SOIL AND WATER AS RESERVOIRS

In this life history model, we consider a vari­ety of organisms, ranging from bacteria that depend on soil or water for their survival (Lis­teria monocytogenes, Nocardia spp.) to organ­isms whose strong propensity to survive and endure in soil or water requires managers to consider the environment as an important part of these organisms’ reservoirs and life history strategies.

LISTERIA MONOCYTOGENES

causative agent Listeria spp. are non- sporing, nonbranching, facultatively anaerobic, short, gram-positive rods (App. 1: Table 7) (Bille et al. 1999). Of at least seven species of Listeria currently considered (Bille et al. 1999), only L. monocytogenes is of regular importance as a potential pathogen for wildlife (Morner 2001a).

host range and geographic distribution Listeria monocytogenes has a worldwide distribution, and has been isolated from at least 50 species of mammals (Gray and Killinger 1966, Morner 2001a), numerous birds (Eveland 1971, Nilsson and Soderind 1974, Fenlon 1985), aquatic reptiles and amphibians (Botzler et al. 1973), and a variety of biting arthropods and other insects, crustaceans, snails, and leeches (Gray and Killinger 1966, Botzler et al. 1973, Farber and Peterkin 1991, Morner 2001a).

reservoirs and transmission Listeria monocytogenes is considered an adaptable envi­ronmental bacterium existing both as an animal pathogen and a plant saprophyte, with a wide array of regulated virulence factors (Low and Donachie 1997).

A transient carrier state can occur in some animals, including humans (Farber and Peterkin 1991, Low and Donachie 1997). However, Listeria monocytogenes almost never is transmitted directly between animals; rather, it is acquired as point source infections from the natural environment, such as contaminated silage and plants (Weis and Seeliger 1975, Low and Donachie 1997). Mammals probably are most commonly exposed by ingesting contami­nated food (Morner 2001a), and this is probably true for birds as well (Gray and Killinger 1966). Although ingestion is the most common route, there also are cases of respiratory, cutaneous, and ocular transmission (Marth 1994).

clinical effects Among mammals, lis- teric infections commonly are associated with encephalitis in ruminants, septicemia in mono­gastric mammals, and uterine infections result­ing in abortions among a variety of others (Gray and Killinger 1966, Low and Donachie 1997, Morner 2001a). Among birds, septicemia seems the most common syndrome (Gray and Killinger 1966), but there have been a variety of pathologic conditions reported, with little consistency in the reported signs and symptoms (Eveland 1971).

population effects Listeric infections rarely affect large numbers of mammals or birds at a given time, although losses can be high on occasion (Kornilova 1956). More typi­cally, the organism tends to have most impact on individual animals that gain the bacteria through point source infections.

special problems No consistent special problems are noted.

control Control of Listeria monocytogenes in the environment is not yet feasible (Eveland 1971, Morner 2001a).

BACILLUS ANTHRACIS

causative agent Bacillus spp. are aero­bic, gram-positive, endospore-producing rods (App. 1: Table 7). Of the approximately 50 cur­rently recognized species, B. anthracis, the cause of anthrax, is of greatest significance as an ani­mal pathogen (Logan and Turnbull 1999).

host range and geographic distribution All mammals appear to be susceptible to anthrax; ruminants seem par­ticularly susceptible (Whitford and Hugh-Jones 1994), and species such as impala (Aepyceros melampus) and bison (Bison spp.) may die in only a matter of hours after initial exposure. Anthrax is an ongoing problem among wild herbivores in many parts of the world, includ­ing Wood Buffalo National Park, Alberta, Canada (Gates et al. 1995); the southeastern United States (Kellogg et al. 1970); Kruger National Park, South Africa (Pienaar 1967); Etosha National Park, Namibia (Ebedes 1977, Lindeque et al. 1996); and to a lesser extent in western Europe (Wetzel and Rieck 1972, Gates et al. 2001). In contrast, carnivores are less sus­ceptible and less likely to die from an infection (Gates et al. 2001). Humans are susceptible to anthrax, but also appear to have an intermedi­ate resistance (Blood and Radostits 1989).

While birds generally are resistant, ostriches (Struthio camelus), crows (Corvus spp.), and ducks appear susceptible to anthrax (Whitford and Hugh-Jones 1994); however, only ostriches have been reported naturally infected (Gates et al. 2001). Bacillus anthracis has a close to worldwide distribution (Whitford and Hugh- Jones 1994, Gates et al. 2001).

reservoirs and transmission The sta­tus of B.

It is proposed that under conditions of alka­line pH, high soil moisture, and the presence of organic matter, B. anthracis may undergo cycles of spore germination, vegetative cell outgrowth, and resporulation, leading to an increase in spore density in soil (Van Ness 1971). However, there also is evidence that B. anthracis cannot compete against normal saprophytic bacteria in soil (Minnett and Dhanda 1941), perhaps because some competing organisms can pro­duce antibiotics or competitively use key nutri­ents (Sterne 1959). Also, death of an infected animals often does not lead to extensive spore contamination of soil from blood (Lindeque and Turnbull 1994). Thus it is likely that B. anthra- cis depends primarily on multiplication within a host rather than in soil or water (Gates et al. 2001). However, the spores have the ability to survive in soil for over 40 years (Umeno and Nobata 1938, Manchee et al. 1990). In Kruger National Park, South Africa, spores were recov­ered from bones estimated to be approximately 200 years old (de Vos 1990). Thus, for manage­ment purposes, it is important to understand this organism’s endurance in the environment.

It is postulated that carnivores and scav­engers, including carrion feeders such as buzzards and vultures, feeding on anthrax carcasses may transmit the organisms and spores to new sites (Ebedes 1977, Lindeque and Turnbull 1994). However, more recent evidence suggests that scavenging by vertebrates is not a critical factor in the life cycle of B.

Transmission can occur through several means, including ingestion, inhalation, direct contact, or arthropod bite (Gates et al. 2001). Herbivores can become infected by grazing, especially when dry periods lead them to crop vegetation close to the soil or to graze more in moist depressions containing abundant spores (Gates et al. 2001). Epizootics following rain are speculated by some to be a result of germi­nation of spores and multiplication in soil, but by others as the rain bringing buried spores to the surface and onto growing vegetation (Dudley 2006). Rutting behavior by bison, including wallowing, during dry periods may result in dust with high concentrations of spores. Necrophilic insects may contaminate forage with spores or vegetative cells (Pienaar 1967, de Vos 1990, Hugh-Jones and deVos 2002) that later are ingested by susceptible ungulates; mechanical transmission of the bacteria also may occur via hematophagous insects (Turell and Knudson 1987).

clinical effects Among wildlife, gas­trointestinal infections caused by ingestion of spores and pulmonary infections caused by inhalation are the most common effects (Gates et al. 2001). Once entering the host, spores germinate into vegetative bacterial cells that are transported to regional lymph nodes, where the bacteria multiply and even­tually produce a septicemia and exotoxin pro­duction (Gates et al. 2001). Although effects vary considerably among wildlife, common observed effects are blood that is dark and clots poorly, hemorrhages in many tissues and organs, edema, enteritis, and splenomeg­aly (Gates et al. 2001).

population effects The effects of anthrax on wild mammal populations are influenced by the frequency of epizootics, their severity, and the specific susceptibility of spe­cies, sex, and age classes (Gates et al. 2001). Massive, catastrophic mortality may occur among some species such as impala (Prins and Weyerhauser 1987) and roan antelope (Hippo­tragus equines) (de Vos and Scheepers 1996), affecting all members of the populations.

special problems In addition to some­times catastrophic mortalities among African ungulates, anthrax has exacerbated the complex problems of brucellosis and tuberculosis among bison of Wood Buffalo National Park, Canada.

control As with many diseases, surveil­lance of high-risk populations for mortality is an important step in management (Hugh-Jones and deVos 2002). Among wild ungulate populations, moving unaffected herds away from contami­nated sites is one strategy that has been used, although the herds have usually returned within a few weeks (Choquette et al. 1972). Once an epizootic begins, control commonly is limited to removing diseased carcasses as sources of envi­ronmental contamination by incineration, use of quicklime, or deep burial of carcasses, preferably at the site they are found (Choquette et al. 1972, Gates et al. 2001, Hugh-Jones and deVos 2002). Quarantine of domestic and wild animals whose movements can be controlled is of considerable importance (Hugh-Jones and deVos 2002). In cases of very large carcasses, covering them with branches of large thorn bushes has discouraged scavengers from opening the carcasses (Gates et al. 2001), although there is other evidence that deterrence or exclusion of vertebrate scavengers likely is ineffective (Bellan et al. 2013). Applica­tion of dilute formaldehyde to the exterior of car­casses also has been effective (Gates et al. 1995); it stops carcass scavenging and disinfects the environment with negligible long-term environ­mental impacts (Hugh-Jones and deVos 2002).

Burning of a habitat in which anthrax is occurring sometimes is used in African parks (Dudley 2006); this probably does not effec­tively kill spores, but does move animals away from browse contaminated by necrophilic blow flies that contaminate the vegetation when they vomit their meals. Burning will remove the spore-covered leaves near a carcass that the flies have been feeding upon. Rinsing of spores from leaves also is why anthrax is believed to stop with the onset of the rainy season in Africa.

Vaccination is a common control technique among domestic cattle in anthrax-infected habitats (Kaufmann 1993). Vaccination of over 10,000 bison in Wood Buffalo National Park and surrounding regions was conducted, but it was not possible to evaluate the effects (Choquette et al. 1972). However, aerial vaccination of sus­ceptible wild herbivores in Kruger National Park has helped to end anthrax epizootics there (de Vos and Scheepers 1996). Antibiotic treat­ment has been used for valuable animals exposed to anthrax (Hugh-Jones and deVos 2002).

Clostridium botulinum Avian botulism is an intoxication rather than an infection, although there are elements in the ecology of the bacterium and the disease that overlap with the definition both of a contagious disease as well as a vector-borne disease (Wobeser 1997a, Rocke and Bollinger 2007). The bacterium and its ecology are addressed in this section because an understanding of the causative bacterium and its unique relation to soil and water is essential to instituting any control.

causative agent The genus Clostridium comprises a very diverse set of microorgan­isms that generally are gram-positive, anaer­obic, spore-forming rods (App. 1: Table 7). Spores form only in the absence of air (Allen et al. 1999). Clostridium botulinum is one of at least 30 species of medical importance in this genus; it can produce botulinum neuro­toxin, the most lethal naturally produced toxin known (Allen et al. 1999). There are seven toxi­genic types of botulism toxin (A through G) (Rocke and Bollinger 2007). Type C toxin can be divided further into two types, C (C_x) and C (C) (Allen et al. 1999). Of the toxin types, C and E are most commonly reported as caus­ing disease in wildlife. The production of type C toxin is dependent on infection of the vege­tative bacterial cell by a specific bacteriophage (bacterial virus) that carries a neurotoxin gene (Ecklund et al. 1987).

host range and geographic distribution For wildlife, almost all signifi­cant occurrences of botulism are among birds, and involve types C and E (Rocke and Friend

1999). Waterfowl epizootics usually are a result of type C toxin whereas fish-eating birds such as loons and gulls more typically are affected by type E toxin (Rocke and Friend 1999).

With the exception of the turkey vulture (Cathartes aura) and some other scaveng­ing birds, virtually all birds are susceptible to type C toxin (Rocke and Friend 1999, Rocke and Bollinger 2007). Among wild birds, water­fowl and shorebird populations experience the greatest losses from type C botulism, but the disease frequently also causes mortality in gulls, and has been reported from upland game birds, herons, raptors, and songbirds (Rocke and Friend 1999). Type C botulism has been confirmed for at least 263 species of birds, from 39 families (Rocke and Bollinger 2007). Type E botulism is reported frequently in gulls and loons and also has been reported in water­fowl (Rocke and Friend 1999); it has been con­firmed in 31 species among 10 families of birds (Rocke and Bollinger 2007).

Type C avian botulism has been known in North America since the early 1900s and has been reported in wild birds from at least 28 countries or territories, and from every con­tinent except Antarctica (Rocke and Bollinger 2007). Type E botulism has been reported primarily in the Great Lakes region of North America, with a few cases in Alaska and the Salton Sea of California; there also is a report from France (Rocke and Bollinger 2007). Avian botulism has been considered the most impor­tant disease of migratory birds on a worldwide basis (Rocke and Friend 1999).

RESERVOIRS AND TRANSMISSION ClθStrid- ium spp. are ubiquitous in nature, and their principal habitats are the soil; C. botulinum is regularly found in soil and wetlands (Smith 1978, Dodds 1992). Clostridium botulinum spores have the capacity to survive for at least several years (Smith et al. 1982, Wobeser et al. 1987, Rocke and Friend 1999), and some clostridial spores can persist in the environment for 30 years or more (Smith and Sugiyana 1988).

Among susceptible waterfowl, type C botu­lism often occurs in late summer and early fall (Rocke and Friend 1999). Decaying animal matter typically has been considered a good substrate to support growth of C. botulinum type C and production of toxin, whereas decay­ing vegetation has been described as a poor substrate (Bell et al. 1955). However, there is conflicting data on this issue, with some evi­dence that vegetation also may serve as a sub­strate at times (Quortrup and Holt 1941, Rocke and Bollinger 2007).

Human activity also can increase the available substrate for toxin production. Flooding and draining, as well as drainage of pesticides and other chemicals into wetlands may kill aquatic life and provide more sub­strate for toxin production. Decaying vegetation and raw sewage are other potential sources of nutrients and energy, and botulism outbreaks in recent years have been associated with sewage oxidation ponds (Rocke and Bollinger 2007).

Several factors, including higher pH, salin­ity, and temperature, as well as lower oxidation­reduction potential in sediments and the water column are associated with an increased likelihood of botulism epizootics in wetlands (Rocke and Samuel 1999). An increase in the risk of botulism epizootics may be related to environmental conditions that elevate wetland sediment temperatures and decrease dissolved oxygen, such as the presence of decaying organic matter and shallow water (Rocke and Friend 1999, Rocke and Samuel 1999).

There are a number of models proposed for the occurrence of botulism in wildlife populations. Among susceptible waterfowl, type C botulism often occurs in late sum­mer and early fall (Rocke and Friend 1999). There is evidence that a carcass-maggot cycle underlies many of these cases of Type C avian botulism in North America (Wobeser 1997a, 1997b; Rocke and Friend 1999; Rocke and Bollinger 2007). Vertebrate carcasses are par­ticularly important, as they provide the organic substrate, an anaerobic environment, and the warm temperatures optimal for growth and toxin production (Wobeser and Galmut 1984, Wobeser 1997a). Animals in a marsh environ­ment ingest spores frequently, and healthy animals often have spores in their intestines or liver (Reed and Rocke 1992). Following the death of an animal for any reason, those with botulism spores can be invaded by C. botuli­num as anaerobic conditions associated with carcass decay develop, leading to toxin produc­tion (Notermans et al. 1980, Smith and Turner 1987). The maggots of sarcophagous flies and other invertebrates feeding on these toxic ver­tebrate carcasses may contain large amounts of toxin (Duncan and Jensen 1976, Hubalek and Halouzka 1991), as well as bacterial cells and spores (Wobeser 1997a). Birds ingesting such maggots die from the toxin and their carcasses subsequently become substrate for clostridia.

Wobeser (1997a) argues that toxin produc­tion and cases of type C botulism may occur commonly at a low level in many marshes. He proposes that the number of secondary botu­lism intoxications resulting from any single toxic carcass occurring in a marsh will be influ­enced by the total number of carcasses occur­ring in a marsh, the probability of a carcass containing spores, the probability of a carcass persisting until toxin-bearing maggots emerge, and the contact rate between live birds and toxin (Wobeser 1997a).

Other models have been proposed as well (Rocke and Bollinger 2007). Some late-winter/ early-spring epizootics of botulism in water­birds are associated with epizootics in the pre­vious fall and the availability of toxic maggots that have settled to the bottom of the wetland being available to diving ducks the subsequent spring (Hubalek and Halouzka 1991). Type C botulism among fish-eating birds at the Salton Sea, California, has been associated with spores germinating in the gut of stressed or morbid fish and high summer temperatures (Rocke et al. 2004, Rocke and Bollinger 2007). Cases of type C botulism among gulls at landfills in Europe and the Middle East are associated with spores brought by birds that subsequently germinate and replicate in the rich organic environment during increasing tempera­ture conditions. Additional epizootiological patterns, including botulism in passerines, in raptors associated with chicken farms, and as a result of gut toxicogenesis also have been reported (Rocke and Bollinger 2007).

clinical effects The disease, botulism, technically is caused by a bacterial intoxication rather than an infection by metabolizing bac­teria of a living host. The toxin is synthesized as a single inactive protein that is released during lysis of the bacterial cells (Lyerly and Allen 1997). Once activated, the botulism toxin functions as a neurotoxin that blocks acetyl­choline release, leading to an acute, ascending flaccid paralysis (Simpson 1986, Allen et al. 1999). Particular manifestations may include difficulty flying, leg weakness, and droop­ing wings; as the toxin has greater effect, the birds may have flaccid paralysis of the legs and wings, and the nictitating membrane of the eye will become immobilized (Wobeser 1997b). Among infected waterfowl, managers often distinguish three classes: I, alert, but cannot fly; II, difficulty walking and holding head erect (“limberneck”); and III, prostrate, para­lyzed, and cannot blink (Hunter et al. 1970).

Botulism is suspected whenever a large number of birds are observed dying at sites with a past history of botulism mortality, especially in late summer in North America. Diagnosis typically is confirmed with a mouse­protection test, with new methods being devel­oped (Wobeser 1997b, Ferreira et al. 2004, Karner and Allerberger 2006).

population effects In North America, there have been at least 13 different years in which mortalities of 100,000 or more waterfowl have been reported in type C epizootic events, and at least three years (1910, 1982, 1997) in which epizootics involving a million or more birds have been reported (Rocke and Friend 1999, Rocke and Bollinger 2007). In addition, botulism mortality figures probably are underestimates because of the considerable difficulty in locating carcasses during epizootics (Stutzenbaker et al. 1986, Cliplef and Wobeser 1993).

Despite the heavy mortalities reported, it is not clear whether botulism has limited or suppressed continental waterfowl populations (Rocke and Bollinger 2007). In one study of mid-continent mallards (Anas platyrhynchos), the impact of botulism could not be assessed with the information available (Samuel 1992). Assessments also are complicated by lack of detection of many smaller epizootics, the likely underestimates of birds affected for many epi­zootics, and differential susceptibility of many species (Rocke and Bollinger 2007).

special problems These are summarized above under Population Effects.

control Prevention, control, and treat­ment of birds each are considerations in addressing botulism among wild birds. Pre­vention generally is designed to reduce the production of toxin and curtail exposure of birds to toxin (Wobeser 1997b). Recommenda­tions include eliminating factors that lead to decaying matter, and reducing organic input (e.g., sewage) into wetlands; some steps include keeping water levels stable to avoid fish kills or invertebrate deaths, and careful surveillance to remove any vertebrate carcasses to minimize formation of toxic maggots (Rocke and Friend 1999, Rocke and Bollinger 2007). However, the effectiveness of these techniques has not been tested (Wobeser 1997b).

Control following onset of a botulism epizo­otic should be directed at minimizing exposure of birds to botulism toxin (Wobeser 1997b). This can involve dispersal of birds from the epizootic site, but most commonly entails col­lection and burning or burying of carcasses to prevent a build-up of toxic maggots (Hunter 1970, Wobeser 1997b, Rocke and Friend 1999). There is limited evidence that carcass removal can help reduce the risk of botulism to healthy birds of an area (Reed and Rocke 1992, Rocke and Bollinger 2007). However, this is compli­cated by the difficulty in finding many of the carcasses during an epizootic (Stutzenbaker et al. 1986, Cliplef and Wobeser 1993, Rocke and Bollinger 2007).

While most management emphasis is focused on preventing and controlling botu­lism epizootics, botulism-intoxicated waterfowl can be treated successfully; however, the high cost and logistical difficulty in larger epizootics usually limit treatment to endangered or high- profile species (Rocke and Friend 1999). Con­sidering the three classes (I, II, III) described in the Clinical Effects section, botulism treatment typically involves giving all sick birds access to freshwater and shade, flushing the proventricu­lus and crop of class II and III birds with water to remove toxin and toxic maggots, as well as administration of antitoxin, if available, to class II and III birds (Wobeser 1997b, Rocke and Friend 1999, Rocke and Bollinger 2007). Use of an eye ointment for severely paralyzed birds is also of value.

other organisms Nocardia spp. are genuine soil organisms that inhabit the soil of most coun­tries; however, they only rarely cause disease in animals (Beaman and Sugar 1983, Hinton and Bale 1991, Brown et al. 1999, Acha and Szyfres 2001). Many bacteria considered in other life history patterns also have the capacity to survive in the environment for extended periods and to be acquired from soil or water by susceptible hosts (Hinton and Bale 1991). These include Salmonella spp. (Winfield and Groisman 2003), Mycobacterium avium (Metchock et al. 1999), Fusobacterium necrophorum (Rosen 1962, Garcia et al. 1971), and Pasteurella multocida (Bredy and Botzler 1989, Price et al. 1992).

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