The role of Climate Change in creating "plastic" amphibians

What does it mean to be plastic?

Plasticity refers to the variation in phenotypes under certain environmental conditions. This means that

one genotype can translate into multiple phenotypes based on the environment. Phenotypic plasticity is widespread in nature, and can significantly alter the relationship between organisms and their [abiotic and biotic] environment¹.

Figure 1 shows how juvenile grasshoppers (S. lineata) express density-dependent phenotypic plasticity in coloration.

The evolution of plasticity

The profile of phenotypes produced by a genotype across environments is known as the “norm of reaction”. It is often described by a curve that relates the contribution of environmental variation to the observed phenotype.

The level of phenotypic response to environmental change is determined by natural selection and can allow a given species to exploit novel environments or provide protection from others.² Just as in any heritable trait, genetic variation is required for the evolution of plasticity. Optimal norms of reaction can be achieved, but similar to Simpson’s Adaptive Landscape, they are dependent upon the ratio of selection and mutation and the amount of genetic variation available.

Why are amphibians a good model for evolutionary studies, particularly plasticity?

Figure 3 shows the typical amphibian life cycle from egg (embryo) to developing tadpole to emerging adult frog. Of course we cannot forget about the under-represented salamanders and caecilians, whose life cycles are very similar to that of frogs. Amphibians have evolved numerous unique characteristics that make their ecological role multi-dimensional.

First, they have a biphasic life cycle in which the developing embryonic and larval forms are directly associated with aquatic environments. Post-development, they emerge from these aquatic systems to become terrestrial breeding adults [there are cases in which this biphasic cycle does not hold true – e.g. Pacific Giant Salamanders!]. This lifestyle requires the individual to be adaptive to multiple interacting ecosystems within a single lifetime; making them both extremely vulnerable, and yet resilient, to environmental change.

Second, amphibian skin is highly permeable and their eggs can readily absorb substances from the environment due to lack of a hard shell. They are able to absorb water and oxygen directly through their skin, thus their reliance on moist environments to prevent desiccation. Because of their permeability in all life stages, amphibians are extremely vulnerable to environmental contamination via pesticides, herbicides, disease, and other contaminants, and are consequently used as indicators of ecosystem health. Their tendency to dry up like a prune in the absence of moisture and their ectothermic life histories make them additionally vulnerable to climatic changes in precipitation and temperature.

Ecologists have long been interested in the way in which environmental factors influence the growth and development of amphibians. So what are the factors that go into making the decision of when and how quickly to metamorphose?

· Temperature

· Hydroperiod

· Resource levels

· Competition

· Predation

· Water quality

Amphibians have been documented plastically increasing larval development rate in response to increases in these environmental stressors. Fascinating! Let’s look at some examples of phenotypic plasticity in amphibians, and discuss why this is relevant.

Examples of phenotypic plasticity in amphibians...

Couch’s Spadefoot (Scaphiopus couchii)

In Southern Arizona’s hot desert environment, there is strong selection pressure on these tadpoles to increase rates of development and minimize the length of development since the late summer monsoon season is so short. In addition to the short wet season, tadpole densities are often very high and there is considerable competition for limited food resources. When temperatures become exceedingly high and the ponds begin to dry, these toads will plastically increase their development rate to emerge as juveniles before food, space, and water runs out³.

Plains Leopard Frog (Rana blairi) and Southern Leopard Frog (Rana sphenocephala)

The effect of hydroperiod on larval growth, development, and survival was used to assess response to a drying aquatic environment for both of these species. The Plains Leopard Frog occurs throughout the Great Plains and into the Midwest. Declines have been reported throughout its range, largely due to the conversion of wetlands to agriculture. The Southern Leopard Frog is found throughout the Southeastern US and is known to be very adaptable to many freshwater habitats.

Interestingly, regardless of their broad distributions and generalist tendencies, both species plastically reduced larval period lengths when exposed to a drying environment⁴. Thus, we are noticing much diversity in the types of amphibians able to adjust their life histories in response to changing environmental conditions.

Mole Salamander (Ambystoma talpoideum)

Much less work has been done on responses of salamander larvae to pond drying, in part because most salamanders do not breed in highly ephemeral habitats. One of the only detailed experimental studies to date involved the effect of pond drying on larval development in Mole Salamanders, a species that breeds in the Carolina bays and other shallow temporary ponds. Reproductive success varied spatially and temporally, but most larval mortality occurred in those ponds that dried early. Individuals able to rapidly metamorphose before pond drying were significantly smaller than their relatives who were ‘living it up’ in constant water⁵. Thus, trade-offs may exist in a species ability to plastically respond to environmental stress and maintain the necessary growth trajectories to sustain life on land.

What about amphibians of the Pacific Northwest? Can plastic traits make some species more adaptable to rapid environmental change (i.e. Climate Change)?

In the Pacific Northwest, changes to freshwater ecosystems as a result of climate change are predicted to increase amphibian extinction rates and impose new challenges for conservationists⁶. The consequences of shifting climate conditions (e.g. earlier snowmelt, higher ambient temperatures, and variable precipitations patters) on amphibian populations utilizing freshwater systems occur concomitantly with other environmental stressors such as disease, UV-B radiation, and invasive species.

Climate models predict extreme seasonal cycles that will lead to decreased water availability in the Pacific Northwest due to declining snowpack levels and significant temperature increases⁷. This trend is most pronounced in the Cascade Mountain Range, which will likely see substantial alterations in regional hydrology⁸. For high-elevation amphibian species, these effects combined with extreme UV-B conditions, are expected to result in population declines and/or species range shifts⁹. However, many amphibian species are able to plastically alter life history traits, such as breeding phenology and larval development rate, and thus may exhibit optimal strategies for resisting synergistic environmental stressors.

Who are the players?

I am using a combination of field surveys, experiments, and modeling to provide a comprehensive analysis of the interactive effects of temperature, hydroperiod, and other environmental stressors on a high-elevation, geographically-restricted amphibian assemblage. This amphibian group consists of four high-elevation species that vary in taxonomic diversity, habitat use, and conservation issues: Cascades Frog (Rana cascadae), Western Toad (Bufo boreas), Pacific Chorus Frog (Pseudacris regilla), and Long-toed Salamander (Ambystoma macrodactylum) (see Figure 4 for distribution maps).

How can we test plasticity in response to climate change?

I want to determine if the combination of these stressors results in non-intuitive responses in species distribution, abundance, and larval development. In other words, can this group of amphibians plastically increase larval development rates in a drying environment with multiple environmental stressors making their situation even worse? Based on this answer and available climate models, I can determine how their distributions and abundances will change at the landscape-level throughout the Cascade Range.

I predict that amphibian diversity will be associated with seasonal water availability and that species with plastic larval development rates will be more resilient to the synergistic impacts of climate change and other environmental stressors, thus persisting in predicted refugia.

To test these predictions I am using 3 distinct methodologies:

1. Field surveys to document presence and absence of amphibian species throughout the Cascade Mountains of Oregon and Washington. Occupancy patterns of sites with varied seasonal water retention (i.e. ephemeral) will be compared to permanent waterbodies in the same watershed. Data collection over multiple breeding seasons will allow me to test for correlations between species occupancy and habitat characteristics.
2. A mesocosm experiment to test if larvae can plastically increase development rate in response to synergistic stressors. Treatments with multiple stressors (especially high UV-B radiation levels and ephemeral hydroperiods) are expected to result in rapid development but smaller body size at metamorphosis and decreased survivorship, compared to treatments with a single stressor.
3. Bioclimatic envelope models to predict climate-driven changes in ecological conditions and amphibian species distributions in the Cascades. Baseline temperature and hydroperiod conditions will be established using temperature and pressure sensors throughout high-elevation breeding sites (deployed during initial field survey). I will then integrate historical and real time climate data from the PRISM and SNOTEL datasets into a RHESSys model to predict water fluxes as a result of changes in seasonal snowpack. I will also apply a bioclimatic model to define the abiotic conditions (climate envelope) in which each of the 4 representative species can exist based on parameter estimates from the mesocosm experiment and modeled occupancy patterns.

These variables will be combined with predicted future climate scenarios from a general circulation model to project potential range shifts. In areas predicted to experience significant climatic changes, I will assess probabilities for amphibian population persistence in predicted refugia given their specific tolerance and avoidance strategies. Given adequate genetic diversity and potential for rapid adaptation, those populations with the characteristics that allow them to cope with the synergistic environmental stressors associated with climate change will likely persist. Alternatively, those species incapable of rapid adaptation in response to altered water availability and increased environmental stress may experience greater population declines and subsequent range contractions.

Management Implications and the future of PNW amphibian species…

Montane studies on global amphibian population decline have generally been scarce and poorly documented, but show a general trend in range contractions upward in elevation and latitude. The rapid loss of habitable climate space has resulted in a disproportionate number of extinctions in mountain-restricted amphibian species¹¹. Consequently the lack of available information on species susceptibility and adaptability confers the need for rapid data acquisition and the immediate implementation of conservation measures.

The conservation of amphibian diversity in available wetland refugia at high-elevations will require a collaborative, ecosystem-based approach to management. Practical adaptive management will require the identification of vulnerable habitats and species using multiple analytical techniques as previously described. The restricted geographic scale at which most amphibians exist provides some unique opportunities for management intervention. Localized actions designed to minimize the loss of amphibians will require intensive monitoring, predictive modeling, and enhanced communication among scientists and citizens.

By incorporating multiple modeling and experimental techniques, I will highlight the feasibility and effectiveness of fast-tracking the application of general adaptive management principles targeted towards freshwater ecosystems. Results from this project will provide a diverse assessment of multi-species differences in synergistic stress response and contribute a baseline analysis of the future of geographically-restricted species in the Pacific Northwest.

Garcia Lab Website, OSU Dept. of Fisheries & Wildlife

http://fw.oregonstate.edu/labs/garcia_lab/

References:

1. Miner, B.G., et al. 2005. Ecological consequences of phenotypic plasticity. TREE 20(12): 685-692.
2. Via, S. and R. Lande. 1985. Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39(3) 505-522.
3. Newman, R. A. 1988. Adaptive plasticity in development of Scaphiopus couchii tadpoles in desert ponds. Evolution 42: 774-783.
4. Parris, M.J. 2000. Experimental analysis of hybridization in leopard frogs (Anura: Ranidae) larval performance in desiccating environments. Copeia 2000: 11-19.
5. Semlitsch, R.D., and H.M. Wilbur. 1988. Effects of pond drying time on metamorphosis and survival in the salamander Ambystoma talpoideum. Copeia 1988: 978-983.
6. Nel, J., et al. 2009. Progress and challenges in freshwater conservation planning. Aquatic Conserv: Mar. Freshw. Ecosyst. 19: 474–485.
7. Mote, P. and E. Salathé. 2010. Future climate in the Pacific Northwest. Climatic Change 102: 29-50.
8. Mote, P. 2003. Trends in snow water equivalent in the Pacific Northwest and their climatic causes. Geophys Res Lett 30: 1601-1604.
9. Blaustein, A., et al. 2010. Direct and Indirect Effects of Climate Change on Amphibian Populations. Diversity 2: 281-313.
10. Blackburn, et al. (2001) US Amphibian Dist. Maps (http://home.bsu.edu/home/00mjlannoo/)
11. Parmesan, C. 2006. Ecological and Evolutionary Responses to Recent Climate ChangeAnnu. Rev. Ecol. Evol. Syst. 37: 637–69