Thermal sensitivity in dual‐breathing ectotherms: Embryos and mothers determine species' vulnerability to climate change

Vorsatz, Lyle Dennis; Mostert, Bruce; McQuaid, Christopher D.; Cannicci, Stefano; Porri, Francesca

doi:10.1002/lol2.10225

Cited by 5 publications

(5 citation statements)

References 40 publications

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“…Variation in seawater temperature is characteristic of many nearshore ecosystems. Our results, covering a wide range of temperatures, showed responses that were consistent with TPCs reported for many traits from a wide array of species [110][111][112][113][114]. Although simple positive or negative responses to increasing temperatures have been reported in some echinoderms (Table 1), these results typically emerge from experiments covering a narrower thermal range…”

Section: Discussionsupporting

confidence: 89%

The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization

et al. 2022

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In an era of climate change, impacts on the marine environment include warming and ocean acidification. These effects can be amplified in shallow coastal regions where conditions often fluctuate widely. This type of environmental variation is potentially important for many nearshore species that are broadcast spawners, releasing eggs and sperm into the water column for fertilization. We conducted two experiments to investigate: 1) the impact of water temperature on sperm swimming characteristics and fertilization rate in sand dollars (Dendraster excentricus; temperatures 8-38°C) and sea urchins (Mesocentrotus franciscanus; temperatures 8-28°C) and; 2) the combined effects of multiple stressors (water temperature and pH) on these traits in sand dollars. We quantify thermal performance curves showing that sand dollar fertilization rates, sperm swimming velocities, and sperm motility display remarkably wide thermal breadths relative to red urchins, perhaps reflecting the wider range of water temperatures experienced by sand dollars at our field sites. For sand dollars, both temperature (8, 16, 24°C) and pH (7.1, 7.5, 7.9) affected fertilization but only temperature influenced sperm swimming velocity and motility. Although sperm velocities and fertilization were positively correlated, our fertilization kinetics model dramatically overestimated measured rates and this discrepancy was most pronounced under extreme temperature and pH conditions. Our results suggest that environmental stressors like temperature and pH likely impair aspects of the reproductive process beyond simple sperm swimming behavior.

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Section: Discussionsupporting

confidence: 89%

The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization

et al. 2022

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“…If female fiddler crabs are more thermally sensitive, they may be the first to succumb to temperature increases, thereby reducing the viability and resilience of populations. Similar results have been observed in spawning fishes (Dahlke et al, 2020) and mangrove crabs (Vorsatz et al, 2021a), suggesting that reproductively active females may constitute an ontogenetic thermal bottleneck in climate change scenarios.…”

Section: Discussionsupporting

confidence: 82%

“…During the reproductive season, female fiddler crabs produce large quantities of eggs (Yamaguchi, 2001;Koch et al, 2005;Litulo, 2005;Castiglioni et al, 2007), at energetic costs higher than the ones involved in sperm production (Hartnoll, 2006;Rennie et al, 2008). A large allocation of energy on reproduction reduces the available aerobic scope of organisms (Sokolova, 2013) and it is assumed to reduce their thermal window (Pörtner and Farrell, 2008;Vorsatz et al, 2021a). If female fiddler crabs are more thermally sensitive, they may be the first to succumb to temperature increases, thereby reducing the viability and resilience of populations.…”

Section: Discussionmentioning

confidence: 99%

Temperature Extremes and Sex-Related Physiology, Not Environmental Variability, Are Key in Explaining Thermal Sensitivity of Bimodal-Breathing Intertidal Crabs

Jiménez

Vorsatz²,

Costa³

et al. 2022

Front. Mar. Sci.

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Global temperature increases are predicted to have pronounced negative effects on the metabolic performance of both terrestrial and aquatic organisms. These metabolic effects may be even more pronounced in intertidal organisms that are subject to multiple, abruptly changing abiotic stressors in the land-sea transition zone. Of the available studies targeting the intertidal environment, emphasis has largely been on water-breathing model organisms and this selective focus resulted in limited reliable forecasts on the impact of global warming on primarily air-breathing intertidal species. We investigated the thermal sensitivity of six phylogenetically related fiddler crab species that occupy different microhabitats on intertidal shores from south America and east Asia to test how bimodal-breathing intertidal ectotherms cope with thermal stress. We examined the metabolic physiology and thermal limits of the crabs by measuring their cardiac function and oxygen consumption along a thermal gradient. Their specific thermal microhabitat was also appraised. We found that subtropical fiddler crab species inhabiting vegetated microhabitats have lower upper lethal temperatures and therefore greater thermal sensitivity in comparison to their tropical counterparts. Additionally, females exhibited higher oxygen consumption and lower lethal temperatures in comparison to males. Our results contradict previous predictions that species from higher latitudes that experience greater temperature variability have broader latitudinal distributions, greater phenotypic plasticity and lower thermal sensitivity. Furthermore, the higher thermal sensitivity demonstrated by female fiddler crabs with respect to males strongly suggests a role of both gametogenesis and physiological dimorphism on the thermal performance of tropical and subtropical intertidal organisms. These observations ultimately, advocates for further studies on sex-biased and development-biased thermal sensitivity before drawing any generalizations based on a single sex or life stage.

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“…Testing the effects of experimental warming on the behavior of ectotherms in late embryonic stages could help to elucidate their thermal tolerances and vulnerabilities under changing environmental conditions ( Collin et al. 2021 ; Vorsatz et al. 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…Oxygen availability and uptake capacity can limit thermal tolerance, and embryos may be particularly strongly affected ( Frederich and Pörtner 2000 ; Smith et al. 2015 ; Vorsatz et al. 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Heat-Induced Hatching of Red-Eyed Treefrog Embryos: Hydration and Clutch Structure Increase Behavioral Thermal Tolerance

Guevara-Molina

Gomes

Warkentin

2022

Integrative Organismal Biology

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Climate change is increasing both environmental temperatures and droughts. Many ectotherms respond behaviorally to heat, thereby avoiding damage from extreme temperatures. Within species, thermal tolerance varies with factors such as hydration as well as ontogenetic stage. Many tropical anurans lay terrestrial eggs, relying on environmental moisture for embryonic development. These eggs are vulnerable to dehydration, and embryos of some species can hatch prematurely to escape from drying eggs. Warmer temperatures can accelerate development, and thus hatching, but excess heat can kill embryos. Thus, we hypothesize that embryos may show a behavioral thermal tolerance limit, hatching prematurely to avoid potentially lethal warming. If so, because warming and drying are often associated, we hypothesize this limit, measurable as a voluntary thermal maximum, may depend on hydration. We manipulated hydration of the terrestrial eggs of Agalychnis callidryas, in intact clutches and egg-groups isolated from clutch jelly, then warmed them to assess if embryos hatch early as a behavioral response to high temperatures and whether their thermal tolerance varies with hydration or surrounding structure. We discovered that heating induces hatching; these embryos show a behavioral escape-hatching response that enables them to avoid potentially lethal warming. Hydrated eggs and clutches lost more water and warmed more slowly than dehydrated ones, indicating that hydration buffers embryos from environmental warming via evaporative cooling. Embryos in hydrated clutches tolerated greater warming before hatching and suffered higher mortality, suggesting their behavioral thermal safety margin is small. In contrast lower thermal tolerance protected dry embryos, and those isolated from clutch jelly, from lethal warming. Heat-induced hatching offers a convenient behavioral assay for thermal tolerance of terrestrial anuran embryos and the interactive effects of warming and dehydration at an early life stage. This work expands the set of threats against which embryos use hatching in self-defense, creating new opportunities for comparative studies of thermal tolerance as well as integrative studies of self-defense mechanisms at the egg stage.

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Thermal sensitivity in dual‐breathing ectotherms: Embryos and mothers determine species' vulnerability to climate change

Cited by 5 publications

References 40 publications

The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization

The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization

Temperature Extremes and Sex-Related Physiology, Not Environmental Variability, Are Key in Explaining Thermal Sensitivity of Bimodal-Breathing Intertidal Crabs

Heat-Induced Hatching of Red-Eyed Treefrog Embryos: Hydration and Clutch Structure Increase Behavioral Thermal Tolerance

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