Armstrong Et Al, 2017

Mar Biol (2017) 164:107 DOI 10.1007/s00227-017-3133-x ORIGINAL PAPER High pCO2 and elevated temperature reduce survival and alter development in early life stages of the tropical sea hare Stylocheilus striatus Eric J. Armstrong1,2 · Trevor R. Allen1 · Maeva Beltrand3,4 · Vaimiti Dubousquet3,4,5 · Jonathon H. Stillman1,2 · Suzanne C. Mills3,4 Received: 3 November 2016 / Accepted: 30 March 2017 © Springer-Verlag Berlin Heidelberg 2017 Abstract Elevated temperature (ocean warming) and high pCO2) resulted in accelerated development, with lar- reduced oceanic pH (ocean acidifcation) are products vae reaching several developmental stages approximately of increased atmospheric pCO2, and have been shown in 48 h in advance of controls. Hatching success was reduced many marine taxa to alter morphology, impede develop- by ~20 and 55% under high pCO2 and warming, respec- ment, and reduce ftness. Here, we investigated the effects tively, while simultaneous exposure to both conditions of high pCO2 and elevated temperature on developmental resulted in a nearly additive 70% reduction in hatching. In rate, hatching success, and veliger morphology of embryos addition to these ontological and lethal effects, exposure of the tropical sea hare, Stylocheilus striatus. Exposure to of embryos to climate change stressors resulted in signif- high pCO2 resulted in signifcant developmental delays, cant morphological effects. Larval shells were nearly 40% postponing hatching by nearly 24 h, whereas exposure to smaller under high pCO2 and warming in isolation and up elevated temperature (in isolation or in combination with to 53% smaller under multi-stressor conditions. In general, elevated temperature had the largest impact on develop- Responsible Editor: H.-O. Pörtner. ment, with temperature-effects nearly 3.5-times the magnitude of high pCO2-effects. These results indicate that oce- Reviewed by Undisclosed experts. anic conditions congruent with climate change predictions for the end of the twenty-frst century suppress successful Electronic supplementary material The online version of this article (doi:10.1007/s00227-017-3133-x) contains supplementary development in S. striatus embryos, potentially reducing material, which is available to authorized users. their viability as pelagic larvae. Eric J. Armstrong and Trevor Allen have contributed equally to this work. Introduction * Eric J. Armstrong [email protected] Decreased oceanic pH (ocean acidifcation) is a product of increased atmospheric pCO , and has been shown in many 1 2 Department of Integrative Biology, University of California, taxa to lead to altered developmental timelines (Stumpp Berkeley, 3040 Valley Life Sciences Building #3140, Berkeley, CA 94720, USA et al. 2011), inhibition of growth (Stumpp et al. 2011; Dorey et al. 2013), malformations in calcitic exoskeletons 2 Romberg Tiburon Center for Environmental Studies, San Francisco State University, Tiburon, CA, USA (Gazeau et al. 2013), and reduced larval ftness (Kroeker et al. 2010). However, the magnitude of these effects can 3 EPHE PSL Research University, USR 3278 CRIOBE CNRS- UPVD, BP 1013, 98729 Mo’orea, French Polynesia vary signifcantly both across taxa (Kroeker et al. 2010; Harvey et al. 2013) and across life history stages within a 4 Laboratoire d’Excellence “CORAIL”, Mo’orea, French Polynesia species (Kurihara 2008; Harvey et al. 2013). Early life history stages are often the most susceptible to acute changes 5 Département de recherche agronomique appliquée, Service du développement rural, BP 100, 98713 Papeete, French in the environment and frequently require a narrower Polynesia range of optimal conditions to successfully complete their 1 3 107 Page 2 of 14 Mar Biol (2017) 164:107 development (Kurihara 2008). Mortality in such stages can 2013); however, less focus has been directed to the impact be extremely high (>90%) even under ambient natural con- of multiple other stressors acting in concert with acidifca- ditions (Kurihara 2008) and thus sensitive early life history tion on calcifying organisms (Harvey et al. 2013; Kroeker stages may represent important bottlenecks for population et al. 2013; Breitburg et al. 2015). For example, increas- growth and persistence under a changing climate (Byrne ing atmospheric pCO2 has also resulted in ocean warm- and Przeslawski 2013). ing which has already had severe consequences for several In several marine taxa studied to date, exposure to acidi- taxa, resulting in shifted biogeographic range distributions fcation stress during early development is associated with and altered ftness (Stillman and Armstrong 2015). Fur- developmental delays (Dupont and Thorndyke 2009; Busby ther, there is mounting evidence that tropical species may et al. 2013) which, for species with planktonic larvae, is be especially sensitive to warming (Stillman 2003; Tewks- likely to have negative ecological consequences through bury et al. 2008; van Heerwaarden et al. 2016) as a result increased risk of loss to predation and delayed settlement of physiological trade-offs incurred in the evolution of high opportunity (Timmins-Schiffman et al. 2013). Indeed, early inherent tolerance limits at the expensive of thermal toler- stage larvae of marine calcifers are thought to be espe- ance plasticity. Such trade-offs may result from thermal cially susceptible to ocean acidifcation for at least two specialization of individual enzymes which are adapted to reasons: frst, developing larvae may have reduced capacity operate at higher temperatures but which lose functionality for compensatory acclimation relative to adults under acidi- more rapidly as the environment warms (Hochachka and fcation stress (Dupont et al. 2008; Kurihara 2008; ‎Pörtner Somero 2002) or because warm-adaptation alters under- et al. 2011), and second, initiation of mineral deposition in lying metabolic processes (e.g. mitochondrial densities or larval forms is thought to begin with a thin layer of amor- oxygen demand) resulting in insuffcient oxygen-supply phous CaCO3 which is the least robust form of CaCO3 and capacity under increasing environmental temperatures highly prone to dissolution (Gazeau et al. 2013). Negative (Pörtner et al. 2006). Whatever the mechanism, patterns of effects of ocean acidifcation on embryonic or larval cal- thermal trade-offs associated with warm-adaptation are per- cifcation have been observed in multiple taxa including vasive and have been observed in many taxa (Deutsch et al. several species of gastropod molluscs (Gazeau et al. 2013; 2008; Tewksbury et al. 2008). However, little is known Manríquez et al. 2014; Noisette et al. 2014), but rarely in about how this potential thermal sensitivity might affect gastropods with encapsulated embryos (Ellis et al. 2009; resilience to other stressors such as ocean acidifcation dur- Manríquez et al. 2014; Montory et al. 2009; Noisette et al. ing simultaneous exposure. In a recent study on tropical 2014) and fewer still investigating the effects of multiple littorinid and opisthobranch molluscs, simultaneous expo- stressors (Harvey et al. 2013; Kroeker et al. 2013). sure to moderate warming reduced the negative impacts of Although embryonic shell development in free-swim- acidifcation on development suggesting that responses of ming gastropod larvae is susceptible to sustained exposure tropical species to mutliple stressors may be complex and, to high pCO2 (Kurihara 2008; Gazeau et al. 2013), such therefore, diffcult to predict a priori (Davis et al. 2013). effects have not been well-studied in species with encapsu- We examined the effects of multiple environmental lated embryos where intracapsular fuids may buffer against stressors (elevated temperature and increased pCO2) on external environmental stressors such as reduced pH and development and survival in early life stages of the circum- lower carbonate ion availability (Ellis et al. 2009; Noisette tropical, capsule-laying opisthobranch sea hare, Stylochei- et al. 2014). In several studies performed to date on acidi- lus striatus (Family Aplysiidae). Gastropods, in particular fcation response of encapsulating gastropods (Crepidulata sea hares, play an important role in benthic reef ecology fornicata, C. dilatata, Littorina obtusata, Concholepas as specialist grazers on toxic cyanobacteria that prevent concholepas, Bembicium nanum, and Dolabifera brazier), the settlement of coral larvae (Kuffner and Paul 2004) encapsulation did not signifcantly reduce the effects of and can cause phase shifts from coral to algal dominated acidifcation on embryonic calcifcation and development reefs (Thacker et al. 2001). Early developmental stages of (Ellis et al. 2009; Montory et al. 2009; Davis et al. 2013; S. striatus have been described (Horwitz et al. 2017) and Manríquez et al. 2014; Noisette et al. 2014). However, in are known to be sensitive to anthropogenic noise pollution, other groups (e.g. polychaetes) negative effects of acidifca- suffering impaired development and increased mortality tion have been shown to be ameliorated through parental among larval hatchlings (Nedelec et al. 2014), but whether investment in brooding or maintenance of embryos in pro- they are susceptible to other environmental stressors is tective egg casings (Lucey et al. 2015). unknown. We hypothesized that (1) despite encapsulation, Recent meta-analyses have highlighted the complex elevated pCO2 will reduce viability of S. striatus embryos, responses of organisms to acidifcation stress in isolation via potential reductions in development rate, net

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