INFECTIVE FUNGI

Many authors distinguish between superficial fungi, to which there is little cellular response from the host and which have only a general cosmetic impact, from cutaneous fungi (der­matophytes) found on the skin and appendages and which can invade keratinous tissues (skin, hair, nails, etc.) of living animals (Friend 1999b, Kane and Summerbell 1999).

Batrachochytrium dendrobatidis (bd)

CAUSATIVE AGENT (MORPHOLOGY AND classification) The genus Batrachochytrium is one of at least 100 genera in the Class Chy- tridiomycetes (chytrids). Most chytrid species are saprophytes, decomposing cellulose, chitin, keratin, other fungi, algae, and various types of plant material, although a few species are para­sitic upon selected invertebrates such as insects (Sparrow 1960, Powell 1993, Longcore et al. 1999). Batrachochytrium dendrobatidis is the only species in this genus (Carey et al. 2006).

HOST RANGE AND GEOGRAPHIC distribution Batrachochytrium dendrobatidis (Bd) infects at least 516 (42%) of 1,240 amphib­ian species among 35 of 40 families of Anura and six of eight families of Caudata (Olson et al.

After Africa, continents with infected amphibians first were observed in 1961 in Quebec, Canada (Ouellet et al. 2005), and shortly thereafter in Colorado (Ouellet et al. 2005), in 1978 in Europe (Garner et al. 2005) and Australia, in 1986 in Ecuador, in 1999 in New Zealand (Johnson and Speare 2003), in 2007 in Japan (http://www.promedmail.org/; http://www.asahi.com/english/Herald- asahi∕TKY200706120087.html), and in 2013 in Southeast Asia (Gilbert et al. 2013). Despite a broad distribution around the world, this parasite has little evidence for genetic diversity among isolates collected in various locations (Morehouse et al. 2003). There is consider­able variation of Bd prevalences and intensi­ties among families of amphibians (Olson et al. 2013).

life cycles and variations This aquatic organism has at least two distinct life stages. A sessile monocentric thallus develops into a reproductive, host-dependent zoosporangium; then motile, uniflagellate, water-borne zoo­spores are released from the zoosporangium and serve as the infective stage to vertebrates (Berger et al. 2005a). After a period of up to 24 hours of motility, zoospores encyst on a susceptible host, resorb their flagella, and form stages called germlings; in turn, these form rhizoids and subsequently develop thalli that again grow and form mature zoosporangia over a few days.

The development of Bd is affected by ambi­ent temperature and moisture. Under experi­mental conditions, optimal growth occurs between 17 and 25°C. Death of the patho­gen occurs above 29°C, below 0°C, or after prolonged desiccation (Piotrowski et al. 2004); Bd can survive in tap water for 3 weeks, in deionized water for 4 weeks, and in lake water for up to 7 weeks after inoculation (Johnson and Speare 2003). In field studies, prevalence varies by season, elevation, or region (Ron 2005); increased prevalence is associated with cooler temperatures and moister conditions (Woodhams et al. 2003; Retallick et al. 2004; Kriger and Hero 2006, 2007).

RESERVOIRS AND TRANSMISSION The fungi are transmitted through water (Kriger and Hero 2006). Among boreal toads (Bufo boreas), transmission can occur by contact with water containing zoospores; no physical con­tact with infected animals is required (Carey et al. 2006). Among yellow-legged frogs (Rana muscosa), tadpoles transmit the fungus among themselves and to postmetamorphic animals (Rachowicz and Vredenburg 2004). Trans­mission among yellow-legged frogs does not vary with degree of crowding or temperature (Rachowicz and Briggs 2007).

Batrachochytrium dendrobatidis survives up to 3 months in sterile, moist river sand and can attach and grow on sterile feathers; it is pro­posed that this fungus may be translocated by movement of moist river sand, and birds may carry it between amphibian habitats (Johnson and Speare 2005). Waterfowl such as geese (Branta canadensis, Anser anser domesticus) also are able to carry the chytrid on their toes and probably transmit the fungus between sites (Garmyn et al. 2012). The parasite also has been identified among crayfish (Procambarus spp.

Some amphibians such as bullfrogs (Rana catesbeiana) (Hanselmann et al. 2004) and tiger salamanders (Ambystoma tigrinum) (Davidson et al. 2003) can carry this fungus on their epidermis without developing lethal infections and may serve as reservoirs for the transmission of this parasite to susceptible spe­cies (Daszak et al. 2004). The bullfrog is the most commonly farmed amphibian and regu­larly escapes and establishes feral populations; it is speculated to be an important source for the spread and establishment of this fun­gus throughout the world (Garner et al. 2006). The Pacific chorus frog (Pseudacris regilla) also appears unaffected by Bd and survives at sites where other species have been extirpated (Reeder et al. 2012).

Batrachochytrium dendrobatidis also can persist in an endemic state among healthy frog populations once an epidemic wave has passed through those populations (Retallick et al. 2004, McDonald et al. 2005). At some sites where Bd has been endemic for at least 10 years, it occurred in two species of stream frogs in very low prevalences, but was not pres­ent in any environmental samples of these sites (Rowley et al. 2007). In Quebec, Canada, there was an overall 18% prevalence among amphib­ians in 1999 through 2001 among many appar­ently healthy populations, with no significant differences when compared to the prevalences of infection of 1960 through 1969 (Ouellet et al. 2005). This pathogen is widely distributed and apparently enzootic in seemingly healthy amphibians in parts of eastern North America (Ouellet et al. 2005).

Infected frogs are more frequently associ­ated with permanent than with temporary water bodies (Kriger and Hero 2007). Of these, stream breeders had a higher prevalence of infection than pond breeders; however, the intensity of frog infections does not differ sig­nificantly between these groups (Kriger and Hero 2007).

Based on ecological niche modeling for Bd, suitable habitats in the New World are exten­sive, including pine-oak forests, dry forests, moist forests, temperate forests, and tropi­cal rainforests throughout the United States, Central America, South America, and the Caribbean (Ron 2005).

CLINICAL EFFECTS AND IDENTIFICATION This fungus infects only keratinized tissues of amphibians (Daszak et al. 1999, Longcore et al. 1999, Pessier et al. 1999), and interferes with normal skin function of susceptible amphibian species, leading to disruption of osmoregula­tion, subsequent electrolyte imbalance, and eventual death (Berger et al. 1998, Voyles et al.

2009). The disease, chytridiomycosis, often involves sloughing of dermatitis (Longcore et al. 1999, Pessier et al. 1999). Although amphib­ian larvae lack keratin in their epidermis, the fungus occurs in the keratinized mouthparts of tadpoles and toes of premetamorphic tadpoles in some species (Berger et al. 1998, Fellers et al. 2001, Marantelli et al. 2004, Rachowicz and Vredenburg 2004). There is considerable inter­specific variation in susceptibility to this parasite among frog tadpoles (Blaustein et al. 2005).

Unique Bd-specific genes containing patho­genic factors have been identified (Joneson et al. 2011). Despite low genetic diversity (Morehouse et al. 2003), there are some strain differences among Bd regarding impacts on amphibians (Retallick and Miera 2007). Among postmeta- morphic boreal toads (Bufo boreas), the time between exposure and death is influenced by the dose of infectious zoospores, duration of exposure, and body size of the toad (Carey et al. 2006); about 10⁷ to 10⁸ sporangia appears to be a minimum threshold needed to cause death in boreal toads. Once infected, variation in air temperature between 12 and 23°C had no significant effect on survival time among infected animals (Carey et al. 2006).

Among adult Australian green tree frogs (Litoria caerulea), large numbers of sporangia occurred in all areas of ventral skin and toes; few or no sporangia occurred on dorsal skin. This difference may be due to the dryness of the dorsal skin or the greater numbers of serous glands there, which produce antifungal peptides (Berger et al.

There are several studies on methods to identify Bd in amphibians (Brem et al. 2007, Hyatt et al. 2007). Polymerase chain-reaction (PCR)-based assays are used to detect both zoo­spores and infections in skin samples (Annis et al. 2004, Boyle et al. 2004). Although less sensitive than some other methods, a PCR test also can be used for non-lethal detection of Bd from swabbed tadpole mouth parts (Retallick et al. 2006).

Congo red is effective for finding zoospo­rangia, zoospores, and germling stages of Bd in epidermal skin swabs of frogs (Briggs and Burgin 2004). Using an indirect immunoper­oxidase test, polyclonal antibodies can be used for diagnosing Bd in amphibians by stain­ing walls, cytoplasm, rhizoids, and zoospores (Berger et al. 2002). This method has been combined with Hollande’s Trichrome keratin stain to simultaneously detect Bd and keratin (Olsen et al. 2004).

population effects Batrachochytrium dendrobatidis has been associated with extir­pations and worldwide population declines in many wild amphibian populations (Daszak et al. 2003, Stuart et al. 2004, Johnson 2006). In several studies, healthy amphibian populations occurred at sites in the absence ofBd, while acute mortalities and population declines occurred immediately after detection of the pathogen (Rachowicz et al. 2005, Lips et al. 2006). Thus the impacts are caused by long-lived or sapro­phytic free-living stages of this pathogen, and there is evidence that Bd has caused direct extinctions of many amphibians (Schloegel et al. 2006, Mitchell et al. 2008). Epizootics in Central and South America are explained by multiple introductions of Bd because the epi­zootics move across the affected regions in the wave-like pattern characteristic of many dis­ease systems (Lips et al. 2008). However, not all are convinced that Bd is the primary cause of mortality, even in regions where it is com­monly reported (Burgin et al. 2005).

The role of weather also has been assessed. Weather-driven simulations of pathogen growth potential with Pearson’s green tree frog (Litoria pearsoniana) were positively related to both prevalence and intensity of Bd infections (Murray et al. 2013). Also, high rainfall, num­bers of rain days, and temperatures between 3 and 30°C were positively correlated with infection levels of the quacking frog (Crinia georgiana) in Australia (Riley et al. 2013). More generally, global warming and contaminants also may exacerbate chytrid outbreaks (Pounds et al. 2006).

special problems Batrachochytrium den­drobatidis is likely a significant contributor to the amphibian declines in many parts of the world, including North America (Bradley et al. 2002, Green et al. 2002), Europe (Bosch et al. 2001), South America (Ron and Merino 2000, Ron et al. 2003, Lampo et al. 2007), Central America (Berger et al. 1998, Lips et al. 2006), the Caribbean (Lips et al. 2003, Alemu et al. 2008), Australia (Berger et al. 1998), and New Zealand (Bishop 2000). This is fur­ther addressed in Case Study on Amphibian Declines, Chapter ιι.

The parasite appears to follow a density­independent pattern of spread, which increases extinction risk in affected populations (Collins

2010), especially among critically endangered species such as the harlequin frog (Atelopus mucubajiensis) (Lampo et al. 2007), Bloody Bay frog (Mannophryne olmonae) (Alemu et al.

2008), and the Sardinian newt (Euproctus platy- cephalus, Order Urodela) (Bovero et al. 2008).

Interestingly, this fungus has been consid­ered as a means of controlling an invasive frog (Eleutherodactylus coqui) on Hawaii. Such an introduction may be of less risk to other native fauna because there are no native amphibians on Hawaii (Beard and O'Neill 2005).

control Amphibians have a variety of anti­microbial defenses including skin peptides that inhibit the growth of mature B. dendrobatidis cells (Woodhams et al. 2007). While antimicro­bial peptides often are effective at both 10°C and 22°C, many are more effective at 10°C (Rollins- Smith et al. 2002). Some infected frogs can clear their own B. dendrobatidis infections entirely (Kriger and Hero 2006). Salamanders also have antimicrobial peptides that inhibit B. den- drobatidis and other microorganisms (Sheafor et al. 2008).

At least eight genera of cutaneous bacte­ria found on amphibians inhibit the growth of B. dendrobatidis (Harris et al. 2006). For example, Pedobacter cryoconitis, a bacterium found on the skin of red-backed salamanders (Plethodon spp.), lessens the effects of Bd when transferred to the skin of yellow-legged frogs, (Lam et al. 2008).

Bioaugmentation of individual amphib­ians and of amphibian habitats with care­fully selected, locally occurring, anti-chytrid microbes may be of potential value in areas under threat from Bd. Several sampling strate­gies and filtering protocols to identify promising probiotics have been proposed (Bletz et al. 2013).

Manipulating environmental conditions can influence success of this fungus. Low tem­peratures, toxic chemicals, and stress inhibit the immune system and may impair natural defenses against B. dendrobatidis (Rollins- Smith et al. 2011). Infected red-eyed tree frogs (Litoria chloris) artificially held at 37°C can be cleared of B. dendrobatidis in less than 16 hours; thus elevated body temperatures to clear frogs of chytrid infection might be used to eliminate the fungal pathogen from captive populations and reduce the likelihood of accidental spread when animals are translocated or released from captivity (Woodhams et al. 2003). In another study where frogs were cleared of infection by the use of heat, mortality ceased and the frogs gained weight; in contrast, frogs in which infection was not cleared gained less weight or continued to die (Retallick and Miera 2007). Among laboratory-infected yellow-legged frogs, fewer frogs died when housed at 22°C than at 17°C; since both temperatures were within the optimal range for growth of B. dendrobatidis, the authors proposed that the difference was from the effect of temperature on the host's resistance to chytridiomycosis rather than any effect on the fungus alone (Andre et al. 2008).

In the laboratory, a number of chemicals, including Path-X^TM, the quaternary ammo­nium compound 128, and itraconazole (Jones et al. 2012), are effective to disinfect in vitro cultures of Bd. In contrast, UV light was inef­fective at the wavelengths tested. Under experi­mental conditions, cultures were sensitive to heating for 4 hours at 37°C, 30 min at 47°C, and 5 min at 60°C (Johnson et al. 2003). Such treatments are applicable to prevent spread by cleaning items contacting amphibians or water (e.g., nets, boots), in captive husbandry, and in the laboratory.

More broadly, the worldwide emergence of this fungal disease has been linked to the spread of infected animals, introducing non­native infected animals into naive populations, and amplifying infections of amphibians by co-housing of mixed populations, as well as discharge of wastewater containing untreated discharge of infectious zoospores into natural water supplies.

In general, the trade in amphibians probably has been an important contributor to the wide dis­tribution of this parasite, and special effort must be made to prevent introduction of this pathogen into remaining uninfected areas (Fisher and Garner 2007). Effective management of chytrid- iomycosis will depend on different countries and regions recognizing the disease as a “threaten­ing process”, defined as a disease that threatens, or may threaten the survival, abundance, or evolutionary development of a native species or ecological community, and that requires strate­gies being implemented for its control (Hyatt et al. 2007). Managerial strategies ultimately will involve detection of infected populations of both laboratory-housed and free-ranging animals, identification of infected geographical areas, and control of human-mediated movement of animals from one location to another (Hyatt et al. 2007). Needed steps include identification of the parasite in adults and tadpoles from cap­tive and free-ranging animals, estimation of prevalence of infection of these populations, identifying specific infected animals or groups for the purposes of control, identifying disease- free zones, and demonstrating the eradication of infections from individuals undergoing treat­ment (Hyatt et al. 2007).

Raising and maintaining chytrid-free labo­ratory populations of vulnerable species until there are mechanisms for safely introducing them back into natural habitats also is being attempted (Stone 2013). Hundreds of frogs were collected from El Valle, an inactive volcano in Panama (Goodman 2006). The Houston Zoo, with the assistance of other zoological groups, is constructing an ex situ facility in Panama's El Valle de Anton region to house Atelopus zeteki and several other native species, serving as a repository and conservation breeding center, a treatment facility, and a nature education center for Panamanians and foreign tourists (www.houstonzoo.org/Golden_Frogs.aqf).

Pseudocymnoascus (ceomyces) destructans [white-nose syndrome (geomycosis)]

causative agent Pseudogymnoascus (Geomyces) destructans (Order Onygenales, Fam­ily Onygenaceae) is a recently described psychro- philic (cold-loving) ascomycete (App. 1: Table 6) (Blehert et al. 2009). It causes, white-nose syn­drome (WNS), a fatal disease in many hibernat­ing bats (Order Chiroptera) (Gargas 2009, Lorch et al. 2011).

host range and geographic distribution In North America, the fungus has been identified in at least 19 states through­out the northeastern and mid-Atlantic regions of the United States as well as the provinces of Ontario and Quebec in Canada (Frick et al. 2010, Cryan 2011). At least six bat spe­cies of North America currently are known to be adversely affected by WNS, including four species of Myotis (M. leibii, M. Iucifugus, M. septentrionalis, and M. sodalis), Perimyotis subfalvus, and Eptesicusfuscus (Cryan 2011). It is possible that many of the 25 species of hibernat­ing bats in North America could be vulnerable to P. destructans (Cryan 2011, Foley et al. 2011).

The fungus is also widespread in Europe and has been observed in at least six species of Myotis in eight countries (Martfnkova et al. 2010, Puechmaille et al. 2010, Wibbelt et al. 2010a, Simonovicov et al. 2011). However, despite extensive monitoring, no major mor­tality events have been documented among European bats (Puechmaille et al. 2011). This intercontinental difference is associated with differences in susceptibility of resident bats in these regions rather than differences in the pathogen (Cryan et al. 2013).

RESERVOIRS AND TRANSMISSION As of 2011, only bats were reported as hosts for P. destructans. There is evidence that the para­site in North America originated in Europe and was transported by human trade or travel (Warnecke et al. 2012). Transmission occurs through direct bat-to-bat contact (Lorch et al.

2011) but also may occur by point source infec­tions from exposure to soil in which fungi are present (Lindner et al. 2010). The fungus has been called a host-generalist pathogen with an abiotic reservoir in caves (Eskew and Todd 2013). Spread of the fungus to new geographic regions and to other vulnerable bat species may result from social and spatial mixing of bats during migration or by social contact, includ­ing mixed groups, during hibernation or some more long-distance movements (Frick et al. 2010, Lorch et al. 2011).

The role of soil as a reservoir for P. destruc­tans is not clear. The fungus has been isolated from soil of hibernacula in areas where white­nose syndrome occurs; there is a very abun­dant and diverse group of the closely related Geomyces spp. cultured among soil organisms sampled in bat hibernacula, many of which are undescribed taxa (Lorch et al. 2013).

CLINICAL EFFECTS AND IDENTIFICATION While some species of Geomyces can colonize skin (Gianni et al. 2003, Foley et al. 2011), P. destructans can invade, digest, and erode the skin of hibernating bats (Meteyer et al. 2009). Known characteristics of WNS include a white filamentous or powdery growth on the nose, ears, and wing membranes, and emaciation, (Blehert et al. 2009); early emergence from hibernacula in mid-winter (Wibbelt et al. 2010b); and ulcerated, necrotic, and scarred wing membranes among bats recently emerged from hibernation (Reichard and Kunz 2009). The disease also may be associated with ele­vated metabolism of bats, reduced flora in the their digestive tracts, and some disruptions in their immune systems (Turner and Reeder

2009). Mortality is linked to rapid depletion of fat reserves during hibernation (Boyles and Willis 2009), disruption of wing-dependent physiological functions after infections (Cryan et al. 2010), and by evaporative water loss (Willis et al. 2011).

Mortality from WNS does not become evident until about 120 days after bats enter hibernation and assume a cold physiological state conducive to proliferation of P. destruc- tans; mortality peaks about 180 days after bats first enter hibernacula (about March) (Lorch et al. 2011). But with supportive laboratory care, infected bats can recover from infection (Meteyer et al. 2011).

Many hibernating animals have a cycle of suppression of cellular immune response dur­ing hibernation and reactivation of the immune response after hibernation (Bouma et al. 2010). The lack of a visible cellular immune response to P. destructans during hibernation, with sub­sequent neutrophil recruitment and seques­tration of P. destructans in homeothermic bats, suggests that bats also have this type of immune regulation (Meteyer et al. 2011). Such a model makes them vulnerable to infections at low temperatures and, while their immune response is enhanced on becoming homeother- mic, it calls upon considerable expenditure of fat reserves to establish the body temperatures needed for effective response. Some mortality is associated with an immune reconstitution inflammatory syndrome, in which immune suppression during hibernation is followed by an intense neutrophil inflammatory response to the P. destructans, resulting in severe pathology and mortality (Meteyer et al. 2012).

Diagnosis of the disease is based on histo­pathology (Meteyer et al. 2009), polymerase chain reaction tests, and laboratory culture (Lorch et al. 2010, Chaturvedi et al. 2011, Foley et al. 2011).

population effects First observed in North America near Albany, New York, in February 2006 (Blehert et al. 2009), this explosive disease has caused unprecedented reductions in the abundance of hibernating bat species in the eastern United States, with up to 95% mortality in some hibernacula and an esti­mated mortality of 6 million or more bats dying from WNS (Froschauer and Coleman 2012). Bat population declines in the northeastern United States since the emergence of WNS may exceed 80 percent (Turner et al. 2011). Some winter colonies that were stable or increasing in numbers for decades have virtually disap­peared (Reichard and Kunz 2009); the little brown bat (Myotis Iucifugus) has been particu­larly severely affected (Frick et al. 2010). Popu­lation decreases at infected hibernacula range from 30 to 99% annually, with a regional mean of 73%, and all surveyed sites have become infected within 2 years of the disease arriving in their region (Frick et al. 2010).

Since its original identification as a disease, WNS has expanded at least 2,000 km westward in North America (Cryan 2011). Because most affected bat species are long-lived and have only one offspring per year, bat populations affected by WNS are not expected to recover quickly (Cryan 2011).

About 25 of the 45 insectivorous bat species in the United States and Canada rely on hiber­nation as a primary strategy to over-winter, including four species and subspecies listed as endangered and an additional 13 listed as federal species of concern (Cryan 2011). The increasing impact of this pathogenic fungus in hibernating bats potentially could undermine the basic survival strategy of over half of the bat species in the United States and 18 of the 22 bat species living above 40°N in North America (Cryan 2011).

special problems The natural cycle of bat hibernation, with reduced metabolism and immune function, has allowed P. destructans to become very successful in bats (Cryan et al.

2010). Pseudogymnoascus (Geomyces) destructans thrives in darkness, low temperatures (5-10°C), and high humidity (>90%), and it cannot grow above 20°C (Cryan 2011); thus it appears to be well suited to persist in the hibernacula of bat caves and mines. It establishes itself in the bats and invades wing membranes and other skin tis­sue when the bat body temperatures are lowered to 2-10°C during hibernation (Cryan 2011). Fun­gal infiltration of the wing membranes of bats may be problematic because the wing surfaces cover about 85% of the bat's total surface area, and healthy wing membranes are vital to regula­tion of body temperature, blood pressure, water balance, and gas exchange (Cryan 2011).

Behavioral strategies of bats also may con­tribute to their vulnerability to infections. For example, selection of humid areas of hibernac­ula or dense clustering to conserve energy and decrease moisture loss could further enhance fungal colonization, growth, and conidial amplification by elevating humidity, as well as by increasing infection prevalence and dispersal of P. destructans through increased contact with infected individuals (Cryan et al. 2010). Finally, the natural reduction of immune function in hibernating species may allow the fungus to invade body tissues without facing a significant immune response (Bouma et al. 2010).

Bats play a very important role in North American ecosystems through predation of noc­turnal insects, including many crop and forest pests. Economic impacts on agriculture from loss of bats is estimated at about $22.9 billion per year, with a range of extremes $3.7 to $53 billion per year (Boyles et al. 2011). These estimates incorporate the reduced costs of pesticide applica­tions not needed to suppress insects consumed by bats (Cleveland et al. 2006). However, such estimates do not include suppression of forest insects, which also is believed to be considerable (Kalka et al. 2008).

control There are no known strategies to reduce the spread or to control WNS in bats. There is evidence that bat hibernacula closer to the site of fungal origin, as well as those of larger size, tend to have higher risk for infec­tion (Wilder et al. 2011). One proposal for reducing WNS impacts includes culling of bats (Szymanski et al. 2009); however, disease models do not support this approach (Hallam and McCracken 2011). Other suggestions for control include providing artificial localized warm areas inside cold caves (Boyles and Willis 2009), treatment of individual bats, enhancing resistance of key populations through vaccines or immunomodulators, nutritional support to reduce starvation or dehydration from the effects of the disease, modifying hibernacula environments to reduce P. destructans, and informing the public to reduce anthropogenic spread (Foley et al. 2011). Most efforts have focused on implementing universal precau­tions, including restricting access of humans to sensitive bat hibernation sites and decontami­nating equipment and clothing when sites are accessed for disease surveillance, research, or recreational purposes (Blehert 2012).

miscellaneous dermatophytes Three other genera of dermatophytes generally are recognized: Trichophyton, Microsporum, and Epidermophyton; all are ascomycetes in the Family Arthodermataceae, Order Onygenales (App. 1: Table 6) (Kane and Summerbell 1999). Some species in each genus infect humans (anthropophilic), with little or no transmission to other species; some species of Trichophyton and Microsporum are pathogens primarily of nonhuman mammals or birds (zoophilic), whereas other species of these two genera are primarily soil-associated organisms (geophilic) that only occasionally infect animal hosts (Kane and Summerbell 1999).

Trichophyton gallinae is the cause of ring­worm; it also is called fowl flavus in wild birds and poultry (Friend 1999b). Trichophyton men- tagrophytes, another ringworm fungus, has been reported among wild foxes (Vulpes vulpes) (Knudtson et al. 1980), opossums (Didelphis marsupialis) (Menges and Georg 1955, McKeever et al. 1958), and as a serious problem among young muskrats (Erethizon zibethicus) (Errington 1963). Among muskrats, there was an 8-12% prevalence among the litters stud­ied, and mortality of about 50-60% among infected young; infected muskrats usually had hairless patches and a dandruff-like scurf (Errington 1963). Although infected muskrats were observed only in Iowa and Maryland, this fungus was assumed to be widespread over North America (Errington 1963). There also are both zoophilic and anthropophilic strains of this species (Knudtson et al. 1980). Infec­tions among red foxes (Vulpes vulpes) were suc­cessfully treated with griseofulvin in the feed (Knudtson et al. 1980).

Transmission of infectious dermatophytes generally occurs by direct contact with carrier animals or contaminated fomites (Kane and Summerbell 1999, Burek 2001). In addition, chewing and sucking lice can be mechanical vectors in some cases (Durden and Musser 1994). Animal host infections typically require some slight trauma or continued moisture or maceration of the skin for the parasites to become established (Burek 2001).

Skin lesions typically begin as focal, round areas of hair or feather loss and may progress to redness, skin depigmentation, and excess keratin production (Burek 2001). Diagnosis often is based on clinical lesions and find­ing arthroconidia or hyphae in skin scrapings digested in 10% potassium hydroxide (Kane and Summerbell 1999). For captive wildlife, systemic therapies include griseofulvin and other drugs (Knudtson et al. 1980, Burek 2001). Most infections are self-limiting, with lesions requir­ing a few weeks to several months to regress, depending on the species of fungus and host, and individual host responses (Burek 2001).