HERPETOLOGICAL NATURAL HISTORY VOL.9 2002 NO. I

Herpetologicall{atLtal Histort', 9( I ), 2002, pages1-14. 02002 by La SierraUniversity

A REVIEW OF 30 YEARS OF ECOLOGICAL RESEARCH ON THE SHEDAO PITVIPER, GLOYDIUSSHEDAOENSIS

Richard Shine BiologicalSciences A08, Universityof Sydney,NSW 2006,Australia Email:rics @ bio.usyd.edu.au

Li-Xin Sun Snakelsland Natural ProtectionDistrict, Lushun,People's Republic of China

ErmiZhao ChengduInstitute of Biology, The ChineseAcademy of Sciences. Chengdu610041. People's Republic of China Email: [email protected]

Xavier Bonnet ConseilG6n6ral Des Deux Sdvres,CEBC, CNRS,79360 Villiers en Bois,France Email: [email protected]

Abstract. Although it remainsvirtually unknown to westernscientists, an insularpopulation of pitvipers in northeasternChina has attractedintensive study for > 30 yr. The small (< I km2) island of Shedaolies on a migratory pathway for .and the regular spring and autumn migrations of thesebirds supporta remarkablydense population of endemicpitvipers (Glot'diu" shedaoensis). Adult pitvipersof both sexes average60-70 cm snout-ventlength and prey almostentirely on birds. Juvenilesnakes feed lessoften than adults,and consumeinvertebrates as well asbirds. Reproductive output is high, perhapsbecause the assured "survival food supply after parturitioneach year minimizes energy-based costsof reproduction."OfTspring size is large, presumablyas an adaptationto the paucity of small prey items on the island. The ambushbirds from treesand shrubsas well as from the ground;arboreal ambush sites are more frequentin juveniles than adults.Snakes are inactive for most of the year apartfrom brief (6-wk) periodsof bird migra- tion in spring and autumn.Even in peak periods,only one-thirdof snakesare active eachday. The snakes display high philopatry and high energy-assimilationefficiency. Research on G. shedaoensishas stimulat- ed major conservationinitiatives to eliminateillegal collecting,reduce fire frequency,increase water avail- ability, reducethe numbersofintroduced weedsand rats,revegetate areas affected by landslides,and some- timesdirectly supplement food suppliesfor the snakes.Since these management strategies commenced. the numbersof pitvipers have increasedsubstantially and the age structureof the populationhas shifted.

Key Words. China: Conservation:Foraging; shedaoensis; Reproduction; .

Studiesof snakeecology have increaseddra- proportion of the world. For example, North maticallyin numberover recentdecades (Shine and American gartersnakes (Thamnophis spp.) and rat- Bonnet 2000).Although this increasehas involved tlesnakes(Crotalus spp.) and European vipers an expansionofthe geographicand taxonomic range (Vipera spp.) continueto be the subjectsof a high of study,most researchhas continuedto focus on a proportionof all studies.Thus, much of the expan- relativelysmall numberof taxa in a relatively small sion ofresearchon snakeecolosv has involved more Herpetological Natural History,Vol. 9(1),2002

work on already-studiedtaxa and areas. Based on the ambitious conservation-orientedecological studies contentsof recentissues of hetpetologicalor ecolog- ever conductedon snakes.Remarkably, the ical journals,or reviewsof snakeecology (Seigel involvedis one that mostprofessional herpetologists andCollins 1993), one could imagine that there have havenever even heard of, let aloneseen. Because it been virtually no detailedstudies on the ecologyof occursin China.and mostpublications about it arein the snakefauna over largeparts of the world. Chinese-languagejournals, the researchcarried out This apparentneglect may tell us as much about on this taxon has attractedvery little attentionfiom the lack of communicationbetween scientists writ- researcherswho publish in western-language ing in diff'erentlanguages. as aboutthe actualdistri- (English,French, etc.) journals. bution of researcheflbrt. In this paperwe review the In an attemptto bring the Chineseresearch to resultsof a prolongedand arnbitiousresearch pro- the attentionof westernscientists, we review major gram on the pitviper Glot'diusshedaoensis (Fig. l), resultsof studieson this system.This is not a a program arguablyrivaling even Henry S. Fitch's straightfbrwardtask. Previous English-language herculeaneftbfts (Fitch 1999)in somerespects. The publicationson this system(Huang 1989;Li 1995) Shedaoresearch program is surely one of the most generally provide conclusionsbut not actual data nor statistical analyses.For the raw data,we have gone to the original pub- lications. In cases where sufficient detail is available.we have carried out statisticaltests on appropriatehypothe- ses(all such testsin this paper are our own, rather than reporting of prior analyses).Most of the Chinesepapers do not includesuch tests, and often they provide only average values (albeit, ofien with accompanyingSDs). It was not always f-easibleto retrieve original data becausenumerous workers have beeninvolved, many of whom are now retired or deceased.We also mention major resultsthat were simply reported as conclusionsin the original studies. BecauseChinese workers have tended to measuretraits other than thosetradi- tionally quantified by westernworkers (againreflecting the lack ofinternation- al communication),we supplementthis review with original data fiom our recentcollaborative studies.

MATERIALS AND METHODS

Study Area Shedao(literally, " island") lies approximatelyl3 km (7 nautical miles) off the coast of the Liaodong Peninsulain northeasternChina. in the BohaiSea (38"57'N, 120"59'E). The islandis 0.73km2 in overallsize. and is Figure l. The Shedaopitviper. Gloydiu.sshetluoensis. in a typical arbo- very steep-sided.The highestpeak on real fbraging pose. the island is 215 m above sea level. Shine et al.-Ecology of Gloydius shedaoensis

mateand lack of standingwater, the island supports 209 speciesof plants.Except for very steepareas, L) most pafis of the island are coveredby shrubsor trees. The species comprise plants typical of NorthernChina. Surveys have revealed 143 invene- brate taxa on Shedao, primarily afihropods. Apart fiom Shedaopitvipers. the only vertebratesliving permanentlyon the island are one microchiropteran bat (Pipistrelltr.subranttts'), the introduced brown rat (Rtrttusrnn,egicus), and seabirds(blacktailed gull Lanrs c'rassircstris'.Chinese egret Egrctta eulo- EESFg€€.qu"siap ltote s ; nofthern white-rumpedsw ift Ap Lrs 1t ucifi r:u s ). Eachyeerr the islandis visitedby largenumbers of migratory birds (at least 84 speciestotal, -50of them passerines:Snake Island Survey Team 1973, 1974.1976; Shine et al. unpubl.data). The migra- tion occursin two discreteseasons. in spring(rnid- April to the end of May) and autumn (late August until the end of October).Most of these transient birds probably remain on the island lbr only a few days(Snake Island Survey Tearn 1974. 1976). The peakof the bird-migrationperiods occurs befbre (in spring)and after (in autumn)the major snake-acriv- EEgEgi€aB8tEity periods,presumably because thermal conditions restrictsnake lbraging more than bird rnigration. Figure 2. Weatherrecords from Shedao,based on a meteorologicalstation set up on the island.The -eraphs History of Ecological Research showmean minima and maxinta (upper graph) and mean Althoughthe islandand its snakesmust have valuesand standard deviations tbr daily records(lower been known to local people (fishermenfiequently graph)over the years 1.990 91. visit the islandin smallboats in calm weather),the first scientiflc reports of the extraordinarydensity Severalephemeral watercourses run in shallowval- of pitvipers on Shedao date from the Japanese leys on the southeasternside of the island,but there occupationof Manchuria(Hasegawa 1932; Koba is no permanentwater except for that provided by 1933,1938; Mori 1932).Although based on only a humanactivities (see below). The islandis fbrmed singleday's data collectionon the island,Koba's by sedimentaryrocks that have beendeeply fblded 1938paper provides a long (20-page),detailed. and and fractured,creating many crevicesthat provide well-illustratedaccount on topics such as the retreatsites for snakes.The island was fbrrned by snakes'morphology, diet, and feeding behavior. uplift about one million years ago, but was con- Chinese scientistsbegan significant research nectedto the mainland(Liaodong Peninsula)inter- on Shedaoin the 1950s,although most paperswere mittently during Pleistocenesea-level f-luctuations brief andmany were semi-popular (Wu 1957,1958, (Li 1993:Zhao 1980). l96l). The initial stimulustbr the work was scien- The climateon Shedaois highly seasonal,with tific curiositybut with increasingunderstanding of an annualmean temperature of about 10"C.Winters this remarkablesystem the emphasisbegan to shifi are severelycold. During the snakes'main activity towardsresearch on conservationissues. Several periods(May and September).air temperaturetypi- major paperswere publishedin the 1970sunder "Snake cally rangesfrom l0-20"C (Fig. 2). Rain falls pri- collectiveauthorship of the IslandSurvey marily in summer(June-August). The island is fie- Team,"including a semi-popularsynthesis of major quentlyexposed to strongwinds, typically fiom the resultsrn 1976.The researchwas broadly-based. southeastfrom March-July but switching to the and includedextensive surveys and analysisof the north in September.Despite its small size,cool cli- island'sflora andfauna, not simplythe snakes(e.g., Herpetological Natural History, Vol. 9(1), 2002

Huang 1979). For example, avian migration pat- the venoms of most other Asian pitvipers (Zhang ternsattracted detailed study. 1989;Zhangand Hsu 1985;Zhao1980; Zhao et al. 1979).Interperitoneally injected LD5es in mice aver- aged0.81 mg&g (Zhangand Hsu 198,5).In compar- Early publications refer to the snake as ison, LDr.,s averaged 0.38 fbr G. intermedius, Agkistrodonhalys,but Zhao describedit as a sepa- 0.33-0.63for G. ussuriensls,0.49-0.88 tor G. bret'i- rate speciesln 1919(Zhao 1919')based on morpho- cattdus,and 0.83 for G. saxcttilis(Zhang and Hsu logical traits.Zhao recognizedtwo disjunctpopula- 1985).A more recentstudy supportsmost of these tions of Agkistrodon shedaoensis,one on Shedao conclusions(Chen et al. 1992).Chinese scientists Island and one in mountainousareas of the main- envenomatedby G. shedaoensishave developed land (QuianshanMountain. 90 km S Shenyang; massivelocal swellingbut few or no systemicsymp- Long-panshanMountain. 100 km N Dalian).A sub- toms (LS, pers.obs.). Hospitalization for up to 2 mo sequentpaper by Zhao (1980)examined the taxo- can occur afier a very severebite (LS, pers.obs.). nomic distinctivenessof the island snakesin much Fangsof adult G. shedaoensisaverage 7.1 mm more detail using a wide array of data including in length (range:4.5-10.0 mm) and rhe venom electrophoreticanalysis of venoms,venom toxicity, gland weighsan averageof 163 mg (50-3l0 mg: immunodiffusion, and scalation counts (see also Wu 1.977a).A singlebite yieldsapproximarely 96.5 Chenet al. 1984).Zhao (1980)also interprered the mg of venom (21.5-156.6 mg). A snakerequires biogeographichistory of the taxon.The distinctive- about 10-15 d to fully replenishits venom supply nessof G. shedaoensi.rwas further demonstratedby after emptying the glands(Wu 1977a). Jiang and Zhao (1980), who compared G. sltedaoensiswith mainland pitvipers in terms of Morphology ecologicaltraits such as habitatuse, food habits, Gloydius shedaoensisis a relatively large daily activity cycles,seasonal activity patterns,tol- species,with a maximum recordedbody length of eranceto low temperatures,and reproductivebiolo- 99 cm (Li 1995).Adults averageabout 60-70 cm gy (datesofparturition, litter sizes,ofIspring sizes). total length. comparedto < 60 cm for most other Since those studies.most authoritieshave Chinesespecies of Gloydius(Zhao 1980).General treatedG. sheduoensisas a separatespecies lsee body shapeis similar to that of congenerictaxa LiteratureCited). However, Ji et al. (1989)treated (Gloyd and Conant 1990).The dorsal scalesare G. shedaoensl.sas a subspeciesof G. saxatilis, stronglykeeled, and the overall color ofthe dorsum based on similarity of colorationand scalation. ranges from dark gray to pale pinkish-gray. Electrophoresisof 23 presumptiveloci failed to dis- Irregular light-colored blotches break up the ani- tinguish betweenG. snxatilis and G. shedaoensis, mal's outline. suchthat the snakesare well camou- althoughthis techniquedifferentiated all other taxa flaged.both in arborealand terestrial situations. investigated(Murphy et al. 1993).Genetic studies Early studiesprovided data from dissectionof indicate that the two G. shedooensispopulations snakesto quantify relative massesof medicinally are very similar to eachother, but distinct from G. important components of the body such as fat saxatilis(Shan et al. 1993).The overallconclusion stores,gall bladdersand venom glands,as well as fiom this work seemsto be that G. shetlaoensisis the gonads (Wu 1911a). This work documenred indeed a distinctivetaxon, albeit closely relatedto higher fat reservesin adult females than in adult G. saxatilis.Recent changes to the understandingof males(Wu 1977a).Li (1995)provided an English- higher-level phylogenetic relationships within languagereview of scalation.body size, color and "Agkistrodon," pitvipers have led to division of skeletalmorphology. with the Asian speciesnow allocatedto Clol'dius Males and females attain similar adult body (Gloyd and Conant1990: Parkinson et al. 1997). sizes(Table l). Analysisof our own dataon SVLs of adult snakesconfirms that meanadult body sizes RESULTS AND DISCUSSION are very similar in the two sexes(unpaired /1a.3 = 1.11,P = 0.25).Body sizesat maturityare known Venom Composition, Toxicity, and Yield with confidence only for females; the smallest The venom of G. shedaoensiscontains ncr f'emaleof 79 animalsrecorded to give birth was 5ul detectableneurotoxins. and henceis lesstoxic tnan cm long (Sunet al.2002). Shine et al.-Ecology of Gloydius shedaoensis

TABLE 1. Body sizesand sexualsize dimorphism of Shedaopitvipers, Gloydius shedaoensis. Table showsvalues tbr total body length,except that the last row showssnout-vent length and is basedonly on adult snakes(estimated at > 50 cm SVL).All measurementsin cm.

Males Females Reference

range mean (SD) range mean (SD)

9 48.0-78.4 1 69.7-84.0 Koba(1938) 87 61.2-82.0 78 60.0-79.0 SnakeIsland Survey Team (1973) 19 53.3-73.0 64.4 28 50.4-78.2 69.3 Zhao(1980) 4t 54.5-80.0 70.2 4l 5t.2-76.1 68.3 Ji et al. (1989) 64 51.0-69.0 59.8(4.5) 81 50.0-74.0 60.7(5.0) Shine et al., unpubl. data

Life History Juvenile snakestend to emergebefbre adults, and Chineseresearchers have classifiedsnakes as adult f'emalesbefbre adult males: such a patternis "adult," "old 'Juvenile," or adult" basedon body quite unusual among snakes(Sun et al. 1993, size, color, scale rugosity,and the presenceand 2001).Even at thepeak ofthe bird abundance,only numberof white spotson a snake'shead and body about one-third of snakes in the population are (Li et al. 1990;Snake Island Survey Team 1979). activeon any givenday (Sunet al. 1990).This esti- "white These spots" are unpigmented scales. mate was derived by paint-marking snakeswithin Although long-termmark-recapture programs have large field enclosures,followed by visual censuses beena centralfeature of researchon snakeecology to determine the proportion of marked snakes in western countries and in Japan (Fitch 1999; active at differenttimes. During summerthe snakes Fukada 1992),they have not been employedin are largely inactive,and remainhidden exceptafter China. Such a study has recently commencedon rain ihowers(Li 1995).The autumnbird-migration Shedao,to clarify growth trajectoriesand agestruc- period engendersa similar level of activity to the ture of the Shedao pitviper population (Sun, spring migration, with the snakesdisappearing to unpubl.data). their hibernation sites in late October. Detailed Demographyhas been well-studied,with sev- analysesreveal subtle seasonal shifts in habitatuse; eral short-termmark-recapture censuses to quantify for example,the proportion of snakesrecorded in both absolutenumbers of snakesand population grassversus trees varies among months. The snakes compositionin terms of sex ratio and age structure. use both habitattypes fairly equally in midsummer Femalesgenerally outnumber males in thesecounts (when there are no birds to eat), but tend to be (53Voof 1638snakes in Li et al. 1990against a null found more often in treesduring the bird-migration p of 50Vo,t = 4.52,df = l, < 0.05).The proportion periodsof springand autumn (SnakeIsland Survey of the populationcomposed ofjuvenile snakeshas Team l9l4; Yang 1986).Such shifts may, however, decreasedthrough time becauseheavy commercial reflect seasonalbiases in observability(due to veg- harvestingremoved many adult snakesduring the etation growth in summer) rather than (or as well earliestyears of study (Huang 1990).With the ces- as) actualchanges in snakebehavior. sationof harvestingin 1980,relative numbers of Becauseparturition is highly seasonal,the age adults have increased.By comparing numbers of structureof the population shows regular seasonal offspring born to the rate of population recovery, f-luctuations.Neonates are most abundantin late Huang (1990) estimatedan annualsurvival rate for autumn, soon after birth (Snake Island Survey neonatalsnakes of approximately567c. Team 1974).

SeasonalActivity Patterns Diel Activity Patterns The snakes hibernate through the colder Within the main seasonsof activity,the snakes months of the year, emergingin mid-April during also display regular diel patterns of movement. the first bird-migrationperiod (Huang 1989; Li et They typically spendthe night on the ground,ofien al. 1993; SnakeIsland Survey Team 1914, 1916). under rocks or grass.They climb to their ambush Herpetological Natural History, Yol. 9(l), 2002

sitesearly in the morning.stay there for a f'ewhours, Many papers report litter sizes. mostly fiom then retreatto the ground in the late mornin-e(Sun dissectionsof gravid females(e.g., Huang 1989; 1990;Shine et al. 2002(1).They returnto the treesln SnakeIsland Survey Team 1974;Wu 1977a).More the late afternoon,descending at dusk. Some ani- extensivedata came from a study in which near- mals remain at their foraging sites overnight, and term femaleswere capturedand rnaintainedin cap- othersmove aboutactively atter dark. tivity until they gavebirth (Sun et al. 1993,199,1, Home rangesof individual snakesinclude an 2002). Stillborn offspring are rare (5.3% ot overnightretreat site (on or under the ground)plus neonateswere stillborn:Sun et al. 1993).The pro- one or more foragin-9sites. These are typically close portionof reproductiveanimals in samplesof adult together (Sun 1990). Individual snakesusually femalesaverages around 257c, suggestinga 4-yr returnto the samefbraging site over long periodsof reproductivecycle (Sunet al. l99zl).For example, time. lf displaced (even to the extent of being Li et al. (1990)reported that72 of 323 adult-size removedfiom the islandand released in the seanear- femaleswere gravid during summer(23ch). Of 64 by), they rapidly return to their original capturesite femaleswith lengths> 900 mm, only ten were (Sun1990). Snakes displaced 500 m tiom rheirusual gravid (15.6'lc).The authorssuggest that this may home rangesreturned within a week (Sun 1990). representa significant decline in reproductivefie- Although thermoregulatorybiology hasplayed quencywith increasingbody size (and thus. per- a central role in the study of snakeecology. it has hapswith age)but statisticalanalysis does not sup- attracted little direct interest from Chirrese port this inf'erence(t = 1.60,df = I , P = 0.25).The researchers.However, they have noted that diel proportion of reproductive may vary in shiftsin ambush-siteselection (especially. the ten- responseto year-to-yearvariation in fbod supply; dencyto spendthe middleof theday on the ground certainly,f'emales are in higher body condition in rather than in the trees)may be driven by therrnal someyears than in others(Sun et al. 1993.2002). cues(e.g., Li 199,5).Also. the snakes' retreat to deep Studies on reproductive output show that burows for the winter is presumablyfbrced by the f'ernaleG. sheclooensl.rproduce a remarkablyheavy fact that the ground fieezesto depthsof up to I m litter relative to maternal mass and produce very (Sun 1990).Burrows used during winter typlcally largeofTspring (Sun et al. 2002).In both respects. haveleaf litter blockingthe entrance,thus providing they diff-ersubstantially tiom related taxa (includ- additionalinsulation against severely low air tern- ing the mainlandpopulation oI G. sheduoen.sis;Lt peratures(Sun 1990).Hibernating snakes typically pers.comm. 2000).The very high relativeclutch displaybody temperaturesbetween 2 and 5"C (Li et mass(0.80 vs. < 0.50 litter massas percentf'emale al. 1993).Thermal factors may alsoexplain why the postpartum body mass fbr most other pitvipers) snakesdo not commencefbraging until after the may reflect the fact that some componentsof the peak of the bird-migrationperiod in spring. and costs of reproduction(post-parturition rnortality?) ceaseforaging prior to the end of the bird-migration are low on Shedao.Because parturition occurs just periodin autumn(Shine et a|.2002b'). befbre the autumn bird rnigration. post-partum f'emalesf'ace little risk of dying fi"om starvation Reproductive Biology before they can obtain fbod (Sun et al. 2002). The Reproductionby Shedaopitvipers has attracred largeoffspring size on Shedao(14 vs.< 7 g in other substantialstudy over a long period of time. Glot'dius) plausibly ref-lectsthe scarcity of small Seasonalcycles basedon sizes and histological prey on the island.Neonatal G. shetluoensi.lthat are examinationof the testesand ovarieswere reported too smallto ingestpasserines must feed on inverte- by Yang (1983).who int'enedfrom thesedata that brates, thus enforcing strong selection for larger most mattng occurred from August to October. sizeat birth (Sunet al. 2002). Testesare largestduring midsummer(June-July: There are few published data on behavrors Yang 1983).Sperm are produced fiom April to July, associatedwith reproduction,because courtship. and testesand epididymesof adult malescontain male-male combat and copulation are rarely mature spermatozoatiom July-October.Ovulatron observedon the isiand(LS. pers.obs.). Copulation occursin June,with parturitionfrom lateAugust to can occur in both arborealand terrestriallocations mid-October(Sun et al. 1993.1994, 2002). Most (Li 1995),and may be relativelybrief (18-min birthsoccur during September (Sun et al. 1993). duration:Snake Island Survey Team 1974,l9l6). Shine et al.-Ecology of Gloydius shedaoensis 1

unpubl. data). Gape-limitation is important.with some birds being killed but then rejected becausethey are too large to swallow (e.g.. doves). Shedao pitvipers are able to swallow prey items that weigh as much asthe snake itself (Li 1995;Fig. 3). Juvenilesnakes take small birds.but alsofeed upon inver- tebrates.Of 12 prey items fiom juvenile snakes.seven were birds. f our were centipedes (.Otostigmuspolitu,s'), and one was an isopod (Meto1tonorthus pruinosus'.Snake Island Survey Team 19711).Researchers have seen pitvipers approachingthe nestsof seagulls(presumably to feed on chicks),but the snakes were attackedby the adult birds (LS,pers. obs.). Shedao pitvipers require 3-7 d (dependingon the size of the prey and weather condi- tions)1r.l fully digesttheir prey (Li et al. 1990),but they do not ceaseforaging during this peri- od. Some snakes in ambush poses contain fieshly-ingested birds. For example.one sample of adult snakes included ten snakeswith empty stomachs,59 snakeswith a single bird in each,nine snakeseach contain- ing two birds, and one with three birds (Snake Island SurveyTeam1974). Of l6juve- Figure 3. A Shedaopitviper. Cloydiu.s.shedaoettsis, swallowing a bird, nile snakes,six had empty stomachs,eight containedsin- gle prey, and two containedtwo prey items each Food Habits (bird plus centipede;centipede plus isopod: Snake Adult Shedaopitvipers feed almostexclusive- lsland SurveyTeam 1974).ln other studies.the pro- ly on birds. Of 8l prey items recordedin adult portion of snakescontaining prey in autumn aver- snakesby the SnakeIsland Survey Team (1974),80 agedabout 20Vctn adultsand 10c/cinjuveniles (Li were birds and the other was a rat (Rattus uon-egi- 1995;Li et al. 1990).Adult femalestypically con- cas).Analyses of stomachcontents have document- tain food more often than do adult males(26c/o vs. ed predation on 24 speciesof birds, all of thern 22Vctn Li et al. 1990).Statistical analysis of theraw passerinesexcept fbr two speciesof quail(Cotunti.r data usedfor theseconclusions reveals that the dif- cotunti.r, Turnix tu*i). Warblersand buntings are t'erencein proportionswith tbod betweenadults and probablythe most importantprey groups (Shine juvenilesis significant(f =9.03. d,f= l. p < 0.003) Herpetological Natural History, Yol. 9(l), 2002

rl$us

Figure 4. A Shedaopitviper, Glol-diusshedaoensis, in rypical terresrrialfbraging pose. whereasthat betweenmales and females is not (12- to 0.5-1 m) and also varies with the time of day 1.05,df = 1,P = 0.31).The lowerrate of f'eedingin (higher in the morning than the afternoon) (Li juvenile snakes may result from gape-limitation: 1995;no raw dataavailable). juvenile snakes are unable to ingest most bird Although most prey are undoubtedly taken speciesin the area(Li et al. 1990). fiom ambush sites, Shedaopitvipers will also eat deadbirds or thosetrapped in mist nets(Sun 1990). Foraging Behavior Thus, they can forage actively as well as ambush Snakescatch birds from ambush,and foraging their prey. Becausesmall snakesoften strike and snakesdisplay distinctivepostures and patternsof kill birds that are too large for them to swallow, an habitat selection.Although some birds are taken actively foraging snakemay well encountera dead from the ground, many are captured on arboreal bird on the ground.The invertebratestaken byjuve- perches.Snakes lie with the head facing outwards nile pitvipers are presumably taken at night by along a branch approximately I m above the active foraging; it is common to see small snakes ground; the forebody is formed into a concertina moving aboutat this time (RS,pers. obs.). shapeto permit a rapid strike when a bird alights in Some birds taken from arboreal perches are front of the pitviper (Fig. a). The incidenceof arbo- retainedafter the initial strike. whereasothers are reality changeswith the size of the snake:approxi- struckand released (RS, pers. obs.). In somecases, mately 907oofjuvenile snakesare found abovethe the snakefalls off its perch either at the time of the ground, whereasthis is true for only 637cof adults strike (as it throws its body forward) or later, as ir (no raw data available;Li 1995). This difl'erence struggleswith a bird that it has seized. In other may be partly attributableto the lower visibility of casesit retainsits hold on the branchand may swal- small snakeson the ground comparedto in a tree low the bird without leaving the tree. (Sunet a1.2001;Shine and Sun 2002).The height Snakesalso ambushbirds from terrestrialsites. above ground to which the snakesclimb to adopt Theseusually involve a tightly coiled posture,often their ambush posture also differs between age with the headt'acing towards an exposedopen area groups(adults typically climb to I - I .5 m, juveniles such as a rock. Commonly a snake will lie with Shine et al.-Ecology of Gloydius shedaoensis

only its head visible, and the rest of the body hid- tion (Zhao et al. 1990).Its slenderbranches do not den under leaf litter (Sun 1990).Surveys suggest provide suitable ambush sites fbr the snakes. that approximatelytwo-thirds of snakesuse arbore- Surveysshowed that snakeabundance was lower in al ratherthan terrestrialforaging sites(Snake lsland plots coveredby Pueraria than in control plots; and SurveyTeam 1974),but this estimatemay be sensi- that the removalof Puerctriaon theseplots was fol- tive to diff'erentialobservability of snakesin the lowed by a significant increasein snakenumbers two environments. (Zhao et al. 1990).This experimentinvolved three Studieson l7 captive snakeshave quantified plots,each 12 x 12 m2.One was coveredby dense the efliciency with which the snakescan turn bird tangledPueraria (typical of 27c of the island'ssur- biomassinto snakebiomass (Wu 1911a.b).These lace area);one by Pueriara growing over othertrees snakesranged in massfrom 53.5-188g prior to the (typicalof 10Vcofthe island'ssurface area); and one experiment.They ingested15.0-62.5 g of mice, was a control (Pueriara-free)plot. The first of these and gained 2.0-36.0 g in body mass.The mass sites contained few snakes (mean - 0.3 snakes gained as a proportion of mass ingestedaveraged recordedper day), whereasthe other two contained 33.47c, and ranged from 7.0-72.77c. Regression more animals(means of 5.3-6.0 snakes).Following analysis revealed no significant relationship removal of Pueraria in spring 1989 and replanting betweenassimilation efficiency (massgained/mass with natlve vegetation,the numbers of birds and ingested)and absolute body mass (n = 17,r = -0.13, snakesin the experimentalplot increasedsubstan- P = 0.61). tially (to a meanof 11.7snakes/day over a 7-d peri- od). Unfortunately, Pueraria is difTicult to kill CONSERVATION ISSUES becauseit is fast-growingand resistantto drought. The other feral organismof potential concern Research by Chinese scientists identified a is the brown rat (Rattus non'egicus); one of these number of potentialor actualthreats to the Shedao animalswas observedattacking a juvenile snakein pitviper population (reviewedby Huang 1989 and the laboratory (Tang 1990).More importantly,the Tang 1990).These can be classifiedinto two major rats' activitiesmay damageplants and soil cover on types: threats that involve human activities, and the island. However. rat numberson the island are "natural" processes. low (averagecapture rate < 5 rats per 100 trap- days:Li 1995),perhaps because the snakesreadily Etl'ectsof Human Activities feed on theserodents. Thus, rats may at times pro- Commercial exploitation. Prior to the com- vide a significantprey resource. mencementof research,the Shedaopitviper popu- Fire. Severalfires prior to 1980destroyed veg- lation was heavily exploited for commercial pur- etation over significant areas of the island (Tang poses(Tang 1990). The snakeswere killed ro make 1990). snakewine or snakepowder, or to feed to domestic pigs. Snake venom was used for medicine. Threats Due to Natural Processes Researchto documentthis threat involved a com- Researchhas identified a series of potential parisonof populationestimates from earlier work- sourcesof mortality which might reducethe rate of ersto assesssnake numbers through time. Although populationrecovery. the data were imprecise, they suggesteda strong Food and water supply. Experimentswith arri- decline from the 1930s (approximately 100,000 ficial hibernaculasuggested that > 407c of neonatal snakes:Koba 1933, 1938) to the 1950s(50,000 snakesdie during winter,possibly due to low energy snakes)and continuing through the 1970s(20,000 reserves prior to hibernation (Wu 1977a,b). snakes)to the early 1980s(10,000 snakes) (Tang Laboratoryexperiments show that neonatalpitvipers 1990).Regular mark-recapture studies (using short- can survive for very long periods without fbod, as term paint-marking) were instituted, to provide long as they have accessto water.In experimental more robustestimates of actualsnake densities. studies,seven neonates survived an averageof 148d Introduction of feral plants and animals. The (range = 30-392 d) under these conditions (Wu leguminousvine Pueraria lobata is the most impor- 1971a').Another eight neonatessurvived an average tant threatin this category.lt is a stranglingcreeper of 214 d (range 53-246 d) under similar circum- that eliminatesor overgrowsnative woody vegeta- stances(Wu 1977a).However, neonates kept with- l0 Herpetological Natural History, Y ol. 9(l), 2002

out water died more quickly (mean= 78.2 d, range since the early 1980s.For example.one of the 34 101d: Wu 1977a).Although there is no standing authorsof this paper (SL) spendsup to 200 d each water naturallyon the island,the snakesfrequently yearon theisland, and has been doing so since1982. drink dew on grass,or directly fiorn the artificial No snakesare removed fiorn the island. although poolsnow in place(Sun 1990).However, rainf'all is venomis sometimestaken lbr medicalresearch. rareduring the mainbird-migration periods in spring Faunal resourcescan also be conservedby andautumn (Fig. 2). markingthem valuablein economicor otherterms. Food may be limiting in somesituations. It is Venom fiom G. shedaoensi.sis usedto treat a wide commonto seerelatively emaciated snakes on the variety of medical conditions.including cerebral island(RS. pers. obs.). and the 4-yr delaybetween thrombosis,atrophic gastritis. tumors, and rheuma- successivelitters by a givenf'emale (see above) sug- tism (Tang 1990).A 100-bedhospital has been set geststhat replenishmentof energystores is a slow up in Dalian in associationwith the SnakeIsland process.Long-term observations suggest that the orgiinization. Tourism also offers resources. numbersof migratingpasserines have declined over Visitorsare brought to the islandduring appropriate the years(Tang 1990). Because this declineis like- tirnesof year.but areonly allowedto remainon the ly to reflect broadscaleenvironmental degradatron islandfor < 30 min and arerestricted to a small area overthe birds' summer or winterhabitats, any solu- nearthe boat-ramp.A smallfee fiom thesetourists tion mustinvolve a massivespatial scale. Ultimate- helpsto defraythe cost of rlainrainingthe f-acilities. ly, the populationdensity of pitviperson Shedao Unsurprisingly,the abundanceof G. .shedaoen- will probablydepend upon processes iit work over a srshas stimulated researchers to usethis speciesfor vastly greaterarea than the island itself. a variety of projects.For example.recent work has Landslides.A typhoonin August 1985caused measuredelectrocardic'rgrams in the laboratory(Xu l8 landslides.covering a total area of 4000 ml et al. 1987)and examinedthe distriburionof tr-ace (Tang 1990).Plants were destroyed,soil was lost. elementswithin the snake'sbody (Xu et al. 199l). and many snakeswere killed. Removal of feral plants and animals. There Predation. Birds of prey are frequently seen have been major atten.rptsto eliminate the intro- on the islandand have been recorded to eiit neona- ducedweed Ptteruriausing herbicides. direct cut- tal pitvipers(Koba 1938:Tang 1990). ting. andreplanting with nativevegetation (Zhao et Disease.Ninety-six of 225 snakesexamined al. 1990). Rodent-trappingprograrns have been on the islandexhibited inflammation of the mouth. introducedalso. Capture rates ranged from 3.8-5.8 presumablydue to injuriessustained during f'eeding ratsper 100trap-nights ovel'a 4-yr period. (Tang 1990).In sevelecases this may reducethe Fire. The control over visitor numbers(and the snake'sability to continuetaking prey. restrictionof thesepeople to a srnall area near the jetty) substantiallyreduces the risk of firesbeing lit MANAGEMENT INITIATIVES by humans.The long-term efTectsof this reduced flre frequencyremain unclear. The snakesselect rel- The researchon Shedaopitvipers has been atively open habitatsfbr ambush-sites(Shine and "hands-on" accompaniedby a seriesof manipula- Sun 2002),so thatan increasein ve-getationdensity tionsto addressthe problemslisted above. may ultimatelyreduce the amountof optimalhabi- tat. On the other hand, an intensefire at the wrong Effects of Human Activities time of year could cause significant rnortality of Commercial exploitation. The island of snakes.Thus, seasonaltiming of fires is important Shedaowas declareda Nature Reservein 1980. in terms of the efl'ecton snakepopulations. Protection was also afforded to a mountain (Laotieshan)on the rnainlandnearby that selvesas a Natural Sourcesof Mortality stopping-overpoint fbr migratingpasserines on their Food and water supply. 800 water-basins way to Shedao.The rnountain was protectedtcl were placedon the island during the 1980s,with ensure fbod supply fbr the island snakes.A two- wateradded or replacedevery l0 d duringdrought storysix-room house was constructedon the island conditions(Tang I 990). Theseare no longer used in 1986 to accommodate research tealns. afferthe 1988construction of fbur muchlarger con- Researchershave been based on the islandfulltinre cretebowls (2 m wide. 2 m deep)to provideaddi- Shine et al.-Ecology of Gloydius shedaoensis ll

Statisticalanalysis is rendereddifficult, however. becauseof the lack of control plots monitoredover the sametime span.ln anotherseries of manipula- o q) J tions, twigs on many of the trees in Shedaohave E 200 beenpruned such that very slenderbranches (strong o enoughto supportbirds but not snakes)have o been L removed. This procedure reduces o the number of I 150 available perching sites where the birds are saf'e E c fiom snakepredation. To addressthe high rate of neonatalmortality, a large (800 rn:; gardenwas built on the mainland. 1990 1991 1992 1993 1994 1996 1997 Neonatesfbund active on the island late in autumn were brought back to this enclosureto hibernate, andthen returned to theisland the fbllowing spring. Constructionof an artificial hibernaculumon the an o island allowed investigatorsto identify optimal J thermal,and hydric conditions E15 during winter, and o henceto mimic thesein the mainlandenclosure (Li g andDiao 1993;Li et al. 1993). o 10 Landslide. Areas aff-ectedby landslideshave .i beenreplanted, in an attemptto stabilizethe soil. s Predation. There has been no attemDtto con- trol birds of prey. Disease. Mouth inf'ectionshave been treated 1990 1991 1992 1993 1994 1996 1997 by capturingsnakes and applyingpotassium per- year manganateand gentianviolet.

Figure5. Overalltrends in abundanceand age structure Effectivenessof Conservation Initiatives of Shedaopitvipers, based on snakesrecorded during Periodic mark-recapturestudies, regularcensus periods. See Sun et al. (2001) fbr details using short- of surveymethods. Bars show one standarderror on term paint-marking,indicate that the populationof eitherside of themean. pitvipers on Shedaohas been steadily increasing since the area was protected.From approximately tional drinking sitesfor snakes.These pools also 9000 snakes in 1982, the population grew to enhance snake f'eeding rates by providing ideal approximately121,000 by 1989(Huang 1984,1990; ambushsites (Huang 1989).Beside one of these Sunet al. 1994).It is currentlyestimated at approx- tanks.a l0-m deepwell generatesa constantwater imately 18.000(Sun unpubl. data). supply.Pumps and hosesallow waterto be moved Changesin population size and age structure amongbowls. over the last decadeare also evident in data fiom In 1986 and 1987,ibod supply was supple- regularcensus activities that do not involve marking menteddirectly by bringingseveral hundred small the snakes.On most daysthroughout the springand birds (chicken,quail, etc.) from the mainlandand autumnbird-migration periods each year, scientists ofl'eringthem to the snakes.A lessdirect methodto walk the same-540-m path and count snakeswithin enhancefeeding rates was trialedin 1992,by tying a 3-m-wide transect(the path and l-m widths on earsof rice to branchesthat were in use as fbraging either side).The snake'ssex and size classare also sitesby snakes(Zheio et al. 1992).The rate of bird recorded.We haveanalyzed the raw datatiom these visitation and of snakeabundance and f'eedingrate countsfor the years1990-97, excluding 1995 (Sun was monitoredfiom 0100-0145 h over 3-day pen- et al. 2001). Over this period total numbersof ods befbre and afier this manipulation.Bird num- snakesaveraged 40.6 per survey(0.31 per m): thus. bers increasedtiom 60-125. snakenumbers liorn the dataset contains 37,980 records of sightingsof approximately17 87, and f-eedingrate per snake snakes.Analysis clearly shows that snakenumbers fiom approximately l0-20c/o (Zhao et al. 1992'). haveincreased through time. with a concurrentshifi 12 Herpetological Natural History, Vol. 9(1), 2002

in the proportion of juvenile to adult animals(Fig. 381-383. HerpetologicalSociety of Japan,Kyoro, 5). The shift in agestructure is characteristicofpop- Japan. ulations recovering from intense harvesting Huang, M. 1990. The presentstate of the Agkistrodon shedaoensispopulation. In: E. Zhao (ed.), From focussedon adult specimens(e.g., Caughley and Water Onto Land, pp. 271-272. China Forestry Sinclair1994; Webb 1995). Press,Beijing, China. In summary,the pitviper populationof Shedao Ji, D., S. Weng, and M. Liu. 1989. Classificationof not only has attractedintensive study over many Agkistrodonhall's in northeastChina. In: M. Matsui, years,but alsohas been a focus tbr the development T. Hikida. and R.C. Goris (eds.), Current Herpetology in East Asia, pp. 185-l 92. and application of conservationinitiatives. Those HerpetologicalSociety of Japan,Kyoto, Japan. programs have been successful,and the Shedao Jiang, Y and E. Zhao. 1980. Ecological data of snake- studies may have much to tell western science island pit-viper and Pallas' pirviper (in Chinese, about innovative approachesto issues of snake English summary). Acta Herpetologica Sinica, biology and conservation. 5efles I ):l-5. Koba, K. 1933.Strange story of SnakeIsland with a hun- dred thousand venomous snakes. Scientific ACKNOWLEDGMENTS Knowledge l3:755-781. Koba. K. 1938. Some notes on Agkistrodon ftalys from We thank JohnWeigel for alerling Shineto the Syoryuzan Island, Kwantung, South Manchuria. existenceof Shedao;our wives and families for tol- Zoological Magazine,Tokyo 50:245-26.1. Li, J. 1993.On the origin of SnakeIsland (in Chinese). eratingour absenceson fieldwork on the island; M. ChineseNature 2:37-38. Kearney photographs; for and the Australian Li, J.-L. 1995.China SnakeIsland. Liaoning Scienceand ResearchCouncil for fundins our studies. TechnologyPress, Dalian, China. Li, J. and Y. Diao. 1993. A preliminary study on the hibernational temperature and moisture LITERATURE CITED of Agkistrodonsaratilis shedaoensis(in Chinese,with English Abstract). Acta Herpetologica Sinica Caughley,G. andA.R.E. Sinclair. 1991. Wildlife Ecologv 12:I l0-114. and Managemenr.Blackwell ScientificPublica- Li, J., Y. Luan, L. Sun, D. Zhao. and Y. Diao. 1990. tions,Boston, Massachusetts, USA. Studieson someproblems of Agkistrodonshedaoen- Chen,Y., X. Wu, andE. Zhao.1984. Classificarion of sls populationdue to seasonalchanges (in Chinese). Agkistrodonspecies in China.Toxicon 22:53-61. ln: E. Zhao (ed.), From Water Onto Land, pp. Chen,Y, D. Zhang,K. Jiang,and Z. Wang. 1992. 273-276. China ForestryPress, Beijing, China. Evaluationof snakevenoms among Agkistrodon Li, J., D. Yang,and L. Sun. 1993.Studies on the ecology speciesin China.Asiatic Herpetological Research of Agkistodon shedaoensisduring hibernation.In: 4:58-61. E. Zhao, B. Chen, and T.J. Papenfuss(eds.), Fitch,H.S. 1999. A KansasSnake Cornmunity.: Composi- Proceedings of the First Asian Herpetological tion and Changes Over 50 Years. Krieger Meeting, pp. 346. China Forestry Press, Beijing, Publishing,Malabar. Florida, USA. China. Fukada,H. 1992.Snake Life History in K,toto. lmpacl Mori, T. 1932.Report of Agkistrodon haly-sintemtedius ShuppankaiCo., Tokyo, Japan. on a small island near Port Arthur. Natural History Cloyd, H.K. and R. Conant.1990. Snakes of the of Korea T3:24-25. AgkistrodonComplex. A MonographicRevietv.. Murphy, R., E. Zhao, D.J. Moratka, and S. Li. 1993. Contributionsto HerpetologyNo. 6. Societyfor the Phylogeneticrelationships of representativespecres Study of Amphibiansand ,Ithaca, New of the genusAgkistrodon and relatedpit vipers. In: York,USA. E. Zhao, B. Chen, and T.J. Papenfuss(eds.), Hasegawa,S. 1932.An islandinhabited only by ven- Proceedings of the First Asian Herpetological omoussnakes. Amoeba 4:30-38. Meeting, p. 353. China Foresrry Press, Beijing. Huang,M. 1979.Surveys of SnakeIsland. Journal of China. Knowledgel:ll4-121. People'sPress of Liaoning Parkinson,C.L., S.M. Moody, and J.E.Ahlquist. 1997. Province.China. Phylogeneticrelationships of the' Agkistrutdon com- Huang,M. 1984.An estimateof the populationof plex' based on mitochondrial DNA sequencedata. Agkistrodonshedaoensis on ShedaoIsland (in Symposia of the Zoological Society of London Chinese,with English Abstract). Acta Herpetologica 70:63-18. Sinica3: l7-22. Seigel,R.A. and J.T. Collins. 7993.Snakes. EcoLog-v and Huang,M. 1989.Studies on Agkistrodonshedaoensrs Behcuior.McGraw-Hill, New York, USA. ecology.In: M. Matsui,T. Hikida,and R.C. Gons Shan,2., D. Ji, andX. Mo. 1993.Analysis of the organi- (eds.), CLtrrentHerpetology in East Asia, pp. zationof genomicDNA of Agtistrodon speciesfiom Shine et al.-Ecology of Gloydius shedaoensis 13

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