SEPTEMBER 2007 SHORT COMMUNICATIONS 235

J. Raptor Res. 41(3):235–238 E 2007 The Raptor Research Foundation, Inc.

WHY DO CONDORS AND VULTURES EAT JUNK?: THE IMPLICATIONS FOR CONSERVATION

DAVID C. HOUSTON1 Ornithology Group, Institute of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ U.K.

ALLAN MEE Zoological Society of San Diego, CRES, 2920 Zoo Drive, San Diego, CA 92101 U.S.A.

MIKE MCGRADY Natural Research Ltd., Am Rosenhu¨ gel 59, A-3500 Krems, Austria

KEY WORDS: vulture; condor; conservation; diet; junk; trash. fulvus) at the Gamla Golan Heights colony. Most nests The seven species of New World condors and vultures are strewn with junk; such quantities have been found in and the 15 species of Old World vultures are taxonomically the stomach of chicks that it can easily be felt, and heard, unrelated, being descended from ancestral storks and ea- by gently palpating the stomach, and this condition has led gles, respectively (Feduccia 1996). They occupy identical to at least one known gut blockage: (Ferro 2002, B. Wood- scavenging roles in their respective ecosystems, being clas- ley and O. Bahat pers. comm.). In Armenia, a griffon vul- sic examples of convergent evolution. Species specialize on ture (G. fulvus) chick ejected 34 g of junk including sheep different parts of carcasses (Kruuk 1967, Hertel 1994) with wool (Fig. 1), and junk is common in and below nest condors [Andean Condor (Vultur gryphus) and California ledges (M. Ghasabian pers. comm.). Junk is routinely Condor (Gymnogyps californianus)] and griffon vultures (all found at nests of G. bengalensis in Pakistan (M. Gilbert pers. eight species of Gyps) taking muscle and viscera from large comm.) In southern Africa, Benson et al. (2004) docu- mammals: our speculation here is mainly concerned with ment the extensive range of junk eaten by Cape Griffon these species, not other vulture species. Among the many (G. coprotheres), and review other studies from this region. similarities between these two groups is the unusual behav- As far as we know, comparable behavior has not been de- ior of swallowing indigestible, nonfood and often human- scribed on this scale for any other birds of prey or owls, made objects. For brevity we call this ‘‘junk.’’ Junk in- despite much intensive pellet analysis which would be ex- cludes fragments of glass, china, and plastic, metal objects pected to reveal such activity (e.g., Yom-Tov and Wool such as bottle tops, small rocks, sticks, grass, wool, and fur, 1997, Akaki and Duke 1998, Redpath et al. 2001). In this among other things. The scale of this behavior has only paper we speculate on the evolutionary function of this become apparent in recent years with the intensive surveil- unusual behavior, and the implications for conservation. lance necessary in conservation projects. In North America We suggest three possible functions for ingesting junk, the critically endangered California Condor has hatched which are not mutually exclusive. Firstly, as is often as- 17 chicks in the wild since the first breeding efforts of sumed, junk may be swallowed in the mistaken belief that reintroduced populations in California and northern Ari- it is a bone fragment. Condors and the larger vultures are zona (2001–2006). Of 10 nestlings hatched in the wild in unusual among birds of prey in that they feed mainly on California (2001–2005), only one survived to fledging the soft tissues (i.e., muscle and viscera) of large ungulate (Mee et al. 2007a). Seven of eight wild-hatched chicks in carcasses. Unlike some other birds of prey, which feed on California examined between 2002–2005 were found to small mammals or birds, they cannot consume their prey have consumed junk, and all nest sites contained this ma- whole. Bones are the primary source of calcium in the diet terial; six chicks had large quantities (30–204.5 g) of junk of birds of prey, but the large mammal carcasses on which in their guts, and three of these died in the nest area (Mee large vultures and condors feed have few bones small et al. 2007b). A fourth was later euthanized and two others enough for them to swallow, other than carpals, tarsals, were released back to the wild after 1.5–2.5 yr recovering at and phalanges. Their diet, if confined to soft tissues, may Los Angeles Zoo (U.S. Fish and Wildlife Service unpubl. therefore be deficient in calcium (Houston 1978). Adult data). This is also a common phenomenon in some Old birds probably can maintain calcium balance on such a di- World griffon vulture colonies. In Israel, there has been et, but, during the breeding season, females need to form heavy nestling mortality among Eurasian Griffons (Gyps eggshells and the chicks need higher calcium levels to mineralize their growing bones. The larger vultures have 1 Email address: [email protected] an unusually slow nestling growth rate, compared to other 236 SHORT COMMUNICATIONS VOL. 41, NO.3

cause of their long necks, condors and griffon vultures may find pellet ejection more difficult than do species with short esophagi. Those vulture species which consume large quantities of skin, such as the Old World Cinereous Vul- ture (Aegypius monachus) and Lappet-faced Vultures (Torgos tracheliotus) or the smaller New World Turkey Vulture (Cathartes aura) and Black Vulture (Coragyps atratus) are able to form large pellets regularly from the substantial quantities of hair they consume, in which smaller undigest- ed objects are embedded (Rea 1973, In˜igo Elias 1987). But vulture species such as condors and griffon vultures, which do not consume such large quantities of skin, may not always have sufficient material to form into functioning pellets, and in our experience do not produce pellets reg- ularly. When these vultures have small, undigested items lodged in their stomach they may deliberately seek other Figure 1. Junk (34 g) regurgitated by a Gyps fulvus nest- indigestible objects to swallow to enable them to accumu- ling in Armenia. Photo by Mike McGrady. late a sufficient volume of material for peristaltic action to eject it all as a pellet. This probably requires both material birds of their size, a growth strategy that may have evolved of sufficient mass and bulk against which the muscular as an adaptation to their low-calcium diet because it re- contractions of the esophagus can act, and sometimes also duces the daily calcium requirements of the chick (Hous- fibrous material to bind such junk together into a single ton 1978). Because of this low-calcium diet, vultures may functional pellet. Both vultures and condors apparently seek out small bones lying on the ground as alternative eat indigestible fibrous material such as grass, leaves, twigs, calcium sources, as is well known for many other bird spe- bark of shrubs, and hair, and such material can be found cies (see references in Ramsay and Houston 1999). Bone incorporated into their pellets together with solid objects can be digested readily in the acidic conditions of the (Koford 1953, Benson et al. 2004). The consumption of stomach (Houston and Copsey 1994). This need to find small, indigestible objects may therefore have been a be- calcium sources might account for condors’ and vultures’ havior that originally had clear adaptive value for condors consumption of pieces of white china, white PVC piping, and griffon vultures, and any naturally occurring junk plastic, glass, and similar white- or brown-colored junk in items swallowed would not normally have been life-threat- the mistaken belief that it is bone. However, it is perhaps ening, but would have assisted in pellet production. How- unlikely that this explanation alone can account for the ever, the situation has changed because humans have now consumption of metal bottle-tops, washers, electrical items, littered the environment with items that have sharp edges brightly colored or clear glass, ammunition casings, rub- which can lodge in, or even penetrate, the gut, and items ber, grass, sticks, and the other bizarre objects vultures which are toxic. These items probably are given to nest- regularly swallow (Collins et al. 2000, Ferro 2000, Benson lings unintentionally. When adults disgorge food from et al. 2004, Mee et al. 2007b), which could not be mistaken their crops into the mouths of the chicks, this transfer is for bone. indiscriminate; the bone fragments taken from the crops A second explanation may also be a consequence of of Cape Griffon chicks are not statistically different in size feeding on the soft tissues of large ungulate carcasses. It from those taken from the crops of adult birds (Benson et concerns the need to form pellets. No vertebrate gut con- al. 2004). But chicks might have weaker muscles in their tains an enzyme to digest keratin, so any keratin structure esophagus walls than do adults, and may not be able to that a bird swallows, including hair, horn, and hoof, will expel pellets as readily. This might explain the accumula- remain undigested once it reaches the stomach. All vul- tion of junk in the stomach of some chicks. In addition, tures will inadvertently eat some such keratin items, and because these species usually nest on rock ledges, chicks some species will consume more than others, depending have little opportunity to seek out fibrous indigestible ma- on the part of the carcass for which they are specialized. terial to help in the deliberate formation of a structured These will impede digestion if they are not ejected from pellet that can be expelled. This may be especially true for the stomach, and this is done through the production of nestling condors, usually confined to inaccessible cave pellets. In the stomach, pellets are formed from all mate- nests. rial that remains undigested by the acid and enzyme ac- A final possible explanation for the consumption of junk tion, and which is too large to pass through the sphincter is the quest for novel food items. We find captive condors into the small intestine. Pellets are expelled from the body, and vultures to be more inquisitive and to show greater largely by peristaltic action of the digestive tract up the exploratory behavior than other birds of prey. This is prob- esophagus (Duke et al. 1975). It is likely that single, small ably of adaptive value, because condors and the larger items cannot be easily expelled in this way. Further, be- vultures are virtually exclusively scavengers and do not kill SEPTEMBER 2007 SHORT COMMUNICATIONS 237 the large mammals on which they feed (Houston 2001). matically illustrated for the three formerly abundant spe- Relying on finding carcasses is a precarious existence. If cies of griffon vulture in southeastern Asia, which within carrion availability is low, birds may need to find alterna- a decade have all become critically endangered; popula- tive sources of energy to survive until a carcass becomes tion modelling has shown that apparently rare mortality available within range. Bone may be one such item, as the events caused by humans are sufficient to cause such a pop- collagen and fat content of bone provides a high energy ulation crash (Green et al. 2004). Just as the increased food of comparable calorific value to meat; the disadvan- mortality caused by long-line fishing seems to be causing tage is that bone is slow to digest (Houston and Copsey the decline of many albatross populations (Tuck et al. 1994). But when birds are food-stressed, they may consume 2001), so too chick mortality induced by anthropogenic any potential energy source. Many species of vultures do junk could be contributing to the worldwide decline of occasionally eat a wide range of apparently unusual items, vulture populations. Such mortality underscores the mag- such as tortoises, eggs, and insects, and the consumption nitude of human impact on the environment. It may be of some junk may be done because it has the potential to notable that the condors released in Arizona, in the rela- contain some digestible material that will release some tively pristine environment of the Grand Canyon, bring energy. Such a strategy, which in the past would have fewer junk items to nest sites and ingestion of this material had short-term survival value, may today be life-threaten- has not been a problem for the chicks there. In addition, ing. there are many published accounts from other bird species Captive birds could be used to test these ideas, but at which have consumed junk showing that this can result in present we have little data on this behavior. The widely toxicity from heavy metals, or endocrine disruption and believed assumption that these items are swallowed in mis- other physiological consequences from the ingestion of take for calcium sources would suggest that there might be plastics (Ryan et al. 1988, Tyler et al. 1998, Tanabe et al. a correlation with local geology. Birds living in areas with 2004). calcium-rich rocks might be expected to show this behav- Within the range of endangered vulture and condor ior less frequently than those living in calcium-poor re- species, wherever possible, the availability of junk items gions, but we know of no data to support this. If calcium should be minimized through effective garbage disposal shortage is the basis of this behavior, the problem may and efficient litter collection at tourist sites, army exercise have been exacerbated by humans. Mundy and Ledger areas, target shooting sites, and sport hunting areas. Public (1976) reported a high frequency of bone abnormalities awareness of this problem should be improved as well. In in Cape Griffon chicks. They suggested that in the areas addition, closure of problem sites to the public within where these birds feed, there may be a shortage of small some species’ ranges should be considered. We also sug- bone fragments because hyenas and lions have been extir- gest that future reintroductions should be targeted on pated from the ecosystem. These carnivores shatter large areas where such human impacts are relatively low and bones when they are feeding, and may leave small bone that an assessment needs to be made of the potential im- fragments behind that are then eaten by the vultures. If portance of this factor in the selection of release sites. such bone fragments are no longer available, vultures may take a greater proportion of junk in the search for calcium- ¿POR QUE´ LOS CO´ NDORES Y BUITRES COMEN BA- rich items. However, this idea has been disputed (Benson SURA?: IMPLICANCIAS PARA LA CONSERVACIO´ N et al. 2004). The provision of piles of small bone chips at vulture feeding stations has now become a common man- RESUMEN.—Estudios recientes sobre la conservacio´n del agement practice throughout the world, and this has not co´ndor Gymnogyps californianus y de los buitres del ge´nero led to any apparent reduction in junk-eating behavior in Gyps han mostrado que los objetos de origen humano, California Condors (but see Mee et al. 2007b). This sug- como fragmentos de vidrio, pueden ser una causa impor- gests that the eating of junk may have more than one un- tante de mortalidad de polluelos. El hecho de tragar este derlying cause. tipo de basura es ma´s comu´n en estas especies que en otras Whatever the evolutionary origin of this behavior, it is especies de aves rapaces. Aquı´ especulamos sobre tres po- clear that the swallowing of junk is a common behavior sibles funciones evolutivas no mutuamente exclusivas, que among griffon vultures and condors. It is also becoming podrı´an explicar este comportamiento inusual: (1) estos clear that much of this junk is made by humans and po- objetos son confundidos con fragmentos de hueso, (2) tentially lethal. At some sites, where intensive nest moni- e´stos pueden ayudar en la formacio´n de egagro´pilas y toring has been conducted, consumption of junk appears (3) e´stos son confundidos con pequen˜as fuentes de ener- to be a major factor in chick mortality. All the large con- gı´a. Sugerimos que este comportamiento evoluciono´ origi- dors and vultures have among the lowest rates of repro- nalmente debido a la naturaleza del alimento disponible duction for bird species, and their populations are only para estas especies, y porque e´ste tenı´a un valor para la stable when mortality is correspondingly low. Because of supervivencia. Sin embargo, la acumulacio´n de basura en their low rate of reproduction, large condors and vultures el ambiente, compuesta por objetos de origen humano cannot readily compensate for any increased mortality act- potencialmente letales, ha transformado este tipo de com- ing on adult or juvenile birds. Recently, this has been dra- portamiento en una nueva causa de mortalidad. Debido 238 SHORT COMMUNICATIONS VOL. 41, NO.3 a que la conservacio´n de estas especies es un asunto pre- IN˜ IGO ELIAS, E.E. 1987. Feeding habits and ingestion of ocupante, consideramos las implicancias de esfuerzos de synthetic products in a Black Vulture population from recuperacio´n en el campo. Chiapas, Mexico. Acta Zool. Mex. 9:1–15. [Traduccio´n del equipo editorial] KOFORD, C.B. 1953. The California Condor. Natl. Audubon Soc. Res. Rep. 4:1–154. CKNOWLEDGMENTS A KRUUK, H. 1967. Competition for food between vultures in We are grateful to Ofer Bahat, Alexander Gavashelish- East Africa. Ardea 55:171–193. vili, Mamikon Ghasabian, Martin Gilbert, and Bill Woodley MEE, A., J.A. HAMBER, AND J. SINCLAIR. 2007a. Low nest for their advice and information, and to Patrick Benson success in a reintroduced population of California Con- and an anonymous referee for their helpful comments on dors. Pages 163–184 in A. Mee and L.S. Hall [EDS.], the manuscript. AM thanks Lloyd Kiff and Mark Anderson California Condors in the 21st Century, Series in Orni- for help locating papers and the ZSSD for funding. thology, No. 2. LITERATURE CITED ———, B.A. RIDEOUT, J.A. HAMBER, J.N. TODD,G.AUSTIN, M. CLARK, AND M.P. WALLACE. 2007b. Junk ingestion AKAKI,C.AND G. DUKE. 1998. Egestion of chitin in pellets and nestling mortality in a reintroduced population of American Kestrels and Eastern Screech Owls. J. Rap- of California Condors Gymnogyps californianus. Bird Con- tor Res. 32:286–289. serv. Int. 17:1–13. BENSON, P.C., I. PLUG, AND J.C. DOBBS. 2004. An analysis of MUNDY, P.J. AND J.A. LEDGER. 1976. Griffon vultures, carni- bones and other materials collected by Cape Vultures vores and bones. S. Afr. J. Sci. 72:106–110. at the Kransberg and Blouberg colonies, Limpopo RAMSAY, S.L. AND D.C. HOUSTON. 1999. Do acid rain and province, South Africa. Ostrich 75:118–132. calcium supply limit eggshell formation for Blue Tits COLLINS, P.W., N.F.R. SNYDER, AND S.D. EMSLIE. 2000. Fau- (Parus caeruleus) in the U.K.? J. Zool. Lond. 247:121–125. nal remains in California Condor nest caves. Condor REA, A.M. 1973. Turkey Vulture casting pellets. Auk 102:222–227. 90:209–210. DUKE, G.E., A.A. JEGERS,G.LOFF, AND O.A. EVANSON. 1975. REDPATH, S.M., R. CLARKE,M.MADDERS, AND S.J. THIRGOOD. Gastric digestion in some raptors. Comp. Biochem. Phys. 2001. Assessing raptor diet: comparing pellets, prey re- 50:649–656. mains, and observational data at Hen Harrier nests. FEDUCCIA, A. 1996. The origin and evolution of birds. Yale Condor 103:184–188. Univ. Press, New Haven, CT U.S.A. RYAN, P.G., A.D. CONNELL, AND B.D. GARDNER. 1988. Plastic FERRO, M. 2000. Consumption of metal artifacts by Eur- ingestion and PCBs in seabirds: is there a relationship? asian Griffons at Gamla Nature Reserve, Israel. Vulture Mar. Pollut. Bull. 19:174–176. News 43:46–48. TANABE, S., M. WATANABE, T.B. MINH,T.KUNISUE,S.NAKA- GREEN, R.E., I. NEWTON,S.SHULTZ, A.A. CUNNINGHAM,M. NISHI,H.ONO, AND H. TANAKA. 2004. PCDD’s, PCDF’s GILBERT, D.J. PAIN, AND V. PRAKASH. 2004. Diclofenac and coplanar PCBs in albatross from the North Pacific poisoning as a cause of vulture populations declines and southern oceans: levels, patterns and toxicological across the Indian subcontinent. J. Appl. Ecol. 41:793– implications. Environ. Sci. Technol. 38:403–413. 800. TYLER, C.R., S. JOBLING, AND J.P. SUMPTER. 1998. Endocrine HERTEL, F. 1994. Diversity in body size and feeding mor- disruption in wildlife: a critical review of the evidence. phology within past and present vulture assemblages. Crit. Rev. Toxicol. 28:319–361. Ecology 75:1074–1084. TUCK, G.N., T. POLACHECK, J.P. CROXALL, AND H. WEIMERS- HOUSTON, D.C. 1978. The effects of food quality on breed- KIRCH. 2001. Modelling the impact of fishery by-catches ing strategy in griffon vultures. J. Zool. Lond. 186:175– on albatross populations. J. Appl. Ecol. 38:1182–1196. 184. YOM-TOV,Y.AND D. WOOL. 1997. Do the contents of Barn ———. 2001. Vultures and condors. Colin Baxter Ltd., Owl pellets accurately represent the proportion of prey Grantown on Spey, Scotland. species in the field? Condor 99:972–976. ——— AND J. COPSEY. 1994. Bone digestion and intestinal morphology of the Bearded Vulture. J. Raptor Res. Received 13 October 2006; accepted 9 March 2007 28:73–78. Associate Editor: Ian G. Warkentin