Paul Snyder - Academia.edu (original) (raw)
Papers by Paul Snyder
Proceedings of The Royal Society B: Biological Sciences, Oct 2, 2019
Immunity is one of the most variable phenotypic traits in animals; however, some individuals may ... more Immunity is one of the most variable phenotypic traits in animals; however, some individuals may show less fluctuation in immune traits, resulting in stable patterns of immune variation over time. It is currently unknown whether immune variation has consequences for infectious disease risk. In this study, we identified moderately stable immune traits in wild African buffalo and asked whether the stability of these traits affected bovine tuberculosis (TB) infection risk. We found that adaptive immune traits such as the level of interferon-γ (IFN-γ) released after white blood cell stimulation, the number of circulating lymphocytes and the level of antibodies against bovine adenovirus-3 were moderately repeatable (i.e. stable) over time, whereas parameters related to innate immunity either had low repeatability (circulating eosinophil numbers) or were not repeatable (e.g. neutrophil numbers, plasma bacteria killing capacity). Intriguingly, individuals with more repeatable IFN-γ and lymphocyte levels were at a significantly higher risk of acquiring TB infection. In stark contrast, average IFN-γ and lymphocyte levels were poor predictors of TB risk, indicating that immune variability rather than absolute response level better captured variation in disease susceptibility. This work highlights the important and under-appreciated role of immune variability as a predictor of infection risk.
Journal of Animal Ecology, Feb 4, 2015
1. There is growing interest in the role that life-history traits of hosts, such as their 'pace-o... more 1. There is growing interest in the role that life-history traits of hosts, such as their 'pace-oflife', play in the evolution of resistance and tolerance to parasites. 2. Theory suggests that, relative to host species that have high syntopy (local spatial and temporal overlap) with parasites, host species with low syntopy should have lower selection pressures for more constitutive (always present) and costly defences, such as tolerance, and greater reliance on more inducible and cheaper defences, such as behaviour. Consequently, we postulated that the degree of host-parasite syntopy, which is negatively correlated with host pace-of-life (an axis reflecting the developmental rate of tadpoles and the inverse of their size at metamorphosis) in our tadpole-parasitic cercarial (trematode) system, would be a negative and positive predictor of behavioural resistance and tolerance, respectively. 3. To test these hypotheses, we exposed seven tadpole species to a range of parasite (cercarial) doses crossed with anaesthesia treatments that controlled for anti-parasite behaviour. We quantified host behaviour, successful and unsuccessful infections, and each species' reaction norm for behavioural resistance and tolerance, defined as the slope between cercarial exposure (or attempted infections) and anti-cercarial behaviours and mass change, respectively. Hence, tolerance is capturing any cost of parasite exposure. 4. As hypothesized, tadpole pace-of-life was a significant positive predictor of behavioural resistance and negative predictor of tolerance, a result that is consistent with a trade-off between behavioural resistance and tolerance across species that warrants further investigation. Moreover, these results were robust to considerations of phylogeny, all possible reorderings of the three fastest or slowest paced species, and various measurements of tolerance. 5. These results suggest that host pace-of-life and host-parasite syntopy are powerful drivers of both the strength and type of host defence strategies against parasites. Future research should evaluate how often and how strongly host pace-of-life and host-parasite syntopy are correlated and which is the better predictor of the strength and type of host investments in anti-parasite defences.
Journal of Herpetology, Sep 1, 2013
Pharmacological anesthetics are used frequently in aquatic animal husbandry and research. Althoug... more Pharmacological anesthetics are used frequently in aquatic animal husbandry and research. Although several studies have investigated the effects of these anesthetic agents on immune responses in fish, none have assessed such effects in amphibians. To address this disparity, we exposed Osteopilus septentrionalis tadpoles to 0.005% benzocaine, 0.1% tricaine methanesulfonate (MS-222), or artificial spring water, and quantified circulating white blood cells and susceptibility to infection by larval trematodes. Exposure to neither MS-222 nor benzocaine elevated circulating white blood cells relative to water-exposed tadpoles. Furthermore, anesthetic treatment did not affect resistance to larval trematode infection. These results indicate that the anesthetics tested here probably do not affect tadpole immune function and should aid researchers in determining anesthetic usage.
Journal of Animal Ecology, 2015
1. There is growing interest in the role that life-history traits of hosts, such as their 'pace-o... more 1. There is growing interest in the role that life-history traits of hosts, such as their 'pace-oflife', play in the evolution of resistance and tolerance to parasites. 2. Theory suggests that, relative to host species that have high syntopy (local spatial and temporal overlap) with parasites, host species with low syntopy should have lower selection pressures for more constitutive (always present) and costly defences, such as tolerance, and greater reliance on more inducible and cheaper defences, such as behaviour. Consequently, we postulated that the degree of host-parasite syntopy, which is negatively correlated with host pace-of-life (an axis reflecting the developmental rate of tadpoles and the inverse of their size at metamorphosis) in our tadpole-parasitic cercarial (trematode) system, would be a negative and positive predictor of behavioural resistance and tolerance, respectively. 3. To test these hypotheses, we exposed seven tadpole species to a range of parasite (cercarial) doses crossed with anaesthesia treatments that controlled for anti-parasite behaviour. We quantified host behaviour, successful and unsuccessful infections, and each species' reaction norm for behavioural resistance and tolerance, defined as the slope between cercarial exposure (or attempted infections) and anti-cercarial behaviours and mass change, respectively. Hence, tolerance is capturing any cost of parasite exposure. 4. As hypothesized, tadpole pace-of-life was a significant positive predictor of behavioural resistance and negative predictor of tolerance, a result that is consistent with a trade-off between behavioural resistance and tolerance across species that warrants further investigation. Moreover, these results were robust to considerations of phylogeny, all possible reorderings of the three fastest or slowest paced species, and various measurements of tolerance. 5. These results suggest that host pace-of-life and host-parasite syntopy are powerful drivers of both the strength and type of host defence strategies against parasites. Future research should evaluate how often and how strongly host pace-of-life and host-parasite syntopy are correlated and which is the better predictor of the strength and type of host investments in anti-parasite defences.
Proceedings of The Royal Society B: Biological Sciences, Jul 7, 2013
Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behav... more Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behaviours affect infection location within the host's body and whether parasite distribution ultimately affects tolerance of infection. To assess these questions, we exposed both anaesthetized (no behaviour) and non-anaesthetized Hyla femoralis tadpoles to plagiorchiid cercariae (larval trematodes), and quantified resistance, tolerance (relationship between mass change and infection intensity) and encystment location. Non-anaesthetized tadpoles had significantly more infections in their tail region than anaesthetized tadpoles, which had the majority of their infections in the head. This pattern indicates that parasites preferred to infect the head, but that hosts shunted infections to the tail when possible. Furthermore, there was a significant effect of encystment location on tolerance, with head-infected tadpoles having poorer tolerance to infection than tail-infected tadpoles. Variance partitioning suggests that, among infected tadpoles, behaviour contributed more to tolerance than resistance. These results suggest that, in addition to using behaviour to resist parasites, H. femoralis tadpoles also use behaviour to enhance infection tolerance by deflecting infections posteriorly, away from their vital sensory organs. These findings highlight the need to assess how widespread and important behaviour is to the tolerance of infections.
Functional Ecology, 2015
• Anthropogenic disturbances involving land use change, climate disruption, pollution, and invasi... more • Anthropogenic disturbances involving land use change, climate disruption, pollution, and invasive species have been shown to impact immune function of wild animals. These immune changes have direct impacts on the fitness of impacted animals and, also, potentially indirect effects on other species and on ecological processes, notably involving the spread of infectious disease. Here, we investigate whether the selective loss of large wildlife can also drive changes in immune function of other consumer species. • Using a long-standing large-scale exclosure experiment in East Africa, we investigated the effects of selective removal of large wildlife on multiple measures of immune function in the dominant small rodent in the system, the East African pouched mouse, Saccostomus mearnsi. • We find support for a general increase in immune function in landscapes where large wildlife has been removed, but with some variation across immune parameters. These changes may be mediated in part by increased pathogen pressure in plots where large wildlife has been removed due to major increases in rodent density in such plots, but other factors such as changes in food resources are also likely involved. • Overall, our research reveals that the elimination of large-bodied wildlife-now recognized as another major form of global anthropogenic change-may have cascading effects on immune health, with the potential for these effects to also impact disease dynamics in ecological communities.
Proceedings of the Royal Society B: Biological Sciences, 2013
Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behav... more Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behaviours affect infection location within the host's body and whether parasite distribution ultimately affects tolerance of infection. To assess these questions, we exposed both anaesthetized (no behaviour) and non-anaesthetized Hyla femoralis tadpoles to plagiorchiid cercariae (larval trematodes), and quantified resistance, tolerance (relationship between mass change and infection intensity) and encystment location. Non-anaesthetized tadpoles had significantly more infections in their tail region than anaesthetized tadpoles, which had the majority of their infections in the head. This pattern indicates that parasites preferred to infect the head, but that hosts shunted infections to the tail when possible. Furthermore, there was a significant effect of encystment location on tolerance, with head-infected tadpoles having poorer tolerance to infection than tail-infected tadpoles. Varianc...
Diversity
Numerous factors are contributing to the loss of biodiversity. These include complex effects of m... more Numerous factors are contributing to the loss of biodiversity. These include complex effects of multiple abiotic and biotic stressors that may drive population losses. These losses are especially illustrated by amphibians, whose populations are declining worldwide. The causes of amphibian population declines are multifaceted and context-dependent. One major factor affecting amphibian populations is emerging infectious disease. Several pathogens and their associated diseases are especially significant contributors to amphibian population declines. These include the fungi Batrachochytrium dendrobatidis and B. salamandrivorans, and ranaviruses. In this review, we assess the effects of these three pathogens on amphibian hosts as found through experimental studies. Such studies offer valuable insights to the causal factors underpinning broad patterns reported through observational studies. We summarize key findings from experimental studies in the laboratory, in mesocosms, and from the f...
Journal of wildlife diseases, 2015
Lungworms are important parasites of wildlife and host infection status is often evaluated using ... more Lungworms are important parasites of wildlife and host infection status is often evaluated using coprologic techniques, most commonly the Baermann method. Recently, the FLOTAC® has emerged as a new tool for diagnosing lungworm infections, and methodologic comparison studies in domestic species suggest that this method outperforms many other established techniques. We compared a modified FLOTAC with the beaker-modified (bm)-Baermann to evaluate the relative performance of the two techniques for counting lungworm larvae in bighorn sheep (Ovis canadensis) feces. Both methods generated equivalent larval counts and both were highly repeatable. The major difference between the two methods was that the FLOTAC was poorer at detecting mixed infections. The ultimate choice between using the FLOTAC and bm-Baermann methods for quantifying lungworm larvae in wildlife studies may depend on the specific nature of the research questions being addressed, balanced by practical constraints.
Journal of Herpetology, 2013
Proceedings of the Royal Society B: Biological Sciences, 2013
Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behav... more Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behaviours affect infection location within the host's body and whether parasite distribution ultimately affects tolerance of infection. To assess these questions, we exposed both anaesthetized (no behaviour) and non-anaesthetized Hyla femoralis tadpoles to plagiorchiid cercariae (larval trematodes), and quantified resistance, tolerance (relationship between mass change and infection intensity) and encystment location. Non-anaesthetized tadpoles had significantly more infections in their tail region than anaesthetized tadpoles, which had the majority of their infections in the head. This pattern indicates that parasites preferred to infect the head, but that hosts shunted infections to the tail when possible. Furthermore, there was a significant effect of encystment location on tolerance, with head-infected tadpoles having poorer tolerance to infection than tail-infected tadpoles. Variance partitioning suggests that, among infected tadpoles, behaviour contributed more to tolerance than resistance. These results suggest that, in addition to using behaviour to resist parasites, H. femoralis tadpoles also use behaviour to enhance infection tolerance by deflecting infections posteriorly, away from their vital sensory organs. These findings highlight the need to assess how widespread and important behaviour is to the tolerance of infections.
Proceedings of The Royal Society B: Biological Sciences, Oct 2, 2019
Immunity is one of the most variable phenotypic traits in animals; however, some individuals may ... more Immunity is one of the most variable phenotypic traits in animals; however, some individuals may show less fluctuation in immune traits, resulting in stable patterns of immune variation over time. It is currently unknown whether immune variation has consequences for infectious disease risk. In this study, we identified moderately stable immune traits in wild African buffalo and asked whether the stability of these traits affected bovine tuberculosis (TB) infection risk. We found that adaptive immune traits such as the level of interferon-γ (IFN-γ) released after white blood cell stimulation, the number of circulating lymphocytes and the level of antibodies against bovine adenovirus-3 were moderately repeatable (i.e. stable) over time, whereas parameters related to innate immunity either had low repeatability (circulating eosinophil numbers) or were not repeatable (e.g. neutrophil numbers, plasma bacteria killing capacity). Intriguingly, individuals with more repeatable IFN-γ and lymphocyte levels were at a significantly higher risk of acquiring TB infection. In stark contrast, average IFN-γ and lymphocyte levels were poor predictors of TB risk, indicating that immune variability rather than absolute response level better captured variation in disease susceptibility. This work highlights the important and under-appreciated role of immune variability as a predictor of infection risk.
Journal of Animal Ecology, Feb 4, 2015
1. There is growing interest in the role that life-history traits of hosts, such as their 'pace-o... more 1. There is growing interest in the role that life-history traits of hosts, such as their 'pace-oflife', play in the evolution of resistance and tolerance to parasites. 2. Theory suggests that, relative to host species that have high syntopy (local spatial and temporal overlap) with parasites, host species with low syntopy should have lower selection pressures for more constitutive (always present) and costly defences, such as tolerance, and greater reliance on more inducible and cheaper defences, such as behaviour. Consequently, we postulated that the degree of host-parasite syntopy, which is negatively correlated with host pace-of-life (an axis reflecting the developmental rate of tadpoles and the inverse of their size at metamorphosis) in our tadpole-parasitic cercarial (trematode) system, would be a negative and positive predictor of behavioural resistance and tolerance, respectively. 3. To test these hypotheses, we exposed seven tadpole species to a range of parasite (cercarial) doses crossed with anaesthesia treatments that controlled for anti-parasite behaviour. We quantified host behaviour, successful and unsuccessful infections, and each species' reaction norm for behavioural resistance and tolerance, defined as the slope between cercarial exposure (or attempted infections) and anti-cercarial behaviours and mass change, respectively. Hence, tolerance is capturing any cost of parasite exposure. 4. As hypothesized, tadpole pace-of-life was a significant positive predictor of behavioural resistance and negative predictor of tolerance, a result that is consistent with a trade-off between behavioural resistance and tolerance across species that warrants further investigation. Moreover, these results were robust to considerations of phylogeny, all possible reorderings of the three fastest or slowest paced species, and various measurements of tolerance. 5. These results suggest that host pace-of-life and host-parasite syntopy are powerful drivers of both the strength and type of host defence strategies against parasites. Future research should evaluate how often and how strongly host pace-of-life and host-parasite syntopy are correlated and which is the better predictor of the strength and type of host investments in anti-parasite defences.
Journal of Herpetology, Sep 1, 2013
Pharmacological anesthetics are used frequently in aquatic animal husbandry and research. Althoug... more Pharmacological anesthetics are used frequently in aquatic animal husbandry and research. Although several studies have investigated the effects of these anesthetic agents on immune responses in fish, none have assessed such effects in amphibians. To address this disparity, we exposed Osteopilus septentrionalis tadpoles to 0.005% benzocaine, 0.1% tricaine methanesulfonate (MS-222), or artificial spring water, and quantified circulating white blood cells and susceptibility to infection by larval trematodes. Exposure to neither MS-222 nor benzocaine elevated circulating white blood cells relative to water-exposed tadpoles. Furthermore, anesthetic treatment did not affect resistance to larval trematode infection. These results indicate that the anesthetics tested here probably do not affect tadpole immune function and should aid researchers in determining anesthetic usage.
Journal of Animal Ecology, 2015
1. There is growing interest in the role that life-history traits of hosts, such as their 'pace-o... more 1. There is growing interest in the role that life-history traits of hosts, such as their 'pace-oflife', play in the evolution of resistance and tolerance to parasites. 2. Theory suggests that, relative to host species that have high syntopy (local spatial and temporal overlap) with parasites, host species with low syntopy should have lower selection pressures for more constitutive (always present) and costly defences, such as tolerance, and greater reliance on more inducible and cheaper defences, such as behaviour. Consequently, we postulated that the degree of host-parasite syntopy, which is negatively correlated with host pace-of-life (an axis reflecting the developmental rate of tadpoles and the inverse of their size at metamorphosis) in our tadpole-parasitic cercarial (trematode) system, would be a negative and positive predictor of behavioural resistance and tolerance, respectively. 3. To test these hypotheses, we exposed seven tadpole species to a range of parasite (cercarial) doses crossed with anaesthesia treatments that controlled for anti-parasite behaviour. We quantified host behaviour, successful and unsuccessful infections, and each species' reaction norm for behavioural resistance and tolerance, defined as the slope between cercarial exposure (or attempted infections) and anti-cercarial behaviours and mass change, respectively. Hence, tolerance is capturing any cost of parasite exposure. 4. As hypothesized, tadpole pace-of-life was a significant positive predictor of behavioural resistance and negative predictor of tolerance, a result that is consistent with a trade-off between behavioural resistance and tolerance across species that warrants further investigation. Moreover, these results were robust to considerations of phylogeny, all possible reorderings of the three fastest or slowest paced species, and various measurements of tolerance. 5. These results suggest that host pace-of-life and host-parasite syntopy are powerful drivers of both the strength and type of host defence strategies against parasites. Future research should evaluate how often and how strongly host pace-of-life and host-parasite syntopy are correlated and which is the better predictor of the strength and type of host investments in anti-parasite defences.
Proceedings of The Royal Society B: Biological Sciences, Jul 7, 2013
Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behav... more Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behaviours affect infection location within the host's body and whether parasite distribution ultimately affects tolerance of infection. To assess these questions, we exposed both anaesthetized (no behaviour) and non-anaesthetized Hyla femoralis tadpoles to plagiorchiid cercariae (larval trematodes), and quantified resistance, tolerance (relationship between mass change and infection intensity) and encystment location. Non-anaesthetized tadpoles had significantly more infections in their tail region than anaesthetized tadpoles, which had the majority of their infections in the head. This pattern indicates that parasites preferred to infect the head, but that hosts shunted infections to the tail when possible. Furthermore, there was a significant effect of encystment location on tolerance, with head-infected tadpoles having poorer tolerance to infection than tail-infected tadpoles. Variance partitioning suggests that, among infected tadpoles, behaviour contributed more to tolerance than resistance. These results suggest that, in addition to using behaviour to resist parasites, H. femoralis tadpoles also use behaviour to enhance infection tolerance by deflecting infections posteriorly, away from their vital sensory organs. These findings highlight the need to assess how widespread and important behaviour is to the tolerance of infections.
Functional Ecology, 2015
• Anthropogenic disturbances involving land use change, climate disruption, pollution, and invasi... more • Anthropogenic disturbances involving land use change, climate disruption, pollution, and invasive species have been shown to impact immune function of wild animals. These immune changes have direct impacts on the fitness of impacted animals and, also, potentially indirect effects on other species and on ecological processes, notably involving the spread of infectious disease. Here, we investigate whether the selective loss of large wildlife can also drive changes in immune function of other consumer species. • Using a long-standing large-scale exclosure experiment in East Africa, we investigated the effects of selective removal of large wildlife on multiple measures of immune function in the dominant small rodent in the system, the East African pouched mouse, Saccostomus mearnsi. • We find support for a general increase in immune function in landscapes where large wildlife has been removed, but with some variation across immune parameters. These changes may be mediated in part by increased pathogen pressure in plots where large wildlife has been removed due to major increases in rodent density in such plots, but other factors such as changes in food resources are also likely involved. • Overall, our research reveals that the elimination of large-bodied wildlife-now recognized as another major form of global anthropogenic change-may have cascading effects on immune health, with the potential for these effects to also impact disease dynamics in ecological communities.
Proceedings of the Royal Society B: Biological Sciences, 2013
Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behav... more Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behaviours affect infection location within the host's body and whether parasite distribution ultimately affects tolerance of infection. To assess these questions, we exposed both anaesthetized (no behaviour) and non-anaesthetized Hyla femoralis tadpoles to plagiorchiid cercariae (larval trematodes), and quantified resistance, tolerance (relationship between mass change and infection intensity) and encystment location. Non-anaesthetized tadpoles had significantly more infections in their tail region than anaesthetized tadpoles, which had the majority of their infections in the head. This pattern indicates that parasites preferred to infect the head, but that hosts shunted infections to the tail when possible. Furthermore, there was a significant effect of encystment location on tolerance, with head-infected tadpoles having poorer tolerance to infection than tail-infected tadpoles. Varianc...
Diversity
Numerous factors are contributing to the loss of biodiversity. These include complex effects of m... more Numerous factors are contributing to the loss of biodiversity. These include complex effects of multiple abiotic and biotic stressors that may drive population losses. These losses are especially illustrated by amphibians, whose populations are declining worldwide. The causes of amphibian population declines are multifaceted and context-dependent. One major factor affecting amphibian populations is emerging infectious disease. Several pathogens and their associated diseases are especially significant contributors to amphibian population declines. These include the fungi Batrachochytrium dendrobatidis and B. salamandrivorans, and ranaviruses. In this review, we assess the effects of these three pathogens on amphibian hosts as found through experimental studies. Such studies offer valuable insights to the causal factors underpinning broad patterns reported through observational studies. We summarize key findings from experimental studies in the laboratory, in mesocosms, and from the f...
Journal of wildlife diseases, 2015
Lungworms are important parasites of wildlife and host infection status is often evaluated using ... more Lungworms are important parasites of wildlife and host infection status is often evaluated using coprologic techniques, most commonly the Baermann method. Recently, the FLOTAC® has emerged as a new tool for diagnosing lungworm infections, and methodologic comparison studies in domestic species suggest that this method outperforms many other established techniques. We compared a modified FLOTAC with the beaker-modified (bm)-Baermann to evaluate the relative performance of the two techniques for counting lungworm larvae in bighorn sheep (Ovis canadensis) feces. Both methods generated equivalent larval counts and both were highly repeatable. The major difference between the two methods was that the FLOTAC was poorer at detecting mixed infections. The ultimate choice between using the FLOTAC and bm-Baermann methods for quantifying lungworm larvae in wildlife studies may depend on the specific nature of the research questions being addressed, balanced by practical constraints.
Journal of Herpetology, 2013
Proceedings of the Royal Society B: Biological Sciences, 2013
Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behav... more Anti-parasite behaviour can reduce parasitic infections, but little is known about how such behaviours affect infection location within the host's body and whether parasite distribution ultimately affects tolerance of infection. To assess these questions, we exposed both anaesthetized (no behaviour) and non-anaesthetized Hyla femoralis tadpoles to plagiorchiid cercariae (larval trematodes), and quantified resistance, tolerance (relationship between mass change and infection intensity) and encystment location. Non-anaesthetized tadpoles had significantly more infections in their tail region than anaesthetized tadpoles, which had the majority of their infections in the head. This pattern indicates that parasites preferred to infect the head, but that hosts shunted infections to the tail when possible. Furthermore, there was a significant effect of encystment location on tolerance, with head-infected tadpoles having poorer tolerance to infection than tail-infected tadpoles. Variance partitioning suggests that, among infected tadpoles, behaviour contributed more to tolerance than resistance. These results suggest that, in addition to using behaviour to resist parasites, H. femoralis tadpoles also use behaviour to enhance infection tolerance by deflecting infections posteriorly, away from their vital sensory organs. These findings highlight the need to assess how widespread and important behaviour is to the tolerance of infections.