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Synopsis The emergence and spread of infectious diseases is a significant contributor to global amphibian declines, requiring increased surveillance and research. We assessed host–vector–parasite dynamics using a population of eastern hellbender salamanders (Cryptobranchus alleganiensis) that harbor leeches (Placobdella appalachiensis) that transmit endoparasitic blood parasites (Trypanosoma spp) to the host, with coinfection frequently occurring. We centered our study on adult males throughout their extended 8-month paternal care period because recent research indicates that nest failure caused by lack of paternal care and filial cannibalism is contributing to hellbender population declines. Recognizing the potential for parasites to modulate host physiology and behavior, we explored how infection severity influences paternal health and reproductive success. We assessed white blood cell profiles of adult male hellbenders in response to parasites, coinfection, and seasonal temperature fluctuations, while also investigating whether parasite infection or coinfection was predictive of nest success. We found that hellbenders exhibited seasonal shifts in white blood cell indices; as temperatures increased across seasons (from 5°C to 20°C), the proportion of neutrophils and eosinophils decreased (by 14% and 46%, respectively) in circulation while the proportion of lymphocytes and basophils increased (by 8% and 101%, respectively). Moreover, the proportion of neutrophil precursors increased by 80% under colder temperatures, which signifies seasonal immune cell recruitment. We demonstrated that neutrophils and eosinophils increased while lymphocytes decreased in response to leech infection. However, as leech and trypanosome infection intensity increased together, the proportion of lymphocytes increased while neutrophils and eosinophils decreased, underscoring the complex interactions between coinfection and immune responses of hellbenders that warrant future research. Despite the influence of infection and coinfection on hellbender physiology, we detected no evidence to support the hypothesis that parasites influence the likelihood of nest failure or whole-clutch filial cannibalism. In light of amphibian declines being exacerbated by climate change and disease, our study emphasizes the need to establish hematological reference values that account for physiological adaptations to seasonal fluctuations in temperature and different life history stages and to study the physiological responses of imperiled amphibian species to parasites.
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Concurrent threats and extinction risk in a long‐lived, highly fecund vertebrate with parental care
Abstract Detecting declines and quantifying extinction risk of long‐lived, highly fecund vertebrates, including fishes, reptiles, and amphibians, can be challenging. In addition to the false notion that large clutches always buffer against population declines, the imperiled status of long‐lived species can often be masked by extinction debt, wherein adults persist on the landscape for several years after populations cease to be viable. Here we develop a demographic model for the eastern hellbender (Cryptobranchus alleganiensis), an imperiled aquatic salamander with paternal care. We examined the individual and interactive effects of three of the leading threats hypothesized to contribute to the species' demise: habitat loss due to siltation, high rates of nest failure, and excess adult mortality caused by fishing and harvest. We parameterized the model using data on their life history and reproductive ecology to model the fates of individual nests and address multiple sources of density‐dependent mortality under both deterministic and stochastic environmental conditions. Our model suggests that high rates of nest failure observed in the field are sufficient to drive hellbender populations toward a geriatric age distribution and eventually to localized extinction but that this process takes decades. Moreover, the combination of limited nest site availability due to siltation, nest failure, and stochastic adult mortality can interact to increase the likelihood and pace of extinction, which was particularly evident under stochastic scenarios. Density dependence in larval survival and recruitment can severely hamper a population's ability to recover from declines. Our model helps to identify tipping points beyond which extinction becomes certain and management interventions become necessary. Our approach can be generalized to understand the interactive effects of various threats to the extinction risk of other long‐lived vertebrates. As we face unprecedented rates of environmental change, holistic approaches incorporating multiple concurrent threats and their impacts on different aspects of life history will be necessary to proactively conserve long‐lived species.
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- Award ID(s):
- 1755055
- PAR ID:
- 10539668
- Publisher / Repository:
- Ecological Society of America
- Date Published:
- Journal Name:
- Ecological Applications
- Volume:
- 34
- Issue:
- 2
- ISSN:
- 1051-0761
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Synopsis The rapid environmental changes associated with the Anthropocene mean that flexible behavioral responses may be a critical determinant of animals’ resiliency to anthropogenic disturbance, particularly for species with long generation times and low vagility. One type of behavior that exemplifies this potentially important flexibility is parental care. Eggs and juvenile animals are sensitive to environmental stressors, and the ability of parents to adjust care behaviors to buffer their offspring from rapidly changing conditions may be critical to successful reproduction. In this study, we explore the role of parental care in buffering eggs from anthropogenic stressors in the long-lived, fully aquatic eastern hellbender salamander (Cryptobranchus alleganiensis alleganiensis). Using custom-designed infrared cameras installed in underwater artificial shelters in a natural stream, we describe hellbender paternal care behaviors in greater detail than has previously been possible, assess the extent to which hellbender fathers buffer their eggs from increasing levels of silt and decreasing concentrations of dissolved oxygen in nesting cavities, and describe the possible trade-offs that hellbender fathers exhibit between paternal care and self-maintenance behaviors. We found that while hellbender parents buffered their offspring from low dissolved oxygen concentrations by increasing parental care, there was an apparent trade-off between parental care and self-maintenance responses to low oxygen. Hellbender fathers did not show evidence of buffering their offspring from the effects of increasing silt or organic material in their nest cavities. We also found that filial cannibalism is a widespread behavior across nests, with almost all fathers exhibiting some cannibalism, although the extent varied widely. Our study indicates that hellbender parents may be able to reduce the impacts of declines in dissolved oxygen concentration on their offspring to a limited extent, but they may be unable to fully protect offspring from increasing silt.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1002/eap.2946
