The Disappearance of Guam's Wildlife

The Disappearance of Guam's Wildlife

The Disappearance of Guam's Wildlife New insights for herpetology, evolutionary ecology, and conservation Gordon H. Rodda, Thornas H. Fritts, and Davi...

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The Disappearance of Guam's Wildlife New insights for herpetology, evolutionary ecology, and conservation Gordon H. Rodda, Thornas H. Fritts, and David Chiszar

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uam is an Amcrican island ne ar the middle of Microncsia, an archipeJago of "miero" islands in the middle of the western Pacifie Ocean. The largest island of }Vlicroncsia, Guam cover<; only 541 km1 , lt is shaped like an clongated peanut, 4 km across thc narrow waLst and 45 km lang. The dosest larger island is Manus, wh ich is 1740 km to the sOllth, across the equator and north of New Guinea. Few ~pecies are found on small, remore islands such as Guam. To reach

aland mass wirh levels ofbiodiversity comparablc to what is fauod on COiltinents, one must travel over 2000 km south to New Guinea, west (0 the Philippincs, or north to Japan (Figure 1). Neither water currents nor wind brings animals from those directions, so Guam's native vertebIates are limited to those spccies that ean f1y (e.g., birJs anJ bats), or whase eggs can ride for many weeks on sma11 clumps of floating vegetation (c.g., small lizards). Large nonvolantvertebrates and even small Gordon H. Rodda is a zoo10gist, and Thomas H. Fritts is chief of the Biological Survey Program, at the Patuxcnt \X'ildlife Research Center, Riological Resourees Division, United States Geological Survey, National Mu<;eum of Natural History, Washington, DC 20560. The}' study tropieal reptiles and the effects of species tramlocations. David Chiszar is a professor in the Department of Psychology, University of Colorado, Bouldcr, CO 80309-0345. His interests revolve around the behavior of reptiles, espccially the feeding adaptations of snakes. © 1997 American Institute of ßiological Seien ces.

October 1997

The Guam experience showed ecologists that snakes can attain densities that are sufficient to suppress prey populations delkate flyers, such as mosquitoes, fad to make the journey without human assistance. Indeed, Microncsia was free of flies and mosquitoes until Spanish conquistadors brought these inseets to Guam (Carano and Sanehez 1964). Ir is difficult to know how many species of animals were found on Guam beiore the arrival of humans, but horn archeological excavations on the nearby island of Rota, scienrists know that ehe original human colonists-or the domestic animals that the colonists broughr with them-extirpated many species thousands of years aga. On Rota, as on Hawaii, approximately half of the native birds were exterminated by prehistüric humans (Steadman 1995); presumably, Guam lost a similar number. But following that spate of prehisroric extinctions, the native wildlife communit)' remained relativel)' stable until the 1960s. Surprisingly, the island's fauna \vas lüde disrupted by the savagc fighting of World War II (Engbring and Pratt 1985), which sn bjected Guam to naval bombardment so severe that

some forests were leveled by artillery fire and morethan 80% ofthe island's structures were destroyed (Morison 1953). After the war, the island was extensively reseeded with an exotic legurne, Leucaena leucocephala, wh ich permanently rcplaced native rrees over vast areas (Craig 1994). As far as is known, no native bird species or other vertebrates were lost as a result of this ecological upheavaJ (Baker 1946). The ecological effccts of the war may have been somewhat analogous to the typhoons that naturally strike Guam every few years. In 1992, for example, Guam was hit by six typhoons, three of which were "super-typhoons" with sustained winds in excess of 240 km/ho The fieree storlllS of the western Pacifie denude forests and thereby seleet for species that can tolerate severe natural habitat modifications. Major changes in Guam's vertebrate fauna became evident in the 1960s, when wildlife authorities noticed that birds were entirely absent from the southern onc-third of the island and that the boundary of birJlessness seemed to be creeping steadily northward. By the end of the 1970s, birds were missing from the southern two-thirds of the island (Engbring 19R3, Jenkins 1983). Ey 1985, most of the bird species \vere either isolated in small pockets at the northern tip of the island 01' \-\iere eompletely gone (hgure 2). What was killing the birds? T\vo theories gcncrated particular interest. One was that pesticides, vvhieh had been Llsed in !arge amuunts after World War 11 to control lllosquitocs,

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• GUAM

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Figure 1. Guam is the largest of the more chan 2 t 00 tiny islands of Microncsia (most are roo small to be seen in this view). Lying north of thc eguator neat the middle of the western Pacific ücean, Guam is roughly equidistanr (over 2000 km) from Japan, the Philippines, aod New Guinea.

had poisoned the birds, as DDT had done to some birds in mainland North

Amer!ca. The second, and leading, hypothesis was that an introduced bird disease, such as had ravaged the birds ofHawaii (vanRiperetal.1986, Warner 1968), had spread catastrophi-

call)' through the birJ populations, pcrhaps carried by the introduced mosquitoes. An avian pathologist,Julie Savidgc, was hired by Guam's Division of Aquatic and Wildlife Resüurees to find the disease that was killing the birds of Guam. In collaboration wirh ather pathologists and pesticide specialists, she scoured the forests and birds of Guam for evidence of this disease, but she ca me up empty-handed (Grue InS, Savidge 1987, Savidgc et al. 1992). She concluded instead that the accidentally introduced brown tree snake,

Figurc 2. These fairy terns afe 3mong the 12 bird species (boch land aud sea birds) that have disappeared from Guam in the wake of the introduction of thc brOWll tree snake.

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Boiga irregularis, was responsibJe for the 1055 of the birds (Figure 3).

The snake turned out to be responsihle for not on!y the extinctions of the birds, bur also the decimation of the island's lizards (Figure 4; Radda and Fritts1992b), mammals (\X' ilcs 1987), and domestic animals (Fritts and McCoid 1991). When Savidge reported her discovery at a meeting of the American Ornithologists' Union in 1983, she met with skeptici sm from some members of the audienee. Marshall (1985) no ted th3t "Few could believe that a mere snake was that efficient a predator and could build up the numbcrs COtnmensurate with such devastation" (p. 260). One commentator responded to Savidge's condusion by devoting a column to promoting the pesticide hypothesis (Diamond 1984). The fact that Sa vidge's conclusion was initially rejeeted hut is now widely accepted, re fleets the growth of ecology. How do we know that thc snake caused the extirpations? Six lines of evidenee point to the brown tree snake as the primary cause of Guam's avifauna extinctions (Savidge 1987): rhe geographie pattern of bird los ses mirrored the simultaneous population expansion of thc snake (th<1t i5, the snake spread northward across Guam on approximately the same sehedule a5 bird distributions retreated to Guam's north end); the snake is an efficient predator of thc species that declined; there is linIe or no eviclencc for alternate eauses of dcclines, such as pestieides, habitat destruction, diseases, or environmental eontaminants; all bird species were affected, including both native and introduced species (thus, the natives did not retreat in response to expansion of introduccd speeies); the brown tree snake is unexpeetedly eornrnon on Guam; and no comparable bird extirpations were observed on sirnilar nearby islands that lacked thc snake. For many of thc skepties, the evidenee that the brown tree snake is uncxpectcdlycommon on Guam \vas the clincher. Counting snakes is tough. Thcy are notoriously difficult to spot (Rodda 1993), and the brown tree sn,lke is partieularly hard (0 find bccause it is nocturnal and arboreal. Ir movcs slowly through the foliage at nighr, looking and often acting like a drab vine. Fcw visitors to Guam evcr see a snake. However, our markBioScience Vol. 47 No. 9

recapture and trapping By Oetober 1996, only 3 studies suggest that the of Guam's 12 native forest snake achieved peak densi~ bird speeies still survived in ties on Guam of approxithe wild. Of these, the Marimarely 100/ha (Radda er al. ana crow, Corvus kubaryi, 1992a). By contrast, large whose population i5 declinsnakes away from water or ing rapidly, appears doomed dens have maximum densi(the1996 count was five ties of 1-10/ha (Parker and individuals); the island Plummer 1987), and such swiftlet, Aerodramus vanisnakes rarelv attain dcnsities korensis, is relatively safe in excess of ~ few individuals (several hundred individuper hcctare. For cxample, als are in one unstable bullsnakes (Pituophis melacolony); and the Micronesnoleucus; Parker and Brown Figure 3. The brown teee snake (13oiga irregularis) is native ian starling, Aplonis opaca, 1980), rat snakes (Elaphe to New Guinea aod nearby areas; it was accidentally intro- is precarious (one probably obsoleta; Stickel et a1. duced to Guam after World War 11, \vith catastrophic viable population of 50-1 00 1980), and rattlesnakes rcsults for native wildlifc. individuals is in one urban (Crotalus horridus; Fitch areal. lt is, perhaps, telling 1982) all have densities of that in Guam a metapopulaless than 1/ha. Small snakes, tion of several hundred birds such as subterranean wormis considered "safe." Unlike eating snakes, can reach very Hawaii, where low-elevahigh densities (e.g., Carphotion forests are densely populated with non-native phis amoenus, worm snake, has been recorded at densibird species, most forests of ties of up to 729/ha; Clark Guam are now empty of 1970), but at 0.3 m, this avian life. The silence is consnake is much smaller than spicuous even to a casual the brown tree snake, whose ob server lJaHe 1994). maximum cotallength is apAlthough Guam's bird proximately 3.1 m. Small cxtirpations have received aquatie snakes, such as the most attention, many Regina alleni, the striped othcr specics are important crayfish snake, whose maxi- Figure 4. Tbe spotted-belly gecko (Perochirus ateles) is found eompooents of the browo tree mum length is 0.6 m, can only in Micronesia and onJapan's tin)' \hrcm; Island (Minami- snakc's diet. Juvenile snakes Tori-shima). It has disappeared from Guam, where it was reaeh densities of 1290/ha common in forests heiore the arrival of the hrown tree snake. eat lizards primarily, and (Gadley 1980), but only in adult snakes eagerIy ingest small water bodies. Snakes small mammals (Greene also reach high concentrations approximately 26/ha. Thus, at the 19S9, Savidge 1988, Shine 1991). AIaround dens, but on a tropieal is- crest of the initial snake population though the disappearance of silent land, such as Guam, no wintering irruption, the predator would have noeturnal marnmals and minute lizbehavior is seen. Thus, in relation to outnumbered potential avian prey ards was not as obvious as the disapthe densities expected of a eompa- by approximatelr 4:1, and the peak pearance of noisy, colorful birds, the rable snake, the peak densities of avian biomass of approximately 0.8 1055 of biodivcrsity was nearly as brown tree snakes on Guam were kg/ha would have been only 15%- complete; only three of Guam's lizunprecedented. 25 % of the peak predator biomass, a ard and mammal species have stable The density of this predator was precarious predator-to-prey ratio. populations. Moreover, two of the also excessive in relation to the den- For comparison, a garter snake three native bat speeies vanished in sity of the prey. Prey densities on predator-prey system in Ohio was reeent decades, leaving ooly the Guam prior to the arrival of thc found to have a peak biomass ratio Marianas fruit bat, Pteropus mariansnake were not known with any ac- of 1 :67, much lower than the 1:4 nus. Compared with the bat populacuracy, but an cstimatc of thc upper ratio that is theoretically sustainable tions on nearby islands that do not limit for numbers of bird individuals (Reiehenbach and Dalrymple 1986). have snake populations, nonvolant can oe calculated by adding the maxi- With the cven higher 4:1 predator- juvenile bats on Guam suffcr near mum densities known foe eaeh of the prey ratio found temporarily in 100% mortality atthe agewhen they species (Engbringand Ramsey 1984). Guam, it is not surprising that such are first eaehed by their foraging This calculation makes the unrealis- predation pressure caused bird abun- mothers (Wiles 1987). An unattended tic assumption that all species might dances to plummet. The Guam expe- nonvolant bat would be highly vulhave been at their maximum density rience showed ecologists that snakes nerable to brown tree snake predain thc same placc, but even so, the can attain densitics that are suffi- tion, and the elevated mortality of aggregate total bird density is only ciene to suppress prey populations. non volant young is presumed [0 be Getoher /997

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the cause of its eontinued example, one does not expopulation declinc. For the pect to hear of a sudden other two bat species, no surplus of garter snakes population data exist to incausing a localized shortdieate the eause of their dcage of frogs. The increase dines on Guam. in snake numbers, if it hapOfGuam's 12 historically pens at a11 in response to an native lizards, on1)' one spcirruption of prey, is likely to cies appcars to be as dense be long term and demoon Guam as on nearby snakcgraphically minor. A good ffee islands; six have been year for rattlers is generally extirpated from Guam (Figthe result of a bumper crop ure 5), three are rare and of rodents, rather than the localized (Figure 6), and two cause of a shortage of roare eommon but reduced in dents. Accordingly, snake abundance (Rodda and Fritts Figure 5. Slevin's skink (Emoitl slevini) is endemie to the numbers are typically reguMariana lslands (an Ameriean chain of islands \vithin 1992b). Theinterpretation of fvlieronesia). Guarn was the largest nf the islands inhahited by lated by "bottom-up" rather these population ehanges is this lizard, but it is na longer faund there, possibly due to than "top-down" trophic interactions. eomplicated by coneurrent in- predation by the inrroduced brown tree snake. troduetions of lizard and By contrast, extinction of prey populations by a mammalian predators and competitors, but it is likely predator is a decidedly topthat the snake caused the dedown proposition. What enablcd the brown tfee dines of severallizard speeies (Roddaandfritts 1992b).All snake to have such an impact on so many of Guam's native lizard speeies persist on Guam's tiny offshore isnative vertebrates? On one level, it is not necessary for lets, which the snake has a snake to bc an exceptional not yet reached. The details of eaeh extincpreuator to exert top-down pressure, it is only necestion may be open to dcbate, but the aggregate impact is sary that the snake be an exception to the generality unquestionably an astanishthat snakes are not abuning loss of biodiversity. Of dant. On Guam, the brown the native vertebrates, only tree snake was abundant. one hird and three lizard Before returning to the quesspecies re ta in lang-term vi- .Figure 6. The oceanic gecko (Gehyra oceanica) is ooe of tion of why the brown tree ability on Guam. severallarge geckos that vanished from Guam forests follo\vThe profound effeets of ing colonization and irruption of thc brown tree snake. This snake became so numerous, we describe how the snake's Guam's snakes stand in gecko is still oeeasionally found on ornamental plants in high population density stark contrast to the earlier Guam's urhan areas. Apparently, the arhoreal snake rarely turned it from an annoygenerali7.ation that snakc visits these iso la ted plants. ance inta a significant probpopulations would be of little ecological consequenee to prey bc small. Indecd, there is no evidence lem tor the human population. populations. That generalization had that snakes routinely reduce prey been based on the relative rarity of populations except on sma11 islands The strange case of Guam's most snake species and on the fact such as Guam. baby bites that their feeding is seasonal aud The fact that snakes nonnally ha vc opportunistie. That is, snakes can little effect on prey populations may The brown tree snake is a member of eat when prey are abundant and fast be related to another eharaetcristie the snake familv Colubridae, most when prey are scarce (Pough 1980). that most snakes share: low repro- of whieh laek - the sophistieatcd This feeding strategy crops the duetive potential. Snakes have far venom apparatus and highly toxie "doomedsurplus" (Errington 1956), fcwer offspring than rodents, frogs, venorn of the "truly" venomous corather than controlling or depress- or other common prey. Snake popu- bras and vipers. Manyofthenatricine ing baselinc prey populations. To lations may inctease following an colubrids (the garter snakcs and their diseourage the wanton killing of irruption of prey, but the subsequent allies) have saliva that can be irritatsnakes, conservationists often advise buildup of the predator is limited ing (McKinstry 1983, Minton 1979), farmers to allow snakes to live for and slow. In response to a prey popu- but the irritation is usually mild. No the purpose of rodent contro\. Hut if lation inerease, snake populations herpetologist would hesitate to snake populations are incapable of rarely increase so mueh that they handle a garter snake. Thus, little controlling the abundanccs of their overtax the food supply and ulti- credibility was aecorded to the early prey, their benefit to the farmer will mately depress prey abundances. For reports of serious snakebites on

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Guam. Srill, the reports kept coming. There have been more than 160 such cases, or approximately 1 in 1200 emergency room vi sirs on Guam, including ni ne ca ses of 1nfants who receivcd ventilation Of intubation to assist breathing (Fritts et al. 1990, 1994). What was shocking about these reports was not the seriousness of the bites but rather the circumstanees of the encounters. Whereas the modal snakebite victim in North America i5 a young adult suHused with a dangerous combination of testosterone and alcohol (lV1inton and Minton 1980), the typical snakebite victim in Guam was a sleeping infant of less than six months of age. In a few cases, the snake a ppeared to select the young infant in preference to larger children: in 2 of 11 medically serious bites, the victim was an infant sleeping between its parents or older siblings who were not bitten. Even if one indudes teenage and adult snakebite victims, 80% of a1l reported bite victims were sleeping at horne, not active Of sleeping outside of their homes. In a small percentage of bites ro sleeping persons (7'Yo), the victim was being constricted by rhe snake when discovered. Although constricrion may not ha ve changed the medical consequenees of anl' bite cases, the occurrenee of constriction is important beeause it suggests snake feeding behavior rather than self-defense. Many bite victims also exhibited multiple bites, as if the snake were repeatedly regripping the victim in an attcmpt to ingest prey thar is far too large. Although inferring motivation is always riskl', this pattern of snakebites more dosely resembles that of predatory strikes than that associared \vith defensive behavior. Apparently, the brown tree snake stumbles inro the eorridors of hornes at night, willing-although presumabll' not seeking-to bite exposed infants (Figure 7). This phenomenon, even if it involves onlr a less venomOllS rear-fanged snake, has added an entirely new perspective to snakebite. Moreover, this snake's apparent willingness to enter occupied buildings mal' help explain how it rcached Guam; it could have accidentally heen transported with shipped goods. October 1997

FigUfC 7. Althollgh most of Guam 's brown tree snakes are onl)' approximately 1 m in length, the spccics rcaches a maximum size of more than 3 m, enabling it to kill or seriollslv harm medillln-sized birds and

mamma'ls, such as chickens, puppies, ami s111all childrcn.

Foraging by brown tree snakes Guam's infant envenomations and wildlife extinctions have, not surprisingly, evoked countermeasures by wildlife managers (Fritts 1988). One of the most suecessful measures has been to trap the snakes (Fritts et al. 1989, Rodda and Fritts 1992a). Perhaps due co their broad diet, brown tree snakes readily enter traps rhat are baited with prey items, typically la bora tory mice (the mice are protected from the snakes and are not harmed by the experienee). In the process of perfecting the trap design, many experiments have been performed to elucidate the searching algorithm that is used by foraging brown tree snakes (Rodda et a1. 1992b), which turns out to be different from rhat used hy most other snakes. For instance, whereas most rattlesnakes hunt hy ambush and garter snakes tl'pically forage activelv, brown tree snakes do both (Rodd~ 1992). Consequent1y, the brown tree snake is likely ro use different sensory modaliries for capruring active and inactive prey. For example, a fIeeing lizard presents a

strong visual stimulus, but a concealed bird egg offers few visual cu es; thus, olfaction probably plays a major role in helping hrown tree snakes to locate eggs. Similarly, aerively fora ging garter snakes, which ofren search for immobile Of slow-moving prey, rely heavily on chemosensation to identify prey. However, the brown tree snake's foraging decisions appear to be more sophisticated. Unlike garter snakes, which will often attack and attempt to swallow an inappropriate objecr (e.g., a cotton swab) that has been soaked with an appropriate odor, brown tree snakes may ignorc food cues that appear out of context. For example, Chiszar et al. (1988b) found that hrown tree snakes ignorc isolated odors of mice burwill attaek oHactorl' cues in more realistic settings (Chiszar et al. 1992,1993). In some situations, brown tree snakes will attack mice that they see hut do not smell (i.e., mice remporarily placed in airtight but transparent boxes). They will also investigate an odor-infused opaque box, but they will not expend comparable eHort on a similar but transparent box (Lankford 1989). Apparently, the visually deteetable absence of prey is sufficient to redireet prey-seeking bchavior. Similarly, in some captive srudies (Chiszar er a1. 1988a), airborne olfactory cues have been insuffieient to elicit prcdation, but suhstrate-borne chemical cues have induced brown tree snakes to follow odor rrails to hidden prey. By contrast, Fritrs et a1. (1989) alld Rodda et al. (1992b) found that wild brown tree snakes were attraetcd to frcchanging traps that were baired with chicken litter but that adding olfactory trails leading to the trap bait did not enhanec trap capture success. Thus, bfown tree snakes appear to be facultative in their use of ChC111ical, visual, and other types of information. The faetors that determine the snakes' reliancc on their variow; sensory modalities are still not understood. Wild brown tree snakes also do not rcspond to pungent mammal baits, even though in the laboratory thel' respond to the same cues \vith high rates of rongue flicking. Brown tree snakes seern to be adept at distinguishing bcrweenlive prey and aJl

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artificial prey; we have yet to find an artificial cue that, in nature, elicits more than approximately 5% of the captures obtained with real prey, although in laboratory tests some prey extracts are indistinguishable from live prey. Consequently, disembodied odors are of minimal use for trapping brown tree snakes, even though it is clear from laboratory work that the snakes are aware of these odors and investigate them. Our working hypothesis is that brown tree snakes use multiple cu es and avoid traps that do not provide mulri-modality cues that confirm the presence of living prey. Given this sophisticated algorithm for identifying prey, it seems remarkable that brown tree snakes would mi stake hopelessly large sleeping infants for potential prey items. However, in laboratory trials, brown tree snakes routinely kill and attempt to eat rodents that are weIl beyond their gape limits. Ir is also possible that when searching visually, brown tree snakes fai! to comprehend that a portion of the infant is concealed by bedding. Forwhatever reason, brown tree snake herpetoculturalists have consistently found that this species has poor judgment with regard to the size of potential prey. Brown tree snakes will attack peey that aee too large for them to swallow; perhaps some of their attacks on ehildren rdleet this error. Nevertheless, brown tree snakes are capable of prodigious meals (Chiszar 1990). A snake's maximum meal size depends on its taxon: Vipers aod other heavy-bodied venomous and nonvenomous snakes are in one dass, whereas the more slender species, including the brown tree snake, are in another (Pough and Groves 1983). However, brown tree snakes stand apart from their class in the size of me als ingested; we have found brown tree snakes in (he wild with prey equal to more than 70 % of their mass. This is without precedent in the nonviper group. Another unexpected feature of brown tree snake foraging is that the snakes readily consume carrion and organic matter, which are not considered typical snake food. Far example, brown tree snakes have been found eating or having eaten dog food, chicken bones, raw hamburger, 570

maggot-infested rabbits, paper toweIs, spareribs, rotting lizards, ornamental betel nuts, larger conspecifics, dog placentas, and soiled feminine hygiene products. Curiousl r, many of these items do not have the visual appearance of a traditional prey item. Moreover, some of these items, such as hetel nuts, do not have the odor, color, temperature, vibration, or behavior of a traditionallive food item (although the fluts do resemble eggs in shape). Perhaps the snake's habit of switching between active and passive foraging modes has preadapted it to a wider, more sophisticated definition of suitable prey or to facultative reliance on sensory systems that are more or less obligat~ in other, less flexible speeies. Undoubtedly, the brown tree snake's liberal attitudes about prospective food items has allowed it to suceessfully colo11ize new habitats, including Guam.

Snakes as colonists Brown tree snakes oceur naturally in castern Tndonesia, New Guinea, the Solomon Islands, and the north and east coasts of Australia. As soon as sailing ships began to ply the seven seas, rats (first Rattus rattus and later Rattus norvel{icus) began appearing throughout the world, on virtually every island contaeted by the ships (Atkinson 1985). By contrast, snakes are not generally considered to be good colonists. With the exception of thc widespread parthenogenetic blindsnake Ramphotyphlops hraminus (cvery individual is a female, and each is capable of starting a population), few snakes have colonized remote islands. Are brown tree snakes uniquely C
terials and loaded them on harges for recycling or disposal on Ameriean soil (i.e., Guam). Once on Guam, the material would have been unloaded during the day, and the snake would, naturally, have remained concealed until nightfall, when its dispersal into the jungle would have gone undetected. Sinee reaching Guam, the brown tree snake has gained access to other previously snake-free islands. In the last six years, more than 40 snakes have been spotted on the previously snake-free island of Saipan, approximate]y 175 km north of Guam. We know of scven occasions in which the brown tree snake has been accidentally transported the 6100 km from Guam to Hawaii. Other individuals have been reported from sites such as Diego Garcia Atoll (Indian Ocean); Corpus Christi, Texas; and Spain. Thus, brown tree snakes seern to experience 110 difficulty in reaching new locations. But a single stowaway snake is unlikely to lead to a new brown tree snake population, unless it happens to be a gravid female. One feature promoting successful colonization in many snake species is the ability of females to store sperm. Although the brown tree snake has never been tested for this ability, other species of the same genus are eapable of storing spen11 for at least two years (Groves 1973), and several c10scly rela(ed snakes store sperm ror at least six years (Haines 1940). Thus, it is theoretically possible for a single snake to start a population, evell if she was not gravid at the time of accidental transport. Scientists do not know how many females were responsible for the Guam population, but it was probably a sm all number because most stowaways probably died in transit or failed to find mates in the newenvironment. If thc initial colonizing population was smalI, then presumably there were special eireumstances on Guam that made it possiblc for a small population to irrupt into an unprecedented infestation. Many explanations have bcell suggested for the extraordinary irruption, and the consequent exccptional impact, of brown tree snakes on Guam (Pimm 1987, Savidge 1987). Of the reasons that BioScience Vol. 47 No . .9

have been suggested, we are most impressed by the importanee of eoevolution between predator and prey. The overwhelming predominance of islands in the reeord of anthropogenie extioetions (Broekie et a1. 1988) is eonsistcnt with a heightened likelihood of predator irruption and prey extinetion when predator and prel' lack a shared evolutionary history. An aneedote from Guarn illustrates this point. In the proeess of searehing for the hypothesized disease that was eradicating Guam's birds, Savidge (1987) housed a flock of bridled white-eyes (Zosterops c. conspicillatus) in a laboratory aviary. While sleeping, these birds roost in aggregation. One night, Savidge discovered that a brown tree snake had found a wal' into the aviary and, by the time it was discovered, had consumed three of six white-eyes slceping side by side on a branch. The surviving three remained in place on the branch near the snout of the advaneing snake. Unlike birds in other locations, bridled white-eyes on Guam appear not to have evolved the behavior of waking or flying when a neighboring bird is eaten. Had Savidge not intervened, the birds' lack of coevolutionary experience with this predator would likely have cast a11 six theif lives. With theif generalist feeding habits, brown tree snakes were preadapted to find suitable forage on Guam, whcre prey density was extraordinarily high. Although prey density on Guam was not measured at the time when the snake arrived (i.e., 1950 or so), measurements from 1993 to 1995 indicate that Guam continues to have higher mamma I and lizard densities than are found on comparable tropieal mainland areas. For example, we reeently removed (in a span of days) an average of 55 rats/ha from a forested area of narthern Guam. Cornparable mainland forests have population densities in the range of -1.5-19/ha (0.8-6 kg/ha) for a11 rodent species combined (Fleming 1975). To measure the absolute dcnsities of Guam's lizards, we placed lizardproof fencing around four 10 x 10m patehes of forest and eounted a11 lizards that we encountered as the vegetation within eaeh pateh was removed. A year prior to the lizard

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sampling, snakes had been eliminated 1s the brown tree from two of the sites, and lizard snake unique? dcnsitics in these sites averaged 19,650fha (52.3 kgfha). In thc two Our understanding of possible snake areas still occupied by snakes, the behaviors and ecological interactions average lizard density was lower has been broadened by the study of (13,290fha; 33.7 kgfha) but still the brown tree snake. However, it is higher than in camparable maioland important not to generalize too mueh areas. For example, Duellman (1987) from a single example. Is this speeies faund an average of 57 lizards/ha exceptional? Or has aur understand(1 kg/ha) in the lowland tropical ing simply been limited by the pauforests of Cuseo Amazonico, Peru. city of opportunities to study tropiComparable data for the density of eal snakes, non-North American either rats ar lizards are not avail- snakes, or nocturnal arboreal snakes? able for the hrown tree snake's na- Does the brown tree snake have attive range, but our relative counts tributes that make it different from indicate that noerurnal lizards are most other snakes? approximately five times as abunTypieal pest speeies often have dant, and diurnal lizards approxi- high rcproduetive rates; however, the rnately four tim es as abundant, on brown tree snake does not. In recent Guam as in the brown tree snake's ycars, the modal size of detected native range. The abundance of liz- clutehes on Guarnhas been 3-4 eggs. ards on Guam is not unique to Guam Thus, it is not surprising that it took but has been reported for many is- many decades for brown tree snakes lands. Thus, the suceess of the brawn to build den se populations throughtree snake on Guam may be due as out the island of Guarn. Unlike the much to the unique eharacteristics of irruption of the zebra mussel, which island environments as to the unique spread over most of the North Ameriattributes of the snakc. can continent in a few years (Benson One unique feature of all modern and ßoydstun 1995), the biodiversity environments is the unprecedented erisis on Guam moved relatively level of human commeree. Guam slowly. However, as is evident from imports virtually all its food, build- the his tory of the human species, ing materials, and other goods. AI- eveo taxa with low reproduetive rates most a11 of this material comes from ean eventua11y overshoot 10eal carloealities with snakes and other po- rying capacities, eausing the extinetentia11y damaging exotic species. For tions of vulnerable prey. The above observations suggest example, a number of snakes, probabIy from mainland United States, re- that in eomparison to all other pocently arrived on Guam in a shipment tential pests, brown tree snakes have of Christmas trees. Similar introdue- relatively low feeundity, hut how do tions are apparent on other islands. they compare with other snake speOkinawa, for example, has recendy eies? Although natrieines and been colonized by eobras that have crotalines (rattlesnakes) have someeseaped from roadside attractions, and what larger average Urters than Hawaiian customs authorities have brown tree snakes (Seigel and Ford intercepted an inbound snake once 1987), neither these taxa nar any every two weeks, on average, in recent other snakes ean be deseribed as vears. 1 Island economies are unusu- highly fee und. Yet the brown tree ~l1y dependent on imports, but most snake case illustrates that an organindustrial communities also obtain the ism need not be highly fee und to be majority of their goods from elsewhere. a successful colooist ar potential pest. Thus, although snakes may not be Thus, in terms of reproductive outparticularly goou colonists under put, the brown tree snake is not natural conditions, present condi- unique; many other species of snakes tions provide an extraordinary num- are more fecund and therefore have ber of opportunities for accidental the reproductive potential to beeome translocation and eolonization. colonists or pests und er appropriate (i.e., undesirable) eircumstanees. The brown tree snake is well lL. l\'akahara, 1992, personal communicaknown for its willingness to eat ,,1 rion. Hawaii Dcpartment of Agricultllre, Honolulu, HJ. diversity of foods. Are other snakes 571

Figure 8. This snake was attempting to eat a baby pigeon out ofa nest on a power pole in Guam in 1988 when the weight of the struggling bird caused the snake and its mcal to sag enough to couta.::t another electrical conductor. The resulting surge of electricity killed the snake :md bird instantly.lt also caused in an islandwide power olltage that deprived 125,000 Guamanians of electricity for approximatdy 8 hours. Most of the 1500 power outages caused by the snakes have affected smaller portions of the island.

precludcd from becoming pestiferous by the specificity of their dietary requirclllcnts? Greene (1989) noted explicitly that the broad diet of the brown tree snake is widely shared b}' its approximately 30 congeners. Many other snakes, including many crotalines, are also similar to the brown rree snake in exhibiting an ontogenetic shift from ectothennic to endothermic pre}'. Moreover, the ingestion of carrion is unusual but not unprecedented among snakes. Crotalines, in particular, will eat nonliving, even putrefying, prey (Gillingharn and Baker 1981). Brown tree snakes are exceptionally good climbers (Chiszar ] 990), enabling them to ga in access to food sources that are denied to more terrestrial snakes (Figure 8). But hundreds of ar boreal snakcs have similar capabilities (Lillywhite and Henderson 1993), and Shine (1983) concluded that food habits of arboreal snakes are stmilar worldwide. Even the bizarre willingness of brown tree snakes to attack sleeping humans is found in South Asian snakes of the genus Bungarus (De Si!va 1992, Hati er al. 1988) and, indeed, other Boiga species. Thus, the dietary habits of thc brown tree snake are not unique. Other aspects of the brown trec snake's histor" on Guam are also not unique. The' introduction of the brown tree snakc to Guam was dependent on humans. Human transport requires of a snake a willingness to be around people and a propensiry for entering artificial objects. Man y other tropical colubrids, especially several spccies that have co10nized tropical istands, share the

572

brown tree snake's willingness to live alongsidc peoplc (Fritts 1993). The brown tree snake's tolerance of the ecological disturbance and human environments on Manus after World War Ir contributed to its arrival to Guam as a stowaway in military traffic. Successful human-aided colonization reqllires not only a likelihood of being placed aboard a ship, but also the eapability to survive during the sea voyage. Colonü,ation is undoubtedly facilitated in species that can fast during dispersal through inhospitable habitat (e.g., on ships or airplanes), and all snakes appear to have an cxceptional ability to fast bet\veen meals (Greene 1983, Pough and Grovcs 1983). A brown tree snake ean coneeal itself in amazingly sm all spaces, but this advantage of supple vermiform morphology is not unique to snakes, much Jess to brown tree snakes. Thus, the brown tree snake is not unique in cither its ecology or its behavior. If thc hrown tree snake is not uniqlle, we are led to two keycondllsions, one applying to herpetology and the other to conservation biology. The herpetological conclusioll is that the insights gained through the studv of the brown tree snakc could ha've been gained through the study of any number of other snakes. A cursory review of the snake ecology papers appearing in the Journal o( Herpetology from 1985 1995 indicates that approximatcly half of the research in this area is devoted to just rattlesnakes and natricines, especially garter snakes. Given that there exist over 2600 species of

'0

snakes, herpetologists should strive to studya wider diversity of species and dades, particularly tropical species. For conservation biologists, the inferencc isthat snakes can cause biodiversity crises in a wide variety of contexts. Prey species on islands seem to be especially vulnerable, but mall}' prey species on continents also lack coevolutionary experience with nocturna! arboreal snake predators. 1f not B. irregularis, the cu I prit could be Roiga trigonata (the gamma cat snake, a native of Asia), Trimorphodon biscutatus (the lyre snake, a native of North America), or the deadly Yrimeresurus flavoviridis (the habu, a native of Japan). These three snakes are, like the brown tree snake, venomous, nocrurnal, and at least partially arboreal-hut so arehundreds of other species. Would thc invasion of the Galapagos lslands by a generalized predatory snake that threatened thc uniqlle radiation of Darwin's finches differ from what occurred on Guam? More important, could it happen? As the world becomes more tightly uni ted through commerce, the probability of global fauna homogenization and catastrophicsnake introductions will grow.

Acknowledgments Our research has becn made possible primarily through the support of the OS Departments of the Interior and of Defense. We thank the Guam Division of Aquatic and Wildlife Resourees for hospitality and assistance. \X-'e greatly apprcciate the skill and persistence of the many people who have assistcd us in the field. We wish to thank ;\larie Timmerman, Kathy Dean-Bradley, and Rcnee Rondeau, who suggested improvements to this article.

References citcd Arkinson TAL 1985. Tht spread of COl11l11Cl1sal species of Rattus to oceanic islands and their effccrs on island avifaunas. Pages .15-R 1 in Moors Pj, ed. COllscrvatiun of island birds. Cambridge (UK): I.nternational Coulleil for Bird l'reservation. T echnicall'l!blication nr 3. Baker RII. t946. Senne effccts ofthc \-var on rhe wildlife of Micronesia. Transactiuns of the North Amcrican Wildlifc Conferenee! J: 207-213. Benson Aj, Boydstun er. '1995. Invasion of the Zeb ra ~lllSSel iTl the United States.

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Pages 445--446 In LaRoe E, Farns G, Puckett C:, Doran P, Mac M, eds. Our living rcsuun:cs: a repurt to the natiun on the distribution, abundance, and health of U.S. planrs, anil11als, alld ecosystel11s. Washington (DC): US Depanment of Interior, National Biological Service. Brockie RE, Loope LL, llsher MR, Hamann O. 1988. Biological inva~iuns of islamj nature preserves. Biological Conservation 44: 9-36. Carano P, Sam:hez pe 1964. A complete his tory of Gualll. Rutland (VT): C. E. Tnttle. C:hiszar D. 1990. The behavior of thc brown tree snake, Boiga irregularis: a srudy in applied comparative p~yehology. Pages 101-123 in ])ew~bllry D, IOd. Contemporar)' issues III comparative psyehology. Sunderland (MA): Sinauer. Chiszar D, Kandler K, Lee R, Smith HM. 1988a. Stimlllu~ wntrol of prt:datory attaek in the brown tree ~nake (Boiga irregularisl. 2. Use of chemiea] eues during foraging. Amphibia-Reptilia 9: 7788. ___ .1 988h. Stimulus contral of predatory attaek in the brown tree snake (Boixa Irregularis) I. Effects of visual cues arising from rrey. The Snake 20: 151-15.1. Chisl.ar D, Fox K, Smith HM. 1992. Stimulus control ofprcdatory behavior in the hrown tree snake (BIJiga irregularis) IV: eHeer of mammalian hlood. ßehavioral and Neural Biology 57: 167-169. Chiszar D, Dunn TM, Smith HM. 1993. Response of brown tree snakes (BO/ga irregularis) to human blood. Journal of Chemieal Ecology 1.9: 91-96. Clark DR Jr. 1970. El"Ological study of the worm snake Carphophis vermis (Kennieott). University of Kansas Publications of the Museum of Katural History 19; 89-194. Craig RJ. 1994. Regeneration of native Mariana Island forest in disturbed habitats. Microne~iea 26: 97-106. De Silva A. 1992. Bungarus caeru!elJ.s; its eeology and bite in Sri Lanka. Page; 746760 in Gopalakrishnakone P, Tan CK, eds. Reecnt ;ldvances in tox:ieology research. Vol. 1. Singapore: National Univcrsity of Singapore. Diamond JM. 1984. Possible effeds of unresrricred pesticide use on tropieal birds. Nature 310: 452. Duellman WE. 1987. Lizards in an Amazonian rain forest community (Peru); [csouree utilization and abunJalh.:e. Narional Geographie Research .1: 489-500. Engbring J. 1983. Fore;;t birds of Guam in critical danger. US Fish & Wildlife Service Endangered Spl'cies Technlcal Bulletin 8: 6-8. EngbringJ, Pnltt HO. 19H5. Endangered birds in Mieronesia: their history, status, and future prospeo.:ts. Pages 71-1 OS in Temple SA, ed. Bin.! con~ervation. Vol. 2. MadiSOll (WJ): University of Wi'icomin Press. Engbring .I, Ramsey FL 1984. Distribution andabundance ofthe forest hirds ofGuam: results of "l 1981 survey. US Fish & Wildlife Service. Pub!Jcation nr FWS/OBS-841 20US. Washington (OC): US rish &Wi!dlife Service.

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Errin,l',ton PL 1956. Factors limitin,l', higher vertehrate populations. Science 124: .104307. Fiteh HS. 1982. Resourees of a snake community in prairie-woodland habitat of northeastern Kansa&. Page, ~3-97 in Scutt :"Jj Jr., ed. Herpetologiea! commuDlties. Wa~hington (DC): US Fish & Wildlife Service Wildlife. Report nr 13. F1eming TH. 1975. The rolc of small mammals in tropical eeosystem~. Pages 269298 in Golley FB. PetrusewicL K, Ryszkowski L, eds_ Small mammals: their productivity and population dynamics. Cambridge (UK): Camhridge University Press. Fritts TH. 19~~. The brown trcesnake, Boiga irregularis, a threat to Pacifie islanos. Biological Reporr nr 88(31). Washington (DC): US Fish & Wildlife Service. ___ . 1993. The common wolf snake, Lycodon aulicus caputinus, a n:cent (;010nist of Christmas Island in the Indian Ocean. Wildlife Rese"lrch 20: 261-266. !-"ritts TH, McCoid MJ. 1991. Predation by the brown tree snake 011 poultry and orher dOl11estieated aniITlals in Guam. The Snake 23: 75-80. Fritts TH, Swtt NJ Jr., Smith BE. ]989. Trapping Boiga irregularis on Guam lISing bird odors. Journal of Herpetology 2.1: 189-192. Fritts TH, .McCoid MJ, Haddock RL. 1990. Risks to infants on Guam fram hites of the hrown rree snake (BoiJ;a lrregularisl. Ameriean Journal of Tropical .Medicine and Hygiene 42: 607-611. ___ . 1994. Symptoms and elfcumstances a~sociated with bites hy the brown tree snake (Colubridae: Hoiga irregularis) un Guam. Journal ofT lerpemlogy 28: 27-33. Cillingham JC, Baker RE. 1981. Evidence for scavenging behavior in the western diamond back rattlesnake (Crotalus atrox). Zeitschrift für fierpsyehologie 55: 217227. Godley JS. 1980. I-"oraging eculogy of tbe striped swamp snake, Regina alleni, in southern F1orida. EcolugicaJ Mon'ographs 50: 411-436. Grecne HW. 1983. Dietary corrclates of tbe origin and radiation of snake~. Ameril'an ~oologisr 23: 431--441. ___ . 1989. EcoJugi;:OlI, evolutionOlry, and conservation implications of feeding biology in Old World eat snakes, genus Boiga (Colubridae). Proceedings of the California Aeademy of Seienees, Serics nr 4, 46: 193-207. Croves JD. 1973. De1ayed fertilization in the mOlke Boiga dendrophila. Herpetologica 29: 20-22. Grue CE. 1985. Pesti(;ldes and tlle decline of Guam's native birds. Nature 316: 30 I. Haines TP. 1940. Delayed fertdization in Leptodeira mmufata po!ystirta. Cupeia 1.940: 116-118. Hati AK, Saha SC, Banerjee 1), Banerjee S, Panda 0. 1.988. CJinic"ll features of poisonmg by (;ommon kraits ami treatment with polyvalent anrivenin. [he ,',nake 20: 140-143. Jaffe M. 1994. Ancl no birds sing. f\iew York: Simon & Schuster. Jenkins JM. 1983. The native forest birds of

Guam. Washington (DC): Ameriean Ornithologisrs' lJnion, Ornithology Monographs 31: 1-61. Lankford JD. 1989. Stimulus controI of foraging in brown tree snakes (Boiga irregularis). Journal of the ColoradoWyoming A~-ademy of Seienees 21: 12. Lillywhite HB, Henderson RW. 1993. Behaviora] and functional eeology of arboreal snakes. l'ages 1-48 in Seige! R, CoJJins J, eds. Snakes: ecology and behavior. New York: McGraw-Hill. Marshall JT .Ir. 1985. Guam: a problem in avian cunservarion. Wilson Bulletin 97: 259-262. MeKinstry DM. 1983. Morphologie evidenee of toxie saliva in coluhrid snakes: a checklist of world genera. Herpetologieal Review "14: 12-lS. Minton SA Jr. 1979. Beware: nonpoisonous snakes. Clinical Toxicology 15: 259-265. Minton SA Jr., Minton MR. ]980. Venomous reptiles. New York: Charles Scribner & Sons. Morison SE. 1953. New Guinea and the Marianas, March 1944-August 1944. Boston: Little, Brown Olnd Co. Parker WS, Brown WS. 1.980. Comparative e(;(l]ogy of [WO eolubrid snakes, Masticophis t. taeniatus and Pituophis melanoleueus deserticola, in northern Utah. Milwaukee Puhlic Museum Puhlications in Biology and Geology 7: 1-104. Parker WS, Plummer MV. 1987. Population ecolog}'. Pages 253-301 in Siegel RA, Collins ]T, Novak SS, eds. Snakes: ecology and evolutionary hiology. "\lew York: MacmiJlan. Pimm SL. 'J 987. The snake that ate Guam. Trends in Ecology & Evolution 2: 293295. Puugh FH. ] 980. The advantages of eetothermy for tetrapods. Amencan Natur,llist 115: 92-112. rough FH, Gruve~ JD. 1983. Speeializations ofthe bodyform and food habits ofsnakes. American'Zoologist 23: 443-454. Reichenbach NG, Dalrymple GH. 1986. Fnergy use, life histories, and the evaluation of potential competition in two species of garter snake. Journal of Herpetology 20: 131-153. Rodda GH. 1992. For"lging behaviour of the brown tree snake, Boiga irregularis. Herpetological Journal 2: 110-1/4. _ _ _ . ] 993. Where's Waldo (and the snakes)? Herpetological Review 24: 4445. Rodda GH, Fritts TH. 1992a. Sampling rechniques for an arboreal snake, Boiga irregularis. Ivticronesica 25: 23-40. ___ . J 992b. The impact of the introducti on of the brown tree snake, BOlxa irregularis, on Guam's liz
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Eco logy 68: 660-66 8. _ _ . 1988. food habi ts of 8 o;/:R irregularis, an introduced preda wr o n Gu am.J ournal of H erpctology 22: 275-282. Savidgr JA, Sileo L, Siegfried LM. \992. Was discasc involved in the decimati on of Guam', avifauna? ,Journal of WilJlife Diseases 28: 206-2 14. Seige! RA, ForJ NB. 1987. R~pruduct i ve e(;Olos y. Pages 210-252 in Seigd R, Co!lins J, Nova k S, eds. Snakcs: C'c ology and evoluriona ry biology. New Yor k: Macmill:m. Sh ine R. 1983 . Arborca lüy in s n ~ kes: ecology o f Ihe Au.~ tra li ;l n ehl pid gen us Hop /ocel'lJalus. Copeia 1983: 198- 205. _ _ . 1991. Strangers in ;1. srrange land: ('.c(l logy of I\u stra lia n "o lubrid snakcs. Cvpeia 1991: 120- 131. Stca dman nw. 1995, Prdli srori c extinetivns vf Pacifü; Islam! bird s: biodiversirr meets zooarchaeology, Scicnce 267 :1123- 1131. Stic kel LF, Stickel Willia m H, Schmid Fe. 1980. Ecology of a Mar yla nd populat ion o f black Tal sna kes (Elaphe o. obsoh>ta). American Mid land Nat ura lisT·103: 1-14. '0'311 H. i p~ r C m, va ll Ri pe r SG, Goff MI., LJ.ird M. 19R 6. The epi 1.Oori ology ;Jnd ~co l og ica ! significance uf malaria in H awaiian land bi rds. Ecolosica l Monographs 56: 327-344. Warntr R.E. 196!:i. Thc role of introduced dise;'lses in the extincrion of the endemie Ha wa iian avifauna. COlldor 70: 10 1-110. Wilcs GJ. 1987. Cu rrcnt research ;llld fu tu re ma .... agc ment of Ma ri :lt13 s fr u it bats (Chi roplc ra: Ptcropod idae ) o n Guam. Aust ra lia n Ma mmal og~' 10: 93- 9S.

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Harvard University Bullard Fellowships in Forest Research

E

ach year, Harvard Un iversity award s a li mited numbcr of Bullard Fellowships to indiv idual:-; in biological, social, phys ~ (ca l, and political sciences (0 promote advanced stud y. research , or imegw(io n of subj ec(s penain ing (0 forested ecosystcms. The Fe llowships, wh ich include st ipends up to $30,000, are intended to prov ide indi viduals in mid~ ca reer with an opponunity to ut ilize the resources an J to interact with pe rsonnel in any depa rtmcnt within Harvard Univers ity in order to dcvelop their uwn sc ientific and professional growth. In recen t years, Bullard Fell mvs luve been associated with the H arv~rd Fores t, Depart~ mem. of O rganismic and Evo lutionary Biology, (ind the J. F. Kennedy School of Gove rnmem and havc wo rked in are
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