Does urbanization influence the diet of a large snake?

Does urbanization influence the diet of a large snake? Urbanization facilitates synanthropic species such as rodents, which benefit the diets of many preda- tors in cities. We investigated how urbanization affects the feeding ecology of dugites Pseudonaja affi- nis, a common elapid snake in south-west Western Australia. We predicted that urban snakes: 1) more frequently contain prey and eat larger meals, 2) eat proportionally more non-native prey, 3) eat a lower diversity of prey species, and 4) are relatively heavier, than non-urban dugites. We analyzed the diet of 453 specimens obtained from the Western Australian Museum and opportunistic road-kill collections. Correcting for size, sex, season, and temporal biases, we tested whether location influenced diet for our 4 predictions. Body size was a strong predictor of diet (larger snakes had larger prey present, a greater number of prey items, and a greater diversity of prey). We identified potential collection biases: urban dugites were relatively smaller (snout-vent length) than non-urban specimens, and females were relatively lighter than males. Accounting for these effects, urban snakes were less likely to have prey present in their stomachs and were relatively lighter than non-urban snakes. Other urban-adapted car- nivores appear to benefit from urbanization through increased food supplementation, but we found the opposite of this: urban dugites were less likely to contain a meal, and their meals were smaller, indicat- ing they did not make greater use of synanthropic species than was evident for non-urban snakes. In contrast to other carnivores, snakes do not appear to fit a consistent directional pattern for size differ- ences between urban and non-urban populations. Key words: adaptation, dissection, feeding ecology, reptile. Urbanization is generally perceived as a negative influence on bio- Many snake species have persisted in or invaded urban areas. diversity (McKinney 2006). Urbanization can be a strong driver of For example black-necked spitting cobras Naja nigricollis in Africa landscape change, and the disturbance associated with cities may (Luiselli and Angelici 2000; Akani et al. 2002), carpet pythons cause local flora and fauna extinctions, where isolation of refugia Morelia spilota mcdowelli (Fearn et al. 2001) and tiger snakes and discrete habitat boundaries lead to mortality of sensitive species Notechis scutatus (Butler et al. 2005; Hamer 2011) in Australia, as (e.g., Fahrig 2001; Williams et al. 2005; Cushman 2006; Garden well as rock pythons Python sebae (Reed and Krysko 2013), corn et al. 2007). A decline of sensitive native species in urban areas can, snakes Elaphe guttata and DeKay’s snakes Storeria dekayi wrighto- therefore, lead to biotic homogenization and the dominance of few rum in the USA (Neill 1950). Despite their prevalence, there have usually invasive species, such as synanthropic rodents and birds been few descriptions of urban snake behavior and feeding ecology. (Blair 1996; McKinney 2008). Coupled with anthropogenic Differences in prey diversity and food availability can influence food sources and domestic animals, these invasive species can in- snake body size in urban areas. For example, invasive brown tree crease prey availability for predators. Many predators, native or snakes Boiga irregularis on Guam feed on different prey in urban introduced, therefore appear to thrive in and around cities (Roth and and non-urban areas, with urban snakes growing larger due to a Lima 2003; Chace and Walsh 2006; Bateman and Fleming 2012). greater range of available prey compared with non-urban sites, V C The Author (2017). Published by Oxford University Press. 311 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 312 Current Zoology, 2018, Vol. 64, No. 3 Figure 1. Collection locations of dugite P. affinis specimens used for this study: a) urban specimens (around the Perth metropolitan area where human population density exceeded 500 personskm at the time of the nearest Australian Bureau of Statistics census) are indicated by black dots, non-urban specimens are shown with grey squares; distribution of dugites containing prey in gut contents for b) urban and c) non-urban specimens. Legend: cross—non-native rodents; dia- mond—native rodents; plus—reptiles. Study location with reference to the wider Australian continent is shown in center right. where there have been local prey extinctions recorded as a result of following predictions for comparisons between urban and non- predation pressure (Savidge 1988). By contrast, P. sebae in suburban urban dugite specimens: areas in Nigeria supplement their diet with synanthropic rats and 1. Urban dugites will more frequently contain prey than non-urban domesticated poultry, but are significantly smaller than conspecifics dugites, and have eaten larger meals. from non-urban environments: the authors did not suggest any rea- 2. Urban dugites will eat proportionally more introduced prey than son for this difference (Luiselli et al. 2001). In the present study, we non-urban dugites. investigate the effect of urbanization on the feeding ecology of the 3. Urban dugites will eat a less diverse range of prey species than dugite Pseudonaja affinis, Elapidae (Gu ¨ nther 1872). This species is non-urban dugites. one of the most common snakes of south-west Western Australia, 4. Urban dugites will be relatively larger than non–urban dugites. thriving in woodlands, heaths, and urban environments (Chapman and Dell 1985), possibly via supplementation from the spread of the invasive house mouse Mus musculus (Shine 1989). Although the Materials and Methods house mouse is a small species, it is larger than the majority of urban lizards in Western Australia (How and Dell 2000), and its commu- Study species nal nesting and prolific breeding (e.g., Gomez et al. 2008; Vadell The dugite is a highly venomous elapid distributed across the south- et al. 2010) appears to provide dugites with frequent opportunities ern part of Western Australia and parts of South Australia to eat multiple individuals (and therefore larger meals). Dugites are (Figure 1a). Dugites are diurnal, active-foraging predators that grow regarded as one of the best urban-adapted large-bodied reptiles in up to 2 m in total length and can travel at least 1.5 km/day (A.K.W., Australia (How and Dell 1993), which makes them ideal model ani- unpublished data). The diet of dugites was explored and compared mals for urban/non-urban comparisons. Assuming dugites bene- with congeners by Shine (1989) who examined 179 museum speci- fit from the presence of synanthropic rodents, then we make the mens, although he did not consider differences across space or time. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 Wolfe et al.  Does urbanization affect snake diet? 313 Table 1. Length and body mass measurements for dugites by location and sex for dugite specimens with complete data Sex (n urban, non-urban) urban non-urban urban non-urban mean SVL 6 SE (range), cm mean body mass 6 SE (range), g Females (44, 75) 90.8 6 28.0 (42.4–132.0) 98.0 6 25.5 (41.5–156.0) 252.2 6 191.0 (16.6–604.9) 287.7 6 200.9 (19.6–1170.0) Males (35, 70) 93.0 6 28.7 (44.3–167.8) 104.3 6 24.5 (40.0–168.5) 296.1 6 335.6 (16.1–1940.0) 336.1 6 312.3 (18.0–1800.0) Undetermined sex* (116, 113) 27.4 6 4.7 (19.6–61.0) 28.1 6 11.3 (16.1–136.0) 7.3 6 8.0 (2.9–89.0) 15.1 6 75.1 (2.3–800.0) *Of the 229 specimens for which we were unable to determine sex, 226 were juveniles, SVL<40cm. Unfortunately, because the specimens attributed to that study were Analyses disposed of we were unable to revisit that dataset. Over half of the museum specimens we dissected had information about the collector (338 unique collectors: general public ¼ 37 speci- mens, scientist¼ 205 specimens, undetermined ¼ 211 specimens). Dissections To test for collection bias in the specimens included in this analysis We dissected 568 dugites, of which 548 were from the Western (n ¼ 453 specimens with complete data records), we used a multiple Australian Museum (WAM) (specimens collected between 1910 and regression to compare body size (log-SVL) as the dependent variable 2015 from across the entire known Western Australian range of the with location (urban¼ 0, non-urban¼ 1) and collector (general pub- species) and 20 were opportunistically collected as road-kill (col- lic¼ 0, undetermined¼ 0.5, scientist ¼ 1). Relatively larger (SVL) lected 2014–2015). Of the 568 dissected dugites, we were able to snakes were collected from non-urban areas (F ¼ 23.25; 2,450 obtain complete data (location, snout-vent length [SVL], wet mass P< 0.001) (Table 1), and by scientists (t ¼ 5.51; P< 0.001). As it of the preserved snake after draining excess preservative liquid [M ], is not possible to distinguish between differences in population and collection date) for 453 specimens, of which 112 dugites con- demographics or collection bias, we were unable to determine if tained prey. The number of individuals included in each analysis there were any real differences in body size between locations. therefore varies accordingly. Because body size is known to influence diet in snakes (e.g., Shine Prior to dissections, we recorded SVL, M , and sex (for all speci- 1989; King 2002; Bryant et al. 2012; Miranda et al. 2017), body mens>40 cm SVL; juveniles, n¼ 226, could not be sexed with confi- size was, therefore, accounted for by including log-SVL as a covari- dence even upon dissection) (Table 1). Each specimen was opened via ate in all analyses. There were also sex differences in body size (of a ventral incision at the subcaudal third, the stomach located and 453 specimens with complete data: female¼ 119, male ¼ 105, un- removed. Whole stomachs (from the end of the esophagus to the be- determined sex ¼ 229) (Table 1), with females being smaller than ginning of the small intestine) were extracted, weighed complete, cut males (M : F ¼ 106.5; P< 0.001; SVL: F ¼ 107.4; b 1,492 1,492 open lengthwise, and examined for any prey contents, and then re- P< 0.001). Therefore, the sex of specimens (female ¼ 0, undeter- weighed empty. Prey items were classified to the lowest possible taxo- mined¼ 0.5, male ¼ 1) was included in analyses to account for this nomic group; prey items were identifiable to species (66%), genus sex bias that could influence diet. We predicted that animals would (6%), and family (28%), which were used for statistical analyses. We be more active and therefore have a greater mass of food in their identified 20 native prey species (129 prey items) and 3 introduced stomachs for warmer months; therefore season (winter ¼ 0, autumn/ species (82 prey items) (see Table 2 for classification). As many of the spring¼ 0.5, summer¼ 1) was included as an independent factor in prey items were partially digested, we counted the total number of analyses. Furthermore, we predicted there would be a decrease in prey items and recorded total wet mass of all preserved prey items prey diversity or availability over time due to homogenization of the (after draining excess preservative) (M ) contained within each prey landscape due to anthropogenic influences, and therefore included stomach. Items such as sand, rocks, and leaves were considered inci- collection date (year) as an independent factor in analyses. dental gut contents and excluded from prey mass calculations. The raw data for this study is provided in Supplementary Appendix 1. Prediction 1: Urban dugites will more frequently contain Classification of urban and non-urban sites prey than non-urban dugites, and have eaten larger meals. Collection dates and GPS coordinates for each snake were available To determine if there was an effect of urbanization on the propor- for all road-killed specimens and 89% of museum specimens tion of specimens (n ¼ 453) containing prey items, we performed a (n ¼ 509) (Figure 1a). To account for urban growth over time, we logistical multiple regression with stomach contents (empty ¼ 0, categorized these GPS coordinates as either “urban” or “non- containing prey¼ 1) as dependent variable, and location, sex, body urban” sites using data for the closest census date (Australian size (log-SVL), season, and collection date as independent variables. Bureau of Statistics census dates: 1911; 1933; 1947; 1955; 1962; To determine if there was an effect of urbanization on the total 1969; 1974; 1982; 1988; 1993; 1997; 2001; and 2011) (see mass of prey eaten (n ¼ 112 dugites containing prey), we performed Supplementary Appendix 2 for references) to calculate the number a multiple regression with log-M as the dependent variable, and prey of people per square kilometer, classed by local government areas. location, sex, body size, season, and collection date as independent All locations that had>500 personskm were considered urban variables. (only sites within the Perth metropolitan region reached this popula- tion density), and all other coordinates were considered non-urban Prediction 2: Urban dugites will eat proportionally more (Figure 1a). To determine if there was a skew in collection dates between urban and non-urban sites, we performed a 2-way chi-s- introduced prey than non-urban dugites. quared analysis comparing collection locations across each decade To determine whether there was an effect of location on diet com- (n ¼ 10) for all specimens with complete records (n ¼ 453). position for n ¼ 112 dugites containing prey, we performed a 2-way Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 314 Current Zoology, 2018, Vol. 64, No. 3 Table 2. Diet of dugites collected from urban and non-urban with prey species richness as the dependent variable. The effect of lo- locations cation on prey diversity was tested by comparing a Shannon diver- sity index between locations via a diversity t-test. Taxon Native (N) or Urban Non-urban introduced (I) Prediction 4: Urban dugites will be relatively larger than Mammals, Rodents (n ¼ 4 taxa) Mus musculus I9 71 non-urban dugites. Notomys mitchelli N– 2 To determine if there was an effect of urbanization on snake body Rattus norvegicus I1 1 condition (i.e., mass relative to body size), we performed a multiple Rattus rattus I2 – logistic regression for n ¼ 453 specimens with log-M as the depend- Reptiles (n ¼ 28) ent variable, and location, sex, body size, season, and collection date Geckos (n ¼ 6 taxa) as independent variables. Christinus marmoratus N3 13 Values are presented as x6 1 Standard Deviation, range: min– Diplodactylus granariensis N– 2 max. Parametric analyses were conducted using STATISTICA 7.1 Diplodactylus pulcher N– 1 (StatSoft Inc. 2006). Non–parametric and diversity analyses (predic- Strophurus assimilis N– 2 Strophurus spinigerus N1 – tions 2 and 3) were conducted using PAST 3.1 (Hammer et al. 2001). Unidentified N – 4 Pygopods (n ¼ 2 taxa) Lialis burtonis N– 1 Results Pygopus lepidopodus N– 1 Agamids (n ¼ 3 taxa) A total of 195 (43%) of the 453 specimens with complete data were Ctenophorus sp. N – 1 collected in urban areas. The majority of collections occurred in Pogona minor N2 1 1960–1989 (Figure 2). There was a significant difference in location Unidentified N – 2 2 of collection over time (v ¼ 22.9; P ¼ 0.003), with a relatively Skinks (n ¼ 10 taxa) greater proportion of urban animals collected over more recent dec- Acritoscincus trilineatus N3 7 ades (Figure 2). We found prey items in the stomach for Ctenotus catenifer N– 1 112 (24.7%) of the 453 specimens with complete data; 44 specimens Ctenotus fallens N– 1 contained more than 1 prey item, and 21 specimens contained more Ctenotus labillardieri N– 9 than 1 prey species. In total we identified 224 prey items of at least Ctenotus sp. N 1 10 Hemiergis peronii N– 1 23 species. Overall observed dugite diet was made up of 38.4% Hemiergis quadrilineata N10 – mammals and 61.6% reptiles (Figure 1b, c). A total of 55 (24.6%) Lerista distinguenda N– 2 prey items were autotomized lizard tails (i.e., no evidence of the liz- Tiliqua rugosa N1 3 ard bodies), which we classified as belonging to geckos and skinks. Unidentified N 15 37 Snakes (n ¼ 2 taxa) Pseudonaja affinis N– 2 Prediction 1: Urban dugites will more frequently contain Unidentified N – 1 prey than non-urban dugites, and have eaten larger Number of prey items 48 176 meals. Number of taxa 11 24 Fewer urban snakes contained prey items than non-urban snakes Evenness 0.63 0.33 (Logistic multiple regression testing whether snakes had prey in their Simpson dominance 0.81 0.78 Shannon H’ 1.94 2.08 stomachs or not: t ¼ 2.8; b ¼ 0.1; P ¼ 0.0046; Table 3). There was also an effect of snake body size, with larger snakes (log-SVL) Urban snakes ate a similar diversity of prey. Collective number of species and more likely to have prey present (Table 3). There was no significant groups identified to the finest possible scale are represented by n for each class effect of sex, season, or year of collection on the presence of prey. and family. Urban snakes contained a similar total mass of prey (x ¼ 3.66 7.2, 0.001–27.7 g) as non-urban snakes (x ¼ 6.06 10.1, non-parametric MANOVA (PERMANOVA) using a Euclidean 0.001–54.5 g) (t ¼–1.0; P ¼ 0.31; Table 3). Larger snakes (log- similarity index and 9,999 permutations, with log-(M þ1) as de- SVL) had a greater mass of prey present, but there was no significant prey pendent factors (mass calculated separately for all agamids, geckos, effect of sex, season, or year of collection on prey mass (Table 3). pygopodids, rodents, skinks, and snakes), location and sex as inde- pendent grouping factors, and body size, season, and collection date Prediction 2: Urban dugites will eat proportionally more as covariates. We then repeated this PERMANOVA analysis using the total log-(M þ1) for all native or all introduced prey species. introduced prey than non-urban dugites. prey There was no significant effect of location on diet composition (2- way PERMANOVA: F ¼ 2.6; P ¼ 0.062) or effect of sex 1,106 Prediction 3: Urban dugites will eat a less diverse range (F ¼ 1.7; P ¼ 0.091). Similarly, there was no location effect on 2,106 of prey species than non-urban dugites. diet composition in terms of whether prey was native or introduced To determine if there was an effect of location on the number of (urban introduced M :x ¼ 2.16 6.7, 0–27.1 g, native: prey prey items for n ¼ 112 dugites containing prey, we performed a mul- x ¼ 1.26 2.4, 0–11.7 g; non–urban introduced x ¼ 4.26 9.4, tiple regression with the total number of prey items per individual as 0–52.5 g, native x ¼ 2.36 5.0, 0–25.7 g) (F ¼ 2.6; P ¼ 0.062). 1,106 dependent variable, and location, sex, body size, season, and collec- There was also no sex effect on diet composition in terms of whether tion date as independent variables. We carried out a similar analysis prey was native or introduced (F ¼ 1.7; P ¼ 0.093). 2,106 Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 Wolfe et al.  Does urbanization affect snake diet? 315 1950s (19) 1960s (171) 1970s (110) 1980s (76) 1990s (39) 2000s (15) 2010s (20) Urban Non-urban Figure 2. Comparison of urban and non-urban specimens collected over time. Only 3 snakes were collected prior to the 1950s: 2 urban snakes in the 1920s and 1 non-urban snake collected from the 1930s. Data represented as Decade (n). Table 3. Summary of multiple regression analyses testing dependent factors addressing the 4 predictions of this study Prediction Dependent factors Independent factors Location Sex Body size Season Year (log-SVL) 1a Prey present (yes/no) t ¼ 2.8; b ¼ 0.12; 0.33; P ¼ 0.74 4.6; b ¼ 0.32; 0.61; P ¼ 0.54 1.0; P ¼ 0.30 P ¼ 0.0046 P < 0.0001 1b Mass of prey (g) t ¼1.0; P ¼ 0.31 0.39; P ¼ 0.69 8.9; b ¼ 3.1; –1.8; P ¼ 0.062 0.31; P ¼ 0.75 P < 0.0001 3a Number of prey t ¼0.061; P ¼ 0.95 0.32; P ¼ 0.75 3.2; b ¼ 2.5; 0.022; P ¼ 0.98 –0.55; P ¼ 0.59 items (count) P ¼ 0.0016 3b Number of prey t ¼ 0.93; P ¼ 0.35 0.72; P ¼ 0.47 2.3; b ¼ 0.53; 0.097; P ¼ 0.92 0.38; P ¼ 0.71 species (count) P ¼ 0.024 4 Dugite body mass t ¼ 2.1; b ¼ 0.023; 2.1; b ¼ 0.032; 151.3; b ¼ 2.8; 1.1; P ¼ 0.27 –1.9; P ¼ 0.059 P ¼ 0.034 P ¼ 0.035 P < 0.0001 Once the effects of body size and potential biases (sex, season, year of collection) were accounted for, urban snakes were less likely to have prey present in their stomachs and were relatively lighter than non-urban snakes. Beta (b) values are provided for significant findings. 0< b represents a trend toward: 1) non-urban snakes for location, 2) males for sex, and 3) larger snakes for log-SVL. Prediction 3: Urban dugites will eat a less diverse range Discussion of prey species than non-urban dugites. Many mammalian urban adapters have access to increased food Urban dugites ate a similar number of prey items as non-urban du- supplementation, providing larger and/or more frequent meals (see gites (t ¼ –0.06; P ¼ 0.95; Table 3). Larger snakes (log-SVL) Bateman and Fleming 2012). This is also indicated in reptiles for had more prey items, but there was no effect of sex, season, or B. irregularis (Savidge 1988) and P. sebae (Luiselli et al. 2001), year of collection on number of prey items (Table 3). Similarly, which take larger prey in urban areas, possibly due to prey availabil- larger snakes ate a greater diversity of prey (number of species), ity. We had, therefore, predicted that the presence of synanthropic but there was no effect of location, sex, season, or year of collec- prey in urban areas would provide greater opportunity for dugites. tion (Table 3). This analysis was supported by a diversity t-test, However, our predictions were not supported by this dataset of 453 which indicated that urban dugites had a similar diversity of prey dugite specimens. Once the effects of body size and potential biases present as non-urban dugites (Shannon t ¼ –0.86; P ¼ 0.39; 111.94 (sex, season, year of collection) were accounted for, urban snakes Table 2). were less likely to have prey present in their stomachs and were rela- tively lighter than non-urban snakes. Location did not affect the Prediction 4: Urban dugites will be relatively larger than number of prey items, the diversity of prey, or the relative propor- tions of native or non-native prey. non-urban dugites. As has been reported across many snake diet studies (e.g., Shine Urban dugites were relatively lighter than non-urban dugites 1989; King 2002; Bryant et al. 2012; Miranda et al. 2017), body (t ¼ 2.1; b ¼ 0.023; P ¼ 0.034; Figure 3a; Table 3) once correl- size (log-SVL) was a strong predictor of dugite diet. Larger snakes ation with body length (log-SVL) was accounted for. Females were more frequently contained meals, and those meals were of a greater relatively lighter than all other specimens (Figure 3b), but there was mass. Larger snakes also contained a greater number and greater di- no significant effect of year or season of collection on relative body versity of prey items than smaller snakes. Body size was also mass (Table 3). Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 316 Current Zoology, 2018, Vol. 64, No. 3 Figure 3. Residual body mass (compared with SVL) for a) urban and non-urban dugites and b) specimens of each sex. Residuals were calculated using a linear re- gression of log-SVL against log-body mass. significantly different between the sexes. Despite dugites, along with urban species, Buchanan’s snake-eyed skink Cryptoblepharus other Australian brown snakes, being considered to not have buchananii (Bush et al. 2010), was not identified as a prey item for marked sexual size dimorphism (Shine 1989), we found that females any snake; however, of the 56 autotomized tails found present in du- were relatively lighter than males. gite stomachs, we expect that some of these may have belonged to Although we predicted urban snakes would be relatively heavier the snake-eyed skinks, as dugites have been observed eating these in than non-urban snakes, our finding to the contrary is not unsurpris- the wild (A.K.W., personal observations). Therefore, dugites do not ing, as living in high-disturbance areas may better suit smaller snake face a lack of native reptile prey in urban areas. individuals (i.e., younger snakes) and smaller-bodied species. For ex- The only introduced mammalian prey were rodents: M. muscu- ample, road mortality from vehicle–wildlife collisions is biased to- lus, Rattus norvegicus (brown rat), and Rattus rattus (black rat); all wards larger-bodied species or individuals (e.g., Shine and Koenig are synanthropic species. Urban dugites did not appear to make 2001; Gibbs and Shriver 2002; Steen et al. 2006). Smaller snakes greater use of synanthropic species than was evident for non-urban may also be better able to find cover in high-disturbance areas. specimens. While both specimens of R. rattus were found in urban Smaller garter snakes Thamnophis ordinoides flee to cover quicker snakes, M. musculus and R. norvegicus were found in the stomachs than larger conspecifics (Bell 2010), and smaller grass snakes Natrix of both urban and non-urban dugites. The prevalence of rodents in natrix are more likely to be found under cover than in the open than landscapes associated with grain farmland is not a particularly sur- larger individuals (Gregory 2016). prising result, and Western Australia’s farming ‘wheatbelt’ com- Our observed dugite diet of mostly mammals (38.4%) and rep- prises 154,862 km , or approximately 30% of the distribution tiles (61.6%) did not vary between urban and non-urban snakes. range of dugites in Western Australia (Wheatbelt Development This diet composition is similar to that recorded by Shine (1989), Commission 2015). Many non-urban specimens found containing who also used WAM specimens (n ¼ 179), but found different pro- rodents were outside of the wheatbelt region; the spread of rodents portions of prey representation to us; his specimens contained birds across the southern half of the dugite range may be exacerbated by and more mammals (grouped together, 51%) than reptiles (47%) as the scattering of towns across southern Western Australia. The ex- prey, and also included frogs (2%). These differences are likely due tensive spread of introduced rodents across southern Western to different snake size ranges of the specimens dissected between the Australia appears to supplement all dugites, not just those in urban two studies (SVL¼ 108.86 2.6 cm for females and 108.56 2.7 cm areas, as we had originally predicted. for males, no significant difference (n.s.), Shine 1989; SVL ¼ 90.86 2.8 cm for females and 104.36 4.5 cm for males, with significant effects of sex and location, this study). Dugites tend to eat Sampling bias more endothermic prey with increasing SVL (Shine 1989), which There was a significant sampling bias of collection location on body may explain why we found more reptiles and fewer mammals in our, size: relatively larger snakes were collected from non-urban areas. on average, smaller specimens. Snakes, in particular, are stigmatized for their potential to have a There was no difference in the relative proportions of native or venomous bite (whether they are venomous or not), and large indi- non-native prey for urban or non-urban dugites, which reflects that viduals are often relocated away from urban areas for safety con- urban snakes make extensive use of native species, despite living in cerns (Shine and Koenig 2001; Department of Parks and Wildlife the urban matrix. All reptiles identified were native (Cogger 2014), 2013), possibly reducing the average size of animals persisting in and many reptile prey species identified are considered common in urban sites. Additionally, although killing any wildlife, including urban bush remnants across Perth (How and Dell 2000; Davis and snakes, is illegal in Western Australia, we have observed dugites Doherty 2015). The most common prey species found exclusively in dead in backyards and on roads in ways that could only be deliber- urban areas was a native reptile, the 2-toed earless skink Hermiergis ate (A.K.W., personal observations). Human predation on snakes, quadrilineata. This skink species occurs within some of the dugite’s therefore, must also play a role in shaping the demographics of non-urban range along the south-western coastline, but it is urban snake populations. Urban development encroachment, intro- recognized as one of the most abundant lizards within the Perth duced predators (e.g., cats, dogs, foxes) and pressures (e.g., modified metropolitan area (Davis and Doherty 2015), and is most commonly land use), or low behavioral plasticity and adaptation to change found near urban environments (Cogger 2014). Another prolific may also potentially contribute to the observed size differences Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 Wolfe et al.  Does urbanization affect snake diet? 317 between urban and non-urban locations. Alternatively, urban snakes suggests that dugites living within the Perth metropolitan area are may exhibit increased secretive behaviors to minimize interactions not using any available extra dietary resources, or using dietary re- with people, inevitably reducing foraging activity and feeding sources differently. Perhaps urban dugites lack feeding innovations opportunities. because native food is abundant for urban dugites, while there is We found that relatively larger dugites were also collected more also an abundance of synanthropic species associated with farming frequently by scientists (as identified by collectors’ names). This pre- in non-urban locations. Some Australasian reptile species such as the sents an interesting point for future studies of museum specimens, as blue-tongue lizard Tiliqua scincoides (Koenig et al. 2001) and the significant biases may result due to the method of capture of speci- common skink Oligosoma nigriplantare polychroma (van Heezik mens. For example, members of the public most likely donated du- and Ludwig 2012) use household gardens for food, water, and gites to the museum that were found dead or were killed on their avoidance of predators, and most of the urban dugite prey species property for fear of a venomous bite, while scientists embark on we identified are both common in gardens/urban remnants and less trapping exercises or encounter specimens of high quality and do- urbanized parts of Western Australia. Perhaps the definitions of nate those exceptional specimens to the museum. We found no evi- urban adaptation are not suited for ectothermic vertebrates, or du- dence of similar studies accounting for such biases, but we gites fit into another category: “urban oblivious”, usually a recommend incorporating this information into future comparative term used for cryptic generalists, usually ignored by humans (Grant analyses, wherever possible. et al. 2011). Although size difference comparisons between urban and non- Unlike other taxa that experience food supplementation by urban snakes in the literature are limited, a consistent directional pat- urban areas, dugites do not appear to derive any particular dietary tern does not currently appear to exist: B. irregularis are larger in benefit from living in cities. However, there is more to urban adap- urban areas (Savidge 1988), while urban individuals of P. sebae are tation than diet alone, and the other factors, such as increased tem- relatively smaller (Luiselli et al. 2001). In human-disturbed sites in peratures (Brazel et al. 2000; Ackley et al. 2015), and available New Hampshire, USA, snakes found within smaller patches were rela- cover (e.g., tin sheeting, brick piles, garden beds) (Brown and tively larger than those found in larger patches (Kjoss and Litvaitis Sleeman 2002; Purkayastha et al. 2011) may provide an anthropo- 2001). In Japan, mamushi snakes Gloydius blomhoffii were relatively genic niche for these snakes that is worth exploiting despite smaller in areas where they are hunted than conspecifics in non- increased predation from domestic pets (Shine and Koenig 2001) hunting grounds, an example of rapid evolutionary responses to preda- and restricted movement due to habitat fragmentation (How and tion pressure (Sasaki et al. 2008). By contrast, the size of massasauga Dell 2000). Finally, a major setback for snakes in urban areas, espe- rattlesnakes Sistrurus catenatus catenatus in Canada, was unaffected cially for venomous species, is their direct conflict with humans by disturbance from humans (Parent and Weatherhead 2000). (Whitaker and Shine 2000; Clemann et al. 2004). Snakes play an im- portant role in controlling rodents and stabilizing food webs, and the persistence of these important predators, therefore, requires that Application of urban ecology theory to snakes we know more about their habitat and diet requirements. Despite all Degrees of adaptation to urbanization have been described as 3 lev- of the potential challenges for snakes in urban areas, dugites, which els: avoidance, adaptation, and exploitation (Blair 1996; McKinney do not appear to conform to standard urban-adaptation conven- 2006). Due to sensitivity to anthropogenic changes, “urban tions, remain one of the best urban-adapted vertebrates in Perth. avoiders” remain in their highest densities in unmodified natural en- vironments. “Urban adapters” prefer areas of intermediate disturb- ance (i.e., suburbia) due to an ability to use novel resources such as Acknowledgments garden plants. Finally, “urban exploiters” appear to show prefer- ence for highly modified areas (i.e., inner metropolitan areas) due to We would like to express our thanks to the Western Australian Museum’s an ability to exploit the availability of anthropogenic resources such Terrestrial Collections Officer Rebecca Bray and Curator for Herpetology Dr. Paul Doughty for their assistance and for allowing us to dissect the specimens. as buildings (shelter) and refuse (food). This classification method has been useful for describing responses to urbanization for birds (Blair 1996), mammals (Randa and Yunger 2006), and insects (McIntyre 2000). Building on this, a set of 5 rules for urban ex- Funding ploiters was developed by Kark et al. (2007) using birds as a model; Funding for this study was provided by the Department of Environment and urban exploiters most commonly are: 1) omnivorous or diet general- Agriculture, Curtin University. This project used road-killed specimens col- ists (with some specialization seen in urban adapters); 2) social; 3) lected from roads in Western Australia under the Department of Parks and sedentary and maintain territories; 4) nest in man-made structures Wildlife’s Regulation 17 license (#SF009895). (though adapters use vegetation); and 5) have relatively larger brains, greater behavioral flexibility, and use novel food items. For mammalian carnivores, body size is also likely to influence the abil- Supplementary Material ity of mammals to exploit the urban landscape, with medium-sized Supplementary material can be found at https://academic.oup.com/cz. (1–20 kg) generalist predator species identified as the best urban adapters: larger species are more likely to attract human attention and smaller species more likely to be sensitive to habitat fragmenta- References tion (see Bateman and Fleming 2012). Ackley JW, Angilletta MJ, DeNardo D, Sullivan B, Wu J, 2015. 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Sources of mortality of large elapid snakes in an How RA, Dell J, 1993. Vertebrate fauna of the Perth metropolitan region: con- agricultural landscape. J Herpetol 34:121–128. sequences of a modified environment. In: Urban Bush Management: Williams NSG, Morgan JW, McDonnell MJ, McCarthy MA, 2005. Plant Proceedings of a seminar held at Gosnells, WA, 23 June 1992 (eds traits and local extinctions in natural grasslands along an urban-rural gradi- Australian Institute of Urban Studies, Greening Western Australia, ent. J Ecol 93:1203–1213. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Zoology Oxford University Press

Does urbanization influence the diet of a large snake?

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Abstract

Urbanization facilitates synanthropic species such as rodents, which benefit the diets of many preda- tors in cities. We investigated how urbanization affects the feeding ecology of dugites Pseudonaja affi- nis, a common elapid snake in south-west Western Australia. We predicted that urban snakes: 1) more frequently contain prey and eat larger meals, 2) eat proportionally more non-native prey, 3) eat a lower diversity of prey species, and 4) are relatively heavier, than non-urban dugites. We analyzed the diet of 453 specimens obtained from the Western Australian Museum and opportunistic road-kill collections. Correcting for size, sex, season, and temporal biases, we tested whether location influenced diet for our 4 predictions. Body size was a strong predictor of diet (larger snakes had larger prey present, a greater number of prey items, and a greater diversity of prey). We identified potential collection biases: urban dugites were relatively smaller (snout-vent length) than non-urban specimens, and females were relatively lighter than males. Accounting for these effects, urban snakes were less likely to have prey present in their stomachs and were relatively lighter than non-urban snakes. Other urban-adapted car- nivores appear to benefit from urbanization through increased food supplementation, but we found the opposite of this: urban dugites were less likely to contain a meal, and their meals were smaller, indicat- ing they did not make greater use of synanthropic species than was evident for non-urban snakes. In contrast to other carnivores, snakes do not appear to fit a consistent directional pattern for size differ- ences between urban and non-urban populations. Key words: adaptation, dissection, feeding ecology, reptile. Urbanization is generally perceived as a negative influence on bio- Many snake species have persisted in or invaded urban areas. diversity (McKinney 2006). Urbanization can be a strong driver of For example black-necked spitting cobras Naja nigricollis in Africa landscape change, and the disturbance associated with cities may (Luiselli and Angelici 2000; Akani et al. 2002), carpet pythons cause local flora and fauna extinctions, where isolation of refugia Morelia spilota mcdowelli (Fearn et al. 2001) and tiger snakes and discrete habitat boundaries lead to mortality of sensitive species Notechis scutatus (Butler et al. 2005; Hamer 2011) in Australia, as (e.g., Fahrig 2001; Williams et al. 2005; Cushman 2006; Garden well as rock pythons Python sebae (Reed and Krysko 2013), corn et al. 2007). A decline of sensitive native species in urban areas can, snakes Elaphe guttata and DeKay’s snakes Storeria dekayi wrighto- therefore, lead to biotic homogenization and the dominance of few rum in the USA (Neill 1950). Despite their prevalence, there have usually invasive species, such as synanthropic rodents and birds been few descriptions of urban snake behavior and feeding ecology. (Blair 1996; McKinney 2008). Coupled with anthropogenic Differences in prey diversity and food availability can influence food sources and domestic animals, these invasive species can in- snake body size in urban areas. For example, invasive brown tree crease prey availability for predators. Many predators, native or snakes Boiga irregularis on Guam feed on different prey in urban introduced, therefore appear to thrive in and around cities (Roth and and non-urban areas, with urban snakes growing larger due to a Lima 2003; Chace and Walsh 2006; Bateman and Fleming 2012). greater range of available prey compared with non-urban sites, V C The Author (2017). Published by Oxford University Press. 311 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 312 Current Zoology, 2018, Vol. 64, No. 3 Figure 1. Collection locations of dugite P. affinis specimens used for this study: a) urban specimens (around the Perth metropolitan area where human population density exceeded 500 personskm at the time of the nearest Australian Bureau of Statistics census) are indicated by black dots, non-urban specimens are shown with grey squares; distribution of dugites containing prey in gut contents for b) urban and c) non-urban specimens. Legend: cross—non-native rodents; dia- mond—native rodents; plus—reptiles. Study location with reference to the wider Australian continent is shown in center right. where there have been local prey extinctions recorded as a result of following predictions for comparisons between urban and non- predation pressure (Savidge 1988). By contrast, P. sebae in suburban urban dugite specimens: areas in Nigeria supplement their diet with synanthropic rats and 1. Urban dugites will more frequently contain prey than non-urban domesticated poultry, but are significantly smaller than conspecifics dugites, and have eaten larger meals. from non-urban environments: the authors did not suggest any rea- 2. Urban dugites will eat proportionally more introduced prey than son for this difference (Luiselli et al. 2001). In the present study, we non-urban dugites. investigate the effect of urbanization on the feeding ecology of the 3. Urban dugites will eat a less diverse range of prey species than dugite Pseudonaja affinis, Elapidae (Gu ¨ nther 1872). This species is non-urban dugites. one of the most common snakes of south-west Western Australia, 4. Urban dugites will be relatively larger than non–urban dugites. thriving in woodlands, heaths, and urban environments (Chapman and Dell 1985), possibly via supplementation from the spread of the invasive house mouse Mus musculus (Shine 1989). Although the Materials and Methods house mouse is a small species, it is larger than the majority of urban lizards in Western Australia (How and Dell 2000), and its commu- Study species nal nesting and prolific breeding (e.g., Gomez et al. 2008; Vadell The dugite is a highly venomous elapid distributed across the south- et al. 2010) appears to provide dugites with frequent opportunities ern part of Western Australia and parts of South Australia to eat multiple individuals (and therefore larger meals). Dugites are (Figure 1a). Dugites are diurnal, active-foraging predators that grow regarded as one of the best urban-adapted large-bodied reptiles in up to 2 m in total length and can travel at least 1.5 km/day (A.K.W., Australia (How and Dell 1993), which makes them ideal model ani- unpublished data). The diet of dugites was explored and compared mals for urban/non-urban comparisons. Assuming dugites bene- with congeners by Shine (1989) who examined 179 museum speci- fit from the presence of synanthropic rodents, then we make the mens, although he did not consider differences across space or time. Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 Wolfe et al.  Does urbanization affect snake diet? 313 Table 1. Length and body mass measurements for dugites by location and sex for dugite specimens with complete data Sex (n urban, non-urban) urban non-urban urban non-urban mean SVL 6 SE (range), cm mean body mass 6 SE (range), g Females (44, 75) 90.8 6 28.0 (42.4–132.0) 98.0 6 25.5 (41.5–156.0) 252.2 6 191.0 (16.6–604.9) 287.7 6 200.9 (19.6–1170.0) Males (35, 70) 93.0 6 28.7 (44.3–167.8) 104.3 6 24.5 (40.0–168.5) 296.1 6 335.6 (16.1–1940.0) 336.1 6 312.3 (18.0–1800.0) Undetermined sex* (116, 113) 27.4 6 4.7 (19.6–61.0) 28.1 6 11.3 (16.1–136.0) 7.3 6 8.0 (2.9–89.0) 15.1 6 75.1 (2.3–800.0) *Of the 229 specimens for which we were unable to determine sex, 226 were juveniles, SVL<40cm. Unfortunately, because the specimens attributed to that study were Analyses disposed of we were unable to revisit that dataset. Over half of the museum specimens we dissected had information about the collector (338 unique collectors: general public ¼ 37 speci- mens, scientist¼ 205 specimens, undetermined ¼ 211 specimens). Dissections To test for collection bias in the specimens included in this analysis We dissected 568 dugites, of which 548 were from the Western (n ¼ 453 specimens with complete data records), we used a multiple Australian Museum (WAM) (specimens collected between 1910 and regression to compare body size (log-SVL) as the dependent variable 2015 from across the entire known Western Australian range of the with location (urban¼ 0, non-urban¼ 1) and collector (general pub- species) and 20 were opportunistically collected as road-kill (col- lic¼ 0, undetermined¼ 0.5, scientist ¼ 1). Relatively larger (SVL) lected 2014–2015). Of the 568 dissected dugites, we were able to snakes were collected from non-urban areas (F ¼ 23.25; 2,450 obtain complete data (location, snout-vent length [SVL], wet mass P< 0.001) (Table 1), and by scientists (t ¼ 5.51; P< 0.001). As it of the preserved snake after draining excess preservative liquid [M ], is not possible to distinguish between differences in population and collection date) for 453 specimens, of which 112 dugites con- demographics or collection bias, we were unable to determine if tained prey. The number of individuals included in each analysis there were any real differences in body size between locations. therefore varies accordingly. Because body size is known to influence diet in snakes (e.g., Shine Prior to dissections, we recorded SVL, M , and sex (for all speci- 1989; King 2002; Bryant et al. 2012; Miranda et al. 2017), body mens>40 cm SVL; juveniles, n¼ 226, could not be sexed with confi- size was, therefore, accounted for by including log-SVL as a covari- dence even upon dissection) (Table 1). Each specimen was opened via ate in all analyses. There were also sex differences in body size (of a ventral incision at the subcaudal third, the stomach located and 453 specimens with complete data: female¼ 119, male ¼ 105, un- removed. Whole stomachs (from the end of the esophagus to the be- determined sex ¼ 229) (Table 1), with females being smaller than ginning of the small intestine) were extracted, weighed complete, cut males (M : F ¼ 106.5; P< 0.001; SVL: F ¼ 107.4; b 1,492 1,492 open lengthwise, and examined for any prey contents, and then re- P< 0.001). Therefore, the sex of specimens (female ¼ 0, undeter- weighed empty. Prey items were classified to the lowest possible taxo- mined¼ 0.5, male ¼ 1) was included in analyses to account for this nomic group; prey items were identifiable to species (66%), genus sex bias that could influence diet. We predicted that animals would (6%), and family (28%), which were used for statistical analyses. We be more active and therefore have a greater mass of food in their identified 20 native prey species (129 prey items) and 3 introduced stomachs for warmer months; therefore season (winter ¼ 0, autumn/ species (82 prey items) (see Table 2 for classification). As many of the spring¼ 0.5, summer¼ 1) was included as an independent factor in prey items were partially digested, we counted the total number of analyses. Furthermore, we predicted there would be a decrease in prey items and recorded total wet mass of all preserved prey items prey diversity or availability over time due to homogenization of the (after draining excess preservative) (M ) contained within each prey landscape due to anthropogenic influences, and therefore included stomach. Items such as sand, rocks, and leaves were considered inci- collection date (year) as an independent factor in analyses. dental gut contents and excluded from prey mass calculations. The raw data for this study is provided in Supplementary Appendix 1. Prediction 1: Urban dugites will more frequently contain Classification of urban and non-urban sites prey than non-urban dugites, and have eaten larger meals. Collection dates and GPS coordinates for each snake were available To determine if there was an effect of urbanization on the propor- for all road-killed specimens and 89% of museum specimens tion of specimens (n ¼ 453) containing prey items, we performed a (n ¼ 509) (Figure 1a). To account for urban growth over time, we logistical multiple regression with stomach contents (empty ¼ 0, categorized these GPS coordinates as either “urban” or “non- containing prey¼ 1) as dependent variable, and location, sex, body urban” sites using data for the closest census date (Australian size (log-SVL), season, and collection date as independent variables. Bureau of Statistics census dates: 1911; 1933; 1947; 1955; 1962; To determine if there was an effect of urbanization on the total 1969; 1974; 1982; 1988; 1993; 1997; 2001; and 2011) (see mass of prey eaten (n ¼ 112 dugites containing prey), we performed Supplementary Appendix 2 for references) to calculate the number a multiple regression with log-M as the dependent variable, and prey of people per square kilometer, classed by local government areas. location, sex, body size, season, and collection date as independent All locations that had>500 personskm were considered urban variables. (only sites within the Perth metropolitan region reached this popula- tion density), and all other coordinates were considered non-urban Prediction 2: Urban dugites will eat proportionally more (Figure 1a). To determine if there was a skew in collection dates between urban and non-urban sites, we performed a 2-way chi-s- introduced prey than non-urban dugites. quared analysis comparing collection locations across each decade To determine whether there was an effect of location on diet com- (n ¼ 10) for all specimens with complete records (n ¼ 453). position for n ¼ 112 dugites containing prey, we performed a 2-way Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 314 Current Zoology, 2018, Vol. 64, No. 3 Table 2. Diet of dugites collected from urban and non-urban with prey species richness as the dependent variable. The effect of lo- locations cation on prey diversity was tested by comparing a Shannon diver- sity index between locations via a diversity t-test. Taxon Native (N) or Urban Non-urban introduced (I) Prediction 4: Urban dugites will be relatively larger than Mammals, Rodents (n ¼ 4 taxa) Mus musculus I9 71 non-urban dugites. Notomys mitchelli N– 2 To determine if there was an effect of urbanization on snake body Rattus norvegicus I1 1 condition (i.e., mass relative to body size), we performed a multiple Rattus rattus I2 – logistic regression for n ¼ 453 specimens with log-M as the depend- Reptiles (n ¼ 28) ent variable, and location, sex, body size, season, and collection date Geckos (n ¼ 6 taxa) as independent variables. Christinus marmoratus N3 13 Values are presented as x6 1 Standard Deviation, range: min– Diplodactylus granariensis N– 2 max. Parametric analyses were conducted using STATISTICA 7.1 Diplodactylus pulcher N– 1 (StatSoft Inc. 2006). Non–parametric and diversity analyses (predic- Strophurus assimilis N– 2 Strophurus spinigerus N1 – tions 2 and 3) were conducted using PAST 3.1 (Hammer et al. 2001). Unidentified N – 4 Pygopods (n ¼ 2 taxa) Lialis burtonis N– 1 Results Pygopus lepidopodus N– 1 Agamids (n ¼ 3 taxa) A total of 195 (43%) of the 453 specimens with complete data were Ctenophorus sp. N – 1 collected in urban areas. The majority of collections occurred in Pogona minor N2 1 1960–1989 (Figure 2). There was a significant difference in location Unidentified N – 2 2 of collection over time (v ¼ 22.9; P ¼ 0.003), with a relatively Skinks (n ¼ 10 taxa) greater proportion of urban animals collected over more recent dec- Acritoscincus trilineatus N3 7 ades (Figure 2). We found prey items in the stomach for Ctenotus catenifer N– 1 112 (24.7%) of the 453 specimens with complete data; 44 specimens Ctenotus fallens N– 1 contained more than 1 prey item, and 21 specimens contained more Ctenotus labillardieri N– 9 than 1 prey species. In total we identified 224 prey items of at least Ctenotus sp. N 1 10 Hemiergis peronii N– 1 23 species. Overall observed dugite diet was made up of 38.4% Hemiergis quadrilineata N10 – mammals and 61.6% reptiles (Figure 1b, c). A total of 55 (24.6%) Lerista distinguenda N– 2 prey items were autotomized lizard tails (i.e., no evidence of the liz- Tiliqua rugosa N1 3 ard bodies), which we classified as belonging to geckos and skinks. Unidentified N 15 37 Snakes (n ¼ 2 taxa) Pseudonaja affinis N– 2 Prediction 1: Urban dugites will more frequently contain Unidentified N – 1 prey than non-urban dugites, and have eaten larger Number of prey items 48 176 meals. Number of taxa 11 24 Fewer urban snakes contained prey items than non-urban snakes Evenness 0.63 0.33 (Logistic multiple regression testing whether snakes had prey in their Simpson dominance 0.81 0.78 Shannon H’ 1.94 2.08 stomachs or not: t ¼ 2.8; b ¼ 0.1; P ¼ 0.0046; Table 3). There was also an effect of snake body size, with larger snakes (log-SVL) Urban snakes ate a similar diversity of prey. Collective number of species and more likely to have prey present (Table 3). There was no significant groups identified to the finest possible scale are represented by n for each class effect of sex, season, or year of collection on the presence of prey. and family. Urban snakes contained a similar total mass of prey (x ¼ 3.66 7.2, 0.001–27.7 g) as non-urban snakes (x ¼ 6.06 10.1, non-parametric MANOVA (PERMANOVA) using a Euclidean 0.001–54.5 g) (t ¼–1.0; P ¼ 0.31; Table 3). Larger snakes (log- similarity index and 9,999 permutations, with log-(M þ1) as de- SVL) had a greater mass of prey present, but there was no significant prey pendent factors (mass calculated separately for all agamids, geckos, effect of sex, season, or year of collection on prey mass (Table 3). pygopodids, rodents, skinks, and snakes), location and sex as inde- pendent grouping factors, and body size, season, and collection date Prediction 2: Urban dugites will eat proportionally more as covariates. We then repeated this PERMANOVA analysis using the total log-(M þ1) for all native or all introduced prey species. introduced prey than non-urban dugites. prey There was no significant effect of location on diet composition (2- way PERMANOVA: F ¼ 2.6; P ¼ 0.062) or effect of sex 1,106 Prediction 3: Urban dugites will eat a less diverse range (F ¼ 1.7; P ¼ 0.091). Similarly, there was no location effect on 2,106 of prey species than non-urban dugites. diet composition in terms of whether prey was native or introduced To determine if there was an effect of location on the number of (urban introduced M :x ¼ 2.16 6.7, 0–27.1 g, native: prey prey items for n ¼ 112 dugites containing prey, we performed a mul- x ¼ 1.26 2.4, 0–11.7 g; non–urban introduced x ¼ 4.26 9.4, tiple regression with the total number of prey items per individual as 0–52.5 g, native x ¼ 2.36 5.0, 0–25.7 g) (F ¼ 2.6; P ¼ 0.062). 1,106 dependent variable, and location, sex, body size, season, and collec- There was also no sex effect on diet composition in terms of whether tion date as independent variables. We carried out a similar analysis prey was native or introduced (F ¼ 1.7; P ¼ 0.093). 2,106 Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 Wolfe et al.  Does urbanization affect snake diet? 315 1950s (19) 1960s (171) 1970s (110) 1980s (76) 1990s (39) 2000s (15) 2010s (20) Urban Non-urban Figure 2. Comparison of urban and non-urban specimens collected over time. Only 3 snakes were collected prior to the 1950s: 2 urban snakes in the 1920s and 1 non-urban snake collected from the 1930s. Data represented as Decade (n). Table 3. Summary of multiple regression analyses testing dependent factors addressing the 4 predictions of this study Prediction Dependent factors Independent factors Location Sex Body size Season Year (log-SVL) 1a Prey present (yes/no) t ¼ 2.8; b ¼ 0.12; 0.33; P ¼ 0.74 4.6; b ¼ 0.32; 0.61; P ¼ 0.54 1.0; P ¼ 0.30 P ¼ 0.0046 P < 0.0001 1b Mass of prey (g) t ¼1.0; P ¼ 0.31 0.39; P ¼ 0.69 8.9; b ¼ 3.1; –1.8; P ¼ 0.062 0.31; P ¼ 0.75 P < 0.0001 3a Number of prey t ¼0.061; P ¼ 0.95 0.32; P ¼ 0.75 3.2; b ¼ 2.5; 0.022; P ¼ 0.98 –0.55; P ¼ 0.59 items (count) P ¼ 0.0016 3b Number of prey t ¼ 0.93; P ¼ 0.35 0.72; P ¼ 0.47 2.3; b ¼ 0.53; 0.097; P ¼ 0.92 0.38; P ¼ 0.71 species (count) P ¼ 0.024 4 Dugite body mass t ¼ 2.1; b ¼ 0.023; 2.1; b ¼ 0.032; 151.3; b ¼ 2.8; 1.1; P ¼ 0.27 –1.9; P ¼ 0.059 P ¼ 0.034 P ¼ 0.035 P < 0.0001 Once the effects of body size and potential biases (sex, season, year of collection) were accounted for, urban snakes were less likely to have prey present in their stomachs and were relatively lighter than non-urban snakes. Beta (b) values are provided for significant findings. 0< b represents a trend toward: 1) non-urban snakes for location, 2) males for sex, and 3) larger snakes for log-SVL. Prediction 3: Urban dugites will eat a less diverse range Discussion of prey species than non-urban dugites. Many mammalian urban adapters have access to increased food Urban dugites ate a similar number of prey items as non-urban du- supplementation, providing larger and/or more frequent meals (see gites (t ¼ –0.06; P ¼ 0.95; Table 3). Larger snakes (log-SVL) Bateman and Fleming 2012). This is also indicated in reptiles for had more prey items, but there was no effect of sex, season, or B. irregularis (Savidge 1988) and P. sebae (Luiselli et al. 2001), year of collection on number of prey items (Table 3). Similarly, which take larger prey in urban areas, possibly due to prey availabil- larger snakes ate a greater diversity of prey (number of species), ity. We had, therefore, predicted that the presence of synanthropic but there was no effect of location, sex, season, or year of collec- prey in urban areas would provide greater opportunity for dugites. tion (Table 3). This analysis was supported by a diversity t-test, However, our predictions were not supported by this dataset of 453 which indicated that urban dugites had a similar diversity of prey dugite specimens. Once the effects of body size and potential biases present as non-urban dugites (Shannon t ¼ –0.86; P ¼ 0.39; 111.94 (sex, season, year of collection) were accounted for, urban snakes Table 2). were less likely to have prey present in their stomachs and were rela- tively lighter than non-urban snakes. Location did not affect the Prediction 4: Urban dugites will be relatively larger than number of prey items, the diversity of prey, or the relative propor- tions of native or non-native prey. non-urban dugites. As has been reported across many snake diet studies (e.g., Shine Urban dugites were relatively lighter than non-urban dugites 1989; King 2002; Bryant et al. 2012; Miranda et al. 2017), body (t ¼ 2.1; b ¼ 0.023; P ¼ 0.034; Figure 3a; Table 3) once correl- size (log-SVL) was a strong predictor of dugite diet. Larger snakes ation with body length (log-SVL) was accounted for. Females were more frequently contained meals, and those meals were of a greater relatively lighter than all other specimens (Figure 3b), but there was mass. Larger snakes also contained a greater number and greater di- no significant effect of year or season of collection on relative body versity of prey items than smaller snakes. Body size was also mass (Table 3). Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 316 Current Zoology, 2018, Vol. 64, No. 3 Figure 3. Residual body mass (compared with SVL) for a) urban and non-urban dugites and b) specimens of each sex. Residuals were calculated using a linear re- gression of log-SVL against log-body mass. significantly different between the sexes. Despite dugites, along with urban species, Buchanan’s snake-eyed skink Cryptoblepharus other Australian brown snakes, being considered to not have buchananii (Bush et al. 2010), was not identified as a prey item for marked sexual size dimorphism (Shine 1989), we found that females any snake; however, of the 56 autotomized tails found present in du- were relatively lighter than males. gite stomachs, we expect that some of these may have belonged to Although we predicted urban snakes would be relatively heavier the snake-eyed skinks, as dugites have been observed eating these in than non-urban snakes, our finding to the contrary is not unsurpris- the wild (A.K.W., personal observations). Therefore, dugites do not ing, as living in high-disturbance areas may better suit smaller snake face a lack of native reptile prey in urban areas. individuals (i.e., younger snakes) and smaller-bodied species. For ex- The only introduced mammalian prey were rodents: M. muscu- ample, road mortality from vehicle–wildlife collisions is biased to- lus, Rattus norvegicus (brown rat), and Rattus rattus (black rat); all wards larger-bodied species or individuals (e.g., Shine and Koenig are synanthropic species. Urban dugites did not appear to make 2001; Gibbs and Shriver 2002; Steen et al. 2006). Smaller snakes greater use of synanthropic species than was evident for non-urban may also be better able to find cover in high-disturbance areas. specimens. While both specimens of R. rattus were found in urban Smaller garter snakes Thamnophis ordinoides flee to cover quicker snakes, M. musculus and R. norvegicus were found in the stomachs than larger conspecifics (Bell 2010), and smaller grass snakes Natrix of both urban and non-urban dugites. The prevalence of rodents in natrix are more likely to be found under cover than in the open than landscapes associated with grain farmland is not a particularly sur- larger individuals (Gregory 2016). prising result, and Western Australia’s farming ‘wheatbelt’ com- Our observed dugite diet of mostly mammals (38.4%) and rep- prises 154,862 km , or approximately 30% of the distribution tiles (61.6%) did not vary between urban and non-urban snakes. range of dugites in Western Australia (Wheatbelt Development This diet composition is similar to that recorded by Shine (1989), Commission 2015). Many non-urban specimens found containing who also used WAM specimens (n ¼ 179), but found different pro- rodents were outside of the wheatbelt region; the spread of rodents portions of prey representation to us; his specimens contained birds across the southern half of the dugite range may be exacerbated by and more mammals (grouped together, 51%) than reptiles (47%) as the scattering of towns across southern Western Australia. The ex- prey, and also included frogs (2%). These differences are likely due tensive spread of introduced rodents across southern Western to different snake size ranges of the specimens dissected between the Australia appears to supplement all dugites, not just those in urban two studies (SVL¼ 108.86 2.6 cm for females and 108.56 2.7 cm areas, as we had originally predicted. for males, no significant difference (n.s.), Shine 1989; SVL ¼ 90.86 2.8 cm for females and 104.36 4.5 cm for males, with significant effects of sex and location, this study). Dugites tend to eat Sampling bias more endothermic prey with increasing SVL (Shine 1989), which There was a significant sampling bias of collection location on body may explain why we found more reptiles and fewer mammals in our, size: relatively larger snakes were collected from non-urban areas. on average, smaller specimens. Snakes, in particular, are stigmatized for their potential to have a There was no difference in the relative proportions of native or venomous bite (whether they are venomous or not), and large indi- non-native prey for urban or non-urban dugites, which reflects that viduals are often relocated away from urban areas for safety con- urban snakes make extensive use of native species, despite living in cerns (Shine and Koenig 2001; Department of Parks and Wildlife the urban matrix. All reptiles identified were native (Cogger 2014), 2013), possibly reducing the average size of animals persisting in and many reptile prey species identified are considered common in urban sites. Additionally, although killing any wildlife, including urban bush remnants across Perth (How and Dell 2000; Davis and snakes, is illegal in Western Australia, we have observed dugites Doherty 2015). The most common prey species found exclusively in dead in backyards and on roads in ways that could only be deliber- urban areas was a native reptile, the 2-toed earless skink Hermiergis ate (A.K.W., personal observations). Human predation on snakes, quadrilineata. This skink species occurs within some of the dugite’s therefore, must also play a role in shaping the demographics of non-urban range along the south-western coastline, but it is urban snake populations. Urban development encroachment, intro- recognized as one of the most abundant lizards within the Perth duced predators (e.g., cats, dogs, foxes) and pressures (e.g., modified metropolitan area (Davis and Doherty 2015), and is most commonly land use), or low behavioral plasticity and adaptation to change found near urban environments (Cogger 2014). Another prolific may also potentially contribute to the observed size differences Downloaded from https://academic.oup.com/cz/article-abstract/64/3/311/3895746 by Ed 'DeepDyve' Gillespie user on 17 June 2018 Wolfe et al.  Does urbanization affect snake diet? 317 between urban and non-urban locations. Alternatively, urban snakes suggests that dugites living within the Perth metropolitan area are may exhibit increased secretive behaviors to minimize interactions not using any available extra dietary resources, or using dietary re- with people, inevitably reducing foraging activity and feeding sources differently. Perhaps urban dugites lack feeding innovations opportunities. because native food is abundant for urban dugites, while there is We found that relatively larger dugites were also collected more also an abundance of synanthropic species associated with farming frequently by scientists (as identified by collectors’ names). This pre- in non-urban locations. Some Australasian reptile species such as the sents an interesting point for future studies of museum specimens, as blue-tongue lizard Tiliqua scincoides (Koenig et al. 2001) and the significant biases may result due to the method of capture of speci- common skink Oligosoma nigriplantare polychroma (van Heezik mens. For example, members of the public most likely donated du- and Ludwig 2012) use household gardens for food, water, and gites to the museum that were found dead or were killed on their avoidance of predators, and most of the urban dugite prey species property for fear of a venomous bite, while scientists embark on we identified are both common in gardens/urban remnants and less trapping exercises or encounter specimens of high quality and do- urbanized parts of Western Australia. Perhaps the definitions of nate those exceptional specimens to the museum. We found no evi- urban adaptation are not suited for ectothermic vertebrates, or du- dence of similar studies accounting for such biases, but we gites fit into another category: “urban oblivious”, usually a recommend incorporating this information into future comparative term used for cryptic generalists, usually ignored by humans (Grant analyses, wherever possible. et al. 2011). Although size difference comparisons between urban and non- Unlike other taxa that experience food supplementation by urban snakes in the literature are limited, a consistent directional pat- urban areas, dugites do not appear to derive any particular dietary tern does not currently appear to exist: B. irregularis are larger in benefit from living in cities. However, there is more to urban adap- urban areas (Savidge 1988), while urban individuals of P. sebae are tation than diet alone, and the other factors, such as increased tem- relatively smaller (Luiselli et al. 2001). In human-disturbed sites in peratures (Brazel et al. 2000; Ackley et al. 2015), and available New Hampshire, USA, snakes found within smaller patches were rela- cover (e.g., tin sheeting, brick piles, garden beds) (Brown and tively larger than those found in larger patches (Kjoss and Litvaitis Sleeman 2002; Purkayastha et al. 2011) may provide an anthropo- 2001). In Japan, mamushi snakes Gloydius blomhoffii were relatively genic niche for these snakes that is worth exploiting despite smaller in areas where they are hunted than conspecifics in non- increased predation from domestic pets (Shine and Koenig 2001) hunting grounds, an example of rapid evolutionary responses to preda- and restricted movement due to habitat fragmentation (How and tion pressure (Sasaki et al. 2008). By contrast, the size of massasauga Dell 2000). Finally, a major setback for snakes in urban areas, espe- rattlesnakes Sistrurus catenatus catenatus in Canada, was unaffected cially for venomous species, is their direct conflict with humans by disturbance from humans (Parent and Weatherhead 2000). (Whitaker and Shine 2000; Clemann et al. 2004). Snakes play an im- portant role in controlling rodents and stabilizing food webs, and the persistence of these important predators, therefore, requires that Application of urban ecology theory to snakes we know more about their habitat and diet requirements. Despite all Degrees of adaptation to urbanization have been described as 3 lev- of the potential challenges for snakes in urban areas, dugites, which els: avoidance, adaptation, and exploitation (Blair 1996; McKinney do not appear to conform to standard urban-adaptation conven- 2006). Due to sensitivity to anthropogenic changes, “urban tions, remain one of the best urban-adapted vertebrates in Perth. avoiders” remain in their highest densities in unmodified natural en- vironments. “Urban adapters” prefer areas of intermediate disturb- ance (i.e., suburbia) due to an ability to use novel resources such as Acknowledgments garden plants. Finally, “urban exploiters” appear to show prefer- ence for highly modified areas (i.e., inner metropolitan areas) due to We would like to express our thanks to the Western Australian Museum’s an ability to exploit the availability of anthropogenic resources such Terrestrial Collections Officer Rebecca Bray and Curator for Herpetology Dr. Paul Doughty for their assistance and for allowing us to dissect the specimens. as buildings (shelter) and refuse (food). This classification method has been useful for describing responses to urbanization for birds (Blair 1996), mammals (Randa and Yunger 2006), and insects (McIntyre 2000). Building on this, a set of 5 rules for urban ex- Funding ploiters was developed by Kark et al. (2007) using birds as a model; Funding for this study was provided by the Department of Environment and urban exploiters most commonly are: 1) omnivorous or diet general- Agriculture, Curtin University. This project used road-killed specimens col- ists (with some specialization seen in urban adapters); 2) social; 3) lected from roads in Western Australia under the Department of Parks and sedentary and maintain territories; 4) nest in man-made structures Wildlife’s Regulation 17 license (#SF009895). (though adapters use vegetation); and 5) have relatively larger brains, greater behavioral flexibility, and use novel food items. For mammalian carnivores, body size is also likely to influence the abil- Supplementary Material ity of mammals to exploit the urban landscape, with medium-sized Supplementary material can be found at https://academic.oup.com/cz. (1–20 kg) generalist predator species identified as the best urban adapters: larger species are more likely to attract human attention and smaller species more likely to be sensitive to habitat fragmenta- References tion (see Bateman and Fleming 2012). Ackley JW, Angilletta MJ, DeNardo D, Sullivan B, Wu J, 2015. 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