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Dropping Dead: Causes and Consequences of Vulture Population Declines Worldwide

Dropping Dead: Causes and Consequences of Vulture Population Declines Worldwide

Ann. N.Y. Acad. Sci. ISSN 0077-8923

ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue: The Year in Ecology and Conservation Biology

Dropping dead: causes and consequences of population declines worldwide

Darcy L. Ogada,1 Felicia Keesing,3 and Munir Z. Virani1,2 1The Peregrine Fund, Boise, Idaho. 2National Museums of , Ornithology Section, Nairobi, Kenya. 3Bard College, Annadale-on-Hudson, New York

Address for correspondence: Darcy L. Ogada, P.O. Box 1629, 00606 Nairobi, Kenya. [email protected]

Vultures are nature’s most successful , and they provide an array of ecological, economic, and cultural services. As the only known obligate scavengers, are uniquely adapted to a scavenging lifestyle. Vultures’ unique adaptations include soaring flight, keen eyesight, and extremely low pH levels in their stomachs. Presently, 14 of 23 (61%) vulture species worldwide are threatened with extinction, and the most rapid declines have occurred in the vulture-rich regions of and . The reasons for the population declines are varied, but poisoning or persecution, or both, feature in the list of nearly every declining species. Deliberate poisoning of carnivores is likely the most widespread cause of vulture poisoning. In Asia, vultures have declined by >95% due to poisoning by the veterinary drug , which was banned by regional governments in 2006. Human persecution of vultures has occurred for centuries, and shooting and deliberate poisoning are the most widely practiced activities. Ecological consequences of vulture declines include changes in community composition of scavengers at carcasses and an increased potential for disease transmission between mammalian scavengers at carcasses. There have been cultural and economic costs of vulture declines as well, particularly in Asia. In the wake of catastrophic vulture declines in Asia, regional governments, the international scientific and donor communities, and the media have given the crisis substantial attention. Even though the Asian vulture crisis focused attention on the plight of vultures worldwide, the situation for African vultures has received relatively little attention especially given the similar levels of population decline. While the Asian crisis has been largely linked to poisoning by diclofenac, vulture population declines in Africa have numerous causes, which have made conserving existing populations more difficult. And in Africa there has been little government support to conserve vultures despite mounting evidence of the major threats. In other regions with successful vulture conservation programs, a common theme is a huge investment of financial resources and highly skilled personnel, as well as political will and community support.

Keywords: ; ; ecosystem services; carcass decomposition; disease transmission; vulture decline; poisoning; persecution; Africa; Asian vulture crisis; vulture conservation; diclofenac; furadan

mals, and wildlife because the abundance of other Introduction scavengers, some of which are well-known disease Charles Darwin thought vultures were “disgust- reservoirs, increases substantially at carcasses with- ing.”1 From a human perspective, perhaps they are, out vultures.2,3,4 Scavenging of carcasses by vultures but vultures are nature’s most successful scavengers, promotes the flow of energy through food webs,5,6 and they provide us with an extensive array of eco- and vultures have been shown to facilitate African logical, economic, and cultural services. Most no- predators, such as lions and , in locating food tably, vultures dispose of carrion and other organic resources.7,8 refuse, providing a free and highly effective sanita- In this review, we highlight the unique adapta- tion service. The vulture-governed cleaning service tions of vultures to scavenging. We then describe protects the health of , domesticated ani- the dramatic recent and historic declines in many

doi: 10.1111/j.1749-6632.2011.06293.x Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. 1 Worldwide decline of vultures Ogada et al. vulture species worldwide. We explore the apparent the way.14 It has been estimated that vultures in the causes and consequences of these declines in differ- Serengeti consume more meat than all the other ent regions, and we conclude by characterizing the mammalian carnivores combined.12 elements that appear to be necessary for successful All vultures locate carcasses using keen eyesight. vulture conservation programs. New World vultures also have a well- developed sense of smell that is used for locating , distribution, and unique , , food in forested areas.16 17 18 Once they have located adaptations to scavenging food, they can travel quickly to reach it, avoiding dis- Globally, there are 23 species of vultures (includ- placement by larger terrestrial scavengers.12 For ex- ing ), of which the majority (n = 16) occur ample, vultures in the Serengeti entirely consumed in the and within the family Accipitri- 84% of experimentally placed carcasses before any dae. The remaining seven species comprise the New mammalian scavengers appeared.8 Facultative scav- World Cathartidae family. Most species (n = 15) engers, such as hyenas and especially lions, use the occupy a range within one continent comprised of activity of vultures to detect carrion,7 but vultures twoormorecountries.Fourspecies,theGriffonvul- more than compensate for this competition by ar- ture (Gyps fulvus), (Gypaetus barba- riving rapidly and in large numbers.12 tus), (Neophron percnopterus), and Vultures are among the largest of flying . ( monachus), have or his- Their size allows them to consume more food at torically had large ranges that span three continents. each carcass discovery and to carry greater body re- Two species, (Cathartes aura)andBlack serves, which is important given their erratic food vultures (Coragyps atratus), range widely within supply. A large body also helps them to outcompete bothNorthandSouthAmerica.Capevultures(G. smaller scavengers at carcasses and because flight coprotheres) in and California con- speed is largely determined by body mass;11 it in- dors (Gymnogyps californianus) in North Amer- creases the area that they can search each day. A ica have historically small ranges,9,10 though fos- recent study using satellite tracking devices deter- sil evidence suggests that California condors were mined that the mean foraging range for two im- once found throughout the United States, south- mature Cape vultures (one was likely a Cape x ern Canada, and northern Mexico.10 Vulture-rich White-backed (G. africanus)hybridvulture)was regions include Central and (n = 6 an astounding 480,000 km2 over an eight-month spp.), (n = 10 spp.), and Africa (n = 11 period.19 Physiologically, vultures have low pH lev- spp.). els in their digestive tracts (pH 1–2); this destroys Outside of the oceans, vultures are the only most microscopic organisms and greatly reduces the known obligate scavengers.11 They are uniquely probability that vultures act as sources of infection adapted to exploit a transient food source that oc- at carcasses.20 Finally, vulture life history is charac- curs intermittently over large areas.11,12 Using glid- terized by delayed maturity, low productivity, and ing flight, vultures take advantage of upward air relatively high adult survivorship. Vultures and es- movements that enable them to travel rapidly over pecially condors have some of the lowest reproduc- long distances with relatively little energy expen- tive rates among birds, and their populations are diture.13 This allows them to search for food effi- particularly vulnerable to high mortality, whether ciently. They can also search communally by ob- by natural or human causes.21 serving other birds from the air. Aerial searching also gives them a considerable advantage over ter- Historical and recent vulture population restrial scavengers because the latter have limited trends feeding ranges, higher energy expenditures to locate carcasses, and comparatively poor visibility from Vulture population declines in and North the ground.14,15 The superior foraging efficiency of American likely began as early as the mid-19th avian scavengers is nowhere more apparent than in century.22,23 One hundred years later, some pop- the Serengeti, where only vultures have the ability ulations of Bearded vultures in Europe and the Cal- to follow migratory over vast distances ifornia condor in were already near- and benefit from heavy mortality that occurs along ing extinction.22,23 Further reports of population

2 Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. Ogada et al. Worldwide decline of vultures

Table 1. Overview of historical vulture declines

Species Range Area declining Peak of declines Causes of decline References

Egyptian vulture Africa, Asia, Europe (first), Asia, 20th century Persecution 26 Europe Africa through poisoning and hunting Bearded vulture Africa, Asia, Europe (first), Began 1860 Persecution, 22, 27 Europe Africa through 1900 poisoning, also when nearly electrocution extirpated North America North America 19th century Lead poisoning, 28, 29 through 1937 persecution, collision with overhead wires, secondary poisoning Southern Africa Southern Africa 1900 Poisoning, decline 9 in food supply, electrocution, persecution, disturbance at breeding sites White-rumped, Asia South Asia 1950–1970s Decline in food 3, 24, 25 Slender-billed, (Malaysia, Laos, supply due to Red-headed , overhunting and vultures rare if changes in not extinct) and livestock Burma, husbandry Bangladesh and practices (primarily) also seriously persecution and declined, with poisoning exception of declines of Cape vultures and of vultures in South ica, which have historically recorded large popula- Asia testify to the global nature of declines that tion declines,22,23,27 the majority of vulture popu- had already begun prior to the mid-20th century lations are now increasing or stable (Table 2). In (Table 1 and Refs. 9, 24, and 25). vulture-rich regions, large population declines have In few areas, if any, have vulture populations occurred in recent decades, particularly in Asia and maintained historical levels of abundance, but there Africa. are substantial differences in the numbers of species Within the Central and South American re- declining and in population trends among regions gion, half of the vulture species are estimated to (Table 2). In the , populations of three be in decline, though the region has compara- species are reported to be in decline in the United tively little published research on vulture popula- Arab Emirates,51 and five species present in are tions apart from that on the (Vultur similarly declining.52 In Europe and North Amer- gryphus).31,53,54,55

Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. 3 Worldwide decline of vultures Ogada et al.

Table 2. of the world’s vultures. References are listed in respect to recent status overviews where available; these are indicated by “and references therein.” For species lacking a recent status overview, important historical and recent references are listed, with BirdLife International (2011) as a general source.

IUCN Red List Species Scientific name Region(s) categorya Current status References

California condor Gymnogyps North America CR Small population 30 and references californianus increasing, therein though lead shot in carcasses remains a threat Cathartes aura Americas LC Population 31–33 and increasing references therein Coragyps atratus Americas LC Population 31–33 and increasing references therein Andean condor Vultur gryphus South America NR Moderately rapid 31, 34 and decline references therein Lesser Cathartes Central and South LC Apparently stable 31 Yellow-headed burrovianus America vulture Greater Cathartes South America LC Slow decline 31 Yellow-headed melambrotus vulture Sarcoramphus Central and South LC Slow decline 31 papa America Egyptian vulture Neophron Europe, Africa, EN Declining 26, 31, 35, 36 percnopterus Middle East, Asia significantly throughout most of its range. Rapid declines in India Bearded vulture Gypaetus barbatus Europe, Africa, LC Slow decline 27, 31 and Middle East, Asia throughout references much of range therein Gyps fulvus Europe, Africa, LC Increasing in 31 Middle East, Asia Europe, stable in central Asia and decreasing in and Turkey Cinereous vulture Aegypius Europe, Africa,b NT Slow to moderate 31, 37 and monachus Middle East, Asia decline references therein

Continued

4 Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. Ogada et al. Worldwide decline of vultures

Table 2. Continued

IUCN Red List Species Scientific name Region(s) categorya Current status References

Hooded vulture Necrosyrtes Africa EN Rapid decline of at 38 and references monachus least 50% over therein three generations White-backed Gyps africanus Africa NT Large declines in 16, 31, 39–42 vulture , but apparently stable in other parts of Africa Ruppell’s¨ vulture Gyps rueppellii Africa NT Extremely rapid 16, 31, 39–42 declines in West Africa and moderate declines elsewhere Lappet-faced Torgos tracheliotos Africa, Middle East VU Moderately rapid 16, 31, 39–42 vulture decline White-headed Trigonoceps Africa VU Declining at slow to 16, 31, 39–42 vulture occipitalis moderate rate Cape vulture Gyps coprotheres Africa VU Declining at ∼20% 9, 31, 43–45 over three generations Palm-nut vulture Gypohierax Africa LC Apparently stable 31 angolensis Gyps indicus Asia CR Extremely rapid 4, 31, 46–49 declines of >97% over 10–15 years Gyps himalayensis Asia LC Apparently stable 31 White-rumped Gyps bengalensis Asia CR Extremely rapid 4, 31, 46–50 vulture decline of >99% over 10–15 years Red-headed vulture Sarcogyps calvus Asia CR Rapid decline in 31, 35 excess of 90% over 10 years in India Slender-billed Gyps tenuirostris Asia CR Extremely rapid 4, 31 vulture declines a IUCN Red List category abbreviations are as follows: LC, least concern; NT, near threatened; V, vulnerable; EN, endangered; CR, . bConsidered extinct in the region.16

Vulture populations in South Asia have in- ladeo National Park, India, which occurred within curred the most precipitous and rapid declines a 10-year period. Subsequent surveys over the next ever recorded. Prakash48 first reported popula- decade confirmed massive declines (>96%) of three tion declines of >95% for Gyps vultures in Keo- species of Gyps vultures in India.4,49 Rapid declines

Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. 5 Worldwide decline of vultures Ogada et al. have been similarly noted in Pakistan46,47,50 and through actions such as shooting, harassment, and .56,57 More recent declines in Egyptian and deliberate poisoning. Red-headed vultures (Sarcogyps calvus)havebeen Vultures are particularly vulnerable to toxic sub- documented throughout India.35 stances due to a combination of foraging behaviors In Africa, recent population collapses have been and life history traits found collectively only in vul- recorded, particularly in West and . In tures.63 First, most vultures are obligate scavengers West Africa, populations of all vultures except the that rely on eating dead or waste products; (Necrosyrtes monachus)havede- this may increase their likelihood of exposure to clined by an average of 95% in rural areas over contaminants. Second, because vultures feed com- the last 30 years.40,41,58 In protected areas of the munally, large numbers can be poisoned at a single Sudanese zone, their collective populations fell by carcass. Finally, vultures are very long lived and at a an average of 42% over the same period.40,41,58 In high trophic level, which increases their vulnerabil- East Africa, vulture declines of 70% were recently ity to bioaccumulation. Bioaccumulation may have recorded over a three-year period in north-central sublethal effects on reproductive success, behavior, Kenya.59 Even the wildlife-rich Masai Mara region immune response, and physiology.64 has lost an average of 62% of its vultures over the The deliberate poisoning by humans of carni- past 30 years, and annual vulture mortality as high as vores, which kills scavengers as well as the intended 25% has recently been recorded.42,60 The situation victims, is likely the most widespread cause of vul- for vultures in North Africa is dire, particularly in ture poisoning. Carnivore poisoning continues to , where two species, Cinereous and Lappet- be common, especially in Europe and Africa.65–75 In faced vultures (Torgos tracheliotos), have been extir- Europe, poisoning is used to kill predators of game pated.61 Others are predicted to follow, and the rest animals (e.g., rabbits, , and ) be- of the region offers little hope for long-term vulture cause hunters believe carnivores such as and conservation.61 Vulture research and conservation mongooses reduce their hunting success.76 In both have a relatively long history in southern Africa, be- Europe and Africa, poisoning is used to “protect” ginning with the formation of the Vulture Study livestock from predators. In Europe, it is regarded Group in 1977. That group produced the seminal as the first option to deter carnivores from attacking book The Vultures of Africa and ingrained vulture livestock, while in Africa poisoning is largely used research within the ornithological community. Vul- to avenge the killing of livestock (D. Ogada, pers. ture populations in the region continue to be the obs.76). best studied in Africa and rival the level of study Some European countries (e.g., and UK) of those in Europe and North America. However, have reduced poisoning incidents through more there are a few species whose populations continue stringent penalties; tougher restrictions on the use to decline, and one, the Egyptian vulture, is be- of toxic chemicals; increased public awareness; lieved to be extinct as a breeding species in southern and cooperation between government ministries, Africa.62 Throughout Africa, the Hooded vulture, landowner associations, and nongovernmental or- a widespread human commensal, has declined by ganizations.76,77 Spain has taken an innovative ap- an average of 62% over the past 40–50 years, and in proach to tackling this problem by training some areas the decline has been much more rapid.38 to detect specific poisons (baits and carcasses of poisoned animals) that are most commonly used against wildlife. Dogs detected 70% more poisoned Causes of declines baits than did specialized (human) detection teams. There are numerous reasons behind the global vul- Funded by the regional government, the canine unit ture decline. However, either poisoning or human assists in the discovery of offenders as well as in persecution, or both, feature in the list of nearly dissuading poisoning through routine inspections every declining vulture population. We define poi- in known hotspots.78 In Africa, interventions are soning as the unintentional killing or harming of largely spearheaded by nongovernmental organi- vultures through consumption of contaminated car- zations, such as the Endangered Wildlife Trust in casses or remains. Human persecution refers to and WildlifeDirect in Kenya. While the intentional killing or disturbance of vultures some success has been achieved, there is a need for

6 Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. Ogada et al. Worldwide decline of vultures greater financial support and more training and en- there were no lead-related condor deaths.87 How- forcement if prevention programs are to be sustain- ever, there were three lead-related condor deaths able and effective (D. Ogada, pers. obs.72). after the 2009 hunting season.30 Poisoning of vultures by ingestion of nonsteroidal In contrast to unintentional poisoning, deliber- anti-inflammatory drugs, particularly diclofenac- ate persecution of vultures has occurred for cen- sodium, has caused rapid and severe population turies. Most vultures have been victimized due to declines in Asian Gyps vultures. During the 1990s, people’s ignorance, superstition, wantonness, and researchers first noted high mortality rates in three retaliation.9 Vultures have been believed to spread Gyps species. Subsequent postmortem analyses in- diseases such as anthrax, to be responsible for blow- dicated the vultures died of renal failure trig- fly plagues, to foul drinking water provided for live- gered by diclofenac residues found in livestock car- stock, and to represent evil spirits, among other be- casses.46,47,79 In South Asia, diclofenac was a widely liefs.9,88 used veterinary analgesic in livestock that typically is Shooting and intentional poisoning are the two consumed by scavengers if they die of disease or in- main forms of persecution. Shooting vultures jury. Studies showed that diclofenac concentrations has long been documented in the United States, in treated livestock were sufficient to cause the high Europe, and North Africa, where the activ- levels of vulture mortality that had been recorded.79 ity appears to be largely for sport.22,28,29,61 Contaminated carcasses were subsequently linked Documented cases of intentional poisoning of to vulture population declines across the subconti- vultures have been noted as being in retaliation for nent, and models further confirmed the correlation the suspected killing of newborn lambs, to disguise between vulture declines and diclofenac residues the locations of poachers’ activities, and to obtain in carcasses.80,81 In response to the vulture cri- vulture parts for traditional medicine.65,72,87,89,90 sis, the governments of three of the most affected The acquisition of vulture parts for traditional countries—India, Pakistan, and Nepal—withdrew medicine has been documented in West and south- manufacturing licenses for veterinary diclofenac in ern Africa72,91–93 and is suspected in parts of East 2006. Recent surveys in India indicate that the ban Africa (N. Baker, pers. comm.). Though it is likely on veterinary use of diclofenac has markedly re- to be a substantial threat to vultures in those areas, duced its presence in livestock carcasses to levels there have been no documented efforts to tackle the almost half of what they were prior to and imme- problem. Interventions by local governments appear diately after the ban.82,83 Despite the reduction of unlikely due to cultural beliefs and practices that re- diclofenac in carcasses, prevalence levels still remain main deeply entrenched in African societies.91,94 In sufficiently high to continue to cause a rapid rate of addition to use in traditional medicines, vultures, vulture decline that has been estimated at 18% year and in particular the Hooded vulture, are hunted for Oriental White-backed vultures (G. bengalen- for food in West Africa.40,41 Though it is difficult to sis).83 ascertain population-level effects of persecution on Lead poisoning through the ingestion of pellets individual species, it is thought to be a significant or fragments of lead-based bullets in hunter-killed cause of mortality for some species and populations, carcasses is a serious threat to some vulture pop- including European Bearded vultures, Cape griffons ulations, most notably the California condor. Lead in South Africa, Hooded vultures in West Africa, and poisoning has been implicated as the leading cause largevulturesinNigeria.22,27,40,41,91,92 of death in the Arizona population of the condor Poisoning and persecution are not the only (∼40% of the worldwide population), and it had threats to vulture survival. Electrocution and col- been estimated that without the intensive interven- lision with power lines have also caused significant tion of veterinarians, this population would not be levels of vulture mortality,95–99 and the recent pro- self-sustaining in the wild.29,84–86 However, in 2005 liferation of wind farms as a source of green energy the Arizona Game and Department imple- production also has had adverse effects. In recent mented a hunter-education campaign and provided studies, Griffon vultures suffered among the high- free, nonlead ammunition for hunters in condor est levels of mortality after collision with wind tur- habitats. With >80% participation by hunters, the bine blades.100,101 Given the rapid increase in the severity of lead exposure during 2007 was low and development of “green” technology and electricity

Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. 7 Worldwide decline of vultures Ogada et al. infrastructure worldwide, these threats are likely to such as feral dogs and rats (Rattus rattus).3,4 Feral increase in coming decades. Mass drowning of vul- dogs have been shown to compete directly with vul- tures (of up to 38 birds at a time) has also been re- tures for food and are capable of displacing vul- ported, particularly in semiarid areas of South Africa tures from carcasses. In areas adjacent to communal where the birds enter artificial reservoirs presumably lands in , feral dogs dominated carcasses, to bathe or cool off, only to be unable to extricate but inside protected reserves, vultures were the ma- themselves due to vertical reservoir walls.67,102 jor scavengers at carcasses.109 Both feral dogs and Other threats to vultures mentioned in the lit- rats are well-known disease reservoirs, and their in- erature include habitat changes and food short- crease at carcasses in the absence of vultures may age. Habitat loss and degradation are suspected to increase rates of infectious disease transmission to have played roles in the dramatic declines (>98%) other species. Diseases such as rabies and bubonic of large vultures outside of protected areas in plague, for which dogs and rats respectively are West Africa where human population growth has the primary reservoirs, may increase as a conse- been very rapid.41,58 Declines in large game birds quence of vulture declines. Wildlife and livestock and have also been noted.41,58 Lack of could also be at increased risk from - and rat- food—due to overhunting or changes in livestock borne pathogens, including canine distemper virus, husbandry—could have major impacts on vul- canine parvovirus, and Leptospira spp. bacteria.3 In tures18 and is thought to have contributed to large- India, rising cases of human anthrax due to handling scale vulture declines in West Africa,40,58 Southeast infected carcasses or consuming poorly cooked meat Asia,24 and Europe.36 More recently, an outbreak of of infected livestock are believed to be linked to the bovine spongiform encephalopathy in Europe led precipitous decline of vultures.110 to the passing of sanitary legislation that restricted Arecentconfirmedtheimportantroleofvultures the use of carcasses and by-products.103 Vul- in decomposing carcasses, maintaining community tures and other avian scavengers have been hard hit structure, and moderating contact between mam- by the ensuing food shortage, which has been linked malian scavengers at carcasses.2 In Kenya, in the ab- to lower breeding success and higher mortality in ju- sence of vultures, carcass decomposition time nearly venile vultures.104 tripled, and both the number of scavenging mam- mals and the time they spent at carcasses increased Consequences of declines threefold. Further, there was a nearly threefold in- Given the rate at which vultures are declining, there crease in the number of contacts between mam- have been surprisingly few studies about the eco- malian scavengers at carcasses without vultures, sug- logical consequences of the widespread disappear- gesting that the demise of vultures could facilitate ance of these scavenging birds.105–107 Communities disease transmission at carcasses.2 of facultative scavengers are highly structured (not In addition to ecological impacts, vulture de- random) and complex, and birds contribute most clines have already had socioeconomic and cul- to this structure because they are the most special- tural impacts in South Asia, where they hold ized scavengers.108 For example, in a Polish , important social significance. Amongst the well-adapted scavengers such as ravens and foxes Zoroastrian-practicing Parsi community in India, were nearly ubiquitous at carcasses, whereas rare or who believe that fire, water, air, and earth are pure sporadic scavengers associated with the main scav- elements that need to be preserved, the dead are enger species and did not scavenge randomly, but laid in “Towers of Silence.” Built on hilltops or low rather on those carcasses where carrion specialists mountains, these circular pillars of stone enclose were present.108 As carrion specialists, the absence corpses that are left in the open to be disposed of by , of vultures from carcasses may affect the commu- scavengers, principally vultures.111 112 This ancient nity composition of scavengers at carcasses, which custom, also known as and similarly prac- could alter scavenging rates for individual species. ticed by Tibetan Buddhists, has come to an abrupt In localized regions where vultures are function- end in the last decade due to the collapse of vulture ally extinct, such as in India, the absence of vul- populations in the region. The Parsi community has tures at carcasses appears to have driven a rapid unsuccessfully turned to solar reflectors in the hopes , increase in the abundance of opportunistic species of hastening decomposition.112 113

8 Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. Ogada et al. Worldwide decline of vultures

Economic consequences of vulture declines in- the Indian states of Rajasthan and Madhya Pradesh clude increased costs to human health. Estimates has already begun to increase.118,119 The identifica- of the human health costs of the loss of vultures tion of veterinary diclofenac as the primary cause and subsequent increases in dogs and rabies are of vulture population declines in South Asia took about $1.5 billion annually in India.111 In Nepal, at least four years of intensive field and diagnos- the economic benefits of conserving vultures were tic research.82,120,121 The results of this work were estimated at $6.9 million, and interviews in commu- published in a prominent journal79 and presented nities within Important Areas showed they were to South Asian government authorities at a Kath- considered significantly beneficial to humans.114 In mandu Summit Meeting organized by The Pere- Uganda, Hooded vultures consume primarily in- grine Fund in February 2004. The dissemination of ternal organs from diseased animals thrown from scientific research to government authorities plus abbatoirs, thereby saving local councils the expense advocacy work can play a crucial role in achieving of a more sophisticated system of collection and conservation results. The key was getting govern- disposal of refuse.115 ments to listen and to understand the gravity of the vulture situation and its consequences should Comparison of the situation in Asia versus conservation interventions fail. The role of conser- Africa vation organizations in India, Nepal, and Pakistan The catastrophic declines in vulture populations was critical in advocating for a ban on the manu- in South Asia have generated considerable atten- facture, sale, and import of veterinary diclofenac. In tion from the media and the scientific community, addition, conservation organizations in South Asia, which has catalyzed vulture research, particularly in along with their overseas partners embarked on Africa.116,117 There are many similarities between large-scale education and outreach programs to en- Africa and South Asia. In particular, both regions sure that rural people understood the lethal impacts harbor human populations that are mostly rural of administering veterinary diclofenac to livestock. and poor, growing rapidly, and divided into many The Indian government in particular was extremely ethnic groups. Although the causes may differ, there supportive in providing the necessary framework for have also been similar levels of decline in vulture legislation, financial support, and assistance with populations in both regions.4,40–42,46,47,59 developing vulture captive breeding and restora- The prospects for vultures and their continued tion efforts (MZV, pers. obs.). Also significant to survival, however, differ between the two regions. In the conservation of vultures on the subcontinent is particular, the regions could not be more disparate the role of vultures in Hindu mythology where they in the level of attention given to the issue from local are highly esteemed, as evidenced by the existence governments, the international scientific and donor of a vulture god, Jatayu, which is regarded as a holy , communities, and the media. There are undoubt- bird.111 113 edly many reasons for this, but the fact that the Asian The situation in Africa is vastly different be- vulture crisis has been largely pinpointed to a single cause there are many significant threats to vultures, source—diclofenac poisoning—may be crucial. The not just one. In addition, the threats vary by re- discovery of diclofenac has focused conservation ef- gion. For example, the cause(s) of vulture disap- forts (and hence funding) and media attention on pearances in West Africa remain unclear, though a single target, and it has provided a mechanism many suggestions have been made, including food whereby success of conservation interventions can shortage, poisoning, and persecution for traditional , be directly measured. medicine and food.40 41 Whereas in South Asia re- Although the situation for Asian vultures is criti- cent population surveys have indicated that declines cal and it will likely remain so over coming decades, have slowed or ceased in some areas and the threat the governments within the region have played a from diclofenac poisoning has reduced substan- , , crucial role in halting the declines and protecting tially,83 118 119 in Africa there is little similar evi- , and bolstering remaining populations.82 Indeed, ev- dence.122 123 idence from four years since the ban on veterinary In addition, the vast majority of African govern- diclofenac has shown that productivity of Indian ments, with the exception of South Africa, have pro- vultures (G. indicus) in southeast Pakistan and in vided little, if any, support for vulture conservation

Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. 9 Worldwide decline of vultures Ogada et al. or have attempted to resolve known vulture threats. United States, Griffon vultures in the Massif Cen- In West Africa, studies of vultures over the past 40 tral region of , and Bearded vultures in the years are virtually nonexistent122 though seven years European .133 In addition to releasing and feed- have passed since the first reports of massive vulture ing vultures, intensive public education programs population declines there were first published.40 were launched that targeted hunters, farmers, and Kenya and Uganda are the only two East African livestock keepers, and all released individuals have countries where some populations of vultures have been marked and in some cases are intensively mon- been studied and monitored for many decades (S. itored.134–136 Common themes among these suc- Thomsett unpub. data,42,115,124). In Kenya, two re- cessful conservation efforts are a huge investment, cent studies have shown large declines in most at both national and international levels, of finan- species, and there exist both scientific and anecdotal cial resources and highly skilled personnel, as well reports linking the declines to poisoning, primarily as political will and community support. to the agricultural pesticide Furadan.42,59,75,125 In While reintroductions have boosted populations addition to over 350 vultures known to have been of some species, populations of Turkey and Black poisoned in the past seven years, Kenya’s lion popu- vultures have experienced major increases through- lation has similarly plummeted, largely due to illegal out much of their ranges in North America since the poisoning.126 Indeed, wildlife poisoning is so rife in mid-1970s without any human intervention.32,137 Kenya that a national taskforce, first spearheaded Although the reasons for their population increases by conservationists and later incorporated under have not been well studied, a number of suggestions the Ministry of Agriculture, was initiated in 2008 have been made, including substantial decreases in to tackle the problem. The primary aim of conser- persecution, increases in food availability due to the vationists engaged in the Stop Wildlife Poisoning large resurgence of White-tailed populations Taskforce was to implore the Kenyan government (Odocoileus virginianus), and decreases in secondary to ban the registration of carbamate pesticides, of poisoning, especially exposure to DDE (through which Furadan is the most notorious, for sale in DDT spraying), which induced eggshell thinning in Kenya.127 In lieu of a ban on carbamate pesticides, many raptor species.32 While both species are sus- the taskforce also lobbied for tighter restrictions on ceptible to the effects of DDT spraying, their sus- the sale of Furadan in Kenya, as it is used to poison ceptibility to other toxins is mixed. Turkey vultures both wildlife and feral dogs. These pesticides are af- have been shown to be relatively insensitive to some fordable, highly effective, and easily accessible.128,129 rodenticides but quite sensitive to strychnine and Apart from reports of wildlife poisoning, Furadan is cyanide. It has also been suggested that both species known to be used to kill birds and fish that are later may be particularly sensitive to lead poisoning.32 sold for human consumption.130–132 Despite the raft A review of poisoning cases in the United States138 of evidence provided to Kenyan government offi- suggests that both Turkey and Black vultures may cials and a report on the situation as requested by be less susceptible to poisoning than some other the Prime Minister’s office,131 the Kenyan govern- raptor species. In general, raptors are more suscep- ment has yet to take any action restricting its use or tible to poisoning compared to birds of a similar sale in the country despite the existence of pesticides size; their stomachs have low pH levels that increase that are purported to be less toxic to wildlife.128 their susceptibility to lead poisoning.138,139 Are- view of data presented by Mineau et al.138 shows Overview of successful conservation that 181 raptor deaths were attributed to the labeled programs and species use of pesticides, implying that the raptor deaths While the Asian vulture crisis is still unfolding and were accidental and were not as a result of perse- the full results of vulture conservation efforts will cution. No mortality of Turkey or Black vultures not be known for some years to come, in Europe was recorded, despite mortality of scavenging Red- and the United States a number of conservation pro- tailed , Bald , and Swainson’s hawks, grams have already succeeded in bolstering dwin- representing 31%, 17%, and 11% of cases, respec- dling vulture populations. Three of the most suc- tively.138 While the results are only suggestive that cessful programs involved the reintroduction and both species may exhibit a reduced susceptibility to supplementary feeding of California Condors in the poisons, they do not suggest whether physiological

10 Ann. N.Y. Acad. Sci. xxxx (2011) 1–15 c 2011 New York Academy of Sciences. Ogada et al. Worldwide decline of vultures and/or behavioral traits may play a greater role. In a and serious population declines in many species. recent study, Turkey vultures showed no signs of tox- Though the long-term impacts of these declines are icity after being dosed with diclofenac at >100 times not fully understood, ecosystem services provided the lethal dose for Gyps vultures.140 Turkey vultures by vultures have already plummeted, and novel re- have also been shown to have exceptional immune search has shown that disease transmission at car- function.141 Behaviorally, vultures may limit their casses may increase. The two most important re- susceptibility to toxins by foraging in smaller group gions for Old World vultures—Asia and Africa— sizes. The mean number of vultures poisoned per have witnessed recent catastrophic population de- carcass appears to be proportional to their forag- clines in most species. While the declines in Asia ing group size (data from Ref. 16). In addition to have been linked to poisoning by the veterinary drug physiological or behavioral adaptations that may diclofenac, the reasons for the declines across Africa benefit populations of Turkey and Black vultures, remain little understood. The Asian vulture crisis we posit that the governments of some countries in has highlighted the importance of collaboration be- the Americas have stronger conservation policies, tween scientists, regional governments, donors, and more political will, and more resources to conserve the media to effectively conserve vultures over the vultures as compared to countries in Asia and Africa. vast areas where they range. In many African coun- Other ongoing and potentially important con- tries, vulture populations remain little known and servation initiatives consist of public involvement even less is being done on the ground to ensure in vulture research or citizen science programs and their survival. In countries such as South Africa increasingly through public education and outreach and Kenya, where vulture conservation programs programs. Citizen science programs have largely fo- are ongoing, efforts are largely driven by or with cused on creating awareness of wing-tagged vul- the support of local conservation organizations. As tures and requesting the public to report sightings of the Asian vulture crisis has shown, without support marked individuals. The use of vulture restaurants and backing from national governments and local could also be particularly useful to obtain reports of communities, any conservation efforts are likely to wing-tagged vultures from citizen scientists. Results be met with limited success over the long term. from South Africa indicate that 4,443 resightings from a sample of 120 vultures have been reported, Acknowledgments largely by citizen scientists at vulture restaurants We thank N. Richards for providing expertise on over a five-year period (A. Botha, pers. comm.). poisoning issues and A. Botha, C. Whelan, and one Public education focused on the plight and impor- anonymous reviewer for their comments on an ear- tance of vultures has recently come to the forefront lier draft of the manuscript. with the recognition of International Vulture Aware- ness Day (www.vultureday.org). International Vul- Conflicts of interest ture Awareness Day aims to have conservation orga- The authors declare no conflicts of interest. nizations worldwide, including zoos and local gov- ernment agencies, organize a one-day celebration References of vultures that publicizes the conservation of vul- 1. Houston, D.C. 2001. Condors and Vultures. Voyageur Press, tures to a wider audience and highlights important Inc., Stilwater, Minnesota, USA. work being carried out by vulture conservationists 2. Ogada, D.L., M.E. Torchin, M.F. Kinnaird & V.O. Ezenwa. throughout the world. In press. Ecological consequences of vulture declines on facultative scavengers and potential implications for mam- Conclusions malian disease transmission in Kenya. Conserv. Biol. 3. Pain, D.J., A.A. Cunningham, P.F. Donald, et al. 2003. A summary of the available evidence has shown Causes and effects of temporospatial declines of Gyps vul- that scavenging birds, and vultures in particular, are tures in Asia. Conserv. Biol. 17: 661–671. the most threatened group of birds in the world, 4. Prakash, V., D.J. Pain, A.A. Cunningham, et al. 2003. Catas- and presently 61% are listed on the IUCN Red List trophic collapse of Indian white-backed Gyps bengalen- 31,106 sis and long-billed Gyps indicus vulture populations. Biol. of . As a consequence of Conserv. 109: 381–390. being highly specialized, vultures are particularly 5. DeVault, T.L., O.E. Rhodes & J.A. Shivik. 2003. Scavenging prone to poisoning, which has led to widespread by vertebrates: behavioural, ecological, and evolutionary

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