In situ developmental responses of tropical sea urchin larvae to ocean acidification conditions at naturally elevated p CO ₂ vent sites

Abstract

Laboratory experiments suggest that calcifying developmental stages of marine invertebrates may be the most ocean acidification (OA)-sensitive life-history stage and represent a life-history bottleneck. To better extrapolate laboratory findings to future OA conditions, developmental responses in sea urchin embryos/larvae were compared under ecologically relevant in situ exposures on vent-elevated p CO 2 and ambient p CO 2 coral reefs in Papua New Guinea. Echinometra embryos/larvae were reared in meshed chambers moored in arrays on either venting reefs or adjacent non-vent reefs. After 24 and 48 h, larval development and morphology were quantified. Compared with controls (mean pH (T) = 7.89–7.92), larvae developing in elevated p CO 2 vent conditions (pH (T) = 7.50–7.72) displayed a significant reduction in size and increased abnormality, with a significant correlation of seawater pH with both larval size and larval asymmetry across all experiments. Reciprocal transplants (embryos from vent adults transplanted to control conditions, and vice versa ) were also undertaken to identify if adult acclimatization can translate resilience to offspring (i.e. transgenerational processes). Embryos originating from vent adults were, however, no more tolerant to reduced pH. Sea temperature and chlorophyll- a concentrations (i.e. larval nutrition) did not contribute to difference in larval size, but abnormality was correlated with chlorophyll levels. This study is the first to examine the response of marine larvae to OA scenarios in the natural environment where, importantly, we found that stunted and abnormal development observed in situ are consistent with laboratory observations reported in sea urchins, in both the direction and magnitude of the response.

Little evidence of adaptation potential to ocean acidification in sea urchins living in “Future Ocean” conditions at a CO2 vent

“…This was despite a low pH that is similar to that expected at the end of this century (Uthicke et al, ). By contrast, in situ Echinometra larval growth studies in these sites showed that exposure to future OA conditions can lead to stunted and abnormal growth (Lamare et al, ). This is in agreement with previous laboratory studies on the same genus (Uthicke, Soars, et al, ) and on a wide variety of sea urchins from tropical to arctic regions (Byrne et al, ).…”

“…In fact, there are a number of studies that point to the potential for adaptation to reduced pH across a range of invertebrate taxa, for example, in bivalves (Zhao et al, ), crustaceans (Thor & Dupont, ) and echinoderms (Kelly, Padilla‐Gamiño, & Hofmann, ). Similarly, experimentation on taxa living in naturally occurring CO 2 vent communities can increase our understanding of the acclimation potential of species both within (Uthicke et al, ) and across generations (Lamare, Liddy, & Uthicke, ).…”

“…The effects of OA on adult Echinometra growth depend on species and experimental setup. A strong decline in growth with increasing P co 2 was reported for a Caribbean species (Courtney, Westfield, & Ries, ), and Echinometra species often demonstrated a reduction in growth of the larval skeleton with increased P co 2 and more asymmetric larvae (Kurihara & Shirayama, ; Lamare et al, ; Uthicke, Soars, Foo, & Byrne, ). By contrast, the effects on several Indo‐Pacific species were only subtle (Uthicke, Liddy, Nguyen, & Byrne, ; Uthicke, Soars, et al, ) or were not detected (Hazan, Wangensteen, & Fine, ; Moulin et al, ; Moulin, Grosjean, Leblud, Batigny, & Dubois, ).…”

“…Vents used for these studies now include Mediterranean rocky shores (Hall‐Spencer et al, ), White Island New Zealand (Nagelkerken, Russell, Gillanders, & Connell, ), and Mariana Islands and Papua New Guinea (PNG) for coral reef environments (Enochs et al, ; Fabricius et al, ). We previously investigated sea urchin adult growth (Uthicke et al, ) and larval development (Lamare et al, ) in Echinometra sp. C at the well‐studied vent sites on Papua New Guinean coral reefs.…”

Effects of ocean warming and acidification on fertilization success and early larval development in the green sea urchin Lytechinus variegatus

“…Specifically, genes central to energy metabolism and biomineralization are downregulated in larvae of L. variegatus and other sea urchins reared in a lower pH, reducing growth rates (O'Donnell et al 2010, Stumpp et al 2011, Raven et al 2005, Kroeker et al 2010), i.e., larvae have smaller total body and average rod lengths. In addition, decreased pH also causes an increase in asymmetry in L. variegatus and other sea urchin larvae (Byrne et al 2013a, Uthicke et al 2013, Lamare et al 2016. Under low pH, larvae allocate the few available calcium carbonate ions disproportionally between rods leading one rod to grow more than the other.…”