Search

Losses in biodiversity can alter disease risk through changes in host species composition. Host species vary in pathogen susceptibility and competence, yet how changes in diversity alter host–pathogen dynamics remains unclear in many systems, particularly with respect to generalist pathogens. Amphibians are experiencing worldwide population declines linked to generalist pathogens, such as ranavirus, and thus represent an ideal group to investigate how host species composition affects disease risk. We conducted experiments in which amphibian larvae of three native species (Pacific tree frogs, Pseudacris regilla; Cascades frogs, Rana cascadae; and Western toads, Anaxyrus boreas) were exposed to ranavirus individually (in the laboratory) or as assemblages (in outdoor mesocosms). In a laboratory experiment, we observed low survival and high viral loads in P. regilla compared to the other species, suggesting that this species was highly susceptible to the pathogen. In the mesocosm experiment, we observed 41% A. boreas mortality when alone and 98% mortality when maintained with P. regilla and R. cascadae. Our results suggest that the presence of highly susceptible species can alter disease dynamics across multiple species, potentially increasing infection risk and mortality in co‐occurring species. [ABSTRACT FROM AUTHOR]

1. Host density is hypothesized to be a major driver of variability in the responses and outcomes of wildlife populations following pathogen invasion. While the effects of host density on pathogen transmission have been extensively studied, these studies are dominated by theoretical analyses and small‐scale experiments. This focus leads to an incomplete picture regarding how host density drives observed variability in disease outcomes in the field. 2. Here, we leveraged a dataset of hundreds of replicate amphibian populations that varied by orders of magnitude in host density. We used these data to test the effects of host density on three outcomes following the arrival of the amphibian‐killing fungal pathogen Batrachochytrium dendrobatidis (Bd): the probability that Bd successfully invaded a host population and led to a pathogen outbreak, the magnitude of the host population‐level decline following an outbreak and within‐host infection dynamics that drive population‐level outcomes in amphibian–pathogen systems. 3. Based on previous small‐scale transmission experiments, we expected that populations with higher densities would be more likely to experience Bd outbreaks and would suffer larger proportional declines following outbreaks. To test these predictions, we developed and fitted a Hidden Markov Model that accounted for imperfectly observed disease outbreak states in the amphibian populations we surveyed. 4. Contrary to our predictions, we found minimal effects of host density on the probability of successful Bd invasion, the magnitude of population decline following Bd invasion and the dynamics of within‐host infection intensity. Environmental conditions, such as summer temperature, winter severity and the presence of pathogen reservoirs, were more predictive of variability in disease outcomes. 5. Our results highlight the limitations of extrapolating findings from small‐scale transmission experiments to observed disease trajectories in the field and provide strong evidence that variability in host density does not necessarily drive variability in host population responses following pathogen arrival. In an applied context, we show that feedbacks between host density and disease will not necessarily affect the success of reintroduction efforts in amphibian‐Bd systems of conservation concern. [ABSTRACT FROM AUTHOR]

Host species that can independently maintain a pathogen in a host community and contribute to infection in other species are important targets for disease management. However, the potential of host species to maintain a pathogen is not fixed over time, and an important challenge is understanding how within‐ and across‐season variability in host maintenance potential affects pathogen persistence over longer time scales relevant for disease management (e.g., years). Here, we sought to understand the causes and consequences of seasonal infection dynamics in leopard frogs (Rana sphenocephala and Rana pipiens) infected with the fungal pathogen Batrachochytrium dendrobatidis (Bd). We addressed three questions broadly applicable to seasonal host–parasite systems. First, to what degree are observed seasonal patterns in infection driven by temperature‐dependent infection processes compared to seasonal host demographic processes? Second, how does seasonal variation in maintenance potential affect long‐term pathogen persistence in multi‐host communities? Third, does high deterministic maintenance potential relate to the long‐term stochastic persistence of pathogens in host populations with seasonal infection dynamics? To answer these questions, we used field data collected over 3 years on >1400 amphibians across four geographic locations, laboratory and mesocosm experiments, and a novel mathematical model. We found that the mechanisms that drive seasonal prevalence were different from those driving seasonal infection intensity. Seasonal variation in Bd prevalence was driven primarily by changes in host contact rates associated with breeding migrations to and from aquatic habitat. In contrast, seasonal changes in infection intensity were driven by temperature‐induced changes in Bd growth rate. Using our model, we found that the maintenance potential of leopard frogs varied significantly throughout the year and that seasonal troughs in infection prevalence made it unlikely that leopard frogs were responsible for long‐term Bd persistence in these seasonal amphibian communities, highlighting the importance of alternative pathogen reservoirs for Bd persistence. Our results have broad implications for management in seasonal host–pathogen systems, showing that seasonal changes in host and pathogen vital rates, rather than the depletion of susceptible hosts, can lead to troughs in pathogen prevalence and stochastic pathogen extirpation. [ABSTRACT FROM AUTHOR]

Resistance and tolerance are unique host defence strategies that can limit the impacts of a pathogen on a host. However, for most wildlife–pathogen systems, there are still fundamental uncertainties regarding (a) how changes in resistance and tolerance can affect disease outcomes and (b) the mechanisms underlying resistance and tolerance in host populations.Here, we first compared observed patterns of resistance and tolerance and their effects on disease outcomes among salamander species that are susceptible to infection and mortality from the emerging fungal pathogen Batrachochytrium salamandrivorans (Bsal). We then tested whether two putative mechanisms that contribute to host resistance and tolerance, skin sloughing and skin lesion reduction, predicted reduced Bsal growth rate or increased host survival during infection, respectively.We performed multi‐dose Bsal challenge experiments on four species of Salamandridae found throughout North America. We combined the laboratory experiments with dynamic models and sensitivity analysis to examine how changes in load‐dependent resistance and tolerance functions affected Bsal‐induced mortality risk. Finally, we used our disease model to test whether skin sloughing and lesion reduction predicted variability in infection outcomes not described by Bsal infection intensity.We found that resistance and tolerance differed significantly among salamander species, with the most susceptible species being both less resistance and less tolerant of Bsal infection. Our dynamic model showed that the relative influence of resistance versus tolerance on host survival was species‐dependent—increasing resistance was only more influential than increasing tolerance for the least tolerant species where changes in pathogen load had a threshold‐like effect on host survival. Testing two candidate mechanisms of resistance and tolerance, skin sloughing and lesion reduction, respectively, we found limited support that either of these processes were strong mechanisms of host defence.Our study contributes to a broader understanding of resistance and tolerance in host–pathogen systems by showing that differences in host tolerance can significantly affect whether changes in resistance or tolerance have larger effects on disease outcomes, highlighting the need for species and even population‐specific management approaches that target host defence strategies. A free Plain Language Summary can be found within the Supporting Information of this article. [ABSTRACT FROM AUTHOR]

Emerging infectious diseases have caused many species declines, changes in communities and even extinctions. There are also many species that persist following devastating declines due to disease. The broad mechanisms that enable host persistence following declines include evolution of resistance or tolerance, changes in immunity and behaviour, compensatory recruitment, pathogen attenuation, environmental refugia, density‐dependent transmission and changes in community composition. Here we examine the case of chytridiomycosis, the most important wildlife disease of the past century. We review the full breadth of mechanisms allowing host persistence, and synthesise research on host, pathogen, environmental and community factors driving persistence following chytridiomycosis‐related declines and overview the current evidence and the information required to support each mechanism. We found that for most species the mechanisms facilitating persistence have not been identified. We illustrate how the mechanisms that drive long‐term host population dynamics determine the most effective conservation management strategies. Therefore, understanding mechanisms of host persistence is important because many species continue to be threatened by disease, some of which will require intervention. The conceptual framework we describe is broadly applicable to other novel disease systems. [ABSTRACT FROM AUTHOR]

World‐wide, infectious diseases represent a major source of mortality in humans and livestock. For wildlife populations, disease‐induced mortality is likely even greater, but remains notoriously difficult to estimate—especially for endemic infections. Approaches for quantifying wildlife mortality due to endemic infections have historically been limited by an inability to directly observe wildlife mortality in nature.Here we address a question that can rarely be answered for endemic pathogens of wildlife: what are the population‐ and landscape‐level effects of infection on host mortality? We combined laboratory experiments, extensive field data and novel mathematical models to indirectly estimate the magnitude of mortality induced by an endemic, virulent trematode parasite (Ribeiroia ondatrae) on hundreds of amphibian populations spanning four native species.We developed a flexible statistical model that uses patterns of aggregation in parasite abundance to infer host mortality. Our model improves on previous approaches for inferring host mortality from parasite abundance data by (i) relaxing restrictive assumptions on the timing of host mortality and sampling, (ii) placing all mortality inference within a Bayesian framework to better quantify uncertainty and (iii) accommodating data from laboratory experiments and field sampling to allow for estimates and comparisons of mortality within and among host populations.Applying our approach to 301 amphibian populations, we found that trematode infection was associated with an average of between 13% and 40% population‐level mortality. For three of the four amphibian species, our models predicted that some populations experienced >90% mortality due to infection, leading to mortality of thousands of amphibian larvae within a pond. At the landscape scale, the total number of amphibians predicted to succumb to infection was driven by a few high mortality sites, with fewer than 20% of sites contributing to greater than 80% of amphibian mortality on the landscape.The mortality estimates in this study provide a rare glimpse into the magnitude of effects that endemic parasites can have on wildlife populations and our theoretical framework for indirectly inferring parasite‐induced mortality can be applied to other host–parasite systems to help reveal the hidden death toll of pathogens on wildlife hosts. [ABSTRACT FROM AUTHOR]

Pathogen persistence in host communities is influenced by processes operating at the individual host to landscape‐level scale, but isolating the relative contributions of these processes is challenging. We developed theory to partition the influence of host species, habitat patches and landscape connectivity on pathogen persistence within metacommunities of hosts and pathogens. We used this framework to quantify the contributions of host species composition and habitat patch identity on the persistence of an amphibian pathogen across the landscape. By sampling over 11 000 hosts of six amphibian species, we found that a single host species could maintain the pathogen in 91% of observed metacommunities. Moreover, this dominant maintenance species contributed, on average, twice as much to landscape‐level pathogen persistence compared to the most influential source patch in a metacommunity. Our analysis demonstrates substantial inequality in how species and patches contribute to pathogen persistence, with important implications for targeted disease management. [ABSTRACT FROM AUTHOR]

Moving animals on a landscape through translocations and reintroductions is an important management tool used in the recovery of endangered species, particularly for the maintenance of population genetic diversity and structure. Management of imperiled amphibian species rely heavily on translocations and reintroductions, especially for species that have been brought to the brink of extinction by habitat loss, introduced species, and disease. One striking example of amphibian declines and associated management efforts is in California's Sequoia and Kings Canyon National Parks with the mountain yellow‐legged frog species complex (Rana sierrae/muscosa). Mountain yellow‐legged frogs have been extirpated from more than 93% of their historic range, and limited knowledge of their population genetics has made long‐term conservation planning difficult. To address this, we used 598 archived skin swabs from both extant and extirpated populations across 48 lake basins to generate a robust Illumina‐based nuclear amplicon data set. We found that samples grouped into three main genetic clusters, concordant with watershed boundaries. We also found evidence for historical gene flow across watershed boundaries with a north‐to‐south axis of migration. Finally, our results indicate that genetic diversity is not significantly different between populations with different disease histories. Our study offers specific management recommendations for imperiled mountain yellow‐legged frogs and, more broadly, provides a population genetic framework for leveraging minimally invasive samples for the conservation of threatened species. [ABSTRACT FROM AUTHOR]

Symbiotic microbial communities are important for host health, but the processes shaping these communities are poorly understood. Understanding how community assembly processes jointly affect microbial community composition is limited because inflexible community models rely on rejecting dispersal and drift before considering selection. We developed a flexible community assembly model based on neutral theory to ask: How do dispersal, drift and selection concurrently affect the microbiome across environmental gradients? We applied this approach to examine how a fungal pathogen affected the assembly processes structuring the amphibian skin microbiome. We found that the rejection of neutrality for the amphibian microbiome across a fungal gradient was not strictly due to selection processes, but was also a result of species‐specific changes in dispersal and drift. Our modelling framework brings the qualitative recognition that niche and neutral processes jointly structure microbiomes into quantitative focus, allowing for improved predictions of microbial community turnover across environmental gradients. [ABSTRACT FROM AUTHOR]

Abstract: A fundamental goal of disease ecology is to determine the landscape and environmental processes that drive disease dynamics at different biological levels to guide management and conservation. Although ranaviruses (family Iridoviridae) are emerging amphibian pathogens, few studies have conducted comprehensive field surveys to assess potential drivers of ranavirus disease dynamics. We examined the factors underlying patterns in site‐level ranavirus presence and individual‐level ranavirus infection in 76 ponds and 1,088 individuals representing five amphibian species within the East Bay region of California. Based on a competing‐model approach followed by variance partitioning, landscape and biotic variables explained the most variation in site‐level presence. However, biotic and individual‐level variables explained the most variation in individual‐level infection. Distance to nearest ranavirus‐infected pond (the landscape factor) was more important than biotic factors at the site level; however, biotic factors were most influential at the individual level. At the site level, the probability of ranavirus presence correlated negatively with distance to nearest ranavirus‐positive pond, suggesting that the movement of water or mobile taxa (e.g., adult amphibians, birds, reptiles) may facilitate the movement of ranavirus between ponds and across the landscape. Taxonomic richness associated positively with ranavirus presence at the site level, but vertebrate richness associated negatively with infection prevalence in the host population. This might reflect the contrasting influences of diversity on pathogen colonisation versus transmission among hosts. Amphibian host species differed in their likelihood of ranavirus infection: American bullfrogs (Rana catesbeiana) had the weakest association with infection while rough‐skinned newts (Taricha granulosa) had the strongest. After accounting for host species effects, hosts with greater snout–vent length had a lower probability of infection. Our study demonstrates the array of landscape, environmental, and individual‐level factors associated with ranavirus epidemiology. Moreover, our study helps illustrate that the importance of these factors varies with biological level. [ABSTRACT FROM AUTHOR]

Identifying the effects of human‐driven perturbations, such as species introductions or habitat fragmentation, on the ecology and dynamics of infectious disease has become a central focus of disease ecologists. Yet, comparatively little is known about how the ecology of zoonotic disease systems responds to catastrophic disturbance events such as wildfires or hurricanes. In California, wildfire disturbance is centrally important to the ecology of forests and oak woodlands and is projected to increase in severity and extent under future climate change. Here, taking advantage of a recent wildfire as a natural experiment, we investigate the effects of wildfire disturbance on the ecology of tick‐borne disease in California oak woodlands. We find that wildfire leads to elevated abundance of questing adult and nymphal western blacklegged ticks (Ixodes pacificus) in the year following fire, relative to unburned control plots, but that vector tick abundance declines sharply in the following two years. We find that the abundance of non‐competent hosts (western fence lizards) for the Lyme disease bacterium is unaffected by fire, but that the abundances of important reproductive hosts (deer) for ticks and reservoir hosts (dusky‐footed woodrats) for tick‐borne pathogens are significantly negatively affected by fire. We found ticks and hosts infected with Borrelia burgdorferi sensu lato only within the burn extent and only in the year following the wildfire, though rates of infection were exceedingly low representing little risk to humans. In aggregate, due to the differential effects of this catastrophic disturbance event on different key host species and vector tick life stages in the transmission of tick‐borne pathogens, we conclude that wildfire may potentially increase risk of exposure to vector ticks in the first year following wildfire in California, but that risk is dampened substantially in following years due to tick population declines and loss of key reservoir hosts from the system. [ABSTRACT FROM AUTHOR]

Abstract: Associations among parasites affect many aspects of host–parasite dynamics, but a lack of analytical tools has limited investigations of parasite correlations in observational data that are often nested across spatial and biological scales. Here we illustrate how hierarchical, multiresponse modelling can characterize parasite associations by allowing for hierarchical structuring, offering estimates of uncertainty and incorporating correlational model structures. After introducing the general approach, we apply this framework to investigate coinfections among four amphibian parasites (the trematodes Ribeiroia ondatrae and Echinostoma spp., the chytrid fungus Batrachochytrium dendrobatidis and ranaviruses) and among >2,000 individual hosts, 90 study sites and five amphibian host species. Ninety‐two percent of sites and 80% of hosts supported two or more pathogen species. Our results revealed strong correlations between parasite pairs that varied by scale (from among hosts to among sites) and classification (microparasite versus macroparasite), but were broadly consistent across taxonomically diverse host species. At the host‐scale, infection by the trematode R. ondatrae correlated positively with the microparasites, B. dendrobatidis and ranavirus, which were themselves positively associated. However, infection by a second trematode (Echinostoma spp.) correlated negatively with B. dendrobatidis and ranavirus, both at the host‐ and site‐level scales, highlighting the importance of differential relationships between micro‐ and macroparasites. Given the extensive number of coinfecting symbiont combinations inherent to natural systems, particularly across multiple host species, multiresponse modelling of cross‐sectional field data offers a valuable tool to identify a tractable number of hypothesized interactions for experimental testing while accounting for uncertainty and potential sources of co‐exposure. For amphibians specifically, the high frequency of co‐occurrence and coinfection among these pathogens—each of which is known to impair host fitness or survival—highlights the urgency of understanding parasite associations for conservation and disease management. [ABSTRACT FROM AUTHOR]

As extinctions continue across the globe, conservation biologists are turning to species reintroduction programs as one optimistic tool for addressing the biodiversity crisis. For repatriation to become a viable strategy, fundamental prerequisites include determining the causes of declines and assessing whether the causes persist in the environment. Invasive species-especially pathogens-are an increasingly significant factor contributing to biodiversity loss. We hypothesized that Batrachochytrium dendrobatidis (Bd), the causative agent of the deadly amphibian disease chytridiomycosis, was important in the rapid (<10 years) localized extirpation of a North American frog ( Rana boylii) and that Bd remains widespread among extant amphibians in the region of extirpation. We used an interdisciplinary approach, combining interviews with herpetological experts, analysis of archived field notes and museum specimen collections, and field sampling of the extant amphibian assemblage to examine (1) historical relative abundance of R. boylii; (2) potential causes of R. boylii declines; and (3) historical and contemporary prevalence of Bd. We found that R. boylii were relatively abundant prior to their rapid extirpation, and an increase in Bd prevalence coincided with R. boylii declines during a time of rapid change in the region, wherein backcountry recreation, urban development, and the amphibian pet trade were all on the rise. In addition, extreme flooding during the winter of 1969 coincided with localized extirpations in R. boylii populations observed by interview respondents. We conclude that Bd likely played an important role in the rapid extirpation of R. boylii from southern California and that multiple natural and anthropogenic factors may have worked in concert to make this possible in a relatively short period of time. This study emphasizes the importance of recognizing historical ecological contexts in making future management and reintroduction decisions. [ABSTRACT FROM AUTHOR]

While disease-induced extinction is generally considered rare, a number of recently emerging infectious diseases with load-dependent pathology have led to extinction in wildlife populations. Transmission is a critical factor affecting disease-induced extinction, but the relative importance of transmission compared to load-dependent host resistance and tolerance is currently unknown. Using a combination of models and experiments on an amphibian species suffering extirpations from the fungal pathogen Batrachochytrium dendrobatidis (Bd), we show that while transmission from an environmental Bd reservoir increased the ability of Bd to invade an amphibian population and the extinction risk of that population, Bd-induced extinction dynamics were far more sensitive to host resistance and tolerance than to Bd transmission. We demonstrate that this is a general result for load-dependent pathogens, where non-linear resistance and tolerance functions can interact such that small changes in these functions lead to drastic changes in extinction dynamics. [ABSTRACT FROM AUTHOR]

Despite calls for improved responses to emerging infectious diseases in wildlife, management is seldom considered until a disease has been detected in affected populations. Reactive approaches may limit the potential for control and increase total response costs. An alternative, proactive management framework can identify immediate actions that reduce future impacts even before a disease is detected, and plan subsequent actions that are conditional on disease emergence. We identify four main obstacles to developing proactive management strategies for the newly discovered salamander pathogen Batrachochytrium salamandrivorans ( Bsal). Given that uncertainty is a hallmark of wildlife disease management and that associated decisions are often complicated by multiple competing objectives, we advocate using decision analysis to create and evaluate trade-offs between proactive (pre-emergence) and reactive (post-emergence) management options. Policy makers and natural resource agency personnel can apply principles from decision analysis to improve strategies for countering emerging infectious diseases. [ABSTRACT FROM AUTHOR]

Freshwater biodiversity is imperiled across the globe, and multiple stressors such as habitat alteration, non-native species invasion, disease, and climate change can act in concert to threaten vulnerable taxa. The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd), which causes the disease chytridiomycosis, is one of the causative factors of severe amphibian declines. The foothill yellow-legged frog (Rana boylii) is a stream-breeding anuran endemic to California and Oregon (USA) that has declined precipitously in recent decades, yet there is little information on its susceptibility to Bd. In the fall of 2013, we observed dead and dying juvenile R. boylii in a San Francisco Bay Area watershed where annual amphibian breeding censuses have been conducted since 1997 in a free-flowing reach and since 2003 in an anthropogenically modified stream reach. High pathogen loads on R. boylii and histologic lesions observed on a dead R. boylii metamorph collected from the site were consistent with lethal chytridiomycosis. The outbreak coincided with extremely low stream flows in autumn that concentrated frogs in drying pools and the absence of high peak flows in winter that allowed non-native American bullfrogs (Rana catesbeiana) to expand their spatial distribution in the stream network. Following the outbreak, we surveyed R. boylii and sympatric anurans at the site for the next two years to determine Bd trends within the population. Using mixed-effects models, we found that bullfrog presence was a positive predictor of both Bd prevalence and Bd load in R. boylii. Prevalence was also influenced by sex and life stage: Adult males were more likely to be infected than either females or juveniles. Moreover, we found that stream flow volume was negatively associated with Bd load. These results indicate that disease, drought, and flow regulation may interact synergistically to impact amphibians in ways not previously recognized, informing stream flow management strategies for native aquatic taxa. [ABSTRACT FROM AUTHOR]

Few hosts have many parasites while many hosts have few parasites. This axiom of macroparasite aggregation is so pervasive it is considered a general law in disease ecology, with important implications for the dynamics of host-parasite systems. Because of these dynamical implications, a significant amount of work has explored both the various mechanisms leading to parasite aggregation patterns and how to infer mechanism from these patterns. However, as many disease mechanisms can produce similar aggregation patterns, it is not clear whether aggregation itself provides any additional information about mechanism. Here we apply a 'constraint-based' approach developed in macroecology that allows us to explore whether parasite aggregation contains any additional information beyond what is provided by mean parasite load. We tested two constraint-based null models, both of which were constrained on the total number of parasites P and hosts H found in a sample, using data from 842 observed amphibian host-trematode parasite distributions. We found that constraint-based models captured ~85% of the observed variation in host-parasite distributions, suggesting that the constraints P and H contain much of the information about the shape of the host-parasite distribution. However, we also found that extending the constraint-based null models can identify the potential role of known aggregating mechanisms (such as host heterogeneity) and disaggregating mechanisms (such as parasite-induced host mortality) in constraining host-parasite distributions. Thus, by providing robust null models, constraint-based approaches can help guide investigations aimed at detecting biological processes that directly affect parasite aggregation above and beyond those that indirectly affect aggregation through P and H. [ABSTRACT FROM AUTHOR]

Host-parasite models are typically constructed under either a microparasite or macroparasite paradigm. However, this has long been recognized as a false dichotomy because many infectious disease agents, including most fungal pathogens, have attributes of both microparasites and macroparasites., We illustrate how Integral Projection Models (IPMs) provide a novel modelling framework to represent both types of pathogens. We build a simple host-parasite IPM that tracks both the number of susceptible and infected hosts and the distribution of parasite burdens in infected hosts., The vital rate functions necessary to build IPMs for disease dynamics share many commonalities with classic micro and macroparasite models and we discuss how these functions can be parameterized to build a host-parasite IPM. We illustrate the utility of this IPM approach by modelling the temperature-dependent epizootic dynamics of amphibian chytrid fungus in Mountain yellow-legged frogs ( Rana muscosa)., The host-parasite IPM can be applied to other diseases such as facial tumour disease in Tasmanian devils and white-nose syndrome in bats. Moreover, the host-parasite IPM can be easily extended to capture more complex disease dynamics and provides an exciting new frontier in modelling wildlife disease. [ABSTRACT FROM AUTHOR]

Species extinctions have the potential to dramatically reshape ecological communities. In the Sierra Nevada mountains of California, the emergence of a lethal amphibian pathogen ( Batrachochytrium dendrobatidis) drives mountain yellow-legged frog ( Rana muscosa and Rana sierrae) populations to local extinction. Prior to population declines, these frogs and their tadpoles were abundant, high-level predators and grazers with high trophic connectance. To quantify how these low diversity aquatic macroinvertebrate communities respond to nonrandom single-species local extinctions, we quantified aquatic macroinvertebrate communities using two approaches: a natural experiment ('Resurveys') and a large-scale synoptic observational study ('Snapshot' surveys). In the Resurveys, we compared benthic macroinvertebrate communities in 22 Sierra Nevada alpine lakes that we categorized as either having extant frog populations, experiencing ongoing disease-driven frog declines, or having previously experienced local disease-driven frog extirpation. In the Resurveys, taxonomic richness was about one taxa (17%) higher in lakes where frogs were declining or extinct, compared to lakes where frogs were extant. However, multivariate analyses revealed no strong dissimilarities among Resurvey communities, and there were no differences in the abundances of individual taxa between lakes in the frogs extant, declining, or extinct categories. In the Snapshot surveys, we reanalyzed previously collected data from a large-scale survey of 157 lakes with and without frogs. In the Snapshot survey, invertebrate taxonomic richness was less than one taxa (9%) lower in lakes without frogs, and multivariate analyses again indicated only small differences between lakes with and without frogs. Overall, disease-driven mountain yellow-legged frog extinctions had small effects on lake benthic macroinvertebrate communities, with no large changes in invertebrate abundance, richness or evenness, no clear secondary extinctions or invasions, and few taxa showing distinct responses to frog extinctions. Our study highlights how even for conspicuous, highly connected, omnivorous taxa that are experiencing large, rapid, and widespread declines and extinctions, the ecological effects of extinctions will sometimes be small and subtle. [ABSTRACT FROM AUTHOR]

Emerging infectious diseases pose an important threat to wildlife. While established protocols exist for combating outbreaks of human and agricultural pathogens, appropriate management actions before, during, and after the invasion of wildlife pathogens have not been developed. We describe stage-specific goals and management actions that minimize disease impacts on wildlife, and the research required to implement them. Before pathogen arrival, reducing the probability of introduction through quarantine and trade restrictions is key because prevention is more cost effective than subsequent responses. On the invasion front, the main goals are limiting pathogen spread and preventing establishment. In locations experiencing an epidemic, management should focus on reducing transmission and disease, and promoting the development of resistance or tolerance. Finally, if pathogen and host populations reach a stable stage, then recovery of host populations in the face of new threats is paramount. Successful management of wildlife disease requires risk-taking, rapid implementation, and an adaptive approach. [ABSTRACT FROM AUTHOR]

Abstract: Virulence of infectious pathogens can be unstable and evolve rapidly depending on the evolutionary dynamics of the organism. Experimental evolution can be used to characterize pathogen evolution, often with the underlying objective of understanding evolution of virulence. We used experimental evolution techniques (serial transfer experiments) to investigate differential growth and virulence of Batrachochytrium dendrobatidis (Bd), a fungal pathogen that causes amphibian chytridiomycosis. We tested two lineages of Bd that were derived from a single cryo‐archived isolate; one lineage (P10) was passaged 10 times, whereas the second lineage (P50) was passaged 50 times. We quantified time to zoospore release, maximum zoospore densities, and timing of zoospore activity and then modeled population growth rates. We also conducted exposure experiments with a susceptible amphibian species, the common green tree frog (Litoria caerulea) to test the differential pathogenicity. We found that the P50 lineage had shorter time to zoospore production (Tmin), faster rate of sporangia death (ds), and an overall greater intrinsic population growth rate (λ). These patterns of population growth in vitro corresponded with higher prevalence and intensities of infection in exposed Litoria caerulea, although the differences were not significant. Our results corroborate studies that suggest that Bd may be able to evolve relatively rapidly. Our findings also challenge the general assumption that pathogens will always attenuate in culture because shifts in Bd virulence may depend on laboratory culturing practices. These findings have practical implications for the laboratory maintenance of Bd isolates and underscore the importance of understanding the evolution of virulence in amphibian chytridiomycosis. [ABSTRACT FROM AUTHOR]

Conventional disease theory suggests that extinction with density-dependent transmission is unlikely as the threshold host density (KT) is greater than zero. Extinction may result if transmission is frequency dependent or the pathogen has an environmental reservoir. Given the importance of understanding how pathogens affect species richness and diversity there are few empirical tests of these conclusions. We used an Ambystoma tigrinum– Ambystoma tigrinum virus (ATV) model system in the laboratory to examine disease transmission dynamics. Susceptible A. tigrinum larvae were exposed to three different densities and proportions of infected larvae for 24 h. We then housed susceptible hosts individually for 28 days and monitored them for infection. The density of infected hosts to which susceptible hosts were exposed was the best predictor of infection (p=0.037). There was no effect of host clutch on the probability of becoming infected (p=0.67). Larvae in the highest density treatments died sooner than larvae in lower density treatments (p<0.001). Asymptomatic but infected hosts shed sufficient virus into the water in a 24-h period to infect susceptible hosts without any direct contact between individuals. ATV transmission was best described by a power function, leading to the prediction that extinction of A. tigrinum as a result of this pathogen is unlikely. Indeed, field observations show that larval salamander populations that experience ATV-driven epidemics may decrease, but not to extinction, and then recover. Disease is proposed as a possible explanation for the global decline of amphibians. Ranaviruses infect many amphibian populations, but based on our results may not be a general cause of declines to extinction. In contrast, frequency dependent transmission, environmental reservoirs and alternative hosts may be the most likely explanation for the enigmatic decline, at times to extinction, of some amphibian populations as a result of emerging infectious diseases, like the chytrid fungus Batrachochytrium dendrobatidis. [ABSTRACT FROM AUTHOR]

Life-history trade-offs allow many animals to maintain reproductive fitness across a range of climatic conditions. When used by parasites and pathogens, these strategies may influence patterns of disease in changing climates. The chytrid fungus, Batrachochytrium dendrobatidis, is linked to global declines of amphibian populations. Short-term growth in culture is maximal at 17°-25°C. This has been used in an argument that global warming, which increases the time that amphibians spend at these temperatures in cloud-covered montane environments, has led to extinctions. Here we show that the amphibian chytrid responds to decreasing temperatures with trade-offs that increase fecundity as maturation rate slows and increase infectivity as growth decreases. At I 7°-25°C, infectious zoospores encyst (settle and develop a cell wall) and develop into the zoospore-producing stage (zoosporangium) faster, while at 7°-10°C, greater numbers of zoospores are produced per zoosporangium; these remain infectious for a longer period of time. We modeled the population growth of B. dendrobatidis through time at various temperatures using delayed differential equations and observational data for four parameters: developmental rate of thalli, fecundity, rate of zoospore encystment, and rate of zoospore survival. From the models, it is clear that life- history trade-offs allow B. dendrobatidis to maintain a relatively high long-term growth rate at low temperatures, so that it maintains high fitness across a range of temperatures. When a seven-day cold shock is simulated, the outcome is intermediate between the two constant temperature regimes, and in culture, a sudden drop in temperature induces zoospore release. These trade-offs can be ecologically important for a variety of organisms with complex life histories, including pathogenic microorganisms. The effect of temperature on amphibian mortality will depend on the interaction between fungal growth and host immune function and will be modified by host ecology, behavior, and life history. These results demonstrate that B. dendrobatidis populations can grow at high rates across a broad range of environmental temperatures and help to explain why it is so successful in cold montane environments. [ABSTRACT FROM AUTHOR]

Although the canonical concept of intraguild predation evokes images of predators and prey, several subdisciplines within ecology have developed theory not specifically framed in terms of predation and competition and often using system-specific terminology, yet functionally quite similar. Here, we formulate models combining exploitation and competition in predator-prey, host-parasitoid, and host-pathogen communities to compare dynamics, food web structure, and coexistence criteria for these disparate communities. Although dynamic stability in the coexistence region varies strongly among systems, in all cases coexistence of two consumers on a single resource occurs only if the intraguild prey species is more efficient than the intraguild predator at suppressing the abundance of the basal resource, and if the intraguild predator accrues a sufficient gain from attacking the intraguild prey. In addition, equilibrial abundances of all species in all three formulations respond similarly to increases in productivity of the basal resource. Our understanding of predator-prey and parasitoid-host communities has benefited from explicit examination of intraguild predation (IGP) theory, and we suggest that future research examining pathogen communities, in particular, will benefit substantially from explicit recognition of predictions from IGP theory. [ABSTRACT FROM AUTHOR]

1. Chytridiomycosis is an emerging infectious disease of amphibians, caused by the fungal pathogen Batrachochytrium dendrobatidis, which has been implicated recently in population declines and possible extinctions throughout the world. 2. The transmission rate of this pathogen was quantified in the mountain yellow-legged frog Rana muscosa through laboratory and field experiments, and a maximum likelihood approach was used to determine the form of the transmission function that was best supported by the experimental data. 3. The proportion of R. muscosa tadpole hosts that became infected increased with the number of previously infected R. muscosa tadpoles to which they were exposed, as would be expected in an infectious disease. 4. The laboratory experiment revealed some support for a transmission function in which the transmission rate levels off as the density of infected individuals increases. However, there was not enough power to distinguish between a frequency-dependent form and several other asymptotic forms of the transmission function. 5. The impacts of crowding and temperature on transmission were also investigated; however, neither of these factors significantly affected the transmission rate. [ABSTRACT FROM AUTHOR]

Intraguild predation (IGP) is a dominant community module in terrestrial food webs that occurs when multiple consumers feed both on each other and on a shared prey. This specific form of omnivory is common in terrestrial communities and is of particular interest for conservation biology and biological control given its potential to disrupt management of threatened or pest species. Extensive theory exists to describe the dynamics of three-species IGP, but these models have largely overlooked the potential for other, exterior interactions, to alter the dynamics within the IGP module. We investigated how three forms of feeding outside of the IGP module by intraguild predators (i.e. trophic supplementation) affect the dynamics of the predators (both IG predator and IG prey) and their shared resource. Specifically, we examined how the provision of a constant donor-controlled resource, the availability of an alternative prey species, and predator plant-feeding affect the dynamics of IGP models. All three forms of trophic supplements modified the basic expectations of IGP theory in two important ways, and their effects were similar. First, coexistence was possible without the IG prey being a superior competitor for the original shared resource if the IG prey could effectively exploit one of the types of trophic supplements. However, supplements to the IG predator restricted the potential for coexistence. Second, supplements to the IG prey ameliorated the disruptive effects of the IG predator on the suppression of the shared resource, promoting effective control of the resource in the presence of both predators. Consideration of these three forms of trophic supplementation, all well documented in natural communities, adds substantial realism and predictive power to intraguild predation theory. [ABSTRACT FROM AUTHOR]

1. Host–parasitoid models often identify foraging behaviour and dispersal distance as important for system persistence. 2. Laboratory observations and field trials were used to characterise foraging behaviour and dispersal capability of Platygaster californica Ashmead (Platygasteridae), a parasitoid of the gall midge Rhopalomyia californica Felt (Cecidomyiidae). 3. Although foraging parasitoids meticulously searched plants in laboratory observations, none of the laboratory trials resulted in 100% parasitism, and the proportion of parasitism declined as midge egg density increased. 4. The field trials showed that the distribution of parasitism over distance from a central release point was hump-shaped, as predicted by a simple diffusion model. Mean parasitoid dispersal distance was 4.5 m, considerably farther than the 1.7 m mean midge dispersal found in previous work. 5. Although the parasitoid appears to search thoroughly for midge eggs and to disperse farther than the midge, the results of this study show how this host–parasitoid system may persist due to spatially variable incomplete parasitism. [ABSTRACT FROM AUTHOR]

A newly discovered infectious disease of amphibians, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis, is implicated in population declines and possible extinctions throughout the world. The purpose of our study was to examine the effects of B. dendrobatidis on the mountain yellow-legged frog (Rana muscosa) in the Sierra Nevada of California (USA). We (1) quantified the prevalence and incidence of B. dendrobatidis through repeat surveys of several hundred R. muscosa populations in the southern Sierra Nevada: (2) described the population level effects of B. dendrobatidis on R. muscosa population abundance; and (3) compared the mortality rates of infected and uninfected R. muscosa individuals from pre-through post-metamorphosis using both laboratory and field experiments. Mouthpart inspections conducted in 144 and 132 R, muscosa populations in 2003 and 2004, respectively, indicated that 19% of R. muscosa populations in both years showed indications of chytridiomycosis. Sixteen percent of populations that were uninfected in 2003 became infected by 2004. Rana muscosa population sizes were reduced by an average of 88% following B, dendrobatidis outbreaks at six sites, but at seven B. dendrobatidis-negative sites, R, muscosa population sizes increased by an average of 45% over the same time period. In the laboratory, all infected R. muscosa developed fatal chytridiomycosis after metamorphosis, while all uninfected individuals remained healthy. In the field experiment in which R. muscosa tadpoles were caged at infected and uninfected sites, 96% of the individuals that metamorphosed at infected sites died vs. 5% at the uninfected sites. These studies indicate that chytridiomycosis causes high mortality in post-metamorphic R. muscosa, that this emerging disease is the proximate cause of numerous observed R. muscosa population declines, and that the disease threatens this species with extirpation at numerous sites in California's Sierra Nevada. [ABSTRACT FROM AUTHOR]

Copyright of Conservation Biology is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.)

The article uses simple models to examine the management relevance of the disconnection between theory and experiments in communities with intraguild predation (IGP). Applied ecology has increasingly used mechanistic models of population dynamics to guide management decisions. This trend has led to many advances in both management and theory. Equilibrium theory shows that IGP can promote coexistence of competitors on a shared resource. However, adding the IGP can result in higher resource densities than in a system with the intraguild prey alone with its resource. This has important management implications when the shared resource is a pest species whose population is controlled by natural enemies. Models discussed in the article demonstrate why short-term experiments and studies ignoring alternate resources may bear no relationship to a system at equilibrium. Short-term experiments quantifying only attack rates can predict a broad range of outcomes. By ignoring conversion efficiency, consumer longevity, and immigration, short-term studies may cause erroneous decisions about the introduction of natural enemies in biological control.

The forest insect pest Bupalus piniarius (pine looper moth) is a classic example of a natural population cycle. As is typical for populations that exhibit regular oscillations in density, there are several biological mechanisms that are hypothesized to be responsible for the cycles; but despite several decades of detailed study there has been no definite conclusion as to which mechanism is most important. We evaluated three hypotheses for which there was direct experimental evidence: (1) food quality (nutritional value of pine needles affected by defoliation); (2) parasitoids (trophic interactions with specialist parasitoids); and (3) maternal effects (maternal body size affects the performance of offspring). We reviewed the empirical evidence for each of these hypotheses and expressed each hypothesis in the form of a mechanistic dynamic model. We used a nonlinear forecasting approach to fit each model to three long-term population time series in Britain that exhibit some degree of regular cycling, and we used parametric bootstrap to evaluate the significance of differences between models in their goodness of fit to the data. The results differed among the three forests: at Culbin, the parasitoid and maternal effects models fit equally well; at Roseisle, the food quality and maternal effects models fit equally well; and at Tentsmuir, the parasitoid model fit best. However, the best-fit parasitism models required that the parasitism rate vary between nearly 0 and nearly 1 during a cycle, greatly exceeding the range of parasitism rates that have been observed in the field. In contrast, the required variation in the observable maternal quality variable (pupal mass) was within the range of empirical observations. Under mild constraints on the parasitism rate (though allowing a much wider range than has been measured in B. piniarius at any location), the fit of the parasitism model fell off dramatically. The maternal effects model then had uniformly strong support, outperforming the constrained parasitism model at all three sites and the food quality model at two; it performed slightly better than the food quality model at the remaining site. This represents the first system in which the maternal effects hypothesis for population cycles has been supported by both strong biological and dynamical evidence. [ABSTRACT FROM AUTHOR]

Abstract Although ecological theory exists to predict dynamics in communities with intraguild predation (IGP), few empirical tests have examined this theory. IGP theory, in particular, predicts that when two competitors interact via IGP, with increasing resource productivity: (1) the IG predator will increase in abundance as the IG prey declines, and (2) increasing dominance of the IG predator will cause resource density to increase. Here, we provide a first test of these predictions in a field community consisting of a scale insect and its two specialist parasitoids, Aphytis melinus (the IG predator) and Encarsia perniciosi (the IG prey). The shared resource, California red scale, is a pest of citrus, and its productivity varies across a threefold range among citrus cultivars. We examined both absolute and relative densities of parasitoids along this natural gradient of scale productivity in three citrus cultivars (orange, grapefruit and lemon). Although both parasitoid species were found in all three cultivars, their abundances reflected those predicted by IGP theory: the IG prey species dominated at low productivity and the IG predator dominated at high productivity. This relationship was caused by an increase in Aphytis density with productivity. In addition, the density of scale increased with the dominance of the IG predator. These results from a field system demonstrate the important dynamic outcomes for food webs with IGP. [ABSTRACT FROM AUTHOR]

Population cycles have been remarkably resistant to explanation, in part because crucial experiments are rarely possible on appropriate spatial and temporal scales. Here we show how new approaches to nonlinear time-series analysis can distinguish between competing hypotheses for population cycles of larch budmoth in the Swiss Alps: delayed effects of budmoth density on food quality, and budmoth-parasitoid interactions. We reexamined data on budmoth density, plant quality, and parasitism rates. Our results suggest that the effect of plant quality on budmoth density is weak. By contrast, a simple model of budmoth-parasitoid interaction accounts for 90% of the variance in budmoth population growth rates. Thus, contrary to previous studies, we find that parasitoid-budmoth interaction appears to be the dominant factor driving the budmoth cycle. [ABSTRACT FROM AUTHOR]

Summary1. The gall-forming midge Rhopalomyia californica was exposed experimentally to parasitism and predation during only the egg stage, during only the larval stage, during neither stage, or during both stages. 2. The combined action of natural enemies that attack during both the egg stage and the larval stage led to the lowest number of midges and total insects (midges + parasitoids) in the next generation, and the highest percentage parasitism. 3. The larval parasitoid killed a large fraction of hosts without producing new parasitoid offspring, while there is some indication that the egg parasitoid on its own tended to produce the most parasitoid offspring. The contrasting implications of host mortality versus parasitoid production for biological control are discussed. 4. Exposure to larval parasitoids resulted in a reduction in the number of egg parasitoid offspring produced, but exposure to the egg parasitoid did not affect the number of larval parasitoid offspring produced significantly. [ABSTRACT FROM AUTHOR]

1. Theoretical studies predict that limited amounts of dispersal of individuals in host-parasitoid systems can both enhance the stability of the subpopulations and promote the co-existence of competing parasitoid species. We investigated the effects of dispersal on the population dynamics and parasitoid community structure of a natural host-multi-parasitoid system consisting of the midge Rhopalomyia californica that forms galls on the shrub Baccharis pilularis and the parasitoids that attack the midge. 2. An experiment involving the release of midges into a field with a low background density of galls demonstrated that the midges, on average, travelled approximately 1·7m in their lifetime. This suggests that the appropriate spatial scale at which to look at the effects of dispersal is relatively small. 3. Dispersal of midges and parasitoids between individual bushes was experimentally eliminated in a caging experiment. The midge populations in all of the uncaged replicates displayed dynamics that were similar to each other, while the dynamics of the midge populations in the caged replicates diverged. The midge dynamics on the uncaged bushes were not significantly more stable than those on the caged bushes. 4. Dispersal among bushes was found to play a major role in co-existence of the competing parasitoid species. There was a dramatic drop in the parasitoid species diversity on the caged bushes, with only a single parasitoid species, Platygaster californica, persisting at high numbers in the caged populations. In accordance with theoretical models, P. californica is the parasitoid species in the community that has the highest attack rate and is most effective at searching for hosts in a restricted area. Alternative explanations for this pattern are discussed. [ABSTRACT FROM AUTHOR]

Focuses on application of statistical and mechanistic modeling to the problem of population cycles. Quantification of hypotheses through mathematical models; Comparison of simulated time-series generated with the observed time series.

Focuses on developments in the ecological theory for biological control. Biological control of insect pests; Competition between natural enemies; Parasitoid aggregation and stability; Effects on biocontrol on parasitoid behavior.

Novel outbreaks of emerging pathogens require rapid responses to enable successful mitigation. We simulated a 1‐day emergency meeting where experts were engaged to recommend mitigation strategies for a new outbreak of the amphibian fungal pathogen Batrachochytrium salamandrivorans. Despite the inevitable uncertainty, experts suggested and discussed several possible strategies. However, their recommendations were undermined by imperfect initial definitions of the objectives and scope of management. This problem is likely to arise in most real‐world emergency situations. The exercise thus highlighted the importance of clearly defining the context, objectives, and spatial–temporal scale of mitigation decisions. Managers are commonly under pressure to act immediately. However, an iterative process in which experts and managers cooperate to clarify objectives and uncertainties, while collecting more information and devising mitigation strategies, may be slightly more time consuming but ultimately lead to better outcomes. [ABSTRACT FROM AUTHOR]