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Human-induced salinization caused by the use of road deicing salts, agricultural practices, mining operations, and climate change is a major threat to the biodiversity and functioning of freshwater ecosystems. Yet, it is unclear if freshwater ecosystems are protected from salinization by current water quality guidelines. Leveraging an experimental network of land-based and in-lake mesocosms across North America and Europe, we tested how salinization-indicated as elevated chloride (Cl-) concentration-will affect lake food webs and if two of the lowest Cl- thresholds found globally are sufficient to protect these food webs. Our results indicated that salinization will cause substantial zooplankton mortality at the lowest Cl- thresholds established in Canada (120 mg Cl-/L) and the United States (230 mg Cl-/L) and throughout Europe where Cl- thresholds are generally higher. For instance, at 73% of our study sites, Cl- concentrations that caused a ≥50% reduction in cladoceran abundance were at or below Cl- thresholds in Canada, in the United States, and throughout Europe. Similar trends occurred for copepod and rotifer zooplankton. The loss of zooplankton triggered a cascading effect causing an increase in phytoplankton biomass at 47% of study sites. Such changes in lake food webs could alter nutrient cycling and water clarity and trigger declines in fish production. Current Cl- thresholds across North America and Europe clearly do not adequately protect lake food webs. Water quality guidelines should be developed where they do not exist, and there is an urgent need to reassess existing guidelines to protect lake ecosystems from human-induced salinization.
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Guías como Asunto , Lagos , Salinidad , Calidad del Agua , Animales , Efectos Antropogénicos , Ecosistema , Europa (Continente) , América del Norte , ZooplanctonRESUMEN
Invasive species can have large effects on native communities. When native and invasive species share parasites, an epidemic in a native species could facilitate or inhibit the invasion. We sought to understand how the incidence and timing of epidemics in native species caused by a generalist parasite influenced the success and impact of an invasive species. We focused on North American native and invasive species of zooplankton (Daphnia dentifera and Daphnia lumholtzi, respectively), that can both become infected with a fungal parasite (Metschnikowia bicuspidata). In a laboratory microcosm experiment, we exposed the native species to varying parasite inocula (none, low, high) and two invasive species introduction times (before or during an epidemic in the native species). We found that the invasive species density in treatments with the parasite was higher compared to uninfected treatments, though only the early invasion, low-parasite and uninfected treatments exhibited significant pairwise differences. However, invasive resting eggs were only found in the uninfected treatments. The density of the native species was lowest with a combination of the parasite present, and the invasive species introduced during the epidemic. Native infection prevalence in these treatments (late invasion, parasite present) was also higher than prevalence in treatments where the invasive species was introduced before the epidemic. Therefore, the timing of an invasion relative to an epidemic can affect both the native and invasive species. Our results suggest that the occurrence and timing of epidemics in native species can influence the impacts of a species invasion.
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Daphnia , Especies Introducidas , Animales , ZooplanctonRESUMEN
Legacy polyfluoroalkyl substances (PFAS) [perfluorooctanesulfonate (PFOS) and perfluorooctanoic acid (PFOA)] are being replaced by various other fluorinated compounds, such as hexafluoropropylene oxide dimer acid (GenX). These alternatives are thought to be less bioaccumulative and, therefore, less toxic than legacy PFAS. Contaminant exposures occur concurrently with exposure to natural stressors, including the fungal pathogen Batrachocytrium dendrobatidis (Bd). Despite evidence that other pollutants can increase the adverse effects of Bd on anurans, no studies have examined the interactive effects of Bd and PFAS. This study tested the growth and developmental effects of PFOS, PFOA, and GenX on gray treefrog (Hyla versicolor) tadpoles, followed by a Bd challenge after metamorphosis. Despite PFAS exposure only occurring during the larval stage, carry-over effects on growth were observed post metamorphosis. Further, PFAS interacted with Bd exposure to influence growth; Bd-exposed animals had significantly shorter SVL [snout-vent length (mm)] with significantly increased body condition, among other time-dependent effects. Our data suggest that larval exposure to PFAS can continue to impact growth in the juvenile stage after exposure has ended. Contrary to predictions, GenX affected terrestrial performance more consistently than its legacy congener, PFOA. Given the role of Bd in amphibian declines, further investigation of interactions of PFAS with Bd and other environmentally relevant pathogens is warranted.
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Ácidos Alcanesulfónicos , Fluorocarburos , Animales , Larva/microbiología , Fluorocarburos/toxicidad , Anuros/microbiología , Ácidos Alcanesulfónicos/toxicidadRESUMEN
It is well-established that both resources and infectious disease can influence species invasions, but little is known regarding interactive effects of these two factors. We performed a series of experiments to understand how resources and parasites can jointly affect the ability of a freshwater invasive zooplankton to establish in a population of a native zooplankton. In a life history trial, we found that both species increased offspring production to the same degree as algal resources increased, suggesting that changes in resources would have similar effects on both species. In a microcosm experiment simulating an invasion, we found that the invasive species reached its highest densities when there was a combination of both high resources and the presence of a shared parasite, but not for each of these conditions alone (i.e., a significant resource x parasite interaction). This result can be explained by changes in native host population density; high resource levels initially led to an increase in the density of the native host, which caused larger epidemics when the parasite was present. This high infection prevalence caused a subsequent reduction in native host density, increasing available resources and allowing the invasive species to establish relatively dense populations. Thus, in this system, native communities with a combination of high resource levels and parasitism may be the most vulnerable to invasions. More generally, our results suggest that parasitism and resource availability can have interactive, non-additive effects on the outcome of invasions.
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Parásitos , Zooplancton , Animales , Daphnia , Agua Dulce , Densidad de PoblaciónRESUMEN
Emerging infectious diseases have been documented in numerous plant and animal populations. The infectious disease amphibian chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), is associated with global amphibian population declines. While much Bd-amphibian research has centered on response variation in hosts, a paucity of information exists on how variation in the pathogen, such as strain differences, affects infection dynamics. To examine how different Bd strains may differentially impact multiple hosts, we conducted laboratory experiments to measure 2 infection outcomes, viz. host survival and pathogen load, in 3 amphibian host species (Pacific treefrog, western toad, and Cascades frog) after exposure to 3 different Bd strains (an additional fourth Bd strain was tested in toads only). Our results confirm that the infection response differs among host species. Western toads experienced significant mortality, but Pacific treefrogs and Cascades frogs did not. Interestingly, our experiment also captured strain-dependent virulence variation but only in 1 host species, the western toad. Increased mortality was observed in 2 of the 4 Bd strains tested in this host species. Toads were also the only host species found to have variable pathogen load dependent on strain type; individuals exposed to the Panama strain harbored significantly higher loads compared to all other strains. These findings underscore the dynamic nature of Bd infection, showing that virulence can vary contingent on host and strain type. We highlight the importance of both host- and pathogen-dependent factors in determining overall infection virulence and show the need for in vivo testing to fully assess pathogenicity.
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Bufonidae/microbiología , Quitridiomicetos/patogenicidad , Enfermedades Transmisibles Emergentes/veterinaria , Micosis/veterinaria , Ranidae/microbiología , Animales , Especificidad del Huésped , Micosis/microbiología , Factores de Tiempo , VirulenciaRESUMEN
Generalist parasites can strongly influence interactions between native and invasive species. Host competence can be used to predict how an invasive species will affect community disease dynamics; the addition of a highly competent, invasive host is predicted to increase disease. However, densities of invasive and native species can also influence the impacts of invasive species on community disease dynamics. We examined whether information on host competence alone could be used to accurately predict the effects of an invasive host on disease in native hosts. We first characterized the relative competence of an invasive species and a native host species to a native parasite. Next, we manipulated species composition in mesocosms and found that host competence results did not accurately predict community dynamics. While the invasive host was more competent than the native, the presence of the native (lower competence) host increased disease in the invasive (higher competence) host. To identify potential mechanisms driving these patterns, we analyzed a two-host, one-parasite model parameterized for our system. Our results demonstrate that patterns of disease were primarily driven by relative population densities, mediated by asymmetry in intra- and interspecific competition. Thus, information on host competence alone may not accurately predict how an invasive species will influence disease in native species.
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Interacciones Huésped-Parásitos , Especies Introducidas , Especificidad del Huésped , Densidad de Población , Dinámica PoblacionalRESUMEN
Global declines in biodiversity are altering disease dynamics in complex and multifaceted ways. Changes in biodiversity can have several outcomes on disease risk, including dilution and amplification effects, both of which can have a profound influence on the effects of disease in a community. The dilution effect occurs when biodiversity and disease risk are inversely related, whereas the amplification effect is a positive relationship between biodiversity and disease risk. We tested these effects with an emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis (Bd), which is responsible for catastrophic amphibian population declines and extinctions worldwide. Despite the rapid and continued spread of Bd, the influence of host diversity on Bd dynamics remains unknown. We experimentally manipulated host diversity and density in the presence of Bd and found a dilution effect where increased species richness reduced disease risk, even when accounting for changes in density. These results demonstrate the general importance of incorporating community structure into studies of disease dynamics and have implications for the effects of Bd in ecosystems that differ in biodiversity.
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Anfibios/microbiología , Quitridiomicetos/patogenicidad , AnimalesRESUMEN
Concentrations of microplastics in aquatic environments continue to rise due to industrial production and pollution. While there are various concerns regarding potential deleterious effects of microplastics on ecosystems, several knowledge gaps remain, including the potential for microplastics to directly and indirectly affect biotic interactions and food web dynamics. We explored the effects of environmentally relevant microplastic concentrations on two co-exposed species of herbaceous freshwater crustaceous zooplankton, filter feeding Daphnia dentifera and selective phytoplankton grazers Arctodiaptomus dorsalis. Study organisms were exposed to different concentrations of microplastics (plastic polyethylene microspheres; low = 2.38 × 10-8 mg/L, medium = 0.023 mg/L, high = 162 mg/L), phytoplankton prey, and predator cues, simulating a simple freshwater food web. Microplastic uptake was greater by D. dentifera, but both species were characterized by decreased algal consumption in the highest microplastic concentration treatment. Importantly, aqueous chlorophyll-a concentrations at the conclusion of the experiment were greater for the high microplastic treatment than all controls and other microplastic treatments. Finally, a predator effect was only apparent for D. dentifera, with greater microplastic uptake in the presence of a predator. We conclude that microplastics may adversely impact the ability of zooplankton to feed on algae and potentially release algae from consumptive control by herbivorous zooplankton. SYNOPSIS: This research aimed to better understand the broader food web effects of environmentally relevant microplastic concentrations on aquatic communities.
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Microplásticos , Contaminantes Químicos del Agua , Animales , Microplásticos/toxicidad , Zooplancton , Plásticos , Cadena Alimentaria , Ecosistema , Contaminantes Químicos del Agua/análisis , Fitoplancton , Polietileno , PlantasRESUMEN
In nature, individual hosts often encounter multiple pathogens simultaneously, which can lead to additive, antagonistic, or synergistic effects on hosts. Synergistic effects on infection prevalence or severity could greatly affect host populations. However, ecologists and managers often overlook the influence of pathogen combinations on hosts. This is especially true in amphibian conservation, even though multiple pathogens coexist within amphibian populations, and several pathogens have been implicated in amphibian population declines and extinctions. Using an amphibian host, Pseudacris regilla (Pacific treefrog), we experimentally investigated interactive effects among three pathogens: the trematode Ribeiroia sp. (hereafter, Ribeiroia), the fungus Batrachochytrium dendrobatidis (hereafter, BD), and the water mold Achlya flagellata. We detected no effects of A. flagellata, but did find effects of Ribeiroia and BD that varied depending on context. Low doses of Ribeiroia caused relatively few malformations, while higher Ribeiroia doses caused numerous deformities dominated by missing and reduced limbs and limb elements. Exposure to low doses of BD accelerated larval host development, despite there being no detectable BD infections, while exposure to higher BD doses caused infection but did not alter developmental rate. Hosts exposed to both Ribeiroia and BD exhibited the highest mortality, although overall evidence of interactive effects of multiple pathogens was limited. We suggest further research on the influence of multi-pathogen assemblages on amphibians, particularly under a variety of ecological conditions and with a wider diversity of hosts and pathogens.
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Achlya/fisiología , Anuros/microbiología , Quitridiomicetos/fisiología , Interacciones Huésped-Patógeno , Trematodos/fisiología , Animales , Anuros/crecimiento & desarrollo , Anuros/parasitología , Anomalías Congénitas/microbiología , Anomalías Congénitas/parasitología , Larva/crecimiento & desarrollo , Larva/microbiología , Larva/parasitología , Metamorfosis Biológica , Micosis/microbiología , Micosis/veterinaria , Infecciones por Trematodos/microbiología , Infecciones por Trematodos/parasitología , Infecciones por Trematodos/veterinariaRESUMEN
Natural populations encounter a variety of threats that can increase their risk of extinction. Populations can avoid extinction through evolutionary rescue (ER), which occurs when an adaptive, genetic response to selection allows a population to recover from an environmental change that would otherwise cause extinction. While the traditional framework for ER was developed with abiotic risk factors in mind, ER may also occur in response to a biotic source of demographic change, such as the introduction of a novel pathogen. We first describe how ER in response to a pathogen differs from the traditional ER framework; density-dependent transmission, pathogen evolution, and pathogen extinction can change the strength of selection imposed by a pathogen and make host population persistence more likely. We also discuss several variables that affect traditional ER (abundance, genetic diversity, population connectivity, and community composition) that also directly affect disease risk resulting in diverse outcomes for ER in host-pathogen systems. Thus, generalizations developed in studies of traditional ER may not be relevant for ER in response to the introduction of a pathogen. Incorporating pathogens into the framework of ER will lead to a better understanding of how and when populations can avoid extinction in response to novel pathogens.
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The ability of an organism to tolerate seasonal temperature changes, such as extremely cold temperatures during the winter, can be influenced by their pathogens. We tested how exposure to a virulent fungal pathogen, Batrachochytrium dendrobatidis (Bd), affected the critical thermal minimum (CTmin) of two frog species, Hyla versicolor (gray treefrog) and Lithobates palustris (pickerel frog). The CTmin is the minimum thermal performance point of an organism, which we estimated via righting response trials. For both frog species, we compared the righting response of Bd-exposed and Bd-unexposed individuals in either a constant (15ºC) environment or with decreasing temperatures (-1°C/2.5 min) starting from 15°C. The CTmin for both species was higher for Bd-exposed frogs than unexposed frogs, and the CTmin of H. versicolor was higher than L. palustris. We also found that Bd-exposed frogs of both species righted themselves significantly fewer times in both decreasing and constant temperature trials. Our findings show that pathogen exposure can reduce cold tolerance and limit the thermal performance range of hosts, which may lead to increased overwintering mortality.
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Introduced pathogens can alter the geographic distribution of susceptible host species. For example, Batrachochytrium dendrobatidis (Bd) is a fungal pathogen that has been linked to the global decline and extinction of numerous amphibian species during the last four decades. A growing number of studies have described the distribution of Bd and susceptible hosts across the globe; however, knowledge on how Bd may shape the climatic niche of susceptible species is still missing. We estimated the effect of Bd on the geographic distribution and niche dynamics of the critically endangered lowland robber frog (Craugastor ranoides) in Costa Rica. We found a reduction of 98% in the geographic range of this species by 1995, following the epizootic outbreaks of Bd that affected Costa Rica in the 1980 and early 1990s. We also quantified niche contraction and found that the species is currently restricted to dry and warm environments that have been considered unsuitable for Bd. Our results contribute to the understanding of how emerging pathogens shape the climatic niches and geographic distribution of susceptible species.
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Anuros , Batrachochytrium/patogenicidad , Especies en Peligro de Extinción , Micosis/veterinaria , Animales , Anuros/microbiología , Clima , Brotes de Enfermedades/veterinaria , Micosis/microbiologíaRESUMEN
It is unclear how suitable human-made wetlands are for supporting wildlife and how they impact wildlife disease risk. Natural wetlands (those that were created without human actions) can support more diverse and resilient communities that are at lower risk of disease outbreaks. We compared frog community composition and infection with the pathogenic fungus Batrachochytrium dendrobatidis (Bd) between human-made and natural wetlands in Tippecanoe County, Indiana, US. We conducted visual encounter surveys of frog communities and quantified Bd infection prevalence at four natural and five human-made wetlands. Water parameters associated with human practices (e.g., pH, salinity) and surrounding land use were also compared across sites. We found higher Bd infection prevalence at human-made sites than at natural sites, with monthly differences showing highest infection in spring and fall, and decreasing infection with increasing water temperature. However, we found no differences between human-made and natural sites regarding amphibian community composition, water quality, or surrounding land use. Further, we found frog density increased with distance to nearest roads among both human-made and natural sites. These findings might suggest that human-made wetlands can support frog communities similar to natural wetlands, but pose a greater risk of Bd infection.
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Anuros/microbiología , Batrachochytrium/aislamiento & purificación , Micosis/veterinaria , Humedales , Animales , Femenino , Humanos , Indiana , Masculino , Micosis/microbiología , Estaciones del AñoRESUMEN
Understanding the transmission and dynamics of infectious diseases in natural communities requires understanding the extent to which the ecology, evolution and epidemiology of those diseases are shaped by alternative hosts. We performed laboratory experiments to test how parasite spillover affected traits associated with transmission in two co-occurring parasites: the bacterium Pasteuria ramosa and the fungus Metschnikowia bicuspidata Both parasites were capable of transmission from the reservoir host (Daphnia dentifera) to the spillover host (Ceriodaphnia dubia), but this occurred at a much higher rate for the fungus than the bacterium. We quantified transmission potential by combining information on parasite transmission and growth rate, and used this to compare parasite fitness in the two host species. For both parasites, transmission potential was lower in the spillover host. For the bacterium, virulence was higher in the spillover host. Transmission back to the original host was high for both parasites, with spillover influencing transmission rate of the fungus but not the bacterium. Thus, while inferior, the spillover host is not a dead-end for either parasite. Overall, our results demonstrate that the presence of multiple hosts in a community can have important consequences for disease transmission, and host and parasite fitness.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.
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Cladóceros/microbiología , Interacciones Huésped-Patógeno , Metschnikowia/fisiología , Pasteuria/fisiología , Animales , Evolución Biológica , Daphnia/microbiología , Femenino , Especificidad del HuéspedRESUMEN
Variation in host responses to pathogens can have cascading effects on populations and communities when some individuals or groups of individuals display disproportionate vulnerability to infection or differ in their competence to transmit infection. The fungal pathogen, Batrachochytrium dendrobatidis (Bd) has been detected in almost 700 different amphibian species and is implicated in numerous global amphibian population declines. Identifying key hosts in the amphibian-Bd system-those who are at greatest risk or who pose the greatest risk for others-is challenging due in part to many extrinsic environmental factors driving spatiotemporal Bd distribution and context-dependent host responses to Bd in the wild. One way to improve predictive risk models and generate testable mechanistic hypotheses about vulnerability is to complement what we know about the spatial epidemiology of Bd with data collected through comparative experimental studies. We used standardized pathogen challenges to quantify amphibian survival and infection trajectories across 20 post-metamorphic North American species raised from eggs. We then incorporated trait-based models to investigate the predictive power of phylogenetic history, habitat use, and ecological and life history traits in explaining responses to Bd. True frogs (Ranidae) displayed the lowest infection intensities, whereas toads (Bufonidae) generally displayed the greatest levels of mortality after Bd exposure. Affiliation with ephemeral aquatic habitat and breadth of habitat use were strong predictors of vulnerability to and intensity of infection and several other traits including body size, lifespan, age at sexual maturity, and geographic range also appeared in top models explaining host responses to Bd. Several of the species examined are highly understudied with respect to Bd such that this study represents the first experimental susceptibility data. Combining insights gained from experimental studies with observations of landscape-level disease prevalence may help explain current and predict future pathogen dynamics in the Bd system.
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Anfibios/microbiología , Quitridiomicetos/patogenicidad , Enfermedades Transmisibles Emergentes/epidemiología , Ecología , Interacciones Huésped-Patógeno , Micosis/microbiología , Animales , Bufonidae/microbiología , Ecosistema , Filogenia , Ranidae/microbiologíaRESUMEN
Wildlife epidemiological outcomes can depend strongly on the composition of an ecological community, particularly when multiple host species are affected by the same pathogen. However, the relationship between host species richness and disease risk can vary with community context and with the degree of spillover transmission that occurs among co-occurring host species. We examined the degree to which host species composition influences infection by Batrachochytrium dendrobatidis (Bd), a widespread fungal pathogen associated with amphibian population declines around the world, and whether transmission occurs from one highly susceptible host species to other co-occurring host species. By manipulating larval assemblages of three sympatric amphibian species in the laboratory, we characterized the relationship between host species richness and infection severity, whether infection mediates growth and survivorship differently across various combinations of host species, and whether Bd is transmitted from experimentally inoculated tadpoles to uninfected tadpoles. We found evidence of a dilution effect where Bd infection severity was dramatically reduced in the most susceptible of the three host species (Anaxyrus boreas). Infection also mediated survival and growth of all three host species such that the presence of multiple host species had both positive (e.g., infection reduction) and negative (e.g., mortality) effects on focal species. However, we found no evidence that Bd infection is transmitted by this species. While these results demonstrate that host species richness as well as species identity underpin infection dynamics in this system, dilution is not the product of reduced transmission via fewer infectious individuals of a susceptible host species. We discuss various mechanisms, including encounter reduction and antagonistic interactions such as competition and opportunistic cannibalism that may act in concert to mediate patterns of infection severity, growth, and mortality observed in multihost communities.
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Recent emergence and spread of the amphibian fungal pathogen, Batrachochytrium dendrobatidis (Bd) has been attributed to a number of factors, including environmental stressors that increase host susceptibility to Bd. Physiological stress can increase circulating levels of the hormone, corticosterone, which can alter a host's physiology and affect its susceptibility to pathogens. We experimentally elevated whole-body levels of corticosterone in both larval and post-metamorphic amphibians, and subsequently tested their susceptibility to Bd. Larvae of three species were tested (Anaxyrus boreas, Rana cascadae, and Lithobates catesbeianus) and one species was tested after metamorphosis (R. cascadae). After exposure to Bd, we measured whole-body corticosterone, infection, mortality, growth, and development. We found that exposure to exogenous corticosterone had no effect on Bd infection in any species or at either life stage. Species varied in whole-body corticosterone levels and exposure to corticosterone reduced mass in A. boreas and R. cascadae larvae. Exposure to Bd did not affect mortality, but had a number of sublethal effects. Across species, larvae exposed to Bd had higher corticosterone levels than unexposed larvae, but the opposite pattern was found in post-metamorphic R. cascadae. Bd exposure also increased larval length in all species and increased mass in R. cascadae larvae. Our results indicate that caution is warranted in assuming a strong link between elevated levels of corticosterone and disease susceptibility in amphibians. The role of physiological stress in altering Bd prevalence in amphibian populations is likely much more complicated than can be explained by examining a single "stress" endpoint.
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Anuros/microbiología , Quitridiomicetos/patogenicidad , Corticosterona/metabolismo , Larva/microbiología , Micosis/veterinaria , Animales , Anuros/crecimiento & desarrollo , Corticosterona/análisis , Susceptibilidad a Enfermedades/microbiología , Interacciones Huésped-Patógeno , Micosis/microbiología , Estrés FisiológicoRESUMEN
Metamorphosis is often characterized by profound changes in morphology and physiology that can affect the dynamics of species interactions. For example, the interaction between a pathogen and its host may differ depending on the life stage of the host or pathogen. One pathogen that infects hosts with complex life cycles is the emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis (Bd). We sought to determine how conditions at the larval stage can affect variation in development and patterns of Bd infection across amphibian life stages. We used outdoor experimental mesocosms to simulate natural pond habitats and manipulated the presence of Bd, the larval density, and the number of host species in larvae of two co-occurring amphibian species (Rana cascadae and Pseudacris regilla). We found that infection differed between species throughout development; P. regilla consistently had higher infection severity compared to R. cascadae. Additionally, while up to 100% of larvae were infected, only 18.2% of R. cascadae and 81.5% of P. regilla were infected after metamorphosis. This indicates that amphibians have the ability to recover from Bd infection as they undergo metamorphosis. Higher larval densities in P. regilla led to a shorter larval period, and individuals with a shorter larval period had lower infection severity. This led to a trend where P. regilla larvae reared at high densities tended to have lower infection prevalence after metamorphosis. We also found that exposure to Bd increased larval mortality and prolonged the larval period in P. regilla, indicating that P. regilla are susceptible to the negative effects of Bd as larvae. This study demonstrates that host density, species composition, and pathogen exposure may all interact to influence development and infection in hosts with complex life cycles.
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Enfermedades Transmisibles/microbiología , Estadios del Ciclo de Vida/fisiología , Ranidae/crecimiento & desarrollo , Animales , Quitridiomicetos/patogenicidad , Humanos , Larva/crecimiento & desarrollo , Larva/microbiología , Metamorfosis Biológica/fisiología , Ranidae/microbiologíaRESUMEN
Direct predation upon parasites has the potential to reduce infection in host populations. For example, the fungal parasite of amphibians, Batrachochytrium dendrobatidis (Bd), is commonly transmitted through a free-swimming zoospore stage that may be vulnerable to predation. Potential predators of Bd include freshwater zooplankton that graze on organisms in the water column. We tested the ability of two species of freshwater crustacean (Daphnia magna and D. dentifera) to consume Bd and to reduce Bd density in water and infection in tadpoles. In a series of laboratory experiments, we allowed Daphnia to graze in water containing Bd while manipulating Daphnia densities, Daphnia species identity, grazing periods and concentrations of suspended algae (Ankistrodesmus falcatus). We then exposed tadpoles to the grazed water. We found that high densities of D. magna reduced the amount of Bd detected in water, leading to a reduction in the proportion of tadpoles that became infected. Daphnia dentifera, a smaller species of Daphnia, also reduced Bd in water samples, but did not have an effect on tadpole infection. We also found that algae affected Bd in complex ways. When Daphnia were absent, less Bd was detected in water and tadpole samples when concentrations of algae were higher, indicating a direct negative effect of algae on Bd. When Daphnia were present, however, the amount of Bd detected in water samples showed the opposite trend, with less Bd when densities of algae were lower. Our results indicate that Daphnia can reduce Bd levels in water and infection in tadpoles, but these effects vary with species, algal concentration, and Daphnia density. Therefore, the ability of predators to consume parasites and reduce infection is likely to vary depending on ecological context.
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The effects of parasites and pathogens on host behaviors may be particularly important in predator-prey contexts, since few animal behaviors are more crucial for ensuring immediate survival than the avoidance of lethal predators in nature. We examined the effects of an emerging fungal pathogen of amphibians, Batrachochytrium dendrobatidis, on anti-predator behaviors of tadpoles of four frog species. We also investigated whether amphibian predators consumed infected prey, and whether B. dendrobatidis caused differences in predation rates among prey in laboratory feeding trials. We found differences in anti-predator behaviors among larvae of four amphibian species, and show that infected tadpoles of one species (Anaxyrus boreas) were more active and sought refuge more frequently when exposed to predator chemical cues. Salamander predators consumed infected and uninfected tadpoles of three other prey species at similar rates in feeding trials, and predation risk among prey was unaffected by B. dendrobatidis. Collectively, our results show that even sub-lethal exposure to B. dendrobatidis can alter fundamental anti-predator behaviors in some amphibian prey species, and suggest the unexplored possibility that indiscriminate predation between infected and uninfected prey (i.e., non-selective predation) could increase the prevalence of this widely distributed pathogen in amphibian populations. Because one of the most prominent types of predators in many amphibian systems is salamanders, and because salamanders are susceptible to B. dendrobatidis, our work suggests the importance of considering host susceptibility and behavioral changes that could arise from infection in both predators and prey.