17. Greenberg, DA; Palen, WJ. (2021) Hydrothermal physiology and climate vulnerability in amphibians.Proc. R. Soc. B-Biol. Sci. 288 Hydrothermal physiology and climate vulnerability in amphibians
dehydration; desiccation; ecophysiology; frogs; global change; thermal performance
Concerns over the consequences of global climate change for biodiversity have spurred a renewed interest in organismal thermal physiology. However, temperature is only one of many environmental axes poised to change in the future. In particular, hydrologic regimes are also expected to shift concurrently with temperature in many regions, yet our understanding of how thermal and hydration physiology jointly affect performance and fitness is still limited for most taxonomic groups. Here, we investigated the relationship between functional performance, hydration state and temperature in three ecologically distinct amphibians, and compare how temperature and water loss can concurrently limit activity under current climate conditions. We found that performance was maintained across a broad range of hydration states in all three species, but then declines abruptly after a threshold of 20-30% mass loss. This rapid performance decline was accelerated when individuals were exposed to warmer temperatures. Combining our empirical hydrothermal performance curves with species-specific biophysical models, we estimated that dehydration can increase restrictions on species' activity by up to 60% compared to restriction by temperature alone. These results illustrate the importance of integrating species' hydration physiology into forecasts of climate vulnerability, as omitting this axis may significantly underestimate the effects of future climate change on Earth's biological diversity. DOI PubMed
16. Gibeau, P; Bradford, MJ; Palen, WJ. (2020) Can the creation of new freshwater habitat demographically offset losses of Pacific salmon from chronic anthropogenic mortality?PLoS One 15 Can the creation of new freshwater habitat demographically offset losses of Pacific salmon from chronic anthropogenic mortality?
Over 1 billion USD are devoted annually to rehabilitating freshwater habitats to improve survival for the recovery of endangered salmon populations. Mitigation often requires the creation of new habitat (e.g. habitat offsetting) to compensate population losses from human activities, however offsetting schemes are rarely evaluated. Anadromous Pacific salmon are ecologically, culturally, and economically important in the US and Canada, and face numerous threats from degradation of freshwater habitats. Here we used a matrix population model of coho salmon (Oncorhynchus kisutch) to determine the amount of habitat offsetting needed to compensate mortality (2-20% per year) caused by a range of development activities. We simulated chronic mortality to three different life stages (egg, parr, smolt/adult), individually and simultaneously, to mimic impacts from development, and evaluated if the number of smolts produced from constructed side-channels demographically offset losses. We show that under ideal conditions, the typical size of a constructed side-channel in the Pacific Northwest (PNW) (3405 m(2)) is sufficient to compensate for only relatively low levels of chronic mortality to either the parr or smolt/adult stages (2-7% per year), but populations do not recover if mortality is >10% per year. When we assumed lower productivity (e.g.; 25(th) percentile), we found that constructed channels would need to be 2.5-4.5 fold larger as compared to the typical size built in the PNW, respectively, to maintain population sizes. Moreover, when we imposed mortality to parr and smolt/adult stages simultaneously, we found that constructed side-channels would need to be between 1.8- and 2.3- fold larger that if the extra chronic mortality was imposed to one life stage only. We conclude that habitat offsetting has the potential to mitigate chronic mortality to early life stages, but that realistic assumptions about productivity of constructed side-channels and cumulative effects of anthropogenic disturbances on multiple life stages need to be considered. DOI PubMed
14. Greenberg, DA; Palen, WJ; Chan, KC; Jetz, W; Mooers, AO. (2018) Evolutionarily distinct amphibians are disproportionately lost from human-modified ecosystems.Ecology Letters 21 Evolutionarily distinct amphibians are disproportionately lost from human-modified ecosystems
diversification; extinction risk; forests; global change; grasslands; habitat loss; land conversion; phylogenetic diversity
Humans continue to alter terrestrial ecosystems, but our understanding of how biodiversity responds is still limited. Anthropogenic habitat conversion has been associated with the loss of evolutionarily distinct bird species at local scales, but whether this evolutionary pattern holds across other clades is unknown. We collate a global dataset on amphibian assemblages in intact forests and nearby human-modified sites to assess whether evolutionary history influences susceptibility to land conversion. We found that evolutionarily distinct amphibian species are disproportionately lost when forested habitats are converted to alternative land-uses. We tested the hypothesis that grassland-associated amphibian lineages have both higher diversification and are pre-adapted to human landscapes, but found only weak evidence supporting this. The loss of evolutionarily distinct amphibians with land conversion suggests that preserving remnant forests will be vital if we aim to preserve the amphibian tree of life in the face of mounting anthropogenic pressures. DOI PubMed
12. Green, SJ; Demes, K; Arbeider, M; Palen, WJ; Salomon, AK; Sisk, TD; Webster, M; Ryan, ME. (2017) Oil sands and the marine environment: current knowledge and future challenges.Frontiers in Ecology and the Environment 15: 74-83 Oil sands and the marine environment: current knowledge and future challenges
The environmental consequences of bitumen extraction from oil sands deposits are at the center of North American natural resource and energy policy debate, yet impacts on ocean environments have received little attention. Using a quantitative framework, we identify knowledge gaps and research needs related to the effects of oil sands development on marine biota. Fifteen sources of stress and disturbance - varying greatly in spatial and temporal scale - are generated via two pathways: (1) the coastal storage and oceanic transport of bitumen products, and (2) the contribution of industry-derived greenhouse gases to climate change in the ocean. Of highest research priority are the fate, behavior, and biological effects of bitumen in the ocean. By contrast, climate-change impacts are scientifically well established but not considered in key regulatory processes. Most stressors co-occur and are generated by other industries, yet cumulative effects are so far unaccounted for in decision making associated with new projects. Our synthesis highlights priority research needed to inform future energy development decisions, and opportunities for policy processes to acknowledge the full scope of potential and realized environmental consequences. DOI
11. Greenberg, DA; Palen, WJ; Mooers, AO. (2017) Amphibian species traits, evolutionary history and environment predict Batrachochytrium dendrobatidis infection patterns, but not extinction risk.Evol. Appl. 10: 1130-1145 Amphibian species traits, evolutionary history and environment predict Batrachochytrium dendrobatidis infection patterns, but not extinction risk
amphibian; Batrachochytrium dendrobatidis; chytridiomycosis; extinction; phylogeny; resistance; tolerance; traits
The fungal pathogen Batrachochytrium dendrobatidis (B.dendrobatidis) has emerged as a major agent of amphibian extinction, requiring conservation intervention for many susceptible species. Identifying susceptible species is challenging, but many aspects of species biology are predicted to influence the evolution of host resistance, tolerance, or avoidance strategies towards disease. In turn, we may expect species exhibiting these distinct strategies to differ in their ability to survive epizootic disease outbreaks. Here, we test for phylogenetic and trait-based patterns of B.dendrobatidis infection risk and infection intensity among 302 amphibian species by compiling a global data set of B.dendrobatidis infection surveys across 95 sites. We then use best-fit models that associate traits, taxonomy and environment with B.dendrobatidis infection risk and intensity to predict host disease mitigation strategies (tolerance, resistance, avoidance) for 122 Neotropical amphibian species that experienced epizootic B.dendrobatidis outbreaks, and noted species persistence or extinction from these events. Aspects of amphibian species life history, habitat use and climatic niche were consistently linked to variation in B.dendrobatidis infection patterns across sites around the world. However, predicted B.dendrobatidis infection risk and intensity based on site environment and species traits did not reveal a consistent pattern between the predicted host disease mitigation strategy and extinction outcome. This suggests that either tolerant or resistant species may have no advantage in ameliorating disease during epizootic events, or that other factors drive the persistence of amphibian populations during chytridiomycosis outbreaks. These results suggest that using a trait-based approach may allow us to identify species with resistance or tolerance to endemic B.dendrobatidis infections, but that this approach may be insufficient to ultimately identify species at risk of extinction from epizootics. DOI
10. Lee, SY; Ryan, ME; Hamlet, AF; Palen, WJ; Lawler, JJ; Halabisky, M. (2015) Projecting the Hydrologic Impacts of Climate Change on Montane Wetlands.PLoS One 10 Projecting the Hydrologic Impacts of Climate Change on Montane Wetlands
Wetlands are globally important ecosystems that provide critical services for natural communities and human society. Montane wetland ecosystems are expected to be among the most sensitive to changing climate, as their persistence depends on factors directly influenced by climate (e.g. precipitation, snowpack, evaporation). Despite their importance and climate sensitivity, wetlands tend to be understudied due to a lack of tools and data relative to what is available for other ecosystem types. Here, we develop and demonstrate a new method for projecting climate-induced hydrologic changes in montane wetlands. Using observed wetland water levels and soil moisture simulated by the physically based Variable Infiltration Capacity (VIC) hydrologic model, we developed site-specific regression models relating soil moisture to observed wetland water levels to simulate the hydrologic behavior of four types of montane wetlands (ephemeral, intermediate, perennial, permanent wetlands) in the U.S. Pacific Northwest. The hybrid models captured observed wetland dynamics in many cases, though were less robust in others. We then used these models to a) hindcast historical wetland behavior in response to observed climate variability (1916-2010 or later) and classify wetland types, and b) project the impacts of climate change on montane wetlands using global climate model scenarios for the 2040s and 2080s (A1B emissions scenario). These future projections show that climate-induced changes to key driving variables (reduced snowpack, higher evapotranspiration, extended summer drought) will result in earlier and faster drawdown in Pacific Northwest montane wetlands, leading to systematic reductions in water levels, shortened wetland hydroperiods, and increased probability of drying. Intermediate hydroperiod wetlands are projected to experience the greatest changes. For the 2080s scenario, widespread conversion of intermediate wetlands to fastdrying ephemeral wetlands will likely reduce wetland habitat availability for many species. DOI
9. Atlas, WI; Palen, WJ. (2014) Prey Vulnerability Limits Top-Down Control and Alters Reciprocal Feedbacks in a Subsidized Model Food Web.PLOS One 9 Prey Vulnerability Limits Top-Down Control and Alters Reciprocal Feedbacks in a Subsidized Model Food Web
Resource subsidies increase the productivity of recipient food webs and can affect ecosystem dynamics. Subsidies of prey often support elevated predator biomass which may intensify top-down control and reduce the flow of reciprocal subsidies into adjacent ecosystems. However, top-down control in subsidized food webs may be limited if primary consumers posses morphological or behavioral traits that limit vulnerability to predation. In forested streams, terrestrial prey support high predator biomass creating the potential for strong top-down control, however armored primary consumers often dominate the invertebrate assemblage. Using empirically based simulation models, we tested the response of stream food webs to variations in subsidy magnitude, prey vulnerability, and the presence of two top predators. While terrestrial prey inputs increased predator biomass (+12%), the presence of armored primary consumers inhibited top-down control, and diverted most aquatic energy (similar to 75%) into the riparian forest through aquatic insect emergence. Food webs without armored invertebrates experienced strong trophic cascades, resulting in higher algal (similar to 50%) and detrital (similar to 1600%) biomass, and reduced insect emergence (-90%). These results suggest prey vulnerability can mediate food web responses to subsidies, and that top-down control can be arrested even when predator-invulnerable consumers are uncommon (20%) regardless of the level of subsidy. DOI
8. Kissel, AM; Palen, WJ; Govindarajulu, P; Bishop, CA. (2014) Quantifying Ecological Life Support: The Biological Efficacy of Alternative Supplementation Strategies for Imperiled Amphibian Populations.Conservation Letters 7: 441-450 Quantifying Ecological Life Support: The Biological Efficacy of Alternative Supplementation Strategies for Imperiled Amphibian Populations
Population supplementation; matrix models; captive breeding; head-start; amphibian conservation; species recovery
Global biodiversity loss has prompted diverse efforts to stem or reverse declines for many species. Such efforts are often implemented before the efficacy of alternative management actions is quantified. Here, we use matrix models to compare the effectiveness of two supplementation strategies, head-starting early life stages and captive breeding for reintroduction, at reducing extinction risk of declining amphibians. We use the imperiled Oregon spotted frog (Rana pretiosa) as a case study and find that when supplementation occurs after metamorphosis, captive breeding is more effective at reducing extinction risk than head-starting, but the difference declines with increasing supplementation effort. We also find that captive breeding with release as larvae yields similar reductions in extinction risk, and is two orders of magnitude more effective at reducing extinction probabilities than head-starting the same stage. Our results highlight that even basic demographic data can be leveraged to assess tradeoffs among alternative supplementation strategies. DOI
7. O'Regan, SM; Palen, WJ; Anderson, SC. (2014) Climate warming mediates negative impacts of rapid pond drying for three amphibian species.Ecology 95: 845-855 Climate warming mediates negative impacts of rapid pond drying for three amphibian species
Spea intermontana; global warming; wetland drying; metamorphosis; phenotypic plasticity; Rana aurora; Pseudacris regilla; life history
Anthropogenic climate change will present both opportunities and challenges for pool-breeding amphibians. Increased water temperature and accelerated drying may directly affect larval growth, development, and survival, yet the combined effects of these processes on larvae with future climate change remain poorly understood. Increased surface temperatures are projected to warm water and decrease water inputs, leading to earlier and faster wetland drying. So it is often assumed that larvae will experience negative synergistic impacts with combined warming and drying. However, an alternative hypothesis is that warming-induced increases in metabolic rate and aquatic resource availability might compensate for faster drying rates, generating antagonistic larval responses. We conducted a mesocosm experiment to test the individual and interactive effects of pool permanency (permanent vs. temporary) and water temperature (ambient vs. +similar to 3 degrees C) on three anurans with fast-to-slow larval development rates (Great Basin spadefoot [Spea intermontana], Pacific chorus frog [Pseudacris regilla], and northern red-legged frog [Rana aurora]). We found that although tadpoles in warmed pools reached metamorphosis 15-17 days earlier, they did so with little cost (<2 mm) to size, likely due to greater periphyton growth in warmed pools easing drying-induced resource competition. Warming and drying combined to act antagonistically on early growth (P = 0.06) and survival (P = 0.06), meaning the combined impact was less than the sum of the individual impacts. Warming and drying acted additively on time to and size at metamorphosis. These nonsynergistic impacts may result from cotolerance of larvae to warming and drying, as well as warming helping to offset negative impacts of drying. Our results indicate that combined pool warming and drying may not always be harmful for larval amphibians. However, they also demonstrate that antagonistic responses are difficult to predict, which poses a challenge to proactive conservation and management. Our study highlights the importance of considering the nature of multiple stressor interactions as amphibians are exposed to an increasing number of anthropogenic threats. DOI
6.Palen, WJ; Sisk, TD; Ryan, ME; Arvai, JL; Jaccard, M; Salomon, AK; Homer-Dixon, T; Lertzman, KP. (2014) Consider the global impacts of oil pipelines.Nature 510: 465-467 Consider the global impacts of oil pipelines
PubMed
5. Sunday, JM; Popovic, I; Palen, WJ; Foreman, MGG; Hart, MW. (2014) Ocean circulation model predicts high genetic structure observed in a long-lived pelagic developer.Molecular Ecology 23: 5036-5047 Ocean circulation model predicts high genetic structure observed in a long-lived pelagic developer
larval dispersal; marine connectivity; oceanographic circulation model; population genetics
Understanding the movement of genes and individuals across marine seascapes is a long-standing challenge in marine ecology and can inform our understanding of local adaptation, the persistence and movement of populations, and the spatial scale of effective management. Patterns of gene flow in the ocean are often inferred based on population genetic analyses coupled with knowledge of species' dispersive life histories. However, genetic structure is the result of time-integrated processes and may not capture present-day connectivity between populations. Here, we use a high-resolution oceanographic circulation model to predict larval dispersal along the complex coastline of western Canada that includes the transition between two well-studied zoogeographic provinces. We simulate dispersal in a benthic sea star with a 6-10week pelagic larval phase and test predictions of this model against previously observed genetic structure including a strong phylogeographic break within the zoogeographical transition zone. We also test predictions with new genetic sampling in a site within the phylogeographic break. We find that the coupled genetic and circulation model predicts the high degree of genetic structure observed in this species, despite its long pelagic duration. High genetic structure on this complex coastline can thus be explained through ocean circulation patterns, which tend to retain passive larvae within 20-50km of their parents, suggesting a necessity for close-knit design of Marine Protected Area networks. DOI PubMed
4. Tsui, MTK; Blum, JD; Finlay, JC; Balogh, SJ; Nollet, YH; Palen, WJ; Power, ME. (2014) Variation in Terrestrial and Aquatic Sources of Methylmercury in Stream Predators as Revealed by Stable Mercury Isotopes.Environmental Science & Technology 48: 10128-10135 Variation in Terrestrial and Aquatic Sources of Methylmercury in Stream Predators as Revealed by Stable Mercury Isotopes
Mercury (Hg) is widely distributed in the environment, and its organic form, methylmercury (MeHg), can extensively bioaccumulate and biomagnify in aquatic and terrestrial food webs. Concentrations of MeHg in organisms are highly variable, and the sources in natural food webs are often not well understood. This study examined stable isotope ratios of MeHg (mass-dependent fractionation, as delta Hg-202(MeHg); and mass-independent fractionation, as Delta Hg-199(MeHg)) in benthic invertebrates, juvenile steelhead trout (Oncorhynchus mykiss), and water striders (Gerris remigis) along a stream productivity gradient, as well as carnivorous terrestrial invertebrates, in a forested watershed at the headwater of South Fork Eel River in northern California. Throughout the sampling sites, delta Hg-202(MeHg) (after correction due to the effect of MeHg photodegradation) was significantly different between benthic (median = -1.40 parts per thousand; range, -2.34 to -0.78 parts per thousand; total number of samples = 29) and terrestrial invertebrates (median = +0.51 parts per thousand; range, -0.37 to +1.40 parts per thousand; total number of samples = 9), but no major difference between these two groups was found for Delta Hg-199(MeHg). Steelhead trout (52 individual fishes) have MeHg of predominantly aquatic origins, with a few exceptions at the upstream locations (e.g., 1 fish collected in a tributary had a purely terrestrial MeHg source and 4 fishes had mixed aquatic and terrestrial MeHg sources). Water striders (seven pooled samples) derive MeHg largely from terrestrial sources throughout headwater sections. These data suggest that direct terrestrial subsidy (e.g., terrestrial invertebrates falling into water) can be important for some stream predators in headwater streams and could represent an important means of transfer of terrestrially derived MeHg (e.g., in situ methylation within forests, atmospheric sources) to aquatic ecosystems. Moreover, these findings show that terrestrial subsidies can enhance MeHg bioaccumulation of consumers in headwater streams where aqueous MeHg levels are very low. DOI PubMed
3. Munshaw, RG; Palen, WJ; Courcelles, DM; Finlay, JC. (2013) Predator-Driven Nutrient Recycling in California Stream Ecosystems.PLOS One 8 Predator-Driven Nutrient Recycling in California Stream Ecosystems
CRITICAL THERMAL MAXIMA; FOOD-WEB STRUCTURE; FRESH-WATER; PHOSPHORUS-LIMITATION; SALAMANDER DENSITY; MOUNTAIN LAKES; WESTERN OREGON; RAINBOW-TROUT; UNITED-STATES; GIZZARD SHAD
Nutrient recycling by consumers in streams can influence ecosystem nutrient availability and the assemblage and growth of photoautotrophs. Stream fishes can play a large role in nutrient recycling, but contributions by other vertebrates to overall recycling rates remain poorly studied. In tributaries of the Pacific Northwest, coastal giant salamanders (Dicamptodon tenebrosus) occur at high densities alongside steelhead trout (Oncorhynchus mykiss) and are top aquatic predators. We surveyed the density and body size distributions of D. tenebrosus and O. mykiss in a California tributary stream, combined with a field study to determine mass-specific excretion rates of ammonium (N) and total dissolved phosphorus (P) for D. tenebrosus. We estimated O. mykiss excretion rates (N, P) by bioenergetics using field-collected data on the nutrient composition of O. mykiss diets from the same system. Despite lower abundance, D. tenebrosus biomass was 2.5 times higher than O. mykiss. Mass-specific excretion summed over 170 m of stream revealed that O. mykiss recycle 1.7 times more N, and 1.2 times more P than D. tenebrosus, and had a higher N:P ratio (8.7) than that of D. tenebrosus (6.0), or the two species combined (7.5). Through simulated trade-offs in biomass, we estimate that shifts from salamander biomass toward fish biomass have the potential to ease nutrient limitation in forested tributary streams. These results suggest that natural and anthropogenic heterogeneity in the relative abundance of these vertebrates and variation in the uptake rates across river networks can affect broad-scale patterns of nutrient limitation. DOI
2. Greig, HS; Kratina, P; Thompson, PL; Palen, WJ; Richardson, JS; Shurin, JB. (2012) Warming, eutrophication, and predator loss amplify subsidies between aquatic and terrestrial ecosystems.Global Change Biology 18: 504-514 Warming, eutrophication, and predator loss amplify subsidies between aquatic and terrestrial ecosystems
allochthonous resources; amphibians; climate warming; detritus decomposition; global change; insect emergence; spatial subsidies; top-down control
The exchange of organisms and energy among ecosystems has major impacts on food web structure and dynamics, yet little is known about how climate warming combines with other pervasive anthropogenic perturbations to affect such exchanges. We used an outdoor freshwater mesocosm experiment to investigate the interactive effects of warming, eutrophication, and changes in top predators on the flux of biomass between aquatic and terrestrial ecosystems. We demonstrated that predatory fish decoupled aquatic and terrestrial ecosystems by reducing the emergence of aquatic organisms and suppressing the decomposition of terrestrial plant detritus. In contrast, warming and nutrients enhanced cross-ecosystem exchanges by increasing emergence and decomposition, and these effects were strongest in the absence of predators. Furthermore, we found that warming advanced while predators delayed the phenology of insect emergence. Our results demonstrate that anthropogenic perturbations may extend well beyond ecosystem boundaries by influencing cross-ecosystem subsidies. We find that these changes are sufficient to substantially impact recipient communities and potentially alter the carbon balance between aquatic and terrestrial ecosystems and the atmosphere. DOI
1.Palen, WJ; Schindler, DE. (2010) Water clarity, maternal behavior, and physiology combine to eliminate UV radiation risk to amphibians in a montane landscape.Proceedings of the National Academy of Sciences of the United States of America 107: 9701-9706 Water clarity, maternal behavior, and physiology combine to eliminate UV radiation risk to amphibians in a montane landscape
amphibian declines; ultraviolet radiation; risk analysis; dissolved organic matter; oviposition behavior
Increasing UV-B radiation (UV-B; 290-320 nm) due to stratospheric ozone depletion has been a leading explanation for the decline in amphibians for nearly 2 decades. Yet, the likelihood that UV-B can influence amphibians at the large spatial scales relevant to population declines has not yet been evaluated. A key limitation has been in relating results from individual sites to the effect of UV-B for populations distributed across heterogeneous landscapes. We measured critical embryonic exposures to UV-B for two species of montane amphibians with contrasting physiological sensitivities, long-toed salamander (Ambystoma macrodactylum) and Cascades frog (Rana cascadae), at field sites spanning a gradient of UV-B attenuation in water. We then used these experimental results to estimate the proportion of embryos exposed to harmful UV-B across a large number of breeding sites. By combining surveys of the incubation timing, incident UV-B, optical transparency of water, and oviposition depth and light exposure of embryos at each site, we present a comprehensive assessment of the risk posed by UV-B for montane amphibians of the Pacific Northwest. We found that only 1.1% of A. macrodactylum and no R. cascadae embryos across a landscape of breeding sites are exposed to UV-B exceeding lethal levels. These results emphasize that accurately estimating the risk posed by environmental stressors requires placing experimental results in a broader ecological context that accounts for the heterogeneity experienced by populations distributed across natural landscapes. DOI
