Gary M. Bucciarelli

Invasion Complexities: The Diverse Impacts of Nonnative Species on Amphibians

Since the first documented declines of amphibian species, researchers have learned how nonnative species can depress amphibian populations and lead to local extinctions. Here, we explore the dimensions of invasions in the context of evolutionary history, anthropogenic disturbance, and climate change. Recent studies indicate that the nonnative groups that have most negatively affected amphibians are plants, fishes, and other amphibians. We review current work aimed at determining the direct and indirect effects of nonnative species on amphibian health, genotypes, and native ecosystem structure, as well as research examining invasions from a community level perspective. We also describe synergistic effects between abiotic, biotic, and nonnative factors. Recent studies have documented the intricacies of invasions and how numerous aspects of invasions can interact additively and complementarily to the detriment of the native ecosystem. Understanding the complexity of invasions means considering if and how biological, environmental, and ecological processes within ecosystems are being reshaped as a result of introduced species. Assessing the ecology and ecosystem dynamics of invasions at multiple levels, from the genome to the ecosystem, is paramount to the conservation, restoration, and future research of invaded amphibian ecosystems.

Individual fluctuations in toxin levels affect breeding site fidelity in a chemically defended amphibian.

Behaviours that influence habitat selection strongly determine species movement patterns. One component of animal behaviour that largely influences movement patterns and habitat choice is site fidelity. California newts (family Salamandridae) demonstrate remarkable site fidelity, typically homing to the same pool of a stream each breeding season. Individuals often occupy a specific pool throughout the breeding season, but some males shift among breeding pools, altering their set of potential mates, competitors, and predators. In this study, we measured dermal concentrations of the chemical defence compound tetrodotoxin (TTX) in recaptured male California newts (Taricha torosa) over five breeding seasons to evaluate whether relative TTX concentrations are associated with breeding site fidelity in the field. Our five years of field sampling indicates that TTX concentrations of individuals and group means fluctuate tremendously, implying that TTX is not a stable phenotypic trait. Despite such fluctuations, we found that an individuals relative TTX concentration explains fidelity to a breeding pool and suggests that newts may be able to assess both their own concentrations of TTX and that of conspecifics to make decisions about remaining in or abandoning a breeding pool. These results provide us a novel dimension to chemical defence phenotypes in nature and their ecological consequences, potentially requiring a re-evaluation of the coevolutionary dynamics of predation pressure on toxin-laden organisms.

Ultraviolet Radiation Influences Perch Selection by a Neotropical Poison-Dart Frog

Ambient ultraviolet-B radiation can harm amphibian eggs, larvae and adults. However, some amphibians avoid UV-B radiation when given the opportunity. The strawberry poison dart frog, Oophaga pumilio, is diurnal and males vocalize throughout the day in light gaps under forest canopies that expose them to solar radiation. Previous studies have demonstrated that males calling from high perches are more successful at mating than those at lower perches. We investigated whether frogs at higher perches receive more ultraviolet-B than those calling from lower perches. We also investigated whether frogs on perches receiving relatively low ultraviolet-B levels maintained their positions for longer compared to individuals calling from perches receiving higher levels of ultraviolet-B. Finally, since it has been hypothesized that some animals utilize levels of UV-A as a visual cue to avoid UV-B damage, we artificially elevated ultraviolet-A levels to examine whether males exposed to artificially elevated ultraviolet-A abandoned their perches sooner compared to males exposed to visible light. We found that frogs called from perches receiving low ultraviolet-B regardless of perch height, and that frogs maintain their positions longer on perches receiving low ultraviolet-B compared to perches receiving even slightly higher ultraviolet-B levels. Exposing the frogs to artificially elevated levels of ultraviolet-A radiation caused males to move off of their perches faster than when they were exposed to a control light source. These experiments suggest that ultraviolet radiation plays an important role in frog behavior related to perch selection, even in rainforests where much of the solar radiation is shielded by the forest canopy.

Effects of newt chemical cues on the distribution and foraging behavior of stream macroinvertebrates

AbstractMany amphibians possess noxious or toxic substances for self defense. These compounds have been characterized largely as chemical defenses, but may promote ecological and evolutionary processes. The California newt, Tarichatorosa, possesses a potent neurotoxin, tetrodotoxin (TTX), which serves as a chemical defense, chemical cue to conspecifics, and selection pressure that has selected for evolved resistance in a predator. However, the potential effects of TTX upon the broader community and on behavior, in general, have been overlooked. Field assays conducted during the newt breeding season indicate that the macroinvertebrate community responds to adult newt chemical cues by altering foraging behavior. In these assays, significantly fewer macroinvertebrates were found in experimental areas with enclosed newts relative to enclosures with a non-predatory amphibian. Laboratory bioassays showed that dragonfly nymphs (Anax junius) reduced predatory behavior and moved less in the presence of adult newt chemical cues. When exposed to TTX, nymph mean angular velocities were reduced four fold and mean velocity magnitude was reduced threefold relative to controls. Overall, these results support the hypothesis that chemical stimuli from predators, and TTX specifically, can shape species interactions at lower trophic levels and potentially affect community organization.

Noxious newts and their natural enemies: experimental effects of tetrodotoxin exposure on trematode parasites and aquatic macroinvertebrates

ABSTRACT The dermal glands of many amphibian species secrete toxins or other noxious substances as a defense strategy against natural enemies. Newts in particular possess the potent neurotoxin tetrodotoxin (TTX), for which the highest concentrations are found in species within the genus Taricha. Adult Taricha are hypothesized to use TTX as a chemical defense against vertebrate predators such as garter snakes (Thamnophis spp.). However, less is known about how TTX functions to defend aquatic‐developing newt larvae against natural enemies, including trematode parasites and aquatic macroinvertebrates. Here we experimentally investigated the effects of exogenous TTX exposure on survivorship of the infectious stages (cercariae) of five species of trematode parasites that infect larval amphibians. Specifically, we used dose‐response curves to test the sensitivity of trematode cercariae to progressively increasing concentrations of TTX (0.0 [control], 0.63, 3.13, 6.26, 31.32, and 62.64 nmol L−1) and how this differed among parasite species. We further compared these results to the effects of TTX exposure (0 and 1000 nmolL−1) over 24 h on seven macroinvertebrate taxa commonly found in aquatic habitats with newt larvae. TTX significantly reduced the survivorship of trematode cercariae for all species, but the magnitude of such effects varied among species. Ribeiroia ondatrae – which causes mortality and limb malformations in amphibians – was the least sensitive to TTX, whereas the kidney‐encysting Echinostoma trivolvis was the most sensitive. Among the macroinvertebrate taxa, only mayflies (Ephemeroptera) showed a significant increase in mortality following exogenous TTX exposure, despite the use of a concentration 16x higher than the maximum used for trematodes. Our results suggest that maternal investment of TTX into larval newts may provide protection against certain trematode infections and highlight the importance of future work assessing the effects of newt toxicity on both parasite infection success and the palatability of larval newts to invertebrate predators. HIGHLIGHTSTrematode cercariae exposed to tetrodotoxin all exhibited reduced survivorship.Trematodes survivorship varied, Ribeiroia ondatrae was the least sensitive to TTX.Host toxicity may decrease infection in naturally occurring populations.Of macroinvertebrates, only mayflies showed a decrease in survivorship to TTX.Maternal investment of TTX into newts may provide protection against trematodes.

An amphibian chemical defense phenotype is inducible across life history stages

Inducible phenotypic responses to environmental variation are ubiquitous across the tree of life, but it remains an open question whether amphibian chemical defense phenotypes are inducible. Tetrodotoxin (TTX) is a key chemical defense trait in North American and Eurasian newts (Salamandridae). We tested if TTX can be induced by exposing populations of adult and larval California newts (Taricha torosa) to sustained stressful conditions while longitudinally quantifying TTX concentrations. Adult newts rapidly increased chemical defenses in response to simulated predator attacks and consistently maintained elevated TTX concentrations relative to wild, non-captive individuals. We also found that laboratory-reared larvae maintained chemical defenses nearly three-fold greater than those of siblings reared in streams. Collectively, our results indicate that amphibian chemical defenses are not fixed. Instead, toxins are maintained at a baseline concentration that can quickly be increased in response to perceived risk with substantial increases to toxicity. Therefore, it is crucial that inducible variation be accounted for when considering ecological dynamics of chemically defended animals and coevolutionary predator-prey and mimic-model relationships.

The effect of newt toxin on an invasive snail

Invasive species are well documented to impact native species where they are introduced. In the Santa Monica Mountains, a native species of amphibian, the California newt (Taricha torosa) possesses a neurotoxin, tetrodotoxin (TTX) that is considered a chemical defense against predation but also appears to facilitate ecological processes and specifically affect freshwater macroinvertebrate behavior. A recently introduced invasive species, the New Zealand mud snail (Potamopyrgus antipodarum), is known to negatively affect ecosystems it invades and means to control its proliferation once introduced are limited. Given the ecological role of newt neurotoxin, we hypothesized that TTX may impact P. antipodarum behavior and tested its effects upon snail movement in laboratory assays and in-stream experiments. When snails were exposed to ecologically realistic TTX concentrations and newt chemical cues that contain TTX they moved significantly less and distance was significantly reduced relative to controls. In a natural stream, significantly more P. antipodarum moved out of areas exposed to newt chemical cues relative to snails in the presence of native tree frog cues (Pseudacris cadaverina). Our results suggest that California newts may help limit the spread of P. antipodarum in streams where T. torosa is both able to persist and possess adequate chemical defenses.

The rainbow trout is affecting the occupancy of native amphibians in Patagonia

In this work, we assessed the occupancy of two native amphibian species of the Valcheta stream in the Somuncura Plateau, northern Patagonia: the Valcheta frog, Pleurodema somuncurense and the Argentine common toad, Rhinella arenarum. We hypothesized that the occupancy of both amphibian species will be shaped by the presence of trout; we also expected a decline in occupancy assuming that the new predator in the system will affect native amphibian populations. Between December 2014 and March 2015, we conducted surveys in 148 sites along the headwaters of Valcheta stream. We modelled the occupancy by including the presence of trout, the temperature of water and the coverage of rocks and vegetation as site-habitat covariates. Models including trout were among the best ranked for both amphibian species. The presence of trout reduced the occupancy of both species and the magnitude of this reduction was much higher in the Valcheta frog than in the Argentine common toad. Overall, our results are of great relevance for land managers considering that the Valcheta frog is among the only three IUCN Critically Endangered amphibians in Argentina.

Assessing effects of nonnative crayfish on mosquito survival: Mosquito Predators

Introductions of non-native predators often reduce biodiversity and affect natural predator-prey relationships and may increase the abundance of potential disease vectors (e.g., mosquitoes) indirectly through competition or predation cascades. The Santa Monica Mountains (California, U.S.A.), situated in a global biodiversity hotspot, is an area of conservation concern due to climate change, urbanization, and the introduction of non-native species. We examined the effect of non-native crayfish (Procambarus clarkii) on an existing native predator, dragonfly nymphs (Aeshna sp.), and their mosquito larvae (Anopheles sp.) prey. We used laboratory experiments to compare the predation efficiency of both predators, separately and together, and field data on counts of dragonfly nymphs and mosquito larvae sampled from 13 local streams. We predicted a lower predation efficiency of crayfish compared with native dragonfly nymphs and a reduced predation efficiency of dragonfly nymphs in the presence of crayfish. Dragonfly nymphs were an order of magnitude more efficient predators than crayfish, and dragonfly nymph predation efficiency was reduced in the presence of crayfish. Field count data showed that populations of dragonfly nymphs and mosquito larvae were strongly correlated with crayfish presence in streams, such that sites with crayfish tended to have fewer dragonfly nymphs and more mosquito larvae. Under natural conditions, it is likely that crayfish reduce the abundance of dragonfly nymphs and their predation efficiency and thereby, directly and indirectly, lead to higher mosquito populations and a loss of ecosystem services related to disease vector control.