Shifts in frog size and phenology: Testing predictions of climate change on a widespread anuran using data from prior to rapid climate warming

Changes in body size and breeding phenology have been identified as two major ecological consequences of climate change, yet it remains unclear whether climate acts directly or indirectly on these variables. To better understand the relationship between climate and ecological changes, it is necessary to determine environmental predictors of both size and phenology using data from prior to the onset of rapid climate warming, and then to examine spatially explicit changes in climate, size, and phenology, not just general spatial and temporal trends. We used 100 years of natural history collection data for the wood frog, Lithobates sylvaticus with a range >9 million km², and spatially explicit environmental data to determine the best predictors of size and phenology prior to rapid climate warming (1901–1960). We then tested how closely size and phenology changes predicted by those environmental variables reflected actual changes from 1961 to 2000. Size, phenology, and climate all changed as expected (smaller, earlier, and warmer, respectively) at broad spatial scales across the entire study range. However, while spatially explicit changes in climate variables accurately predicted changes in phenology, they did not accurately predict size changes during recent climate change (1961–2000), contrary to expectations from numerous recent studies. Our results suggest that changes in climate are directly linked to observed phenological shifts. However, the mechanisms driving observed body size changes are yet to be determined, given the less straightforward relationship between size and climate factors examined in this study. We recommend that caution be used in “space‐for‐time” studies where measures of a species’ traits at lower latitudes or elevations are considered representative of those under future projected climate conditions. Future studies should aim to determine mechanisms driving trends in phenology and body size, as well as the impact of climate on population density, which may influence body size.     

Rapid morphological change in stream beetle museum specimens correlates with climate change

Abstract 1. Climate change has been occurring at unprecedented rates and its impacts on biological populations is beginning to be well documented in the literature. For many species, however, long‐term records are not available, and trends have not been documented. 2. Using museum specimens from southern USA, we show that the stream‐dwelling beetle Gyretes sinuatus has shown an 8% increase in body size and change in body shape (fineness ratio) from 1928 to 1988. Any directional morphological change observed over time could be an indicator of a microevolutionary response. 3. During these 60 years, there have also been changes in temperature, precipitation, and location of collection sites. Unlike the global trend, mean annual temperature in the region has decreased, and furthermore, total annual precipitation has increased. By investigating how these various ecological and geographical variables may affect body size and shape, we can examine which pressures may promote larger and/or thinner beetles. 4. Results indicate that mean annual temperature was the most predictive variable for the change in size and shape. We suggest there is an adaptive role for temperature on body size and shape of stream dwelling organisms. 5. We found that museum specimens can be invaluable resources of information when collection date and location information is available. We promote the use of such specimens for future studies of the morphological response to climate change.     

Predicted population trends for Cozumel Curassows (Crax rubra griscomi): empirical evidence and predictive models in the face of climate change

ABSTRACT We assessed the current conservation status and population trends of Cozumel Curassows (Crax rubra griscomi), a critically endangered and endemic cracid of Cozumel Island, Mexico. Distance sampling was used to estimate the population size in 2005 and compare it with a previous estimate in 1995. Population viability analysis (PVA) was used to model population trends, considering ecological and environmental conditions prevailing in 1995 and 2005. Additional PVA models were constructed using different hypothetical scenarios to assess the effects of particular factors and management strategies on population trends. We estimated a population size of 372 ± 155 curassows in the island's tropical semideciduous forest, before two hurricanes hit Cozumel Island in 2005. PVA modeling predicted a steep decline in population size in the ensuing decades as a result of an increased frequency and intensity of hurricanes related to global climate change, and an observed female bias in the sex ratio likely caused by a higher mortality rate for adult males. We recommend urgent management actions for the long‐term conservation of Cozumel Curassows, including a ban on hunting, eradication of the feral fauna, particularly dogs, and implementation of a captive‐breeding program to supplement the wild population.     

Toward a conceptual synthesis for climate change responses

Aim To identify hypotheses for how climate change affects long‐term population persistence that can be used as a framework for future syntheses of ecological responses to climate change. Location Global. Methods We surveyed ecological and evolutionary concepts related to how a changing climate might alter population persistence. We organized established concepts into a two‐stage framework that relates abiotic change to population persistence via changes in the rates or outcomes of ecological and evolutionary processes. We surveyed reviews of climate change responses, and evaluated patterns in light of our conceptual framework. Results We classified hypotheses for population responses to climate change as one of two types: (1) hypotheses that relate rates of ecological and evolutionary processes (plasticity, dispersal, population growth and evolution) to abiotic change, and (2) hypotheses that relate changes in these processes to four fundamental population‐level responses (colonization, acclimatization, adaptation or extinction). We found that a disproportionate emphasis on response in the climate change literature is difficult to reconcile with ecological and evolutionary theories that emphasize processes. We discuss a set of 24 hypotheses that represent gaps in the literature that limit our ability determine whether observed climate change responses are sufficient to facilitate persistence through future climate change. Main conclusions Though theory relates environmental change to fundamental ecological and evolutionary processes and population‐level responses, clear hypotheses based on theory have not been systematically formulated and tested in the context of climate change. Stronger links between basic theory and observed impacts of climate change are required to assess which responses are common, likely or able to facilitate population persistence despite ongoing environmental change. We anticipate that a hypothesis‐testing framework will reveal that indirect effects of climate change responses are more pervasive than previously thought and related to a few general processes, even though the patterns they create are incredibly diverse.     

Temperature‐dependent oxygen limitation and the rise of Bergmann's rule in species with aquatic respiration

Bergmann's rule is the propensity for species‐mean body size to decrease with increasing temperature. Temperature‐dependent oxygen limitation has been hypothesized to help drive temperature–size relationships among ectotherms, including Bergmann's rule, where organisms reduce body size under warm oxygen‐limited conditions, thereby maintaining aerobic scope. Temperature‐dependent oxygen limitation should be most pronounced among aquatic ectotherms that cannot breathe aerially, as oxygen solubility in water decreases with increasing temperature. We use phylogenetically explicit analyses to show that species‐mean adult size of aquatic salamanders with branchial or cutaneous oxygen uptake becomes small in warm environments and large in cool environments, whereas body size of aquatic species with lungs (i.e., that respire aerially), as well as size of semiaquatic and terrestrial species do not decrease with temperature. We argue that oxygen limitation drives the evolution of small size in warm aquatic environments for species with aquatic respiration. More broadly, the stronger decline in size with temperature observed in aquatic versus terrestrial salamander species mirrors the relatively strong plastic declines in size observed previously among aquatic versus terrestrial invertebrates, suggesting that temperature‐dependent oxygen availability can help drive patterns of plasticity, micro‐ and macroevolution.     

Digit reduction, body size, and paedomorphosis in salamanders

SUMMARY The loss of digits is a widespread evolutionary trend in tetrapods which occurs in nearly every major clade. Alberch and Gale showed that the order in which digits are evolutionarily lost in salamanders versus frogs corresponds to the order in which they develop in each group, providing a classic example of developmental constraint. However, what actually drives the loss of digits in salamanders has remained unclear. Alberch and Gale suggested that loss of digits might be associated with paedomorphosis or with reduced body size. We test these hypotheses by combining morphometric and phylogenetic information for 98 species of salamanders. We find that digit loss is associated with both paedomorphosis and reduction in body size. However, these trends are surprisingly contradictory, in that paedomorphosis is significantly associated with an increase in body size in salamanders. Thus, much of the extreme digit reduction is found in the smaller species within paedomorphic clades that have, on average, unusually large body size. Our results show that the consequences of changes in body size on morphology are highly context dependent. We also show (possibly for the first time) a significant association between paedomorphosis and increased body size, rather than the expected association with reduced body size.     

Dynamics of phenotypic change: wing length declines in a resident farmland passerine despite survival advantage of longer wings

In many taxa, environmental changes that alter resource availability and energetics, such as climate change and land use change, are associated with changes in body size. We use wing length as a proxy for overall structural body size to examine a paradoxical trend of declining wing length within a Yellowhammer Emberiza citrinella population sampled over 21 years, in which it has been previously shown that longer wings are associated with higher survival rates. Higher temperatures during the previous winter (prior to the moult determining current wing length) explained 23% of wing length decrease within our population, but changes may also be correlated with non‐climatic environmental variation such as changes in farming mechanisms linked to food availability. We found no evidence for within‐individual wing length shrinkage with age, but our data suggested a progressive decline in the sizes of immature birds recruiting to the population. This trend was weaker, although not significantly so, among adults, suggesting that the decline in the sizes of recruits was offset by higher subsequent survival of larger birds post‐recruitment. These data suggest that ecological processes can contribute more than selection to observed phenotypic trends and highlight the importance of long‐term studies for providing longitudinal insights into population processes.     

THE MICRO AND MACRO IN BODY SIZE EVOLUTION

The diversity of body sizes of organisms has traditionally been explained in terms of microevolutionary processes: natural selection owing to differential fitness of individual organisms, or to macroevolutionary processes: species selection owing to the differential proliferation of phylogenetic lineages. Data for terrestrial mammals and birds indicate that even on a logarithmic scale frequency distributions of body mass among species are significantly skewed towards larger sizes. We used simulation models to evaluate the extent to which macro- and microevolutionary processes are sufficient to explain these distributions. Simulations of a purely cladogenetic process with no bias in extinction or speciation rates for different body sizes did not produce skewed log body mass distributions. Simulations that included size-biased extinction rates, especially those that incorporated anagenetic size change within species between speciation and extinction events, regularly produced skewed distributions. We conclude that although cladogenetic processes probably play a significant role in body size evolution, there must also be a significant anagenetic component. The regular variation in the form of mammalian body size distributions among different-sized islands and continents suggests that environmental conditions, operating through both macro- and microevolutionary processes, determine to a large extent the diversification of body sizes within faunas. Macroevolution is not decoupled from microevolution.     

Morphological Change to Birds over 120 Years Is Not Explained by Thermal Adaptation to Climate Change

Changes in morphology have been postulated as one of the responses of animals to global warming, with increasing ambient temperatures leading to decreasing body size. However, the results of previous studies are inconsistent. Problems related to the analyses of trends in body size may be related to the short-term nature of data sets, to the selection of surrogates for body size, to the appropriate models for data analyses, and to the interpretation as morphology may change in response to ecological drivers other than climate and irrespective of size. Using generalized additive models, we analysed trends in three morphological traits of 4529 specimens of eleven bird species collected between 1889 and 2010 in southern Germany and adjacent areas. Changes and trends in morphology over time were not consistent when all species and traits were considered. Six of the eleven species displayed a significant association of tarsus length with time but the direction of the association varied. Wing length decreased in the majority of species but there were few significant trends in wing pointedness. Few of the traits were significantly associated with mean ambient temperatures. We argue that although there are significant changes in morphology over time there is no consistent trend for decreasing body size and therefore no support for the hypothesis of decreasing body size because of climate change. Non-consistent trends of change in surrogates for size within species indicate that fluctuations are influenced by factors other than temperature, and that not all surrogates may represent size appropriately. Future analyses should carefully select measures of body size and consider alternative hypotheses for change.     

Morphological variation in salamanders and their potential response to climate change

Despite the recognition that some species might quickly adapt to new conditions under climate change, demonstrating and predicting such a fundamental response is challenging. Morphological variations in response to climate may be caused by evolutionary changes or phenotypic plasticity, or both, but teasing apart these processes is difficult. Here, we built on the number of thoracic vertebrae (NTV) in ectothermic vertebrates, a known genetically based feature, to establish a link with body size and evaluate how climate change might affect the future morphological response of this group of species. First, we show that in old‐world salamanders, NTV variation is strongly related to changes in body size. Secondly, using 22 salamander species as a case study, we found support for relationships between the spatial variation in selected bioclimatic variables and NTV for most of species. For 44% of species, precipitation and aridity were the predominant drivers of geographical variation of the NTV. Temperature features were dominant for 31% of species, while for 19% temperature and precipitation played a comparable role. This two‐step analysis demonstrates that ectothermic vertebrates may evolve in response to climate change by modifying the number of thoracic vertebrae. These findings allow to develop scenarios for potential morphological evolution under future climate change and to identify areas and species in which the most marked evolutionary responses are expected. Resistance to climate change estimated from species distribution models was positively related to present‐day species morphological response, suggesting that the ability of morphological evolution may play a role for species’ persistence under climate change. The possibility that present‐day capacity for local adaptation might help the resistance response to climate change can be integrated into analyses of the impact of global changes and should also be considered when planning management actions favouring species persistence.     

Geographical Variation in Body Size and Sexual Size Dimorphism in an Australian Lizard,Boulenger's Skink (Morethia boulengeri)

Ecogeographical rules help explain spatial and temporal patterns in intraspecific body size. However, many of these rules, when applied to ectothermic organisms such as reptiles, are controversial and require further investigation. To explore factors that influence body size in reptiles, we performed a heuristic study to examine body size variation in an Australian lizard, Boulenger''s Skink Morethia boulengeri from agricultural landscapes in southern New South Wales, south-eastern Australia. We collected tissue and morphological data on 337 adult lizards across a broad elevation and climate gradient. We used a model-selection procedure to determine if environmental or ecological variables best explained body size variation. We explored the relationship between morphology and phylogenetic structure before modeling candidate variables from four broad domains: (1) geography (latitude, longitude and elevation), (2) climate (temperature and rainfall), (3) habitat (vegetation type, number of logs and ground cover attributes), and (4) management (land use and grazing history). Broad phylogenetic structure was evident, but on a scale larger than our study area. Lizards were sexually dimorphic, whereby females had longer snout-vent length than males, providing support for the fecundity selection hypothesis. Body size variation in M. boulengeri was correlated with temperature and rainfall, a pattern consistent with larger individuals occupying cooler and more productive parts of the landscape. Climate change forecasts, which predict warmer temperature and increased aridity, may result in reduced lizard biomass and decoupling of trophic interactions with potential implications for community organization and ecosystem function.     

Evaluating the role and measures of juvenile growth rate: latitudinal variation in insect life histories

Latitudinal and elevational trends in body size are found in numerous animal taxa, with various adaptive explanations proposed. It is however debatable whether geographic trends in adult body size are accompanied by corresponding differences in juvenile growth rate (= mass gain per unit time). Respective studies have been complicated by conceptual and methodological problems related to defining and measuring this variable, particularly in organisms with discontinuous growth like arthropods. Using an original method for estimating differential (instantaneous) juvenile growth rates, we compared geographically distant European populations of six insect species in a common garden experiment. We found no among population differences in differential growth rate in any of the species. This result is in concert with concurrent increase in both adult size and developmental time towards the south. While opposite examples exist, we interpret our results as challenging the view that growth rate is a trait that readily responds to environmentally based selective pressures. Our results thus advocate the more classical view of growth rate maximisation within its physiological limits. We discuss the advantages of using differential (rather than integral) measures of growth rate in evolutionary ecological studies and evaluate the reasons for the detected latitudinal trends in life history traits.     

Assessing five decades of change in a high Arctic parasitoid community

Arctic ecosystems are fragile, and are particularly sensitive to the pressures of climate change. Both average temperature and precipitation have increased over the past five decades on Ellesmere Island, Nunavut, Canada in the high Arctic. Altered growth forms and increased biomass in dominant plant species on Ellesmere Island have been observed concurrent with the changing climate, but shifts in the diversity or rank abundance of plant and bird species have not been detected. Changes in diversity may take longer to appear, or may be assessed better using organisms with shorter generation times such as insects. We explored the ecological impacts of climate change on Ellesmere Island using historical and contemporary communities of ichneumonid wasps. We compared community diversity, functional composition, and body size of two common species using ichneumonid specimens collected in 1961–1965, 1980–1982, 1989–1992, and 2010. We found high compositional similarity between collections, overlapping estimates of species richness, no change in the proportion of idiobiont genera in the community, and no clear pattern in body size over time. The greatest amount of variation over time was detected in parasitoids of herbivores; proportionally fewer herbivore‐parasitizing genera were found in 2010 than in historical collections, and the two genera that were only found in one of the four collections were both parasitoids of herbivores. Our results point to the need to assess climate change effects in Arctic systems using a range of taxa, and responses to large‐scale environmental disturbances may be idiosyncratic and difficult to predict.     

Body size variation in insects: a macroecological perspective

Body size is a key feature of organisms and varies continuously because of the effects of natural selection on the size-dependency of resource acquisition and mortality rates. This review provides a critical and synthetic overview of body size variation in insects from a predominantly macroecological (large-scale temporal and spatial) perspective. Because of the importance of understanding the proximate determinants of adult size, it commences with a brief summary of the physiological mechanisms underlying adult body size and its variation, based mostly on findings for the model species Drosophila melanogaster and Manduca sexta . Variation in nutrition and temperature have variable effects on critical weight, the interval to cessation of growth (or terminal growth period) and growth rates, so influencing final adult size. Ontogenetic and phylogenetic variation in size, compensatory growth, scaling at the intra- and interspecific levels, sexual size dimorphism, and body size optimisation are then reviewed in light of their influences on individual and species body size frequency distributions. Explicit attention is given to evolutionary trends, including gigantism, Cope's rule and the rates at which size change has taken place, and to temporal ecological trends such as variation in size with succession and size-selectivity during the invasion process. Large-scale spatial variation in size at the intraspecific, interspecific and assemblage levels is considered, with special attention being given to the mechanisms proposed to underlie clinal variation in adult body size. Finally, areas particularly in need of additional research are identified.     

Predicting woodrat (Neotoma) responses to anthropogenic warming from studies of the palaeomidden record

Aim The influence of anthropogenic climate change on organisms is an area of great scientific concern. Increasingly there is recognition that abrupt climate transitions have occurred over the late Quaternary; studies of these shifts may yield insights into likely biotic responses to contemporary warming. Here, we review research undertaken over the past decade investigating the response of Neotoma (woodrats) body size and distribution to climate change over the late Quaternary (the last 40,000 years). By integrating information from woodrat palaeomiddens, historical museum specimens and field studies of modern populations, we identify potential evolutionary responses to climate change occurring over a variety of temporal and spatial scales. Specifically, we characterize climatic thresholds in the past that led to local species extirpation and/or range alterations rather than in situ adaptation, and apply them to anticipate potential biotic responses to anthropogenic climate change. Location Middens were collected at about 55 sites scattered across the western United States, ranging from about 34 to 46° N and about 104 to 116° W, respectively. Data for modern populations were drawn from studies conducted in Death Valley, California, Missoula, Montana and the Sevilleta LTER site in central New Mexico. Methods We analysed faecal pellets from midden series collected at numerous cave sites across the western United States. From these we estimated body mass using techniques validated in earlier studies. We compared body size fluctuations at different elevations in different regions and integrated these results with studies investigating temperature–body size tradeoffs in modern animals. We also quantify the rapidity of the size changes over the late Quaternary to estimate the evolutionary capacity of woodrats to deal with predicted rates of anthropogenic climate change over the next century. Results We find remarkable similarities across the geographical range to late Quaternary climate change. In the middle of the geographical range woodrats respond in accordance to Bergmann's rule: colder climatic conditions select for larger body size and warmer conditions select for smaller body size. Patterns are more complicated at range boundaries, and local environmental conditions influence the observed response. In general, woodrat body size fluctuates with approximately the same amplitude and frequency as climate; there is a significant and positive correlation between woodrat body size and generalized climate proxies (such as ice core records). Woodrats have achieved evolutionary rates of change equal to or greater than those needed to adapt in situ to anthropogenic climate change. Main conclusions In situ body size evolution is a likely outcome of climate change, and such shifts are part of a normal spectrum of adaptation. Woodrats appear to be subject to ongoing body size selection in response to fluctuating environmental conditions. Allometric considerations suggest that these shifts in body size lead to substantial changes in the physiology, life history and ecology of woodrats, and on their direct and indirect interactions with other organisms in the ecosystem. Our work highlights the importance of a finely resolved and long‐term record in understanding biotic responses to climatic shifts.     

Physiological constraints on organismal response to global warming: Mechanistic insights from clinally varying populations and implications for assessing endangerment

Recent syntheses indicate that global warming affects diverse biological processes, but also highlight the potential for some species to adapt behaviourally or evolutionarily to rapid climate change. Far less attention has addressed the alternative, that organisms lacking this ability may face extinction, a fate projected to befall one-quarter of global biodiversity. This conclusion is controversial, in part because there exist few mechanistic studies that show how climate change could precipitate extinction. We provide a concrete, mechanistic example of warming as a stressor of organisms that are closely adapted to cool climates from a comparative analysis of organismal tolerance among clinally varying populations along a natural thermal gradient. We found that two montane salamanders exhibit significant metabolic depression at temperatures within the natural thermal range experienced by low and middle elevation populations. Moreover, the magnitude of depression was inversely related to native elevation, suggesting that low elevation populations are already living near the limit of their physiological tolerances. If this finding generally applies to other montane specialists, the prognosis for biodiversity loss in typically diverse montane systems is sobering. We propose that indices of warming-induced stress tolerance may provide a critical new tool for quantitative assessments of endangerment due to anthropogenic climate change across diverse species.     

Abundance of montane salamanders over an elevational gradient

Climate change is expected to systematically alter the distribution and population dynamics of species around the world. The effects are expected to be particularly strong at high latitudes and elevations, and for ectothermic species with small ranges and limited movement potential, such as salamanders in the southern Appalachian Mountains. In this study, we sought to establish baseline abundance estimates for plethodontid salamanders (family: Plethodontidae) over an elevational gradient in Great Smoky Mountains National Park. In addition to generating these baseline data for multiple species, we describe methods for surveying salamanders that allow for meaningful comparisons over time by separating observation and ecological processes generating the data. We found that Plethodon jordani had a mid‐elevation peak (1,500 m) in abundance and Desmognathus wrighti increased in abundance with elevation up to the highest areas of the park (2025 m), whereas Eurycea wilderae increased in abundance up to 1,600 m and then plateaued with increasing uncertainty. Litter depth, herbaceous ground cover, and proximity to stream were also important predictors of abundance (dependent upon species), whereas daily temperature, precipitation, ground cover, and humidity influenced detection rates. Our data provide some of the first minimally biased information for future studies to assess changes in the abundance and distribution of salamanders in this region. Understanding abundance patterns along with detailed baseline distributions will be critical for comparisons with future surveys to understand the population and community‐level effects of climate change on montane salamanders.     

Climate warming is associated with smaller body size and shorter lifespans in moose near their southern range limit

Despite the importance of body size for individual fitness, population dynamics and community dynamics, the influence of climate change on growth and body size is inadequately understood, particularly for long‐lived vertebrates. Although temporal trends in body size have been documented, it remains unclear whether these changes represent the adverse impact of climate change (environmental stress constraining phenotypes) or its mitigation (via phenotypic plasticity or evolution). Concerns have also been raised about whether climate change is indeed the causal agent of these phenotypic shifts, given the length of time‐series analysed and that studies often do not evaluate – and thereby sufficiently rule out – other potential causes. Here, we evaluate evidence for climate‐related changes in adult body size (indexed by skull size) over a 4–decade period for a population of moose (Alces alces) near the southern limit of their range whilst also considering changes in density, predation, and human activities. In particular, we document: (i) a trend of increasing winter temperatures and concurrent decline in skull size (decline of 19% for males and 13% for females) and (ii) evidence of a negative relationship between skull size and winter temperatures during the first year of life. These patterns could be plausibly interpreted as an adaptive phenotypic response to climate warming given that latitudinal/temperature clines are often accepted as evidence of adaptation to local climate. However, we also observed: (iii) that moose with smaller skulls had shorter lifespans, (iv) a reduction in lifespan over the 4‐decade study period, and (v) a negative relationship between lifespan and winter temperatures during the first year of life. Those observations indicate that this phenotypic change is not an adaptive response to climate change. However, this decline in lifespan was not accompanied by an obvious change in population dynamics, suggesting that climate change may affect population dynamics and life‐histories differently.     

Asynchronous demographic responses to Pleistocene climate change in Eastern Nearctic vertebrates

Pleistocene climatic cycles altered species distributions in the Eastern Nearctic of North America, yet the degree of congruent demographic response to the Pleistocene among codistributed taxa remains unknown. We use a hierarchical approximate Bayesian computational approach to test if population sizes across lineages of snakes, lizards, turtles, mammals, birds, salamanders and frogs in this region expanded synchronously to Late Pleistocene climate changes. Expansion occurred in 75% of 74 lineages, and of these, population size trajectories across the community were partially synchronous, with coexpansion found in at least 50% of lineages in each taxonomic group. For those taxa expanding outside of these synchronous pulses, factors related to when they entered the community, ecological thresholds or biotic interactions likely condition their timing of response to Pleistocene climate change. Unified timing of population size change across communities in response to Pleistocene climate cycles is likely rare in North America.