ANDUNCERTAINTIES REGARDING TRENDSIN IRONIES, MISCONCEPTIONS, BEARPOPULATIONS INVITED PAPER MinnesotaDepartmentof NaturalResources, 1201 East Highway2, GrandRapids,MN55744, USA,email: DAVIDL.GARSHELIS, [email protected] Abstract: Despite our rapidly increasingknowledge of bears, there are few places in the world where we really know how bear populationsare faring. I arguethat bear conservationwould benefit by highlightingratherthanhiding this uncertainty.Assessments of bearpopulationsoften are based on recordsof dead animalsandtrendsin habitatavailability.These dataproducedubiousindicationsof populationtrend. Case studiesrelating to the tradein bearparts,sportharvests,and nuisancekills indicatethatrecordsof human-killedbearsmay not be accurateand may not necessarily reflect changes in populationsize. Increasingbear populationsmay continue to rise with increasedlevels of humanexploitation(as long as it is below the maximumsustainabletake), whereasdeclining populationsmay continueto plummetdespite reducedexploitation. Similarly,whereas loss of habitat(forest area)probablyengendersa decline (of unknownmagnitude)in bearpopulations,unchangingor increasingforestedareamay not necessarilyresultin stableor increasingbearnumbers. Ironically,bearpopulationsthathave been managedfor sustainedharvestshave generally fared betterthan populationsin which huntinghas been prohibited,mainly because the formerbettercontrols illicit huntingthan the latter. Longtermconservationof bearsrequiresbetterinformationon populationtrends,butbettertechniquesareunlikelyto be developed if faults andinadequacies of currentdata are not clearly recognized. Ursus 13:321-334 (2002) Keywords: Asia, bears,conservation,habitatloss, harvest,NorthAmerica,poaching,populationsize, populationtrend,tradein bearparts, uncertainty In most human societies, knowledge empowers, whereas uncertainty signifies fallibility, timidity, and weakness. Scientistsarepresumedto be knowledgeable, andthusable to produceaccuratefacts, explanations,and predictions;those thatdo so with certaintytendto be held in high esteem by the public. The soothsayersof the past were probablywrong more often than are modem forecastersof environmentalandastronomicalevents,buteven today's complicatedcomputermodels are prone to error because we lack a full understandingof most naturalsystems. A majorconcern in today's world is the threatof species extinctions due to the activities of humans. Thereis a strongrelationshipbetween humanpopulationsize and threat of extinction of native fauna (McKinney 2001). Although we recognize the basic causes of extinction (Diamond 1989) and we have been able to identify taxa, ecosystems, and geographicareas that are most susceptible to extinctions(Cole et al. 1994, Mace andBalmford 2000), ecologists and conservationbiologists have been strugglingto understandhow to relieve species from extinctionthreats.Seeminglybasicquestions,suchas "What is the minimumviable populationsize and what level of human exploitation is sustainable? What habitatsdoes the species require and how much area should be protected within reserves?"are routinely debated, because empiricaldataare lacking. Unfortunately,the science of ecology is by natureinexact and laden with uncertainty. Shrader-Frechette andMcCoy (1993:123-124) contend that due to the inherentcomplexity of ecology, there are few governing principles, so case studies are the best means for achieving understanding.The methodof case studiesinvolves scrutinizingthe detailsof particularsituations in an attemptto "makesense" of them. Accumulating and comparingresultsfrom a series of relatedcase studies advancesthe science. For large mammals such as bears, experimentationis rarelyemployed as a partof the case study. Instead,bear biologists tend to reachconclusions based on patternsin the data, logic, insight, and knowledge of other studies. Case studies generallyenterthe body of science through a process of peer-review,althoughmuch informationis containedin less formalreportsand even raw data. At periodicjuncturesit is worthwhileto review the basis of conclusions and direction of thinking. In experimentalsciences,predictionsthatarenotupheldempirically areultimatelydiscarded. In sciences based on case studies, apparentanomaliesmay representtrulyuniquesituations, making it difficult to tease out erroneous information. Nevertheless, occasional re-examinations may prove to be fruitful- if not to correctthe past, to guide the future- especially in termsof species conservation. In this paperI drawattentionto severalmisconceptions relatedto the monitoringand conservationof bearpopulations. I rely heavily on case studies to illustrate my points. These are used mainly as counter-examplesto prevailingviews or to exemplify common problems. A principalpurposeof this critiqueis to highlight the uncertainty,andhence fallibility,of our understandingof bearpopulations.Therearefew places in the worldwhere biologists would admit to not knowing whether a bear populationwas increasing,decreasing,or stable, yet the realityis thattherearefew placeswherewe reallydo know 322 Ursus 13:2002 for surehow bearsare faring. Seemingly contraryto my openingremarks,I believe thatultimatelywe, as bearbiologists benefit - because bears benefit - by critically examining the basis of our knowledge and admittingto our foibles anduncertainties. MISCONCEPTIONS REGARDING TREND POPULATION TrendAscertainedfromNumbersof Dead Bears In a populationof unknown size, a large death toll is obviously unnerving. Because most bearpopulationsare of unknownsize, a recordof increasingknown deathsis often taken as primafacie evidence of a populationdecline. Moreover,even poor recordswith no clear trend but occasionaldocumentationof a surgeof deathsmay be cause to fear a populationdecline. Recordsof bearparts(principallygall bladders)traded amongAsian countriesare a salient example of tallies of deadbearsbeing used to interpretpopulationtrends. Several good investigative reports exposed the broad geographicscopeof thistrade(Mills andServheen1991;Mills 1995; Mills et al. 1995, 1997), althoughit was not possible to accuratelyquantifyit. Some evidence suggested increases or decreases in bear kills in certain countries, based on documentedor estimatednumbersof exported or importedparts.However,populationtrendassessments based on trendsin the tradein bearparts,andhence numbers of bearskilled, have been inconsistent. Considerthe cases of 3 countriesthat have been heavily involved in this trade. China.-In China,the killing of bears(otherthangiant pandas[Ailuropodamelanoleuca])for theirpartswas legal until 1989. In the decade preceding this restriction (1979-88), several thousandbear gall bladderswere exportedfromChinato Japan(Servheen1990). Additional, but smaller numbersof gall bladderswere exported to South Korea (Mills et al. 1995). However, trends and quantitiesof bearskilled for the tradein gall bladdersare nearlyimpossible to discernfrombile exportdata,due to manyconfoundingissues, includingtradein fake bearbile (gall from animals other than bears that are claimed as bears) and farmed bile (bile drainedfrom live, captive bears)(Box 1). Farmingbears for their bile began in China in 1984. During 1985-89 hundredsor thousandsof bearswere removed from the wild to stock captive populations(Fan and Song 1997). However, since 1989, all of the species of bears in China (brown [Ursus arctos], Asiatic black [U. thibetanus],andsun[Helarctosmalayanus])havebeen protected,inasmuchas killing or capturingis illegal with- out a special permit,and selling of partsof wild bearsis also prohibited(Mills and Servheen 1991, Fan and Song 1997). Has this supposedchangein exploitationof bears enabledbearpopulationsto increase? The answeris unclear. Santiapillaiand Santiapillai(1997:23) indicated that China,bearpopulationsarein decline."They "throughout cite an estimate of 15,000-20,000 Asiatic black bears in China, which matches the range reportedby Ma and Li (1999), based on "1994 statistics". Ma andLi (1999) believed that over-huntingfor bear parts was causing this species to decline, althoughtheir chief evidence for recentdeclineswerediminishingnumbersof purchasedbear skins during1986-1991. Cheng (1999:123), referringto these same data, concludedthat "In recent years, ... the numberof bears [bothblack andbrown,in one province] has droppedsignificantly..." Li et al. (1996; citing Ma et al. [1994]),presentedhigherpopulationestimates(20,00032,000 Asiatic black bears and 12,000-14,000 brown bears), but also suggested that populationswere shrinking. Fan and Song (1997:11) called these estimates "an emotional guess" and presentedtheir own estimates of 46,500 Asiatic black bears, 14,800 brownbears,and400 sun bears,based on field surveys and interviewswith local people. They claimed thatafterbears were protected in 1989,populationsincreased.Ma et al. (2001) conducted a more recent survey, also based on field sign and local interviews,and concludedthat Asiatic black bearsnumbered <20,000 and were still declining numericallyand geographically. Differences in these opinions appearto be just that- beliefs lacking much factualbasis. Russia.-Exportation of bear gall bladdersincreased dramaticallyin Russia in the early 1990s for variouspolitical and economic reasons (Chestin 1998). Chestin (1998) believed that because of increasedeconomic incentives, legal harvestsof brownbears,generallytotaling 4,000-4,500 nationwide,mighthave been matchedby an equalnumberof illegally taken(poached)bears. Imports of bile to South Korea from Russia showed a sharpincrease in the 1990s, but still representeda small number of bears killed/year(Box 1). Priorto this rise in poaching, the total numberof Russianbrown bears appearsto have increased,from an estimatedpopulationof 80,000 in 1981 to 125,000 in 1990, and the geographic range expandedconcomitantly(Chestin1999). Annualsustainable harvestquotas were establishedso as not to exceed 10% of the population,but in reality appearedto be far below that. Thus,even if poachingwas as high as posited by Chestin(1998), the overallrateof humanexploitation may have been sustainable.Most killing for gall bladders has occurredin the RussianFarEast (Kamchatka),where some reports suggested an annual take of 1,500-2,000 brownbears,possibly 20% of the population(Nikolaeno UNCERTAINTIES INPOPULATION TRENDS* Garshelis 323 Box 1. Records of bile imports or exports have been used to estimate the number of bears killed to support that trade. Tabulatedbelowarethe supposed numbersof bears killed/yearto accountfor importsof bearbile recordedby the Korean CustomsAdministration (Mills1995,Millset al. 1995)for 4 countriesof origindiscussed in the text. Although these numbersseem to indicate clear trends in bears killed over time, the data are too confoundedto drawsuch conclusions. Severalmajordifficultiesexist in convertingbile to bears. Variationin Gall BladderMass.-The amountof bile in gall bladdersvaries by species, geographic area, and time of year, so any conversionof bile mass to dead bear equivalentsis subjectto appreciableerror. Values tabulated are based on 30 grams/whole,driedbear gall bladder (Lay 2001). Mills (1995) suggestedan averageof 60 grams/gallbladder,but did not presentsupportingdocumentation. Furtheruncertaintyinvolves whetherthe Korean customs records relate to grams of bile, grams of whole gall bladders,or a combinationof both. Changes in Regulations,Enforcement,and Recording ofImports.-Mills (1995) andMills et al. (1995) reported Korean bile import data by decade, covering 24 years, 1970-93. The Republicof Koreajoined the Convention on InternationalTrade in EndangeredSpecies of Wild Faunaand Flora (CITES) in July 1993, and in 1996 acceptedthe AppendixII listing of bearswhose populations were not consideredthreatened;this listingrequiresdocumentationto ensure legal import. Korea also concomi- tantly improved surveillance and enforcement. These actions resulted in better recordingof bear imports and more seizures, so the total amountof bile rose by nearly an orderof magnitudefromthe 1990-93 periodshown in the table to 1994-99 (Mills et al. 1997, Yoon 1997, Sohn 2001). CounterfeitBile.-Several investigativereports(Lauet al. 1994, Changet al. 1995, Gaski 1997) indicatedthat a very high proportionof the presumedbear gall bladders on the Asian market (94-98%) are from animals other than bears. This would severely inflate the estimate of dead bearsbased on bile imports. Tradein non-beargall bladderslikely explains the unreasonablylarge quantity of bile from Indonesiaand Japanin the 1970s. It would be impossible to remove >7,000 bears annually for 10 yearsfroma Japanesepopulationof 10,000-15,000 black bears(Hazumi1999) and2,000-3,000 brownbears(Moll 2001). Moreover,Japanalso has an internalmarketfor bear bile, and exports to countriesother than South Korea, so the amountof bile obtainedin Japanis far more thanindicatedon Koreancustoms records. Farmed Bile.-Bile obtained from catheterized,captive (farmed)bearsprobablyexplains the sharpincrease in imports from China in the 1990s. Lau et al. (1994) indicatedthat virtuallyall the bile importedfrom China (into Hong Kong) in the early 1990s was from captive bears, not dead bears. The Korean import data do not discriminatebetween powdered bile (most likely from farmedbears)andwhole gall bladders(deadanimals,most of which are not bears). 1993, cited in Chestin 1999). In this area it is assumed thatnumbersdeclined,althoughpopulationestimatesfrom aerialsurveysshowedan equivocaltrend(Revenko1998). Commercially-motivatedpoaching of Asiatic black bearsin the RussianFarEast (the only areaof Russia inhabitedby this species) also has increased,but estimates of populationsize andpresumedratesof declinehavebeen highly variable and contradictory(Yudin 1993). Moreover,referencesto populationdeclinesin this species generally referto the distantpast. Chestinand Yudin(1999) suggested that Russian Asiatic black bears numbered 25,000-35,000 at the beginningof the 1800s, only 6,0008,000 in 1970, and4,000-5,000 by 1985, which is thought to be about the same remainingat present. Until 1983, Russianslegally harvested300-400 Asiatic black bears/ year. Since then,blackbearhuntinghas been illegal. It is uncertainwhetherthe previous legal harvestof 300-400 was sustainable(it would seem so if the populationwas 4,000-5,000), and if so, whetherillegal harvestsnow ex- ceed that. Sustainabilityof the harvestrelatesonly to the numberof bearskilled, not whetherthey were legally or illegally taken. Of course the formeris more readily adjusted to remainsustainable,but the lateris not by definition unsustainable. Japan.-Japan is an importerandexporterof bearbile, as well as a user of productsobtainedfrom native bears. Both import and export of bile appearedto decline dramatically from the 1970s to the early 1990s (Mills et al. 1995), althoughthese data are difficult to interpret(Box 1). Harvestingof brownbears (on Hokkaido)and black bears(on Honshu)is legal, but ratherloosely regulatedin partbecausetherehas been a long-term,purposefuleffort to reduce numbersof bears. Hunterscan legally sell all partsof bearsthey harvest,and thereare no governmentimposed restrictionson the numberthey can take during the huntingseason. It is believed thatthe opportunityto sell bearpartsis largely what sustainsinterestin hunting (Moll 2001). Calculatednumberof bearskilled/year Countryof origin 1970s 1980s China Russia Japan Indonesia 3 0 7100 690 3 0 26 3 1990s 490 15 7 0 324 Ursus 13:2002 Some hunting restrictions were imposed during the 1980s and 1990s (e.g., eliminationof the brownbearseason during spring when hunterscould snow-trackbears to or from their dens) (Mano 1998, Moll 2001); this reduced the kill, but not in all areas(Kaji and Mano 1996). Mano and Moll (1999:129) thoughtthatbrownbearharvests still exceededsustainablelimitsin some places, such as the Oshimapeninsula,threateningthe "long-termpersistence of that subpopulation."In anotherreport,however, Mano (1998:179) indicatedthatthe Oshimabrown bearpopulation"persistsin high numbers,"but suggested that bears in more lightly hunted areas were declining. Aoi (1991:135) described the overall Hokkaido brown bear population as "declining rapidly," whereas Kaji (1992:413) thought that "Furtherstudies are needed to analyze the populationtrend..." It seems clear from the conflicting reportsthatKaji's call for more study is warranted. Approximately2,000 Asiatic black bears have been taken annuallyon Honshu, half by huntingand half explicitly for pest control(Hazumi1994). Based on density estimatesproducedfrom springtimesnow-tracking,capture-recapture,and habitatassessmentacross the island, the total populationsize has been estimated at 10,00015,000. The veracityof this estimateis difficultto assess, and even if it is assumedto be accurate,the span is wide enoughto precludejudgmentas to whetherpresentlevels of exploitationare sustainable. Hazumi(1999:209) consideredJapaneseblack bears to be "facing a crisis," due to the combinedeffects of habitatdegradationanduncontrolledharvesting,but he had no real evidence of a populationdecline. Some prefecturalgovernmentstudieshave attemptedto assess local populationtrends,but flaws in theirmethodologyunderminedthe credibilityof theirresults (Huygens and Hayashi2001). Generalities.-The 3 countrieshighlightedabove were selected not because they exemplified situationswith inadequatedata on bear populationtrends, but ratherbecause, comparedto otherAsian countriesimpactedby the gall bladdertrade, they had considerablymore data on their bear populations. Additionally,unlike most of the other Asian countries, some records of the gall bladder tradeexist for these 3, and each of the 3 exhibitedan apparenttemporaltrendin the volume of this trade(Box 1). Despitethese data,bearpopulationtrendsin these 3 countriesareequivocal,even controversial.The statusof bears in otherAsian countriesis even more uncertain. I am not suggesting that the gall bladdertrade is not cause for grave concern- certainlyit is. But this concern should arise from the uncertainty,not the certainty, of the impacts. We cannotdiscountthe possibility thatin many areas,the exploitationof bearsfor partsis sustain- able. That is, we cannotreject the null hypothesisof no detrimentaleffect. However,employingstatisticalterminology, we have insufficientpower (due to a paucity of data)to rejectthishypothesis.Normally,we areconcerned mainly with type-I errors: we attemptto avoid erroneously rejectinga truenull hypothesis. However,in cases involving harm,to people or the environment,it may be ethicallymoreresponsibleto erron the side of cautionby trying to avert effects that may be nonexistent(i.e., putting moreefforttowardavoidingtype-IIerrors;Mapstone 1995). Shrader-Frechetteand McCoy (1993:153) put it this way: "incases of uncertainty[my emphasis],ecologists ought to adopt an ethical (ratherthan purely scientific) account of ecological rationality." Thus, for rare species, the burdenof proof should switch from proving that a populationdecline has occurred,to proving that it has not (Taylorand Gerrodette1993). A problemwith emphasizingthe avoidanceof type-II errorsin cases of potentialharm,especially irreversible harmsuch as extirpation,is losing trackof the underlying uncertainty. It can become all too easy, once accepting thata detrimentaleffect may exist, to begin to prophesize the magnitudeof the effect. Withoutreal data, this can become a game of emotionalguesstimation.In cases such as the gall bladdertrade, where to most Westernersthe practice is culturallyalien and repugnant,claims of effects often become exaggerated, especially if they are thoughtto help instigateremedialaction. Hence, assertions of Asianbearpopulationsbeing "devastated,""decimated",or "depleted"(Knights 1996) tend to be widely accepted, or at least not questioned. It is doubtfulthat such unsubstantiatedclaims servethe best interestof bear conservation. I believe they do not, mainly because they falsely reflectthe certaintyof ourknowledge. Hence,they create more opportunityfor furthermisinformation,especially relatedto populationlevel effects of highly visible mortality. Increasesor decreasesin levels of humanexploitation may not necessarilyresult in attendantchanges in population size. An increasing populationmay continue to increasein the face of heightenedexploitation,whereasa declining populationmay continue to plummet despite reducedexploitation. The discovery of a massive shipment of gall bladders or a large numberof dead bears should not, in itself, be construedto representa population decline, and neither should the absence of these be cause for complacency. The examplesso farconcernedAsian bearsandthe gall bladdertrade. Becausethis exploitationis largelyunregulated,it is presumedto be unsustainable.In contrast,recreational (sport) harvests are overseen by management agencies whose responsibilityis to ensure that they are IN POPULATION TRENDS * Garshelis UNCERTAINTIES sustainable. Nevertheless,unusuallylarge sportharvests often raise concerns, if not by the managementagency, by others interestedin bears. I offer 2 examples dealing with Americanblack bears (U. americanus). Tennessee.-The legal harvest of black bears in Tennessee in 1997 was at least twice that of previous years, due to a naturalfood failurethatpromptedmany bearsto leave the sanctuaryof the Great Smoky MountainsNational Park. Pelton (1998:26) reportedthatin reactionto this high harvest,some biologists, bearadvocacygroups, and alarmistsin the generalpublicclaimedthatthe popuand"drivento extirpation." lationwas being"slaughtered" Long-termresearch(Pelton and van Manen 1996), however, showed thatthe populationhad been increasingfor manyyearsandcontinuedto increaseafterwards.Unfortunately,the body count was obvious, whereas the biological data either were not appreciated or did not constituteas appealinga story. Minnesota.-Hunting of black bearsin Minnesotahas, since 1982, been regulatedby restrictions(quotas)on the numbersof licenses available. This system was implementedto reducethe rateof harveston whatwas thought to be a decliningpopulation. Aftera few yearsof sharply curtailedharvests,therewas ampleevidencethatthepopulation was growing. However,a food failurein 1985 disrupted normal feeding activities, which resulted in an unusuallylargenumberof bearsbeing killed as nuisances. This large killing attractedconsiderableattentionby the news media. Moreover,one bearbiologist, who hadbeen monitoring a few radiocollaredbears at the time, suggested, in a memo to the managementagency, that the food failurecaused "severemalnutrition,"possibly leading to reducedreproductionand starvationof cubs. He also warnedthat2 age classes of young bearsmight have been "virtuallyeliminated,"thus compoundingthe high kill (L. Rogers, 1986, unpublishedreport). Based on this report,an environmentalgroupconcludedthat "it would be surprisingif the black bearpopulationhas not already been nearlyeliminated..." (SierraClub,NorthStarChapter, Minneapolis,Minnesota, 1986, unpublishedreport). Hindsight showed these forecasts to be wrong. Collections of bearteethfrom subsequentharvests,used for age determination,showedno indicationof weakcohorts.Furthermore,population modeling interfacedwith 2 statewide, mark-recapture populationestimates(Garshelisand Visser 1997) indicatedthat the populationgrew steadily at -5% annually (D. Garshelis,unpublisheddata). Fifteen years after the 1985 "high kill" the populationhad tripled, and despite steadily increasing harvests, the agency's goal of stabilizingpopulationsize had not been achieved. As in the otherexamplesabove,these datademonstratethat population trend cannot reliably be ascertainedfrom numbersof dead bears. 325 TrendAscertainedfromAreaof Habitat It seems almost tautologicalthat bear populationsdecline as a resultof habitatloss. However,the explanation for this relationshipis not as simple as it may at first appear. If humansdid not exploit bears, bear populations would likely exist at or nearthe carryingcapacity(K) of the habitatover the long-term. Any loss of habitatin this case would diminishK, eventuallyresultingin a population decline from increasednaturalmortality,diminished reproduction,or both. In the moder world, however, very few bearpopulationsexist at K. Conceivablythen, habitatloss would not necessarily cause a populationto decline. As an example: if, due to humanexploitation,a bear populationexisted at 1/3 K, and the area of habitat was reduced by 1/3, this reduced area could still easily supportthe existing population, which - other things being equal - would now be at 1/2 K (Fig. 1). This seeming paradoxis resolved by consideringfurther ramificationsof the loss of habitat. If the level of human exploitationremainedconstant,the above situation might indeed occur;habitatcould be lost withoutaffecting bear numbersuntil the point that the remaining population,confined to a smaller area, exceeded K. In reality though, bear mortalitywould likely increase inside the smaller patch of habitatbecause of heightened human exploitation (Fig. 1). Exploitationlevels would tendto increasefor severalreasons. (1) The reducedarea would increasethe proportionof bearsliving at the edge, andthese edge animalswouldbe morevulnerableto hunters and also more likely to wander into adjoining crop fields and be killed as pests. This explanationseemed to account for dramatic declines in orangutans (Pongo pygmaeus) following logging (van Schaik et al. 2001). (2) The diminishedsize of the patchwould makethe interior areamore accessible to huntersthat kill bears either intentionallyor inadvertentlywhen seeking otherspecies (e.g., by snaring);in essence,thereducedareawouldlessen the chance for some part of the region to function as a bear sanctuary. (3) Because bears are known to travel widely,especiallyduringyearsof naturalfood failure,they would be more likely to leave the bounds of the smaller patch of habitatand thus be exposed to greaterhuman contact. Recent studies have shown that althoughprotectedareas(e.g., nationalparks)arereasonablyeffective in maintaininghabitat(vegetation)for animals(Bruneret al. 2001), the persistenceof wide-ranginganimals(including bears),arestronglyrelatedto edge effects (Woodroffe and Ginsberg 1998, Revilla et al. 2001) and surrounding humandensity(Woodroffe2000). Among the carnivores, it is ironicthatthemoreopportunistic-natured bears,which can often adaptto alteredhabitats,are thusmoreproneto encounteringhumansand associatedrisks of mortality. Therearealso many additionalsynergisticinteractions 326 Ursus 13:2002 A. B. - Fig. 1. Hypothetical representation of the effects of habitat loss on bears. In panel A, 10 bears, whose home ranges are indicated by convex polygons, are below carrying capacity because of human exploitation. In panel B, these same 10 bears are forced into a smaller patch of habitat, the fringes of which have been converted to agriculture. This remaining patch of habitat might still suffice to support the 10 bears. However, the smaller size and more irregular shape of the patch makes bears more vulnerable to human exploitation because bears at the edge may be more prone to venture out into the agricultural fields, and people can more easily reach once-secluded areas in the middle. between habitatloss and other factors that might impact bearpopulations.Smallpatchesof habitataremoreprone to catastrophicfires or food failures(Cochrane2001) and have less capacity to regeneratefruit-bearingplants because frugivorousseed-dispersersare less likely to visit there (Cordeiro and Howe 2001). Shrinking, isolated patchesof habitatalso may be less likely to attractimmigrantbears, so whereas local overharvestin contiguous habitatcan be overcome throughsource-sink dynamics (what Brown and Kodric-Brown[1977] called the "rescue effect"), small, insular patches of habitatare more prone to extirpation(Peres 2001). Finally, and perhaps most importantly,decreased habitatlimits the potential for a populationto increase;even if habitatloss does not directly cause a populationdecline, it may preclude recovery. For these reasons, habitatloss should be foretellingof reducedbearnumbersandpopulationviability. However, the actual relationshipbetween habitatloss and population decline is far from clear. Moreover,sustainedor increasedhabitatis not necessarilyindicativeof a stableor increasingbear population. These points are illustrated by examples from Asia. Giant Pandas in China.-Two range-wide surveys of giant pandashave been conducted(and a thirdis nearly completed). These surveys accomplished 2 things: (1) they estimatedpandanumbers,and (2) they estimatedthe areaof remaininghabitat. In the first survey,conducted during the mid-1970s, some 3,000 people scoured the panda's range, recordingpanda sightings and scats. A "rough"populationestimateof 1,050-1,100 was obtained (Schaller et al. 1985:15-16). This narrowrange belies the inherentinaccuraciesof the method employed and variabilityamongsurveyparticipants(Schaller 1993). A decade later,a smallerteam of 35 biologists repeatedthe surveyusing morerigoroussamplingproceduresto measure density of sign, including both scats and bedsites. The resulting estimate of about 900-1,400 pandas provided no indicationof populationchange. A majorfinding from these surveys, though, was that pandahabitatwas being lost at a rapidrate. Largetracts of agriculturalland bisected the range into small, fragmentedpopulations. Moreover,low elevation areasthat once likely providedoptimalhabitatwere no longeravailable to pandas(Reid andGong 1999). In response,many more protectedareashave been established(total>30) to preventfurtherloss of habitat. However, it has become increasinglyclear thatthis alone is insufficientto ensure viability of panda populationsbecause these protected areas are small and disconnectedby expanses of unsuitable habitat (Loucks et al. 2001); furthermore,habitat quality,even within some of the protectedareas,is deteriorating.A case in point is WolongNatureReserve,one of the originalandpresentlylargestof the NatureReserves establishedexplicitlyfortheprotectionof pandas.Wolong is also an InternationalBiosphereReserve and the site of botha pandabreedingfacility andthe firstintensivestudy of radiocollaredpandas(Schalleret al. 1985). In 1975, the size of this reservewas expanded10-fold (to 200,000 ha) to improve protectionof pandahabitat. Since then, the humanpopulationwithin the reserve (mainly minority ethnic groups, who are exempt from China's restric- UNCERTAINTIES INPOPULATION TRENDS* Garshelis tions on family size) has grown by nearly 70% and the numberof households has more than doubled (Liu et al. 1999). Numberof householdsis significantbecause it is related to timberand fuelwood consumption,which has increased dramatically(An et al. 2001). Accordingly, suitabilityof the habitatfor pandasin Wolonghas steadily diminished(Liu et al. 2001a). Thereis some debateas to whetherWolong is atypical (Baragona2001, Brooks et al. 2001) orjust the worst-caseof a growingproblem(Liu et al. 2001b), but either way it exemplifies the point that habitatqualitycan deterioratefromthe bear'sperspective while outwardlyseeming intactfromthe humanperspective. A good deal of effort is presently being expended to map as well as assess remainingpandahabitatusing sophisticatedproceduresfor estimatingdensityof theirstaple food, bamboo, from satellite imagery (Lindermanet al. 2000, Loucks and Wang 2002). This is a promisingapproach,althoughthe knowledgeto define suitablehabitat for this species is still lacking(e.g., species anddensityof bamboo, overstorytrees, den trees, hill slope; Reid and Hu 1991, Reid and Gong 1999). Thus, quantifying changesin densityof bamboo,althoughbetterthansimple habitatmapping,might still not accuratelydepictpopulation trend(Reid 1994). Sun and SlothBears in SouthernAsia.-During 199496, J.L.D. Smith and I attemptedto initiate a field study of sun bears in Thailand. Our greatestdifficulty was in locating an area with sufficient bear density. The Khoa Ang Rue Nai Wildlife Sanctuaryin southeasternThailand was recommendedto us because it had a new researchfacility andsatellitemapsshowedit to have a dense forest. The southernborder of the reserve abuts other densely-forestedprotectedareas. Stewart-Cox(1995:107) characterizedthis areaas "thelargesttractof lowlandevergreenforest in Thailand." A few roads and trailspenetratedthe forest,which facilitatedaccess for trappingand radiotracking.The mainentrancewas guardedandgated, and therewere several guardstationsinside. Fromthese indicationswe expected this to be an ideal study site. We set out trapsand baits and conductedsign surveys. Although we found some old sign, we soon concluded thattherewere few bearsin this reserve;in fact, therewas little sign of any medium-largemammals,even at places where they would typically congregate,such as fig trees (Ficus spp.) laden with fruit, salt licks, and waterholes. We heard numerous reports of poaching, saw signs of poachingencampments,andheardgunshots. One nighta binturong (Arctictis binturong) was poached near our camp. We noticedthatduringboth day and night,motorcyclists rode freely aroundthe closed gates and past the guards. We learnedthatone of the roads throughthe reserve was a main thoroughfareconnecting two parallel 327 highways. This sanctuarywas certainlynot the "secluded world"thatStewart-Cox(1995:107) had described. Despite suitable habitat, this area exemplified what Redford(1992:412)calledan "emptyforest.""Oftentrees remainin a forest that humanactivities have emptied of manyof its largeanimals...We mustnot let a forestfull of trees fool us into believing all is well." We encountered a similar situation with sloth bears (Melursus ursinus) in Nepal. We surveyed their entire range,a narrowstripof lowlandforestandscatteredgrasslands called the terai. Sloth bears were abundant in Chitwan National Park, in the center of this range, but were absentat the easternand westernextremitiesof the range,despitesuitablehabitat. These areashad good forest cover and abundanttermites (a staple food for sloth bears)(Garsheliset al. 1999a), but sloth bearshad apparently been poached out during the previous 2 decades (Garsheliset al. 1999b), creatingvacantbearhabitat. Sun Bears in Borneo.-Meijaard (2001) reportedjust the opposite situationfor sun bearsin Kalimantan(IndonesianBorneo). Here, disappearingforests seemed to be filled withbears,despitesupposedperiodsof heavypoaching. Duringthe 1970s poachingof sun bearsappearedto be rampantin Indonesia,as evidenced by the amountof bile illegally exported. During that decade, Meijaard (1999) estimatedthatgall bladdersfrom about7,000 Indonesian sun bears were sent to South Korea;additional shipmentsof gall went to other countries. I previously showed thatquantitiesof tradedbile cannotbe converted to reliable estimates of numbersof dead bears, or even used to construetrendsin levels of bear mortality(Box 1). Nevertheless,it appearsfromthepresentlylow amount of bile exported,low in-countrydemand,and according to informationfromlocal people, few bearskilled for their parts,thatduringthe past 2 decades,the tradein partshas not resulted in large numbersof bears killed (Meijaard 1999). Interviewswith local people across Kalimantanin the mid-1990s indicatedthat sun bears were still "relatively abundant"in most forested areas (Meijaard2001). The forests, however,were rapidlybeing cut, which presumably would escalatehuman-relatedmortalityandthusreduce numbersof bears (Fig. 1). It is difficult, though,to acceptMeijaard's(2001) estimatethathabitatloss caused 10,000 sun bears to die in Kalimantanduringthe 1980s, given his evidence that human-causedsun bear deaths appearedto be relatively low duringthat decade. Also, while habitatloss is obviouslytroubling,equallytroubling is Meijaard's(2001) tenuous predictionthat within anotherdecade, 14,000-28,000 more bears will die. An irony in presentingsuch alarmingnumbersis that one coulduse themto back-calculateanestimateof present numbersof sun bears. Meijaard(2001) convertedhabitat 328 Ursus 13:2002 loss to numbersof dead bears using a "verycrude"density estimate of 1 bear/4 km2presentedby Davies and Payne (1981). This estimateof densitywas derivedfrom only 2 bearsightingsand9 observationsof sign. Extrapolating this density to all of Kalimantan would yield >90,000 sun bears. Extendingthis densityto forestedareas of Malaysian Borneo (Sabah and Sarawak) and Sumatrawould increasethe total to about 190,000 bears (forest areasfrom Mayauxet al. 1998). Even if sun bear densitiesin mainlandsoutheastAsia are much lower, the total world populationwould still well exceed 200,000, which would makethis species numericallyequivalentto brownbearson a global scale, and second only to American black bears. The reality is that sun bears are listed by the IUCN as "datadeficient,"becausereliableestimatesof population size and trendare unavailable(Baillie and Groombridge 1996). Creatingunsubstantiatedestimatesin the hope of rousingmoreconservationinterestmay,as illustratedhere, contravenethe intendedresult. Withoutfar betterinformationon the relationshipbetweenbeardensityandhabitat, attemptsto quantify bear numbersand trends from forest cover dataare likely to be misguided. IRONIESREGARDINGHUNTINGAND TREND POPULATION A particularlynoteworthyirony regardingbear populationsis thatmost legally-protectedpopulationsseem to be declining,whereasmosthuntedpopulationsareincreasing. One explanationis thatprotectedpopulationstendto be small, and thus moreproneto decline as a simple consequenceof low numbers(Caughley 1994). Anotherexplanation is that many of these legally-protected populationsare really heavily exploited. Oftentimes,the level of humanexploitationmay be less undera system of managedhuntingthan supposedtotal protection. The reasons for this seeming contradictionhave a lot to do withthe people,finances,energies,andideologiesentailed in a managed harvest, resulting in an infrastructureof managers,scientists,bureaucrats,and hunters,with nonhuntersandanti-huntersas overseers.This complexstructureis oftenlackingin the managementof protectedareas. However,it is also truethatcountrieswith managedbear huntingtend to have strongereconomies, which can supportbear managementactivities (e.g., research,enforcement) better than countries where hunting is banned. These points are illustratedfirst by contrastingthe management of Americanand Asiatic black bears, followed by an example regardingpolarbears (U. maritimus). AmericanversusAsiatic Black Bears.-The 2 species of black bears are similarin terms of their life histories, and seem similar in terms of reproductivepotential, al- though reproductivedata on wild Asiatic black bears is presentlyinsufficient to enable a true quantitativecomparison (Garshelis 2002). However, the 2 species are managedverydifferently.Legalhuntingis themainsource of mortalityfor American black bears in most parts of theirrange,whereashuntingfor Asiatic blackbearsis legal only in Japan.Most Americanblackbearpopulations appearto be increasing(Williamson2002), whereasAsiatic black bearsarethoughtto be decliningin most areas. The difference is that human exploitation is monitored and controlledin the formercase, surreptitiousin the latter. A reviewer of this paper asserted that the cause and effect thesis posed here is reversed. That is, legalized huntingdid not resultin numericallyabundantbearpopulations;rather,huntingwas legalized because bearswere numericallyabundant. I disagree with this. American blackbearswereseverelyover-exploitedthroughtheearlymid 1900s. Althoughregulatedexploitationof otherNorth Americanspecies, such as white-taileddeer (Odocoileus virginianus),datesto the 1600s (GilbertandDodds 1987), black bears were much less valued as food so did not inspire efforts to limit the take. Moreover,bears did not generate much interest among recreationalhunters on whose behalf game laws were made (Schullery 1983). In fact, mainly duringthe 1800s and early 1900s, federal, state, and local governmentssupportedprogramsto destroybothblackbearsandgrizzlybearsbecausethey were considereddetrimentalto raising livestock and crops as well as potentially dangerousto people (Spencer 1955, Cardoza1976, Brown 1996). An evolution in ideology, beginningin some U.S. statesin the early 1900s, eventually led to the designationof black bears as a big game species, with the objective of a sustainedharvest(Miller 1990). These laws were passedbecausebearpopulations had noticeably diminished. Minnesota was one of the last states to classify black bears as big game (1971). In one Minnesotacounty where bears had been considered "verynearlyextinct"priorto theirbig game listing (Cahn 1921:70,SpecialCommitteeon the Conservationof Wildlife Resources1940),a long-termtelemetrystudyrevealed a high density of bearsfollowing 20 years of legal hunting (D. Garshelis,unpublisheddata). There are many factors - economical, political, historical, cultural,and spiritual- that make it difficult to transferto Asia the Westerntraditionsof sustained-yield hunting. Proponents of sustainable use in developing countriesarguethat people are more apt to conserve resourceswhen they have a vested interestin a returnfrom theseresources(Gadgil1992,Kothariet al. 1995,Saberwal 1996). Others,though, have observed that high human densities, abjectpoverty,class systems, and corruptgovernmentscreate a situationwhere it is nearly impossible UNCERTAINTIES INPOPULATION TRENDS* Garshelis to regulate harvests (Bennett and Robinson 2000, Madhusudanand Karanth2000, Meijaard2001). A high marketvalue for bearsin Asia makes the regulation of harvestan even more dauntingproblem. In Korea, for example, Asiatic black bears were subjectedto the same sort of government-supportedremoval efforts as Americanblackbearsduringthe early-mid1900s (Won 2001). Unlike the situationin North America, however, Korean bear populations continued to plummet from overexploitation into recent times because they were soughtcommercially. A lesson learnedduringthe evolution of the NorthAmericansystem was thatmarkethunting was detrimental to wildlife populations and was thereforeincompatiblewith recreationaland subsistence hunting(Geist 1988, 1994). In fact, recreationalhunting enthusiastswere largely responsible for legislation that eventuallyprohibitedmarkethuntingfor wildlife in North America (Reiger 1978). Harvestinganimalsfor profit,though,is not uniformly detrimentalto wildlife populations. In North America, many species of furbearingmammalsaretrappedspecifically for sale of theirpelts, so the kill fluctuateswith fur prices;nevertheless,theirpopulationshave been carefully managed by governmentagencies (Novak et al. 1987). In severalEuropeancountries,huntersroutinelysell their game for personalprofitor for income for the landowner or huntingclub; in some cases, hunterscan only retaina portionof theirtake. This system has workedfor centuries (Bolen and Robinson 1995). In Japan,Moll (2001) suggested thata prohibitionagainstthe sale of bearparts might lead to diminishedinterestin legitimatebearhunting and higherprices for beargall, which togethercould result in reduced stewardshipof the resourceand hence increaseddangerof bearsbeing over-exploitedby poachers. To be clear,my purposehere was to pointout the seemingly paradoxicaleffects of legal hunting,not to suggest that sporthunting should be promotedwhere it does not now occur. Simplyinstitutinga legal harvestis obviously not the solution to declining bearnumbers. Historically though, in both North America and Europe, managed huntinghas been an effective system for protectingbear populations.It has workedbecauseit has enlisteda clientele interestedin ensuringcontinuedabundanceof the resource. It also has worked because, for species such as bears that can be a nuisance and a threat,it transfersthe killing of animals from the general public to a smaller groupof people (i.e., the hunters). Both these issues have been instrumentalin shapingbear managementand conservation in North America, Europe (Klenzendorf and Vaughan1999,Zedrosseret al. 2001), andJapan(Huygens et al. 2001, Moll 2001). Linnell et al. (2001:348) commented "Thereis no doubt that the concept of hunting 329 large carnivoresas game species is far older in Europe thanin NorthAmericaandhas contributedgreatlyto their persistence."Ironically,in places suchas IndiaandNepal, wherebearhuntingis now prohibited,preservesthatwere set aside explicitly for hunting (by both local and European aristocrats)duringthe 1800s formed the basis of a system of parksand wildlife sanctuariesthatnow constitute virtually the only remainingareas of intact habitat withviablepopulationsof largemammals,includingbears (Israel and Sinclair 1987, Mishra and Jefferies 1991, Rangarajan2001; negative consequences of these royal hunts and exclusionary policies notwithstanding [Saberwalet al. 2001]). Polar Bears.-During the 1960s it became evident that polar bears were being over hunted. In 1973 an historic conservationagreementwas signed among all 5 nations with populationsof polar bears (U.S., Canada,Norway [for Svalbard],Denmark[for Greenland],and the former U.S.S.R.). Interestingly,the InternationalAgreementon the Conservationof PolarBears (InternationalLegal Materials 13:13-18), which took effect in 1976, did not prohibit hunting,but ratherlimited it to native people using traditionalmethods (IUCN/SSC Polar Bear Specialist Group1999). Withinthis restriction,the membernations went in differentdirections. Canadianjurisdictionsimposedhuntingquotasin mostareas,whereasthe U.S. could not, underthe constraintof the MarineMammalProtection Act of 1972 (16 U.S. Code 1361-1407). However, non-mandatoryharvestguidelines have been developed for native communities in Alaska. In Greenland,there are no quotas on polarbears but the harvestis limited to native people who hunt or fish full time. In Svalbard, huntingof polarbearswas forbiddenafterthe Agreement. In Russia, a prohibitionon the huntingof polarbearspredated(1956) the Agreement.Russiathusappearsthe most restrictivefor the longest time, yet in reality,the strongest concerns about poaching polar bears exist in Russia (IUCN/SSC Polar Bear Specialist Group 1999). What may superficiallyseem ironicbutpertinentto this discussion is a recentagreementto permitnativeRussianpeople to huntpolarbearsin the populationsharedwith Alaska. The presumptionis thata legal hunt,with the self-serving interestto remainwithinsustainablelimits,wouldbe more effective at conservingthispopulationthanstriving(probably unsuccessfully) for total protection. Management for harvesttends to be more successful because it broadens the numberand scope of people with a stakein maintaininga healthypopulation. UNCERTAINTY AND CONSERVATION The only real certaintyin bearconservationis thathumanintrusion,via both directover-exploitationandhabi- 330 Ursus 13:2002 tatdestruction,is the mainfactorthreateningbearsworldwide. The degree of threat,however, is very uncertain. The best informationexists for NorthAmericanand European bear populations. Geographic ranges are generally well-delineated, and population estimates and growthrates, though often inexact, are usually based on some research data (Table 1). For Andean bears (Tremarctosornatus) of South America, there are good distributionmaps but no data-basedestimates of abundance or trend (Peyton et al. 1998). Good range maps and an estimateof populationsize exist for giantpandas, butthereis no good informationon populationtrend(Reid andGong 1999). Verygeneralizedrangemaps,poorpopulation estimates, and weak evidence of populationtrend are available for the other Asian species (Table 1). All these species, though,are perceivedto be in trouble. To aid in the conservationof these species, many believe it is necessary to provide populationnumbersand extinction scenarios. Populationviability analyses are certainlyproductiveexercises thatmay be especially importantin illuminatingsensitivepopulationparametersand weaknessesin the data(Sether et al. 1998, Wiegandet al. 1998);however,these shouldnot be confusedwith actual populationprojections(Mills et al. 1996, White 2000). We have rarelybeen able to trackpopulationtrendsin the present,andbecausewe lack vital biological information for many of the species (Garshelis 2002), it seems improbablethatforecastingthe futurewould be very accurate. Referringto largewhales, but describinga situation applicable to bears, Gerberet al. (2000:318) observed: "ourlimitedknowledge... makes it extremelydifficultto quantifythe degree to which a populationmay go extinct in a specific period of time... Unfortunately,the public and the press have not been entirelyawareof these difficulties. Worse,advocacygroupson both sides of the environmentalcontinuum and even some scientists have filled this void with inaccuracies." Some believe that admitting to uncertainty would muddythe message, and therebydetractfrom conservation initiatives. Thatview holds thatfirm,bold, andclear assertions,even if not entirelybackedby factualinformation, yield betterresults in terms of protectingenvironmentalwelfare thandoes revealinguncertainties.Those opposing this approachwarn of blurringthe distinction between science and advocacy, which can be especially temptingwhen both are harboredin the same individual andMcCoy (Bowen and Karl 1999). Schrader-Frechette (1999) arguethat occasionally compromisingscience in favor of advocacy will ultimately create the perception thatscience was abandoned.If we do not universallyadhere to all the principlesof science, then we must be prepared to wade into ethical battles, where scientific viewpoints no longer have ascendancy. There is an obvious counter-argumentto this reasoning: brandishinguncertaintymaynotbe a powerfulmeans of swaying policies towardbetterconservationof bears. Acknowledgmentof uncertaintyin the scientific arenais one thing; highlighting it in the political arena is quite another. There is certainly some wisdom in this, but I offer severalreasonswhy thereis usually greatermeritin makingthe uncertaintiesclearto the publicandthe politicians. (1) If new data do not supportprevious suppositions (e.g., about a population decline), and if the uncertaintiesinherentin the original suppositionswere not madeclear,scientific credibilitywill be damagedand future conservationefforts based on scientific information may be compromised. (2) Optimismgenerallyprovides more motivation for conservation action than pessimism(Beever2000), and,in manycases, uncertainty provides a greaterarrayof optimistic scenarios. Uncertainty in this context should not be confused with ignorance,which is always detrimental(Garshelis1997). (3) Incognizanceof uncertaintiesmay detractfromeffortsto gathermoredataandimprovemethodologies. False con- Table1. Relativedegreeof certaintyregardinggeographicrange,populationnumbers,andpopulationtrendsof the 8 species of bears. Symbols (++ reasonablygood, + fair, 0 poor or nonexistent)representsubjectiveratingsby the author for comparisonswithinand amongcolumns. Informationalquality" Species Americanblack Brown Polar Andean Giantpanda Asiaticblack Sloth Sun a Based Geographicarea NorthAmerica NorthAmerica Europe Asia Arctic SouthAmerica Asia Asia Asia Asia Range ++ ++ ++ + ++ ++ ++ + + + Numbers + + + 0 + 0 + 0 0 0 Trend + + + 0 + 0 0 0 0 0 mainly on Servheen(990), Servheenet al. (1999), Williamson(1999), Sathyakumar(2001), and Zedrosseret al. (2001), plus accumulatedknowledge and personalexperience. UNCERTAINTIES INPOPULATION TRENDS* Garshelis fidence in presumptionsabout populationdeclines thus may inhibitdiscoveries thatcould aid in detectingpopulation change. This is an extension of Gibbs et al.'s (1998:940) view: "The primaryconsequence of failing to improve methodologies for identifying population changein ecology will be a chronicfailureto detectpopulation change. Unfortunately,these statisticalerrorswill frequentlybe misconstruedas reflectingpopulation'stability,' lack of treatmenteffect, or ineffectivenessof management." Hence, if the uncertaintiesare not eventually remedied,even effectiveconservationprogramsmay yield no measureof success because it will not be possible to detect a populationincrease. I contend thatin the interestsof both science and conservation,biologists should emphasizethe uncertainties of populationassessmentsandthusthe necessity for more rigorous research. This may seem counter-intuitivein terms of conservation,but the logic is this: in the presence of uncertaintyefforts shouldbe directedtowardensuringno irreparableharm. The wide rangeof uncertainty aboutbearpopulationsshouldbe reasonenoughfor claiming a wide berthin erringon the side of caution. ACKNOWLEDGMENTS I thank S.D. Miller for the invitation and encouragement to write this paper. Commentsby an anonymous reviewerandAssociate EditorL.S. Mills promptedme to better elaborate my arguments. Discussions with C. Servheenand S.C. Amstrupclarifiedissues regardingthe tradein bearpartsand the huntingof polarbears,respectively. I am especially gratefulto J.L.D. Smithfor sparking my interest in Asian bears. This paper was written with support of the Minnesota Departmentof Natural Resources. 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