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msocc: Fit and analyse computationally efficient multi‐scale occupancy models in R

Environmental DNA (eDNA) sampling is a promising tool for the detection of rare and cryptic taxa, such as aquatic pathogens, parasites and invasive species. Environmental DNA sampling workflows commonly rely on multi‐stage hierarchical sampling designs that induce complicated dependencies within the data. This complex dependence structure can be intuitively modelled with Bayesian multi‐scale occupancy models. However, current software for such models are computationally demanding, impeding their use. We present an r package, msocc , that implements a data augmentation strategy to fit fully Bayesian, computationally efficient multi‐scale occupancy models. The msocc package allows users to fit multi‐scale occupancy models, to estimate and visualize posterior summaries of site, sample and replicate‐level occupancy, and to compare different models using Bayesian information criterion. Additionally, we provide a supplemental web application that allows users to investigate study design for multi‐scale occupancy models and acts as a graphical user interface to the msocc package. The utility of the msocc package is illustrated on a published dataset and the functions in msocc are compared to the primary Bayesian toolkit for multi‐scale occupancy modelling, eDNAoccupancy , using various computational benchmarks. These benchmarks indicate that msocc is capable of fitting models 50 times faster than eDNAoccupancy . We hope that access to software that efficiently fits, analyses and conducts study design investigations for multi‐scale occupancy models facilitates their implementation by the research and wildlife management communities.

Methods in Ecology and Evolution↗

Disease dynamics during wildlife translocations: disruptions to the host population and potential consequences for transmission in desert tortoise contact networks

Wildlife managers consider animal translocation a means of increasing the viability of a local population. However, augmentation may disrupt existing resident disease dynamics and initiate an outbreak that would effectively offset any advantages the translocation may have achieved. This paper examines fundamental concepts of disease ecology and identifies the conditions that will increase the likelihood of a disease outbreak following translocation. We highlight the importance of susceptibility to infection, population size and population connectivity – a characteristic likely affected by translocation but not often considered in risk assessments – in estimating outbreak risk due to translocation. We then explore these features in a species of conservation concern often translocated in the presence of infectious disease, the Mojave Desert tortoise, and use data from experimental tortoise translocations to detect changes in population connectivity that may influence pathogen transmission. Preliminary analyses comparing contact networks inferred from spatial data at control and translocation plots and infection simulation results through these networks suggest increased outbreak risk following translocation due to dispersal-driven changes in contact frequency and network structure. We outline future research goals to test these concepts and aid managers in designing effective risk assessment and intervention strategies that will improve translocation success.

Animal Conservation↗

Optimal management decisions are robust to unknown dynamics in an amphibian metapopulation plagued by disease

Identifying conservation actions to recover threatened species can be challenging due to many ecological uncertainties. For example, major threats to a species' conservation are commonly known or suspected, but the specific impacts on population or metapopulation dynamics can be uncertain. This is frequently the case with emerging infectious diseases, including chytridiomycosis, a global driver of amphibian population declines caused by the fungal pathogens Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans . While these diseases are known to cause amphibian declines and extirpations, the mechanisms of their landscape-scale spread are still largely unknown. Such uncertainty can lead to inaction which may jeopardize timely recovery of a species. Decision analysis is a pragmatic approach to making transparent and defensible decisions while dealing with uncertainties. We investigated whether optimal actions aimed at recovering boreal toad ( Anaxyrus boreas boreas ) metapopulations in the southern Rocky Mountains are robust to the unknown dynamics of Bd spread using value of information and regret analyses. Value of information is a decision-analytic tool for calculating the value of new information in terms of performance on management objectives, while regret measures the cost of acting under incorrect information. We further conducted a stochastic sensitivity analysis to identify the relative effects of metapopulation parameters on system dynamics. We found optimal actions were robust to the unknown dynamics of Bd spread. While boreal toad breeding occurrence is highly sensitive to Bd distribution, the optimal decision is not. Resolving the unknown dynamics of Bd spread would lead to a minimal gain of less than one breeding toad subpopulation at the end of 50 years, given the currently available management actions. Applying a decision-analytic framework coupled with value of information and regret analyses can help frame how uncertainties affect decisions in a way that empowers decision makers.

Animal Conservation↗

Plague bacterium as a transformer species in prairie dogs and the grasslands of western North America

Invasive transformer species change the character, condition, form, or nature of ecosystems and deserve considerable attention from conservation scientists. We applied the transformer species concept to the plague bacterium Yersinia pestis in western North America, where the pathogen was introduced around 1900. Y. pestis transforms grassland ecosystems by severely depleting the abundance of prairie dogs ( Cynomys spp. ) and thereby causing declines in native species abundance and diversity, including threatened and endangered species; altering food web connections; altering the import and export of nutrients; causing a loss of ecosystem resilience to encroaching invasive plants; and modifying prairie dog burrows. Y. pestis poses an important challenge to conservation biologists because it causes trophic-level perturbations that affect the stability of ecosystems. Unfortunately, understanding of the effects of Y. pestis on ecosystems is rudimentary, highlighting an acute need for continued research.

Conservation Biology↗

Transmission of influenza reflects seasonality of wild birds across the annual cycle

Influenza A Viruses (IAV) in nature must overcome shifting transmission barriers caused by the mobility of their primary host, migratory wild birds, that change throughout the annual cycle. Using a phylogenetic network of viral sequences from North American wild birds (2008–2011) we demonstrate a shift from intraspecific to interspecific transmission that along with reassortment, allows IAV to achieve viral flow across successive seasons from summer to winter. Our study supports amplification of IAV during summer breeding seeded by overwintering virus persisting locally and virus introduced from a wide range of latitudes. As birds migrate from breeding sites to lower latitudes, they become involved in transmission networks with greater connectivity to other bird species, with interspecies transmission of reassortant viruses peaking during the winter. We propose that switching transmission dynamics may be a critical strategy for pathogens that infect mobile hosts inhabiting regions with strong seasonality.

Ecology Letters↗

Inferring infection hazard in wildlife populations by linking data across individual and population scales

Our ability to infer unobservable disease-dynamic processes such as force of infection (infection hazard for susceptible hosts) has transformed our understanding of disease transmission mechanisms and capacity to predict disease dynamics. Conventional methods for inferring FOI estimate a time-averaged value and are based on population-level processes. Because many pathogens exhibit epidemic cycling and FOI is the result of processes acting across the scales of individuals and populations, a flexible framework that extends to epidemic dynamics and links within-host processes to FOI is needed. Specifically, within-host antibody kinetics in wildlife hosts can be short-lived and produce patterns that are repeatable across individuals, suggesting individual-level antibody concentrations could be used to infer time since infection and hence FOI. Using simulations and case studies (influenza A in lesser snow geese and Yersinia pestis in coyotes), we argue that with careful experimental and surveillance design, the population-level FOI signal can be recovered from individual-level antibody kinetics, despite substantial individual-level variation. In addition to improving inference, the cross-scale quantitative antibody approach we describe can reveal insights into drivers of individual-based variation in disease response, and the role of poorly understood processes such as secondary infections, in population-level dynamics of disease.

Ecology Letters↗

Waterfowl move less in heterogeneous and human-populated landscapes, with implications for spread of avian influenza viruses

Animal movements contribute to the spread of infectious diseases and are driven in part by environmental conditions. We investigated the links among the environment, animal movement, and infectious disease dynamics in waterfowl, which are among the primary wildlife hosts of avian influenza viruses. By combining telemetry data on 4606 individuals from 26 waterfowl species with data on land cover, weather, and vegetation, we found that waterfowl moved less in areas of higher land cover heterogeneity and higher human population density. Moreover, predicted waterfowl movement distances were weakly but positively correlated with distances between detections of H5N1 highly pathogenic avian influenza in wild waterfowl, suggesting that environmental conditions might contribute to the spread of this disease via their effects on bird movements. By considering wildlife movements alongside other drivers of infectious disease dynamics, such as livestock production and human mobility, we move closer to predicting outbreaks and informing interventions.

Ecology Letters↗

Intercontinental genetic structure and gene flow in Dunlin (Calidris alpina), a potential vector of avian influenza

Waterfowl (Anseriformes) and shorebirds (Charadriiformes) are the most common wild vectors of influenza A viruses. Due to their migratory behavior, some may transmit disease over long distances. Migratory connectivity studies can link breeding and nonbreeding grounds while illustrating potential interactions among populations that may spread diseases. We investigated Dunlin ( Calidris alpina ), a shorebird with a subspecies ( C. a. arcticola ) that migrates from nonbreeding areas endemic to avian influenza in eastern Asia to breeding grounds in northern Alaska. Using microsatellites and mitochondrial DNA, we illustrate genetic structure among six subspecies: C. a. arcticola , C. a. pacifica , C. a. hudsonia , C. a. sakhalina , C. a. kistchinski , and C. a. actites . We demonstrate that mitochondrial DNA can help distinguish C. a. arcticola on the Asian nonbreeding grounds with >70% accuracy depending on their relative abundance, indicating that genetics can help determine whether C. a. arcticola occurs where they may be exposed to highly pathogenic avian influenza (HPAI) during outbreaks. Our data reveal asymmetric intercontinental gene flow, with some C. a. arcticola short-stopping migration to breed with C. a. pacifica in western Alaska. Because C. a. pacifica migrates along the Pacific Coast of North America, interactions between these subspecies and other taxa provide route for transmission of HPAI into other parts of North America.

Evolutionary Applications↗

Population genomics of free-ranging Great Plains white-tailed and mule deer reflects a long history of interspecific hybridization

Hybridization is a natural process at species-range boundaries that may variably promote the speciation process or break down species barriers but minimally will influence management outcomes of distinct populations. White-tailed deer ( Odocoileus virginianus ) and mule deer ( Odocoileus hemionus ) have broad and overlapping distributions in North America and a recognized capacity for interspecific hybridization. In response to contemporary environmental change to any of one or multiple still-unknown factors, mule deer range is contracting westward accompanied by a westward expansion of white-tailed deer, leading to increasing interactions, opportunities for gene flow, and associated conservation implications. To quantify genetic diversity, phylogenomic structure, and dynamics of hybridization in sympatric populations of white-tailed and mule deer, we used mitochondrial cytochrome b data coupled with SNP loci discovered with double-digest restriction site-associated DNA sequencing. We recovered 25,018 SNPs across 92 deer samples from both species, collected from two regions of western Kansas. Eight individuals with unambiguous external morphology representing both species were of hybrid origin (8.7%), and represented the product of multi-generational backcrossing. Mitochondrial data showed both ancient and recent directional discordance with morphological species assignments, reflecting a legacy of mule deer males mating with white-tailed deer females. Mule deer had lower genetic diversity than white-tailed deer, and both mitochondrial and nuclear data suggest contemporary mule deer effective population decline. Landscape genetic analyses show relative isolation between the two study regions for white-tailed deer, but greater connectivity among mule deer, with predominant movement from north to south. Collectively, our results suggest a long history of gene flow between these species in the Great Plains and hint at evolutionary processes that purge incompatible functional genomic elements as a result of hybridization. Surviving hybrids evidently may be reproductive, but with unknown consequences for the future integrity of these species, population trajectories, or relative susceptibility to emerging pathogens.

Kansas↗

Will a warmer and wetter future cause extinction of native Hawaiian forest birds?

Isolation of the Hawaiian archipelago produced a highly endemic and unique avifauna. Avian malaria ( Plasmodium relictum ), an introduced mosquito-borne pathogen, is a primary cause of extinctions and declines of these endemic honeycreepers. Our research assesses how global climate change will affect future malaria risk and native bird populations. We used an epidemiological model to evaluate future bird-mosquito-malaria dynamics in response to alternative climate projections from the Coupled Model Intercomparison Project (CMIP). Climate changes during the second half of the century accelerate malaria transmission and cause a dramatic decline in bird abundance. Different temperature and precipitation patterns produce divergent trajectories where native birds persist with low malaria infection under a warmer and dryer projection (RCP4.5), but suffer high malaria infection and severe reductions under hot and dry (RCP8.5) or warm and wet (A1B) futures. We conclude that future global climate change will cause significant decreases in the abundance and diversity of remaining Hawaiian bird communities. Because these effects appear unlikely before mid-century, natural resource managers have time to implement conservation strategies to protect this unique avifauna from further decimation. Similar climatic drivers for avian and human malaria suggest that mitigation strategies for Hawai'i have broad application to human health.

Hawai'i↗

Contributing areas to domestic wells in dipping sedimentary rocks under extreme recharge events

We use particle tracking to determine contributing areas (CAs) to wells for transient flow models that simulate cyclic domestic pumping and extreme recharge events in a small synthetic watershed underlain by dipping sedimentary rocks. The CAs consist of strike-oriented bands at locations where the water table intersects high-hydraulic conductivity beds, and from which groundwater flows to the pumping well. Factors that affect the size and location of the CAs include topographic flow directions, rock dip direction, cross-bed fracture density, and position of the well relative to streams. For an effective fracture porosity (n e ) of 10 -4 , the fastest advective travel times from CAs to wells are only a few hours. These results indicate that wells in this type of geologic setting can be highly vulnerable to contaminants or pathogens flushed into the subsurface during extreme recharge events. Increasing n e to 10 -3 results in modestly smaller CAs and delayed well vulnerability due to slower travel times. CAs determined for steady-state models of the same setting, but with long-term average recharge and pumping rates, are smaller than CAs in the models with extreme recharge. Also, the earliest-arriving particles arrive at the wells later in the steady-state models than in the extreme-recharge models. The results highlight the importance of characterizing geologic structure, simulating plausible effective porosities, and simulating pumping and recharge transience when determining CAs in fractured rock aquifers to assess well vulnerability under extreme precipitation events.

Groundwater↗

Answering key bumble bee conservation questions by studying discovered wild nests: A Bombus affinis case study

The nesting ecology of wild bumble bees is not well resolved, but information learned from discovered nests can be of great conservation value. Data collected at nests on foraging patterns, caste-specific behaviour and health (e.g., pathogens) are invaluable for understanding bumble bee behaviour and ecology, but difficult to decipher solely from foraging observations away from the nest. Post-senescence nest excavation allows the estimation of colony size, caste numbers, documents pest incidence and provides opportunities to examine nest material for stressors (e.g., pesticides) and to use nest material for training purposes (e.g., conservation dogs). Wild nests are often found opportunistically, and there is an absence of standardised guidance on data collection. We provide an action plan to ensure the data collection is comparable across studies. This framework includes key conservation questions and methodological guidelines for both for in situ and post-season nest data collection and is ordered by increasing complexity of data collection methods. To illustrate our framework, we provide an example with recently discovered Bombus affinis (rusty patched bumble bee) nests. Through observations at B. affinis nests, we discovered novel patterns of activity, changing activity levels over time, the timing of male and gyne production, variable timing in nest senescence, and associations of nests with past rodent activity. Although individual nest discoveries may be of limited value in forwarding conservation strategies, the aggregate collections of many similar datasets can be of critical importance for species of conservation concern.

Insect Conservation and Diversity↗

Bacteriological analysis of unionid hemolymph collected from freshwater mussel populations in the Pacific northwestern United States

Native freshwater mussel (Unionidae) mortality events have been occurring with increased frequency in recent decades, with few investigations into potential etiological agents. In the western United States, no surveys have been published regarding the bacteria associated with unionid mussels. Herein, we examine locations of known mussel mortality events in the Chehalis River (Washington), in the Crooked River (Oregon), and Owyhee River (Oregon). Mussel populations considered healthy were sampled in the Skookumchuck River (Washington) for comparison. A variety of bacteria were isolated from these populations, and most notably, Acinetobacter spp. were identified from 82% of moribund individuals of Gonidea angulata in the Owyhee River. Future work evaluating whether Acinetobacter spp. are pathogenic to freshwater mussels could be valuable in unraveling the factors associated with these enigmatic mortality events.

Oregon, Washington↗

Disease, predation and demography: Assessing the impacts of bovine tuberculosis on African buffalo by monitoring at individual and population levels

Summary Understanding the effects of disease is critical to determining appropriate management responses, but estimating those effects in wildlife species is challenging. We used bovine tuberculosis (BTB) in the African buffalo Syncerus caffer population of Kruger National Park, South Africa, as a case study to highlight the issues associated with estimating chronic disease effects in a long‐lived host. We used known and radiocollared buffalo, aerial census data, and a natural gradient in pathogen prevalence to investigate if: (i) at the individual level, BTB infection reduces reproduction; (ii) BTB infection increases vulnerability to predation; and (iii) at the population level, increased BTB prevalence causes reduced population growth. There was only a marginal reduction in calving success associated with BTB infection, as indexed by the probability of sighting a known adult female with or without a calf ( P = 0·065). Since 1991, BTB prevalence increased from 27 to 45% in the southern region and from 4 to 28% in the central region of Kruger National Park. The prevalence in the northern regions was only 1·5% in 1998. Buffalo population growth rates, however, were neither statistically different among regions nor declining over time. Lions Panthera leo did not appear to preferentially kill test‐positive buffalo. The best (Akaike's Information Criterion corrected for small sample size) AIC c model with BTB as a covariate [exp(β) = 0·49; 95% CI = (0·24–1·02)] suggested that the mortality hazard for positive individuals was no greater than for test‐negative individuals. Synthesis and applications . Test accuracy, time‐varying disease status, and movement among populations are some of the issues that make the detection of chronic disease impacts challenging. For these reasons, the demographic impacts of bovine tuberculosis in the Kruger National Park remain undetectable despite 6 years of study on known individuals and 40 years of population counts. However, the rainfall and forage conditions during this study were relatively good and the impacts of many chronic diseases may be a non‐linear function of environmental conditions such that they are only detectable in stressful periods.

Kruger National Park↗

Compensatory effects of recruitment and survival when amphibian populations are perturbed by disease

The need to increase our understanding of factors that regulate animal population dynamics has been catalysed by recent, observed declines in wildlife populations worldwide. Reliable estimates of demographic parameters are critical for addressing basic and applied ecological questions and understanding the response of parameters to perturbations (e.g. disease, habitat loss, climate change). However, to fully assess the impact of perturbation on population dynamics, all parameters contributing to the response of the target population must be estimated. We applied the reverse‐time model of Pradel in Program mark to 6 years of capture–recapture data from two populations of Anaxyrus boreas (boreal toad) populations, one with disease and one without. We then assessed a priori hypotheses about differences in survival and recruitment relative to local environmental conditions and the presence of disease. We further explored the relative contribution of survival probability and recruitment rate to population growth and investigated how shifts in these parameters can alter population dynamics when a population is perturbed. High recruitment rates (0·41) are probably compensating for low survival probability (range 0·51–0·54) in the population challenged by an emerging pathogen, resulting in a relatively slow rate of decline. In contrast, the population with no evidence of disease had high survival probability (range 0·75–0·78) but lower recruitment rates (0·25). Synthesis and applications. We suggest that the relationship between survival and recruitment may be compensatory, providing evidence that populations challenged with disease are not necessarily doomed to extinction. A better understanding of these interactions may help to explain, and be used to predict, population regulation and persistence for wildlife threatened with disease. Further, reliable estimates of population parameters such as recruitment and survival can guide the formulation and implementation of conservation actions such as repatriations or habitat management aimed to improve recruitment.

Journal of Applied Ecology↗

Pilot- and bench-scale testing of faecal indicator bacteria survival in marine beach sand near point sources

Aim: Factors affecting faecal indicator bacteria (FIB) and pathogen survival/persistence in sand remain largely unstudied. This work elucidates how biological and physical factors affect die-off in beach sand following sewage spills. Methods and Results: Solar disinfection with mechanical mixing was pilot-tested as a disinfection procedure after a large sewage spill in Los Angeles. Effects of solar exposure, mechanical mixing, predation and/or competition, season, and moisture were tested at bench scale. First-order decay constants for Escherichia coli ranged between -0??23 and -1??02 per day, and for enterococci between -0??5 and -1??0 per day. Desiccation was a dominant factor for E. coli but not enterococci inactivation. Effects of season were investigated through a comparison of experimental results from winter, spring, and fall. Conclusions: Moisture was the dominant factor controlling E. coli inactivation kinetics. Initial microbial community and sand temperature were also important factors. Mechanical mixing, common in beach grooming, did not consistently reduce bacterial levels. Significance and Impact of the Study: Inactivation rates are mainly dependent on moisture and high sand temperature. Chlorination was an effective disinfection treatment in sand microcosms inoculated with raw influent. ?? 2009 The Society for Applied Microbiology.

Journal of Applied Microbiology↗

Effects of temperature on biochemical reactions and drug resistance of virulent and avirulent Aeromonas salmonicida

Incubation temperatures of 11°, 18° and 28° did not substantially affect biochemical reactions of either virulent or avirulent forms of Aeromonas salmonicida subspecies salmonicida. The only change observed, amygdalin fermentation, was positive at 11° and 18° but negative at 28°C. Several isolates utilized sucrose, a characteristic not normally recognized for A. salmonicida subspecies salmonicida. Antimicrobial susceptibility screening indicated resistance to novobiocin increased at the higher incubation temperatures. Standardized drug sensitivity testing procedures and precise zone diameter interpretive standards for bacterial fish pathogens are needed.

Journal of Fish Diseases↗

Infectious haematopoietic necrosis virus genogroup-specific virulence mechanisms in sockeye salmon, Oncorhynchus nerka (Walbaum), from Redfish Lake, Idaho

Characterization of infectious haematopoietic necrosis virus (IHNV) field isolates from North America has established three main genogroups (U, M and L) that differ in host-specific virulence. In sockeye salmon, Oncorhynchus nerka, the U genogroup is highly virulent, whereas the M genogroup is nearly non-pathogenic. In this study, we sought to characterize the virus-host dynamics that contribute to genogroup-specific virulence in a captive stock of sockeye salmon from Redfish Lake in Idaho. Juvenile sockeye salmon were challenged by immersion and injection with either a representative U or M viral strain and sampled periodically until 14 days post-infection (p.i.). Fish challenged with each strain had positive viral titre by day 3, regardless of challenge route, but the fish exposed to the M genogroup virus had significantly lower virus titres than fish exposed to the U genogroup virus. Gene expression analysis by quantitative reverse transcriptase PCR was used to simultaneously assess viral load and host interferon (IFN) response in the anterior kidney. Viral load was significantly higher in the U-challenged fish relative to M-challenged fish. Both viruses induced expression of the IFN-stimulated genes (ISGs), but expression was usually significantly lower in the M-challenged group, particularly at later time points (7 and 14 days p.i.). However, ISG expression was comparable with 3 days post-immersion challenge despite a significant difference in viral load. Our data indicated that the M genogroup virus entered the host, replicated and spread in the sockeye salmon tissues, but to a lesser extent than the U genogroup. Both virus types induced a host IFN response, but the high virulence strain (U) continued to replicate in the presence of this response, whereas the low virulence strain (M) was cleared below detectable levels. We hypothesize that high virulence is associated with early in vivo replication allowing the virus to achieve a threshold level, which the host innate immune system cannot control. ?? 2009 Blackwell Publishing Ltd.

Journal of Fish Diseases↗