Title: Thermal suppression of gametogenesis can explain historical collapses in larval recruitment in Strongylocentrotus purpuratus
Abstract Projections for population viability under climate change are often made using estimates of thermal lethal thresholds. These estimates vary across life history stages and can be valuable for explaining or forecasting shifts in population viability. However, sublethal temperatures can also depress vital rates and shape fluctuations in the reproductive viability of populations. For example, heatwaves may suppress reproduction, causing recruitment failure before lethal temperatures are reached. Despite a growing awareness of this issue, tying sublethal effects to observed recruitment failure remains a challenge especially in marine environments. For the urchinStrongylocentrotus purpuratus, larval supply is known to decline near the southern edge of the range during marine heatwaves despite temperatures remaining below temperatures thought to limit larval survival. We experimentally show that sublethal suppression of gametogenesis by marine heatwaves can partially explain these historical collapses in recruitment. This response differs by sex: male spermatogenesis is less sensitive to elevated temperatures and marine heatwaves than females who exhibit substantial reductions in production of mature oocytes. Results were similar between animals from warmer and cooler regions of their range. Overall, we show sublethal thermal sensitivities of reproduction can narrow the thermal envelope for population viability compared to predictions from lethal limits. more »« less
Okamoto, Daniel K; Spindel, Nathan B; Mustermann, Maya J; Karelitz, Sam; Collicutt, Brenna; Gimenez, Iria; Rolheiser, Kate; Cronmiller, Evan; Foss, Megan; Mahara, Natalie; et al
(, bioRxiv)
Inglis, John; Sever, Richard
(Ed.)
Abstract Projections for population viability under climate change are often made using estimates of thermal lethal thresholds. These estimates vary across life history stages and can be valuable for explaining or forecasting shifts in population viability. However, sublethal temperatures can also depress vital rates and shape fluctuations in the reproductive viability of populations. For example, heatwaves may suppress reproduction, leading to recruitment failure before lethal temperatures are reached. Despite a growing awareness of this issue, tying sublethal effects to observed recruitment failure remains a challenge especially in marine environments. We experimentally show that sublethal suppression of female gametogenesis by marine heatwaves can partially explain historical collapses in urchin recruitment. These responses differ by sex but are similar between animals from warmer or cooler regions of their range. Overall, we show sublethal thermal sensitivities of reproduction can narrow the thermal envelope for population viability compared to predictions from lethal limits.
Leach, Terence S.; Hofmann, Gretchen E.
(, Frontiers in Physiology)
Marine heatwave (MHW) events, characterized by periods of anomalous temperatures, are an increasingly prevalent threat to coastal marine ecosystems. Given the seasonal phenology of MHWs, the full extent of their biological consequences may depend on how these thermal stress events align with an organism’s reproductive cycle. In organisms with more complex life cycles (e.g., many marine invertebrate species) the alignment of adult and larval environments may be an important factor determining offspring success, setting the stage for MHW events to influence reproduction and development in situ . Here, the influence of MHW-like temperatures on the early development of the California purple sea urchin, Strongylocentrotus purpuratus , were explored within the context of paternal thermal history. Based on temperature data collected during MHW events seen in Southern California from 2014–2020, adult urchins were acclimated to either MHW or non-MHW temperatures for 28 days before their sperm was used to produce embryos that were subsequently raised under varying thermal conditions. Once offspring reached an early larval stage, the impact of paternal and offspring environments were assessed on two aspects of offspring performance: larval size and thermal tolerance. Exposure to elevated temperatures during early development resulted in larger, more thermally tolerant larvae, with further influences of paternal identity and thermal history, respectively. The alignment of paternal and offspring exposure to MHW temperatures had additional positive benefits on larval thermal tolerance, but this tolerance significantly decreased when their thermal experience mismatched. As the highest recorded temperatures within past MHW events have occurred during the gametogenesis of many kelp forest benthic marine invertebrate species, such as the purple sea urchin, such parental mediated impacts may represent important drivers of future recruitment and population composition for these species.
Okamoto, Daniel K.; Schroeter, Stephen C.; Reed, Daniel C.
(, Limnology and Oceanography)
Abstract Sea urchins are voracious herbivores that influence the ecological structure and function of nearshore ecosystems throughout the world. Like many species that produce planktonic larvae, their recruitment is thought to be particularly sensitive to climatic fluctuations that directly or indirectly affect adult reproduction and larval transport and survival. Yet how climate alters sea urchin populations in space and time by modifying larval recruitment and year‐class strength on the time‐scales that regulate populations remains understudied. Using a, spatially replicated weekly‐biweekly data set spanning 27 yr and 1100 km of coastline, we characterized seasonal, interannual, and spatial patterns of larval settlement of the purple sea urchin (Strongylocentrotus purpuratus). We show that large spatial differences in temporal patterns of larval settlement were associated with different responses to fluctuations in ocean temperature and climate. Importantly, we found a strong correlation between larval settlement and regional year class strength suggesting that such temporal and spatial variation in settlement plays an important role in controlling population dynamics. These results provide strong evidence over extensive temporal and spatial domains that climatic fluctuations shape broad‐scale patterns of larval settlement and subsequent population structure of an important marine herbivore known to control the productivity, community state, and provisioning services of marine ecosystems.
Abstract Marine heatwaves (MHWs) are projected to increase in intensity and frequency over the coming decades, and it is imperative to assess the adaptive capacity of marine organisms to these extreme temperature events. Given the nature of MHWs to last days to weeks in a region, these events may have overarching impacts on phenological events like reproduction and development. Here, the role of adult thermal history and transgenerational plasticity may be an important pathway by which MHWs are transduced to impact community structure. In this study, we sought to explore the effects of paternal thermal history in the purple urchin,Strongylocentrotus purpuratus, on a crucial aspect of reproduction, fertilization. Using ecologically relevant temperatures representative of both MHW events that occurred in 2014–2020 and non-MHW temperatures in our region of the California Large Marine Ecosystem, we conditioned maleS. purpuratusfor 28 days to either a high, MHW or a low, non-MHW temperature. Following the temperature acclimation of adults, sperm performance was tested for individual males by conducting fertilization success trials at varying temperatures and sperm concentrations. While sperm appeared robust to elevated temperature during fertilization, sperm produced by high-temperature-acclimated males had overall diminished performance as compared to those acclimated to non-MHW temperatures. These results suggest MHW events will have a negative impact on fertilization in situ forS. purpuratuspopulations. Furthermore, these results highlight the importance of considering both male and female environmental history in projections of reproduction under climate change scenarios.
Streeter, Margaret; Le_François, Nathalie R; Desvignes, Thomas; Grondin, Jacob; Postlethwait, John H; Detrich, H William; Daane, Jacob M
(, bioRxiv)
Abstract Rising ocean temperatures pose significant threats to marine ectotherms. Sensitivity to temperature change varies across life stages, with embryos often being less tolerant to thermal perturbation than adults. Antarctic notothenioid fishes evolved to occupy a narrow, cold thermal regime (−2 to +2°C) as the high-latitude Southern Ocean (SO) cooled to its present icy temperatures, and they are particularly vulnerable to small temperature changes, which makes them ideal sentinel species for assessing climate change impacts. Here, we detail how predicted warming of the SO may affect embryonic development in the Antarctic bullhead notothen,Notothenia coriiceps. Experimental embryos were incubated at +4°C, a temperature projected for the high-latitude SO within the next 100–200 years under high emission climate models, whereas control embryos were incubated at present-day ambient temperature, ∼0°C. Elevated temperature caused a high incidence of embryonic morphological abnormalities, including body axis kinking/curvature and reduced body size. Experimental embryos also developed more rapidly, such that they hatched 68 days earlier than controls (87 vs. 155 days post-fertilization). Accelerated development disrupted the evolved timing of seasonal hatching, shifting larval emergence into the polar winter when food availability is scarce. Transcriptomic analyses revealed molecular signatures of hypoxia and disrupted protein-folding in near-hatching embryos, indicative of severe cellular stress. Predictive modeling suggested that temperature-induced developmental disruptions would narrow seasonal reproductive windows, thereby threatening population viability under future climate scenarios. Together, our findings underscore the vulnerability of Antarctic fish embryos to higher water temperature and highlight the urgent need to understand the consequences of disruption of this important trophic component on ecosystem stability in the SO. Significance StatementAntarctic fishes evolved cold-adapted phenotypes suited to the stable thermal conditions of the Southern Ocean, yet are threatened by rising temperatures. The impact of rising temperatures on early life stages in Antarctic fishes is not well understood; our findings show that projected warming may induce premature hatching, developmental abnormalities, and molecular stress responses in embryos, potentially reducing recruitment and leading to population instability and trophic-level ecosystem disruptions. These results underscore the urgency of assessing climate-driven vulnerabilities across life stages of Antarctic marine organisms to refine population projections and enhance conservation strategies amid ongoing environmental change.
@article{osti_10645755,
place = {Country unknown/Code not available},
title = {Thermal suppression of gametogenesis can explain historical collapses in larval recruitment in Strongylocentrotus purpuratus},
url = {https://par.nsf.gov/biblio/10645755},
DOI = {10.1038/s42003-025-08829-8},
abstractNote = {Abstract Projections for population viability under climate change are often made using estimates of thermal lethal thresholds. These estimates vary across life history stages and can be valuable for explaining or forecasting shifts in population viability. However, sublethal temperatures can also depress vital rates and shape fluctuations in the reproductive viability of populations. For example, heatwaves may suppress reproduction, causing recruitment failure before lethal temperatures are reached. Despite a growing awareness of this issue, tying sublethal effects to observed recruitment failure remains a challenge especially in marine environments. For the urchinStrongylocentrotus purpuratus, larval supply is known to decline near the southern edge of the range during marine heatwaves despite temperatures remaining below temperatures thought to limit larval survival. We experimentally show that sublethal suppression of gametogenesis by marine heatwaves can partially explain these historical collapses in recruitment. This response differs by sex: male spermatogenesis is less sensitive to elevated temperatures and marine heatwaves than females who exhibit substantial reductions in production of mature oocytes. Results were similar between animals from warmer and cooler regions of their range. Overall, we show sublethal thermal sensitivities of reproduction can narrow the thermal envelope for population viability compared to predictions from lethal limits.},
journal = {Communications Biology},
volume = {8},
number = {1},
publisher = {Nature Publishing Group},
author = {Okamoto, Daniel_K and Spindel, Nathan_B and Munstermann, Maya_J and Karelitz, Sam and Collicutt, Brenna and Gimenez, Iria and Rolheiser, Kate and Cronmiller, Evan and Foss, Megan and Mahara, Natalie and Swezey, Dan and Ferraro, Rachele and Rogers-Bennett, Laura and Schroeter, Stephen_C},
}
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