Assessing effects of non-native crayfish on mosquito survival.

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.

A discrete stage-structured model of California newt population dynamics during a period of drought.

We introduce a mathematical model for studying the population dynamics under drought of the California newt (Taricha torosa), a species of special concern in the state of California. Since 2012, California has experienced a record-setting drought, and multiple studies predict drought conditions currently underway will persist and even increase in severity. Recent declines and local extinctions of California newt populations in Santa Monica Mountain streams motivate our study of the impact of drought on newt population sizes. Although newts are terrestrial salamanders, they migrate to streams each spring to breed and lay eggs. Since egg and larval stages occur in water, a precipitation deficit due to drought conditions reduces the space for newt egg-laying and the necessary habitat for larval development. To mathematically forecast newt population dynamics, we develop a nonlinear system of discrete equations that includes demographic parameters such as survival rates for newt life stages and egg production, which depend on habitat availability and rainfall. We estimate these demographic parameters using 15 years of stream survey data collected from Cold Creek in Los Angeles County, California, and our model captures the observed decline of the parameterized Cold Creek newt population. Based upon data analysis, we predict how the number of available newt egg-laying sites varies with annual precipitation. Our model allows us to make predictions about how the length and severity of drought can affect the likelihood of persistence and the time to critical endangerment of a local newt population. We predict that sustained severe drought will critically endanger the newt population but that the newt population can rebound if a drought is sufficiently short.

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 individual's 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.

Native amphibian toxin reduces invasive crayfish feeding with potential benefits to stream biodiversity.

BACKGROUND: Biodiversity is generally reduced when non-native species invade an ecosystem. Invasive crayfish, Procambarus clarkii, populate California freshwater streams, and in the Santa Monica Mountains (Los Angeles, USA), their introduction has led to trophic cascades due to omnivorous feeding behavior and a rapid rate of population growth. The native California newt, Taricha torosa, possesses a neurotoxin, tetrodotoxin (TTX), that affects freshwater animal behavior. Given P. clarkii has a limited evolutionary history with TTX, we hypothesized that TTX may affect crayfish feeding behaviors. To determine if TTX affects P. clarkii behavior, we measured cumulative movement and various feeding behaviors of P. clarkii exposed to (i) waterborne, ecologically realistic concentrations of TTX (~ 3.0 × 10- 8 moles/L), (ii) an anuran chemical cue to account for intraguild cues, or (iii) a T. torosa chemical cue with quantitated TTX in it (~ 6.2 × 10- 8 moles/L). RESULTS: We found that the presence of TTX in any form significantly reduced crayfish movement and decreased the amount of food consumed over time. Crayfish responses to the anuran treatment did not significantly differ from controls. CONCLUSION: Our laboratory results show that naturally occurring neurotoxin from native California newts limits invasive crayfish foraging and feeding rates, which may play a role in preserving local stream ecosystems by limiting invasive crayfish behaviors that are detrimental to biodiversity.

A natural experiment identifies an impending ecological trap for a neotropical amphibian in response to extreme weather events.

Extreme weather events are predicted to increase as a result of climate change, yet amphibian responses to extreme disturbance events remain understudied, especially in the Neotropics. Recently, an unprecedented windstorm within a protected Costa Rican rainforest opened large light gaps in sites where we have studied behavioral responses of diurnal strawberry poison frogs (Oophaga pumilio) to ultraviolet radiation for nearly two decades. Previous studies demonstrate that O. pumilio selects and defends perches where ultraviolet radiation (UV-B) is relatively low, likely because of the lethal and sublethal effects of UV-B. In this natural experiment, we quantified disturbance to O. pumilio habitat, surveyed for the presence of O. pumilio in both high-disturbance and low-disturbance areas of the forest, and assessed UV-B levels and perch selection behavior in both disturbance levels. Fewer frogs were detected in high-disturbance habitat than in low-disturbance habitat. In general, frogs were found vocalizing at perches in both disturbance levels, and in both cases, in significantly lower UV-B levels relative to ambient adjacent surroundings. However, frogs at perches in high-disturbance areas were exposed to UV-B levels nearly 10 times greater than males at perches in low-disturbance areas. Thus, behavioral avoidance of UV-B may not reduce the risks associated with elevated exposure under these novel conditions, and similarly, if future climate and human-driven land-use change lead to sustained analogous environments.

From Poison to Promise: The Evolution of Tetrodotoxin and Its Potential as a Therapeutic.

Tetrodotoxin (TTX) is a potent neurotoxin that was first identified in pufferfish but has since been isolated from an array of taxa that host TTX-producing bacteria. However, determining its origin, ecosystem roles, and biomedical applications has challenged researchers for decades. Recognized as a poison and for its lethal effects on humans when ingested, TTX is primarily a powerful sodium channel inhibitor that targets voltage-gated sodium channels, including six of the nine mammalian isoforms. Although lethal doses for humans range from 1.5-2.0 mg TTX (blood level 9 ng/mL), when it is administered at levels far below LD50, TTX exhibits therapeutic properties, especially to treat cancer-related pain, neuropathic pain, and visceral pain. Furthermore, TTX can potentially treat a variety of medical ailments, including heroin and cocaine withdrawal symptoms, spinal cord injuries, brain trauma, and some kinds of tumors. Here, we (i) describe the perplexing evolution and ecology of tetrodotoxin, (ii) review its mechanisms and modes of action, and (iii) offer an overview of the numerous ways it may be applied as a therapeutic. There is much to be explored in these three areas, and we offer ideas for future research that combine evolutionary biology with therapeutics. The TTX system holds great promise as a therapeutic and understanding the origin and chemical ecology of TTX as a poison will only improve its general benefit to humanity.

Amphibian responses in the aftermath of extreme climate events.

Climate change-induced extinctions are estimated to eliminate one in six known species by the end of the century. One major factor that will contribute to these extinctions is extreme climatic events. Here, we show the ecological impacts of recent record warm air temperatures and simultaneous peak drought conditions in California. From 2008-2016, the southern populations of a wide-ranging endemic amphibian (the California newt, Taricha torosa) showed a 20% reduction to mean body condition and significant losses to variation in body condition linked with extreme climate deviations. However, body condition in northern populations remained relatively unaffected during this period. Range-wide population estimates of change to body condition under future climate change scenarios within the next 50 years suggest that northern populations will mirror the loss of body condition recently observed in southern populations. This change is predicated on latter 21st century climate deviations that resemble recent conditions in Southern California. Thus, the ecological consequences of climate change have already occurred across the warmer, drier regions of Southern California, and our results suggest that predicted climate vulnerable regions in the more mesic northern range likely will not provide climate refuge for numerous amphibian communities.

Quantifying climate sensitivity and climate-driven change in North American amphibian communities.

Changing climate will impact species' ranges only when environmental variability directly impacts the demography of local populations. However, measurement of demographic responses to climate change has largely been limited to single species and locations. Here we show that amphibian communities are responsive to climatic variability, using >500,000 time-series observations for 81 species across 86 North American study areas. The effect of climate on local colonization and persistence probabilities varies among eco-regions and depends on local climate, species life-histories, and taxonomic classification. We found that local species richness is most sensitive to changes in water availability during breeding and changes in winter conditions. Based on the relationships we measure, recent changes in climate cannot explain why local species richness of North American amphibians has rapidly declined. However, changing climate does explain why some populations are declining faster than others. Our results provide important insights into how amphibians respond to climate and a general framework for measuring climate impacts on species richness.

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.

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

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.

Aquatic invasive species: challenges for the future.

Humans have effectively transported thousands of species around the globe and, with accelerated trade; the rate of introductions has increased over time. Aquatic ecosystems seem at particular risk from invasive species because of threats to biodiversity and human needs for water resources. Here, we review some known aspects of aquatic invasive species (AIS) and explore several new questions. We describe impacts of AIS, factors limiting their dispersal, and the role that humans play in transporting AIS. We also review the characteristics of species that should be the greatest threat for future invasions, including those that pave the way for invasions by other species ("invasional meltdown"). Susceptible aquatic communities, such as reservoirs, may serve as stepping stones for invasions of new landscapes. Some microbes disperse long distance, infect new hosts and grow in the external aquatic medium, a process that has consequences for human health. We also discuss the interaction between species invasions and other human impacts (climate change, landscape conversion), as well as the possible connection of invasions with regime shifts in lakes. Since many invaders become permanent features of the environment, we discuss how humans live with invasive species, and conclude with questions for future research.

Impact of chaparral wildfire-induced sedimentation on oviposition of stream-breeding California newts (Taricha torosa).

We examined the effects of chaparral wildfire on stream-breeding California newts (Taricha torosa) in a 750-m stretch of a perennial Santa Monica Mountain stream (Los Angeles County). Detailed field surveys of 1992 and 1993 established the composition (run, riffle, pool) of this habitat and determined the oviposition sites of newts. We also quantified California newt egg mass density and estimated the density of newt adults. A chaparral wildfire burned the entire study site on 2 November 1993. Using the same methods, we collected field survey data in 1994 and 1996. Erosion following the 1993 wildfire produced major changes in stream morphology and composition. Pools and runs represented approximately 40-50% of pre-fire stream area. In the spring following the fire, the stream consisted of less than 20% run and pool. Pools that did remain were often smaller and shallower. The average density of adult California newts did not differ among years. The total number of newt egg masses observed in the spring after the fire was approximately one-third of egg mass counts from pre-fire surveys. Most California newt egg masses were laid in pools and runs; California newts prefer deeper slow-moving water. We conclude that fire-induced landslides and siltation have eliminated pools and runs, thus reducing the amount of habitat suitable for oviposition. Habitat alterations caused by fire likely account for the observed reduction of egg masses at the stream.

Quantifying tetrodotoxin levels in the California newt using a non-destructive sampling method.

Toxic or noxious substances often serve as a means of chemical defense for numerous taxa. However, such compounds may also facilitate ecological or evolutionary processes. The neurotoxin, tetrodotoxin (TTX), which is found in newts of the genus Taricha, acts as a selection pressure upon predatory garter snakes, is a chemical cue to conspecific larvae, which elicits antipredator behavior, and may also affect macroinvertebrate foraging behavior. To understand selection patterns and how potential variation might affect ecological and evolutionary processes, it is necessary to quantify TTX levels within individuals and populations. To do so has often required that animals be destructively sampled or removed from breeding habitats and brought into the laboratory. Here we demonstrate a non-destructive method of sampling adult Taricha that obviates the need to capture and collect individuals. We also show that embryos from oviposited California newt (Taricha torosa) egg masses can be individually sampled and TTX quantified from embryos. We employed three different extraction techniques to isolate TTX. Using a custom fabricated high performance liquid chromatography (HPLC) system we quantified recovery of TTX. We found that a newly developed micro-extraction technique significantly improved recovery compared to previously used methods. Results also indicate our improvements to the HPLC method have high repeatability and increased sensitivity, with a detection limit of 48 pg (0.15 pmol) TTX. The quantified amounts of TTX in adult newts suggest fine geographic variation in toxin levels between sampling localities isolated by as little as 3 km.

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.

The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses.

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.