martens, sables, and fishers

BIOLOGY AND CONSERVATION OF

MARTENS, SABLES, AND FISHERS A New Synthesis EDITED BY

Keith B. Aubry, William J. Zielinski, Martin G. Raphael, Gilbert Proulx, and Steven W. Buskirk This document may not be reproduced or distributed in any form without permission in writing from Cornell University Press

Copyright © 2012 by Cornell University except for chapters 4, 15, and 19 and portions of chapters 3, 10, 12, 13, 16, and 17, which were written by federal employees and cannot be copyrighted. All rights reserved. Except for brief quotations in a review, this book, or parts thereof, must not be reproduced in any form without permission in writing from the publisher. For information, address Cornell University Press, Sage House, 512 East State Street, Ithaca, New York 14850. First published 2012 by Cornell University Press Printed in the United States of America Library of Congress Cataloging-in-Publication Data Biology and conservation of martens, sables, and fishers : a new synthesis / edited by Keith B. Aubry … [et al.]. p. cm. Includes bibliographical references and index. ISBN 978-0-8014-5088-4 (cloth : alk. paper) 1. Martes. 2. Martes—Ecology. 3. Wildlife conservation. I. Aubry, Keith Baker. QL737.C25B516 2012 599.76'65—dc23 2012003137 Cornell University Press strives to use environmentally responsible suppliers and materials to the fullest extent possible in the publishing of its books. Such materials include vegetable-based, low-VOC inks and acid-free papers that are recycled, totally chlorine-free, or partly composed of nonwood fibers. For further information, visit our website at www.cornellpress.cornell.edu. Cloth printing

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7 Pathogens and Parasites of Martes Species Management and Conservation Implications MOURAD W. GABRIEL, GRETA M. WENGERT, AND RICHARD N. BROWN

ABSTRACT The impacts of pathogens and parasites and their associated diseases are integral to understanding potential threats to Martes populations. In this chapter, we summarize the known relations of pathogens and parasites to their Martes hosts and review the epidemiology and life cycles of 4 selected pathogens that may be particularly important to Martes species, including rabies viruses, canine distemper virus, parvoviruses, and Toxoplasma gondii. We also address management options for dealing with disease issues and their implications for conservation efforts for Martes species. These implications include disease risk in reintroduction programs, handling of potentially diseased individuals, and protocols for disease assessment and prevention. Finally, we suggest future directions and roles of wildlife disease ecology in the research and management of Martes species. Our overall goal is to provide information that will be helpful for wildlife biologists, wildlife veterinarians, and others concerned about the biology, management, and conservation of Martes species.

Introduction

Despite the extensive and growing body of ecological research conducted on Martes species, relatively little is known about their infections by pathogens or infestations by parasites. The threat of disease is integral to conservation programs aimed at protecting members of this genus because of the insular nature of many Martes species and concern over the long-term stability of small Martes populations (Woodroffe 1999; Broekhuizen 2006; Saeki 2006). First, we will defi ne some terms frequently used in this chapter but possibly used in a somewhat different sense by other authors. A pathogen is any 138

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disease-causing organism, and a parasite is an organism that lives in or on the host tissue at the expense of its host (Hudson et al. 2004; Collinge and Ray 2006). Disease is commonly defi ned as an impairment that leads to a deleterious change in a host’s body condition, which may or may not result in death (Wobeser 2006); this defi nition is broad but generally refers to some kind of pathology. In many cases, identifying the point when a pathogen or parasite causes disease is difficult, primarily because of the scarcity of studies that have proven a causal relation between the organism and insult through experiment (i.e., Koch’s postulates) or of pathological investigations of mortalities. The study of the occurrence of disease in populations is referred to as disease ecology or epidemiology, whereby a pathogen can either be enzootic (occurring at an expected, constant, or low rate) or epizootic (occurring at an unexpected rate or pattern; Wobeser 2007). Potential Effects of Selected Pathogens

Parasites and disease are often lumped into a single category of agents that cause adverse effects on populations. Such generalizations should be avoided, however, because they can create misunderstandings that may lead to poor management decisions. In fact, most parasites cause minimal or only mild signs of disease (Ewald 1995; Lafferty 2008). The remainder commonly cause considerable morbidity or death of individuals, but impacts on host populations can be subtle, and interactions may be complicated; even so, such parasites may influence the evolution of host populations as well as the dynamics of communities and food webs (Collinge et al. 2008; Lafferty 2008). Parasites also have the potential to cause severe diseases and may limit population numbers. These types of effects are usually most profound in small, insular populations, or when diseases act synergistically with other populationlimiting factors (e.g., habitat loss or degradation, predation, competition, nutritional stress), or when exotic pathogens are introduced to a population (Daszak et al. 2001; Fenton and Pedersen 2005; Lafferty 2008). Consideration of parasites that can cause severe disease and have the potential to limit populations should be included in conservation planning (Murray et al. 1999; Pedersen et al. 2007; Roemer et al. 2009). The virulence of parasitic organisms varies among host species and populations, among parasite populations and strains, and through time. Evolutionary pressures may result in a reduction of parasite virulence when, on average, host morbidity or mortality reduces parasite fitness. The severity of disease and pathogen propagation increases, however, as a result of gains in virulence (Ewald 1995; McCarthy et al. 2007; Lafferty 2008). Although it is tempting to encourage managers and conservationists to consider all possible hostparasite interactions, limited resources typically dictate that only the most significant of interactions merit intervention.


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Mourad W. Gabriel et al.

Associations of pathogens with Martes species have been reported inconsistently in the literature, and most reports are of occurrence rather than of disease. Several pathogens that infect mustelids are known to cause disease in a wide array of carnivore species. Thus, to evaluate the potential impacts of pathogens on Martes populations, we must rely to some extent on knowledge extrapolated from related host taxa. The impacts of some pathogens and diseases have been well studied for several mustelid species, including domestic ferrets (Mustela putorius furo; Hillyer and Quesenberry 1997; Fox et al. 1998; Langlois 2005), black-footed ferrets (Mustela nigripes; Williams and Thorne 1996; Gompper and Williams 1998; Bronson et al. 2007), American minks (Neovison vison; Dubey and Hedstrom 1993; Simpson 2001; Cunningham et al. 2009), southern sea otters (Enhydra lutris neris; Kreuder et al. 2003; Mayer et al. 2003; Jessup et al. 2007), and northern river otters (Lontra canadensis; Hoover et al. 1984; Hoberg et al. 1997; Mos et al. 2003). Parasites that can infect many host species (generalists) and those associated with exotic species often pose the greatest conservation threats (Begon 2008; Perkins et al. 2008; Kelly et al. 2009a). Generalist parasites are supported by a large assemblage of hosts, and low-density host populations may experience high levels of parasite exposures as a result of interspecific spillover from community reservoirs (Woodroffe 1999; Daszak et al. 2000; Cleaveland et al. 2007). Parasites of exotic hosts, including feral domestics and native hosts undergoing range expansion, are often associated with greater virulence in native species (Daszak et al. 2000, 2001; Begon 2008). Highly virulent parasites can devastate wildlife populations (Woodroffe 1999). The pathogens most often associated with the decline or extirpation of carnivore populations, and therefore of greatest concern for the management and conservation of Martes species, are rabies viruses, canine distemper virus, parvoviruses, and Toxoplasma gondii (Woodroffe 1999; Cleaveland et al. 2007; Pedersen et al. 2007). We discuss each of these pathogens in the following sections; see Williams and Barker (2001) and Samuel et al. (2001) for more detailed information on these topics. Rabies Rabies is caused by a group of widely distributed RNA viruses in the genus Lyssavirus, and historical accounts date back several millennia (Rupprecht et al. 2001). Rabies viruses can infect all species of mammals (Rupprecht et al. 2001). Carnivores and bats provide rabies reservoirs throughout most of the world, and viral strains are typically associated with the local reservoir host species (Rupprecht et al. 2001; Krebs et al. 2003; Müller et al. 2004).


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Transmission of rabies typically occurs when a susceptible host is bitten or otherwise comes into direct contact with infected saliva (Rupprecht et al. 2001; Langlois 2005). Less common routes of transmission include contact with ocular and nasal exudates or the consumption of infected animals as prey or carrion (Ramsden and Johnston 1975; Charlton 1994). Rabies viruses display strong tropism for neural tissue, especially in the central nervous system (CNS), where replication occurs at a rapid pace (Rupprecht et al. 2001). Such neural tropism leads to the spread of the virus through various neural pathways to the brainstem, resulting in neurological distress (Rupprecht et al. 2001). As virions pass back to peripheral systems, infection of salivary glands contributes to elevated levels of virions in salivary secretions (Rupprecht et al. 2001; Langlois 2005). Behavioral changes occur after incubation of the virus and are dependent on the strain and proximity of the bite to the CNS (Rupprecht et al. 2001). Both the incubation period and prodromal stage (early signs) can last for days to several months (Rupprecht et al. 2001). Although rabies has been documented in several Martes species, clinical signs have been described only in stone martens (M. foina; Müller et al. 2004). Individuals were either asymptomatic or exhibited severely abnormal behaviors, including lack of fear, lethargy, and aggression (Müller et al. 2004; Dacheux et al. 2009), as reported in other mammals (Rupprecht et al. 2001). Rabies is generally considered a fatal disease, but survival after infection has been reported (Rupprecht et al. 2001). Rabies remains a serious conservation concern for many carnivore communities and is especially alarming when species of concern are threatened with local extinctions (Woodroffe 1999; Cleaveland et al. 2007; Knobel et al. 2007). In some cases, domestic dogs (Canis familiaris) living in or near areas occupied by wild carnivores have exacerbated the risk of rabies to species in peril (Woodroffe 1999; Cleaveland et al. 2007), and such risks likely extend to Martes species. Canine Distemper Virus Canine distemper virus (CDV) is a highly labile RNA virus that infects and causes significant disease in many carnivores worldwide, including mustelids (Deem et al. 2000; Williams 2001). Juveniles and immunosuppressed individuals are usually affected in greater proportions than are healthy adults (Van Moll et al. 1995; Deem et al. 2000; Williams 2001). Distemper is believed to be a factor that led to the near extirpation of the black-footed ferret in the wild (Thorne and Williams 1988). The epidemiology of CDV for Martes species is not fully understood, but in other carnivores, it has shown cyclical patterns and temporal variance suggestive of density-dependent transmission (Roscoe 1993; Van Moll et al. 1995; Williams 2001).


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The transmission of CDV is primarily by direct contact with the oralrespiratory or ocular fluids of infected individuals (Deem et al. 2000; Williams 2001). Although the virus can be transmitted via environmental contamination of feces or urine, infection through these routes is less likely because of the virus’ instability in the environment (Deem et al. 2000; Williams 2001). After the virus enters the respiratory system and pervades the respiratory epithelium, it can spread rapidly through the lymphatic and vascular systems and infect other organs (Deem et al. 2000; Williams 2001). The clinical signs of CDV in Martes species have rarely been documented. In one of the few studies available, stone martens exhibited lack of fear, ataxia, and high levels of salivation and ocular discharge (Van Moll et al. 1995). In a suspected CDV epizootic in Newfoundland, Canada, where American martens (M. americana) were believed infected, individuals exhibited similar symptoms, including short periods of full-body convulsions; however, attempts to confi rm CDV infection by histological, serological, or molecular assays were unsuccessful (Fredrickson 1990). In a recent epizootic in an insular population of fishers (M. pennanti) in California, several mortalities were confi rmed to be caused by CDV (S. Keller and M. Gabriel, University of California at Davis, unpublished data). Gross clinical signs of infection included hyperkeratosis, skin lesions, and severe emaciation (M. Gabriel, unpublished data; Figure 7.1). In addition, radiotelemetry data provided indirect evidence of lethargy and abnormal movement shortly before mortality (R. Sweitzer, University of California at Berkeley, unpublished data). In mustelids, CDV tends to affect multiple sites in the central nervous system (Van Moll et al. 1995; Deem et al. 2000; Williams 2001). The strongly immunosuppressive effects of CDV also act synergistically with subclinical or latent infections by other pathogens or parasites to enhance the severity of disease and increase the probability of death (Van Moll et al. 1995; Deem et al. 2000; Williams 2001). For example, clinical signs of a secondary infection by Hepatozoan spp. were observed in a stone marten with CDV (Van Moll et al. 1995). Similarly, CDV has been associated with toxoplasmosis in other mustelids (Diters and Nielsen 1978; Van Moll et al. 1995; Frank 2001). Given the devastating effects of CDV outbreaks on captive and wild populations of carnivores, the conservation implications of infections with CDV could be significant. Likewise, CDV-related mortalities in small or insular Martes populations could have a significant effect on their persistence and viability. Parvoviruses Parvoviruses are single-stranded DNA viruses, and each strain is generally named for the species in which it was isolated initially (Barker and Parrish


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Figure 7.1. Canine distemper virus (CDV) mortality of a fisher displaying gross clinical signs of (A) paw pad hyperkeratosis and ulcerative lesions, (B) ulceration and hyperkeratosis of the skin along the gum line, and (C) eye. (D) Full body of CDV-infected fisher displaying severe emaciation and no subcutaneous fat.

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2001; Steinel et al. 2001; Parrish and Kawaoka 2005). The feline parvovirus subgroup (FPV) affects a wide variety of carnivores throughout the world (Steinel et al. 2000, 2001; Barker and Parrish 2001). Several related viruses occur within this subgroup, including feline panleukopenia virus (FPL), mink enteritis virus (MEV), raccoon parvovirus (RPV), blue-fox parvovirus (BFPV), and canine parvovirus types 1 and 2 (CPV-1 and CPV-2, respectively), that have similar genetic and antigen properties (Barker and Parrish 2001; Steinel et al. 2001). Interestingly, CPV-2 emerged rapidly in 1978, such that by the end of that decade, more than 80% of all domestic canids were infected globally (Parrish et al. 1988; Parrish and Kawaoka 2005). Another parvovirus, Aleutian disease virus (ADV), infects various carnivores (including mustelids) but is dissimilar to the FPV subgroup (Barker and Parrish 2001; Steinel et al. 2001). We expect that these viruses have the potential to infect all Martes species. Parvoviruses are highly resistant to environmental degradation and, under suitable conditions, can persist for months and possibly years (Bouillant and Hanson 1965; Gordon and Angrick 1986; Barker and Parrish 2001). Transmission is generally through the fecal-oral route, rather than by direct transmission, and feces deposited at marking sites, latrines, and trap sites are potential sources of exposure for Martes species (Barker and Parrish 2001; McCaw and Hoskins 2006). Vertical transmission (the transmission of a pathogen from parent to offspring in utero or during birth) has been shown to occur in pregnant domestic ferrets (Kilham et al. 1967) and might occur in other mustelids. Parvoviruses display strong tropism toward rapidly dividing cells, facilitating exponential replication of the virus and systemwide infections (Steinel et al. 2001; McCaw and Hoskins 2006). Neonates and juveniles, which have high levels of mitotically active cells, are usually the most susceptible segments of the population (Steinel et al. 2001). Susceptibility of adults is greatest in the rapidly dividing cells of the intestinal epithelium and the lymphatic systems (Steinel et al. 2001). The clinical effects of parvoviruses on Martes neonates, juveniles, and adults are unknown. In other mustelids, however, neonates and juveniles have displayed clinical disease and mortality when infected with MEV, FPL, and ADV through natural and experimental infections (Kilham et al. 1967; Duenwald et al. 1971; Steinel et al. 2001). Adults seldom displayed clinical disease with viruses of the FPV subgroup but exhibited clinical signs when infected with ADV (Barker and Parrish 2001; Steinel et al. 2001). The detection of parvovirus virions in Martes feces (Kenyon et al. 1978; Brown et al. 2006; Gabriel et al. 2010) suggests that viral replication is occurring in the crypts and microvilli of the intestinal epithelium, as it does in other carnivores (Steinel et al. 2001; McCaw and Hoskins 2006). The frequency of clinical disease from parvoviruses and its related effects in Martes species re-


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mains uncertain. In some mustelids, panleukopenia, anemia, gastrointestinal lesions, diarrhea, and dehydration are common symptoms of the disease (Barker and Parrish 2001), and cerebral hyperplasia was reported in fetal domestic ferrets whose mothers were infected experimentally with FPL (Kilham et al. 1967). Parvoviral infections are unlikely to limit wild carnivore populations, with the possible exception of small or otherwise vulnerable populations (Barker and Parrish 2001). Furthermore, the risk of spillover from nearby infected individuals or fomites (inanimate objects that carry disease organisms) is important because of the environmental resistance of these viruses. Techniques to reduce some of these risks are described in a later section of this chapter. Toxoplasma gondii Toxoplasma gondii is an obligate intracellular protozoan parasite with a complex life cycle involving many parasitic stages, and both intermediate and defi nitive hosts (Dubey et al. 2001). It occurs worldwide and probably has the potential to infect all avian and mammalian species (Tenter et al. 2000). Only felids are capable of shedding the infective stage of T. gondii through feces; other species serve only as intermediate hosts (Dubey et al. 2001). Animals can be infected by ingesting either infective oocysts in the environment or the tissues of infected intermediate hosts (Dubey et al. 1998). Most tissue cysts do not cause obvious harm and remain intact throughout the host’s life (Dubey et al. 2001). Although subclinical effects of this parasite are little understood, they are probably consequential (McAllister 2005). Acute toxoplasmosis is thought to be rare in healthy, nonimmunosuppressed individuals (Dubey et al. 2001), but outbreaks have resulted in significant mortality in black-footed ferrets (Burns et al. 2003b) and American minks (Pridham and Belcher 1958) in captive-breeding programs, and in free-ranging southern sea otters (Cole et al. 2000). Some of these cases in mustelids and closely related species were preceded by infection with canine distemper, which causes immunosuppression (Diters and Nielsen 1978; Van Moll et al. 1995; Frank 2001). Pathogenesis of toxoplasmosis begins when an ingested oocyst releases sporozoites in the intestine that multiply and spread to lymph nodes, where the more effectively spreading (and tissue-damaging) tachyzoites are produced (Jones et al. 1997). In intermediate hosts, the predilection of T. gondii for the central nervous system is likely the reason for neurological symptoms and pathology (Webster 2007). The only recorded episode of toxoplasmosis in Martes species is a recent case in California in which a fisher died of inflammation of the meninges and the brain, caused by an infection with T. gondii (M. Gabriel, unpublished data). Clinical signs observed in other mustelids with toxoplasmosis include head tremors and ataxia, circling, limb lameness, lethargy, blindness,


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loss of appetite, anorexia, difficulty chewing and swallowing, and abortion (Frank 2001; Burns et al. 2003b; Kreuder et al. 2003; Jones et al. 2006). The subclinical effects of this pathogen may be important (McAllister 2005). As such, the deleterious effects on behavior from T. gondii infection are just beginning to be fully understood (Webster 2007). Norway rats (Rattus norvegicus) infected with T. gondii were more active and displayed less fear of novel stimuli than uninfected rats (Webster et al. 1994; Berdoy et al. 1995). These effects can cause a greater susceptibility to predation (Webster 2007); for example, in southern sea otters, a strong correlation was found between T. gondii encephalitis and fatal shark attacks (Kreuder et al. 2003). The rare but significant effects of toxoplasmosis epizootics in other mustelids demonstrate the potential importance of this parasite for Martes populations worldwide (Dubey et al. 2001). For example, it is possible that a heightened susceptibility to predation from toxoplasmosis could be related to the high predation rates currently experienced by fisher populations in California (G. Wengert, unpublished data). Taken together, this evidence warrants consideration of T. gondii as a threat to Martes species that should be addressed in current and future research and conservation programs. Disease Management and Conservation Strategies

Recognition and management of disease risks are becoming common strategies in conservation programs. Managing disease includes efforts to prevent and control the spread of pathogens. In some cases, knowledge of transmission cycles allows avoidance of risks. In other cases, individuals may need to be vaccinated or treated clinically to prevent disease outbreaks. The topics we address below are just a few of the many disease-management options currently available to resource managers, and each could encompass an entire chapter because of differences in Martes niche characteristics, sympatric communities, and parasite distributions that may warrant different approaches. Here, we highlight general strategies that can be used to maintain the health of Martes populations. We recommend thorough investigations into the appropriateness and feasibility of these methods for all Martes populations being managed for conservation purposes. Vaccinations One strategy for managing infectious disease in wildlife is the use of vaccines (Haydon et al. 2006). Immunization with vaccines can prevent or reduce the clinical manifestations of many virulent pathogens, thereby reducing transmission to susceptible animals; however, a lack of success in some vaccination programs demonstrates the need for caution (Thorne and Williams


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1988; Woodroffe 1999). Vaccines are typically developed for domestic animals and must be assessed before being given to free-ranging wildlife (Woodroffe 1999). In addition, success is often difficult to gauge, since decisions to leave control groups (unvaccinated cohorts) in species or populations of concern may be politically or ethically unjustifiable (Woodroffe 1999). Several primary concerns can be cited about use of vaccines in wildlife programs. First, a vaccine is usually constructed to protect against a specific pathogen; however, immunized individuals may remain susceptible to infections when wild pathogen strains gain virulence factors and antigenic sites that differ from those used to create the vaccine. Furthermore, protective immunity typically wanes over time, and many vaccines require the immune system to be primed with one or several boosters. Finally, to thoroughly understand a vaccine’s efficacy and safety, proactive experimental-challenge studies must be conducted; unfortunately, fi nancial, logistical, and ethical constraints often preclude such studies. A vaccine should meet several criteria before being used in wildlife species. First, the vaccine should produce no significant disease in the host. In a well-known example of vaccine-induced disease, wildlife managers used a modified live-distemper vaccine in the black-footed ferret conservation program that produced the disease they were intending to prevent (Carpenter et al. 1976). From this and other unfortunate examples, it is now well understood that vaccines developed for domestic or companion animals must be used with caution in wildlife. Second, because of the impracticality of vaccinating a population or many individuals multiple times, a vaccine should produce long-lasting protective immunity. There are several categories of vaccines, and killed or inactivated vaccines often fail to properly stimulate the immune system to produce a long-term response (Thorne and Williams 1988). Third, the vaccine should be able to provide protection from several antigenic variants, thereby affording the host protection from various forms of the pathogen they may encounter. Approved vaccines for Martes species are currently limited; however, the American Association of Zoo Veterinarians (2010) has developed a list of vaccines recommended for small carnivores, including mustelids, some of which have been used in Martes species. Distemper To date, no experimental trials have been conducted to ascertain the effectiveness and safety of current CDV vaccines for use in Martes species; however, the currently accepted vaccination of mustelids for distemper virus is a recombinant vaccine marketed as PUREVAX ferret distemper vaccine (Merial Ltd., Duluth, Georgia, USA) (Wimsatt et al. 2006; Lewis and Happe 2008; Jessup et al. 2009). PUREVAX recombinant vaccines were used safely in both black-footed ferrets and sea otters (Wimsatt et al. 2006; Jessup et al.


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2009). At present, most of the vaccination programs for Martes species have been conducted during translocation efforts that provided limited data on the effects or efficacy of the vaccine (Mitcheltree et al. 1997; Lewis and Happe 2008). Reintroduced fishers vaccinated with the discontinued modified-live Fervac-D (United Vaccines, Madison, Wisconsin, USA) (Mitcheltree et al. 1997) and PUREVAX vaccines (Lewis and Happe 2008) (D. Clifford, California Department of Fish and Game, unpublished data) showed mixed results regarding their performance. Mitcheltree et al. (1997) vaccinated ~45 fishers with Fervac-D prior to release during a reintroduction program in Pennsylvania, with a small subset receiving a secondary booster if they were held in captivity 12 days; however, several fishers did not develop antibodies to CDV after either the fi rst or the booster vaccination. Vaccinations with PUREVAX were administered in the Washington and California reintroduction programs (Lewis and Happe 2008; D. Clifford, unpublished data). Available data from these efforts showed elevated titers for IgM and IgG antibodies (M. Gabriel and D. Clifford, unpublished data), but it was unknown whether these responses were sufficient to protect against a natural infection. Indeed, the effectiveness of recombinant vaccines for use in Martes species is generally unknown because of lack of data on their effects. Rabies Because of the virulence of rabies viruses, killed vaccines are the only ones currently recommended for Martes species (American Association of Zoo Veterinarians 2010). Imrab-3 (Merial Ltd., Duluth, Georgia, USA) is a killed rabies vaccine that has been used in various zoo and free-ranging wildlife species, including fishers (Lewis and Happe 2008; D. Clifford, unpublished data). Because this vaccine contains a killed virus, annual vaccination of each individual is recommended (American Association of Zoo Veterinarians 2010). There are numerous accounts of a single dose failing to provide adequate protection, or even measurable seroconversion, within populations (Woodroffe 2001; Haydon et al. 2006). For example, primary vaccinations in Ethiopian wolves (Canis simensis) provided protection from infection for