ONE
Introduction
CONTENTS
Why Study Wildlife Diseases 1 Density and Disease 10 Human Health 2 Disease Models 11 Domestic Animal Health 3 Causes of Disease 12 Wildlife Health 4 Role of Diseases in Wildlife Populations 13 Select Definitions and Concepts 6 Can Diseases Regulate Wild Populations? 15 Health and Disease 6 Overview and Summary 17 Parasitism 6 Literature Cited 18 Diseases in Populations 9
The study of wildlife diseases encompasses the Why Study Wildlife Diseases health, disease, and fitness of wildlife, and the broad range of factors that can potentially A focus on the health and well-being of wildlife affect their well-being. These factors include themselves is of relatively recent origin. Histori- a wide array of infectious organisms such as cally, much of the initial interest in the health and helminths, arthropods, and microorganisms, diseases of wildlife stemmed from other con- as well as toxins, traumas, metabolic dysfunc- cerns, particularly human health and the health tions, genetic problems, and habitat fragmen- of domestic animals (Friend 1976, Gulland 1995, tation. Such factors not only act individually, Simpson 2002). In time, more direct interest but also may interact synergistically in complex emerged in the wildlife themselves, with an effort ways to affect wildlife health. In this first chap- to gain a more complete biological and ecological ter we give a brief summary of the basis for the understanding of how diseases interact with host emergence of wildlife diseases as a discipline populations; this is exemplified by the emergence and provide some key general concepts used of wildlife health and conservation medicine as throughout this text. distinctive disciplines.
1 More broadly, because parasitism is such to humans or from humans to nonhumans, a common mode of life, with parasites com- (b) diseases that are transmitted to humans and prising the majority of species on earth for which humans typically are a dead-end host (Zimmer 2000), there is considerable interest (zooanthroponoses), and (c) diseases transmit- in understanding the basic biological relations ted from humans to nonhumans and for which parasitism entails, so as to better understand nonhumans typically are a dead-end host evolutionary history and ecological principles. (anthropozoonoses). Interestingly, in Russian In conventional Darwinian theory, natural literature the opposite definitions are given for selection adapts creatures to their immediate each term (Bender 2007). Estimates for the local environments through a process of spe- number of zoonotic diseases range from as low cialization, operating to produce features that as 100 (Benenson 1990) to as high as 3,000 reduce organismal flexibility for future evolu- if all 2,000 serotypes of Salmonella spp. are tion; for example, specialization through simpli- counted as separate species (Beran and Steele fication and loss of structures among helminth 1994, Ashford and Crewe 2003), with new zoo- parasites often has been extreme (Gould 2002). notic pathogens being described every year. In Wildlife provide important models to better one detailed count, an estimate of 816 zoonotic understand key host–parasite relationships. pathogens was made after omitting the numer- In recent years, an increased sense of ous Salmonella spp. serotypes (Woolhouse and human responsibility toward the natural world, Gowtage-Sequeria 2005). including a greater concern for wildlife, has Along with their health impacts, some emerged. Two examples of these concerns are zoonoses have had particularly significant socio- the growing interest among the public in wild- logical impacts. Bubonic plague, caused by the life rehabilitation, as well as concerns over envi- bacterium Yersinia pestis, is considered to have ronmental issues such as oil spills and other given rise to at least three major world-wide epi- forms of pollution. In recent years, increased demics (Stenseth et al. 2008) and to be one of tensions in global political relationships and the greatest natural disasters in human history a desire for greater national and international (Fig. 1.1). In the fourteenth century alone, it is biosecurity (Dudley 2004) have further stimu- estimated that plague caused or contributed to lated interest in a number of wildlife diseases. the death of one-fourth of the western European population and of 2 million persons in England alone (Poland et al. 1994). Equally important Human Health was the nearly complete social disruption that Public health risks were an early concern, and accompanied many plague epidemics, with they remain a significant source of interest in consequent shifts in world politics and power the study of wildlife diseases (Beran and Steele (McNeill 1977). On a historical note, the old chil- 1994, Ashford and Crewe 2003). These inter- dren’s nursery rhyme “Ring-around-the-Rosie” ests have been focused primarily on wildlife sometimes has been described as a poem stem- diseases to which humans are susceptible, ming from plague epidemics. However, this such as rabies, bubonic plague, avian influ- appears to be fallacious, as the poem was not enza, Lyme disease, hantavirus pulmonary syn- recognized until the eighteenth century, long drome, and West Nile fever in North America. after the most significant plague epidemics in Such diseases transmitted between humans humans; also, the poem has many variations and other vertebrate animals are termed zoo- that contain little apparent connection to plague noses (sing. zoonosis) (Soulsby 1974). We apply (Munro 1996) and include one proposed to the term zoonosis as including (a) diseases depict a smallpox epidemic (Glickman 1987). common to both humans and nonhumans and Rabies is another disease that has had which may be transmitted from nonhumans a significant impact on human cultures.
2 introduction human diseases have been identified as zoo- notic (Lederberg et al. 1992); one estimate is that about three-fourths of the emerging dis- eases in humans are zoonoses (Taylor and Woodhouse 2000). Many emergent diseases in humans have followed changes in habitat or populations of wild hosts, with rodent species frequently being of special concern (Mills et al. 1994, Poss et al. 2002). Hantavirus infec- tions and avian influenza both can produce sig- nificant human mortality and loom as potential sources of serious zoonoses. Besides giving insights into the sources and risks of zoonotic diseases to humans, the study of diseases in wildlife also may provide models for better understanding similar human diseases. Alternatively, the understanding of human diseases can provide important insights into diseases transmitted to nonhumans (anthropo- zoonoses), including other primates (Cranfield et al. 2002).
Figure 1.1 Plague cemetery in Nürnberg, Germany. Domestic Animal Health Headstones often were laid on top of graves to prevent wild pigs and other animals from scavenging the dead In addition to disease agents shared with (photo by R. Botzler). humans, wildlife also share many disease agents with domestic animals. Rinderpest (lit- erally “cattle pestilence”), caused by a morbilliv- The “big bad wolf” from the Little Red Riding irus closely related to the human measles virus, Hood fairy tale may play on the fear many of was considered a great scourge among domes- European ancestry held for wolves (Canis lupus); tic cattle and wildlife in Africa (Branagan and this fear has been traced to a severe wolf rabies Hammond 1965, Plowright 1982) before its outbreak in Europe during the 1760s (Clarke eradication (Anonymous 2011). The impacts of 1971). However, in a more extensive study, this disease on imported cattle were so severe Linnell et al. (2002) considered most wolf that strenuous efforts were made to contain attacks on humans in France during the 1760s infections; these efforts included establishing to be predatory rather than rabies-induced. The belts of immune cattle in key habitats, and even authors cite a number of reported wolf attacks constructing a 265-km barrier fence between on humans, especially in Finland, France, and Lake Tanganyika and Lake Nyassa in Africa, Estonia, and more recently India, Russia, and with a 40-km game-free strip maintained on additional regions of Asia; but they also assert each side of the fence by professional shooters that attacks by normal, healthy wolves are quite (Plowright 1982, McCallum and Dobson 1995). rare and unusual, and have not been reported This led to considerable wildlife mortality dur- in North America (Linnell et al. 2002). ing the ongoing slaughter of animals in this Public health concerns have played an game-free strip; the fence further disrupted the important role in the study of many other natural daily and seasonal migration patterns wildlife diseases. For example, most emerging for wildlife between key habitats.
introduction 3 In addition to the concern for humans, rabies also may have a considerable impact on wildlife and domestic animal populations (Beran 1994). Rabies in vampire bats (Desmodus rotundus) occurs from tropical Mexico to northern Argentina and Chile, and the disease has led to direct losses of millions of dollars annually among cat- tle, as well as additional losses through reduc- tion in production and secondary infections among livestock (Kverno and Mitchell 1976). Rabid bats also have contributed considerably to public health costs for rabies control and post- Figure 1.2 A sheep dying from effects of liver flukes (Fasciola hepatica) in habitat typical of the snail bite prophylaxis of humans. The environmental intermediate host (Courtesy of W. Frank, Universität and ecological effects of killing vampire bats as Hohenheim, Germany). a means of control have not been assessed. Avian cholera, caused by the bacterium African mammals of both canine distemper Pasteurella multocida, is a serious disease (Harder et al. 1995, Roelke-Parker et al. 1996, among both domestic (Heddleston 1972) and Carpenter et al. 1998) and rabies (Cleaveland many wild birds, including migratory wildfowl and Dye 1995) followed transmission of (Botzler 1991, Samuel et al. 2007). In North these viruses from domestic dog reservoirs in America, the first known epizootics among conjunction with increasing encroachment wildfowl occurred in Texas (Gordus 1993) and of human populations on wildlife reserves California (Rosen and Bischoff 1949, 1950) and (Poss et al. 2002). As an added concern, some were associated with exposure to carcasses of of the emerging infectious diseases in both domestic chickens that had died from avian wildlife and domestic animals also are zoonotic cholera. However, despite these historical con- (Mahy and Brown 2000, Friend et al. 2001, nections and an ongoing concern that wild birds Daszak and Cunningham 2002, Kahn 2006). may be a source of infection for domestic birds, Some diseases intersect with public health, there is little direct evidence for consistent trans- domestic animals, and wildlife. Influenza, mission of Pasteurella multocida between wild caused by a myxovirus, is an example. Wild and domestic birds (Snipes et al. 1988, 1989; ducks, geese, shorebirds, and domestic pigs are Christiansen et al. 1992). important reservoirs for these viruses and can Many helminth parasites and protozoa also transmit them to domestic fowl (Slemons and are shared between domestic animals and wild- Brugh 1994, Acha and Szyfres 2003, Fouchier life (Fig. 1.2). These include lungworms and intes- et al. 2005). Human cases usually occur after tinal nematodes, tapeworms and flukes among exposure to infected domestic animals such mammals (Longhurst et al. 1952, Soulsby 1968, as pigs and fowl, in which viral strains have Dunn 1969, Fraser and Mays 1986), as well as a undergone a genetic recombination (Slemons number of intestinal parasites among domestic and Brugh 1994, Alexander and Brown 2000); (Soulsby 1968) and wild (Wehr 1971) birds. human cases of the highly pathogenic avian Although interest in shared diseases influenza H5N1 have been tied to domestic fowl. between wildlife and domestic animals initially stemmed from veterinary concerns about the Wildlife Health role of wildlife as sources of diseases for domestic animals, it also is important to note that wildlife While research addressing the role of wildlife can be adversely affected by diseases acquired diseases among humans and domestic from domestic animals. Recent epizootics in animals has occurred over many years, a focus
4 introduction Figure 1.3 An American coot (Fulica americana) dying from avian cholera (Pasteurella multocida infection). Note the convulsions and torticollis (“twisted neck”). on wildlife diseases with a specific concern on general fitness (survival, fecundity, mate for the wildlife themselves has developed selection) for all wildlife species. Concern more recently, emerging first as a formal for diseases in threatened and endangered discipline about 1951, with the founding of species, and in relocation and translocation the Wildlife Disease Association. Initially, programs also has increased. Many disease most available information among interested investigations in conservation programs con- professionals was transmitted through tinue to be focused on high-profile species that the Wildlife Disease Association Newsletter, have undergone a sudden demographic crash which was replaced with the Bulletin of the (Munson and Karesh 2002). Wildlife Disease Association in 1965, which, Recent emerging infectious diseases of wild- in turn, was continued as the Journal of life include the chytrid fungus (Batrachochy- Wildlife Diseases after 1970. Several books trium dendrobatidis) (Daszak et al. 2004), white emerged during and after the 1960s that nose syndrome (Pseudogymnoascus [Geomyces] also helped establish wildlife disease as a destructans) (Blehert et al. 2009), and devil facial distinct discipline (McDiarmid 1962, 1969; tumor disease (Hawkins et al. 2006). Emerging Davis et al. 1970, 1971; Davis and Anderson wildlife diseases can have a particularly severe 1971; Page 1976; von Braunschweig 1979; impact on small, fragmented populations Davis et al. 1981; Fowler 1981; Wobeser 1981; (Daszak and Cunningham 2002) and have been Edwards and McDonnell 1982; Hoff and responsible for some local and regional extinc- Davis 1982; Fairbrother et al. 1996; Samuel tions (McCallum and Dobson 1995, Daszak and et al. 2001; Williams and Barker 2001; Cunningham 1999, Woodroffe 1999). Reasons Majumdar et al. 2005; Wobeser 2006; Thomas proposed for the intensified transmission and et al. 2007; Atkinson et al. 2008). better detection of emerging diseases include Most early concerns about wildlife diseases removal of geographic barriers to human and among biologists and managers were focused animal transport, as well as ecosystem disrup- on major mortality events or mortality factors tion, climate change, and habitat fragmentation affecting the management of economically (Graczyk 2002). important game species (e.g., waterfowl, ungu- In a broader sense, devising conserva- lates, upland game) (Fig. 1.3). In recent years, tion strategies that are practical in the cur- greater emphasis has been placed on better rent understanding of the “state of the Earth” assessing the role of parasites and diseases will require models that address disease risks
introduction 5 (Munson and Karesh 2002), including risks to adaptability to change (Wylie 1970). Less impor- humans, domestic animals and plants, wildlife, tant here is the number of parasites or prob- and whole ecosystems, and that further recog- lems an animal or population encounters than nize that all of these groups have shared risks its response and adaptability to these stresses. and cannot be viewed in isolation from the One working definition of human health is the others. Such strategies call for a better under- capacity to achieve socially determined goals standing of the role of wildlife in these larger (mental, physical, and social well-being, vigor, disease models, as well as call for policies and resilience, productivity, flourishing) within a approaches to integrate human, agriculture, set of socioecological constraints, only one of and wildlife disease studies, as addressed in which is disease (Murray et al. 2002). Munson the One Health concept (www.onehealth.com). and Karesh (2002) view disease as any disor- der of body functions, systems, or organs; such a disorder is not necessarily confined to one Select Definitions and Concepts caused by an extrinsic factor such as viral or Prior to detailed discussions of wildlife dis- bacterial infection, infestation with parasites, ease topics, it is useful to consider some or exposure to toxins (Munson and Karesh basic definitions. 2002). In a very broad outlook, disease has been defined simply as a reduction in fitness (Clayton and Moore 1997). Health and Disease For purposes of this text, we use the defini- Two approaches commonly have been used to tion that wildlife disease is “any impairment that provide a conceptual base for health and disease interferes with or modifies the performance of in wildlife (Wylie 1970). In one, health is normal functions, including responses to envi- viewed as a concept analogous to temperature. ronmental factors such as nutrition, toxicants, As such, while there may be lower limits (death and climate; infectious agents; inherent or con- or absolute zero, respectively), there is no true genital defects, or combinations of these factors” upper limit for either health or temperature. (Wobeser 1981). Such a definition can be applied In such an analogy, health is the concept to to both individuals and populations. Our pri- be understood and measured, and one seeks to mary emphasis in this text is on infectious and, assess how far from death an organism may be. secondarily, noninfectious causes of disease. Among humans, features used to assess health can entail physical, mental, emotional, and Parasitism spiritual components. Considering just physi- cal features, states of human health have been Parasitism is a term used to describe one set of assessed by body mass index, body fat, erythro- interspecific relationships along a broad contin- cyte and serum enzyme measures, and urine uum of relationships between species (Dindal metabolites (Berkow and Fletcher 1992). For 1975). Broadly, the term symbiology (literally, wildlife and other nonhuman animals, far less is “living together”) has been used to describe the understood regarding what normal physiological study of any persistent relationship (symbio- values constitute physical health. Measures used sis) between two different species; parasitism also may include body weights, fat indices, as well is one part of that larger set of relationships as a variety of red blood cell, serum enzyme, and (Read 1970). It sometimes is argued that while urine metabolite values (Malpas 1977, Warren parasites may elude clear definition, they gener- and Kirkpatrick 1978, Seal et al. 1981, DelGuidice ally are “known primarily when we see them” et al. 1990, Harder and Kirkpatrick 1994). (Moore 2002). In contrast to viewing health on a purported Broadly, parasites are organisms living linear scale, health also may be assessed as partly or completely at the expense of another
6 introduction organism (its host). Parasitic lifestyles are direct life cycles and are termed “monoxenous” regularly represented among four of the major (Gr. mono 5 one, xenous 5 host). However, kingdoms: Animalia, Fungi, Protista, and others, including many parasitic helminths and Monera (with a much less common occurrence protozoa, require two or more hosts to complete among Plantae). Viruses raise an interesting their life cycle; these have indirect life cycles and problem; they have some features of living are termed “heteroxenous.” For parasites with systems (e.g., genome, replication, evolution), an indirect life cycle, the host in which the but are not functionally active outside their sexually mature stage of the parasite occurs is host cells and generally are not considered to called the definitive host. An intermediate host is be living microorganisms (van Regenmortel an additional required host for those parasites and Mahy 2004); however, they commonly to complete their life cycle. In the intermediate are treated as highly specialized parasites and host, the parasites undergo some developmen- included with other microorganisms in this tal changes and may multiply, but do not reach text. Prions, infectious proteins lacking nucleic their sexually mature stage; the intermediate acids, also raise interesting problems and are host typically is a different taxonomic group addressed as a special topic in Chapter 11. from the definitive host. A less common type of Parasitic relationships can overlap with host is a paratenic (transport) host, an organism some forms of predation (e.g., parasitoid wasps which serves to transfer a larval stage or stages and some fly maggots that kill their hosts) as from one host to another but in which little or well as certain mutualistic relationships (e.g., no development takes place (Anderson 1992). many intestinal bacteria). Generally, parasites A paratenic host is not required for completion live in relatively long contact with the host for of the life cycle, but often is a prey species of part of their life cycle; in contrast, predators the definitive host and facilitates completion and prey generally have a relatively short period of the life cycle; a paratenic host often is con- of contact that ends in death and consumption sidered an “optional” host. The term vector is of the prey by the predators. Further, parasites defined by some as any host that transmits typically relinquish the role of regulating their parasites, including intermediate, definitive, relationship with the external environment to and paratenic hosts (Clayton and Moore 1997); the host during part of their life cycle. in contrast, other scholars tend to restrict the Endoparasites live within a host’s body during term primarily or exclusively to arthropods at least part of their life cycle and depend com- (Wobeser 2006). pletely on the host to regulate their relationship The persistent presence of a parasite in with the external environment during that time; a host is termed an infection (Pratt 1963); a examples of endoparasites include some hel- related term, infestation, is used to describe the minths, fungi, protozoa, and many infectious persistent presence of ectoparasites. Prevalence microorganisms. Parasites living on the exterior is the number of animals infected by a parasite of the host are termed ectoparasites; these have a divided by the number of animals in the popu- partial dependence on the host to regulate their lation examined, and commonly is reported relationship with the external environment as a percent value (Margolis et al. 1982, Bush when they are present on the host; examples et al. 1997). In contrast, incidence is the num- include parasitic arthropods such as ticks, fleas, ber of new hosts that become infected with a lice, and mites. Finally, parasites generally are particular parasite during a specified time characterized as competing with the host for interval, divided by the number of uninfected its resources, and often reduce host fitness (e.g., hosts present at the start of that time interval survival, fecundity) (Clayton and Moore 1997). (Margolis et al. 1982, Bush et al. 1997); Many parasites are transmitted directly incidence often is reported as number per between susceptible hosts; these species have 1,000 in the population. Intensity is the number
introduction 7 of parasites of a particular species in or on a single infected animal; mean intensity is the total number of parasites of a particular species found in each host, divided by the number of hosts infected with that parasite (Margolis et al. 1982, Bush et al. 1997). Mortality refers to the death of a host and morbidity is the condition of having an illness, weakness, or other disability. In contrast, necrosis refers to a localized area of death in a tissue or Figure 1.4 Sigmoid curve typical of an LD test (Courtesy organ rather than the death of a whole organism. 50 of National Library of Medicine. Based on original from Virulence is a measure of the impact of para- http://aquaticpath.umd.edu/appliedtox/images=toxtutor/ sites upon their host. Broadly, virulence can be chart-5.gif. Drawn by Patient Education Institute). defined as any collective effects on host fitness, including mortality, morbidity, and reduced fecundity (Clayton and Moore 1997). Virulence physical damage and blood loss are common also has been described more precisely as a causes of morbidity and mortality. Among bac- complex property comprising three characteris- teria, toxins affecting the nervous system, heart, tics: infectivity, invasiveness, and pathogenicity or kidney are more typical causes of pathogenic- (Frobisher 1962, Pratt 1963). ity (Pratt 1963). In the laboratory, pathogenicity This latter definition has been applied pri- in living animals commonly has been measured marily to microorganisms and is considered by an LD50 test; an LD50 is the dose of an infective here in further detail. Infectivity is defined as agent or toxin lethal for 50% of a test population the ability to initiate and maintain an infection (Fig. 1.4) (Reed and Muench 1938). in the host (Pratt 1963). This trait is dependent The LD50 test has been highly regarded on the capacity of a parasite to establish a per- as a measure of pathogenicity because of its sistent presence by evading or overcoming local consistency and its requirement for relatively defense mechanisms of the host. For example, few test animals. However, the LD50 test also bacteria causing plague (Yersinia pestis), typhoid is limited to assessing mortality and cannot fever (Salmonella typhi), or shigellosis (Shigella assess more subtle influences such as morbid- spp.) do not have high infectivity to laboratory ity, reduced reproductive success, or increased workers under normal circumstances (Pratt susceptibility to predation; further, it also is 1963). In contrast, Francisella tularensis, the useful only for single, isolated mortality factors cause of tularemia, is a highly infectious bacte- and is not readily adapted to assessing syner- rium readily transferred to workers within the gystic relationships between two or more fac- laboratory (Pratt 1963, Hopla and Hopla 1994). tors influencing mortality. In recent years, the Invasiveness is defined as the ability to prog- LD50 (and the consequent killing of laboratory ress further into the host from the initial site animals) increasingly has been replaced by of infection (Pratt 1963). For example, many alternative tests to measure pathogenicity, such bacteria, including Pasteurella multocida, the as assessment of cellular pathology through cause of avian cholera, commonly invade the the use of tissue cultures. However, it still is blood stream, causing a septicemia (presence of used in toxicology, where every registered pes- pathogenic bacteria or their toxins in the blood) ticide must have at least three avian LD50 tests among infected wildfowl. (A. Fairbrother, pers. comm.). Pathogenicity is the ability to injure a host In summary, for a microorganism to be con- (Pratt 1963) by damaging host tissues. For larger sidered virulent, it must simultaneously be infec- parasites such as helminths and arthropods, tive, invasive, and pathogenic for a given host
8 introduction (Pratt 1963). For example, Mycobacterium tuber- upon; dem: people) refers to a disease affecting culosis, a cause of human tuberculosis, is very many people within an area at one time, at a invasive and highly pathogenic to guinea pigs significantly greater occurrence than expected. (Cavia porcellus) in the laboratory (Wämoscher Examples include outbreaks of bubonic plague and Stöcklin 1927, Dörr and Gold 1932, and human influenza. The term epizootic Wilson and Miles 1964); yet there are no evident has been used to refer to epidemics within reports of its occurrence among guinea pigs in nonhuman animals and the term epornitic their natural habitats (Shope 1927, Wilson and occasionally is used to refer to epidemics among Miles 1964, Williams 2001). Thus, while very avian populations. The term pandemic refers invasive and pathogenic, an apparent absence to a worldwide epidemic (among humans, of infectivity would result in the bacteria not since most other species don’t have the same being considered virulent for guinea pigs. Like- broad distribution). For example, human influ- wise, although Pasteurella multocida, the cause enza is estimated to have caused the death of of avian cholera, is virulent to at least 180 spe- >20 million humans worldwide during the cies of birds (Samuel et al. 2007), there is no pandemic of 1918–19 (Slemons and Brugh evidence that P. multocida can invade the blood 1994). Bubonic plague also has caused numer- stream (cause a septicemia) or cause a clinical ous pandemics among humans (McNeill 1977). disease among turkey vultures (Cathartes aura) In contrast, the term endemic refers to a (Botzler 1991, Samuel et al. 2007); thus by defi- parasite or disease with a low incidence, but nition P. multocida is not invasive, and conse- one that is regularly present in a host popula- quently not virulent, for turkey vultures. tion. Enzootic is a similar term that has been Historically, microparasite virulence was used in reference to diseases characteristic of viewed as a sign of recent association between a nonhumans. For example, Yersinia pestis, the host and parasite, and it was argued that subse- cause of bubonic plague, is maintained among quent host–parasite co-evolution would lead to some rodent populations such as the California a reduction of virulence and even the develop- vole (Microtus californicus) and the deer mouse ment of commensalism or mutualism (Burnet (Peromyscus maniculatus) in western North and White 1972). A more recent hypothesis is America; Y. pestis is considered enzootic in these that virulence also can be maintained by natural species (Poland et al. 1994). One potentially con- selection and may increase or decrease in evolu- fusing aspect of the term endemic is that in eco- tionary response to environmental conditions or logical literature it commonly refers to a species the density and behavior of hosts (Levin 1996). that evolved solely in a limited area or region, as Thus the level of virulence expressed by para- on certain islands (Van Dyke 2003); use of the sites may result from the strategy developed by alternative term “enzootic” in disease literature the infective agent for optimal transmission and can help reduce that potential confusion. survival (Ewald 1994). Alternatively, it also has The terms endemic and enzootic also have been proposed that the virulence of micropara- been used to signify a parasite or disease char- sites is coincidental to parasite-expressed charac- acteristic of a geographic region (rather than ters that evolved for other functions, or emerged a particular host species). Thus, plague also as the product of short-sighted evolution in can be characterized as enzootic to dry grass- infected hosts (Levin 1996). All of these factors lands, mountain meadows, and some deserts of may play a role in different circumstances. western North American and other regions of the world. As another example, avian cholera, caused by Pasteurella multocida, regularly Diseases in Populations causes epornitics among wildfowl of North Several key terms are used in describing dis- America; while found in all North American eases in populations. The term epidemic (epi: flyways, it generally is considered enzootic to
introduction 9 northern California, Nebraska’s Rainwater High Basin, and the Texas playa lakes (Friend 1999). A The term reservoir has been used by authors Proportion in several ways. Simply stated, it can be defined dying or risk B as the sum of all sources of infection—the of infection natural habitat of the parasite (Pratt 1963). More specifically, a reservoir of infection has been defined as an ecologic system in which an Low High infectious agent survives indefinitely (Ashford Host density
1997); such an ecologic system would encom- Figure 1.5 Contrast of density dependent (A) and pass all of the vertebrate and invertebrate host density-independent (B) disease impacts. populations and encompass the pertinent environmental factors as well as any quantita- tive factors, such as critical community size, reservoir (e.g., in Chapters 9 and 10) will gener- needed to maintain an infectious agent indefi- ally take an annual or multi-year perspective, nitely (Ashford 2003). For our use, we generally and thus we will refer to arthropod–vertebrate refer to Ashford’s modified 2003 definition of reservoirs in these chapters, even where some a reservoir. members (e.g., arthropods) play a smaller Examples of reservoirs range from red foxes role during some parts of the year. (Vulpes vulpes) for rabies viruses in Europe (Rupprecht et al. 2001), to soil, mud, or water Density and Disease as reservoirs for the bacterium Listeria monocy- togenes (Bille et al. 1999). However, the notion Parasites and diseases whose risk of infection of reservoir for a parasite or disease may vary or impact varies consistently with the density with geographic scale, such as that occurring (number per unit area) of their host popula- within a specific watershed versus a more tions are termed density-dependent, whereas general assessment of the reservoir on a world- those whose risk or impact do not change in wide basis. Further, in describing reservoirs, response to differing densities are calleddensity- researchers only address a limited number of independent. Thus, for a density-dependent aspects of the environment and thus may miss disease, the rate of transmission of a disease key criteria in their descriptions. The term reser- through a population, or risk of infection for the voir species has been used in a specialized sense susceptible individual, varies consistently with to refer to an introduced host that has artificially the density of the host population (Fig. 1.5). Gen- raised the size of the collective host populations erally, parasites transmitted directly between or densities, consequently allowing pathogen hosts of a susceptible species, without the need transmission even when the endemic host pop- for intermediate hosts or vectors, cause density- ulation had been reduced below the density at dependent diseases (Scott 1988). which a pathogen is able to maintain effective Rabies often is cited as a classical density- transmission (Daszak and Cunningham 2002). dependent disease (Macdonald 1980, Bacon Time scale is another important factor. 1985). One would expect that a rabid fox would Arthropod-borne agents of vertebrates that sur- have a higher probability of encountering an vive in temperate regions often survive during uninfected, susceptible fox in a high-density a period of time (e.g., cold, dry) when arthro- fox population, compared to a low-density fox pod survival is low. In some cases the infective population. Thus the risk of rabies transmis- agent survives primarily in the vertebrate popu- sion would be higher in a high-density than lation and the vertebrates could be considered in a low-density population of susceptible the primary reservoir. However, our use of animals.
10 introduction In contrast, among density-independent dis- affected by the density of wolves shedding eggs eases, the rate of transmission of the causative than by the density of other hydatid-infected agent through a population, or risk of infec- moose. Thus, over a shorter term, such as a tion for the host, is independent of the density single season, risks of acquiring indirect life of the susceptible host population. Pesticides cycle parasites tend to be density independent. and environmental toxins, infectious diseases However, over several seasons, one would with reservoirs in soil or water, severe weather, expect that increases in wolves (shedding eggs) and accidents tend to have density-independent would lead to increases in infected moose, impacts. For example, the risk to an individual which, in turn, would lead to increases in the bird of flying into a power line during a migra- prevalence of infection among the wolves (eat- tion would not be expected to change in a con- ing infected moose); thus, over a longer term, sistent fashion if the flock size increased or risks of acquiring indirect life cycle parasites decreased. Also, one of the devastating impacts can become density dependent. of some pesticides is that their lethal effects are There is some similarity for arthropod- unabated even as the host populations reach borne parasites (e.g., West Nile virus) to the very low levels (Hickey and Anderson 1968, relationship described above for indirect life Risebrough 1978, Peek 1986). cycle parasites. However, arthropod-borne It is important to note that the significant parasite life cycles are complicated by addi- distinguishing feature between density- tional factors such as the repeated feeding dependent and density-independent diseases is by some arthropods in a season, with their the proportion (rather than the actual number) consequent increased likelihood of acquiring of a susceptible population affected. For exam- parasites. In such cases, the risk of infection ple, if the hosts in a susceptible population have to a susceptible vertebrate host is potentially a 5% risk of mortality (in a density-independent dependent on both the density of infected situation), one would expect approximately vectors and the density of the other infected 5 hosts in a population 100, or approximately vertebrates. Likewise, the risk of infection to 50 hosts in a population 1,000, to die. Thus, a vector is certainly influenced by the density while the total numbers of animals dying of infected vertebrates, but also can be influ- increases in larger populations, the actual pro- enced by the density of other infected vectors portion of animals affected (5%) is unchanged that may infect vertebrates and make them when transmission is density independent. available later in a season to the uninfected Density dependence becomes more com- vectors. It is more difficult to break the cycle in plicated with parasites undergoing indirect this case as both vertebrate hosts and vectors life cycles. For example, among parasitic hel- can contribute to a condition more closely rep- minths, the intestinal tapeworm Echinococcus resenting that of density dependence. While granulosus involves large canids (e.g., wolves, over a shorter term, such as a single season, Canis lupus; coyotes, Canis latrans) as definitive arthropod-borne diseases often tend to be den- hosts and ungulates (e.g., moose, Alces alces; sity independent, the influences of multiple deer, Odocoileus spp.) as intermediate hosts. For feeding each season may lead to an additional a given season, the risk of infection to wolves by density-dependent influence as well, over sev- ingesting the tapeworm infective stage (hydatid eral seasons. cysts) is more directly dependent on the density of hydatid-infected moose than on the density Disease Models of the other infected wolves (who are shedding eggs infective to moose). Likewise, in a given We present two models to use as founda- season the risk of moose becoming parasitized tions for conceptualizing key relationships by ingesting tapeworm eggs is more directly in the field of wildlife diseases. One entails
introduction 11 Parasite nidi are more permanently associated with spe- cific regions and habitat types. Within each nidus is an ecological association termed a biocoenosis, composed of Environment the infective agent, the wild vertebrate reservoir Host species, intermediate hosts or vectors (typically arthropods or other invertebrates), and any Figure 1.6 Parasites, hosts, and their environments are closely intertwined—each affecting the other two in wild vertebrate amplifying hosts. All of these varying degrees. organisms are limited in their geographic and ecological distribution by the environmental an understanding of three general components: determinants of the habitat. These biocoenoses parasites and other causative agents of diseases, allow circulation of the parasites indefinitely the affected vertebrate and invertebratehosts, and can be viewed as integrated wholes and the environment in which these occur. In (Pavlovski 1966). Microscale disease foci are this model each component interacts with the influenced by qualities of the entire ecosystem. other two, and must be described and under- Focal diseases in discrete sites may spread stood in relation to the other two (Fig. 1.6). Any out from the nidi to cause epizootics among change in one can drastically alter the balance susceptible hosts. Susceptible wildlife, humans, of a resulting disease. or other domestic animals might become An earlier and more complex disease involved if they invade an active nidus. This model, proposed in 1939 by Soviet biologist holistic approach to the study of disease ecology Evgeny N. Pavlovsky, first was used to describe has been used as a foundation for the study of arthropod-borne diseases (Pavlovski 1966). It plague in North America (Nelson 1980) as well variously has been termed the Natural Nidality as a number of other diseases (Pavlovski 1966). Doctrine of Transmissible Diseases, the Land- scape Theory of Epidemiology, the Landscape Causes of Disease Theory of Zoonotic Diseases (Pollitzer and Meyer 1961, Pavlovski 1966), and the Natural Nidality Diseases can be caused both by infective agents Theory (Nelson 1980). and by noninfectious causes including toxins, Pavlovski believed that most transmissible tumors, nutritional and metabolic problems diseases exist in nature as discrete foci or nidi traumas, and many others. Most diseases we (sing. nidus, “hearth,” “home”). A nidus is address are caused by infective agents. Infec- defined as that portion of a region with a defi- tive agents most commonly are living organ- nite geographic character, and would be similar isms and typically are classified among five in usage to that of the terms biotope, ecosystem, major kingdoms (Whittaker 1969). Viruses and or habitat type. A nidus can be a small local area prions are additional agents that, while not con- or a broad geographic region (Pavlovski 1966). sidered living entities, also are infective agents Thus, rabies in the range of infected red foxes (Büchen-Osmond 2003). (Vulpes vulpes) in Europe would be an example Living organisms with a parasitic lifestyle of a broad nidus; likewise, plague would be seen comprise the majority of species in the world; as having nidi among dry grasslands (steppes), by one estimate parasites outnumber free-living mountain meadows, and some desert habitats species in a four to one ratio (Zimmer 2000). in western North America and Asia. A nidus Among living organisms, an initial division also can be dynamic, as in the cases of a rabies typically is made between eukaryotic and pro- nidus among red foxes moving across Europe karyotic organisms. Eukaryotic organisms all (Macdonald 1980), or a plague nidus shifting in have double-stranded DNA enclosed within a North America (Barnes 1982). However, most nuclear membrane, an endoplasmic reticulum,
12 introduction mitochondria, Golgi apparatuses, lysosomes, variety of noninfectious diseases to which wild- and other cellular organelles; these organisms life are subject (Fairbrother et al. 1996). Two divide by mitosis or meiosis. Traditionally they that we will address include cancers and toxins. have been distributed among the Kingdoms Protista (single-celled eukaryotes), Plantae, Ani- Role of Diseases in malia, and Fungi (Whittaker 1969) (Appendix 1). Wildlife Populations In contrast, prokaryotic organisms lack true nuclei and have single-stranded DNA; they also Disease agents function by reducing the fitness lack such organelles as mitochondria, endo- of their hosts in a variety of ways (Scott 1988). In plasmic reticula, Golgi apparatuses, and lyso- wildlife management, factors that directly reduce somes (Murray et al. 1999). Prokaryotes divide wildlife numbers have been termed decimating by fission rather than by mitosis or meiosis. factors, and diseases are one of many different Prokaryotes include both the Archaebacteria decimating factors (Leopold 1933). In contrast, and Eubacteria (“true bacteria”) (Murray welfare factors are non-lethal factors such as a et al. 1999) and are classified in the Kingdom shortage of food, water, or cover that reduce wild- Monera (Whittaker 1969) (Appendix 1). life reproductive success (Leopold 1933) or make Viruses lie at the boundary between life and wildlife more susceptible to other mortality fac- inert matter and are not typically included in tors such as predation, accidents, and so on; dis- classifications of living organisms, even though eases also can function as welfare factors. they regularly replicate, mutate, evolve, and Historically, a major focus of wildlife man- serve as significant influences on the evolu- agers was on the role of diseases as decimating tion of their hosts (Villarreal 2004). Classifica- factors, especially among economically impor- tion schemes have emerged for viruses based tant wildlife such as ungulates, waterfowl, and on their proposed evolutionary relationships upland game. These kinds of diseases often (Büchen-Osmond 2003, van Regenmortel are exemplified by microparasites that undergo and Mahy 2004). Recently, considerable inter- multiplication within their hosts. Such diseases est has emerged in the role of infectious pro- commonly produce epizootics where waves of teins (“prions”), which have no nucleic acids infection pass through populations, alternating (Büchen-Osmond 2003) but are important con- with periods in which the pathogen disappears tributors to some wildlife diseases. following a loss of susceptible hosts as they Views about the evolutionary relationships die or survive and become immune. Examples within and between various groups have been include avian cholera in wildfowl (Botzler 1991, changing (Doolittle 1999). We note some of Samuel et al. 2007), hemorrhagic diseases the recent changes in proposed classifications of deer and other ungulates (Howerth et al. (e.g., Adl et al. 2005); however, because of its 2001), or tularemia in rabbits (Mörner and long and well-established history, we base our Addison 2001). The 1988 epizootic of phocine discussions on the traditional five-kingdom distemper virus in the North Sea population of system (Monera, Protista, Fungi, Animalia, harbor seals (Phoca vitulina) is a particularly and Plantae) (Whittaker 1969) in this text well-documented example of a decimating (Appendix 1). Viruses and prions are treated as disease (Hudson et al. 2003). Here the parasite addenda to the five-kingdom system. For each appeared in a series of harbor seal populations major group we provide a general definition of around the coasts of northern Europe, and then the group, a brief description of some of its dis- disappeared following a lack of new susceptible tinctive features, and a summary of any recent animals (Hudson et al. 2003). taxonomic changes. Disease also can serve as a welfare factor by Although our main focus is on diseases reducing the reproductive success of suscep- caused by infective agents, there also is a wide tible animals (Gulland 1995). Among bacteria,
introduction 13 Salmonella pullorum reduces the egg-laying diseases, such as canine distemper or rabies, capacity of ring-necked pheasants (Phasianus may enhance the likelihood of some terrestrial colchicus) by 75% or more, and hatched birds mammals dying from highway mortality or often are stunted and less fit (Biester and other accidents. Schwarte 1965). Brucella abortus infects and Sexual selection also may be influenced by causes abortions in bison (Bison bison), elk parasites and diseases. For example, secondary (Cervus elaphus), and other ungulates (Thorne sexual characteristics of male birds, includ- 2001). Infections by many viruses, including ing brightness or color and vocalizations, may members of the families Parvoviridae, Herpes- signal a male’s overall well-being and freedom viridae, Paramyxoviridae, and Orbiviridae, can from parasites. Males resistant to parasites result in abortion or neonatal death. Because within a species may be more attractive to neonatal mortality or reproductive failure breeding females due to their brighter plum- resulting from infectious agents may be dif- age, more vigorous songs, or other superior ficult to discern, host population size may be mating behaviors, compared to infected males modulated by virus infection in the absence of (Hamilton and Zuk 1982, Loye and Zuk 1991, measurable adult mortality (Poss et al. 2002). MØller 1991, Zuk 1991). Linked to these find- Diseases also can reduce the energy ings is evidence that parasitism may be more resources available for host immunity and lead common among individual animals affected to greater susceptibility to other parasites. Such by developmental asymmetry of secondary parasites benefit when poor nutrition or other sexual characteristics (MØller 1996, MØller environmental conditions reduce the efficiency and Swaddle 1997, Thornhill and MØller of the immune system, making their hosts 1997). Conversely, higher parasite levels may more vulnerable (Chandra and Newberne 1977, contribute to greater asymmetry of secondary Gershwin et al. 1985). For example, normally characteristics. For example, parasite-infected quiescent but opportunistic bacteria carried reindeer (Rangifer tarandus) have less sym- in the intestinal tract (e.g., Salmonella spp.) metrical antlers (Folstad et al. 1996), and mite- or respiratory tract (e.g., Pasteurella spp.) can infected barn swallows (Hirundo rustica) have cause overt disease in the presence of a com- higher levels of asymmetry in wing length and promised immune system. Also, some species tail feathers compared to uninfected members experiencing diseases are more susceptible to of their respective species (MØller 1992). In other stresses such as cold or food shortage turn, such levels of asymmetry could influence (Sheppe and Adams 1957), thus contributing females seeking males for mating (MØller to diminished well-being of individuals and and Swaddle 1997) and thereby affect mating populations. There also are interactions with success and fitness. malnourishment, infections, and environ- The cost in fitness from an infectious bacte- mental chemicals on growth and reproduction rium or virus that kills an animal or weakens it (Porter et al. 1984) to the point where it is susceptible to predation or Also, macroparasites commonly occur as starvation is self-evident. The fitness costs from enzootic infections, more commonly causing arthropods, intestinal nematodes, and some host morbidity than mortality. Sick animals microparasites often are far more subtle (Hart may be less cautious and have slower reflexes 1997). For example, a light parasite load that may than healthy animals (Poulin 1994). Such not noticeably impact a healthy, well-fed adult behavioral changes in animals may lead to bird may severely affect it in times of nutritional greater susceptibility to predation or accidents. or socially related stress, or in conjunction with Likewise, lead poisoning (plumbism) and the physiological demands of laying and incu- botulism intoxication may make waterfowl bating eggs, provisioning nestlings, escaping more susceptible to predation. Neurological from a predator, or fighting with conspecifics
14 introduction (Hart 1997). In cases where male offspring grow well as near extinction of black-footed ferrets larger and more quickly than female offspring, (Mustela nigripes) (Thorne and Williams 1988). parasitism can impede the ability of avian moth- Among macroparasites, there are a num- ers to raise males, shifting the sex ratio and ber of studies with evidence for helminth and affecting population viability; removing their arthropod parasites effectively controlling wild parasites allows the mothers to forage longer and animal populations through reduced survival rear more sons (Reed et al. 2008). Also, among or fecundity of the hosts (Tompkins and Begon polygynous species, pathogens are dispersed by 1999). The parasites involved included two spe- infected females after the resident male dies, cies of fleas, four species of mites, two species and the effects of pathogen-mediated dispersal of bugs, one species of fly, and three species of increases as the harem size (number of females) nematodes; the affected hosts included eight increases (Nunn et al. 2008). species of birds and three of mammals. One of the best documented cases involves Trichostron- gylus tenuis, an intestinal nematode, that helps Can Diseases Regulate drive population cycles of red grouse (Lagopus Wild Populations? lagopus) in Scotland (Potts et al. 1984; Hudson Although the mortality from a disease can et al. 1985; Hudson and Dobson 1989; Dobson and be dramatic, there often is little relationship Hudson 1992; Hudson et al. 1992, 1998, 2003). between observed mortality and the effective- Among toxins, there is strong evidence that ness of a disease in limiting or regulating a host during their regular use, dichlorodiphenyltri- population. For example, avian cholera can be chloroethane (DDT) and other environmental an explosive local disease, killing thousands of toxins suppressed populations of raptors and birds on a given site (Friend 1999). Approxi- fish-eating birds (Hickey and Anderson 1968). mately 37,000 birds died in one California For example, use of DDT depressed peregrine epornitic, yet it was estimated that even such falcon (Falco peregrinus) populations by reduc- severe mortality affected only about 0.5% of the ing eggshell thickness, interfering with cal- California waterfowl populations and that these cium carbonate deposition in eggshells, and losses could be recovered readily on the breeding altering reproductive behaviors (Enderson and grounds (Rosen 1972). Among waterfowl, avian Berger 1970). Significant recovery of several cholera generally is less important than habitat raptorial and other bird species occurred after destruction or hunting in limiting populations. banning many persistent and bioaccumulative However, there are cases where diseases pesticides in the United States (Anderson et al. can substantially influence wildlife popula- 1975, Spitzer et al. 1978, Grier 1982, Grue et al. tions, especially on initial introduction to a 1983, Bolen and Robinson 2003). population. Some microorganisms can sup- Pathogens infecting a broad range of host press wild host populations through reduced species can cause serious problems for endan- survival, reduced fecundity, or both (Scott gered populations (McCallum and Dobson 1988, Tompkins and Begon 1999, Hudson 1995), and species-wide extinctions have been et al. 2003). In a classic case, myxoma virus, linked to diseases. For example, there is good a poxvirus, has caused a long-term depression evidence that avian malaria (Plasmodium relic- of European rabbit (Oryctolagus cuniculus) tum capistranoae) and avian pox (Poxviridae) populations in Australia (Fenner and Ratcliffe have caused some population suppressions, 1965) and Europe (Ross 1982). Rabies also can local extirpations, and even species extinctions temporarily suppress affected host populations among native Hawaiian birds. These losses (Bacon 1985). Canine distemper, a viral disease, involved some complex interactions among has caused severe declines of some African lion the native hosts, introduced species of hosts, (Panthera leo) populations (Morell 1994) as parasites, and vectors, as well as well as habitat
introduction 15 (Warner 1968, van Riper et al. 1986). Interest- of European cattle and were slaughtered in ingly, there also is recent evidence for limited areas around cattle ranches. However, control species recovery among some native Hawaiian of rinderpest in Tanganyika wildlife through birds that did not become extinct (Woodworth use of a vaccine in cattle in the 1950s provided et al. 2005). While it is highly likely that disease evidence that cattle, rather than wildlife, played caused at least some of these extinctions, the evi- a central role as rinderpest reservoirs (Branagan dence still is indirect. The first known definitive and Hammond 1965). Plowright later concluded report of a parasite causing species extinction is that even large populations, in excess of 100,000, the loss of a land snail (Pardula turgida) brought of susceptible wild African ungulates were about by a microsporidian parasite (Steinhausia unable to sustain rinderpest infections in the spp.) (Cunningham and Daszak 1998). absence of cattle (Plowright 1982). Following a Bighorn sheep (Ovis canadensis) introduced worldwide cattle vaccination campaign to combat into Lava Beds National Monument, California, the disease, rinderpest was declared to be only were locally extirpated from effects ofPasteu - the second disease to be eradicated on a worldwide rella multocida pneumonia in July 1980 follow- basis, following smallpox (Anonymous 2011). ing their apparent contact with domestic sheep Mathematical models of microparasitic on adjacent grazing leases (Foreyt and Jessup diseases were developed to assess expected 1982). The response of managers to prevent impacts of these diseases on their hosts this loss was complicated by political conflicts (McCallum and Dobson 1995). Some generaliza- among the several federal and state agencies tions that emerged are that most pathogens do and ranchers with responsibilities for the ani- not depress host population equilibria far below mals or land. There also is evidence that local their disease-free carrying capacity (Anderson populations of prairie dogs (Cynomys spp.) can 1979), and that parasites highly pathogenic for be extirpated by bubonic plague in short-grass individuals usually have only a minor effect on prairies (Kartman et al. 1962, Barnes 1982). host populations. Often, if a disease is detect- Rinderpest, a morbillivirus infection, able at high prevalence, it probably is mild and historically caused substantial reductions among unlikely to be a major problem to an endangered wild ungulate populations in Africa, including species. Also some parasites highly pathogenic local extirpations of some species and significant in the laboratory are unlikely to cause problems changes in the species composition of African in low-density populations because infected ungulates in many regions (Talbot and Talbot animals die before the disease can be spread. 1963, Holmes 1982, Plowright 1982, McCallum These conclusions are subject to two major and Dobson 1995). This introduced pathogen qualifications. First, they apply to single-host swept through southern Africa between 1890 species models, and many pathogens implicated and 1899 and killed up to 90% of the populations in extinctions of one host have other reservoir of some native wild species (Plowright 1982). hosts in which they are relatively benign (van Rinderpest is benign in its ancient cattle host Riper et al. 1986, Thorne and Williams 1988). (McCallum and Dobson 1995), but highly virulent Thus if a pathogen is a generalist and an to the wildebeest (Connochaetes taurinus) and cape endangered species is susceptible, the pathogen buffalo (Syncerus caffer), as well as introduced can cause the endangered species to decline if it cattle recently exposed to this morbillivirus has a sympatric host species (reservoir species). (Plowright 1982). Rinderpest exemplifies a Second, the mathematical models assume the disease in populations lacking past exposure or disease primarily increases host mortality. If innate immunity; the causative virus infected a the disease decreases fecundity, then diseases large proportion of the susceptible populations at high prevalence may have a significant and mortality was high. Wild ungulates were impact on host populations without causing blamed as reservoir hosts for susceptible breeds increased deaths (McCallum 1994); DDT had
16 introduction such effects (Enderson and Berger 1970). elements affecting host population numbers Similar generalizations have been drawn from over time (Scott 1988). It often is difficult to models of helminth and other macroparasitic clearly distinguish the specific role of diseases infections (Anderson 1980). as decimating factors. It is even more difficult Where diseases affect hosts differentially, to document their roles as welfare factors in occurrence of sympatric populations of vertebrate interactions with nutrition, stress, genetic prob- hosts with a shared parasite can result in one lems, predator–prey interactions, accidents, host benefiting by a greater impact of the para- climate, or other ancillary factors. site on the other (Hudson and Greenman 1998). Diseases may exert selective pressures on Parasite-mediated competition can act when an various social behaviors. For example, mat- invading species introduces a parasite to a vulner- ing behaviors, social avoidance, group size, able resident species. One example is the likely and group isolation may have been affected by significant impact on the native red squirrel selection pressures to reduce transmission of (Sciurus vulgaris) of the introduction of a parapox pathogens (Loehle 1995). virus by the introduced eastern gray squirrel A final, positive note is that while parasites (S. carolinensis) (Tompkins et al. 2002). Similarly, can be detrimental to host fitness in one envi- diseases introduced with domestic dogs have ronment, they can be beneficial to it in another. exerted significant impact on rarer and endan- There is some evidence that parasitized gered indigenous species as Ethiopian wolves individuals may enjoy a selective advantage (Canis simensis) (Laurenson et al. 1998) and wild over unparasitized conspecific hosts in some dogs (Lycaon picta) (Kat et al. 1995). Likewise, circumstances (Thomas et al. 2000). bighorn sheep are more susceptible to the effects of Pasteurella multocida than are domestic sheep, Overview and Summary and the pasteurellae caused a likely extirpation of bighorns from Lava Beds National Monument Overall, wildlife diseases can be serious deci- (Foreyt and Jessup 1982, Foreyt 1989). Parasite- mating factors to affected host populations. They mediated competition also has been proposed can suppress and regulate these populations, as a mode of action among white-tailed deer cause local extirpations, and have been associ- (Odocoileus virginianus) in gaining competitive ated with species extinction. Most of the empha- advantage over moose (Alces alces) in areas of sis in this book will focus on the role of diseases the eastern United States and Canada (Kearney as decimating factors. Additionally, diseases can and Gilbert 1976). The parasite Parelaphostron- serve as welfare factors and may reduce repro- gylus tenuis is a meningeal nematode with little ductive success or increase the likelihood of or no impact on white-tailed deer; in contrast, death from other causes. Diseases can influence other ungulate species are far more susceptible sexual selection among hosts. Further, diseases (Lankester 2001). However, this purported role of may interact with other extrinsic factors such regulating moose populations by the parasite has as nutrition and stress in their hosts, and even been controversial (Nudds 1990). In this context, have been proposed as a means by which their it has been proposed that where a parasite species hosts can gain an advantage over a competing infects more than one host species, the pathogen host species. With this brief introduction, we will be least pathogenic to the host with the larger are ready to begin a more detailed look into the range and more pathogenic to the species with fascinating world of wildlife diseases. limited range; such a relationship has potentially We begin (Chapter 2) with a summary of serious impacts for rare and endangered species the tools and strategies wildlife hosts can use in with limited distributions (Price et al. 1988). protecting themselves from the effects of vari- However, it must be recognized that para- ous diseases they encounter, so as to be able to site infections or toxins are only one of several clearly address these defense mechanisms in
introduction 17 later discussion of these diseases. In many ways, and evolutionary approach of key taxonomic the relationships between hosts and parasites groups, rather than emphasizing a clinical and can be described as an evolutionary “dance,” a pathological perspective. Hosts and parasites constant competition with each side seeking to are constantly interacting with each other in a respond appropriately to the moves of the other dynamic fashion. Each species tries to optimize to optimize their own success and avoid a loss its own success, and the degree of sophistica- of fitness. Considering disease in an evolution- tion that has evolved in that process is remark- ary context, there never are ideal phenotypes able. Methods of transmission and types of (Ewald 1994). Hosts and parasites each are full host defenses are among the more striking of compromises, and each is under considerable examples. It is a sense of this larger picture we selective pressure as it evolves an optimal level of wish to emphasize. success. Many of the discomforts felt by organ- In approaching a study of wildlife diseases, isms experiencing a disease (e.g., fever, diarrhea, we remind readers that we work from the per- allergies, anxiety) are connected with contempo- spective of contemporary Western science. This rary defense mechanisms (Ewald 1994). approach has led to enormous advancements We then assess the major macroparasites in human understanding of the natural world, by taxonomic group in Chapters 3 through 5. including significant insights into the under- For purposes of this text, we provide the taxo- standing of the health and diseases of wildlife. nomic information appropriate to a level that It also is a system with some limitations and is most practical for an introduction to wildlife often is characterized as being hierarchical, diseases; the actual taxonomic levels addressed elitist, and dualistic in its approach; many argue among various parasite and host groups are not that no one cultural worldview is privileged consistent. Next we address eukaryotic single- (Klukhohn and Leighton 1946/1962, Feyerabend celled organisms by basic taxonomic group in 1987, Abram 1996, Nakashima 1998, Berkes Chapters 6 and 7. 1999), and we acknowledge that Western sci- Then our emphasis is upon prokaryotic and ence is only one of a number a ways of viewing other microparasites, including bacteria and an understanding of wildlife health and dis- viruses, in Chapters 8 through 10. Understand- eases. Of course, we also recognize the many ing the basic life cycles and life history strate- benefits and values of using Western science as gies of each parasite group as their selective a foundation for understanding the world. pressures work to optimize their biological suc- Finally, the major emphasis is on disease in cess, the problems they encounter, and how they wildlife populations rather than a focus on overcome them, underlie an understanding of individuals. The effects of wildlife diseases on how these diseases ultimately can be managed. individual animals is covered well in veterinary In Chapter 11 we address a few special top- references focusing on captive wildlife (Fraser ics such as noninfectious diseases, including and Mays 1986, Fowler et al. 2003) as well toxins, cancers, prion diseases, and the global as more general veterinary texts (Fraser and amphibian decline. While of more recent inter- Mays 1986). There also are some valuable refer- est, these issues increasingly are recognized as ences covering more specialized topics (Murphy having considerable importance for wildlife. et al. 1999, Mullen and Durden 2002, Finally, in Chapter 12 we address specific Stockham and Scott 2002). applications and special topics, including emer- gent diseases, special problems, and a look at future wildlife disease studies, management, Literature Cited and conservation. Abram, D. 1996. A more-than-human world. In Our goal is to provide a broader understand- A. Weston (editor), An invitation to environmental ing of wildlife diseases from an ecological philosophy. Oxford University Press, New York.
18 introduction Acha, P. N., and B. Szyfres. 2003. Influenza. Barnes, A. M. 1982. Surveillance and control of Pp. 155–172 in Zoonoses and communicable bubonic plague in the United States. Symposia of disease common to man and animals. Pan the Zoological Society of London 50:237–270. American Health Organization Scientific and Bender, J. 2007. Chimpanzees, antibiotic resistance— Technical Publication No. 580, Washington, DC. Uganda (02). International Society for Infectious Adl, S. M., A. G. B. Simpson, M. A. Farmer, Diseases.
introduction 19 Carpenter, M. A., M. J. Appel, M. E. Roelke-Parker, Davis, J. W., L. H. Karstad, and D. O. Trainer (edi- L. Munson, H. Hofer, M. East, and S. J. O’Brien. tors). 1970. Infectious diseases of wild mammals. 1998. Genetic characterization of canine Iowa State University Press, Ames, IA. distemper virus in Serengeti carnivores. Davis, J. W., L. H. Karstad, and D. O. Trainer (edi- Veterinary Immunology and Immunopathology tors). 1981. Infectious diseases of wild mammals. 65:259–266. 2nd ed. Iowa State University Press, Ames, IA. Chandra, R. K., and P. M. Newberne. 1977. Nutri- DelGuidice, G. D., L. D. Mech, and U. S. Seal. 1990. tion, immunity, and infection. Plenum Press, Effects of winter undernutrition on body composi- New York. tion and physiological profiles of white-tailed deer. Christiansen, K. H., T. E. Carpenter, K. P. Snipes, Journal of Wildlife Management 54:539–550. D. W. Hird, and G. Y. Ghazikhanian. 1992. Dindal, D. L. 1975. Symbiosis: Nomenclature Restriction endonuclease analysis of Pasteurella and proposed classification. The Biologist multocida isolates from three California turkey 57:129–142. premises. Avian Diseases 36:272–281. Dobson, A. P., and P. J. Hudson. 1992. Regulation Clarke, C. H. D. 1971. The beast of Gévaudan. and stability of a free-living host–parasite system: Natural History 80:44–51, 66–73. Trichostrongylus tenuis in red grouse. II: Population Clayton, D. H., and J. Moore (editors). 1997. Host– models. Journal of Animal Ecology 61:487–498. parasite evolution: General principles and avian Doolittle, W. F. 1999. Phylogenetic classification models. Oxford University Press, Oxford, UK. and the universal tree. Science 284:2124–2128. Cleaveland, S., and C. Dye. 1995. Maintenance of Dörr, R., and E. Gold. 1932. Zur Frage der “Viru- a microparasite infecting several host species: lenz” der Tuberkelbazillen. Zeitschrift für Immu- Rabies in the Serengeti. Parasitology 111:S33–S47. noforschung 74:7–24. Cranfield, M., L. Gaffikin, J. Sleeman, andM. Rooney. Dudley, J. P. 2004. Global zoonotic disease surveil- 2002. The mountain gorilla and conservation lance: An emerging public health and biosecurity medicine. Pp. 282–296 in A. A. Aguirre, imperative. BioScience 54:982–983. R. S. Ostfeld, G. M. Tabor, C. House, and Dunn, A. M. 1969. The wild ruminant as reservoir M. C. Pearl (editors), Conservation medicine: host of helminth infection. In A. McDiarmid Ecological health in practice. Oxford University (editor), Diseases in free-living wild animals. Press, Oxford, UK. Symposia of the Zoological Society of London Cunningham, A. A., and P. Daszak. 1998. Extinc- No. 24. Academic Press, London, UK. tion of a species of land snail due to infection Edwards, M. A., and U. McDonnell (editors). 1982. with a microsporidian parasite. Conservation Animal disease in relation to animal conserva- Biology 12:1139–1141. tion. Symposia of the Zoological Society of Daszak, P., and A. A. Cunningham. 1999. Extinc- London No. 50. Academic Press, London, UK. tion by infection. Trends in Ecology and Enderson, J. H., and D. D. Berger. 1970. Pesticides: Evolution 14:279. Eggshell thinning and lowered production of Daszak, P., and A. A. Cunningham. 2002. Emerging young in prairie falcons. BioScience 20:355–356. infectious diseases: A key role for conservation Ewald, P. W. 1994. Evolution of infectious disease. medicine. Pp. 40–61 in A. A. Aguirre, Oxford University Press, Oxford, UK. R. S. Ostfeld, G. M. Tabor, C. House, and M. C. Pearl Fairbrother, A., L. N. Locke, and G. L. Hoff. 1996. (editors). Conservation medicine: Ecological health Noninfectious diseases of wildlife. 2nd ed. Iowa in practice. Oxford University Press, Oxford, UK. State University Press, Ames, IA. Daszak, P., A. Strieby, A. A. Cunningham, Fenner, F., and F. N. Ratcliffe. 1965. Myxomatosis. J. E. Longcore, C. C. Brown, and D. Porter. 2004. Cambridge University Press, New York. Experimental evidence that the bullfrog (Rana Feyerabend, P. 1987. Farewell to reason. Verso, catesbeiana) is a potential carrier of chytridiomy- London, UK. cosis, an emerging fungal disease of amphibians. Folstad, I., P. Arneberg, and A. J. Karter. 1996. Herpetological Journal 14:201–207. Antlers and parasites. Oecologia 105:556–558. Davis, J. W., and R. C. Anderson (editors). 1971. Foreyt, W. J. 1989. Fatal Pasteurella haemolytica Parasitic diseases of wild mammals. Iowa State pneumonia in bighorn sheep after direct contact University Press, Ames, IA. with clinically normal domestic sheep. American Davis, J. W., R. C. Anderson, L. Karstad, and Journal of Veterinary Research 50:341–344. D. O. Trainer. 1971. Infectious and parasitic dis- Foreyt, W. J., and D. A. Jessup. 1982. Fatal pneumonia eases of wild birds. Iowa State University Press, of bighorn sheep following association with domes- Ames, IA. tic sheep. Journal of Wildlife Diseases 18:163–168.
20 introduction Fouchier, R. A. M., V. Munster, A. Wallensten, Ecology of infectious diseases in natural popula- T. M. Bestebroer, S. Herfst, D. Smith, tions. Cambridge University Press, Cambridge, UK. G. F. Rimmelzwaan, B. Olsen, and Hamilton, W. D., and M. Zuk. 1982. Heritable true A. D. M. E. Osterhaus. 2005. Characterization of fitness and bright birds: A role for parasites? a novel Influenza A virus hemagglutinin subtype Science 218:384–387. (H16) obtained from black-headed gulls. Journal Harder, J. D., and R. L. Kirkpatrick. 1994. Physiolog- of Virology 79:2814–2822. ical methods in wildlife research. Pp. 275–306 in Fowler, M. E. (editor). 1981. Wildlife diseases of T. A. Bookhout (editor), Research and manage- the Pacific Basin and other countries. Fruitridge ment techniques for wildlife and habitats. The Printing, Sacramento, CA. Wildlife Society, Bethesda, MD. Fowler, M. E., R. E. Miller, and Morris Animal Foun- Harder, T. C., M. Kenter, M. J. Appel, M. E. Roelke- dation. 2003. Zoo and wild animal medicine. Parker, T. Barrett, and A. D. Osterhaus. 1995. 5th ed. Saunders, St. Louis, MO. Phylogenetic evidence of canine distemper virus Fraser, C. M., and A. Mays. 1986. The Merck veterinary in Serengeti’s lions. Vaccine 13:521–523. manual. 6th ed. Merck & Co., Inc., Rahway, NJ. Hart, B. L. 1997. Behavioural defence. Pp. 59–77 Friend, M. 1976. Philosophical considerations. in D. H. Clayton and J. Moore (editors), Host– Pp. 7–18 in L. A. Page (editor), Wildlife diseases. parasite evolution: General principles and avian Plenum Press, New York models. Oxford University Press, Oxford, UK. Friend, M. 1999. Avian cholera. Pp. 75–92 in Hawkins, C. E., C. Baars, H. Hesterman, M. Friend and J. C. Franson (editors), Field man- G. J. Hocking, M. E. Jones, B. Lazenby, D. Mann, ual of wildlife diseases: General field procedures N. Mooney, D. Pemberton, S. Pyecroft, M. Restani, and diseases of birds. U.S. Geological Survey, and J. Wiersma. 2006. Emerging disease and Biological Resources Division, Washington, DC. population decline of an island endemic, the Friend, M., R. G. McLean, and F. J. Dein. 2001. Tasmanian devil Sarcophilus harrisii. Biological Disease emergence in birds: Challenges for the Conservation 131:307–324. twenty-first century. The Auk 118:290–303. Heddleston, K. L. 1972. Avian pasteurellosis. Frobisher, M. 1962. Fundamentals of microbiology. Pp. 219–251 in M. S. Hofstad, B. W. Calnek, W. B. Saunders Company, Philadelphia, PA. C. F. Helmboldt, W. M. Reid, and J. N. W. Yoder Gershwin, M. E., R. S. Beach, and L. S. Hurley. (editors), Diseases of poultry. Iowa State Univer- 1985. Nutrition and immunity. Academic Press, sity Press, Ames, IA. Orlando, FL. Hickey, J. J., and D. W. Anderson. 1968. Chlorinated Glickman, F. S. 1987. “A ring around the rosie” (the hydrocarbons and eggshell changes in raptorial rash that was). Journal of the American Academy and fish-eating birds. Science 162:271–272. of Dermatology 16:1282–1282. Hoff, G. L., and J. W. Davis (editors). 1982. Nonin- Gordus, A. G. 1993. Notes on the first known avian fectious diseases of wildlife. Iowa State Univer- cholera epizootic in wildfowl in North America. sity Press, Ames, IA. Journal of Wildlife Diseases 29:367. Holmes, J. C. 1982. Impact of infectious disease Gould, S. J. 2002. The structure of evolutionary agents on the population growth and geographical theory. Belknap Press of Harvard University distribution of animals. Pp. 37–51 in Press, Cambridge, MA. R. M. Anderson and R. M. May (editors), Graczyk, T. K. 2002. Zoonotic infections and con- Population biology of infectious diseases. servation. Pp. 220–228 in R. S. O. A. A. Aguirre, Springer-Verlag, New York. G. M. Tabor, C. House, and M. C. Pearl (editors), Hopla, C. E., and A. K. Hopla. 1994. Tularemia. Conservation medicine: Ecological health in Pp. 113–126 in G. W. Beran (editor), Handbook of practice. Oxford University Press, New York. zoonoses. CRC Press, Boca Raton, FL. Grier, J. W. 1982. Ban of DDT and subsequent of Howerth, E. W., D. E. Stallknecht, and P. D. Kirkland. reproduction in bald eagles. Science 218:1232–1235. 2001. Bluetongue, epizootic hemorrhagic disease, Grue, C. E., W. J. Fleming, D. G. Busby, and and other orbivirus-related diseases. Pp. 77–97 in E. F. Hill. 1983. Assessing hazards of organophos- E. S. Williams and I. K. Barker (editors), Infec- phate pesticides to wildlife. Transactions of the tious diseases of wild mammals. Iowa State North American Wildlife and Natural Resources University Press, Ames, IA. Conference 48:200–220. Hudson, P. J., and A. P. Dobson. 1989. Population Gulland, F. M. D. 1995. Impact of infectious diseases biology of Trichostrongylus tenuis, a parasite of on wild animal populations: A review. Pp. 20–51 economic importance for red grouse manage- in B. T. Grenfell and A. P. Dobson (editors), ment. Parasitology Today 5:283–291.
introduction 21 Hudson, P. J., A. P. Dobson, and D. Newborn. 1985. in the United States. Institute of Medicine, Cyclic and non-cyclic populations of red grouse: National Academies Press, Washington, DC. A role for parasitism. In D. Rollinson and Leopold, A. S. 1933. Game management. Charles R. M. Anderson (editors), Ecology and genetics Scribner’s Sons, New York. of host-parasite interactions. Linnean Society Levin, B. R. 1996. The evolution and maintenance Symposium Series, Vol. 11. of virulence in microparasites. Emerging Infec- Hudson, P. J., A. P. Dobson, and D. Newborn. 1998. tious Diseases 2:93–102. Prevention of population cycles by parasite Linnell, J. D., R. A. C., Z. Andersone, removal. Science 282:2256–2258. J. C. B. L. Balciauskas, L. Boitani, S. Brainerd, Hudson, P. J., and J. Greenman. 1998. Competition U. Bretienmoser, I. Kojola, O. Liberg, J. Loe, mediated by parasites: Biological and theoreti- H. Okarma, H. C. Pedersen, C. Promberger, cal progress. Trends in Ecology and Evolution H. Sand, E. J. Solberg, H. Valdmann, and 13:387–390. P. Wabakken. 2002. The fear of wolves: A review Hudson, P. J., D. Newborn, and A. P. Dobson. 1992. of wolf attacks on humans. Norsk Institut for Regulation and stability of a free-living host– Naturforskning (NINA), Trondheim, Norway. parasite system: Trichostrongylus tenuis in red Loehle, C. 1995. Social barriers to pathogen trans- grouse. I: Monitoring and parasite reduction exper- mission in wild animal populations. Ecology iments. Journal of Animal Ecology 61:477–486. 76:326–335. Hudson, P. J., A. Rizzoli, B. T. Grenfell, Longhurst, W. M., A. S. Leopold, and R. F. Dasmann. H. Heesterbeek, and A. P. Dobson (editors). 2003. 1952. A survey of California deer herds: Their The ecology of wildlife diseases. Oxford Univer- ranges and management problems. California sity Press, Oxford, UK. Department of Fish and Game, Bureau of Game Kahn, L. H. 2006. Confronting zoonoses, linking Conservation Game Bulletin No. 6. human and veterinary medicine. Emerging Loye, J. E., and M. Zuk (editors). 1991. Bird–parasite Infectious Diseases 12:556–561. interactions. Oxford University Press, Oxford, UK. Kartman, L., S. F. Quan, and R. R. Lechleitner. Macdonald, D. W. 1980. Rabies and wildlife: A 1962. Die-off of a Gunnison’s prairie dog colony biologist’s perspective. Oxford University Press, in central Colorado. II: Retrospective determina- Oxford, UK. tion of plague infection in flea vectors, rodents, Mahy, B. W. J., and C. C. Brown. 2000. Emerging and man. Zoonoses Research 1:201–224. zoonoses: Crossing the species barrier. Revue Kat, P. W., K. A. Alexander, J. S. Smith, and Scientifique et Technique Office International L. Munson. 1995. Rabies and African wild dogs des Epizooties 19:33–40. in Kenya. Proceedings of the Royal Society B: Majumdar, S. K., J. E. Huffman, F. J. Brenner, and Biological Sciences 262:229–233. A. I. Panah (editors). 2005. Wildlife diseases: Kearney, S. R., and F. F. Gilbert. 1976. Habitat use Landscape epidemiology, spatial distribution by white-tailed deer and moose on sympatric and utilization of remote sensing technology. range. Journal of Wildlife Management Pennsylvania Academy of Science, Easton, PA. 40:645–657. Malpas, R. C. 1977. Diet and the condition and Klukhohn, C., and D. Leighton. 1946/1962. The growth of elephants in Uganda. Journal of Navaho. Doubleday and Co., Garden City, NY. Applied Ecology 14:489–504. Kverno, N. B., and G. C. Mitchell. 1976. Vampire Margolis, L., G. W. Esch, J. C. Holmes, A. M. Kuris, bats and their effect on cattle production in Latin and G. A. Schad. 1982. The use of ecological America. World Animal Review 17:1–7. terms in parasitology (report of an ad hoc Lankester, M. W. 2001. Extrapulmonary lungworms committee of the American Society of Parasitolo- of cervids. Pp. 228–278 in W. M. Samuel, gists). Journal of Parasitology 68:131–133. M. J. Pybus, and A. A. Kocan (editors). Parasitic McCallum, H. 1994. Quantifying the impact of diseases of wild mammals. Iowa State University disease on threatened species. Pacific Conserva- Press, Ames, IA. tion Biology 1:107–117. Laurenson, K., C. Sillero-Zubiri, H. Thompson, McCallum, H., and A. Dobson. 1995. Detecting dis- F. Shiferaw, S. Thirgood, and J. Malcolm. 1998. ease and parasite threats to endangered species Disease as a threat to endangered species: and ecosystems. Trends in Ecology and Evolution Ethiopian wolves, domestic dogs and canine 10:190–194. pathogens. Animal Conservation 1:273–280. McDiarmid, A. 1962. Diseases of free-living wild Lederberg, J., R. E. Shope, and J. S. C. Oakes. 1992. animals. Food and Agriculture Organization of Emerging infections: Microbial threats to health the United Nations, Rome, Italy.
22 introduction McDiarmid, A. (editor). 1969. Diseases in free-living G. M. Tabor, C. House, and M. C. Pearl (editors), wild animals. Symposia of the Zoological Society Conservation medicine: Ecological health in of London No. 24. Academic Press, London, UK. practice. Oxford University Press Oxford, UK. McNeill, W. H. 1977. Plagues and peoples. Anchor Nakashima, D. J. 1998. Conceptualizing nature: Press, Doubleday, Garden City, NY. The cultural context of resource management. Mills, J. N., B. A. Ellis, J. E. Childs, J. K. T. McKee, Nature and Resources 34:8–22. J. I. Maiztegui, C. J. Peters, T. G. Ksiazek, and Nelson, B. C. 1980. Plague studies in California: P. B. Jahrling. 1994. Prevalence of infection The roles of various species of sylvatic rodents in with Junin virus in rodent populations in the plague ecology in California. Proceedings of the epidemic area of Argentine hemorrhagic fever. Vertebrate Pest Conference 9:89–96. American journal of Tropical Medicine and Nudds, T. 1990. Retroductive logic in retrospect: Hygiene 51:554–562. The ecological effects of meningeal worms. MØller, A. P. 1991. Parasites, sexual ornaments, and Journal of Wildlife Management 54:396–402. mate choice in the barn swallow. Pp. 328–343 in Nunn, C. L., P. H. Thrall, K. Stewart, and J. E. Loye and M. Zuk (editors), Bird–parasite Inter- A. H. Harcourt. 2008. Emerging infectious actions. Oxford University Press, Oxford, UK. diseases and animal social systems. Evolutionary MØller, A. P. 1992. Parasites differentially increase Ecology 22:519–543. the degree of fluctuating symmetry in secondary Page, L. A. 1976. Wildlife diseases. Plenum Press, sexual characters. Journal of Evolutionary New York. Biology 5:691–699. Pavlovski, E. N. 1966. Natural nidality of transmissible MØller, A. P. 1996. Parasitism and developmental diseases. University of Illinois Press, Urbana, IL. instability of hosts: A review. Oikos 77:189–196. Peek, J. M. 1986. Pesticides and herbicides. MØller, A. P., and J. P. Swaddle. 1997. Asymmetry, Pp. 205–223 in A review of wildlife management. developmental stability, and evolution. Oxford Prentice-Hall, Englewood Cliffs, NJ. University Press, Oxford, UK. Plowright, W. 1982. The effects of rinderpest and Moore, J. 2002. Parasites and the behavior of ani- rinderpest control on wildlife in Africa. Pp. 1–28 mals. Oxford University Press, Oxford, UK. in M. A. Edwards and U. McDonnell (editors), Morell, V. 1994. Serengeti’s big cats going to the Symposia of the Zoological Society of London dogs. Science 264:1664. No. 50. Academic Press, London, UK. Mörner, T., and E. Addison. 2001. Tularemia. Poland, J., T. J. Quan, and A. M. Barnes. 1994. Pp. 303–312 in E. S. Williams and I. K. Barker Plague. Pp. 93–112 in G. W. Beran and J. H. Steele (editors), Infectious diseases of wild mammals. (editors), Handbook of zoonoses, Section A: Iowa State University Press, Ames, IA. Bacterial, rickettsial, chlamydial, and mycotic. Mullen, G., and L. Durden (editors). 2002. Medical CRC Press, Boca Raton, FL. and veterinary entomology. Academic Press, Pollitzer, R., and K. F. Meyer. 1961. The ecology of Boston, MA. plague. Pp. 433–501 in J. M. May (editor), Studies Munro, I. 1996. “Ring around the rosie” mini-FAQ. in disease ecology. Hafner Publishing Company,
introduction 23 Poulin, R. 1994. Meta-analysis of parasite-induced Samuel, W. M., M. J. Pybus, and A. A. Kocan. 2001. behavioural changes. Animal Behaviour Parasitic diseases of wild mammals. 2nd ed. Iowa 48:137–146. State University Press, Ames, IA. Pratt, H. D. 1963. Epidemiology and control Scott, M. E. 1988. The impact of infection and disease of vector-borne diseases. U.S. Public Health on animal populations: Implications for conserva- Service, Communicable Disease Center, tion biology. Conservation Biology 2:40–56. Atlanta, GA. Seal, U. S., L. J. Verme, and J. J. Ozoga. 1981. Physi- Price, P. W., M. Westoby, and B. Rice. 1988. ologic values. Pp. 17–33 in W. R. Davidson, Parasite-mediated competition: Some predictions F. A. Hayes, V. F. Nettles, and F. E. Kellogg (edi- and tests. American Naturalist 131:544–555. tors), Diseases and parasites of white-tailed deer. Read, C. P. 1970. Parasitism and symbiology. Miscellaneous Publication No. 7. Tall Timbers Ronald Press, New York. Research Station, Tallahassee, FL. Reed, L. J., and H. A. Muench. 1938. A simple Sheppe, W. A., and J. R. Adams. 1957. The patho- method of estimating fifty percent endpoints. genic effect of Trypanosoma duttoni in hosts under American Journal of Hygiene 27:493–497. stress conditions. Journal of Parasitology 43:55–59. Reed, T. E., F. Daunt, M. E. Hall, R. A. Phillips, Shope, R. E. 1927. The quantity of cholesterol in S. Wanless, and E. J. A. Cunningham. 2008. the blood serum of the guinea pig as an inher- Parasite treatment affects maternal investment in ited character: Its relation to natural resistance sons. Science 321:1681–1682. to tuberculosis, and to tuberculosis infection. Risebrough, R. W. 1978. Pesticides and other Journal of Experimental Medicine 45:59–68. toxicants. In H. P. Brokaw (editor), Wildlife and Simpson, V. R. 2002. Wild animals as reservoirs America. Council on Environmental Quality, of infectious diseases in the UK. The Veterinary Washington, DC. Journal 163:128–146. Roelke-Parker, L. M. M. E., C. Packer, R. Kock, Slemons, R. D., and M. Brugh. 1994. Influenza. S. Cleaveland, M. Carpenter, S. J. O’Brien, Pp. 385–395 in G. W. Beran (editor), Handbook of A. Pospischil, R. Hofmann-Lehmann, J. Lutz, zoonoses. CRC Press, Boca Raton, FL. G. L. M. Mwamengele, M. N. Mgasa, Snipes, K. P., T. E. Carpenter, J. L. Corn, R. W. Kasten, G. A. Machange, B. A. Summers, and D. W. Hirsh, D. W. Hird, and R. H. McCapes. M. J. G. Appel. 1996. A canine distemper virus 1988. Pasteurella multocida in wild mammals and epidemic in Serengeti lions (Panthera leo). birds in California: Prevalence and virulence for Nature 379:441–445. turkeys. Avian Diseases 32:9–15. Rosen, M. N. 1972. The 1970–71 avian cholera Snipes, K. P., D. W. Hirsh, R. W. Kasten, L. M. Hansen, epornitic’s impact on certain species. Journal of D. W. Hird, T. E. Carpenter, and R. H. McCapes. Wildlife Diseases 8:75–78. 1989. Use of an rRNA probe and restriction Rosen, M. N., and A. I. Bischoff. 1949. The 1948–49 endonuclease analysis to fingerprintPasteurella outbreak of fowl cholera in birds in the San multocida isolated from turkeys and wildlife. Francisco Bay area and surrounding counties. Journal of Clinical Microbiology 27:1847–1853. California Fish and Game 35:185–192. Soulsby, E. J. L. 1968. Helminths, arthropods and Rosen, M. N., and A. I. Bischoff. 1950. The epide- protozoa of domesticated animals (Mönnig). miology of fowl cholera as it occurs in the wild. Williams and Wilkins Company, Baltimore, MD. Transactions of the North American Wildlife Soulsby, E. J. L. 1974. Parasitic zoonoses, clinical and Conference 15:147–154. experimental studies. Academic Press, New York. Ross, J. 1982. Myxomatosis: The natural evolution Spitzer, P. R., R. W. Risebrough, W. Walker, of the disease. Pp. 77–95 in Symposium of the R. Hernandez, A. Poole, D. Puleston, and Zoological Society of London No. 50. Academic I. C. Nisbet. 1978. Productivity of ospreys in Press, London, UK. Connecticut–Long Island increases as DDE Rupprecht, C. E., K. Stöhr, and C. Meredith. 2001. residues decline. Science 202:333–335. Rabies. Pp. 3–36 in E. S. Williams and I. K. Barker Stenseth, N. C., B. B. Atshabar, M. Begon, (editors), Infectious diseases of wild mammals. S. R. Belmain, E. Bertherat, E. Carniel, Iowa State University Press, Ames, IA. K. L. Gage, H. Leirs, and L. Rahalison. 2008. Samuel, M. D., R. G. Botzler, and G. A. Wobeser. Plague: Past, present, and future. Public Library 2007. Avian cholera. Pp. 239–269 in of Science Medicine 5:0009–0013 (e0003). N. J. Thomas, D. B. Hunter, and C. T. Atkinson Stockham, S. L., and M. A. Scott. 2002. Fundamen- (editors), Infectious diseases of wild birds. tals of veterinary clinical pathology. Iowa State Blackwell Publishing Professional, Ames, IA. University Press, Ames, IA.
24 introduction Talbot, L. M., and M. H. Talbot. 1963. The wilde- Warren, R. J., and R. L. Kirkpatrick. 1978. Indices beest in western Masailand, East Africa. Wildlife of nutritional status in cottontail rabbits fed Monographs 12:1–88. controlled diets. Journal of Wildlife Management Taylor, L. H., and M. E. J. Woodhouse. 2000. Zoono- 42:154–158. ses and the risk of disease emergence. Poster 122 in Wehr, E. E. 1971. Nematodes. Pp. 185–233 in International Conference on Emerging Infectious J. W. Davis, R. C. Anderson, L. Karstad, and Diseases. Centers for Disease Control, Atlanta, GA. D. O. Trainer (editors), Infectious and parasitic Thomas, F., R. Poulin, J.-F. Guégan, Y. Michalakis, diseases of wild birds. Iowa State University and F. Renaud. 2000. Are there pros as well as cons Press, Ames, IA. to being parasitized? Parasitology Today 16:533–536. Whittaker, R. H. 1969. New concepts of kingdoms Thomas, N. J., D. B. Hunter, and C. T. Atkinson. of organisms. Science 163:150–160. 2007. Infectious diseases of wild birds. Blackwell Williams, E. S. 2001. Paratuberculosis and other Publishing Professional, Ames, IA. mycobacterial diseases. Pp. 361–371 in Thorne, E. T. 2001. Brucellosis. Pp. 372–395 in E. S. Williams and I. K. Barker (editors), E. S. Williams and I. K. Barker (editors), Infec- Infectious diseases of wild mammals. Iowa State tious diseases of wild mammals. Iowa State University Press, Ames, IA. University Press, Ames, IA. Williams, E. S., and I. K. Barker (editors). 2001. Thorne, E. T., and E. S. Williams. 1988. Disease and Infectious diseases of wild mammals. 3rd ed. endangered species: The black-footed ferret as a Iowa State University Press, Ames, IA. recent example. Conservation Biology 2:66–74. Wilson, G. S., and A. A. Miles. 1964. Topley and Thornhill, R., and A. P. MØller. 1997. Developmen- Wilson’s Principles of bacteriology and immu- tal stability, disease and medicine. Biological nity. 5th ed. Williams and Wilkins Company, Reviews (Cambridge) 72:497–548. Baltimore, MD. Tompkins, D. M., and M. Begon. 1999. Parasites Wobeser, G. A. 1981. Diseases of wild waterfowl. can regulate wildlife populations. Parasitology Plenum Press, New York. Today 15:311–313. Wobeser, G. A. 2006. Essentials of disease in wild Tompkins, D. M., A. W. Sainsbury, P. Nettleton, animals. Blackwell Publishing Professional, D. Buxton, and J. Gurnell. 2002. Parapoxvirus Ames, IA. causes a deleterious disease in red squirrels Woodroffe, R. 1999. Managing disease threats associated with UK population declines. to wild mammals. Animal Conservation Proceedings of the Royal Society B: Biological 2:185–193. Sciences 269:529–533. Woodworth, B. L., C. T. Atkinson, D. A. LaPointe, Van Dyke, F. 2003. Conservation biology: Founda- P. J. Hart, C. S. Spiegel, E. J. Tweed, tions, concepts, applications. McGraw-Hill, C. Henneman, J. LeBrun, T. Denette, R. DeMots, Boston, MA. K. L. Kozar, D. Triglia, D. Lease, A. Gregor, van Regenmortel, M. H. V., and B. W. J. Mahy. 2004. T. Smith, and D. Duffy. 2005. Host population Emerging issues in virus taxonomy. Emerging persistence in the face of introduced vector- Infectious Diseases 10:8–13. borne diseases: Hawaii amakihi and avian van Riper, C. H., III, S. G. van Riper, M. L. Goff, and malaria. Proceedings of The National Academy M. Laird. 1986. The epizootiology and ecological of Sciences of the United States of America significance of malaria in Hawaiian land birds. 102:1531–1536. Ecological Monographs 56:327–344. Woolhouse, M. E. J., and S. Gowtage-Sequeria. Villarreal, L. P. 2004. Are viruses alive? Scientific 2005. Host range and emerging and reemerg- American 291:101–105. ing pathogens. Emerging Infectious Diseases von Braunschweig, A. 1979. Wildkrankheiten. 11:1842–1847. Landbuch-Verlag, Gmbh, Hannover, West Wylie, C. M. 1970. The definition and measurement Germany. of health and disease. Public Health Reports Wämoscher, L., and H. Stöcklin. 1927. Infektions- 85:100–104. versuche mit enzelnen Tuberkelbazillen, durchge- Zimmer, C. 2000. Parasite rex: Inside the bizarre führt mit der mikrurgischen Methode. Centralblatt world of nature’s most dangerous creatures. Free für Bakteriologie, Parasitenkunde und Infektionsk- Press, New York. rankheiten. 1 Abteilung. Originale 104:86–90. Zuk, M. 1991. Parasites and bright birds: New data Warner, R. E. 1968. The role of introduced diseases and a new prediction. Pp. 317–327 in J. E. Loye in the extinction of the endemic Hawaiian and M. Zuk (editors), Bird–parasite interactions. avifauna. The Condor 70:101–120. Oxford University Press, Oxford, UK
introduction 25