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Ecol Evol
2017 Mar 01;76:1737-1750. doi: 10.1002/ece3.2776.
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Sensitivity of sea urchin fertilization to pH varies across a natural pH mosaic.
Kapsenberg L
,
Okamoto DK
,
Dutton JM
,
Hofmann GE
.
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In the coastal ocean, temporal fluctuations in pH vary dramatically across biogeographic ranges. How such spatial differences in pH variability regimes might shape ocean acidification resistance in marine species remains unknown. We assessed the pH sensitivity of the sea urchin Strongylocentrotus purpuratus in the context of ocean pH variability. Using unique male-female pairs, originating from three sites with similar mean pH but different variability and frequency of low pH (pHT ≤ 7.8) exposures, fertilization was tested across a range of pH (pHT 7.61-8.03) and sperm concentrations. High fertilization success was maintained at low pH via a slight right shift in the fertilization function across sperm concentration. This pH effect differed by site. Urchins from the site with the narrowest pH variability regime exhibited the greatest pH sensitivity. At this site, mechanistic fertilization dynamics models support a decrease in sperm-egg interaction rate with decreasing pH. The site differences in pH sensitivity build upon recent evidence of local pH adaptation in S. purpuratus and highlight the need to incorporate environmental variability in the study of global change biology.
Figure 1. Conceptual diagram describing the climate variability hypothesis. In the context of ocean acidification, the environmental parameter is pH. As low pH exposures increase in frequency and the pH variability envelope widens (Site 2), the pH range within which organismal physiology must operate also widens. Through local environmental conditioning or natural selection, this may cause spatial differences in a species’ tolerance window across its biogeographic range (dashed lines)
Figure 2. Map of study sites in the California Current Large Marine Ecosystem (a) and normal fertilization (NF) functions of Strongylocentrotus purpuratus from those sites by pH treatment (b). Sites span >10° latitude from Oregon (FC) to California (BMR, SB) and exhibit similar mean pH values but unique pH variability regimes as described by percent of pH observations ≤7.80 and coefficient of variation (CV) of pH sensor observations (FC and BMR, Aprilâ€October, 2011–2013; SB, 2012–2015). For the NF functions (b), the gray band with dotted line represents the “global†normal fertilization curve (pooled site and pH treatment) at the 95% confidence interval, while points and thin lines represent mean site–pH treatment combinations. Extreme outliers under the fertilization curve originate largely from two pairs from BMR
Figure 3. Proportion total fertilization over a range of sperm concentrations for Strongylocentrotus purpuratus from FC, BMR, and SB by pH treatment (colors are the same as in Figure 2b). The dotted line represents the global mean estimate. Solid, thick lines represent the site–pH treatment level estimates with the 95% confidence interval as the colored band. Thin, solid lines represent unique pair estimates (i.e., random effects) for each site–pH treatment. The horizontal line denotes 50% total fertilization. Only three pH treatments were tested per site
Figure 4. Proportion abnormal fertilization over a range of sperm concentrations for Strongylocentrotus purpuratus from FC, BMR, and SB by pH treatment (colors are the same as in Figure 2b). The dotted line represents the global mean estimate. Solid, thick lines represent the site–pH treatment level estimates with the 95% confidence interval as the colored band. Thin, solid lines represent unique pair estimates (i.e., random effects) for each site–pH treatment. The horizontal line denotes 25% abnormal fertilization. Only three pH treatments were tested per site
Figure 5. Estimated sperm concentrations required to reach 50% normal fertilization (SNF
50), optimal normal fertilization (SO
pt
NF), and 25% abnormal fertilization (SA
bnF25) under different pH treatments (yâ€axis), for Strongylocentrotus purpuratus from FC, BMR, and SB. Points within a populationâ€metric combination that do not share a common letter within a metric are significantly different (α = 0.017, following a Bonferroni correction for three comparisons under a parametric bootstrap). Those with no letters indicate no significant differences among treatments (within site, per metric). Percentages are the estimated peak levels of normal fertilization. Error bars are 95% confidence intervals estimated via parametric bootstrap. Colors are the same as in Figure 2b
Figure 6. Parameter estimates for the instantaneous per capita sperm–egg interaction rate (per no., per second, aâ€c) and polyspermy block rate (per second, dâ€f) by pH treatment, for Strongylocentrotus purpuratus from FC (a, d), BMR (b, e), and SB (c, f), using the mechanistic model of Okamoto (2016). Large symbols represent amongâ€pair means with 95% posterior credibility intervals (error bars) and horizontal dashes are the pairâ€specific mean estimates. Asterisk denotes mean estimates with >95% posterior probability of a decline compared to the ambient (pHT = 8.03) treatment. Colors are the same as in Figure 2b
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