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Juvenile Growth of the Tropical Sea Urchin Lytechinus Variegatus Exposed to Near-Future Ocean Acidification Scenarios

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Juvenile Growth of the Tropical Sea Urchin Lytechinus Variegatus Exposed to Near-Future Ocean Acidification Scenarios Journal of Experimental Marine Biology and Ecology 426–427 (2012) 12–17 Contents lists available at SciVerse ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe Juvenile growth of the tropical sea urchin Lytechinus variegatus exposed to near-future ocean acidification scenarios Rebecca Albright a,⁎, Charnelle Bland a, Phillip Gillette a, Joseph E. Serafy a,b, Chris Langdon a, Thomas R. Capo a a Rosenstiel School of Marine and Atmospheric Science, Division of Marine Biology and Fisheries, 4600 Rickenbacker Causeway, University of Miami, Miami, FL 33149, USA b National Marine Fisheries Service, SEFSC, 75 Virginia Beach Drive, Miami, FL 33149, USA article info abstract Article history: To evaluate the effect of elevated pCO2 exposure on the juvenile growth of the sea urchin Lytechinus variegatus, Received 8 March 2012 we reared individuals for 3 months in one of three target pCO2 levels: ambient seawater (380 μatm) and two Received in revised form 15 May 2012 scenarios that are projected to occur by the middle (560 μatm) and end (800 μatm) of this century. At the end Accepted 18 May 2012 of 89 days, urchins reared at ambient pCO weighed 12% more than those reared at 560 μatm and 28% more Available online 8 June 2012 2 than those reared at 800 μatm. Skeletons were analyzed using scanning electron microscopy, revealing degra- dation of spines in urchins reared at elevated pCO (800 μatm). Our results indicate that elevated pCO levels Keywords: 2 2 fi Carbon dioxide projected to occur this century may adversely affect the development of juvenile sea urchins. Acidi cation- CO2 induced changes to juvenile urchin development would likely impair performance and functioning of juvenile Development stages with implications for adult populations. Echinoderm © 2012 Elsevier B.V. All rights reserved. Invertebrate pCO2 pH 1. Introduction Sea urchins are one of the most heavily studied groups of organ- isms with respect to ocean acidification, and early life history stages As a result of oceanic uptake of atmospheric carbon dioxide, the are thought to be particularly vulnerable to changing water chemistry world's oceans are slowly becoming more acidic (ocean acidification, (Dupont and Thorndyke, 2009; Kurihara, 2008). To date, the majority OA). Approximately 30% (148 Pg C) of anthropogenic CO2 emissions of work evaluating the effects of ocean acidification on early life his- have been absorbed by the oceans (Sabine et al., 2011). Consequently, tory stages of urchins has focused on pre-metamorphic processes in- seawater carbonate concentrations have been depleted by cluding pre-larval (e.g., fertilization, embryonic development) and ~30 μmol kg−1, simultaneously reducing the pH of the ocean's surface larval stages (Table 1). While increasing information is available on waters by 0.1 units relative to the pre-industrial era (a 30% increase in the effects of ocean acidification on pre-metamorphic life history acidity) (IPCC, 2007). Further reductions of 0.3–0.5 pH units are projec- stages of sea urchins, there is a clear lack of information regarding ted to occur by the end of this century as the oceans continue to absorb the sensitivity of post-metamorphic (i.e., juvenile) stages. Only two anthropogenic CO2 (IPCC, 2007). studies to date have evaluated the effect(s) of elevated pCO2 exposure Documenting and predicting the response(s) of various marine or- on juvenile urchin growth. Shirayama and Thornton (2005) reported ganisms to changing ocean chemistry has been of recent concern in decreased juvenile growth of two species of urchin, Echinometra the scientific community. Mounting experimental evidence suggests mathaei and Hemicentrotus pulcherrimus, during six-months exposure that ocean acidification may hold negative consequences for a variety to elevated pCO2 (560 μatm). Increased mortality was also reported in of marine organisms (Gattuso and Hansson, 2011), primarily one of two trials. Byrne et al. (2011) reported an increased number of calcifiers that depend on the delicate balance of inorganic carbon spe- abnormal Heliocidaris erythrogramma juveniles exposed to depressed cies to form their CaCO3 shells or skeletons (Doney et al., 2009; Fabry pH (−0.2 and −0.4 pH units) and elevated temperature (+2 °C and et al., 2008; Kroeker et al., 2010). +4 °C). Metamorphosis marks the transition from a planktonic larva to a benthic juvenile and as such, larvae and juveniles differ substan- tially with respect to their morphology, physiology, and ecology and ⁎ Corresponding author at: Australian Institute of Marine Science, Townsville MC, may differ in susceptibility to environmental stressors such as ocean Townsville QLD 4810, Australia. Tel.: +61 7 4753 4140 (Office). acidification. It is, therefore, important to better understand post- E-mail addresses: [email protected] (R. Albright), [email protected] (C. Bland), [email protected] (P. Gillette), [email protected] (J.E. Serafy), metamorphic susceptibility to OA to couple with our growing knowl- [email protected] (C. Langdon), [email protected] (T.R. Capo). edge of pre-metamorphic effects. 0022-0981/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2012.05.017 Table 1 Compilation of recent studies investigating the effects of ocean acidification (pH change) on early life history stages of sea urchins. This listing is restricted to comprehensive studies for which methods, data, and statistical analyses are available and is focused on studies conducted over the last decade, under the context of near-future ocean acidification scenarios. Life stage abbreviations are as follows: PL=pre-larval (fertilization and/or embryogenesis); L=larval; J=juvenile. Taxon Life stage CO2 or HCl (ppm) pH Temp °C Exposure Effect Source period Echinometra mathaei PL, L HCl and CO2 (365–10,360) 6.8–8.1 3 days pHb7.8, skeletal malformation, reduced larval size and fertilization Kurihara and Shirayama, 2004 b Echinometra mathaei JCO2 (ambt., 560) 7.90, 7.94 30 6 months Decreased growth at 12 week; mortality in 1 of 2 expts. Shirayama and Thornton, 2005 R. Albright et al. / Journal of Experimental Marine Biology and Ecology 426 Hemicentrotus pulcherrimus PL, L HCl and CO2 6.8–8.0 3 days pHb7.8, skeletal malformation, reduced larval size and fertilization Kurihara and Shirayama, 2004 (365–10,360) Hemicentrotus pulcherrimus JCO2 (ambt., 560) 7.90, 7.94 b30 6 months Decreased growth at 14 week; mortality in 1 of 2 expts. Shirayama and Thornton, 2005 Heliocidaris erythrogramma PL CO2 (ambt.,1000) 7.7, 8.1 20.5 24 h Decreased sperm motility, swimming speed, and fertilization Havenhand et al., 2008 Heliocidaris erythrogramma PL CO2 (230–690) 7.6–8.2 20–26 4 days No effect of CO2 on fertilization or development; T effect on development, Byrne et al., 2009 not fertilization; no T*CO2 interaction Heliocidaris erythrogramma PL CO2 (370, 1100, 1850) 7.6–8.2 20–26 2 h No effect of T or CO2 on fertilization Byrne et al., 2010a Strongylocentrotus PL CO2 (400, 800, 1800) 7.6, 7.8, 8.0 10 3 h Decreased fertilization efficiency; increased susceptibility to polyspermy at Reuter et al., 2010 franciscanus 1580 ppm; CO2 effect dependent on sperm concentration Strongylocentrotus PL, L CO2 (380, 540, 970) 7.87, 7.98, 8.04 15, 19, 21, 23, ~96 h Gametes (larvae) fertilized (reared) at elevated CO2 showed reduced O'Donnell et al., 2009 franciscanus 25, 27, 29, 31 expression of heat shock proteins in response to acute T stress (1 h); T of max. induction was shifted Strongylocentrotus purpuratus LCO2 (380, 540, 1020) 7.88, 7.96, 8.01 15 b72 h Decreased gene expression in 4 major cellular processes: biomineralization, Todgham and Hofmann, 2009 cellular stress response, metabolism, apoptosis Tripneustes gratilla LCO2 (450, 1200, 1900) 8.15, 7.8, 7.6 24, 27, 30 5 days pCO2 decreased larval growth; Tb30 °C increased growth; interaction of Sheppard Brennand et al., 2010 — – CO2 *T 3° warming (24° 27°) diminished CO2 effect Tripneustes gratilla LCO2 (395–1119) 6.0–8.1 26 4 days Decreased calcification and size; no effect on fine skeletal morphology; Clark et al., 2009 (tropical spp.) decreased survival at pHb7.0 Pseudechinus huttoni LCO2 (429–1282) 6.0–8.1 10–15 9 days Decreased calcification and size; degradation of fine skeletal morphology; Clark et al., 2009 (temp. spp.) decreased survival at pHb7.0 Evechinus chloroticus LCO2 (438–1320) 6.0–8.1 10–15 13 days Decreased calcification and size; degradation of fine skeletal morphology; Clark et al., 2009 (temp. spp.) decreased survival at pHb7.0 Sterechinus neumayeri LCO2 (521–1380) 6.0–8.1 −1 7 days No effect on calcification; no effect on fine skeletal morphology; Clark et al., 2009 (polar spp.) decreased survival at pHb7.0 – Lytechinus pictus LCO2 (380, 540, 970) 7.78, 7.87, 7.93 18.5 6 days Altered larval size, shape; down-regulation of genes central to energy O'Donnell et al., 2010 427 (2012) 12 metabolism, biomineralization; up-regulation of genes involved in ion regulation and acid–base balance pathways Paracentrotus lividus PL, L CO2 (400, 700, 1100, 7.0, 7.25, 7.5, 20 3 days No effect on fertilization or larval survival; slowed larval growth at low pH; Martin et al., 2011 1900, 3600, 6600) 7.7, 7.9, 8.1 upregulation of development and biomineralization candidate genes Heliocidaris erythrogramma PL CO2 (330–1828) 7.6–8.25 18–26 15 min No effect of T or CO2 on fertilization at the sperm concentration used Byrne et al., 2010b – 17 Heliocidaris tuberculata PL CO2 (330–1828) 7.6–8.25 18–26 15 min No effect of T or CO2 on fertilization at the sperm concentration used Byrne et al., 2010b Tripneustes gratilla PL CO2 (330–1828) 7.6–8.25 18–26 15 min No effect of T or CO2 on fertilization at the sperm concentration used Byrne et al., 2010b Centrostephanus rodgersii PL CO2 (330–1828) 7.6–8.25 18–26 15 min No effect of T or CO2 on fertilization at the sperm concentration used Byrne et al., 2010b Strongylocentrotus purpuratus LCO2 (375, 1264) 7.7, 8.1 14 21 days.
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