Behavioral responses of three venerid bivalves to fluctuating salinity stress
Introduction
For organisms that live within sediments, responses to stressors are often mysterious because of our limited ability to quantify the activities of infauna. As a consequence, measurements of emergent properties are frequently substituted for direct measurements of stressor impact. Benthic productivity and nutrient fluxes are examples of commonly measured emergent properties used for sedimentary systems (Solan et al., 2006; Pratt et al., 2014; Belley et al., 2016). The danger of such indirect metrics is the assumption that the researchers understand the mechanisms by which changes in the metric occurred. The link however between changes in organism activity and change in the metric is commonly poorly understood, resulting in false assumptions about mechanism as discussed by Woodin et al. (2016) and Gammal et al. (2018). This is a critical problem particularly in understanding the seafloor. Over 70% is sedimentary and the majority of the organisms responsible for its properties live within the sediment and their activities within the sediment drive ecosystem functioning (Snelgrove et al., 2014). Understanding the link between organism activities and ecosystem functioning is fundamental to the interpretation of changes in the integrated metrics of ecosystem process and function such as release of nutrients from sediments and benthic primary production (Thrush et al., 2014). An essential component is how these activities change with stress; given the expansion of hydrological alteration, eutrophication and pollution of shallow seas, evaluation of sublethal impacts is essential (Snelgrove et al., 2004; Weslawski et al., 2004).
On the Spanish Northwestern Atlantic coast, particularly in Galicia, is the largest artisanal fishery in Spain in terms of landings and employment (78 million euros in 2018 and 7100 fishers in 2017; Macho et al., 2013; www.pescadegalicia.com). Sixty to 68% of the catch in 2017 to 2019 was comprised of bivalves and three species of venerid bivalve were sixty to 70% of the bivalve harvest value (www.pescadegalicia.com). These venerid species are clearly very important to the success of this artisanal fishery within the intertidal and shallow subtidal as well as being important components of the sedimentary ecosystem (Macho et al., 2016). Two are native species, Venerupis corrugata (Gmelin, 1791) and Ruditapes decussatus (Linnaeus, 1758); the third, the manila clam Ruditapes philippinarum (Adams and Reeve, 1850) was introduced for aquaculture in the 1980's (Pérez-Camacho and Cuña, 1985) and is now widespread in Galicia. All three burrow within the sediments, living primarily in semi-protected embayments both in the intertidal and shallow subtidal (Macho et al., 2016). These are habitats with low bottom flows, <5 cm s−1 (deCastro et al., 2000; Souto et al., 2003). R. philippinarum lives most shallowly of the three in the top 4 cm, V. corrugata typically at mid-depths of 5–6 cm and R. decussatus most deeply at 8 cm or more (Macho et al., 2016). All are suspension feeders and all affect nutrient releases from the sediment through both feeding and excretion and via a variety of hydraulic activities such as repositioning, burrowing, ejection of rejected materials (pseudofeces), expansion of oxic surfaces, etc. (Christensen et al., 2000; Kristensen et al., 2014; Woodin et al., 2016). Sediment porewater is an important source of nitrogen, carbon, silicate and other limiting nutrients and availability of these is critical to benthic-pelagic coupling. The degree to which these nutrients are accessible is a function of the hydraulic activities of infauna, which alter porewater pressure and flux through the sediment water interface (Chennu et al., 2015). During burrowing and repositioning, for example, additional water is injected by organisms into the sediment thus momentarily elevating porewater pressure and causing expulsion from the sediment of nutrient-enriched porewater and oxygenating the subsurface sediments, changing the rate of remineralization (Volkenborn et al., 2016). Both benthic and water column primary productivity are often nutrient limited; so, the degree to which organisms such as these bivalves cease activity and thus break the link between the nutrient source and the nutrient utilizers is critical, particularly in the very productive shallows of the coastal ocean. Additionally, such hydraulic behaviors are linked to essential activities for the health and growth of the organism, such as food capture and excretion so that cessation has implications for growth and ultimately reproduction and survival.
Here we consider effects of salinity because for bivalves it is one of the most influential environmental variables in terms of both physiology and behavior (Hauton, 2016; Smyth and Elliott, 2016). Within the rías of Galicia, salinity can fluctuate dramatically between periods dominated by river flow, particularly low tide periods during and following rains, and those dominated by seawater input. As illustrated by the historical analysis of Parada et al. (2012), episodes of significant mortality in field populations correlate with exposure to salinities ≤15 for several days or more with V. corrugata more susceptible than R. philippinarum, and R. decussatus the least susceptible. This is consistent with laboratory data on mortality and biochemical changes during continuous low salinity exposures of 6 days: V. corrugata was the most susceptible, then R. philippinarum, and then R. decussatus (Carregosa et al., 2014).
In the majority of laboratory studies, the organisms are exposed to low salinity for several days outside of sediments. However in the field, these organisms live in sediments, and during rainfall events, the salinity of the overlying waters in the shallow subtidal and intertidal is typically higher during incoming and high tides and lower during ebbing and low tides. This pattern develops because high salinity ocean water flows toward the head of estuaries during flood and high tide, and fresh water from river and land runoff dominates during ebb and low tide (Parada et al., 2012). Such short-term low salinity events, like heat waves, can have impacts on the biological performance of estuarine species, particularly in shallow water, by reducing growth and reproduction, in addition to the more commonly monitored effects on mortality (Parada et al., 2012; Defeo et al., 2018).
To understand the sublethal impact of short-term, tidally varying salinity exposures on activities of clams in sediment, a mesocosm experiment was run with salinity events of different magnitudes. The objective was to determine the alteration of behaviors of the three most important clams (from a fisheries and environmental perspective) in the intertidal of Galicia exposed to such short-term fluctuations in salinity. To assess impacts on bivalve activities, we used metrics allowing determination of hydraulic activities within the sediment (pressure sensors) as well as feeding activities visible on the sediment surface (siphon exposure and fecal deposition). Experiments were run in March and in May to assess consistency of responses.
The literature strongly suggests that salinities of 15 or below are significantly stressful for these species resulting in higher mortality rates and denigration of biochemical responses with V. corrugata comparatively more sensitive than R. philippinarum and R. decussatus the least affected (Parada et al., 2012; Carregosa et al., 2014). The expected response of bivalves to salinity stress is to close their valves, reducing exposure of tissues to osmotic stress. We thus predicted that both feeding responses (visible siphons and fecal deposition) and repositioning and burrowing (pressure sensor data) would be greatly reduced at salinities at or below 15 relative to those metrics above 15; thus, we predicted the existence of a behavioral threshold between salinities of 15 and 20. Additionally, we expected an asymptote to the behavioral response because counts of bivalve siphons exposed for example cannot exceed the number of animals present. The predicted pattern is that of a logistic function, low activities at low salinities followed by a rapid rise to an asymptote once salinities exceed the behavioral threshold. We expected the strength of the response to be greatest for the most sensitive species, V. corrugata. The experiment was designed to address the impact of tidally varying, short-term impacts; thus, we did not expect to observe increases in mortality.
Section snippets
Materials and methods
Clams were collected by hand from shellfish beds of O Sarrido, the San Antonio Shellfisheries Guild at Cambados Spain (42°30.917′ N, 08°48.883′ W) on the day preceding initiation of the experiment and were transported to the laboratory in refrigerated containers. After measurement and marking the clams were placed onto the sediment surface in tanks with running seawater and allowed to burrow. Individuals which failed to burrow overnight were removed and replaced. Means and standard deviations
Siphon activity
In both V. corrugata and R. philippinarum many more siphons were observed during periods of high salinity (≥ 20) than during periods of low salinity (≤ 15). As expected, the apparent breakpoint for active siphons was between 15 and 20 and there appeared to be an asymptote to activity at ≥20 (Fig. 3). This was true in both the March and the May experiments and both the inflection point and the asymptote were highly significant (Table 1A).
For R. decussatus direct counts of siphons on the surface
Discussion
Behavioral responses, their magnitude and duration as well as their delay in change with stress, drive ecosystem function (Huey and Bennett, 1990; Riedel et al., 2014; Woodin et al., 2016). As discussed by Riedel et al. (2014), behavioral changes can result in alterations of predator-prey relationships, reproductive success, community composition, etc. and one can use behavioral changes to predict ecosystem alterations. The rapidity with which organisms respond to a stress and recover once a
Acknowledgements
This work was funded by grants from the Ministerio de Economía y Competitividad of the Spanish Government to EV and CO (MARISCO CTM2014-51935-R) and the National Aeronautics and Space Administration of the United States to DSW and SAW (NNX11AP77G). Facilities were kindly provided by the Estación de Ciencias Mariñas de Toralla (ECIMAT) of the Universidade de Vigo. The ECIMAT staff provided the phytoplankton supply and Damián Costas the clam diet information. The Cofradías de Mariscadores of
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