance of grounddwelling prey as Coleoptera, Orthoptera, Formi-
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Figure 3. Prey abundances (number of items for the most common prey categories) in fecal pellets in males, females and juveniles in both years of study (abbreviations as in fig. 1).
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Figure 4. Comparative prey abundances in fecal pellets of females in 2004 and 2005 (abbreviations as in fig. 1).
cidae or Homoptera is consistent with this behaviour. Alpine meadows are very poor in terms of invertebrate productivity, experiencing some temporal fluctuation, as studies of invertebrate prey productivity reveals (see, for example the case of Val d’Aran, Central Pyrenees, at 1800 m in Roig, 1998). At higher altitudes, rocky slopes inhabited by I. aurelioi, could be even more trophically restricted. The diet of I. aurelioi reflects this poor availability, with a low prey diversity and high consumption of ants and other Hymenoptera, as well as the unusual inclusion of conspecifics. Lizards from comparatively more productive and unpredictable Mediterranean habitats also include large quantities of ants in their diet (Pollo and PérezMellado, 1988). As lacertid lizards eating their shed skin has been never reported, despite the large number
of researches and field observations, the presence of lizard remains suggests the existence of aggressive encounters among individuals, resulting in tail or digit ingestion. This behaviour was observed in insular lizards submitted to an intense competition for prey in populations of high lizard density (Pérez-Mellado, 1989; Pérez-Mellado and Corti, 1993 and references therein). In Aurelio’s lizard, the situation seems rather different, as lizard density is comparatively lower than in other lizard populations (99-235 individuals/hectare, unpublished results from a capture-mark and recapture study). Based on the low occurrence of lizard remains in the diet, this feeding strategy can be considered an opportunistic activity, but could be important as a response to low prey availability. An additional evidence of low food availability is the large diet overlap among sex and age cate-
336 gories, as in other alpine lizards (Pérez-Mellado et al., 1991; Roig, 1998). The slight diet differences between males, females, and juveniles and the reduced tendency to eat smaller prey in juveniles, could be an additional indication of prey competition. Nevertheless, we showed small sexual, seasonal and annual differences in prey presence and abundance. Temporal patterns of invertebrate abundances in alpine meadows (Roig et al., 1998) indicated that some potential prey as Orthoptera, are strongly seasonal. Diet diversity of I. aurelioi (Bs = 0.117) is extremely low compared to other lacertid lizards living in the Mediterranean basin (in Podarcis tiliguerta, Bs = 0.60, and in Algyroides fitzingeri, Bs = 0.35, see Capula and Luiselli, 1994; for Scelarcis perspicillata, Bs ranged from 0.225 to 0.638, see Perera et al., 2006) or in alpine habitats for Iberolacerta cyreni (Bs = 0.238, Pérez-Mellado et al., 1991). We suggest that low prey availability in the alpine environment inhabited by Iberolacerta aurelioi is probably the cause of its lower diet diversity.
Acknowledgement. Funding and logistic help was provided by Ministeri d’Agricultura i Medi Ambient of Andorra and specially by Josep Maria Naudí. We also thanks Joan Manuel Roig his help in field work.
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Received: August 26, 2007. Accepted: February 10, 2008.
