Disease is often implicated as a factor in population declines of wildlife and plants. Understand... more Disease is often implicated as a factor in population declines of wildlife and plants. Understanding the characteristics that may predispose a species to infection by a particular pathogen can help direct conservation efforts. Recent declines in amphibian populations worldwide are a major conservation issue and may be caused in part by a fungal pathogen, Batrachochytrium dendrobatidis (Bd). We used Random Forest, a machine learning approach, to identify species-level characteristics that may be related to susceptibility to Bd. Our results suggest that body size at maturity, aspects of egg laying behavior, taxonomic order and family, and reliance on water are good predictors of documented infection for species in the continental United States. These results suggest that, whereas local-scale environmental variables are important to the spread of Bd, species-level characteristics may also influence susceptibility to Bd. The relationships identified in this study suggest future experimental tests, and may target species for conservation efforts.
Population losses and extinctions of species are occurring at unprecedented rates, as exemplified... more Population losses and extinctions of species are occurring at unprecedented rates, as exemplified by declines and extinctions of amphibians worldwide. However, studies of amphibian population declines generally do not address the complexity of the phenomenon or its implications for ecological communities, focusing instead on single factors affecting particular amphibian species. We argue that the causes for amphibian population declines are complex; may differ among species, populations, and life stages within a population; and are context dependent with multiple stressors interacting to drive declines. Because amphibians are key components of communities, we emphasize the importance of investigating amphibian declines at the community level. Selection pressures over evolutionary time have molded amphibian life history characteristics, such that they may remain static even in the face of strong, recent human-induced selection pressures.
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...
In nature, individual hosts often encounter multiple pathogens simultaneously, which can lead to ... more In nature, individual hosts often encounter multiple pathogens simultaneously, which can lead to additive, antagonistic, or synergistic effects on hosts. Synergistic effects on infection prevalence or severity could greatly affect host populations. However, ecologists and managers often overlook the influence of pathogen combinations on hosts. This is especially true in amphibian conservation, even though multiple pathogens coexist within amphibian populations, and several pathogens have been implicated in amphibian population declines and extinctions. Using an amphibian host, Pseudacris regilla (Pacific treefrog), we experimentally investigated interactive effects among three pathogens: the trematode Ribeiroia sp. (hereafter, Ribeiroia), the fungus Batrachochytrium dendrobatidis (hereafter, BD), and the water mold Achlya flagellata. We detected no effects of A. flagellata, but did find effects of Ribeiroia and BD that varied depending on context. Low doses of Ribeiroia caused relatively few malformations, while higher Ribeiroia doses caused numerous deformities dominated by missing and reduced limbs and limb elements. Exposure to low doses of BD accelerated larval host development, despite there being no detectable BD infections, while exposure to higher BD doses caused infection but did not alter developmental rate. Hosts exposed to both Ribeiroia and BD exhibited the highest mortality, although overall evidence of interactive effects of multiple pathogens was limited. We suggest further research on the influence of multi-pathogen assemblages on amphibians, particularly under a variety of ecological conditions and with a wider diversity of hosts and pathogens.
We explored the importance of interactions between parasite infection and predation in driving an... more We explored the importance of interactions between parasite infection and predation in driving an emerging phenomenon of conservation importance: amphibian limb malformations. We suggest that injury resulting from intraspecific predation in combination with trematode infection contributes to the frequency and severity of malformations in salamanders. By integrating field surveys and experiments, we evaluated the individual and combined effects of conspecific attack and parasite (Ribeiroia ondatrae) infection on limb development of long-toed salamanders (Ambystoma macrodactylum). In the absence of Ribeiroia, abnormalities involved missing digits, feet, or limbs and were similar to those produced by cannibalistic attack in experimental trials. At field sites that supported Ribeiroia, malformations were dominated by extra limbs and digits. Correspondingly, laboratory exposure of larval salamanders to Ribeiroia cercariae over a 30-day period induced high frequencies of malformations, including extra digits, extra limbs, cutaneous fusion, and micromelia. However, salamander limbs exposed to both injury and infection exhibited 3-5 times more abnormalities than those exposed to either factor alone. Infection also caused significant delays in limb regeneration and time-to-metamorphosis. Taken together, these results help to explain malformation patterns observed in natural salamander populations while emphasizing the importance of interactions between parasitism and predation in driving disease.
Parasites and pathogens can influence the survivorship, behavior, and very structure of their hos... more Parasites and pathogens can influence the survivorship, behavior, and very structure of their host species. For example, experimental studies have shown that trematode parasites can cause high frequencies of severe limb malformations in amphibians. In a broad-scale field survey covering parts of California, Oregon, Washington, Idaho, and Montana, we examined relationships between the frequency and types of morphological abnormalities in amphibians and the abundance of trematode parasite infection, pH, concentrations of 61 pesticides, and levels of orthophosphate and total nitrate. We recorded severe malformations at frequencies ranging from 1% to 90% in nine amphibian species from 53 aquatic systems. Infection of larvae by the trematode Ribeiroia ondatrae was associated with, and functionally related to, higher frequencies of amphibian limb malformations than found in uninfected populations (Յ5%). Parasites were concentrated around the basal tissue of hind limbs in infected anurans, and malformations associated with infection included skin webbings, supernumerary limbs and digits, and missing or malformed hind limbs. In the absence of Ribeiroia, amphibian populations exhibited low (0-5%) frequencies of abnormalities involving missing digits or distal portions of a hind limb. Species were affected differentially by the parasite, and Ambystoma macrodactylum, Hyla regilla, Rana aurora, R. luteiventris, and Taricha torosa typically exhibited the highest frequencies of abnormalities. None of the water-quality variables measured was associated with malformed amphibians, but aquatic snail hosts (Planorbella spp.) were significant predictors of the presence and abundance of Ribeiroia infection. Morphological comparisons of adult specimens of Ribeiroia collected from different sites and raised in experimental definitive hosts suggested that all samples represented the same species-R. ondatrae. These field results, coupled with experimental research on the effects of Ribeiroia on amphibians, demonstrate that Ribeiroia infection is an important and widespread cause of amphibian limb malformations in the western United States. The relevance of trematode infection to declines of amphibian populations and the influence of habitat modification on the pathology and life cycle of Ribeiroia are emphasized as areas requiring further research.
As part of an overall biodiversity crisis many amphibian populations are in decline throughout th... more As part of an overall biodiversity crisis many amphibian populations are in decline throughout the world. Numerous causes have been invoked to explain these declines. These include habitat destruction, climate change, increasing levels of ultraviolet radiation, environmental contamination, and the introduction of non-native species and diseases. Several types of pathogens have been implicated in contributing to amphibian population declines: viruses, bacteria, oomycetes, and fungi. One particular fungus, the chytridiomycete Batrachochytrium dendrobatidis may have caused amphibian population declines in several regions. This pathogen causes chytridiomycosis, which is fatal to newly metamorphic and adult amphibians of certain species. We present experimental evidence that larval stages may also be susceptible to exposure to Batrachochytrium. There was, however, differential sensitivity to B. dendrobatidis in larvae we examined. In laboratory experiments, larval western toads (Bufo boreas) exposed to B. dendrobatidis experienced increased mortality and behaviors that suggested they were affected by exposure compared with unexposed control tadpoles. Larvae of Cascades frogs (Rana cascadae), bullfrogs (R. catesbeiana), and Pacific treefrogs (Hyla regilla) did not die after exposure to Batrachochytrium and appeared to behave normally. R. cascadae larvae exposed to B. dendrobatidis, however, showed an increase incidence in mouthpart abnormalities, a characteristic effect of chytridiomycosis, compared with unexposed controls. These results show that Batrachochytrium can negatively affect some species of amphibians at the larval stage and not others. The implications of interspecific variation in susceptibility to fungal infection are broad.
Many animals, plants, and microorganisms are harmed by ultraviolet-B radiation. In particular, se... more Many animals, plants, and microorganisms are harmed by ultraviolet-B radiation. In particular, several members of class amphibia are negatively affected by exposure to ultraviolet-B radiation. Exposure to ultraviolet-B radiation can cause death or various types of sublethal damage in amphibians. One mechanism to lessen the effect of harmful ultraviolet-B radiation is to limit exposure to sunlight behaviorally. Few studies have examined the behavioral sensitivity of adult amphibians to ultraviolet-B radiation. Using both field experiments and field observations, we found that two species of diurnal poison-dart frogs in Costa Rica (Dendrobates pumilio, D. auratus) consistently preferred areas in the field and within experimental testing chambers that offered low levels of ultraviolet-B radiation. In field observations, vocalizing D. pumilio were found at locations with significantly lower levels of ambient ultraviolet-B compared to random locations throughout their natural habitat. Ultraviolet-B avoidance behavior may be an important behavioral response for tropical frogs in light of recent evidence suggesting a significant increase in the levels of ambient ultraviolet-B radiation in the tropics over the past decade.
Behaviors have evolved in response to various selection pressures over evolutionary time. However... more Behaviors have evolved in response to various selection pressures over evolutionary time. However, not all behaviors are adaptive. Some presumably "ancient" behaviors, persistent for millions of years, may be detrimental in the face of novel selection pressures in modern times. These pressures include a multitude of emerging infectious diseases which may be stimulated by environmental changes. We examined how a globally emerging amphibian pathogen, Batrachochytrium dendrobatidis (BD), affected two key evolutionarily persistent behaviors displayed by amphibian larvae: aggregation and thermoregulation. Larval aggregation behavior is often essential for foraging, thermoregulation, and antipredator defense, but varies among species. Thermoregulatory behavior speeds larval development in ephemeral habitats. Specifically, we examined whether aggregation and thermoregulatory behaviors changed when exposed to the BD pathogen in two species (Bufo boreas and Rana cascadae) whose larvae aggregate in nature. In laboratory choice tests, larvae of neither species avoided infected conspecifics. BD-exposed B. boreas larvae aggregated, while unexposed R. cascadae larvae associated more frequently with BD-exposed conspecifics. There was no evidence of behavioral fever or altered thermoregulation in larvae of four species we examined (Pseudacris regilla, Rana aurora, B. boreas, R. cascadae). The absence of behavioral fever may suggest an inability of the larvae of some host species to mediate infection risk by this pathogen. Thermoregulatory behaviors may exhibit a high degree of evolutionary inertia in amphibian hosts because they are linked with host physiology and developmental rates, while altered aggregation behaviors could potentially elevate pathogen transmission rates, leading to increased infection risk in social amphibian species.
Relatively few studies of amphibian diseases have employed standard ecological experimental desig... more Relatively few studies of amphibian diseases have employed standard ecological experimental designs. We discuss what constitutes a well-designed ecological experiment and encourage their use in disease studies. We illustrate how well-designed experiments can be used to determine the effects of pathogens on amphibians and we illustrate how ancillary information, including that collected using molecular tools, can be used to enhance the value of such experiments.
The ability of an animal to discriminate between kin and non-kin (kin recognition) has been the s... more The ability of an animal to discriminate between kin and non-kin (kin recognition) has been the subject of numerous recent investigations. Grafen (Anim. Behav., 1990, 39, 42-54) recently reported that the evidence in support of kin recognition is weak and the data illustrating a preference for kin to associate in the laboratory may be more consistently explained as species recognition. It is suggested here, however, that in many cases it may be impossible to distinguish between species recognition and kin recognition, but in some cases, kin recognition seems apparent. It is also emphasized that very little is known about the adaptive value of kin recognition. The ability of an animal to discriminate between kin and non-kin (often called kin recognition) is an important phenomenon associated with kin selection theory (Hamilton 1964a, b). It is therefore a great concern to those interested in the evolution of social behaviour. Recently, Grafen (1990), in a stimulating and provocative paper, concluded that the empirical evidence in support of kin recognition is weak and that data illustrating a preference for kin to associate in the laboratory may be more consistently explained as species recognition. By narrowly defining kin recognition, Grafen is forced to conclude that kin do not recognize one another except rarely. Here, we (1) add some additional pertinent information to Grafen's point concerning species recognition and (2) make a point of which many biologists seem to be unaware; namely that, there is at best, a very poor understanding of the adaptive value of kin recognition in most species that have been investigated. KIN RECOGNITION OR SPECIES RECOGNITION? Grafen uses data obtained from studies of tadpoles to illustrate how species recognition, in general, may be achieved. He suggests that a species recognition mechanism would work well if, for example, all members of the species had essentially the same smell and some genetic variation in the smell. Then, individuals will 'acquire a standard (the smell of themselves) which is slightly more like relatives than it is like conspecifics in general' (page 44). Thus, when an individual uses its species recognition capability to join a tadpole aggregation, it will be biased to join a more related group because such a group is perceived as being closer to the 'acquired standard' (i.e. the individual itself).
Worldwide declines in amphibian populations have been the subject of numerous recent reports, and... more Worldwide declines in amphibian populations have been the subject of numerous recent reports, and numerous hypotheses have been constructed to address the causes. There is no evidence for a single cause for the declines. We identify and describe the spread of a pathogenic jungus that appears to be largely responsible for egg mortality in one population of western toad Bufo boreas. This is the first study documenting contemporary mortality in an amphibian population with identification of the attributed pathogenic species. The fungus we identify is circumglobally distributed and we suggest that this fungal infection could also be a major contributor to other amphibian populations declines.
We examined diet-dependent plasticity in head shape in larvae of the eastern long-toed salamander... more We examined diet-dependent plasticity in head shape in larvae of the eastern long-toed salamander, Ambystoma macrodactylum columbianum. Larvae in some populations of this species exhibit trophic polymorphism, with some individuals possessing exaggerated trophic features characteristic of a cannibalistic morphology in larval Ambystoma; e.g. a disproportionately broad head and hypertrophied vomerine teeth. We hypothesized that 1) head shape variation results from feeding upon different types of prey and that 2) cannibal morphs are induced by consumption of conspecifics. To induce variation, we fed three groups of larvae different diets: 1) brine shrimp nauplii only; 2) nauplii plus anuran tadpoles; 3) nauplii, tadpoles and conspecific larval salamanders. Comparisons of size (mass)-adjusted means revealed that this manipulation of diet induced significant variation in six measures of head shape, but not in the area of the vomerine tooth patch. For five of the six head traits, larvae that ate tadpoles and brine shrimp nauplii developed significantly broader, longer and deeper heads than did larvae that only ate brine shrimp nauplii. The ingestion of conspecifics, in addition to nauplii and tadpoles, significantly altered two head traits (interocular width and head depth), compared to larvae only fed nauplii and tadpoles. Canonical discriminant function analysis detected two statistically reliable canonical variables: head depth was most highly associated with the first canonical variable, whereas three measures of head width (at the jaws, gills and eyes) and interocular width were most highly associated with the second canonical variable. Despite this diet-enhanced morphological variation, there was no indication that any of the three types of diet (including conspecific prey) induced the exaggerated trophic features of the "cannibal" morph in this species. These results illustrate that ingestion of different types of prey contributes to plasticity in head shape, but that some other proximate cue(s), either alone or in combination with diet variation, is essential to induce the extremes of trophic polymorphism in this species.
Sibling recognition was studied experimentally in tadpoles of the Cascades frog, Rana cascadae. S... more Sibling recognition was studied experimentally in tadpoles of the Cascades frog, Rana cascadae. Sibships were divided into two groups at an early developmental stage. One group was reared with siblings and the second with a mixture of siblings and non-siblings. When given a choice of associating with a sibling or non-sibling group, individuals reared with siblings preferred siblings. One mixed-reared group spent more time associating with unfamiliar siblings than unfamiliar nonsiblings. Tadpoles of another mixed-reared group preferred to associate with pure siblings over a mixture of siblings and non-siblings with which they were reared. When the stimulus animals were taken exclusively from the mixed-rearing tank, two mixed-reared groups showed no sibling preferences. Our results suggest that early association with non-siblings does not affect sibling recognition in this species.
Relatively few studies of amphibian diseases have employed standard ecological experimental desig... more Relatively few studies of amphibian diseases have employed standard ecological experimental designs. We discuss what constitutes a well-designed ecological experiment and encourage their use in disease studies. We illustrate how well-designed experiments can be used to determine the effects of pathogens on amphibians and we illustrate how ancillary information, including that collected using molecular tools, can be used to enhance the value of such experiments.
The populations of many amphibian species, in widely scattered habitats, appear to be in severe d... more The populations of many amphibian species, in widely scattered habitats, appear to be in severe decline; other amphibians show no such declines. There is no known single cause for the declines, but their widespread distribution suggests involvement of global agents-increased UV-B radiation, for example. We addressed the hypothesis that differential sensitivity among species to UV radiation contributes to these population declines. We focused on species-specific differences in the abilities of eggs to repair UV radiation damage to DNA and differential hatching success of embryos exposed to solar radiation at natural oviposition sites. Quantitative comparisons of activities of a key UV-damage-specific repair enzyme, photolyase, among oocytes and eggs from 10 amphibian species were reproducibly characteristic for a given species but varied >80-fold among the species. Levels of photolyase generally correlated with expected exposure of eggs to sunlight. Among the frog and toad species studied, the highest activity was shown by the Pacific treefrog (Hyla regilla), whose populations are not known to be in decline. The Western toad (Bufo boreas) and the Cascades frog (Rana cascadae), whose populations have declined markedly, showed significantly lower photolyase levels. In field experiments, the hatching success of embryos exposed to UV radiation was significantly greater in H. regkla than in R. cascadae and B. boreas. Moreover, in R. cascadae and B. boreas, hatching success was greater in regimes shielded from UV radiation compared with regimes that allowed UV radiation. These observations are thus consistent with the UV-sensitivity hypothesis.
Disease is often implicated as a factor in population declines of wildlife and plants. Understand... more Disease is often implicated as a factor in population declines of wildlife and plants. Understanding the characteristics that may predispose a species to infection by a particular pathogen can help direct conservation efforts. Recent declines in amphibian populations worldwide are a major conservation issue and may be caused in part by a fungal pathogen, Batrachochytrium dendrobatidis (Bd). We used Random Forest, a machine learning approach, to identify species-level characteristics that may be related to susceptibility to Bd. Our results suggest that body size at maturity, aspects of egg laying behavior, taxonomic order and family, and reliance on water are good predictors of documented infection for species in the continental United States. These results suggest that, whereas local-scale environmental variables are important to the spread of Bd, species-level characteristics may also influence susceptibility to Bd. The relationships identified in this study suggest future experimental tests, and may target species for conservation efforts.
Population losses and extinctions of species are occurring at unprecedented rates, as exemplified... more Population losses and extinctions of species are occurring at unprecedented rates, as exemplified by declines and extinctions of amphibians worldwide. However, studies of amphibian population declines generally do not address the complexity of the phenomenon or its implications for ecological communities, focusing instead on single factors affecting particular amphibian species. We argue that the causes for amphibian population declines are complex; may differ among species, populations, and life stages within a population; and are context dependent with multiple stressors interacting to drive declines. Because amphibians are key components of communities, we emphasize the importance of investigating amphibian declines at the community level. Selection pressures over evolutionary time have molded amphibian life history characteristics, such that they may remain static even in the face of strong, recent human-induced selection pressures.
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...
In nature, individual hosts often encounter multiple pathogens simultaneously, which can lead to ... more In nature, individual hosts often encounter multiple pathogens simultaneously, which can lead to additive, antagonistic, or synergistic effects on hosts. Synergistic effects on infection prevalence or severity could greatly affect host populations. However, ecologists and managers often overlook the influence of pathogen combinations on hosts. This is especially true in amphibian conservation, even though multiple pathogens coexist within amphibian populations, and several pathogens have been implicated in amphibian population declines and extinctions. Using an amphibian host, Pseudacris regilla (Pacific treefrog), we experimentally investigated interactive effects among three pathogens: the trematode Ribeiroia sp. (hereafter, Ribeiroia), the fungus Batrachochytrium dendrobatidis (hereafter, BD), and the water mold Achlya flagellata. We detected no effects of A. flagellata, but did find effects of Ribeiroia and BD that varied depending on context. Low doses of Ribeiroia caused relatively few malformations, while higher Ribeiroia doses caused numerous deformities dominated by missing and reduced limbs and limb elements. Exposure to low doses of BD accelerated larval host development, despite there being no detectable BD infections, while exposure to higher BD doses caused infection but did not alter developmental rate. Hosts exposed to both Ribeiroia and BD exhibited the highest mortality, although overall evidence of interactive effects of multiple pathogens was limited. We suggest further research on the influence of multi-pathogen assemblages on amphibians, particularly under a variety of ecological conditions and with a wider diversity of hosts and pathogens.
We explored the importance of interactions between parasite infection and predation in driving an... more We explored the importance of interactions between parasite infection and predation in driving an emerging phenomenon of conservation importance: amphibian limb malformations. We suggest that injury resulting from intraspecific predation in combination with trematode infection contributes to the frequency and severity of malformations in salamanders. By integrating field surveys and experiments, we evaluated the individual and combined effects of conspecific attack and parasite (Ribeiroia ondatrae) infection on limb development of long-toed salamanders (Ambystoma macrodactylum). In the absence of Ribeiroia, abnormalities involved missing digits, feet, or limbs and were similar to those produced by cannibalistic attack in experimental trials. At field sites that supported Ribeiroia, malformations were dominated by extra limbs and digits. Correspondingly, laboratory exposure of larval salamanders to Ribeiroia cercariae over a 30-day period induced high frequencies of malformations, including extra digits, extra limbs, cutaneous fusion, and micromelia. However, salamander limbs exposed to both injury and infection exhibited 3-5 times more abnormalities than those exposed to either factor alone. Infection also caused significant delays in limb regeneration and time-to-metamorphosis. Taken together, these results help to explain malformation patterns observed in natural salamander populations while emphasizing the importance of interactions between parasitism and predation in driving disease.
Parasites and pathogens can influence the survivorship, behavior, and very structure of their hos... more Parasites and pathogens can influence the survivorship, behavior, and very structure of their host species. For example, experimental studies have shown that trematode parasites can cause high frequencies of severe limb malformations in amphibians. In a broad-scale field survey covering parts of California, Oregon, Washington, Idaho, and Montana, we examined relationships between the frequency and types of morphological abnormalities in amphibians and the abundance of trematode parasite infection, pH, concentrations of 61 pesticides, and levels of orthophosphate and total nitrate. We recorded severe malformations at frequencies ranging from 1% to 90% in nine amphibian species from 53 aquatic systems. Infection of larvae by the trematode Ribeiroia ondatrae was associated with, and functionally related to, higher frequencies of amphibian limb malformations than found in uninfected populations (Յ5%). Parasites were concentrated around the basal tissue of hind limbs in infected anurans, and malformations associated with infection included skin webbings, supernumerary limbs and digits, and missing or malformed hind limbs. In the absence of Ribeiroia, amphibian populations exhibited low (0-5%) frequencies of abnormalities involving missing digits or distal portions of a hind limb. Species were affected differentially by the parasite, and Ambystoma macrodactylum, Hyla regilla, Rana aurora, R. luteiventris, and Taricha torosa typically exhibited the highest frequencies of abnormalities. None of the water-quality variables measured was associated with malformed amphibians, but aquatic snail hosts (Planorbella spp.) were significant predictors of the presence and abundance of Ribeiroia infection. Morphological comparisons of adult specimens of Ribeiroia collected from different sites and raised in experimental definitive hosts suggested that all samples represented the same species-R. ondatrae. These field results, coupled with experimental research on the effects of Ribeiroia on amphibians, demonstrate that Ribeiroia infection is an important and widespread cause of amphibian limb malformations in the western United States. The relevance of trematode infection to declines of amphibian populations and the influence of habitat modification on the pathology and life cycle of Ribeiroia are emphasized as areas requiring further research.
As part of an overall biodiversity crisis many amphibian populations are in decline throughout th... more As part of an overall biodiversity crisis many amphibian populations are in decline throughout the world. Numerous causes have been invoked to explain these declines. These include habitat destruction, climate change, increasing levels of ultraviolet radiation, environmental contamination, and the introduction of non-native species and diseases. Several types of pathogens have been implicated in contributing to amphibian population declines: viruses, bacteria, oomycetes, and fungi. One particular fungus, the chytridiomycete Batrachochytrium dendrobatidis may have caused amphibian population declines in several regions. This pathogen causes chytridiomycosis, which is fatal to newly metamorphic and adult amphibians of certain species. We present experimental evidence that larval stages may also be susceptible to exposure to Batrachochytrium. There was, however, differential sensitivity to B. dendrobatidis in larvae we examined. In laboratory experiments, larval western toads (Bufo boreas) exposed to B. dendrobatidis experienced increased mortality and behaviors that suggested they were affected by exposure compared with unexposed control tadpoles. Larvae of Cascades frogs (Rana cascadae), bullfrogs (R. catesbeiana), and Pacific treefrogs (Hyla regilla) did not die after exposure to Batrachochytrium and appeared to behave normally. R. cascadae larvae exposed to B. dendrobatidis, however, showed an increase incidence in mouthpart abnormalities, a characteristic effect of chytridiomycosis, compared with unexposed controls. These results show that Batrachochytrium can negatively affect some species of amphibians at the larval stage and not others. The implications of interspecific variation in susceptibility to fungal infection are broad.
Many animals, plants, and microorganisms are harmed by ultraviolet-B radiation. In particular, se... more Many animals, plants, and microorganisms are harmed by ultraviolet-B radiation. In particular, several members of class amphibia are negatively affected by exposure to ultraviolet-B radiation. Exposure to ultraviolet-B radiation can cause death or various types of sublethal damage in amphibians. One mechanism to lessen the effect of harmful ultraviolet-B radiation is to limit exposure to sunlight behaviorally. Few studies have examined the behavioral sensitivity of adult amphibians to ultraviolet-B radiation. Using both field experiments and field observations, we found that two species of diurnal poison-dart frogs in Costa Rica (Dendrobates pumilio, D. auratus) consistently preferred areas in the field and within experimental testing chambers that offered low levels of ultraviolet-B radiation. In field observations, vocalizing D. pumilio were found at locations with significantly lower levels of ambient ultraviolet-B compared to random locations throughout their natural habitat. Ultraviolet-B avoidance behavior may be an important behavioral response for tropical frogs in light of recent evidence suggesting a significant increase in the levels of ambient ultraviolet-B radiation in the tropics over the past decade.
Behaviors have evolved in response to various selection pressures over evolutionary time. However... more Behaviors have evolved in response to various selection pressures over evolutionary time. However, not all behaviors are adaptive. Some presumably "ancient" behaviors, persistent for millions of years, may be detrimental in the face of novel selection pressures in modern times. These pressures include a multitude of emerging infectious diseases which may be stimulated by environmental changes. We examined how a globally emerging amphibian pathogen, Batrachochytrium dendrobatidis (BD), affected two key evolutionarily persistent behaviors displayed by amphibian larvae: aggregation and thermoregulation. Larval aggregation behavior is often essential for foraging, thermoregulation, and antipredator defense, but varies among species. Thermoregulatory behavior speeds larval development in ephemeral habitats. Specifically, we examined whether aggregation and thermoregulatory behaviors changed when exposed to the BD pathogen in two species (Bufo boreas and Rana cascadae) whose larvae aggregate in nature. In laboratory choice tests, larvae of neither species avoided infected conspecifics. BD-exposed B. boreas larvae aggregated, while unexposed R. cascadae larvae associated more frequently with BD-exposed conspecifics. There was no evidence of behavioral fever or altered thermoregulation in larvae of four species we examined (Pseudacris regilla, Rana aurora, B. boreas, R. cascadae). The absence of behavioral fever may suggest an inability of the larvae of some host species to mediate infection risk by this pathogen. Thermoregulatory behaviors may exhibit a high degree of evolutionary inertia in amphibian hosts because they are linked with host physiology and developmental rates, while altered aggregation behaviors could potentially elevate pathogen transmission rates, leading to increased infection risk in social amphibian species.
Relatively few studies of amphibian diseases have employed standard ecological experimental desig... more Relatively few studies of amphibian diseases have employed standard ecological experimental designs. We discuss what constitutes a well-designed ecological experiment and encourage their use in disease studies. We illustrate how well-designed experiments can be used to determine the effects of pathogens on amphibians and we illustrate how ancillary information, including that collected using molecular tools, can be used to enhance the value of such experiments.
The ability of an animal to discriminate between kin and non-kin (kin recognition) has been the s... more The ability of an animal to discriminate between kin and non-kin (kin recognition) has been the subject of numerous recent investigations. Grafen (Anim. Behav., 1990, 39, 42-54) recently reported that the evidence in support of kin recognition is weak and the data illustrating a preference for kin to associate in the laboratory may be more consistently explained as species recognition. It is suggested here, however, that in many cases it may be impossible to distinguish between species recognition and kin recognition, but in some cases, kin recognition seems apparent. It is also emphasized that very little is known about the adaptive value of kin recognition. The ability of an animal to discriminate between kin and non-kin (often called kin recognition) is an important phenomenon associated with kin selection theory (Hamilton 1964a, b). It is therefore a great concern to those interested in the evolution of social behaviour. Recently, Grafen (1990), in a stimulating and provocative paper, concluded that the empirical evidence in support of kin recognition is weak and that data illustrating a preference for kin to associate in the laboratory may be more consistently explained as species recognition. By narrowly defining kin recognition, Grafen is forced to conclude that kin do not recognize one another except rarely. Here, we (1) add some additional pertinent information to Grafen's point concerning species recognition and (2) make a point of which many biologists seem to be unaware; namely that, there is at best, a very poor understanding of the adaptive value of kin recognition in most species that have been investigated. KIN RECOGNITION OR SPECIES RECOGNITION? Grafen uses data obtained from studies of tadpoles to illustrate how species recognition, in general, may be achieved. He suggests that a species recognition mechanism would work well if, for example, all members of the species had essentially the same smell and some genetic variation in the smell. Then, individuals will 'acquire a standard (the smell of themselves) which is slightly more like relatives than it is like conspecifics in general' (page 44). Thus, when an individual uses its species recognition capability to join a tadpole aggregation, it will be biased to join a more related group because such a group is perceived as being closer to the 'acquired standard' (i.e. the individual itself).
Worldwide declines in amphibian populations have been the subject of numerous recent reports, and... more Worldwide declines in amphibian populations have been the subject of numerous recent reports, and numerous hypotheses have been constructed to address the causes. There is no evidence for a single cause for the declines. We identify and describe the spread of a pathogenic jungus that appears to be largely responsible for egg mortality in one population of western toad Bufo boreas. This is the first study documenting contemporary mortality in an amphibian population with identification of the attributed pathogenic species. The fungus we identify is circumglobally distributed and we suggest that this fungal infection could also be a major contributor to other amphibian populations declines.
We examined diet-dependent plasticity in head shape in larvae of the eastern long-toed salamander... more We examined diet-dependent plasticity in head shape in larvae of the eastern long-toed salamander, Ambystoma macrodactylum columbianum. Larvae in some populations of this species exhibit trophic polymorphism, with some individuals possessing exaggerated trophic features characteristic of a cannibalistic morphology in larval Ambystoma; e.g. a disproportionately broad head and hypertrophied vomerine teeth. We hypothesized that 1) head shape variation results from feeding upon different types of prey and that 2) cannibal morphs are induced by consumption of conspecifics. To induce variation, we fed three groups of larvae different diets: 1) brine shrimp nauplii only; 2) nauplii plus anuran tadpoles; 3) nauplii, tadpoles and conspecific larval salamanders. Comparisons of size (mass)-adjusted means revealed that this manipulation of diet induced significant variation in six measures of head shape, but not in the area of the vomerine tooth patch. For five of the six head traits, larvae that ate tadpoles and brine shrimp nauplii developed significantly broader, longer and deeper heads than did larvae that only ate brine shrimp nauplii. The ingestion of conspecifics, in addition to nauplii and tadpoles, significantly altered two head traits (interocular width and head depth), compared to larvae only fed nauplii and tadpoles. Canonical discriminant function analysis detected two statistically reliable canonical variables: head depth was most highly associated with the first canonical variable, whereas three measures of head width (at the jaws, gills and eyes) and interocular width were most highly associated with the second canonical variable. Despite this diet-enhanced morphological variation, there was no indication that any of the three types of diet (including conspecific prey) induced the exaggerated trophic features of the "cannibal" morph in this species. These results illustrate that ingestion of different types of prey contributes to plasticity in head shape, but that some other proximate cue(s), either alone or in combination with diet variation, is essential to induce the extremes of trophic polymorphism in this species.
Sibling recognition was studied experimentally in tadpoles of the Cascades frog, Rana cascadae. S... more Sibling recognition was studied experimentally in tadpoles of the Cascades frog, Rana cascadae. Sibships were divided into two groups at an early developmental stage. One group was reared with siblings and the second with a mixture of siblings and non-siblings. When given a choice of associating with a sibling or non-sibling group, individuals reared with siblings preferred siblings. One mixed-reared group spent more time associating with unfamiliar siblings than unfamiliar nonsiblings. Tadpoles of another mixed-reared group preferred to associate with pure siblings over a mixture of siblings and non-siblings with which they were reared. When the stimulus animals were taken exclusively from the mixed-rearing tank, two mixed-reared groups showed no sibling preferences. Our results suggest that early association with non-siblings does not affect sibling recognition in this species.
Relatively few studies of amphibian diseases have employed standard ecological experimental desig... more Relatively few studies of amphibian diseases have employed standard ecological experimental designs. We discuss what constitutes a well-designed ecological experiment and encourage their use in disease studies. We illustrate how well-designed experiments can be used to determine the effects of pathogens on amphibians and we illustrate how ancillary information, including that collected using molecular tools, can be used to enhance the value of such experiments.
The populations of many amphibian species, in widely scattered habitats, appear to be in severe d... more The populations of many amphibian species, in widely scattered habitats, appear to be in severe decline; other amphibians show no such declines. There is no known single cause for the declines, but their widespread distribution suggests involvement of global agents-increased UV-B radiation, for example. We addressed the hypothesis that differential sensitivity among species to UV radiation contributes to these population declines. We focused on species-specific differences in the abilities of eggs to repair UV radiation damage to DNA and differential hatching success of embryos exposed to solar radiation at natural oviposition sites. Quantitative comparisons of activities of a key UV-damage-specific repair enzyme, photolyase, among oocytes and eggs from 10 amphibian species were reproducibly characteristic for a given species but varied >80-fold among the species. Levels of photolyase generally correlated with expected exposure of eggs to sunlight. Among the frog and toad species studied, the highest activity was shown by the Pacific treefrog (Hyla regilla), whose populations are not known to be in decline. The Western toad (Bufo boreas) and the Cascades frog (Rana cascadae), whose populations have declined markedly, showed significantly lower photolyase levels. In field experiments, the hatching success of embryos exposed to UV radiation was significantly greater in H. regkla than in R. cascadae and B. boreas. Moreover, in R. cascadae and B. boreas, hatching success was greater in regimes shielded from UV radiation compared with regimes that allowed UV radiation. These observations are thus consistent with the UV-sensitivity hypothesis.
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Papers by A. Blaustein