Food Habits of Boiga irregularis, an Introduced Predator on Guam di A. Savidge Journal of Herpetology, Vol. 22, No. 3. (Sep., 1988), pp. 275-2 Stable URL http: flinksjstor-org/sici?sici=0022-15 1 1% 28198809%2922%3A3%3C275%3 AFHOBIA%3E2.0,.CO%3B2-8 Journal of Herpetology is currently published by Society for the Study of Amphibians and Reptiles. Your use of the ISTOR archive indicates your acceptance of JSTOR’s Terms and Conditions of Use, available at bhupulwww.jstororg/about/terms.hunl. JSTOR’s Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of « journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial us. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at hupuhwww jstor.org/journalsssar html Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission, JSTOR is an independent not-for-profit organization dedicated to ereating and preserving a digital archive of scholarly journals. For more information regarding JSTOR, please contact support @jstor.org, hupslwwwjstororg/ Wed Nov 1 10:01:20 2006few of Het, V2, No.3 9p 275-3819 Epyih es Steyr the Sat Apsas ad epee Food Habits of Boiga irregularis, an Introduced Predator on Guam Juute A. Savincet Division of Aquatic and Wildife Resoures, P.O. Box 2950, Agana, Guam 96910 and Department of Ecology, Ethology, and Evolution, University of inci, Champag, Hinas 61820, USA AnstRact.— Introduced brown tree snakes (Boiga iregularis) from a variety of habitats on Guam were ‘examined for prey remains to determine how B.irregularis has maintained its population despite the ‘overexploitation or extinction ofits more vulnerable prey, principally birds and small mammals. Stomach and intestinal tract analyses revealed that B. iregularis consumes primarily birds and their eggs, small ‘mammals, lizards, and lizard eggs. The snakes appeared to be somewhat opportunistic in prey choice. No significant differences were found in the overall diets of males and females of the same size clases. Ontogenetic differences in diet were present. Birds and small mammals were consumed by medium to large snakes; the abundance of both of these prey classes has been severely affected by B.irregularis, Small lizards in general are very abundant on Guam and appear to be an important food source for mai um-sized snakes. The overlap of lizard and larger vertebrate prey taken by the intermediate- ized snakes allows the snake population to maintain relatively hi small to met larger prey. Boiga irregularis, an arboreal, nocturnal snake, is responsible for the extinctions and range reductions of Guam’s forest avifauna as well as the decline of several introduced species of birds and small mammals (Sav- idge, 1986, 1987). There are relatively few studies on the diets of tropical arboreal snakes because of their low densities and secretive nature and no detailed accounts of the diet of Boiga irregularis, This species occurs naturally in Australia, New Guinea, and the Solomon Islands, and was intro- duced to Guam in the late 1940's or early 1950's, possibly as a stow-away on military ships traveling between the Solomons or New Guinea and Guam, Since its arrival ‘on Guam it has spread throughout the is- land, and the population has attained high densities (Fritts and Scott, 1985; Savidge, 1986). This rear-fanged colubrid can now be found in virtually all habitats on Guam but is most common in primary and sec- ondary forests (Savidge, 1986) This paper reports the results of necrop- sies of B.irregularis collected from a variety of habitats on Guam and analyzes how this exotic predator could have caused the ex- tinetions and range reductions of its avian "Present address: Dept. Forestry, Fisheries & Wild- Life, 202 Natural Resources Hall, University of Ne- bratka, Est Campus, Lincoln, Nebraska 68583 USA. 8 ies despite the overexploit and mammalian prey without suffering a similar decline in its own population. Since stenophagous predators often show a nu- merical relationship with their prey, I hy- pothesized that B. irregularis should be somewhat generalized in its feeding hab- its. Ontogenetic, sexual, and individual preferences in the diet of B.irregularis were also examined. Stupy Sire AND MeTHops Guam is a tropical island located about half-way between Japan and New Guinea. The northern half of the island is a lime- stone plateau dominated by second-growth forest, whereas the south is mainly of vol- canic origin, with savanna and ravine for- est the most frequently encountered hab- itat types. Just prior to the arrival of B. irregularis, the resident vertebrate fauna of Guam consisted of 18 native and seven in- troduced species of birds (see Jenkins, 1983), a native fruit bat (Pteropus marian rus), several introduced mammals includ- ing three species of Rattus, a shrew (Suncus ‘murinus), and house mouse (Mus musculus), a blind snake (Rhamphotyphlops braminus), six species of geckos, possibly five species of skinks, and the anole Anolis carolinensis. Specimens of B. irregular were received from the public, or collected by searching forest habitats for live animals and roads276 for road-kills, and from baited funnel traps. Between 1982 and May 1986, the entire intestinal tract of snakes collected on Guam was examined. If prey were found in the stomach and/or intestine, the minimum possible number was estimated based on reconstruction of the items. Determination of the actual number of prey items in the intestinal tract was not always possible be- cause some items were digested beyond recognition. Prior to 1982, snake stomachs were examined by biologists of the Guam Division of Aquatic and Wildlife Resources (DAWR), and data from those analyses are also included in this paper. Besides examining field-collected snakes, potential prey items were given to captive snakes of various snout-vent lengths (SVL) to determine prey preferences Resutts Diet Composition. —A total of 683 snakes from various habitats on Guam was nec- ropsied. Eighty-nine of these snakes were examined between 1967 and 1981 by DAWR staff. Of 353 snakes examined by DAWR and me that contained prey, 28.1% were birds or bird eggs, 8.7% small mam- ‘mals, and 63.2% lizards and lizard eggs (Ta- ble 1). Although most birds and their eggs were domestic or feral poultry due to the near absence of native forest birds on Guam, some native species were found. A snake collected from south-central Guam in 1967 contained a native Cardinal Hon- eyeater (Myzomela cardinals), while another snake taken from southern Guam in 1975 had the remains of an adult Guam Rail (Ral- lus owstoni), an endemic, flightless species. In 1980, a native adult Micronesian Star- ling (Aplonis opaca) was discovered in the stomach of a 216 cm (total length) snake found dead on a road in northern Guam. Several birds, including a native Mariana Fruit-Dove (Pilinopus reseicaplla), two na- tive Micronesian Kingfishers (Halcyon c. cinnamomina), and an introduced Black Drongo (Dicrurus macrocercus) were found dead in the field after they were killed by snakes as indicated by partially digested skin on the heads and shoulders and a cov- ering of saliva. I interpret the latter spec- mens to have been rejected by B.irregularis, JULIE A. SAVIDGE possibly due to excessive size, following an attempt to swallow the birds. This is commonly observed in captive snakes giv- en prey too large to swallow. Food of snakes taken after 1981 from iso- lated forest habitats that were nearly de- void of birds (160 snakes with prey items) consisted of 93.3% skinks, anoles, geckos, and their eggs, 4.8% small mammals, and 1.9% bird eggs (two chicken eggs in one snake and two Philippine Turtle-Dove eggs, Sireptopelia bitorquata, in a second snake). The snake found with chicken eggs ‘was on military land in northern Guam and approximately 6 km from the nearest human habitation. Although relatively un- common, feral chickens (Gallus gallus) are found in Guam’s forests and presumably this snake obtained the eggs from a feral clutch, Several miscellaneous items were found during necropsies. Insects observed in- cluded various Arachnida, Hymenoptera (Formicidae), and Hemiptera. All were small and generally less than 1 cm in length. Most snakes with insects also had lizards in the gut. However, ten snakes, ranging from 61-195 cm in SVL, had in- sects alone. Even though insects were found in 30 snakes, I believe that insects were ‘consumed incidentally along with lizards largely because of the small size of all in- sects encountered, In those cases where in- sect parts but no lizards were found, the lizard remains may have been digested at a faster rate than the sclerotized insect exo- skeleton, None of my captive snakes, rang- ing in size from 62 cm to 225 cm SVL, consumed any insects provided. Presum- ably the plant material observed was also ingested inadvertently, perhaps while tak- ing prey. There were two confirmed cases of snakes consuming the poisonous toad Bufo marinus. One snake with a toad in its ‘mouth was found dead by a Guam resident, and the second was found dead on a road with a B. marinus in its esophagus. A third snake was found dead in a small pool of water with a dead Bufo floating beside it, Three cooked spareribs were found inside a snake captured within a Guam residence. Individual, Sexual, and Ontogenctic Prefer- ences. —Out of 306 snakes in which the en-FOOD HABITS OF BOIGA Tame 1 wT Prey of Boigs irregulais based on the analysis of 494 prey items along with miscellaneous prey from 353 snake stomachs and intestinal tracts examined primarily between 1980-1985: Birds Introduced birds! 2 50 es 4007 2 cage bindst 833 Pouley! 75 ° 58S 2 Native bindst 3 3 2 Unknown bird 313 Unknown eR mo 42 Total birds/eges mi 463 ° Mammals Rattus spp. 2 50 4 Suncus marinas n 46 5 Mus musculus 2 08 Orytolagus curculs 1 oo Unknown 33 1 Total mammals 2» 2110 Reptiles Skinks? a om 9 Geckos! 136330 ‘Anolis carolinensis 5 63 OB ‘Unknown lizard 5 38s Lizard eggs 0 83 2 Varamus rious 2 Total reptle/eggs 100 417194 Mise ‘Bufo marinus 2 Sparerib 3 Insects! a 19 Plant material! 5 3 1 28 326 09 6 12 2 49 020 2 49 2 40 09 1 kw 14 306 09 2 04 3 06 498k 420019 6338 19 4 9840 23 32 2 08 1 02 os. 408 453738 Ml 6) ae L103. 85 $98 a 300 73 nr 2 4908 09 2 08 ol B92 wD ‘Dats fom two snakes examined in 1967 and 1975 ne lo ncaded *Rlumbers in parenthese ae numberof sakes with food in their ntact ‘Eurasian Teee-spurow (Poser montane), Philipine Turte-Dove (Sreplpte Brorust). “acgerigar (Melpetacas wate), Canary (Gers ana Domestic Chicken Gil gain), Cotunix Quail (Couric (Cola) 2) Cockatiel (Nymphs ald), Zebra Finch (Porphils ris) Domestic Mallard (Anas plalthychs), Domestic Pigeon "Mest sinks and geckon found inthe intestinal tats were unidentifiable to species. "Numer of sakes with insets or plant material ae Usted rather than numberof insects and pants. tire intestinal tract was examined and prey were found, 258 (84.3%) had prey of a single type (ie., lizard, lizard egg, bird, bird egg, or mammal). Although consid- ered to have only one prey type, six snakes had both geckos (generally nocturnally ac- tive) and skinks (generally diurnally ac- tive), and a seventh snake had both a gecko and an anole, the latter being generally diurnally active. Of the snakes with prey of a single type, 220 snakes (85.3%) had one prey item, 33 (12.8%) had two prey items of the same prey type, three (1.2%) had three items, one (0.4%) had four, and one snake (0.4%) had five domestic chicken eggs probably encountered in one clutch. Mul- tiple prey types were found in 48 snakes (15.7%; Table 2). Three snakes had three different prey types. Lizards and lizard eggs were the most frequent combination en-78 ‘Tams 2. Prey class combinations found in stom ache and intestinal tracts of Boig regulars ‘Lizard lizard eggs B Mamma /izard Bird eggs/mameal Bird eggs/lizard mammal epge/lizard lizard eggs nal lizard lizard eggs countered, but these may not always be separate acts of predation. In cases where lizards were largely dissolved and one or two eggs were nearby, the eggs probably ‘were carried inside the lizard when the female was consumed. However, one snake had six eggs and only one skink, and there ‘were snakes with eggs in the lower intes- tine and a lizard in the stomach indicating the items were eaten at different times. Only four snakes had lizard eggs and no evidence of having consumed lizards. ‘A Chi-Square test was done between ‘males and females of B. irregular less than 140 cm SVL in forest and urban habitat since adequate samples of both sexes were obtained forall size classes below this SVL. Both sexes in these size classes took equiv- alent numbers of lizards, lizard eggs, mam- mals, bird eggs, and birds (mu = 6.232, df = 3, 0.05

140 cm SVL examined, only four were females. ‘An analysis of all snakes revealed no sig- nificant difference between the sexes in forest habitat (x° = 5.907, df = 3, 0.1 < P = 0.2). However, a significant difference between the sexes in urban habitat was found due to the preponderance of birds, bird eggs, and mammals in the diet of the large male snakes (x! = 17.176, df =4,0.001

176 cm SVL never consumed small lizards when offered. Snakes were analyzed according to whether or not they had prey in their stomach or intestinal tract. Since urban snakes had a choice of a variety of prey, SVL groupings were chosen based on prey utilization patterns observed in urban hab- itat (Fig. 1B). The groups were: (1) snakes with lizards and lizards eggs comprising >50% of the diet (snakes <120 cm SVL); (2) snakes with birds, bird eggs, and mam- mals accounting for > 50% of the diet (> 120 ‘cm SVL); and (3) snakes with >95% of the diet consisting of birds, bird eggs and ‘mammals (>150 cm SVL). When compar- ing stomach and intestinal tracts of these groups in forest habitats where the larger prey items (birds and mammals) were scarce, 112 of 251 snakes (44.6%) <120 cm SVL were without prey, while 48 snakes >120 cm SVL (68.8%) did not have prey. Thirteen of 15 snakes (86.7%) > 150 cm SVL found in forest habitats were empty. In urban habitat, 85 of 171 snakes <120 cm SVL (49.7%) did not have prey, 37 of 74 snakes >120 cm SVL (50.0%) were without prey, and 24 of 49 snakes >150 cm SVL (49.0%) were empty. While there was no significant difference in the percent of snakes without prey in the three different ‘groups in urban habitat (x? = 0.021, df = 2,P > 0.95), differences between the groups in forest habitat were highly significant (2 = 40.197, df= 2, P = 0.001) due to finding significantly more larger snakes without rey. Prey composition of Boge regulars by snout-vent length, Snout-vent lengths were grouped in {intervals of 10 em and the mid-point of each interval i listed. Sample size for each interval is leted in parentheses, A is for forest habitat, B for urban habitat, and C combines snakes from forest, urban, and Einknown habitats,FOOD HABITS OF BOIGA Lizard eggs EI Lizards Mammals 1 Bideogs MI Birds CO Nodata 38 45 55 65 75 85 95 105 115 125 195 145 155 105 175, GG G9) 48) Cd) 0) BHO) (6) @) (4) (OM) CD 45 55 65 75 85 95 105 115 125 195 145 155 165 175 185 195 (0) (8) (12) 7 22) (12) (5) (6) (1) (8) (10) (@) (2) 2) 35 45 55 65 75 85. 95 105 115 125 195 145 155 165 175 185 195 (1) (22) 28484460} (55) (25) (13}(11) (6) (B) (12) @) Snout-Vent Length 29Discussion Members of the genus Boiga are reported to prey on reptiles, birds, and small mam- mals (Zwinenberg, 1978). The mangrove snake, Boiga dendrophila, has been described as an indiscriminate feeder taking birds, ‘mammals, snakes, lizards, frogs and pos- sibly invertebrates (Campden-Main, 1970; Minton and Dunson, 1978). Boigairregularis consumes a variety of prey, and its diet on Guam is similar to that reported from its native range. In Australia B. irregulars feeds mostly on birds, small mammals, and liz~ ards (Worrell, 1963; Cogger, 1975), and it is commonly found in bird cages (Worrell, 1963; Zwinenberg, 1978). McCoy (1980) ‘mentions the importance of geckos in the diet of B.irregularsin the Solomon Islands. Based largely on the strong correlation between the range expansion of B.irregu- laris and the avian range contraction, as well as experimental evidence on preda- tion pressure by B. irregularis in various habitats on Guam, largued that this species ‘was responsible for the extinction and range reduction of the native and many of the introduced birds on Guam (Savidge, 1987). Relatively few native birds were found in stomach samples, but this finding is not surprising as most bird populations ‘on Guam were close to extinction at the start of this study. However, limited ex- amination of snake stomachs collected prior to 1982 and native birds found dead in the field document that B. irregularis consumes native birds. The abundance of birds or ‘eggs in the diet of urban-collected snakes further demonstrates utilization of avian prey. Small mammals have also declined drastically in fields near forest habitat, but have remained abundant in savanna, a habitat not preferred by B.irregularis (Sav- idge, 1987). Due to the scarcity of avian and mammalian prey in field habitats, B. iregulars is now maintaining its field pop- ulation largely on lizards. Small lizards are common and the reproductive potential of some of the species appears high enough to withstand predation. ‘An attempt was made to analyze indi- vidual variation in prey preference. Most snakes had single prey items. Of those with JULIE A. SAVIDGE multiple prey (86 snakes), 48 had con- sumed multiple prey types, indicating that at least some individuals of B. irregularis are ‘opportunistic in their feeding and will take a diversity of prey types within the range of types consumed by the respective size class. Both nocturnally active (rats, shrews, geckos) and nocturnally quiescent prey (birds, skinks, anoles, all eggs) are con- sumed, and some individuals had both types within their intestinal tract. Hen- derson (1984), in discussing the diets of Hispaniolan colubrid snakes, states that ac- tive prey are taken by sit-and-wait strate- gists, quiescent prey by active foragers, and that one species he studied that consumed both types of prey exhibited both foraging modes. I have observed B. irregularis ac- tively foraging in the field, but it may em- ploy both foraging modes. Additionally, both terrestrial (i.e., poultry and their eggs and many skinks) and arboreal prey were consumed, indicating that B.irregulars, in addition to varying its foraging strategies, will forage on the ground as well as in trees. Seib (1985) found no difference in num- bers of various prey consumed by male and female Coniophanes fisidens. Mushinsky et al, (1982) reported that the largest individ- uals in two species of Nerodia were females and that these females ate a different array ‘of prey than smaller conspecific males, Most large snakes in my sample were males col- lected from urban habitats where a variety of prey is still available, and when all size classes from urban habitats were grouped together, there was a significant difference between prey types consumed by the sexes. ‘These differences are attributed to the larg- er size attained by the male snakes and thus that larger prey can be consumed, rather than to different preferences of the sexes, There was no significant difference in diet between male and female brown tree snakes <140 em SVL. Ithas been noted that larger snakes often take larger prey, and several studies have shown ontogenetic shifts in prey con- sumption (Carpenter, 1952; Fitch, 1965; Godley, 1980; Mushinsky et a., 1982). Seib (1985) in a study of the tropical snake Co-FOOD HABITS OF BOIGA niophanes fssdens observed that although ontogenetic shifts in prey type were not present, small individuals took smaller- sized prey, larger individuals took both large and small-sized prey, and the largest snakes avoided the smallest-sized prey that dominated the diet of the small snakes. Large Boiga in the lab would not take liz- ards even when hungry, and the largest snakes in my sample took only mammals, birds, and bird eggs. Large snakes are rare in forest habitats where avian and mam- ‘malian prey are now either extinct or ex- tremely rare (pers. obs.), and the higher percentage of forest-collected large snakes without prey indicates they are experienc- ing difficulty in finding acceptable food items. The small snakes consume lizards and lizard eggs, and their diet is probably restricted to prey of a mass and diameter that can be physically consumed. It is un- known if snakes <65 cm SVL take small nestling birds or infant mice if encoun- tered. The diet of medium-sized snakes broadens to include birds and mammals in addition to lizards and lizard eggs. These intermediate classes are the most common in the forest and may be largely respon- sible for the ultimate local extinction of the native forest birds because they can subsist on lizards when avian and mammalian prey ‘become rare. Although small and large snakes were relatively stenophagic in prey choice, the overall diet of B. irregularis can be consid- ered generalized. It regularly consumes three vertebrate classes and appears to eat a variety of species within each class. The diet demonstrates how ontogenetic shifts in prey preference may result in the over- exploitation of prey utilized by larger size classes as a result of relatively unrestricted prey availability for smaller size classes. This raises the question of the role of re- source availability to smaller size classes of B. irregularis versus other population reg- ulation mechanisms such as predation, dis- ease, etc., in controlling the population of B. irregularis in its native habitat. In summary, Guam offers an unique op- portunity to study the dynamics of an ex- otic predator in an insular environment The high densities attained by B. irregularis 281 on Guam, its ability to adapt to various environments, and its varied vertebrate diet, have allowed Boiga to severely affect its avian and mammalian prey. Since me- dium-sized snakes are reproductively ac- tive (pers. obs.), one might predict that as long as small lizard populations remain stable, present densities of B.irregularis will also remain stable and that its population size structure will reflect the available prey base in various habitats. Acknowledgments.—I thank T. Fritts and R. Henderson for reviewing an earlier draft of this manuscript and give special thanks to T. Seibert for providing constructive criticism and many helpful ideas through- out the study. Several people associated with the Guam Division of Aquatic and Wildlife Resources assisted in this study in fone way or another, and I am particularly indebted to Georganne Neubauer for her help in conducting the snake necropsies. Research was supported in part by the Fed- eral Aid in Fish and Wildlife Restoration Program, Project FW-2R and the Endan- gered Species Conservation Program, Proj- ect Eel. Lirexaruns Cr CCamrony-MAms,S, 1970, A field guide tothe snakes ‘of South Vietnam. Smithsonian Inst, Washington, C65 pp, CARPENTER, C.C. 1952. Comparative ecology of the common garter snake (Thamnophis sal), the ribbon snake (Thomnophiss. satus), and Butler's garter snake (Thammophis butler) in mixed popu Tations. Ecol, Monogr. 22:235-258, Cocom, H. G.”1975. Reptiles and amphibians of “Australia. A.H. de A.W. Reed, Sydney. 584 pp. Fire H.S. 1965, An ecological study ofthe gorter snake, Thannophis stalic Univ. Kans. Publ. Mus, Nat Hist 1545-5 Faris, T.H., AND N. J. Scorr,JR_ 1985, The brown, ‘tree snake on Guam: studies ofits ecology, contol, and threats to other islands. Unpubl. report sub: mitted to the US. Fish and Wildlife Service, Re Bion 1, Portland, Oregon. CGobLEy, J 5.1980, Foraging ecology ofthe striped ‘swamp snake, Regina allem, In southern Florida, Ecol. Monogr. 50:411-836, Hevpmtson, R'W. 1984. The diets of Hispaniolan ‘olubrid stakes I, Introduction and prey gene Gecologia 62:234-239, JENKINS, JM. 1983. The native forest birds of Guam "Amer. Ornithol. Union, Onithol. Monogr. No.3, ‘Washington, D.C. 61 pp. McCoy, M- 1980, Reptiles ofthe Solomon Islands ‘Wau Ecology Institute, No. 780 pp.282 [MIvTON, S.A. AND W. A. DUNSON. 1978. Observar tions on the Palawan mangrove snake, Boga de Arophla malticincta (Reptilia, Serpentes, Colubrs de) J. 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