Physiological Responses and Scope for Growth in a Marine Scavenging
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ICES Journal of Marine Science ICES Journal of Marine Science (2016), 73(3), 814–824. doi:10.1093/icesjms/fsv208 Contribution to Special Issue: ‘Towards a Broader Perspective on Ocean Acidification Research’ Original Article Physiological responses and scope for growth in a marine Downloaded from https://academic.oup.com/icesjms/article/73/3/814/2458919 by guest on 29 September 2021 scavenging gastropod, Nassarius festivus (Powys, 1835), are affected by salinity and temperature but not by ocean acidification Haoyu Zhang1, Paul K. S. Shin1,2, and Siu Gin Cheung1,2* 1Department of Biology and Chemistry, City University of Hong Kong, Hong Kong, China 2State Key Laboratory in Marine Pollution, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong, China *Corresponding author: tel: + 852 34427749; fax: + 852 34420522; e-mail: [email protected] Zhang, H., Shin, P. K. S., and Cheung, S. G. Physiological responses and scope for growth in a marine scavenging gastropod, Nassarius festivus (Powys, 1835), are affected by salinity and temperature but not by ocean acidification. – ICES Journal of Marine Science, 73: 814–824. Received 4 June 2015; revised 17 September 2015; accepted 19 October 2015; advance access publication 11 November 2015. In the past few years, there has been a dramatic increase in the number of studies revealing negative or positive effects of ocean acidification on marine organisms including corals, echinoderms, copepods, molluscs, and fish. However, scavenging gastropods have received little attention despite being major players in energy flow, removing carrion, and recycling materials in marine benthic communities. The present study investi- gated the physiological responses (ingestion, absorption rate and efficiency, respiration, and excretion) and scope for growth (SfG) of an intertidal scavenging gastropod, Nassarius festivus, to the combined effects of ocean acidification (pCO2 levels: 380, 950, and 1250 matm), salinity (10 and 30 psu), and temperature (15 and 308C) for 31 d. Low salinity (10 psu) reduced ingestion, absorption rate, respiration, excretion, and SfG of N. festivus throughout the exposure period. Low temperature (158C) had a similar effect on these parameters, except for SfG at the end of the exposure period (31 d). However, elevated pCO2 levels had no effects in isolation on all physiological parameters and only weak interactions with temperature and/or salinity for excretion and SfG. In conclusion, elevated pCO2 will not affect the energy budget of adult N. festivus at the pCO2 level predicted to occur by the Intergovernmental Panel on Climate Change (IPCC) in the year 2300. Keywords: Nassarius festivus, ocean acidification, physiological energetics, salinity, scope for growth, temperature. Introduction corals are considered to be one of the most vulnerable groups For over 800 000 years, carbon dioxide has been relatively stable in (Bramanti et al., 2013; Reyes-Nivia et al., 2013). For molluscs, the atmosphere at 172–300 matm by volume concentration (Luthi Abduraji and Danilo (2015) found that the pH-driven survival et al., 2008). The level reached in 2000 (395 matm) is predicted rate of Haliotis asinina was reduced from 86.3 to 47.2% at pH to rise to 1000 matm by 2100 (Collins et al., 2013). During the 7.99, and 18.3% at pH 7.62 and 7.42, respectively, after 20 d of ex- period 2000–2008, approximately one quarter of anthropogenic posure. Acidified seawateralso restrained pteropods from maintain- carbon dioxide was dissolved in the ocean (Le Que´re´ et al., 2009), ing shells made up of aragonite (Honjo et al., 2000). Dissolution of and increasing CO2 availability is causing a global decrease in pH the shell at the growing edge of the aperture was observed in the of seawater, a phenomenon known as ocean acidification. pteropod Clio pyramidata within 48 h of exposure to 788 matm Effects of ocean acidification have been extensively reported pCO2 (Orr et al., 2005). among marine organisms including bacteria, plants, and animals Physiological responses of ocean acidification are species-specific [reviewed by Caldeira and Wickett (2003)]. The unsaturated state with differential responses being observed in closely related species. + + of calcium carbonate caused by excess H and lower Ca2 availabil- For example, the Mediterranean mussel Mytilus galloprovincialis ity in acidifying seawater makes calcifying invertebrates potential showed a reduced metabolic rate and slower growth when exposed victims of changes to ocean chemistry. Among such organisms, to pH 7.3 for 3 months (Michaelidis et al., 2005). In contrast, no # International Council for the Exploration of the Sea 2015. All rights reserved. For Permissions, please email: [email protected] Physiological responses and scope for growth in a marine scavenging gastropod 815 physiological disturbance was observed in the blue mussel Mytilus 1120 matm pCO2 for 39 weeks with no acclimation observed edulis at pH 7.14 for 60 d (Thomsen and Melzner, 2010). Some (Appelhans et al., 2014). In addition, SfG measurements of the sea species are robust or show positive responses to ocean acidification urchin Strongylocentrotus purpuratus raised under high pCO2 [reviewed by Andersson et al.(2011)]. The brittlestar Amphiura fili- (129 Pa, 1271 matm) indicate that an average of 39–45% of the formis showed an increase in metabolism and calcificationwith a sub- available energy was spent in somatic growth, while control larvae stantial cost (muscle wastage) upon exposure to acidified seawater could allocate between 78 and 80% of the available energy to (pH7.7) for40 d(Wood et al., 2008). Neutral responses in metabolic growth processes. rates have been observed in three echinoderms, Asterias rubens, As one of the most dominant and competitive scavengers on Ophiothrix fragilis,andA. filiformis after 1 week of exposure to pH sandy shores in Hong Kong, Nassarius festivus plays an important 7.5 (Carey et al., 2014). High metabolic rates commonly found in role in matter cycling and energy flow, and serves as an important crustaceans facilitate the control of extracellular pH through active cleaner in removing carrion (Briton and Morton, 1992). Previous ion transport (Whiteley, 2011), hence reducing the impact of ocean studies on physiological energetics have shown that this species is tol- acidification. For instance, after 10 d of incubation, there were no erant of environmental stresses, including low salinity and hypoxia Downloaded from https://academic.oup.com/icesjms/article/73/3/814/2458919 by guest on 29 September 2021 net changes in survival or overall development of larvae of the bar- (Cheung and Lam, 1995; Chan et al., 2008). The interactive effects nacle Amphibalanus improvisus raised at pH 7.6 compared with the of ocean acidification, high temperature, and low salinity increased control pH of 8.0 (Pansch et al., 2013). This may be partly due to the mortality of the veliger larvae (Zhang et al., 2014). The mainten- the absence of calcified structures in barnacle larvae that are devel- ance cost, as shown by the respiration rate, also increased with oped only when they settle and metamorphose into the juvenile stage. temperature and pCO2 level. In the present study, N. festivus adults Shifts in energy allocation upon exposure to ocean acidification were exposed to the combined effect of ocean acidification, tempera- may reduce fitness and produce low functional capacities, hence in- ture, and salinity for 31 d. The acute responses to the combined stres- creasing sensitivity to environmental stressors such as temperature, ses and physiological adjustments, if any, following prolonged food supply, and salinity (Zittier et al., 2013; Carey et al., 2014). exposure to the stresses were investigated. To understand if there According to Po¨rtner (2008), ocean acidification enhances sensitiv- are any life-stage differences in sensitivities to multiple stressors ity to thermal stress, resulting in a narrowing of the thermal toler- that could create a bottleneck in population performance, results ance window and aerobic capacity. For example, the brown crab were compared with those obtained for the larvae in a previous Cancer pagurus reduced its upper thermal limit of aerobic scope study (Zhang et al., 2014). Reduction in population performance by 58C under hypercapnia (pH 7.06) exposure for 16 h (Metzger could eventually lessen the role of N. festivus in removing carrion et al., 2007). The scope for performance of the Arctic spider crab on sandy shores, hence resulting in a deterioration of environmental Hyas araneus was reduced at the limits of thermal tolerance (48C) quality. and exacerbated by an elevated CO2 level of 3000 matm (Zittier Based on climate models in the IPCC Fifth Assessment Report et al., 2013). Synergistic effects have also been observed between (AR5), The Hong Kong Observatory has predicted the temperature ocean acidification and low salinity. Combined exposure to hyper- and rainfall changes in Hong Kong in the 21st century (http://www capnia and low salinity negatively affected mortality, tissue growth, .hko.gov.hk/climate_change/proj_hk_rainfall_e.htm). Under the energy storage, and mechanical properties of shells of juvenile high greenhouse gas concentration scenario (RCP8.5) proposed in oysters Crassostrea virginica (Dickinson et al., 2012). In addition, this report, temperature is expected to rise by 1.5–3 and 3–68Cin the larval mortality of a subtidal scavenging gastropod Nassarius the mid-21st century (2051–2060) and late 21st century (2091– conoidalis was enhanced by high pCO2 level (1250 matm) at low sal- 2100), respectively, when compared with the 1986–2005 average inity (10 psu) but not at normal salinity (30 psu; Zhang et al., 2014). of 23.38C. The number of extremely wet years is expected to increase Acclimation occurs when organisms adjust physiologically to from 3 in 1885–2005 to about 12 in 2006–2100. The annual rainfall changes in the environment, allowing them to maintain performance in the late 21st century is expected to rise by 180 mm when com- relatively independently of the changes. Such adjustment occurs pared with the 1986–2005 average.