Microclimate‐driven trends in spring‐emergence phenology in a temperate reptile (Vipera berus): Evidence for a potential “climate trap”?

Abstract

Climate change can not only increase the exposure of organisms to higher temperatures but can also drive phenological shifts that alter their susceptibility to conditions at the onset of breeding cycles. Organisms rely on climatic cues to time annual life cycle events, but the extent to which climate change has altered cue reliability remains unclear. Here, we examined the risk of a “climate trap”—a climatically driven desynchronization of the cues that determine life cycle events and fitness later in the season in a temperate reptile, the European adder ( Vipera berus) . During the winter, adders hibernate underground, buffered against subzero temperatures, and re‐emerge in the spring to reproduce. We derived annual spring‐emergence trends between 1983 and 2017 from historical observations in Cornwall, UK, and related these trends to the microclimatic conditions that adders experienced. Using a mechanistic microclimate model, we computed below‐ and near‐ground temperatures to derive accumulated degree‐hour and absolute temperature thresholds that predicted annual spring‐emergence timing. Trends in annual‐emergence timing and subsequent exposure to ground frost were then quantified. We found that adders have advanced their phenology toward earlier emergence. Earlier emergence was associated with increased exposure to ground frost and, contradicting the expected effects of macroclimate warming, increased post‐emergence exposure to ground frost at some locations. The susceptibility of adders to this “climate trap” was related to the rate at which frost risk diminishes relative to advancement in phenology, which depends on the seasonality of climate. We emphasize the need to consider exposure to changing microclimatic conditions when forecasting biological impacts of climate change.

A quantitative synthesis of and predictive framework for studying winter warming effects in reptiles

“…While we have interpreted these effects as “positive”—consistent with the expectation that advancing springs will extend the suitable period for reproduction and offspring growth (Adolph and Porter 1993 ; Sperry et al 2010 ; Clarke and Zani 2012 )—the true fitness consequences of changes in phenology likely depend on population-specific environmental factors (Urban et al 2014 ; Prodon et al 2017). In many regions, mild winters are followed by late cold spells, which can expose individuals close to the surface to tissue damage (Benard 2015 ; Turner and Maclean 2022 ). Reptiles that specialize on invertebrate prey could also face trophic mismatch, as insects are highly sensitive to short-term climatic shifts and have been shown to advance phenologies at faster rates than insectivorous predators (Vafidis et al 2019 and references therein).…”

“…Phenological advancements in response to climate change have been documented across plant and animal species (Parmesan 2007 ; Cohen et al 2018 ) and regional and taxon-specific assessments suggest that reptiles are no exception (Urban et al 2014 ; Prodon et al 2020 ). Shorter winters and longer growing seasons are expected to have positive impacts on temperate reptiles by extending periods available for activity/reproduction (Adolph and Porter 1993 ; Sperry et al 2010 ), although early emergence could also confer deleterious effects such as greater exposure to late-season frosts (Turner and Maclean 2022 ).…”

Four decades of phenology in an alpine amphibian: trends, stasis, and climatic drivers

“…While we could expect climate change to act linearly on the shift towards earlier breeding dates, it is possible that other site-specific conditions prevail at smaller temporal and geographical scales, creating an heterogenous mosaic of climate conditions, especially at high elevations (Scherrer & Körner, 2011; Feldmeier et al, 2020). Populations therefore will not necessarily respond the same way, as they are experiencing different microclimates (Miller et al, 2018; Arietta et al, 2020; Turner & Maclean, 2022). Our data on climatic variables was limited to the 100 m x 100 m cell which includes the pond, and since we do not exactly know where the toads hibernate in the surrounding landscape, we cannot exclude that they are experiencing different microclimates compared to the pond.…”

“…In fact, extreme early breeding is associated with reduced hibernation periods which can decrease the body condition in spring (Reading, 2007). Additionally, early breeding can expose eggs and tadpoles to late frost events (Muir et al, 2014; Bison et al, 2021; Turner & Maclean, 2022). Delayed breeding can potentially pose a problem as well if the pond dries out during late spring warm conditions or if juveniles cannot accomplish full growth before hibernation.…”

“…High elevation habitats can also show different climates at very small geographical scales (Scherrer & Körner, 2011; Feldmeier et al, 2020). The phenology of populations experiencing these different microclimates will therefore not necessarily be affected in the same way (Miller et al, 2018; Arietta et al, 2020; Turner & Maclean, 2022). In our case, the data on climatic variables was limited to the 100 metres x 100 metres cell which includes the pond, and since we do not exactly know where the toads hibernate in the surrounding landscape, we cannot exclude that they are experiencing different microclimates compared to the pond and its surrounding area.…”