The effects of different cold‐temperature regimes on development, growth, and susceptibility to an abiotic and biotic stressor

Wersebe, Matthew; Blackwood, Paradyse E.; Guo, Ying Tong; Jaeger, Jared; May, Dyllan; Meindl, George A.; Ryan, Sean; Wong, Vivian C.; Hua, Jessica

doi:10.1002/ece3.4957

Cited by 8 publications

(7 citation statements)

References 73 publications

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“…Indeed, only the eggs located at the pond surface may be impacted by cold air temperatures, which do not concern the entire population. In addition, pre-metamorphosis stages have variable sensitivity to cold temperature (Moore, 1942;Herreid and Kinney, 1967;Muir et al, 2014;Wersebe et al, 2019). Earlier breeding increased the risk of frost exposure at both elevations, but this may also allow juveniles to reach larger size at metamorphosis and thus increase survival probability as adults (Altwegg and Reyer, 2003;Loman, 2009).…”

Section: Discussionmentioning

confidence: 99%

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

Bison¹,

Yoccoz

Carlson³

et al. 2021

Front. Ecol. Evol.

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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.

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Section: Discussionmentioning

confidence: 99%

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

Bison¹,

Yoccoz

Carlson³

et al. 2021

Front. Ecol. Evol.

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“…We additionally found that wood frog tadpoles from the later-breeding cohort of 2018 were less tolerant of NaCl than tadpoles from the earlier-breeding cohort of the same year. While direct exposure to cold temperatures has been documented to lower immune responses [ 16 , 54 ], reduce larval growth and development [ 63 ], and interact synergistically with other stressors [ 57 ], it is important to note that in this study, tadpoles were not directly exposed to the cold temperatures of the parental environment. Thus, the reduced baseline tolerance to NaCl of the late breeding cohort may reflect cross-generational consequences of parental exposure to suboptimal temperatures [ 51 ].…”

Section: Discussionmentioning

confidence: 99%

“…The later-breeding R. sylvatica cohort in 2018 experienced a more severe winter weather event than the later-breeding cohort in 2019 (5 versus 2 days of freezing temperatures in 2018 and 2019, respectively). The later-breeding cohort in 2018 therefore likely experienced greater physiological stress from the freeze than the later-breeding cohort in 2019; there are costly physiological responses to low temperatures [ 19 , 63 ] and maternal stress is often transferred to developing eggs [ 18 , 62 ] in a variety of herpetofauna. The higher level of stress experienced by the later-breeding cohort in 2018 may be one potential cause of reduced offspring baseline tolerance to NaCl compared to that in 2019.…”

Section: Discussionmentioning

confidence: 99%

“…Overall, had offspring been reared in a field setting, it is likely that a) earlier cohorts in 2018 and 2019 would have experienced greater freeze-related mortality, and b) all larvae in 2019 would have experienced slowed development and exposure to stressful (cold) conditions. The consequences of these freezing conditions are evaluated in a companion paper [ 63 ]. Taken together, our data suggests that freezes following false springs (exacerbated by warmer average winter temperatures), particularly when combined with chemical stressors, are likely to be a major concern for spring breeding amphibian populations.…”

Section: Discussionmentioning

confidence: 99%

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Amphibian breeding phenology influences offspring size and response to a common wetland contaminant

2021

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Background Increases in temperature variability associated with climate change have critical implications for the phenology of wildlife across the globe. For example, warmer winter temperatures can induce forward shifts in breeding phenology across taxa (“false springs”), which can put organisms at risk of freezing conditions during reproduction or vulnerable early life stages. As human activities continue to encroach on natural ecosystems, it is also important to consider how breeding phenology interacts with other anthropogenic stressors (e.g., pollutants). Using 14 populations of a widespread amphibian (wood frog; Rana sylvatica), we compared 1) growth; 2) tolerance to a common wetland contaminant (NaCl); and 3) the ability of tadpoles to acclimate to lethal NaCl exposure following sublethal exposure earlier in life. We evaluated these metrics across two breeding seasons (2018 and 2019) and across populations of tadpoles whose parents differed in breeding phenology (earlier- versus later-breeding cohorts). In both years, the earlier-breeding cohorts completed breeding activity prior to a winter storm and later-breeding cohorts completed breeding activities after a winter storm. The freezing conditions that later-breeding cohorts were exposed to in 2018 were more severe in both magnitude and duration than those in 2019. Results In 2018, offspring of the later-breeding cohort were larger but less tolerant of NaCl compared to offspring of the earlier-breeding cohort. The offspring of the earlier-breeding cohort additionally were able to acclimate to a lethal concentration of NaCl following sublethal exposure earlier in life, while the later-breeding cohort became less tolerant of NaCl following acclimation. Interestingly, in 2019, the warmer of the two breeding seasons, we did not detect the negative effects of later breeding phenology on responses to NaCl. Conclusions These results suggest that phenological shifts that expose breeding amphibians to freezing conditions can have cascading consequences on offspring mass and ability to tolerate future stressors but likely depends on the severity of the freeze event.

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“…Increasing global temperature has a profound effect on the functioning of biological systems, e.g. it advances the timing of spring events (earlier arrival and breeding of migrant birds, earlier Communicated by W. Hughes appearance of butterflies, earlier spawning of amphibians or plant flowering), shifts species distribution poleward in latitude and upward in elevation, alters community composition and could result in the widespread phenological desynchronization among species (Walther et al 2002;Parmesan and Yohe 2003;Thackeray et al 2016;Wersebe et al 2019). The importance of temperature was neatly emphasised in this sentence: 'unlike many other variables that concern biologists, the temperature is not just a property of life; it is a property of matter.…”

Section: Introductionmentioning

confidence: 99%

The influence of age and development temperature on the temperature-related foraging risk of Formica cinerea ants

Ślipiński

Trigos-Peral

Maák

et al. 2021

Behav Ecol Sociobiol

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Climate change and the subsequent increase of global temperature are the most current and important threats to biodiversity. Despite the importance of temperature, our knowledge about the level of behavioural and physiological adaptations of ant species from temperate regions to cope with high temperatures is limited compared to the broad knowledge of typical thermal specialists from warmer regions. In the current study, we investigated the temperature-related foraging risk of xerothermic ant species from the temperate climate in Europe, Formica cinerea. Our aims were to check how an increase in external soil temperature affects the foraging activity of workers and how the temperature during development and worker age affects foraging activity in high temperatures. Based on our results, we can draw the following conclusions: (1) the majority of workers utilize a risk-aversive strategy in relation to foraging in high surface temperatures; (2) pupal development temperature affects the risk taken by adult workers: workers that developed in a higher temperature forage more often but for shorter intervals compared to workers that developed in a lower temperature; (3) age is an important factor in temperature-related foraging activity, as with increasing age, workers forage significantly longer at the highest temperatures. Our study is one of the first to assess the potential factors that can affect the foraging risk of ants from a temperate climate in high ambient temperatures. Significance statement Our study is the first direct test of workers' age and the development temperature of pupae on the thermal-related foraging strategy of adult F. cinerea workers. It shows that worker age and the development temperature of pupae interact to promote tolerance of thermal stress. We found that with increasing age, workers are prone to forage significantly longer at the highest and riskiest temperatures. Workers that developed in the high temperature (28°C) foraged more often but for shorter intervals compared to workers that developed in the lower temperature (20°C). Interestingly, the factor of age is more significant for ants that developed in the higher temperature of 28°C; the foraging time of these ants significantly increased with their age.

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The effects of different cold‐temperature regimes on development, growth, and susceptibility to an abiotic and biotic stressor

Cited by 8 publications

References 73 publications

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

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

Amphibian breeding phenology influences offspring size and response to a common wetland contaminant

The influence of age and development temperature on the temperature-related foraging risk of Formica cinerea ants

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