Explanation for missing limbs in deformed amphibians

Ballengée, Brandon; Sessions, Stanley K.

doi:10.1002/jez.b.21296

Cited by 49 publications

(65 citation statements)

References 33 publications

(19 reference statements)

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“…Based on these results, we predict that warmer and more degraded water quality-conditions projected to occur under global change scenarios-will cause dragonfly predators to have greater capture success for L. sylvaticus tadpole prey. Although nonfatal attacks may not directly decrease tadpole populations, they can cause injuries and malformations that may also be detrimental to survival (Ballengée and Sessions 2009, Reeves et al 2010). …”

Section: Discussionmentioning

confidence: 99%

Thrice as easy to catch! Copper and temperature modulate predator‐prey interactions in larval dragonflies and anurans

Hayden

Reeves

Holyoak³

et al. 2015

Ecosphere

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Abstract. Amphibians are important indicators of environmental health, and their populations are in worldwide decline. The causes of these declines are diverse and not well understood. In some cases multiple stressors and complex causal mechanisms have been identified. Experimental studies have shown that contaminants can cause the failure of Lithobates sylvaticus tadpoles to initiate predator avoidance behaviors, potentially leading to increased tadpole capture and injury. Copper is a contaminant known to negatively affect amphibians and other aquatic organisms at sub-lethal levels. Mining waste, certain pesticides, vehicle exhaust and brake pad dust are sources of copper, which can enter hydrologic systems through runoff. Additionally, temperature is known to influence predator-prey interactions of ectotherms and is predicted to rise in some areas as climate changes. We examined how copper and temperature affected behavior and predation dynamics between an odonate predator (Aeshna sitchensis) and larval L. sylvaticus prey. We found that sublethal concentrations of copper near the analytical detection limits for this element (1.85 lg Cu/L) significantly reduced tadpole and odonate activity. Above-average temperatures (228C) significantly increased tadpole activity and decreased dragonfly activity, compared with ambienttemperature treatments (178C). These behavioral responses culminated in an approximately three-fold increase in the number of dragonfly attacks on tadpoles in the elevated-temperature, copper-exposed treatments. We suggest that increased concentrations of dissolved copper and elevated water temperatures are harmful to amphibian prey through maladaptive behavioral responses in the presence of predators.

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Section: Discussionmentioning

confidence: 99%

Thrice as easy to catch! Copper and temperature modulate predator‐prey interactions in larval dragonflies and anurans

Hayden

Reeves

Holyoak³

et al. 2015

Ecosphere

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“…A lack of bottom preference may make Cu-intoxicated tadpoles more vulnerable to attack from odonate predators like the climbing libellulid dragonflies, which hunt visually, clinging to vegetation below the water surface (Pritchard 1965). This type of odonate specifically has been shown to cause amphibian limb malformations by preferentially chewing the hind limbs off of tadpoles during non-lethal attacks (Ballengée and Sessions 2009). …”

Section: Discussionmentioning

confidence: 99%

“…We followed up on an earlier study in which we found strong correlations between chemical contaminants, odonate predators and the occurrence of limb abnormalities in frogs . The causes of limb abnormalities in general are a current and controversial topic (Ballengée and Sessions 2009, Sessions and Ballengée 2010, Skelly and Benard 2010. Possible causes include parasites, predators, UV-B, and contaminants (reviewed in .…”

Section: Introductionmentioning

confidence: 99%

“…High frequencies of abnormalities in sites lacking R. ondatrae have been correlated with aquatic predators, which may amputate the developing limbs of tadpoles as they prey on them Sessions 2009, Bowerman et al 2010), Reeves et al 2010). Because amputated limbs regenerate only partially before metamorphosis, tadpole limb amputations can cause shrunken or missing limbs in post-metamorphic frogs (Fry 1966, Ballengée and Sessions 2009. Nevertheless, the predator hypothesis is controversial because aquatic pred-ators are common in amphibian breeding habitats, yet frogs with missing or shrunken limb abnormalities are not so widely distributed , Sessions and Ballengée 2010, Skelly and Benard 2010.…”

Section: Introductionmentioning

confidence: 99%

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Twice as easy to catch? A toxicant and a predator cue cause additive reductions in larval amphibian activity

et al. 2011

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Abstract. Toxicants may harm predators or prey differentially, hindering clear determination of multiple stressor effects on predation dynamics in polluted aquatic systems. We built on a prior field study in which we demonstrated that a chemical contaminant, copper (Cu) and odonate predators were correlated with more frequent observations of skeletal abnormalities in Alaskan wood frog (Rana sylvatica) tadpoles. Our prior study established a multiple stressor effect linked to an important environmental phenomenon (malformed amphibians) but did not provide clear mechanisms that might guide management. We here investigated behavioral mechanisms because of their potential to produce large changes in predation dynamics, and because in published studies low concentrations of Cu produced behavioral changes in predator-detection in fish. Surprisingly, low but environmentally relevant concentrations of Cu (5 lg/L) combined with chemical cues from a predator (Aeshna sitchensis) to produce large changes in the behavior of larval amphibians. Experiments demonstrated that a low concentration of Cu did not inhibit the ability of wood frog tadpoles to detect chemical cues of predators by olfactory means, but produced strong behavioral effects, causing tadpoles to reduce activity and alter microhabitat use. These results occurred with Cu at an exposure level lower than any we could find reported as toxic to amphibians in the literature. When Cu and predator cues were administered together, the activity reduction was additive and stronger at earlier life stages. We suggest that Cu intoxication would be disadvantageous to larval amphibian prey with prolonged exposure to predators during development, and we present field data from 2010 that support this assertion. Our study demonstrates the need to use sensitive behavioral assays and to investigate multiple stressor mechanisms to understand how multiple threats combine to affect organisms in nature.Key words: Alaska; amphibian; copper; frog; Lithobates sylvaticus; multiple stressor; predator; toxicity; trait-mediated interaction; Rana sylvatica.

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“…Instead, biotic interactions and environmental factors are often highlighted as the cause. Predation can give rise to deformities due to problems in the regeneration process (epimorphosis) following trauma (Ballengée Sessions, 2009). Equally, infection by teratogenic viruses, fungi and other parasites have been associated with the emergence of deformities.…”

mentioning

confidence: 99%

From a local observation to a European-wide phenomenon: Amphibian deformities at Serra da Estrela Natural Park, Portugal

Laurentino¹,

Pais²,

Rosa

2016

Basic Appl Herpetol

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In the last decades increasing records of morphological abnormalities in many amphibian populations have become subject of scientific interest. Once considered a mere curiosity, this worldwide phenomenon has been highlighted as a potential local conservation issue, for it appears to be yet another threat to amphibian diversity. Our study reports the first cases of amphibian deformities for North-Central Portugal, which are put in context with a review comprising European records since the 18 th century. Amphibian populations (Lissotriton boscai, Triturus marmoratus and Pelophylax perezi) were sampled for four sampling years at Serra da Estrela Natural Park. With approximately 1400 post-metamorphic individuals examined, we found 12 cases of deformity including anophtalmy, brachydactyly, ectrodactyly, ectomely, polydactyly and polyphalangy. Deformity prevalence varied between years and species, rarely exceeding 2%. Our results are in accordance with European trends, since the majority of the recorded cases were found in limbs of urodeles. The presence of deformities in three different species points toward environmental causes, with predation as the most parsimonious explanation. Although not alarming, we reinforce the need for continuous monitoring of amphibian communities, from an interdisciplinary perspective, since even protected and pristine areas are not immune to new emerging threats that can act in synergy. Key words: Lissotriton boscai; malformations; morphology; Pelophylax perezi; Triturus marmoratus.De una observación local a un fenómeno paneuropeo: malformaciones de anfibios en el Parque Natural de la Serra da Estrela, Portugal. Durante las últimas décadas, el creciente número de registros de malformaciones morfológicas en anfibios ha suscitado el interés de la comunidad científica. Si bien al principio este fenómeno se consideraba apenas por mera curiosidad, el hecho de que se repita en todo el planeta lo ha convertido en un asunto de interés para la conservación a nivel local al postularse como una amenaza para la diversidad de anfibios. Nuestro estudio

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Explanation for missing limbs in deformed amphibians

Cited by 49 publications

References 33 publications

Thrice as easy to catch! Copper and temperature modulate predator‐prey interactions in larval dragonflies and anurans

Thrice as easy to catch! Copper and temperature modulate predator‐prey interactions in larval dragonflies and anurans

Twice as easy to catch? A toxicant and a predator cue cause additive reductions in larval amphibian activity

From a local observation to a European-wide phenomenon: Amphibian deformities at Serra da Estrela Natural Park, Portugal

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