Contrasting demographic responses of toad populations to regionally synchronous pathogen (Batrachochytrium dendrobatidis) dynamics

Hossack, Blake R.; Russell, Robin E.; McCaffery, Rebecca

doi:10.1016/j.biocon.2019.108373

Cited by 14 publications

(5 citation statements)

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“…An earlier study of the Lost Trail population (2003–2009) found lower survival for male toads with Bd than uninfected individuals (Pilliod et al 2010). More recently, the effect of Bd on survival of male toads captured at John's Pond between 2007–2016 was uncertain (Hossack et al 2020 b ), mirroring our current results from across the entire refuge from 2003–2018. Potential causes for an uncertain effect of Bd on survival include reduced pathogen virulence or increased resistance by hosts (Briggs et al 2010, Voyles et al 2018), insufficient sampling of toads for Bd and reliance on detection of Bd rather than quantifying infection severity (Briggs et al 2010, DiRenzo et al 2018), and the possibility that Bd did in fact reduce survival but the signature was overwhelmed by declines influenced by other factors.…”

Section: Discussionsupporting

confidence: 82%

“…The boreal toad ( Anaxyrus boreas boreas ) is a species of concern in Montana that has experienced widespread declines in other parts of its range. Previous research has implicated Bd in these declines (Muths et al 2003, Scherer et al 2005, Pilliod et al 2010, Hossack et al 2020 b ), but its overall effect on population dynamics is complex and poorly understood (Hossack et al 2020 b ). For example, climate and microhabitat conditions may influence the prevalence and intensity of Bd infection, complicating our understanding of how disease may influence species at a population or regional scale (Kilpatrick et al 2010, Terrell et al 2014).…”

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confidence: 99%

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Enigmatic Near‐Extirpation in a Boreal Toad Metapopulation in Northwestern Montana

2021

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North America's protected lands harbor biodiversity and provide habitats where species threatened by a variety of stressors in other environments can thrive. Yet disease, climate change, and other threats are not limited by land management boundaries and can interact with conditions within protected landscapes to affect sensitive populations. We examined the population dynamics of a boreal toad (Anaxyrus boreas boreas) metapopulation at a wildlife refuge in northwestern Montana, USA, over a 16‐year period (2003–2018). We used robust design capture‐recapture models to estimate male population size, recruitment, and apparent survival over time and in relation to the amphibian chytrid fungus (Batrachochytrium dendrobatidis). We estimated female population size in years with sufficient captures. Finally, we examined trends in male and female toad body size and condition. We found no evidence of an effect of disease or time on male toad survival but detected a strong negative trend in recruitment of new males to the population. Estimates of male and female abundance decreased over time. Body size of males and females was inversely related to estimated population size, consistent with reduced recruitment to replace adults, but body condition of adult males was only weakly associated with abundance. Together, these results describe the demography of a near‐extirpation event, and point to dramatic decreases in the recruitment of new individuals to the breeding population as the cause of this decline. We surmise that processes related to the restoration of historical hydrology within the refuge adversely affected amphibian breeding habitat, and that these changes interacted with disease, life history, and other factors to restrict the recruitment of new individuals to the breeding population over time. Our results point to challenges in understanding and predicting factors that influence population change and highlight that current metrics for assessing population status can have limited predictive ability. Published 2021. This article is a U.S. Government work and is in the public domain in the USA.

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Section: Discussionsupporting

confidence: 82%

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confidence: 99%

Enigmatic Near‐Extirpation in a Boreal Toad Metapopulation in Northwestern Montana

2021

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“…Because diversity is low across the SRM, it may become necessary for managers to consider source populations from outside the SRM to provide an influx of standing genetic variation into extant boreal toad populations. This is particularly true if non-SRM boreal toads have higher fitness when challenged with Bd, as field studies suggest (Hardy et al, 2022;Hossack et al, 2020;Pilliod et al, 2010). Future laboratory infection trials using wild sources of SRM and non-SRM boreal toads will add valuable information for conservation decision-making for SRM boreal toads.…”

Section: Population Structure and Genomic Diversitymentioning

confidence: 99%

Conservation genomics of an endangered montane amphibian reveals low population structure, low genomic diversity and selection pressure from disease

Trumbo,

Hardy,

Crockett

et al. 2023

Molecular Ecology

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Wildlife diseases are a major global threat to biodiversity. Boreal toads (Anaxyrus [Bufo] boreas) are a state‐endangered species in the southern Rocky Mountains of Colorado and New Mexico, and a species of concern in Wyoming, largely due to lethal skin infections caused by the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd). We performed conservation and landscape genomic analyses using single nucleotide polymorphisms from double‐digest, restriction site‐associated DNA sequencing in combination with the development of the first boreal toad (and first North American toad) reference genome to investigate population structure, genomic diversity, landscape connectivity and adaptive divergence. Genomic diversity (π = 0.00034–0.00040) and effective population sizes (Ne = 8.9–38.4) were low, likely due to post‐Pleistocene founder effects and Bd‐related population crashes over the last three decades. Population structure was also low, likely due to formerly high connectivity among a higher density of geographically proximate populations. Boreal toad gene flow was facilitated by low precipitation, cold minimum temperatures, less tree canopy, low heat load and less urbanization. We found >8X more putatively adaptive loci related to Bd intensity than to all other environmental factors combined, and evidence for genes under selection related to immune response, heart development and regulation and skin function. These data suggest boreal toads in habitats with Bd have experienced stronger selection pressure from disease than from other, broad‐scale environmental variations. These findings can be used by managers to conserve and recover the species through actions including reintroduction and supplementation of populations that have declined due to Bd.

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“…Boreal toad populations in the United States have experienced severe declines and extirpations due to Bd in the southern Rocky Mountains region of their range in Colorado and southeastern Wyoming (Hardy et al 2023; Mosher et al 2018; Muths et al 2003). Conversely, populations in western Wyoming and Montana have persisted despite high Bd prevalence within and among populations (Hossack et al 2020; Pilliod et al 2010; Muths et al 2011; Russell et al 2019). This apparent dichotomy in demographic responses provides an ideal natural laboratory to investigate whether intraspecific variation in resistance or tolerance to Bd exists within boreal toads.…”

Section: Introductionmentioning

confidence: 99%

Quantifying Intraspecific Variation in Host Resistance and Tolerance to a Lethal Pathogen

Hardy,

Muths,

Funk

et al. 2023

Preprint

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Due to the ubiquity of disease in natural systems, hosts have evolved strategies of disease resistance and tolerance to defend themselves from further harm once infected. Resistance strategies directly limit pathogen growth, typically leading to lower infection burdens in the host. A tolerance approach limits the fitness consequences caused by the pathogen but does not directly inhibit pathogen growth. Testing for intraspecific variation in wild host populations is important for informing conservation decisions about captive breeding, translocation, and disease treatment. Here, we test for the relative importance of tolerance and resistance in multiple populations of boreal toads (Anaxyrus boreas boreas) againstBatrachochytrium dendrobatidis(Bd), the amphibian fungal pathogen responsible for the greatest host biodiversity loss due to disease. Boreal toads have severely declined in Colorado (CO) due to Bd, but toad populations challenged with Bd in western Wyoming (WY) appear to be less affected. We used a common garden infection experiment to expose post-metamorphic toads sourced from four populations (2 in CO and 2 in WY) to Bd and monitored changes in mass, pathogen burden, and survival for eight weeks. We used a multi-state modeling approach to estimate weekly survival and transition probabilities between infected and cleared states, reflecting a dynamic infection process that traditional approaches fail to capture. We found that WY boreal toads are highly tolerant to Bd infection with higher survival probabilities than those in CO when infected with identical pathogen burdens. WY toads also had higher probabilities of clearing infections and took an average of five days longer to reach peak infection burdens. Our results demonstrate strong intraspecific differences in tolerance and resistance that explain why population declines vary regionally across the species. We used a robust, multi-state framework to gain inference on typically hidden disease processes when testing for host tolerance or resistance and demonstrated that describing an entire species as ‘tolerant’ or ‘resistant’ is unwise without testing for intraspecific variation in host defenses.

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Contrasting demographic responses of toad populations to regionally synchronous pathogen (Batrachochytrium dendrobatidis) dynamics

Cited by 14 publications

References 62 publications

Enigmatic Near‐Extirpation in a Boreal Toad Metapopulation in Northwestern Montana

Enigmatic Near‐Extirpation in a Boreal Toad Metapopulation in Northwestern Montana

Conservation genomics of an endangered montane amphibian reveals low population structure, low genomic diversity and selection pressure from disease

Quantifying Intraspecific Variation in Host Resistance and Tolerance to a Lethal Pathogen

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