Implications of raccoon latrines in the epizootiology of baylisascariasis.

Raccoons (Procyon lotor) frequently establish defecation sites, termed latrines, on large logs, stumps, rocks, and other horizontally oriented structures/surfaces. These latrines are important foci of infective eggs of Baylisascaris procyonis, a nematode parasite of raccoons which is pathogenic to numerous species of mammals and birds. To examine the role of raccoon latrines in this animal-parasite interaction, we documented animal visitations to raccoon latrines in two large forested tracts and two woodlots in Indiana (USA) during 1994 and 1995. Species richness of vertebrate visitors did not differ between sites or years, but species composition differed by site and year. Fourteen mammal and 15 bird species were documented visiting raccoon latrines. Small granivorous mammals, including white-footed mice (Peromyscus leucopus), eastern chipmunks (Tamias striatus), and tree squirrels (Sciurus carolinensis, S. niger, Tamiasciurus hudsonicus) were the most common visitors to latrine sites. White-footed mice, chipmunks, white-breasted nuthatches (Sitta carolinensis), and opossums (Didelphis virginiana) were photographed foraging on undigested seeds in raccoon feces. Active foraging at latrines also was shown experimentally; seeds embedded in raccoon feces were removed at a greater rate at latrine sites than at nonlatrines. We conclude that raccoon latrines are visited routinely by a variety of vertebrates, especially small granivorous rodents and birds which forage for seeds in raccoon feces, and that raccoon latrines are probable sites of transmission of B. procyonis to susceptible mammals and birds.     

Land-use effects on prevalence of raccoon roundworm (Baylisascaris procyonis)

The raccoon (Procyon lotor) is the definitive host of Baylisascaris procyonis, a large intestinal roundworm that is zoonotic and can result in fatal or severe central nervous system disease in young children. Prevalence of infection among raccoon populations often is high, and in the midwestern United States, B. procyonis has been reported in 68-82% of raccoons. Raccoon populations have increased in response to changes in human land use, and often reach higher densities in urban and suburban landscapes than rural landscapes. However, shifts in foraging behavior among urban raccoons could impact the transmission of B. procyonis if small vertebrate intermediate hosts are not a significant part of the raccoon diet. The objective of this study was to compare prevalence of B. procyonis infection between urban and rural raccoon populations on a regional scale. Necropsy was done on 204 raccoons collected from September through February during 2000-2005 from seven states across the Midwest (regional sample). Baylisascaris procyonis was found in 54% of examined raccoons. Prevalence differed between land-use types (chi2=11.56, df=1, P=0.0007), and was higher among animals collected from rural locations (65%) than those collected in urban locations (41%). Intensity of infection also differed (F=5.52, df=1, P=0.02), with rural raccoons having greater worm burdens (x=29.63+/-36.42) than urban raccoons (x=13.85+/-18.47). Despite high densities of raccoons in urban landscapes, fewer urban raccoons were infected with B. procyonis, suggesting decreased dependence on intermediate hosts as a food source. This possible explanation was supported by a similar trend in prevalence among subsamples of raccoons collected from three Chicago-area populations (local samples) with differing levels of urbanization, population densities, and foraging behavior that had been intensively monitored during 1995-2002. Decreased transmission of B. procyonis in urban landscapes may be due to decreased predation of intermediate hosts, and contact of juvenile raccoons with B. procyonis eggs may be an important factor in maintaining infections within such populations.     

Survey of raccoons on Key Largo, Florida, USA, for Baylisascaris procyonis

Numbers of the endangered Key Largo woodrat (KLWR; Neotoma floridana smalli) have been declining for at least 25 yr. The raccoon (Procyon lotor) roundworm, Baylisascaris procyonis, has been found to have an adverse effect on the survival of Alleghany woodrats (N. magister). High densities of raccoons can exacerbate this problem by increasing the amount of feces containing viable eggs of B. procyonis available to woodrats. In 2002, 64 fecal samples were collected and examined for eggs of B. procyonis from >32 raccoons within the KLWR's known range on Key Largo, Florida, USA. All samples were negative for eggs of B. procyonis. Raccoon density in this area was approximately 0.62 raccoons/ha. Despite this high density of raccoons, B. procyonis does not appear to be a threat to the KLWR population.     

Detection of DNA from the zoonotic raccoon roundworm Baylisascaris procyonis in a French wolf

Baylisascaris procyonis is a zoonotic nematode whose main definitive host is the raccoon, an invasive carnivore in Europe introduced from the United States. B. procyonis causes larva migrans with poor prognosis in humans. This parasite was unexpectedly detected in France for the first time upon molecular screening of wolf faecal samples. Because no patent infection was found, the wolf cannot be considered as a definitive host. This discovery of B. procyonis in France nonetheless raises questions about the parasite status of the expanding raccoon populations in the country, which will be investigated in the future.     

Frequency of deposition and location of Baylisascaris procyonis eggs in raccoon feces

Baylisascaris procyonis is a large ascarid nematode found in the small intestine of raccoons (Procyon lotor). Infection with larvae of B. procyonis can produce visceral, ocular, and neural larval migrans in humans. Infected raccoons can shed millions of eggs a day in their feces. However, it is unknown whether eggs are consistently shed or whether eggs occur at irregular intervals by the population of female nematodes within a host. We trapped, infected, and collected daily fecal samples from 11 raccoons maintained in captivity. Eggs from B. procyonis were obtained from anterior, central, and posterior sections of raccoon feces, isolated by flotation, and quantified under 100× magnification. Naturally infected raccoons were collected and used as a comparison with the experimentally infected group. All raccoons in the experimental group (n=11) became infected with B. procyonis after consuming one infected mouse. Additionally, differential egg deposition rates were observed among individual raccoons from the experimental and naturally infected groups. Mean number of eggs per gram of feces (means±SE) was 16,563±4,321, which was less than previously reported for the species. However, no differences (F(2,30)=0.84, P=0.45) were noted in mean number of eggs per gram of feces among fecal sections. Wildlife biologists, veterinarians, health officials, and researchers of B. procyonis should collect daily fecal samples for a minimum of 3 days before identifying a raccoon as negative for B. procyonis infection. However, it does not matter where within the fecal matter the sample is obtained.     

Fear of feces? Tradeoffs between disease risk and foraging drive animal activity around raccoon latrines

Fear of predation alters prey behavior, which can indirectly alter entire landscapes. A parasite‐induced ecology of fear might also exist if animals avoid parasite‐contaminated resources when infection costs outweigh foraging benefits. To investigate whether animals avoid parasite contaminated sites, and if such avoidance balances disease costs and foraging gains, we monitored animal behavior at raccoon latrines – sites that concentrate both seeds and pathogenic parasite eggs. Using wildlife cameras, we documented over 40 potentially susceptible vertebrate species in latrines and adjacent habitat. Latrine contact rates reflected background activity, diet preferences and disease risk. Disease‐tolerant raccoons and rats displayed significant site attraction, while susceptible birds and small mammals avoided these high‐risk sites. This suggests that parasites, like predators, might create a landscape of fear for vulnerable hosts. Such non‐consumptive parasite effects could alter disease transmission, population dynamics, and even ecosystem structure.     

Baylisascaris procyonis (Nematoda: Ascarididae) larva migrans in free-ranging wildlife in Orange County,California

Baylisascaris procyonis is well recognized as a cause of visceral (VLM), ocular, and neural (NLM) larva migrans in birds and mammals, including man. A study of the prevalence of larva migrans in free-ranging wildlife associated with raccoon latrines as well as a retrospective study of wildlife mortalities with neurological disease was conducted in 2000 in Orange County, California. Eighty-seven birds of 18 species and 64 mammals of 8 species were found to have NLM or VLM or both. NLM clinical signs included convulsions, torticollis, opisthotonus, head-tilts, circling, ataxia, paralysis, and visual defects. NLM lesions were characterized by focally disseminated, frequently linear, "tracklike" areas of parenchymal degeneration with varying degrees of astrocytosis in the white matter of the cerebrum, cerebellum, brain stem, and spinal cord. Larvae were rarely found in these lesions but were rather isolated in the brain-spinal cord parenchyma. At least 1 larva was isolated by digestion from each case of NLM and identified as Baylisascaris sp., most likely B. procyonis. VLM lesions consisted of granulomatous reactions surrounding intact or degenerative larvae in the parenchyma of the liver, kidney, diaphragm, and, occasionally, the lymph nodes. This report broadens the range of species of wild birds and mammals that have been found to be susceptible to larva migrans caused by B. procyonis and reaffirms the importance of raccoon latrine sites as contaminative foci for wildlife.     

Gnathostoma procyonis from south Georgia and north Florida raccoons

From 2004 to 2006, 511 raccoons collected by the United States Department of Agriculture Wildlife Services as part of a study to evaluate the effects of mesomammalian predator removal on bobwhite-quail reproduction, were examined for the presence of Gnathostoma procyonis, a nematode that parasitizes the stomach of its definitive host, the raccoon. One hundred forty-one raccoons (27.6%) contained G. procyonis, with males being equally infected (27.5%) as females (27.8%). Mean intensity did not differ significantly between sexes (males-mean = 2.88, range 1-17; females-mean = 2.78, range 1-10) or between collection sites. A significant seasonal prevalence of G. procyonis was noted with a peak in March (43.3%, n = 120) and a minimum in September (5.4%, n = 37). Both collection sites exhibited significant seasonal decreases in G. procyonis, but were not significantly different from each other. There was no cumulative seasonal pattern in mean intensity of G. procyonis, and no seasonal pattern at either collection site. Host weight was not related to either G. procyonis prevalence or mean intensity. Host removal did not have an apparent effect on prevalence or mean intensity of G. procyonis.     

Diffuse retinochoroiditis due to Baylisascaris procyonis in Monglian gerbils

Baylisascaris procyonis, raccoon roundworm, causes a severe retinal lesion in humans. The lesion is termed as diffuse unilateral subacute neuroretinitis (DUSN). To understand the pathogenesis of B. procyonis in gerbils, we inoculated 17 embryonated eggs/g body weight of B. procyonis into 15 male Mongolian gerbils, Merionis ungiculatus, and monitored their fundi with an ophthalmoscope. Six of 15 gerbils (40%) showed severe retinitis with a sinuous track due to larval movement. The lesions extended across nearly half of the affected fundi. Histopathological examination revealed perivasculitis in the optic disk region, inflammatory proliferation of the pigment cells, and vitreitis in most cases. These findings were similar to those in human cases of DUSN, suggesting that gerbils might be a useful model for understanding the pathogenesis of B. procyonis infection in humans.     

Baylisascaris procyonis (Nematoda: Ascaridoidea) eggs in raccoon (Procyon lotol) latrine scats in Orange County,California

Baylisascaris procyonis is the common intestinal nematode of the raccoon and is well-recognized as a cause of visceral, ocular, and neural larva migrans in many species of wild and domestic birds and mammals, including humans. To develop data on the prevalence of B. procyonis in Orange County, California, 800 distinct raccoon latrine sites were sampled in 4 spatial zones from 15 January to 31 December 2000. Counts of fecal eggs per gram (EPG) were determined and evaluated with reference to spatial zone and season of collection. No significant differences in EPG were noted among the spatial zones. However, EPG exhibited a significant rise (37,730 +/- 1,865) in the fall and a significant decline (26,204 +/- 1,446) in the winter (ANOVA, P = 0.045). The overall egg prevalence was 100%, and the overall mean EPG was 30,265 +/- 867.     

Changes in transmission of Baylisascaris procyonis to intermediate hosts as a function of spatial scale

Physical changes in landscapes alter the abundance and distribution of species. Higher-order effects can occur when changes in ecological processes result in altered interspecific interactions and subsequent changes in a species' abundance or persistence. Baylisascaris procyonis , a roundworm parasite of raccoons ( Procyon lotor ), is pathogenic to numerous small vertebrates that serve as intermediate hosts, including white-footed mice ( Peromyscus leucopus ). Raccoons have responded positively to agriculturally induced changes in landscapes, with potential consequences for intermediate hosts of B . procyonis . We examined white-footed mice from a homogeneous, predominantly forested landscape in south-central Indiana and a heterogeneous, predominantly agricultural landscape in northwestern Indiana for presence of larval B . procyonis . We compared prevalence of infection, intensity of infection, and average number of larvae per mouse between the landscapes, and among forest patches within the highly fragmented agricultural landscape. Prevalence, intensity of infection, and average number of larvae were significantly higher in the highly fragmented landscape. Within the agricultural landscape, regression models predicted probability of infection, intensity of infection, and average number of larvae per mouse per patch as functions of forest patch area and isolation. We conclude that positive responses of raccoons to agriculturally induced fragmentation of forests have resulted in increased encounter rates between white-footed mice and infective stages of B . procyonis between and within landscapes, resulting in increased transmission of the parasite to intermediate hosts.     

Helminth parasites of an introduced invasive carnivore species, the raccoon ( Procyon lotor L.), from the Warta Mouth National Park (Poland)

We evaluated helminth parasites of the introduced North American raccoon ( Procyon lotor L.) in Poland. From June 2006 to May 2007, 91 raccoon fecal samples were collected in the Warta Mouth National Park situated in western Poland near the Polish-German border. Coprological analyses involved flotation and sedimentation. In total, 7 helminth taxa were identified in the feces: Ancylostoma spp., Baylisascaris procyonis, Capillariidae, Placoconus lotoris, Spirocerca lupi, Strongyloides procyonis, and Echinostoma sp. The parasite assemblage in the raccoon exhibited a low diversity. The results were compared with data from other European and North American studies and suggest a lower prevalence of parasites in newly invaded areas, compared with earlier invaded areas or the native range.     

Raccoon dog scent marking by scats and its significance in social behaviour

Utilization pattern of latrines by raccoon dogs,Nyctereutes procyonoides viverrinus, was studied on a small island in western Kyushu, Japan. Seventy-eight latrines were spread over the study areas, these were mainly formed on the flat surface in woody areas. Although the site and number of latrines were fairly stable throughout the year, distribution of the utilized latrines and number of scats per latrine were changed seasonally. Latrines were grouped into several clusters and communal utilization of latrines by several animals was observed within the cluster. Seasonal changes of utilization pattern observed in communal utilization rate and cluster formation was assumed to be caused by the changing of the social unit of raccoon dogs. Familiarization within the home range and information site to conspecifics may be concluded as the function of latrines.     

Epizootiology of an outbreak of cerebrospinal nematodiasis in cottontail rabbits and woodchucks

An epizootic of cerebrospinal nematodiasis in cottontail rabbits (Sylvilagus floridanus) and woodchucks (Marmota monax) caused by Baylisascaris procyonis larvae followed the establishment of an ascarid-infected raccoon (Procyon lotor) population in a woodlot. Five of seven raccoons examined from the woodlot harbored ascarids, with one heavily infected animal shedding approximately 27,500 eggs per gram of feces. A laboratory-reared cottontail rabbit developed neurologic disease due to larval migration 80 days after infection with B. procyonis eggs from the raccoons.     

Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors

Within any parasite species, variation among populations in standard infection parameters (prevalence, intensity and abundance) is an accepted fact. The proportion of hosts infected and the mean number of parasites per host are not fixed values across the entire geographic range of any parasite species. The question is whether this inter-population variation occurs within a narrow, species-specific range and is thus driven mainly by the biological features of the parasite, or whether it is substantial and unpredictable, leaving population parameters at the mercy of local conditions. Here, the repeatability of estimates of prevalence, intensity and abundance of infection was assessed across populations of the same parasite species, for 77 metazoan parasite species of Canadian freshwater fishes. Overall, parameter values from different populations of the same parasite species were more similar to each other and more different from those of other species, than expected by chance alone. Much of the variation in parameter values in the dataset was associated with differences between parasite species, rather than with differences among populations within species. This was particularly true for intensity and abundance of infection; in contrast, prevalence values, while somewhat repeatable among populations of the same species, still showed considerable variation. Among the higher taxa investigated (monogeneans, trematodes, cestodes, nematodes, acanthocephalans, copepods), there was no evidence that species of one taxon display intrinsically greater variation in population parameters than species of other taxa. Overall, the results suggest that intensity and abundance of infection are real species characters, though somewhat variable. This conclusion supports the view that the biological features of parasite species can potentially override local environmental conditions in driving parasite population dynamics.     

New information on the location of Capillaria procyonis (Nematoda: Trichuroidea) in the tongue of a raccoon (Procyon lotor)

Histologic examination of the tongue of one juvenile male raccoon demonstrated the presence of adults and unembryonated eggs of the nematode Capillaria procyonis within parasite-induced tunnels in the stratified squamous epithelium. There was no inflammatory infiltrate within the epithelium or the subjacent lamina propria. The shape of tunnels approximated that of the resident nematodes and were lined by flattened and attenuated epithelial cells. Therefore, the site of infection of C. procyonis in the raccoon includes the oral, lingual and pharyngeal epithelium in addition to the esophagus.     

Scaling up from epidemiology to biogeography: local infection patterns predict geographical distribution in fish parasites

Aim We investigated how the spatial distribution of parasites, measured as either their geographical range size or their frequency of occurrence among localities, relates to either their average local abundance or the variance in their abundance among localities where they occur. Location We used data on the abundance of 46 metazoan parasite species in 66 populations of threespine sticklebacks, Gasterosteus aculeatus, from Europe and North America. Methods For each parasite species, frequency of occurrence was calculated as the proportion of stickleback populations in which it occurred, and geographical range size as the area within the smallest possible polygon delimited using the coordinates of the localities where it occurred. Generalized linear models were used to assess how these two measures of spatial distribution were influenced by several predictor variables: geographical region (North America or Europe), life cycle (simple or complex), average local abundance, the coefficient of variation in abundance across localities, and median prevalence (proportion of infected hosts within a locality). Results Our analyses uncovered four patterns. First, parasites in North America tend to have higher frequencies of occurrence among surveyed localities, but not broader geographical ranges, than those in Europe. Second, parasite species with simple life cycles have wider geographical ranges than those with complex cycles. Third, there was a positive relationship between average abundance of the different parasite species and their frequency of occurrence, but not between average abundance and geographical range size. Fourth, the coefficient of variation in abundance covaried positively with both the frequency of occurrence and geographical range size across the different parasite species. Thus, all else being equal, parasites showing greater site‐to‐site variability in abundance occur in a greater proportion of localities and over a broader geographical area than those with a more stable abundance among sites. Main conclusions Local infection patterns are linked with large‐scale distributional patterns in fish parasites, independently of host effects, such that local commonness translates into regional commonness. The mechanisms linking parasite success at both scales remain unclear, but may include those that maintain the continuum between specialist and generalist parasites. Regardless, the observed patterns have implications for the predicted changes in the geographical distributions of many parasites in response to climate change.     

Trematodes in snails near raccoon latrines suggest a final host role for this mammal in California salt marshes

Of the 18 trematode species that use the horn snail, Cerithidea californica, as a first intermediate host, 6 have the potential to use raccoons as a final host. The presence of raccoon latrines in Carpinteria Salt Marsh, California, allowed us to investigate associations between raccoons and trematodes in snails. Two trematode species, Probolocoryphe uca and Stictodora hancocki, occurred at higher prevalences in snails near raccoon latrines than in snails away from latrines, suggesting that raccoons may serve as final hosts for these species. Fecal remains indicated that raccoons fed on shore crabs, the second intermediate host for P. uca, and fish, the second intermediate host for S. hancocki. The increase in raccoon populations in the suburban areas surrounding west coast salt marshes could increase their importance as final hosts for trematodes in this system.     

Pancreatic duct hyperplasia in a raccoon (Procyon lotor) caused by Atriotaenia procyonis

A raccoon (Procyon lotor) live-trapped in Philadelphia, Pennsylvania was heavily infected with the tapeworm Atriotaenia procyonis. Histopathologic examination of the duodenum revealed this tapeworm attached to the mucosa; the mucosa was mildly hyperplastic without a significant inflammatory infiltrate. This tapeworm was seen also within the proximal pancreatic duct and histopathologic lesions associated with its presence consisted of marked hyperplasia of mucosal cells, causing the formation of an extensive papillary projection into the duct lumen. Inflammatory cellular reaction was minimal, consisting primarily of lymphocytes, and was seen in the mucosa and submucosa of the duct. The presence of A. procyonis in the pancreas of this raccoon is considered to be an aberrant location for this parasite and has not been reported previously.     

Similar yet different: co-analysis of the genetic diversity and structure of an invasive nematode parasite and its invasive mammalian host

Animal parasitic nematodes can cause serious diseases and their emergence in new areas can be an issue of major concern for biodiversity conservation and human health. Their ability to adapt to new environments and hosts is likely to be affected by their degree of genetic diversity, with gene flow between distinct populations counteracting genetic drift and increasing effective population size. The raccoon roundworm (Baylisascaris procyonis), a gastrointestinal parasite of the raccoon (Procyon lotor), has increased its global geographic range after being translocated with its host. The raccoon has been introduced multiple times to Germany, but not all its populations are infected with the parasite. While fewer introduced individuals may have led to reduced diversity in the parasite, admixture between different founder populations may have counteracted genetic drift and bottlenecks. Here, we analyse the population genetic structure of the roundworm and its raccoon host at the intersection of distinct raccoon populations infected with B. procyonis. We found evidence for two parasite clusters resulting from independent introductions. Both clusters exhibited an extremely low genetic diversity, suggesting small founding populations subjected to inbreeding and genetic drift with no, or very limited, genetic influx from population admixture. Comparison of the population genetic structures of both host and parasite suggested that the parasite spread to an uninfected raccoon founder population. On the other hand, an almost perfect match between cluster boundaries also suggested that the population genetic structure of B. procyonis has remained stable since its introduction, mirroring that of its raccoon host.