2020 Sub Lethal Predatory Shell Damage
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Sub-lethal predatory shell damage does not affect physiologyunder high ANGOR UNIVERSITY CO2 in the intertidal gastropod Tritia reticulata Yokoyama, Leonardo; Turra, Alexander; Suckling, Coleen; Torres, Gabriela; Davies, Andrew; McCarthy, Ian Ocean and Coastal Management DOI: https://doi.org/10.1590/s2675-28242020068274 PRIFYSGOL BANGOR / B Published: 01/01/2020 Publisher's PDF, also known as Version of record Cyswllt i'r cyhoeddiad / Link to publication Dyfyniad o'r fersiwn a gyhoeddwyd / Citation for published version (APA): Yokoyama, L., Turra, A., Suckling, C., Torres, G., Davies, A., & McCarthy, I. (2020). Sub-lethal predatory shell damage does not affect physiologyunder high CO in the intertidal gastropod Tritia reticulata. 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Sep. 2021 OCEAN AND COASTAL ORIGINAL ARTICLE http://dx.doi.org/10.1590/S2675-28242020068274 RESEARCH Sub-lethal predatory shell damage does not affect physiology under high CO2 in the intertidal gastropod Tritia reticulata Leonardo Querobim Yokoyama1,2* , Alexander Turra1, Coleen Suckling3,4, Gabriela Torres3,5, Andrew Davies3,6, Ian McCarthy3 1 Instituto Oceanográfico, Universidade de São Paulo, Laboratório de Manejo, Ecologia e Gestão Costeira, Departamento de Oceanografia Biológica (Praça do Oceanográfico, 191 - Butantã - SP - 05508-120 - Brazil) 2 Universidade Federal de São Paulo, Laboratório de Ecologia e Gestão Costeira, Instituto do Mar (Rua Carvalho de Mendonça, n° 144 - Santos - SP - 11070-100 - Brazil) 3 Bangor University, School of Ocean Sciences (Menai Bridge, Anglesey, LL59 5AB, United Kingdom) 4 University of Rhode Island, Department of Fisheries, Animal and Veterinary Sciences (129 Woodward Hall, 9 East Alumni Avenue, Kingston, RI 02881 - United States) 5 Alfred-Wegener-Institute, Helmholtz Centre for Polar and Marine Research (Biologische Anstalt Helgoland Postfach 180 27483- Helgoland - Germany) 6 University of Rhode Island, Department of Biological Sciences, (Kingston - RI 02881 - United States) *Corresponding author: [email protected] ABSTRACT Ocean acidification (OA) poses a major threat to marine animals, especially marine shelled invertebrates such as molluscs. Although many organisms are capable of compensating for the effects of OA, this can impose physiological costs and impact performance (e.g. through increased metabolism and decreased growth). Sublethal injuries on shells may provoke changes in energy allocation. Under acidified conditions, organisms would spend less energy on reproduction and somatic growth to repair the damage. Therefore, we analysed the physiological responses of the intertidal gastropod Tritia reticulata during shell regeneration under OA conditions. We simulated a sub-lethal predation event (a notch in the outer lip of the shell) and individuals were exposed to control (pH 8.08) and low pH scenarios (pH 7.88 and 7.65). After two months exposure, all individuals showed shell repair, with a full repair rate observed in 75% of individuals. Contrary to expectations, shell repair following sub-lethal damage and OA had no apparent impact on physiological state in terms of energy reserves (as measured by whole-animal Carbon/Nitrogen) or growth potential (as measured by whole-animal RNA:Protein and RNA:DNA ratios). As an intertidal organism, T. reticulata could be resilient to future global environmental change because of compensatory mechanisms that are inherent in intertidal animals, and may represent a robust species with which to study future scenarios of OA in temperate coastal ecosystems. However, unrestricted food availability during experiment could have played a role in the results and therefore food limitation should be considered in future studies regarding shell repair and metabolism under the effects of OA. Descriptors: Ocean acidification, Metabolism, Intertidal, Gastropod, Shell repair. INTRODUCTION more energy on buffering their acid-base relation- ship (Sokolova et al., 2012). However, OA can also One of the biggest threats of ocean acidification affect biological processes such as growth (Harris (OA) is the need for marine organisms to expend et al., 1999), reproduction (Suckling et al., 2015), development (Dupont et al., 2008; Brennand et al., Submitted on: 27/June/2019 2010) and calcification of hard skeleton structures Approved on: 17/March/2020 (Courtney et al., 2013). Molluscs are one of the taxa Editor: Rubens M. Lopes with the greatest potential to be affected by acidifi- cation since molluscs shells are composed of calcium © 2019 The authors. This is an open access article distributed under the terms of the Creative Commons license. carbonate (calcite and/or aragonite; Addadi et al., Ocean and Coastal Research 2020, v68:e20274 1 Yokoyama et al.: Ocean acidification and Tritia reticulata 2006). Acidification alters the saturation state of cal- is a common gastropod species from European cium carbonate (CaCO3), which hinders CaCO3 extrac- coastal waters (Barroso et al., 2005a), occurring on tion from the water and elevates the dissolution of shallow sandy bottoms and in intertidal rock pools skeletal CaCO3 (Watson et al., 2012). Amongst marine (Tallmark, 1980). As a scavenger benthic species, it is Gastropoda, the responses to increased pCO2 (caus- responsible for diagenetic processes in surface sedi- ing pH reduction) have varied depending on species ments, because of its movements in the surface layer, and duration of exposure with no consensus on or- where organic matter is more abundant (Donazzolo ganismal response (see review by Parker et al., 2013). et al., 1989). The biology and ecology of T. reticulata Reduction in growth and calcification under acidified has been well studied (Tallmark, 1980; Barroso et al., environments is expected (Shirayama and Thorton, 2005a, 2005b; Chatzinikolaou and Richardson, 2007, 2005), but some species are capable of raising their 2008) but the effects of OA are not known although calcification rates (Langer et al., 2014) whereas other they have been studied for closely-related Nassarius species maintain the deposition of CaCO3, although at spp. (Zhang et al., 2014, 2015, 2016). T. reticulata can the cost of their metabolic rates (Findlay et al., 2011). vary shell growth and thickening depending on lo- Similarly, physiological responses to increased pCO2 cation and in areas protected from wave action and varies in gastropods with negative (Bibby et al., 2007; with high abundance of predators it tends to pro- Harvey et al., 2016), positive (Harvey et al., 2016) and duce thicker shells (Chatzinikolaou and Richardson, absence of effects (Marchant et al., 2010) depending 2007). Therefore, in populations of T. reticulata, on the study species and parameters measured. shell dissolution by acidification could pose a po- In an acidified environment, reduction in calci- tential challenge through increased predation risk. fication may reduce shell strength and/or thickness Regeneration of parts of the shell lost by sub-lethal (Bibby et al., 2007) making species more vulnerable to predation is a costly process and, even in natural con- predation (Gazeau et al., 2013). For coastal molluscs, ditions, animals will be required to divert energy from the magnitude and consequences of OA on predator- other sources such as somatic growth or reproduc- prey interactions at the population, community and tion (Geller, 1990). ecosystem levels are still unknown because of the In marine ecology, various biochemical indi- varying range of possible outcomes (Kroeker et al., cators such as nucleic acid ratios (RNA:DNA and 2014). Sub-lethal events from predator-prey interac- RNA:Protein) and proximate composition (proteins, tions normally leaves the molluscan prey with a dam- lipids, elemental analysis) have been used as cor- aged shell (Blundon and Vermeij, 1983). This injury relates of condition and growth rate (reviewed in is common in many gastropods (Turra et al., 2005; Houlihan et al., 1993; Fraser and Rogers, 2007). The Dietl and Alexander, 2009; Stafford et al., 2015) and RNA:DNA ratio provides a measure of protein syn- may increase the risk of death because of impaired thesis and recent growth since the amount of DNA movement due to regeneration and the potential in somatic cells remains relatively constant whilst loss of body fluids (Blundon and Vermeij, 1983). The the amount of RNA involved in protein synthesis will available evidence indicates that regrowth scars are vary with nutritional state, age, life-stage, size and not a weak point in the shell (Blundon and Vermeij, changing environmental conditions (Buckley et al., 1983) and gastropods with damaged shells can have 1999; Chícharo and Chícharo, 2008).