Comparative Food Habits and Body Size of Five Populations of Elaphe quatuorlineata : The Effects of Habitat Variation, and the Consequences of Intersexual Body Size Dimorphism on Diet Divergence
Authors: ERNESTO FILIPPI, LORENZO RUGIERO, MASSIMO CAPULA, DARIO CAPIZZI, AND LUCA LUISELLI
The comparative diet and body size of the Four-Lined Snake (Elaphe quatuorlineata ), one of the largest and more vulnerable species of snakes in Mediterranean central Italy, were studied in ?ve different habitats. Data given here collated both literature and original data. Overall, females were signi?cantly larger than males but the strength of these differences varied considerably with sample size. Overall, small mammals (almost exclusively rodents) accounted for the main part of the diet (66.7%), followed by birds and their eggs (mainly Passeriformes; 26.4%), and by lizards (6.9%), although the number of eggs in the diet was probably greatly underestimated. In qualitative terms, both sexes fed on the same prey types, but, quantitatively, males and females differed signi?cantly in terms of prey composition; females fed on more birds and fewer lizards than males. Rodents were the most important prey source in most habitat types, although birds were preyed upon slightly more frequently in the wet habitat than rodents, which, nonetheless, still represented a important prey source. Four-Lined Snakes started feeding in early April and continued feeding until early November. The monthly frequency of occurrence of birds in snake stomachs differed signi?cantly from that of small mammals; birds were taken almost exclusively in April and May (and mainly by females), and small mammals were taken all throughout the annual feeding cycle of snakes.
Studies on the feeding ecology of snakes have proliferated during the last decade, and we have learned a great deal about the general ecological correlates of snake dietary habits, especially about the relationships between snake body size and prey preferences (Shine, 1991; Greene, 1997). This applies to species found in Europe, North America, and Australia, where research efforts are most concentrated (e.g., Gregory, 1984; Drobenkov, 1995; Gregory and Skebo, 1998), but also in Africa (e.g., Luiselli et al., 2002a, b; Luiselli, 2003), Asia (e.g., Shine and Sun, 2002, 2003), and South America (e.g., Costa Pinto and Lema, 2002; Lopez and Giraudo, 2004), including marine species as well (e.g., Shine et al., 2004). Hence, detailed data on food habits (especially lists of prey items collected from free-ranging individuals) and body size (especially highlighting sexual size dimorphism, e.g., Shine, 1991, 1994) are now available for tens of different species belonging to many snake clades and from divergent ecological contexts.
However, the great majority of these studies report data on single populations (e.g., Luiselli et al., 1996, 1997) or a collection of prey items from specimens opportunistically collected in numerous localities across a species’ range (e.g.,Shine et al., 1996), and few attempts have been made to compare variation in diets and body size among populations of a single snake species. However, these comparative studies are crucial if we are to gain a thorough understanding of the feeding strategies of the various species (e.g., Luiselli et al., 2002b; Luiselli, 2003). Indeed, some comparative analyses of interpopulational variation in diet composition have already been published (e.g., Kephard, 1982; Gregory and Nelson, 1991; King, 1993), although no such comparisons are available as yet for most species.
The Four-Lined Snake (Elaphe quatuorlineata ), one of the largest snake species in Europe (>2 m in length), is distributed across central and southern Italy, the Balkans, Romania, and part of the former Soviet Union (i.e., regions surrounding the Black Sea and the Caspian Sea) (Bruno and Maugeri, 1990). Currently, it is regarded as vulnerable in several areas of its range and in particular in Italy, because of forest habitat fragmentation (Luiselli and Capizzi, 1997; Filippi and Luiselli, 2000) and probably because of the accumulation of pesticides in prey tissues (Cattaneo and Carpaneto, 2000). Although this species has been the subject of some ecological studies (e.g., Pozio, 1976; Cattaneo, 1979; Capizzi and Luiselli, 1997), there has been no comprehensive study into its feeding ecology and its body size variation in relation to sex and habitat type.
TABLE 1. ATTRIBUTES OF THE STUDY AREAS AND SAMPLE SIZES.N = number of snakes examined; n = number of prey items; sample sizes for N include both ?rst captures and later recaptures.
|Study area||Habitat features/Sample sizes||Reference|
|La Marcigliana||agro-forest land; 50 m a.s.l.||Capizzi and Luiselli, 1996|
|N = 82 (43 males, 39 females); n = 49|
|Tolfa Mountains||open grassy area with interspersed bushes; 150-250 m a.s.l.||Capizzi and Luiselli, 1997|
|N = 89 (44 males, 45 females); n = 62|
|Tor Lupara||mixed forest fragment surrounded by unsuitable areas; 50 m a.s.l.||Rugiero and Luiselli, 1996|
|N = 65 (35 males, 30 females); n = 30|
|Monterano||dense chaparral-type bushland; 200 m a.s.1.||this study|
|N = 56 (23 males, 33 females); n = 12|
|Rio Fiume valley||banks of a stream with wet marshes around; 150 m a.s.l.||this study|
|N = 53 (27 males, 26 females); n = 21|
The purpose of this paper is to document interpopulational variation in feeding ecology and body size of Four-Lined Snakes in different habitats in Mediterranean central Italy. More speci?cally, we ask the following questions: (1) Considering that the genus Elaphe is a problematic and genetically heterogeneous group (Utiger et al., 2002), and that some species showed larger-male sexual size dimorphism (SSD) while other species showed larger-female SSD (e.g., Bruno and Maugeri, 1990; Shine, 1994; Rugiero et al., 2002), does the Four-Lined Snake exhibit a larger-male or a larger-female SSD? (2) If indeed an SSD exists in this species, does it in?uence the intersexual dietary preferences? We ask this question because body size differences between the sexes may parallel differences in prey size and type (Shine, 1986; Camilleri and Shine, 1990; Houston and Shine, 1993). However, another reason for dietary differences between the sexes may be the higher nutritional requirements of reproductive females compared to males (Bonnet et al., 1998, 2001; Shine, 2003). (3) Does diet composition of Four-Lined Snakes vary among different habitat types in Mediterranean central Italy? (4) Considering that the Mediterranean climate is strongly seasonal and hence seasonal variations in the diets can be expected, are there seasonal differences in dietary composition of the Four-Lined Snakes?
MATERIALS AND METHODS
Study areas.— Our study is based on original ?eld research conducted from March 1985 to September 2004 and also includes datasets from previously published research on E. quatuorlineata (Rugiero and Luiselli, 1996; Capizzi and Luiselli, 1996, 1997). The study is based on data collected from Four-Lined Snake populations at ?ve different study areas, each representing different habitat types where these rare snakes are found (Table 1): (1) Agro-forest area (‘‘La Marcigliana,’’ about 15 km northeast of Rome, central Italy) was characterized by a coppiced wooded area (Quercus cerris , Quercus robur , Ulmus minor , Acer campestris , Fraxinus ornus , and Laurus nobilis as main trees) with thick underbrush (Crataegus monogyna , Rosa canina , Prunus spinosa , and Euonimus europaeus ), surrounded by semi-cultivated ?elds; (2) bushy pasture area (‘‘Tolfa,’’ about 60 km north of Rome) was a hilly area with herbaceous pastures, interspersed with bushes (Rubus ulmifolius , C. monogyna , and Cytisus scoparius ) and pilestones; (3) residual forest area (‘‘Tor Lupara,’’ about 17 km east of Rome) was a small (= 30 ha surface) forest patch (of Q. cerris , U. minor , and Carpinus betulus ) entirely surrounded by herbaceous pastures and busy roads; (4) ‘‘Macchia’’ area (Monterano, about 50 km north of Rome) was hilly and characterized by thick evergreen Mediterranean chaparral uniformly distributed throughout the whole study area (about 100 ha); (5) wet area (Rio Fiume valley, about 70 km northwest of Rome) included the evergreen vegetation growing along the banks of a seasonal, transparent-water stream, on average with water depth >1.2 m from March to June, and <0.5 m from July to October.
All these study areas are characterized by a nearly identical microclimate, which has been classi?ed by Spada (1978) as ‘‘hypomesaxeric Mediterranean subregion type B.’’ Hence, the eventual interpopulation differences observed in snake feeding ecologies are not likely to be in?uenced by any local difference in microclimates.
Protocol.— Field methods were nearly identical at all study areas and are detailed in the original literature sources (see Table 1). Fieldwork was conducted under all climatic conditions. We searched for snakes along standardized routes in the various micro-habitats frequented by snakes at the study areas. At each study area, we spent the same research effort (33 days in the ?eld in each year of study), and each ?eld day lasted 7 to 8 hours. Every effort was made to maintain an equal effort during the various diel phases. Snakes were captured by hand. Upon capture, a number of different variables was recorded: sex, by analyzing the shape of the cloacal region, snout-vent length (SVL, to the nearest ± 0.5 cm), head length, and weight (measured to ± 0.1 g with an electronic balance). Adults were recognized from juveniles and sub-adults based on differing dorsal color patterns (Bruno and Maugeri, 1990). Snakes were individually marked by ventral scute clipping for future identi?cation. Snakes were then palpated until regurgitation of ingested food or defecation occurred. In addition, specimens found dead during our surveys (e.g., snakes killed by farmers, cars, etc.) were dissected to determine if prey were present.
Prey items were identi?ed to the lowest taxonomic level possible. The mass of prey items was estimated at the time of ingestion, when possible, by comparing the item to intact con-speci?cs of various sizes from our own personal collection or measuring biomass when specimens were undigested. Data were collected from both stomachs and feces. To avoid double counts of the same food item, we generally recorded prey data from either stomach contents or feces but not both, unless fecal and stomach samples contained obviously different material (e.g., mammal hair vs. a lizard).
In the case of stomach contents, we always counted the number of prey items rather than number of snakes with a particular prey type. Because Four-Lined Snakes are among the rarest snakes in central Italy, it is dif?cult to get a considerable number of prey items from each study area by analyzing every captured specimen for food only once. Therefore, we included food data collected on different occasions from the same individuals that were captured several times. Although this method may have some bias in the case that a single specimen may have a disproportionate preference for a particular type of food, it appeared to be the best method to get a large enough sample of food items for inter-locality comparisons. Diet data were not collected from snakes if they were recaptured within 14 days from the previous capture. Vouchers (of both prey and predators) were deposited in the herpetological collections of the Centre of Environmental Studies ‘‘Demetra’’ (Rome), F.I.Z.V. (Rome), and Municipal Museum of Zoology (Rome).
All statistical tests were done with alpha set at 0.05. Means and ± 1 SD are presented. Statistical tests were done by Statistica version 6.0 for Windows PC package. A multivariate analysis of similarity in diet composition among the different populations of snakes was done by a grouping analysis of UPGMA type (Unweighted Pair-Group Method using Arithmetic Averages) applied to a Euclidean distance matrix (Digby and Kempton, 1987), and the reliability of the results were evaluated by the co-phenetic correlation coef?cient calculated by NTSYS 87 program elaborated by James Rohlf (Digby and Kempton, 1987).
Mean body sizes.— SVL means and dispersion measures for both sexes at the various study areas are given in Fig. 1. Overall, females were larger than males (x = 139.9 ± 32.3 cm, n = 70 versus x = 124.6 ± 17.2 cm, n = 82; t = -3.51, df = 150, P = 0.0003). A two-way ANOVA (SVL X habitat type + sex) revealed that there were signi?cant differences in (ln-transformed) SVL between sexes at each locality (= female larger; F1, 142 = 62.38, P < 0.0001) and among localities (F4, 142 = 11.18, P < 0.0001), and the interaction term in the ANOVA between sex and locality was not signi?cant (F4, 142 = 0.70, P = 0.595; in this case it represents % divergence, not absolute SVL differences between the sexes).
Fig. 1. Mean SVL (±SD and SE) for Four-Lined Snakes in the ?ve study areas. Only the SVL of snakes captured for the ?rst time are included. Symbols: AG = agro-forest; BP = bushy pasture; RF = residual forest; MA = macchia; WET = wet area; M = males; F = females. Sample sizes: AG–8 and 8 (males and females), BP–17 and 14, RF–13 and 11, MA–24 and 16, WET–20 and 21. For statistical details, see the text.
A Tukey HSD post hoc test revealed that, with regard to males, specimens from bushy pastures were signi?cantly smaller than males from any other study area (at least P < 0.006 in each pairwise comparison). Females from agro-forest and bushy pastures habitats were signi?cantly smaller than those of the other three study areas (at least P -0.008 in each pairwise comparison). Repeating the analyses with the largest 20% of each sex in the sample (in order to overcome problems of one sex maturing at a smaller size, and hence to demonstrate which sex attains larger maximum size, not just average size), it resulted that females were signi?cantly larger than males (x = 162.7 ± 11.6 cm, n = 14 versus x = 146.1 ± 5.7 cm, n = 21; one-way ANOVA: F1, 33 = 31.79, P < 0.0001).
Overall diet analysis.— In total, we examined 345 snakes, of which 154 had identi?able prey items (44.6% of the total sample examined), for a total of 174 prey items (Table 2). Overall, small mammals made up the majority of the diet (66.7% of the total number of prey items), followed by birds, bird eggs (primarily Passeriformes; 26.4%), and by lizards (6.9%). The number of bird eggs was probably underestimated, because of dif?culties in detecting egg remains by abdominal palpation and fecal analysis. Rodents accounted for by far the greatest proportion of prey ingested (Table 3), especially species of Apodemus (n = 42 items) and Rattus (n = 30). The frequency of these two genera in the diet was also probably underestimated because several of the rodent remains that remained unidenti?ed (cf. Table 2) belonged to one of the two genera but were too damaged for de?nitive identi?cation. Rattus spp. accounted for a total biomass of approximately 6869g versus 1097g for Apodemus spp.
TABLE 2. SUMMARY OF THE DIET DATA OF FOUR-LINED SNAKES,POOLED BY STUDY AREA AND DIVIDED BY SEX.
|Chicks or eggs of aquatic birds||4||4.4||5||5.9|
* Because the number of eggs eaten was impossible to count exactly, we indicate the number of snakes containing eggs as a prey item.
TABLE 3. SUMMARY OF THE DIET DATA OF FOUR-LINED SNAKESFROMTHE VARIOUS STUDY AREAS. Data are pooled for males and females. Data came from Capizzi and Luiselli, 1996 (agro-forest); Capizzi and Luiselli, 1997 (bushy pastures), Rugiero and Luiselli, 1996 (residual forest), and original (macchia and wet area).
|Agro Forest||Bushy Pastures||Residual Forest||Macchia||Wet Area|
|Apodemus sp.||15 (30.6%)||11 (16.9%)||12 (40.0%)||4 (33.3%)|
|Rattus rattus||5 (10.2%)||3 (4.6%)||4 (33.3%)|
|Rattus norvegicus||3 (6.1%)||3 (4.6%)||6 (28.6%)|
|Rattus sp.||3 (10.0%)||3 (14.3%)|
|Mus domesticus||2 (3.1%)|
|Clethrionomys glareolus||7 (14.3%)||11 (16.9%)|
|Microtus savii||1 (8.3%)|
|Muscardinus avellanarius||4 (6.2%)|
|Undetermined Rodentia||13 (20.0%)||3 (10.0%)|
|Crocidura sp.||3 (6.1%)|
|Turdus merula||4 (6.1%)|
|Carduelis sp.||1 (1.5%)|
|Serinus sp.||2 (3.1%)|
|Undetermined passerines||12 (24.5%)||4 (6.2%)||5 (16.7%)||2 (16.7%)||3 (14.3%)|
|Undetermined eggs*||4 (6.2%)|
|Pulli or eggs of aquatic birds||9 (42.9%)|
|Podarcis muralis||4 (8.2%)||7 (23.3%)|
|Podarcis sicula||1 (8.3%)|
* Because the number of eggs eaten was impossible to count exactly, we indicate the number of snakes containing eggs as a prey item.
To examine dietary differences between the sexes, we pooled data from all the study areas to increase sample size. We collected 90 prey items from males and 84 from females (Table 2). Qualitatively, both sexes fed on almost the same prey types, but, quantitatively, males and females differed signi?cantly in terms of prey composition (X2 = 19.56, df = 2, P < 0.0001).
Mean ingested biomass per snake was 43.7 ± 31.7g in male snakes (approximately 11% of the snake biomass), and 47.2 ± 32.1g in female snakes (approximately 9% of the snake biomass). Prey mass and predator mass were signi?cantly correlated in both males (r = 0.61, n = 42, P < 0.0001) and females (r = 0.57, n = 37, P < 0.0001).
Diet composition in the various habitat types.— Rodents were always an important prey source for Four-Lined Snakes, and in four out of ?ve habitats, the principal food source (Table 3). An exception was the wet area, where birds were preyed upon slightly more frequently than rodents, which, nonetheless, still represented a very important prey source (Table 3). The frequency of occurrence of rodents in snake diets did not differ signi?cantly among study areas (P = 0.36 in X2 test), whereas birds occurred in the diets more frequently at the wet area than at any other study area (P < 0.05 in X2 test).
Seasonal variations in the diet composition.— Four-Lined Snakes started to feed in early April and continued feeding until early November (Fig. 2). To detect monthly differences in prey type composition, we considered only small mammals and birds in our analyses (the number of lizards eaten was too small to detect any monthly variation) and then pooled data by habitat type + sex. The monthly frequency of occurrence of birds in the snake diets was signi?cantly different from that of small mammals (X2 = 223.86, df = 7, P < 0.0001); birds were eaten almost exclusively in April and May (and mainly by females, see above), whereas small mammals were eaten throughout the annual feeding cycle of snakes (Fig. 2).
The proportion of males with food in the stomach during the months of April and May was <5%, and ranged from 25–60% in the rest of the months. The proportion of fed females was >35% in April and May, and ranged from 25–60% between June and September. Dividing the percent of fed animals in our snake sample by season of capture (three groups: March to May; June to August; September to November), sex, and locality of capture, and analyzing the data by three-way ANOVA, it resulted that neither locality (F4, 25 = 0.14, P = 0.966) nor season (F2, 27 = 1.54, P = 0.232) had any effect on the percent of fed snakes, whereas both sex (F1, 28 = 5.07, P < 0.032) and the interaction between sex and season (F3, 25 = 11.39, P < 0.001) had a signi?cant effect on percent of fed snakes. A Tukey HSD post hoc test indicated that (i) the percent of fed males was signi?cantly less than that of females during the period March–May, (ii) the percent of fed males was signi?cantly less in March–May than in the other two seasons, and (iii) these patterns were independent of the locality studied.
A UPGMA analysis of prey types among study areas indicated that snake diets were most similar in the agro-forest and the bushy pasture habitats; the residual forest habitat also clustered with the agro-forest/bushy pasture group (Fig. 3). Diets of snakes found in the wet area were clearly distinct from any other habitat type. The greatest contribution to the difference between the wet area and all other areas can be attributed to the greater predation of birds, particularly aquatic species.
In general terms, a diet based on wood mice, rats and birds (including eggs), as found in E. quatuorlineata , is consistent with data available for other rat snakes (genus Elaphe , sensu lato ), including both North American (e.g., Fitch, 1963, 1999; Reynolds and Scott, 1982) and European species (e.g., Rugiero et al., 1998; Capula and Luiselli, 2002; Gomille, 2002). This evidence suggests a constant pattern of feeding preferences within Elaphe , even though the ge-nus Elaphe is regarded as a problematic and genetically heterogeneous group of species whose systematic relationships are still unclear (Utiger et al., 2002). An apparent exception is represented by the Japanese Elaphe quadrivirgata that often feeds more on frogs, toads, skinks, and lizards rather than on small mammals, birds, and bird eggs (Hasegawa and Moriguchi, 1989; Fukada, 1992; Tanaka and Ota, 2002).
Fig. 3. Dendrogram resulting from a hierarchical cluster analysis (UPGMA, standardized to 100%) of percentage composition of snake diets in the various habitat types (study areas).
In E. quatuorlineata , like other rat snakes (e.g., Fitch, 1963, 1999; Rugiero et al., 2002), the newborns and juveniles probably also consume a high percentage of lizards (Rugiero and Luiselli, 1996), but we did not examine this aspect because we were unable to collect a suf?cient-sized sample of juveniles in all the study populations (Four-Lined Snake juveniles are extremely elusive and apparently very rare in the ?eld; see Filippi, 1995; Rugiero and Luiselli, 1996).
Our study also documented that E. quatuorlineata populations showed a constant pattern of reversed sexual size dimorphism (SSD), where females had longer bodies than males (see also Rugiero and Luiselli, 1996, for data on a single population of conspeci?cs). This pattern is not general for rat snakes; indeed, in several populations studied to date, the males are signi?cantly longer than the females (e.g., Shine, 1994 for Elaphe obsoleta; Rugiero et al., 1998 for Elaphe situla ; Scali and Montonati, 2000 for Elaphe longissima ) or are of similar body length as females (e.g., Shine, 1994 for Elaphe climacophora ). Thus, the remarkable SSD of E. quatuorlineata can introduce the potential for this species to show divergent adaptations for foraging in each sex (Shine, 1991), as observed in some species (Shine, 1986; Houston and Shine, 1993) but not in others (Luiselli et al., 2002a).
Indeed, although at a much less spectacular level than observed in other species (e.g., Shine, 1986; Houston and Shine, 1993), E. quatuorlineata males and females differed signi?cantly in terms of their dietary composition, with the smaller sex tending (unsurprisingly) to prey more often upon smaller-sized prey (lizards) than the larger sex. Our analyses also showed that the other major intersexual difference (i.e., the presence of birds and their eggs more often in females than in males) is independent of SSD, but more related to the sex-related differences in annual activity cycle. Birds (and their eggs) are found in snake diets almost only in April and May, which is the mating season for these snakes. During the mating season of temperate zone species, the males are usually anorexic because high plasma levels of testosterone inhibit foraging activity (Saint Girons, 1952), so that the absence of many birds in male snakes is dependent merely on the absence of predatory activity in this sex during the period in which birds are readily available. These data are of signi?cant interest not only for herpetology, but address more general issues also. Indeed, to the best of our knowledge, this is the ?rst example of such a phenomenon (prey type differing between sexes because feeding seasons differ intersexually) in snakes, and it may be of great interest to study other examples of snakes that may present the potentiality for such a phenomenon to occur.
We would like to thank F. Angelici for the valuable criticisms on an early version of this paper. LL and EF were supported by funds from the Parco Naturale Regionale di Canale Monterano, and MC was supported by funds of the M.U.R.S.T. (40% grants). Snakes were captured under authorization of the Regione Lazio-Assessorato Ambiente e Protezione Civile (protocols no. 44MC-LL-84bis and 2000-EF-LL-329bis), the Natural Reserve of Canale Monterano (authorization to EF and LL made by F. M. Mantero), and RomaNatura (authorization to LR made by R. De Filippis). No animals have been damaged or killed during the present project, and all were handled according to the standards of the Italian Ministry for Scienti?c Research and Technology.
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(EF) F.I.Z.V., HERPETOLOGY SECTION, VIA GABRIO CASATI 43, I-00139 ROME,ITALY; (LR) F.I.Z.V., HERPETOLOGY SECTION, VIA DOMENICO CIMAROSA 13, I-00198 ROME,ITALY; (MC) MUSEO CIVICO DI ZOOLOGIA,SECTION OF HERPETOLOGY, VIA ULISSE ALDROVANDI 18, I-00197 ROME,ITALY; (DC) REGIONE LAZIO,AGENZIA
REGIONALE PER I PARCHI (ARP), VIA INDONESIA 00198 ROME,ITALY. E-mail: (LL) lucamlu@ 33, I-00144 ROME,ITALY; AND (LL) F.I.Z.V. tin.it. Send reprint requests to LL. Submitted: ECOLOGY SECTION AND CENTRE OF ENVIRON-27 Dec. 2004. Accepted: 5 March 2005. Sec-MENTAL STUDIES DEMETRA, VIA OLONA 7, I-tion editor: M. J. Lannoo.
Thanks to The American Society of Ichthyologists and Herpetologists
Copeia, 2005(3), pp. 517–525
Published under an open access licence, non commercial use.