RESERVOIRS TYPES USED BY BACTERIA AND VIRUSES

As with transmission patterns, there also can be considerable variation in the life history strategies u sed by bacteria and viruses for their long-term survival; transmission patterns and reservoir models often are closely linked.

We simplify this complexity by emphasiz­ing major types of reservoirs observed and providing salient examples of pathogens using these models. We have built on some of the initial insights of Shope (1965) regarding epidemiological patterns among viruses and rickettsiae, and have modified them in light of more recent knowledge of wildlife pathogens. There always is a risk in simplifying such complex matters. For example, reducing such complexity into simple broad patterns does not always allow a full appreciation of the rich and subtle variations that may occur among the bacteria and viruses classified within a reser­voir type as they work out their own specific strategies for success. Also, this simplification does not always fully acknowledge that some bacteria and viruses may opportunistically use more than one reservoir type for their survival and success.

Despite the risks of simplified systems, most pathogenic bacteria and viruses of impor­tance to wildlife diseases can be reasonably described and understood in the context of one (or more) of these reservoirs, and there are advantages to thinking in these broader patterns.

We define five basic reservoir types. We first consider two reservoir models in which the microparasite depends primarily or exclusively on infected vertebrate hosts; one is a reservoir dependent on apparently healthy carriers (latent infections), and the other is a reservoir dependent on the continuing presence of clini­cally active infections among the vertebrate hosts. We then consider two reservoir models in which the bacteria and viruses require both a vertebrate and an invertebrate host. One is a reservoir requiring both a vertebrate and an arthropod; in the other reservoir type, the mic­roparasite uses a combination of a vertebrate and a helminth capable of infecting that verte­brate as a reservoir of the microparasite. Finally, we address bacteria and viruses that use soil or water as an integral part of their reservoir.

Within these basic life history models, there is considerable variation in the specific strate­gies these bacteria and viruses employ for their long-term survival and success. In contrast to most eukaryotic parasites, for example, many bacteria and viruses are able to capitalize on two or even more life history models, as their circumstances warrant.

We first give a brief overview of these pat­terns in this introduction, and then develop each of them more fully in Chapters 9 (on bacte­ria) and 10 (on viruses). The particular bacteria and viruses addressed are often, but not always, significant mortality factors among wildlife. In other cases, the bacteria and viruses may be particularly good examples of microparasites using a specific reservoir, are important emerg­ing diseases, or may illustrate special problems managers encounter with wildlife diseases.

Vertebrate-dependent Reservoirs

Latent Infections (Apparently Healthy Carriers)

In the latent infection reservoir, bacteria and viruses persist in the tissues and organs of a vertebrate host for extended periods, some­times for the life of the infected host, and are shed by the infected carriers as the source of infection to other susceptible hosts. This type of reservoir is used by many pathogens infecting the intestinal or respiratory tracts of vertebrates. Most commonly, newly infected animals become clinically ill on initial infec­tion by the microparasite, recover, and then become recovered carriers, serving as a source of infection for other susceptible animals. There are a limited number of cases in which parasites live in apparently healthy carrier hosts that typically do not experience clinical illness (i.e., silent carriers), but these carriers then serve as a source of infection for other, susceptible hosts (i.e., indicator hosts) (Shope 1965).

Latent infections may be the single most common reservoir type among bacteria. Examples of bacteria frequently using this life history pattern are found in a wide variety of taxonomic groups, and include Salmonella spp. (Matyas 1988), Brucella abortus (Thorne 2001), Chlamydophila (Chlamydia) psittaci (Meyer and Eddie 1932-33), Pasteurella multo- cida and Mannheimia (Pasteurella) haemolytica (Miller 2001), Mycoplasma spp.

This reservoir type also is common among viruses and involves many herpesviruses (Burnet and Williams 1939), including duck plague virus (Burgess et al. 1979), as well as hantaviruses (Childs et al. 1994), some retroviruses (Worley 2001), foot-and-mouth disease viruses (Thomson et al. 2001), and influenza viruses (Acha and Szyfres 2003).

Most known examples of silent carrier infections involve viruses, and include herpes­viruses such as malignant catarrhal fever virus (alcelaphine herpesvirus) (de Kock and Neitz 1950, Heuschele and Reid 2001), pigeon her­pesvirus (Vindevogel and Pastoret 1981, Aini et al. 1993), and the Herpes B virus (Sabin and Wright 1934); another example is the African swine fever virus (Montgomery 1921). Viruses associated with silent carriers typically are con­tracted at an early age, cause mild or inapparent infections, and may persist indefinitely in the silent carrier hosts. In some cases, the bacteria and viruses may be difficult to detect in silent carriers (Shope 1965).

Depending on the site of infection in the vertebrate, the bacteria and viruses may be shed in feces, urine, mucous membranes, saliva, or conjunctival fluids. Typically, susceptible animals are infected by direct or close contact with an infected carrier, an infective aerosol, or ingestion of food or water contaminated by a shedding animal.

The coexistence of infection and immunity often is a delicate balance that can easily shift from the immune system successfully sup­pressing the infective agent to the agent causing a relapse. Clinical relapses often occur among recovered carriers and can be exacerbated by stress (Shope 1965).

Although this reservoir type is widespread among bacteria and viruses, there still is only limited information on effective prevention or control methods. One general strategy is to separate susceptible animals from sources of infection, including infected carrier ani­mals and habitats contaminated with infective agents by carriers.

Clinically Active Infections

In this reservoir type, the bacteria and viruses are dependent on an unbroken series of clini­cally active infections among susceptible hosts to sustain the parasite population among verte­brate hosts of a region. Currently infected hosts or recovered immune hosts are not considered part of the pool of susceptible hosts that must be available (Swinton et al. 2002).

Very few bacteria depend primarily on clini­cal infections as their primary reservoir for long-term sustainability. Mycobacterium spp., such as M. bovis in free-ranging deer (Schmitt et al. 1997), are presented as one example. Neisseria gonorrhoeae, a venereal disease among humans, as well as some virulent strains of Streptococcus spp., also can fit into this reservoir type (Knapp and Koumans 1999, Ruoff et al. 1999). This reservoir type is found more com­monly among viruses, including rabies and other lyssaviruses (Baer 1975), some avian pox­viruses (Karstad 1971b), morbilliviruses such as rinderpest virus (Rossiter 2001), and many papillomaviruses (Sundberg et al. 2001).

Bacteria and viruses in this life history group typically are transmitted through direct contact with infected animals or contaminated fomites, ingestion of fecally contaminated food or water, droplet inhalation, or salivary con­tamination, including bites. Parasites in this reservoir type tend to be density-dependent, and their risk of transmission is increased as the density of susceptible animals is increased; conversely, the risk of transmission tends to decline as the density of susceptible hosts declines. Overall, the effects ofimmunity are the same as death; they remove susceptible hosts and effectively reduce the density of the popula­tion susceptible to infection.

For infections typically leading to rapid dis­ease outcomes (immunity or death), as caused by some viruses, success of the microparasite is increased with relatively shorter incubation times between initial infection and the start of shedding, relatively longer time periods during which hosts are able to shed the bacteria and viruses, higher numbers (intensity) of bacteria and viruses shed by the clinically ill host over time, and an efficient means of transmission to new susceptible hosts. With such parasites, epizootics may occur at regular intervals, partly depending on the rate at which the host population increases during recovery from a previous epizootic. New epizootics begin both when the population of susceptible animals becomes dense enough to support a chain of transmission and when the infective agent is reintroduced from another, infected host popu­lation. Among many fast-acting viral diseases, surviving hosts have a strong, even lifelong immunity and do not contribute further to maintaining the parasite (Swinton et al. 2002).

In such cases the susceptible host populations often are composed of relatively young and previously unexposed hosts.

For a few bacteria and viruses, such as mycobacteriae and poxviruses, clinical diseases tend to develop slowly and persistently, even­tually resulting in either a domination by the parasite and death of the host, or domination of the parasite by the host and resolution of the disease through host immunity; yet in many cases the host may die from other causes before the disease balance is resolved. In such slow- developing diseases as tuberculosis, host mor­tality typically is well below the replacement rate from typical host reproductive success and there is an adequate addition of young, previ­ously unexposed hosts to sustain the bacterium.

Distinguishing whether bacteria and viruses are using a recovered carrier or a clini­cal infection type of reservoir occasionally can be difficult, as when there appears to be a very low prevalence of carriers detected in an infected population. This can occur because the detectable numbers of microparasites in the recovered carriers drop below detection levels based on current laboratory techniques, as with Salmonella spp.; it may only be after a host is stressed that the microparasite num­bers rise again to become detectable (Williams and Newell 1970). But in general, bacteria and viruses in the clinically active infection res­ervoir do not use previously infected hosts as continuing sources of infections following their recovery, nor do they generally causes clinical relapses in these former hosts, in contrast to bacteria and viruses using a carrier reservoir. In some cases, bacteria and viruses may have a carrier state in one species, but can cause epizootics in another. Examples include some avian influenza viruses (Webster et al. 1992) and Mycoplasma gallisepticum (Dhondt et al. 1998) in birds. Generally, however, hosts expe­riencing these epizootics are not able to sustain the microparasite in the absence of the other infected carrier species. In such cases, the bac­teria and viruses still are classified as part of the latent infection reservoir.

Control typically is directed at breaking the chain of infection by reducing the density of susceptible hosts to a level below the parasite’s requirement to maintain a chain of infection. Two strategies commonly have been employed. Population reduction has been used to reduce the density of infected and susceptible animals (e.g., rabies, rinderpest). Also, vaccination pro­grams typically have been used with captive wildlife, domestic animals, and humans, when vaccines are available. Use of vaccination in free-living wildlife is an emerging technology that holds considerable promise.

Invertebrate-Vertebrate Reservoirs

Two additional models are addressed under this general category: arthropod-vertebrate and helminth-vertebrate reservoirs. Both reservoirs are complicated from an ecological standpoint because they involve interactions with two hosts (invertebrate, vertebrate), each with very different physiological and ecological charac­teristics. With the helminth-vertebrate system, the physiological and ecological constraints superimposed by any helminth intermediate hosts add an even greater complexity to the relationships considered.

Arthropod-Vertebrate Reservoir

This reservoir type generally entails the combi­nation of a vertebrate host and a hematophagous arthropod. Common examples of arthropods involved include fleas, mosquitoes, lice, biting flies, ticks, and mites. Occasionally, nonhema- tophagous arthropods such as flies feeding on conjunctival fluids or other infected materials can regularly transmit infectious agents. Bac­teria and viruses using this reservoir typically multiply in their invertebrate host, and thus have a propagative form of transmission.

Examples of bacteria classified in this res­ervoir type include tick-borne parasites such as Borrelia burgdorferi, the cause of Lyme disease (Brown and Burgess 2001), Francisella tularen- sis, the cause of tularemia (Morner and Addison 2001), Anaplasma spp, the cause ofgranulocytic ehrlichiosis (Davidson and Goff 2001), and the flea-borne bacterium Yersinia pestis, causative agent of sylvatic and bubonic plague (Gasper and Watson 2001). Examples of viruses using this reservoir type include numerous arbovi­ruses (Karstad 1971a, Yuill and Seymour 2001), such as the mosquito-borne flaviviruses of West Nile disease and eastern and western equine encephalitis, the Culicoides-borne hemorrhagic disease orbiviruses of cervids (Howerth et al. 2001), and the flea-borne myxoma and other, mosquito-borne, poxviruses (Karstad 1971b, Robinson and Kerr 2001).

There are important distinctions in the disease ecology between bacteria and viruses transmitted by free-flying arthropods or ticks, compared to those transmitted by more host­bound ectoparasites such as lice and fleas (Smith 1982). Arthropods that live much of their life independent of the host often are more affected by the ecological constraints of their specific habitat requirements, including seasonality. This is particularly true regarding the seasonal availability of arthropods in more temperate regions where over-wintering strategies may become an important problem for many of these bacteria and viruses. Consequently, the success of parasites using this reservoir type is affected by the specific ecological and habitat constraints of both vertebrate and invertebrate.

Control strategies typically are aimed at reducing arthropod populations or preventing infected arthropods from reaching susceptible hosts. Less commonly, treating or immunizing susceptible vertebrate hosts is used.

Helminth-Vertebrate Reservoir

Bacteria and viruses in this reservoir model are in a complex relationship involving both vertebrate hosts and one or more helminth parasites infecting that vertebrate. As with the arthropod-helminth model, the ecological rela­tionships in this model can be complicated by the special physiological and ecological factors resulting from involvement of both helminths and vertebrates, in addition to any intermediate hosts for the carrier helminth. One important feature proposed for this model is that the mic­roparasite may survive for extended periods in the helminth between periods in which it causes clinical disease among vertebrates (Syverton et al. 1947, Shope 1965).

One well-established example involving an obligatory relationship with helminths and vertebrates involves members of the bacte­rial genus Neorickettsia (Rikihisa et al. 2004). Claims of possible helminth-vertebrate reser­voirs have been made for some viruses (Shope 1965); both the classic swine fever (hog cholera) virus (Shope 1958) and swine influenza virus (Shope 1941, 1943a, 1943b; Sen et al. 1961) cycle between swine and a swine lungworm, Meta- strongylus spp. A similar claim for a helminth­vertebrate reservoir involving swine influenza virus among rats and mice, with a rat nema­tode (Strongyloides ratti), also has been made (Shotts et al. 1968). However, the evidence that helminths are an essential part of the reservoir for these viruses has been seriously challenged (Wallace 1977). Another bacterium, Brucella spp., recovered from the harbor seal (Phoca vitulina richardsi), may use infected lungworms (Parafilaroides spp.) as part of its reservoir (Garner et al. 1997, Dunn et al. 2001).

One recent example of interest is the San Miguel Sea Lion Virus 5, a virus that may be maintained by a combination of marine mam­mals and lungworm Parafilaroides decorus, as well as a liver fluke (Zalophatrema spp.) (Smith et al. 1978, 1980; Smith and Boyt 1990; Smith et al. 1998; Kennedy-Stoskopf 2001). However, there is a need for further clarification on the role of the helminth as part of the viral reservoir.

Other than for Neorickettsia spp., the over­all importance of helminths in the reservoirs of these bacteria and viruses has been unclear. While a number of viruses and bacteria may capitalize on helminths as one of several means for transmission, it is more likely that only a few bacteria and viruses require the helminth as an essential part of their reservoir. For many of the viruses, the helminth-vertebrate relationship may be only one part of a more complex reser­voir system that also involves latent infections in one or more vertebrate species. For example, waterfowl and shorebird carriers are an impor­tant source for many influenza viruses affect­ing other species (Stallknecht and Shane 1988, Webster et al. 1992, Campen and Early 2001). There also is evidence that the San Miguel sea lion virus may be a parasite of the opaleye perch (Girella nigricans), with the perch playing an important role in the ongoing occurrence of this virus among marine mammals (Smith and Boyt 1990, Kennedy-Stoskopf 2001).

Thus, this reservoir type currently involves few clearly established examples, and for most bacteria and viruses proposed for this reservoir type, the role of the helminth in the survival and success of these microparasites must be more clearly established. Interestingly, this reservoir type has been used successfully by eukaryotic as well as prokaryotic organisms of concern to wildlife. The flagellated protozoon Histomonas meleagridis is closely tied to the life cycle of the nematode Heterakis gallinae for its survival and success (Graybill and Smith 1920, Wehr 1971); this parasite was addressed in Chapter 6 (on Protista). However, with the apparent success of a helminth-vertebrate relationship among at least a few bacteria and viruses, it seems likely that, with searching, other examples will emerge.

For obligatory helminth-vertebrate relation­ships, control likely would be the same as that directed toward control of helminth infections; an attempt could be made to break the helminth life cycle. For relationships involving enhanced transmission, but non-obligatory relations between the microparasite and helminth, helminth control would have only limited success. In all cases, one could immunize or treat individual hosts if they were of particular importance to human or domestic animals health, or were members of listed species.

Soil and Water as Reservoirs

In this reservoir model, we include bacteria and viruses with a range of ecological capabilities. All established examples occur among bacteria. Such organisms share a capacity to survive for extended periods in soil and water, and can use this capacity as an important part of their long­term strategy for survival and success. A few bacteria in this reservoir live independently as true saprophytes in the environment, including Listeria monocytogenes and Nocardia spp. For these cases, infections in vertebrate hosts are an insignificant aspect of the bacterial reser­voir because infected animals are “dead-end” hosts; these bacteria rarely are transmitted directly from infected animals to other suscep­tible hosts. In addition, Clostridium botulinum, a bacterium causing an intoxication from a neurotoxin rather than a true bacterial infec­tion, is considered in this section because of its long survival in wetlands; it also is sapro­phytic, depending on decaying animal matter (Bell et al. 1955, Dodds 1992).

We also include in this reservoir bacteria and viruses that may depend upon another reservoir, but also have the ability to survive and endure in soil or water for such an extended period that the environment becomes an important part of their strategy for success and, for management purposes, it becomes sensible to consider soil or water as a significant part of their overall reservoir. These examples are virtually all bacteria. Some of these bacteria are linked to carrier animals and ultimately depend on them as a source of organisms to contami­nate the environment, but also have extended survival in the environment. In these cases, the infected animals and soil and water can serve as important complements in the reservoir. Examples include Bacillus anthracis (Logan and Turnbull 1999), Mycobacterium spp. (Metchock et al. 1999), Aeromonas hydrophila (Altwegg 1999), and Salmonella spp. (Winfield and Groisman 2003).

Further, we note the extended capacity of a few viruses to survive in the environment as an important element of their endurance between active infections and transmission, even though they are inert and lack any evidence for metabolism or replication outside of a living host cell. Examples include parvoviruses, avian influenza viruses, enteroviruses, and hepatitis A virus (Hurst et al. 1980, Yates et al. 1985, Gordon and Angrick 1986, Stallknecht et al. 1990, Gantzer et al. 1998, Brown et al. 2007).

Bacteria and viruses using soil or water as part of their reservoir typically are transmitted to susceptible hosts by ingestion of food or water contaminated from environmental sources. Occasionally these bacteria and viruses can be transmitted through wounds that came into contact with contaminated soil or water.

Diseases associated with soil and water reservoirs are classically density-independent diseases. Varying the density of the hosts has little or no impact on the risk of infection to an individual in a population.

The capacity for some bacteria not normally considered soil and water organisms to survive in the environment for extended periods can be influenced by their ability to successfully infect free-living amebae; after being ingested by the amebae, the bacteria grow, multiply, and even­tually lyse the amebae and are released back into the environment. In addition to occurring with the soil saprophyte Listeria monocytogenes (Ly and Muller 1990), this unique relation­ship has been linked with extended environ­mental survival for Francisella tularensis (Abd et al. 2003), Salmonella enterica (Tezcan-Merdol et al. 2004), Chlamydia pneumoniae (Essig et al. 1997), Pasteurella multocida (Hundt and Ruffolo 2005), and Mycobacterium avium (Cirillo et al. 1997, Steinert et al. 1998), among others. Thus, even where these bacteria are not true soil and water organisms, their extended capacity to survive in the environment by parasitizing protozoa complicates the development of strate­gies to control them.

Control strategies most commonly involve keeping susceptible hosts out of environ­mentally contaminated areas. In some cases, one can treat hosts contracting the illness. Both strategies have been used in the case of avian botulism.

As noted in the previous discussion, there is evidence that some pathogens regularly use more than one type of reservoir. As an example, Francisella tularensis may use recovered carrier animals such as voles (Microtus spp.) (Olsufev and Shlygina 1979, Shlygina and Olsuf'ev 1982), can be part of an arthropod-vertebrate reservoir (Jellison 1974), and can live in natural waters in the absence of known infections among animals (Parker et al. 1951, Ul'yanova et al. 1982, Morner and Addison 2001).

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