The Role of the Species Survival Plan in Maned Wolf Chrysocyon Brachyurus Conservation N

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International Zoo Yearbook

136 BEARS AND CANIDS

Int. Zoo Yb. (2010)44: 136-148 DOI:10.1111/j.l748-1090.2009.00093.x

The role of the Species Survival Plan in Maned wolf Chrysocyon brachyurus conservation N. SONGSASEN & M. D. RODDEN1 Smithsonian's National Zoological Park, Conservation & Research Center, 1500 Remount Road, Front Royal, Virginia 22630, USA E-mail: roddenm(a),si.edu

The Association of Zoos and Aquariums Maned Wolf Maned wolf may be extinct in Uruguay Species Survival Plan (MWSSP) was established almost (Dietz, 1985) with other populations increas- 25 years ago. The goals of the MWSSP are to (1) maintain a viable self-sustaining captive population in North Amer- ingly at risk as a result of habitat loss to ica, (2) enhance health and well-being of individuals living agriculture (Dietz, 1984; Rodden et al., in North American zoos and (3) promote conservation of 2004). It was estimated during the first Popu- this species through education and field-conservation lation and Habitat Viability Assessment initiatives. Since its inception, the MWSSP and member Workshop held in the Serra da Canastra institutions have supported studies on nutrition, medical management, behaviour and reproductive biology, and National Park (PNSC), Brazil in October published a husbandry manual, which serves as a guide 2005, that about 20 000 individuals remain for captive management of Maned wolves Chrysocyon in Brazil, the country believed to have the brachyurus in North and South American zoos. Further- most animals, with only a few thousand more, the MWSSP has provided funding for field studies aimed at identifying potential threats to wild populations living in the other range countries. in range countries, including Brazil, Bolivia and Argenti- Historical studbook records indicate that na, as well as for the first Population and Habitat Viability Maned wolves have been housed in zoologi- Assessment Workshop for this species. Finally, the cal institutions for more that 40 years. Eur- MWSSP has played an active role in promoting education opean zoos, including Frankfurt, Krefeld and and outreach efforts in both the United States and range countries. In this paper, we review and discuss the roles of Berlin, all in Germany, and Antwerp in the the MWSSP in ex situ and in situ conservation of the Near Netherlands began importing Maned wolves Threatened Maned wolf. from Brazil and Argentina in the 1960s (Dmoch, 2008). From 1965 to 1967, the first Key-words: captive breeding; field research; husbandry; maned wolf; South America; SSP. seven [4.3 (c?-?)] Maned wolves were imported from South America to several zoos in the United States (Dmoch, 2008). Partner- INTRODUCTION ships among North American and European The Maned wolf Chrysocyon brachyurus is a zoos facilitated exchanges between the two Neotropical canid that lives in habitats se- continents, and over the following 8 years, an verely compromised by agricultural develop- additional six (3.3) and five (3.2) animals ment. The species is native to the grasslands were imported to the United States from of South America (known as the Cerrado in South American and European zoos, respec- Brazil) and found exclusively in Brazil, Boli- tively These animals, plus several more re- via, Argentina, Peru and Paraguay (Dietz, cent imports from South America and 1984; Rodden et al., 2004). Although listed exchanges with European zoos, formed the as Near Threatened on the 2008 IUCN Red core-breeding group represented in the current List of Threatened Species (IUCN, 2008), the population of 80 (38.42) individuals

Corresponding author: Melissa D. Rodden, Smithsonian's National Zoological Park, Conservation & Research Center, 1500 Remount Road, Front Royal, VA 22630, USA. E-mail: [email protected]

Int. Zoo Yb. (2010) 44: 136-148. © 2010 The Authors. Journal compilation © 2010 The Zoological Society of London RhVIhW: MANb'D WOLF CONSERVATION AND SSI' 137 descended from 32 founders. The Association CAPTIVE-BREEDING PROGRAMME of Zoos and Aquariums (AZA) added the Maned wolf to its fledgling Species Survival The ultimate goal of the captive-breeding Plan (SSP) programme in 1985. The goals of programme is to maintain a healthy and the Maned Wolf SSP (MWSSP) are to (1) viable population of Maned wolves in zoos maintain a viable self-sustaining captive po- (Plate 1). The MWSSP is a cooperative pulation in North America, (2) enhance the management programme involving all 28 health and well-being of individuals living in North American zoos currently holding North American zoos and (3) promote con- Maned wolves. While there are no formal ties servation of this species through education between the MWSSP and similar pro- and field conservation initiatives. Since its grammes in Europe, such as the European inception, the MWSSP and its member insti- Endangered Species Programme, and other tutions have participated in or provided finan- regions of the world, exchanges of both cial or in-kind support to captive-management animals and information within the global studies of nutrition, medical management, zoo community has proved invaluable in behaviour and reproductive biology. More sustaining genetic diversity and increased recently, the MWSSP has provided funding our understanding of Maned wolf husbandry. for field studies conducted in range countries, The MWSSP is a committee-driven process including Brazil, Bolivia and Argentina. composed of a Species Coordinator and a Management Committee, comprising a small group of elected or appointed representatives from the participating institutions. In addition, experts in the fields of reproductive biology, veterinary medicine and pathology, nutrition, education and behaviour act as scientific advisors to assist the Management Committee in formulating in situ and ex situ research goals and projects. The Management Committee produces an annual Population Management Plan that is distributed to all holding institutions and posted on the AZA website (http://www.aza.org). Genetic and demographic analyses of studbook data using PM2000 (Pollak et al., 2005) provide the basis for determining population growth goals, and making breeding and transfer recommendations for each individual. The primary objective of this activity is to maximize the retention of genetic diversity and minimize inbreeding. Target population sizes, based on space surveys conducted at regular intervals, are determined for each species that falls within the purview of the AZA Canid & Hyaenid Taxon Advisory Group; the target population for Maned wolves is 100 animals. Between 2003 and 2007 the North American popula- Plate 1. Maned wolf Chrysocyon brachyurus at Smith- sonian's National Zoological Park, Washington, DC. tion remained close to 95 individuals through Jessie Cohen, National Zoological Park, Washington, restricting breeding to a specific number of DC pairings. By pairing animals with the rarest

Int. Zoo Yb. (2010) 44: 136-148. © 2010 The Authors. Journal compilation © 2010 The Zoological Society of London 138 BEARS AND CANIDS alleles (i.e. high Mean Kinship rank) and a guideline for management of this species in minimizing the inbreeding coefficients of off- captivity. The Manual was first published in spring, the population has maintained gene 1987, updated in 1995 and completely re- diversity around 0 • 93 and the mean inbreed- vised in 2007 (MWSSP, 2007). It has been ing coefficient (F) of c. 0 • 015. Inexplicably distributed to all holding institutions in North poor reproduction for the past 2 years has America and is posted on the AZA website. reduced the population to 80 animals, A Portuguese translation was sent to zoos although genetic parameters have not yet and government agencies in Brazil, and a been adversely affected. The Management Spanish translation, once completed, will be Committee has responded by increasing the made available to zoos and wildlife depart- number of pairings recommended to repro- ments in Spanish-speaking range countries. duce in 2009, in order to increase the popula- The Manual will continue to be updated as tion. Simultaneously, efforts are under way to new information becomes available. examine more closely reproductive hormone levels and the role that stress and/or diet may Nutrition and medical management be playing in recent reproductive failures. Supporting research into all aspects of In nature, the diet of Maned wolves as Maned wolf husbandry is another critical role identified by scat analysis is typical for a played by the MWSSP. Since its inception, generalist omnivore with c. 50% being plant the MWSSP, working closely with several materials and the rest being small mammals scientific advisors, has supported studies of [rodents, armadillos (Dasypodidae)], birds reproductive behaviour and physiology, nu- and insects (Dietz, 1984; Motta-Junior et al., trition and medical management. Most of the 1996; Bestelmeyer, 2000). It has been shown research is conducted by scientists affiliated that there are seasonal changes in the food with zoos in the MWSSP. Proposals, includ- habits of wild wolves. Small mammal re- ing budgets, are submitted to the Manage- mains are found more frequently in dry- ment Committee for review and approval. season scats, while fruit and insect remains The Committee prioritizes projects based on were more common in the wet season (Dietz, the needs of the programme and assists in 1984; Motta-Junior et al, 1996). However, funding through direct appeals to the the seeds of the fruit Tobeira' Solanum lyco- MWSSP zoos. Working with the AZA, the carpum, the main plant item consumed by MWSSP created a fund that is managed by Maned wolves in Brazil, are found in wolf the Dickerson Park Zoo (Springfield, MO, scat throughout the year. USA). Contributions from individual zoos Appropriate diet management is a key and from external grants are deposited into component for the health and well-being of the fund and utilized based on priorities wildlife maintained in zoos. Although the determined by the Management Committee. food habits of wild Maned wolves have been While only a few zoos are able to offer direct well characterized (Dietz, 1984; Motta-Junior funding to ex situ projects, virtually all zoos et al., 1996; Bestelmeyer, 2000), formulation in the programme provide support; for exam- of optimal diets for captive Maned wolves ple, by providing samples or collecting beha- has been a major challenge for North Amer- vioural data or management information ican zoos, possibly owing to the unique requested by the Principal Investigators of physiology of the species and susceptibility approved projects. The majority of funding to cystinuria (Bush, 1980; Bovee et al., for captive-management projects, totalling 1981). Maned wolves have a very sensitive over US SI 00 000, has been obtained through gastrointestinal tract and often respond to external grants awarded to MWSSP-affiliated minor management changes (e.g. diet manip- scientists. Findings from these studies have ulation) with diarrhoea and poor body condi- been summarized and formulated into the tion (Bush, 1980). Diets fed to captive Maned Maned Wolf Husbandry Manual, serving as wolves were originally based on formulations

Int. Zoo Yb. (2010) 44: 136-148. © 2010 The Authors. Journal compilation © 2010 The Zoological Society of London RhVIhW: MANb'D WOLF CONSERVATION AND SSI' 139 for Domestic dogs Canis lupus familiaris. linkage between long-term feeding of the However, it has been shown that there is new diet and poor reproduction prompted species specificity in digestibility (Childs- the MWSSP to err on the side of caution and Sanford & Angel, 2006). Specifically, Maned discontinue feeding the new diet pending wolves have lower digestibility of dry matter, further investigation. US zoos have returned energy and several minerals, including cop- to feeding dog chow-based diets supplemen- per, magnesium, iron and sodium (Childs- ted with a variety of fruits and vegetables as Sanford & Angel, 2006), than Domestic well as small amounts of whole prey items. dogs. Thus, diets formulated for the latter Maned wolves fed these diets are generally in may not be completely appropriate for Maned good health (15 year life span on average). wolves, emphasizing the need for additional However, identifying the optimal diet for research to develop a diet specifically for the captive Maned wolves remains a high priority Maned wolf. for the MWSSP. A detailed survey of all diets The Maned wolf is predisposed to cysti- being fed in US zoos was carried out late in nuria, a metabolic disorder that results in the 2006. The survey collected information about urinary excretion of the amino acid cystine all components of the diet, body weights, (Bovee et al., 1981). It has been shown that current medical conditions and medications, cystinuria occurs in both wild and captive urine pH and faecal consistency scores. No individuals (Bovee et al., 1981). Although correlations have yet been found between the clinical significance of cystinuria for wild diet, health and reproductive success, but Maned wolves is unclear, this metabolic dis- analysis of the data is still under way. One order has posed a considerable health threat finding was very clear: out of the 24 zoos to individuals in captivity. The clinical signs responding to the survey, 15 different brands of cystinuria include urinary straining, fre- of chow were being offered and there was a quent urination and obstruction of the urethra great deal of variation in the amount and type by calculi that can lead to obstruction and of vegetable, fruit and whole-prey supple- secondary rupture of the urinary bladder and ments fed (M. Rodden, unpubl. data). death (Bovee et al., 1981). It has been Standardizing the nutrients we offer the suggested that the occurrence of cystinuria in Maned wolves in our care is a priority for captive Maned wolves is related to a diet high the MWSSP. As a first step in that direction, in animal protein, such as the carnivore diets the MWSSP has recently initiated a new originally fed to this species. High-protein project to characterize circulating nutritional diets tend to increase urine acidity that in turn profiles in captive animals. This pilot project increases the insolubility of cystine, resulting aims to (1) determine baseline data on serum in the formation of calculi in the kidneys and and plasma nutritional parameters, including bladder. In response to the increasing inci- amino acids, fatty acids, vitamins A and E, dence of clinical illness related to cystinuria, various minerals, cholesterol and triglycer- efforts were made to formulate a Maned wolf ides, and (2) correlate circulating nutritional diet that reduced and prevented the disease profiles with demographic variables, such as (Boniface, 1998). The resulting diet, having age and gender, in addition to health status low cystine content and high fibre, was and diet composition. Once parameters in shown to reduce the concentration of urinary captive Maned wolves have been character- cystine and total nitrogen significantly. Sub- ized, we hope to compare the results with data sequent modification of this formula in- obtained from wild Maned wolves through creased the proportion of protein derived collaborations with field researchers in range from plant materials and lowered the amount countries and use the information to formulate of sodium in the diet (Childs-Sanford, 2005). a standard diet that will better meet the Maned This modified formula has been shown to wolf's unique nutritional requirements. The increase the urinary pH in Maned wolves. MWSSP also hopes to initiate a dialog with However, in 2002 concerns about a possible colleagues in other regions of the world in

Int. Zoo Yb. (2010) 44: 136-148. © 2010 The Authors. Journal compilation © 2010 The Zoological Society of London 140 BEARS AND CANIDS order to compare diets and health concerns last several minutes (Rodden et al, 1996, throughout the global captive population. 2004). There are no data on the precise onset of sexual maturity. However, analysis of the 2007 Reproductive biology and behaviours International Studbook for the Maned Wolf Because reproduction is the essence of spe- using PM2000 (Pollak et al, 2005; Dmoch, cies survival, the MWSSP has promoted 2008) shows that both sexes can reproduce significant efforts into studies aimed at char- before 2 years of age, although rarely. Bitches acterizing reproductive physiology, determin- can produce pups at 10-12 years of age but ing the cause of poor reproductive success in this is uncommon. However, for both sexes, captive individuals. In addition, these studies the preponderance of breeding occurs from 3 have laid the groundwork for the develop- to 8 years of age, an interval generally consid- ment of assisted-reproduction techniques ered prime for reproduction. (e.g. induction of oestrus, semen cryopreser- Parturition in captivity peaks in June and vation and artificial insemination), which will December in South and North America, re- provide zoos with another tool for genetic spectively (Maia & Gouveia, 2002). Litter management of zoo populations. size ranges from one to seven pups (mean Behavioural field studies of primarily noc- SEM, 2-6 ±0-2) following a c.65day gesta- turnal, solitary and secretive animals that tion (Maia & Gouveia, 2002). Neonatal range over large areas can be extremely mortality rates in situ are not known but difficult, thus zoos provide an extraordinary historical data from captive records indicates opportunity to increase our understanding of 53% of pups are lost in the first year, with reproductive behaviour. The Maned wolf is almost 78% of the deaths occurring in the first monoestrus with a well-known and distinc- 30 days (Maia & Gouveia, 2002). Pups re- tive 3-5 month breeding season in captivity, main in the den for the first 4 weeks. Nursing occurring from April to June in the southern bouts begin to decline after the first month, hemisphere and October to February in North when pups begin consuming solids regurgi- America and Europe (Maia & Gouveia, tated by the parents (Brady & Ditton, 1979; 2002). Pro-oestrus lasts for c. 2 weeks and is Rodden et al, 2004), and weaning is com- characterized by vaginal swelling and secre- pleted by around 15 weeks. PM2000 analysis tions (Velloso et al, 1998). The MWSSP (Pollak et al, 2005) indicates the maximum sponsored a long-term study of Maned wolf life span for captive Maned wolves is 16- social behaviour that involved standardized 17 years, although the mortality rate begins to data collected by zoo staff and trained volun- increase significantly by 10 years of age. teers from 52 pairs housed at 17 zoos in the Patterns of reproductive hormones in the programme over seven breeding seasons. The Maned wolf, as measured by radio- published results describe breeding beha- immunoassays and enzyme immunoassay, viours and present a technique for utilizing reveal that profiles of gonadal hormones in $ discriminant function analysis to help assess Maned wolves are similar to those of Domes- whether a pair has bred and, further, whether tic dogs, especially during the preovulatory a $ is pregnant based on behavioural mea- period (Velloso et al, 1998; Songsasen et al, surements (Rodden et al, 1996). The amount 2006). Oestrogen concentration gradually in- of time a pair spends in close proximity creases beginning about 2 weeks before increases significantly during the oestrous per- breeding and declines to baseline on the day iod, which lasts from one to 10 days (Rodden of lordosis and copulation. Progestins steadily et al, 1996). Courtship is characterized by rise during late pro-oestrus and throughout frequent approaches, mutual anogenital inves- oestrus and remain elevated throughout the tigation and playful interactions. Mounting pregnant or non-pregnant luteal phase (Vello- may occur frequently during oestrus. Success- so etal, 1998; Songsasen etal, 2006). When ful breeding includes a copulatory tie that may sexual behaviours are correlated with gonadal

Int. Zoo Yb. (2010) 44: 136-148. © 2010 The Authors. Journal compilation © 2010 The Zoological Society of London RhVIhW: MANb'D WOLF CONSERVATION AND SSI' 141 hormone profiles, copulatory ties are observed born over 1980-1998 survived to 1 year of as early as 2 days before or 9 days after the age. They further stated that in 1982-1998 oestrogen peak (Velloso et al., 1998; Songsa- 77 • 7% of pup deaths occurred in the first sen et al., 2006). Non-pregnant $$ excrete 30 days, of which 88-1% were classified as overall lower concentrations of progestins 'parental incompetence' (Maia & Gouveia, than their pregnant counterparts (Velloso 2002). Thus far, the cause of neonatal mortal- et al., 1998; Songsasen et al., 2006). There is ity in this species has not been fully eluci- evidence suggesting that $ wolves may play a dated, although it has been hypothesized that role in oestrus induction and/or ovulation in stress associated with suboptimal manage- conspecific $? (Songsasen et al., 2006). ment is a contributing factor to low reproduc- Seasonally clearly affects semen produc- tive success in Maned wolves. It has recently tion. Analysis of semen samples collected at been demonstrated that dams experiencing 4-8 week intervals during two breeding sea- neonatal deaths produced less progesterone sons in North America (September through during the second half of gestation compared March) reveals a definitive temporal change with $$ successfully rearing young (Songsa- in sperm concentration throughout the breed- sen et al., 2006). Retrospective evaluations ing season (N. Songsasen, unpubl. data). Se- also demonstrated that wolves losing pups men samples contain low sperm-cell numbers produced higher faecal corticoid metabolite in November, and a peak in cell concentration concentrations during the periovulatory inter- in December, followed by an immediate val than those that successfully raised their decline. Analysis of faecal testosterone meta- young (N. Songsasen, unpubl. data). The bolites shows a positive correlation between Maned Wolf Husbandry Manual recommends testosterone concentration and semen produc- minimizing potential stress during gestation tion (N. Songsasen, unpubl. data). and pup rearing by providing multiple den When data are analysed on the basis of sites to breeding pairs and installing video reproductive history, j*j* of proven fertility cameras so that pregnant $$ can be closely (n = 6) have higher (P< 0 • 05) proportions of monitored (MWSSP, 2007). structurally normal sperm than unproven Historically, zoos often removed a j* be- counterparts in = 3). With one exception fore birth to avoid pup mortality associated (seminal volume), there also is a strong with the aggression of a sire towards his tendency for other semen characteristics to young. However, it has been shown that the be higher in proven wolves than in unproven presence of the sire increases pup survival to individuals but the difference is not signifi- 6 months of age (Bestelmeyer, 2000; see also cant (f >0 05), probably owing to small Veado, 1997, 2005) partly owing to de- sample size (D. Wildt, C. Platz & M. Bush, creased aggression of dams to pups. Dams unpubl. data). provide the majority of care while pups are in Reproductive success of Maned wolves the den; however, the rate at which sires housed in US zoos is relatively poor. During interact with pups significantly increases the past 5 years, the North American popula- when the young emerge from the den (Bes- tion has declined 20% (from 100 to 80 telmeyer, 2000). Based on this study, the individuals), mainly as a result of the failure MWSSP currently recommends leaving the of paired individuals to reproduce and rear breeding pair housed together during gesta- pups successfully. From 1996 through 2007, tion and pup rearing (MWSSP, 2007). only 38% of 166 recommended breeding pairs produced pups, with 50% of pregnant Zoo education $$ losing neonates within a few days of birth. Neonatal mortality has been a global issue for Educating zoo visitors about the plight of Maned wolves historically. In a review of the threatened species and habitats is a critically international studbook data, Maia & Gouveia important role played by zoological institutions (2002) reported that only 44% of 1532 pups throughout the world. Several years ago, the

MWSSP developed an Education Bulletin for by Rumiz & Sainz (2002) at 118 breeding use in zoo education programmes for school pairs fragmented among six isolated savannas children. The Bulletin summarizes Maned wolf within 3600 km2 of suitable habitat in the natural history and describes the threats facing Park (one-quarter of the area of the Park). wild populations and habitats. It also includes However, data from radio-telemetry suggests an activity page for recording behavioural that the number of breeding pairs is probably observations. The Bulletin has been translated only about 30 (L. Emmons, pers. comm.). into Portuguese and Spanish and several hun- The Park is adjacent to the Brazilian states of dred copies have been distributed to zoos and Rondonia and Mato Grosso, and is diverse in wildlife parks in range countries. habitat characteristics consisting of high- ground humid forests, flooded and riverside IN SITU CONSERVATION forest to dry forests, high plains and marshes. Because of its vast protected area and pristine Although the original goal of the MWSSP state, PNNKM is a United Nations Educa- was to maintain a viable and healthy popula- tional, Scientific and Cultural Organization tion of Maned wolves in North American World Heritage Site. In comparison to other zoos, the SSP has become increasingly in- ecosystems in South America that are being volved in field conservation initiatives in destroyed at an accelerated rate, the majority range countries. Recent projects include ecol- of this Park remains untouched by human ogy and health studies conducted in the Noel activities (http://www.discoveringbolivia.com). Kempff Mercado National Park (PNNKM), The MWSSP has provided support to a Bolivia, and the PNSC, Brazil, an initial long-term ecological study of mammal com- examination of genetic diversity in three munities in PNNKM headed by Dr Louise range countries, as well as education and Emmons, Smithsonian's National Museum of outreach efforts carried out in north-eastern Natural History. The specific objectives of Argentina. Furthermore, the MWSSP played this multidisciplinary project are to (1) gen- an instrumental role in raising funds for the erate ecological information of wolves living first Maned Wolf Population and Habitat in the PNNKM, (2) determine genetic diver- Viability Assessment workshop, held in the sity of individual living in this region and (3) PNSC, Brazil, in October 2005. The findings, evaluate the potential of diseases transmitted recommendations and action plans resulting from local Domestic dogs to Maned wolves. from the workshop have been published in Ecological analysis showed that seasonal- Portuguese, English and Spanish (de Paula ly influenced the movement and habitat use et at, 2008). Field collaborators submit re- of Maned wolves in this region (L. Emmons, search proposals to the Management Com- pers. comm.). However, the most alarming mittee for review and approval, in much the result of this study was evidence of a sig- same way as for ex situ projects. Over nificant decline in the Maned wolf prey base US$20 000 has been contributed by c. 25% of small rodents within the study savanna of the zoos in the programme toward in situ (Emmons, 2009). The effects of fluctuations conservation efforts since 2003, and close to in prey availability on the area's Maned wolf half the zoos in the MWSSP donated population are currently being analysed. c. US$9000 to support the PHVA in 2005. To date, health analyses have been con- The majority of support for in situ projects, ducted on 11 Maned wolves. All wolves tested c. US$140 000, has been obtained through positive to adenovirus, with the majority ex- external grants awarded to zoo-affiliated hibiting antibodies against Dirofilaria immitis scientists. (i.e. heartworm), Toxoplasma gondii, Ehrli- chia canis, Borrelia burgdorferi and Rickettsia PNNKM, Bolivia rickettsii (Deem et ah, 2008). In addition, Bolivia's PNNKM hosts one of the largest several individuals had antibodies against ra- protected Maned wolf populations, estimated bies, canine distemper, canine parvovirus and

Int. Zoo Yb. (2010) 44: 136-148. © 2010 The Authors. Journal compilation © 2010 The Zoological Society of London RhVIhW: MANb'D WOLF CONSERVATION AND SSI' 143 herpes virus (Deem et al., 2008). Serological among transitional rocky fields, with the analysis of Domestic dogs living around Park remaining being seasonal, tropical forest borders showed that the majority of dogs had (Dietz, 1984). antibodies against the same infectious diseases A collaborative project including scientists found in the Maned wolf population (Bronson from Brazilian universities, governmental et al., 2007), suggesting that these pathogens [National Research Center for Conservation were directly or indirectly transmitted to of Natural Predators (CENAP), ICM-Bio] wolves by dogs. Findings from this study and non-governmental (Institute for Conser- demonstrate that despite the isolated and pris- vation of Neotropical Carnivores) agencies, tine location of the Park, disease exposure and the Smithsonian's National Zoological from domestic animals may be a significant Park was initiated in 2004 with the main cause of morbidity or mortality (Deem & objective of determining the influence of hu- Emmons, 2005; Bronson et al., 2007; Deem man disturbance on wild Maned wolves liv- et al., 2008). Based on these findings, the ing in the PNSC and the surrounding areas. investigators have recommended that Park The project involves longitudinal monitoring managers develop vaccination campaigns of the ecology, behaviour, health and repro- against rabies and distemper virus in Domestic duction of large numbers of wolves (43 dogs (Deem et al., 2008). Furthermore, with individuals have been captured and radio- support from the MWSSP, the researchers collared since 2004) living in low versus high have produced and disseminated posters de- human-activity areas. In addition, investiga- scribing the importance of a pet vaccination tors are evaluating the impact of domesticated programme throughout the region. animals, especially Domestic dogs, on the health of the carnivore community, in parti- cular Maned wolves. Finally, an education PNSC, Brazil and outreach programme has been developed Within the Brazilian Cerrado, the PNSC is to target misperceptions of local communities one of the habitats maintaining the highest about the species and to reduce human-wolf density of Maned wolves in the country conflict (Songsasen & de Paula, 2007). Be- (IBAMA, 2004). The Park is located in the cause the Cerrado habitat has been increas- state of Minas Gerais in south-eastern Brazil, ingly utilized by humans, findings generated encompassing 2000km; 715 2km are from this study will not only improve our regulated and managed by Chico Mendes understanding of anthropogenic threats to Institute of Biodiversity Conservation (ICM- Maned wolves living in the Serra da Canastra Bio), and the remainder is privately held. In region but also can be applied to the develop- contrast to the PNNKM where the majority of ment of wildlife management plans through- the habitat remains untouched by humans, the out the Cerrado ecosystem. effects of prior human habitation and more It is estimated that 80 wolves currently live recent eco-tourism are visible throughout inside the national Park (Songsasen & de PNSC. The area adjacent to the Park bound- Paula, 2007). Wolves living in this region ary comprises small ranches (1 km or less), have overlapping home ranges, especially all of which have undergone extensive habitat those living inside the Park and around the alterations. Agricultural activities range from Park border. This ecological characteristic is subsistence farming to large coffee and corn different from that described by Dietz (1984) plantations. The Park comprises hills and and is probably the result of greater food ridges that rise abruptly from surrounding availability and less competition for suitable agriculture lands to elevations of nearly habitat that exists in the Park today compared 1500m and descend into valleys of c. 800 m. with the late 1970s. When Dietz conducted Approximately half of the Park is grassland his study from 1978 to 1980, PNSC was only with another 35% consisting of typical and a 'paper park'; people and livestock were diverse Cerrado vegetation interspersed commonly found living inside the Park. In

1979 the Brazilian Environmental Agency, loss), road mortality, the potential for infec- after strongly encouraging farmers to leave tious diseases spread by Domestic dogs and the protected area, began managing Canastra persecution resulting from widely held super- as a national park. Although development on stitions and beliefs, are the primary threats the periphery of the Park has been increasing, facing Maned wolves in Argentina. Field a decline in human pressure inside the Park studies have focused on determining popula- has increased its capacity to maintain wolves. tion distribution and density, and habitat use Notably, there is significantly less home- in relation to the other carnivores in the range overlap for wolves living outside the region. Initial results indicate that Maned Park boundaries than for those living within wolves show a preference for open grassland the Park. Landscape analysis using geo- habitats and are also utilizing perturbed areas; graphic information system has revealed that for example, cattle ranches (Soler & Caren- wolves living in cultivated areas avoid tended ton, 2008). Direct competition with other fields and appear to forage and use the carnivores has not been observed; however, remaining natural habitat fragments (Songsa- scat analysis reveals that Maned wolves, sen & de Paula, 2007). Crab-eating fox Cerdocyon thous and Pam- Although ecological studies may suggest pas fox Lycalopex gymnocercus (Pseudalo- that Maned wolves in the Serra da Canastra pex gymnocercus) consume many of the same area are able to exist in disturbed habitats, the prey species (Soler & Carenton, 2008). health analysis suggested that direct or indir- Educating the local people about Maned ect disturbance by humans and domestic wolves and other endemic carnivores and species may impact the well-being of Maned involving them directly in the field project is wolves. Haematology and blood biochemis- a significant component of current conserva- tries differed among animals living inside tion efforts in Argentina (Soler, 2008). Ex- versus outside the Park boundaries (May tensive surveys of farmers and ranchers have et ah, 2009). Specifically, erythrocyte count provided valuable information about the dis- and serum cholinesterase were lower in tribution of the species and also about peo- wolves living inside the Park than in those ple's attitudes towards Maned wolves and living around Park borders and on surround- other carnivores. Education programmes ing farms. Furthermore, preliminary hormo- aimed at changing negative perceptions of nal analysis of faecal samples revealed that carnivores and increasing appreciation of the wolves living on surrounding farmlands ex- unique role carnivores play in maintaining creted higher corticoid concentrations in biodiversity have been developed and pre- faeces compared with wolves living within sented to school children throughout the the Park (K. Spercoski, unpubl. data). Based region, utilizing dramatizations, puppet on these findings, it was suggested that inter- shows, presentations and other educational action with humans and domestic species, tools (Soler, 2008). Support from the and a lack of sufficient resources resulting MWSSP enabled the project coordinators to from habitat alteration, may contribute to print and distribute posters describing the increased levels of stress experienced by fallacy of some of the negative local folklore wolves living in disturbed areas. surrounding the Maned wolf.

North-eastern Argentina Genetic diversity It is estimated that c. 1000 Maned wolves The MWSSP supplied partial funding for a inhabit the grasslands (Chaco) of north- collaborative pilot study aimed at providing eastern Argentina, although the population is insight into the evolutionary history of this thought to be in decline (Soler & Carenton, species in South America in order to under- 2008). As in other areas of the range of the stand better the amount and patterns of gene species, conflicts with people (e.g. habitat flow and diversity between populations in

Int. Zoo Yb. (2010) 44: 136-148. © 2010 The Authors. Journal compilation © 2010 The Zoological Society of London RhVIhW: MANb'D WOLF CONSERVATION AND SSI' 145 different areas of the geographic range. Mi- funded by the MWSSP, Busch Garden Con- tochondria! DNA (mtDNA) analysis of both servation Fund, US Fish and Wildlife Ser- control region (D-loop) and cytochrome b vice, Wild Dog Foundation, ICM-Bio and the sequences was used to characterize the genet- United National Development Program. ic variability of 89 samples obtained in Boli- There were 45 participants from Argentina via and Argentina in addition to samples (7), Brazil (30), Paraguay (3), Uruguay (1) provided by captive animals of known Brazi- and the United States (4), with six facilitators lian origin (Franco Berriel, 2005). The sam- from the International Union for Conserva- ples were primarily faeces but also included tion of Nature (IUCN) Species Survival blood, hair and bone. Overall, gene diversity Commission (SSC) Conservation Breeding was quite low, as only seven different haplo- Specialist Group. The goal of this workshop types (haplotypes A-G) were found in the was to bring together wildlife biologists, rapidly-evolving D-loop region and two in educators, captive-breeding specialists, the more slowly evolving cytochrome b re- governmental agencies and wildlife non- gion (Franco Berriel, 2005). In the control governmental organizations from range coun- region, only one (haplotype B) was found in tries systematically to gather information re- samples from all three geographic areas (Ar- garding Maned wolf ecology, reproduction, gentina, Bolivia and Brazil) (Franco Berriel, social organization, health and possible threats. 2005). The most common haplotype (D) was During the 3 day workshop, issues includ- found in Bolivian and Brazilian samples, but ing (1) threats and habitat management, (2) not in Argentina, and the remaining five were species status and distribution, (3) sociology each unique to one of the three geographic and environmental education, and (4) ex situ areas, although all were found in low propor- conservation were discussed. Estimations of tions. The mtDNA analysis combined with the Maned wolf population and an assess- subsequent microsatellite analysis of a subset ment of extinction risk for each range coun- of samples indicates that the Argentinean try were also conducted using VORTEX population is significantly differentiated from simulation models (Lacy, 2000). It should the Bolivian animals and is more closely be noted that data were not available for the associated with the Brazilian population populations in Bolivia and Uruguay; thus (Franco Berriel, 2005). The small sample size simulation modelling was not performed for precludes any definitive conclusions but, gen- these regions. erally, the results indicate that population size It was estimated that there are ten popula- has fluctuated over history, possibly as a tions of Maned wolves (600-800 individuals) result of climate change affecting the grass- remaining in Argentina. The main threat to land habitats and more recently from conver- Argentinean Maned wolf populations is per- sion of grasslands for agricultural use (Franco secution associated with harvesting of body Berriel, 2005). Additional samples collected parts and human conflict. Therefore, educa- from more widely distributed areas of the tion campaigns, in collaboration with govern- species' range are needed to further elucidate mental agencies, aimed at reducing genetic diversity and the degree of phyloge- persecution rate, are considered the highest netic partitioning that exists in the remaining priority in this region. Among the ten popula- wild populations. tions, only one population in the Formosa region of north-east Argentina was identified Population and habitat viability as potentially viable with a low probability of extinction over the next 100 years; this popu- assessment workshop lation was designated as the highest conser- The first Maned Wolf Population and Habitat vation priority. Viability Assessment workshop was held in For Brazil, it was estimated that there are October 2005 at the PNSC, Brazil. The work- nine populations totalling c. 20 000 wolves in shop was organized by CENAP/ICM-Bio and this country. The main threats to Maned

Int. Zoo Yb. (2010) 44: 136-148. © 2010 The Authors. Journal compilation © 2010 The Zoological Society of London 146 BEARS AND CANIDS wolves in Brazil include habitat loss and The MWSSP is one of 113 SSP pro- mortality associated with road kill and human grammes established by the AZA since conflict. Because of the large number of 1980. During the past two decades, the Maned wolves in this country, there is low focus of the MWSSP has expanded from probability of extinction over the next solely engaging in ex situ conservation 100 years, although the persistence in popula- (breeding and conducting scientific studies tion threats may lead to local extinction in to improve health and well-being of captive some regions. Therefore, conservation prio- individuals) to integrating in situ conserva- rities in Brazil should include preservation tion and education projects into the Action and restoration of suitable habitat and reduc- Plan. Through the support of the MWSSP, tion of human-Maned wolf conflict. scientists both in the United States and range Eight hundred Maned wolves are esti- countries have generated important informa- mated to exist in four suitable habitats in tion contributing to our understanding of the Paraguay. Very little is known about the biology of Maned wolves (including ecology, status and distribution of Maned wolves in diet, behaviour, reproductive physiology, sus- this country, and further research is required ceptibility to diseases) and how this species to estimate the population size accurately. responds to environmental changes related to The main threats to Maned wolves in Para- human encroachment into the grassland habi- guay are mortality caused by road kill and tats. However, several challenges remain, persecution. including (1) formulating a suitable diet for Regarding ex situ conservation, poor re- Maned wolves maintained in North American production in captivity is the main concern in zoos, (2) improving the reproductive fitness the United States, Argentina and Paraguay, of captive individuals, (3) evaluating the while surplus animals and overcrowding re- significance of disease threats to wild popula- sulting from large influxes of confiscated tions and (4) promoting and supporting con- individuals are the most important issues in servation efforts in range countries to Brazil. Thus, conservation priorities for zoo preserve habitat and reduce human-wolf con- populations include research addressing poor flict. The MWSSP is committed to the pre- reproductive success in captivity and working servation of this unique canid and the with Brazilian agencies to (1) provide facil- critically threatened grasslands of South ities to accommodate confiscated species and America, and will continue to collaborate (2) control the number of wild wolves enter- with scientists and wildlife educators to en- ing zoos by increasing efforts to reduce hu- sure the existence of the species long into the man-wolf conflict (see also Vanstreels & future. Pessutti, 2010).

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