Earlier Snowmelt Advances Breeding Phenology of the Common Frog (Rana temporaria) but Increases the Risk of Frost Exposure and Wetland Drying

Abstract

The alarming decline of amphibians around the world calls for complementary studies to better understand their responses to climate change. In mountain environments, water resources linked to snowmelt play a major role in allowing amphibians to complete tadpole metamorphosis. As snow cover duration has significantly decreased since the 1970s, amphibian populations could be strongly impacted by climate warming, and even more in high elevation sites where air temperatures are increasing at a higher rate than at low elevation. In this context, we investigated common frog (Rana temporaria) breeding phenology at two different elevations and explored the threats that this species faces in a climate change context. Our objectives were to understand how environmental variables influence the timing of breeding phenology of the common frog, and explore the threats that amphibians face in the context of climate change in mountain areas. To address these questions, we collected 11 years (2009–2019) of data on egg-spawning date, tadpole development stages, snowmelt date, air temperature, rainfall and drying up of wetland pools at ∼1,300 and ∼1,900 m a.s.l. in the French Alps. We found an advancement of the egg-spawning date and snowmelt date at low elevation but a delay at high elevations for both variables. Our results demonstrated a strong positive relationship between egg-spawning date and snowmelt date at both elevations. We also observed that the risk of frost exposure increased faster at high elevation as egg-spawning date advanced than at low elevation, and that drying up of wetland pools led to tadpole mortality at the high elevation site. Within the context of climate change, egg-spawning date is expected to happen earlier in the future and eggs and tadpoles of common frogs may face higher risk of frost exposure, while wetland drying may lead to higher larval mortality. However, population dynamics studies are needed to test these hypotheses and to assess impacts at the population level. Our results highlight climate-related threats to common frog populations in mountain environments, but additional research should be conducted to forecast how climate change may benefit or harm amphibian populations, and inform conservation and land management plans in the future.

In-situ Temperature Stations Elucidate Species’ Phenological Responses to Climate in the Alps, but Meteorological and Snow Reanalysis Facilitates Broad Scale and Long-Term Studies

“…CREA Mont-Blanc installed temperature stations in species monitoring sites throughout the southwestern Alps to provide local temperature measurements. Using Phenoclim data, Pellerin et al (2012); Asse et al (2018Asse et al ( , 2020; Bison et al (2020) and Bison et al (2021) documented the effects of climate variability on trees, coal tits (Periparus ater), and common frogs (Rana temporaria), respectively. We use temperature and phelogical data from the Phenoclim program for the present work.…”

“…We investigated the effects of snow melt-out on common frog maximum egg-spawning date (Rana temporaria) using S2M and station datasets. The common frog egg-laying dates were noted for several ponds at Loriaz (1970 m) and Vallorcine (1,340 m, Figure 1A) by CREA Mont-Blanc employees and volunteers (Bison et al, 2021). We then calculated the maximum eggspawning date as the date with the maximum number of spawn in the ponds.…”

“…For instance, eggspawning dates of frogs usually occurred before dates of snow melt-out estimated by S2M, in contrast to snow melt-out consistently preceding egg-spawning when snow cover predictors were derived from station data. Given the observed link between snow melt-out and rapidly ensuing spawning of the European common frog in mountain habitats (Bison et al, 2021), in order to avoid erroneous predictions, it seems important to have not only a statistical correlation but also an ecologically relevant estimate of local snow melt-out timing. In many cases, accurate meteorological and snowpack data appear essential not only to understand phenological mechanisms, but also in order to predict non-linear and threshold-based responses to climate variability and change.…”

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

“…While most studies on amphibians across species and locations have found earlier spring breeding in response to climate change (Beebee, 1995; Blaustein et al, 2001; Parmesan, 2007; While & Uller, 2014), phenological delays have also been observed (e.g., Arnfield et al, 2012; Arietta et al, 2020). The direction and magnitude of these phenological shifts are therefore variable among and within species, as they can depend on the specific environmental conditions that the populations are experiencing at the local scale, or on the genetic structure of said populations (Phillimore et al, 2010; Bison et al, 2021).…”

“…Shifts in phenology can have adverse effects on amphibians, as phenological mismatches can affect predator-prey dynamics and food availability (Todd et al, 2011; Reinhardt et al, 2015; Jara et al, 2019; Visser & Gienapp, 2019). In temperate regions, early breeding can expose eggs and hatched tadpoles more frequently to late frost events, thus increasing mortality (Muir et al, 2014; Bison et al, 2021). On the other hand, in the absence of frost or drying events, earlier breeding might be beneficial as it allows post-metamorphic toadlets more time to fully develop in summer before hibernation (Reading & Clarke, 1999; Reading, 2010).…”