Larval Hannemania sp. infestations of Spea spp. in the Southern High Plains, Texas, USA

We describe a case history of larval Hannemania sp. (Acari: Trombiculidae) infestations in two spadefoot toads (Spea spp. Anura: Pelobatidae) captured from playa wetlands in the Southern High Plains, Texas. Hannemania sp. larvae were superficially attached to the skin, not encysted, and dermal changes were not observed. Gross field examinations revealed a presumed occurrence of Hannemania sp. in Spea spp. at four of 24 wetlands in 2003 and 2004. Although other species of amphibians were present (Ambystoma tigrinum mavortium, Bufo cognatus, Bufo debilis insidior, Pseudacris clarkii, Gastrophryne olivacea, Rana blairi, Scaphiopus couchii), investigators did not observe infestations in these species. Future research should focus on identifying this Hannemania to species level and determining if it influences Spea spp. survival.     

Helminth community structure of sympatric eastern American toad, Bufo americanus americanus, northern leopard frog, Rana pipiens, and blue-spotted salamander, Ambystoma laterale, from southeastern Wisconsin

One-hundred twelve amphibians, including 51 blue-spotted salamanders, Ambystoma laterale, 30 eastern American toads, Bufo americanus americanus, and 31 northern leopard frogs, Rana pipiens, were collected during April-October 1996 from Waukesha County, Wisconsin and examined for helminth parasites. The helminth compound community of this amphibian assemblage consisted of at least 10 species: 9 in American toads, 8 in leopard frogs, and 3 in blue-spotted salamanders. American toads shared 7 species with leopard frogs, and 2 species occurred in all 3 host species. Although there was a high degree of helminth species overlap among these sympatric amphibians, statistically significant differences were found among host species and percent of indirect or direct-life cycle parasites of amphibian species individual component communities (chi2 = 1,015, P < 0.001). American toads had a higher relative abundance of nematodes, 59%, than larval cestodes, 31%, and larval and adult trematodes, 10%, whereas leopard frogs had a higher relative abundance of larval cestodes, 71.3%, and larval and adult trematodes, 25.3%, than nematodes 3.4%. This is related to ecological differences in habitat and dietary preferences between these 2 anuran species. Helminth communities of blue-spotted salamanders were depauperate and were dominated by larval trematodes, 94%, and few nematodes, 6%. Low helminth species richness in this host species is related to this salamander's relatively small host body size, smaller gape size, lower vagility, and more fossorial habitat preference than the other 2 anuran species. Adult leopard frogs and toads had significantly higher mean helminth species richness than metamorphs, but there was no significant difference in mean helminth species richness among adult and metamorph blue-spotted salamanders. Considering adult helminths, the low species richness and low vagility of caudatans as compared with anurans suggest that local factors may be more important in structuring caudatan helminth communities of salamanders than of anuran hosts. Helminth species infecting salamanders may be more clumped in their geographic distribution as compared with anurans, and the role of other hosts and their parasites at the compound community level may be important in structuring helminth communities of salamanders.     

Diversity and disease: community structure drives parasite transmission and host fitness

Changes in host diversity and community structure have been linked to disease, but the mechanisms underlying such relationships and their applicability to non-vector-borne disease systems remain conjectural. Here we experimentally investigated how changes in host community structure affected the transmission and pathology of the multi-host parasite Ribeiroia ondatrae, which is a widespread cause of amphibian limb deformities. We exposed larval amphibians to parasites in monospecific or heterospecific communities, and varied host number to differentiate between density- and diversity-mediated effects on transmission. In monospecific communities, exposure to Ribeiroia significantly increased mortality (15%), malformations (40%) and time-to-metamorphosis in toads. However, the presence of tree frogs significantly reduced infection in toads, leading to fewer malformations and higher survival than observed in monospecific communities, providing evidence of parasite-mediated facilitation. Our results suggest that interspecific variation in parasite resistance can inhibit parasite transmission in multi-species communities, reducing infection and pathology in sensitive hosts.     

Biases in Trapping Larval Amphibians in Playa Wetlands

Abstract: Standardized, effective sampling methods are required to monitor amphibian population trends and community composition. Funnel traps have been used to ostensibly estimate species richness and relative abundance of larval amphibians. We tested whether funnel traps can be used to provide unbiased estimates of amphibian community composition in playa wetlands by comparing seining—dip netting and passive funnel-trapping results. Plains spadefoots (Spea bombifrons) were more prone to be captured in funnel traps whereas New Mexico spadefoots (S. multiplicata) were less likely captured by funnel traps than by seines and dip nets. In playas funnel traps should be used only for collecting specimens and not for estimating amphibian community composition.     

Ectoparasitism by Eutrombicula alfreddugesi larvae (Acari: Trombiculidae) on Liolaemus tenuis lizard in a Chilean fragmented temperate forest

We compared parasite load (prevalence and mean intensity) of Eutrombicula alfreddugesi larvae on the lizard Liolaemus tenuis sampled during January 2006 and 2007 from the interior and edges of large forest tracts in the coastal Maulino Forest (35 degrees 59'S, 72 degrees 41'W) and from nearby forest fragments (1.5-20 ha). All lizards were parasitized by chiggers regardless of location (prevalence, 100%); however, mean intensity of infestation was significantly lower at forest fragment edges compared with either large forest interiors or forest edges. We attribute differences in mean intensity to differences in microclimate among localities; maximum air temperature was significantly higher and relative humidity significantly lower in fragment edges compared with either large forest tract interior or edges.     

Patterns of infestation by the trombiculid mite Eutrombicula alfreddugesi in four sympatric lizard species (genus Tropidurus) in northeastern Brazil

We studied the parasitism by the chigger mite Eutrombicula alfreddugesi on four sympatric lizard species of the genus Tropidurus in Morro do Chapéu, Bahia state, Brazil: T. hispidus, T. cocorobensis, T. semitaeniatus and T. erythrocephalus. For each species, we investigated the patterns of infestation and analyzed to which extent they varied among the hosts. We calculated the spatial niche breadth of the chigger mite on the body of each host species and the distribution of mites along the hosts' bodies for each Tropidurus species. All four species of Tropidurus at Morro do Chapéu were parasited by the chigger mite, with high (97-100%) prevalences. Host body size significantly explained the intensity of mite infestation for all species, except T. erythrocephalus. The body regions with highest intensity of infestation in the four lizard species were the mite pockets. The spacial niche width of the chigger varied consistently among the four lizards species studied being highest for T. erytrocephalus and lowest for T. cocorobensis. We conclude that the distribution and intensity with which lizards of the genus Tropidurus are infested by Eutrombicula alfreddugesi larvae results from the interaction between aspects of host morphology (such as body size and the occurrence and distribution of mite pockets) and ecology (especially microhabitat use).     

Metacercariae of Clinostomum attenuatum in Ambystoma tigrinum mavortium, Bufo cognatus and Spea multiplicata from west Texas

Tissues from barred tiger salamanders (Ambystoma tigrinum mavortium), Great Plains toads (Bufo cognatus) and New Mexico spadefoots (Spea multiplicata) collected from 16 playa wetlands in Texas during 1999 and 2000 were examined by light microscopy. Digenean cysts were primarily distributed subcutaneously throughout the specimens and occasionally coelomic invasion was noted. The parasites within the cysts were 1.5-2 mm in diameter, with a thin (c. 10 microm wide) eosinophilic-staining tegument, two suckers (oral and ventral), posteriorly located primordial genitalia and paired digestive caeca. These digeneans were identified as the metacercariae of Clinostomum attenuatum. This is the first record of Clinostomum attenuatum in these amphibian species.     

A review of the role of parasites in the ecology of reptiles and amphibians

A great diversity of parasites, from viruses and bacteria to a range of remarkable eukaryotic organisms, exploit reptile and amphibian hosts. Recent increases in the emergence of infectious disease have revealed the importance of understanding the effects of interactions between hosts and their parasites. Here we review the effects of parasite infection on a range of demographic, behavioural, genomic and physiological factors in reptile and amphibian species. Reviewing these parasite roles collectively, and prioritising areas for research, advances our ecological understanding and guides direction for conservation in a time of rapid species decline. Poorly resolved systems include Gymnophionan amphibians and Crocodilian hosts, in addition to viral and bacterial parasites. Future research should seek to understand processes enabling population recovery and examining synergistic interactions of parasites with fragmentation, climate change and other processes that threaten species persistence.     

Ecology of helminth communities in tropical Australian amphibians.

Less than 50% of Australian amphibians have been recorded as hosts for helminth parasites. Despite developments in parasite community ecology in amphibians elsewhere, Australia lags behind with only two publications on this subject. Reasons advanced for this are that much of the collecting and taxonomic studies were conducted earlier this century before more recent discoveries of host genera and species as well as species complexes in the amphibian fauna. Consequently, there is a need for re-collection of hosts and parasites, and taxonomic revision of the parasites. In addition, as shown in this study, the parasite fauna in Australian amphibians is depauperate. Composition of the parasite fauna was largely dependent on the ecological associations of the host animal species. Frogs were infected with few helminth species and these occurred at low intensity, indicating, as in Europe and North America, that a depauperate fauna is also characteristic of amphibians in tropical regions.     

Density dependence in the terrestrial life history stage of two anurans

Populations of species with complex life cycles have the potential to be regulated at multiple life history stages. However, research tends to focus on single stage density-dependence, which can lead to inaccurate conclusions about population regulation and subsequently hinder conservation efforts. In amphibians, many studies have demonstrated strong effects of larval density and have often assumed that populations are regulated at this life history stage. However, studies examining density regulation in the terrestrial stages are rare, and the functional relationships between terrestrial density and vital rates in amphibians are unknown. We determined the effects of population density on survival, growth and reproductive development in the terrestrial stage of two amphibians by raising juvenile wood frogs (Rana sylvatica) and American toads (Bufo americanus) at six densities in terrestrial enclosures. Density had strong negative effects on survival, growth and reproductive development in both species. We fitted a priori recruitment functions to describe the relationship between initial density and the density of survivors after one year, and determined the functional relationship between initial density and mass after one year. Animals raised at the lowest densities experienced growth and survival rates that were over twice as great as those raised at the highest density. All female wood frogs in the lowest density treatment showed signs of reproductive development, compared to only 6% in the highest density treatment. Female American toads reached minimum reproductive size only at low densities, and male wood frogs and American toads reached maturity only in the three lowest density treatments. Our results demonstrate that in the complex life cycle of amphibians, density in the terrestrial stage can reduce growth, survival and reproductive development and may play an important role in amphibian population regulation. We discuss the implications of these results for population regulation in complex life cycles and for amphibian conservation.     

Parasites lost? An overlooked hypothesis for the evolution of alternative reproductive strategies in amphibians

Amphibians exhibit the greatest diversity of reproductive strategies of all tetrapod vertebrates. While authors have traditionally attributed the evolution of these strategies to factors such as complex topography, unpredictable larval environments, and predation on larvae and eggs, support for any of these hypotheses has been limited. Importantly, most authors have ignored parasites, including unicellular pathogens and multicellular parasites, as selective agents capable of influencing amphibian evolution. Insights in disease transmission, amphibian immunity, and their interaction with various life histories require that we consider parasites to be selective pressures in our exploration of the evolution of amphibian reproductive strategies. I review recent findings and describe how these principles converge to form a novel conceptual hypothesis for the evolution of alternative reproductive strategies in amphibians. I offer some specific predictions and recommend that parasites be considered with other selective pressures when constructing formal, falsifiable hypotheses during evaluative studies of amphibian reproductive behavior.     

Whether larval amphibians school does not affect the parasite aggregation rule: testing the effects of host spatial heterogeneity in field and experimental studies

Almost all macroparasites show over‐dispersed infections within natural host populations such that most parasites are distributed among a few heavily‐infected individuals. Despite the importance of parasite aggregation for understanding system stability, the potential for population regulation, and super‐spreading events, many questions persist about its underlying drivers. Theoretically, aggregation results from heterogeneity in host exposure, resistance, and tolerance. However, few studies have examined how host spatial arrangement – which likely affects both parasite encounter and density‐dependent interactions – influences infection and dispersion, representing a critical gap in our current knowledge regarding the possible drivers of parasite aggregation. Using field data from over 165 ponds and 8000 hosts, we evaluated how the spatial clustering of amphibian larvae within ponds 1) varied among different amphibian species, and 2), affected the distribution of parasites within the host population using Taylor's power law. A complementary mesocosm experiment used field‐guided manipulations of the spatial arrangement of larval amphibians to create a gradient in host clustering while controlling host density, thereby testing for spatial effects on both infection success and aggregation by three different trematode species. Our field data indicated that larval amphibians exhibited significant spatial clustering that was well captured by Taylor's power law (R² 0.92 to 0.97 for different host species), but the residual variation only weakly correlated with observed patterns of trematode parasite over‐dispersion. Correspondingly, experimental manipulation of host clustering had no effects on parasite infection success or the degree of parasite aggregation among cages or mesocosms. Given the importance of parasite over‐dispersion for host populations and disease dynamics, we advocate for further investigations of host and parasite spatial aggregation, particularly studies that incorporate and/or control for heterogeneity in exposure and susceptibility.     

Ecological consequences of amphibian larvae and their native and alien predators on the community structure of temporary ponds

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Making the right choice: testing the drivers of asymmetric infections within hosts and their consequences for pathology

Despite the ubiquity of bilateral symmetry among animals, a long‐standing mystery centers on why parasites that infect paired organs often do so non‐randomly. Examples from diverse host and parasite taxa continue to accumulate, yet little is known about their causes or implications for host–parasite fitness. We combined field surveys, experimental infections, and parasite choice assays to evaluate both competing explanations for – and consequences of – asymmetric infections of amphibian kidneys by echinostome trematodes, which are widespread and potentially pathogenic infections of larval amphibians. Samples from 6001 hosts representing 26 species indicated that echinostome infections exhibit a consistent, right‐kidney bias, with ? 62% of parasites in the right kidney. This pattern could not be explained by variation in kidney size or total infection. Experimental infections of three anuran species reproduced this pattern, with 64% of infections in the right kidney, and indicated it was not the result of differential host or parasite mortality. Based on sequential infection experiments and parasite choice assays, we further showed that earlier infections did not affect the distribution of subsequently colonizing parasites and that echinostome cercariae followed host‐derived cues rather than exhibiting congenital ‘sidedness’. We advance the hypothesis that variation in the position of the right kidney along the anterior–posterior axis controls cue strength in the right nephric duct and thus determines parasite encystment. Correspondingly, anatomical measurements from a subset of larval amphibian hosts revealed that the relative position of the right kidney explained 83% of the variation in infection bias, with no additional contributions associated with kidney volume or host size. We also show that the degree of right‐kidney bias associated positively with host growth in experiments. Morphological asymmetries could therefore function as a unique form of tolerance to mitigate the consequences of infection, despite the oft‐cited costs of asymmetry for mate selection and enemy vulnerability.     

Macroparasite Infections of Amphibians: What Can They Tell Us?

Understanding linkages between environmental changes and disease emergence in human and wildlife populations represents one of the greatest challenges to ecologists and parasitologists. While there is considerable interest in drivers of amphibian microparasite infections and the resulting consequences, comparatively little research has addressed such questions for amphibian macroparasites. What work has been done in this area has largely focused on nematodes of the genus Rhabdias and on two genera of trematodes (Ribeiroia and Echinostoma). Here, we provide a synopsis of amphibian macroparasites, explore how macroparasites may affect amphibian hosts and populations, and evaluate the significance of these parasites in larger community and ecosystem contexts. In addition, we consider environmental influences on amphibian-macroparasite interactions by exploring contemporary ecological factors known or hypothesized to affect patterns of infection. While some macroparasites of amphibians have direct negative effects on individual hosts, no studies have explicitly examined whether such infections can affect amphibian populations. Moreover, due to their complex life cycles and varying degrees of host specificity, amphibian macroparasites have rich potential as bioindicators of environmental modifications, especially providing insights into changes in food webs. Because of their documented pathologies and value as bioindicators, we emphasize the need for broader investigation of this understudied group, noting that ecological drivers affecting these parasites may also influence disease patterns in other aquatic fauna.     

Land Use and Wetland Spatial Position Jointly Determine Amphibian Parasite Communities

Land use change is one of the most commonly cited contributing factors to infectious disease emergence, yet the mechanisms responsible for such changes and the spatial scales at which they operate are rarely identified. The distributions of parasites with complex life cycles depend on interactions between multiple host species, suggesting the net effects of land use on infection patterns may be difficult to predict a priori. Here, we used an information-theoretic approach to evaluate the importance of land use and spatial scale (local, watershed, and regional) in determining the presence and abundance of multi-host trematodes of amphibians. Among 40 wetlands and 160 hosts sampled, trematode abundance, species richness, and the presence and abundance of pathogenic species were strongly influenced by variables at the watershed and regional scales. Based on model averaging results, overall parasite richness and abundance were higher in forested wetlands than in agricultural areas; however, this pattern was influenced by a wetland's proximity to the Mississippi Flyway at the regional scale. These patterns likely reflect the activity of trematode definitive hosts, such as mammals and especially birds, such that infections decreased with increasing distance from the Mississippi River. Interestingly, despite lower mean infections, agricultural wetlands had higher variances and maximum infections. At the wetland scale, phosphorus concentrations and the abundances of intermediate hosts, such as snails and larval amphibians, positively affected parasite distributions. Taken together, these results contribute to our understanding of how altered landscapes affect parasite communities and inform further research on the environmental drivers of amphibian parasite infections.     

Experimental warming drives a seasonal shift in the timing of host‐parasite dynamics with consequences for disease risk

Multi‐species experiments are critical for identifying the mechanisms through which climate change influences population dynamics and community interactions within ecological systems, including infectious diseases. Using a host–parasite system involving freshwater snails, amphibians and trematode parasites, we conducted a year‐long, outdoor experiment to evaluate how warming affected net parasite production, the timing of infection and the resultant pathology. Warming of 3 °C caused snail intermediate hosts to release parasites 9 months earlier and increased infected snail mortality by fourfold, leading to decreased overlap between amphibians and parasites. As a result, warming halved amphibian infection loads and reduced pathology by 67%, despite comparable total parasite production across temperature treatments. These results demonstrate that climate–disease theory should be expanded to account for predicted changes in host and parasite phenology, which may often be more important than changes in total parasite output for predicting climate‐driven changes in disease risk.     

Acanthocephalus bufonis (Acanthocephala) from Bufo marinus (Bufonidae: Amphibia) in Hawaii.

During a survey of the helminth parasites of the introduced toad, Bufo marinus, on O'ahu, Hawaii, an acanthocephalan corresponding to Acanthocephalus bufonis (Shipley, 1903) was found in the intestinal tract. This is a new host and locality record for A. bufonis which has only previously been recorded from amphibians in the Orient. Possible mechanisms for the introduction of A. bufonis to Hawaii, and its transmission to the toad, are discussed. Almost 98% of toads were infected with a mean intensity of 28.6 acanthocephalans per infected toad. There was a significant negative correlation between host length and intensity of infection with subadult toads having significantly higher infection levels than adult male and female toads. Trunk length of both male and female acanthocephalans was significantly related to host length.     

Juvenile western toads, Bufo boreas, avoid chemical cues of snakes fed juvenile, but not larval, conspecifics

Previous investigations have demonstrated the importance of predator diet in chemically mediated antipredator behaviour. However, there are few data on responses to life-stage-specific predator diets, which could be important for animals like amphibians that undergo metamorphosis and must respond to different suites of predators at different life-history stages. In laboratory choice tests, we investigated the chemically mediated avoidance response of juvenile western toads, Bufo boreas, to four different chemical stimuli: (1) live conspecific juveniles; (2) live earthworms; (3) snakes fed juvenile conspecifics; and (4) snakes fed larval conspecifics (tadpoles). Juvenile toads avoided chemical cues from snakes that had eaten juvenile conspecifics, but did not respond to the other three stimuli, including chemical cues from snakes fed larval conspecifics. In addition, the response to cues from snakes fed juveniles differed significantly from that of snakes fed larvae. To our knowledge, this is the first study to demonstrate the importance of diet in predator avoidance of juvenile anurans and the ability of juvenile toads to distinguish between chemical cues from predators that have consumed larval versus juvenile conspecifics. Copyright 2000 The Association for the Study of Animal Behaviour.     

Temperature, hydric environment, and prior pathogen exposure alter the experimental severity of chytridiomycosis in boreal toads

Prevalence of the pathogen Batrachochytrium dendrobatidis (Bd), implicated in amphibian population declines worldwide, is associated with habitat moisture and temperature, but few studies have varied these factors and measured the response to infection in amphibian hosts. We evaluated how varying humidity, contact with water, and temperature affected the manifestation of chytridiomycosis in boreal toads Anaxyrus (Bufo) boreas boreas and how prior exposure to Bd affects the likelihood of survival after re-exposure, such as may occur seasonally in long-lived species. Humidity did not affect survival or the degree of Bd infection, but a longer time in contact with water increased the likelihood of mortality. After exposure to approximately 10(6) Bd zoospores, all toads in continuous contact with water died within 30 d. Moreover, Bd-exposed toads that were disease-free after 64 d under dry conditions, developed lethal chytridiomycosis within 70 d of transfer to wet conditions. Toads in unheated aquaria (mean = 15 degrees C) survived less than 48 d, while those in moderately heated aquaria (mean = 18 degrees C) survived 115 d post-exposure and exhibited behavioral fever, selecting warmer sites across a temperature gradient. We also found benefits of prior Bd infection: previously exposed toads survived 3 times longer than Bd-na?ve toads after re-exposure to 106 zoospores (89 vs. 30 d), but only when dry microenvironments were available. This study illustrates how the outcome of Bd infection in boreal toads is environmentally dependent: when continuously wet, high reinfection rates may overwhelm defenses, but periodic drying, moderate warming, and previous infection may allow infected toads to extend their survival.