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PLoS One
2022 Jan 01;1712:e0276134. doi: 10.1371/journal.pone.0276134.
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The effects of temperature and pH on the reproductive ecology of sand dollars and sea urchins: Impacts on sperm swimming and fertilization.
Leuchtenberger SG
,
Daleo M
,
Gullickson P
,
Delgado A
,
Lo C
,
Nishizaki MT
.
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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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36454769
???displayArticle.pmcLink???PMC9714736 ???displayArticle.link???PLoS One
Fig 1. Sand dollar embryos 3 hours post-fertilization.(A). fertilized and unfertilized embryos at 50× magnification. (B). Close up at 112× magnification highlighting fertilization membrane. Z-stack images were captured using an Axio Zoom V16 stereo microscope equipped with an Axiocam 506 color camera (Zeiss, Germany).
Fig 2. Effect of water temperature on reproductive traits of sand dollars, Dendraster excentricus.(A). fertilization rates, (B). sperm curvilinear velocity, and (C). proportion of sperm that were motile. Data for the three traits were fitted with non-linear functions (quadratic, modified gaussian and gaussian respectively) and plotted with 95% confidence intervals (shaded areas) determined by residual bootstrapping [102].
Fig 3. Effect of water temperature on reproductive traits of red urchins, Mesocentrotus franciscanus.(A). fertilization rates (B). sperm swimming velocity, and (C). proportion of sperm that are motile. Data were fitted with non-linear functions (modified gaussian for fertilization, quadratic for sperm velocity and motility) and plotted with 95% confidence intervals (shaded areas) determined by residual bootstrapping [102].
Fig 4. Estimates for derived parameters from thermal performance curves of sand dollar and sea urchin reproductive traits.Reproductive parameters include rmax = maximum rate, Topt = thermal optimum, and Breadth = thermal breadth in panels A-C respectively. Error bars represent the 95% bootstrap confidence intervals.
Fig 5. Combined effects of temperature and pH on reproductive traits of sand dollars, Dendraster excentricus.(A). fertilization rate, (B). sperm curvilinear velocity and, (C). sperm motility. N = 3 adult pairs. Error bars represent 1 SE.
Fig 6. Comparison of empirical and modelled fertilization rates in single factor experiments.Fertilization responses to sperm swimming velocity (panels A, D), motility (panels B, E) and water temperatures (panels C, F). Top row are for sand dollars and bottom row are for sea urchins. Lines represent estimates from fertilization kinetics model [97, 109] parameterized with swimming velocities and symbols represent empirical fertilization rates from this study.
Fig 7. Comparison of empirically measured versus modelled sand dollar fertilization rates.Fertilization responses to: (A). sperm swimming velocity; (B). sperm motility; (C). water temperature and; (D) pH. Lines represent estimates from fertilization kinetics model parameterized with swimming velocities and symbols represent empirical fertilization rates from this study [97, 109].
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