Marine Mussels. Elizabeth Gosling
which juvenile M. trossulus relocate from protective filamentous algal habitat to adult habitat, suggesting ontogenetic shifts in habitat use by juvenile M. trossulus are a response to changing sensitivity to desiccation. In a scenario of global warming, survival of newly settled mussels, and thus possibly the persistence of mussel populations, will likely depend even more upon the persistence of protective microhabitats created by filamentous and fucoid algae.
Body temperature during aerial exposure is driven by multiple interacting climatic factors, and extremes during low tide far exceed those during submersion (Helmuth 2002). Physiological effects of thermal stress in both low‐ and high‐tide conditions were compared between M. galloprovincialis and M. trossulus under laboratory conditions (Schneider 2008). To simulate the natural range of tidal thermal stress, mussel populations of the two species were established in seawater tanks that mimicked a daily tidal cycle by filling and draining at different times. During high tide, mussels were completely immersed in water, while during low tide, they were exposed to one of three aerial temperature treatments: 20 °C (cool), 25 °C (warm) or 30 °C (hot). A subtidal control group, which remained underwater during the entire tidal cycle, was also established. Separate experiments were carried out in two different water temperatures, 18 and 12 °C, which represented those pertaining where the species co‐occur in California (Braby & Somero 2006a) and found during the summer along the west coast of the United States. In 18 °C water, there was no effect of the aerial treatments on growth or survival in either species. In contrast, in 12 °C water, aerial exposure affected the survival and growth of both species. Growth and survival rates of M. galloprovincialis were higher in all conditions than those of M. trossulus, especially in the 18 °C water experiments and in the aerial exposure treatments of the 12 °C water experiment. M. galloprovincialis seems to be warm‐adapted with regard to both low‐ and high‐tide thermal stress. These results suggest that M. galloprovincialis will spread, at least compared to M. trossulus, as water and air temperatures increase in a global warming scenario.
M. californianus has a large distributional range (Washington to southern California, United States) and experiences a correspondingly wide geographical range in temperature. Therefore, one might ask to what extent its temperature regime can be predicted from latitudinal position, or even from a few temperature measurements taken at a site in air or water over a relatively short period of time. To investigate this, Helmuth et al. (2006) used long‐term (five years) high‐frequency temperature data from biomimetic sensors deployed at 10 locations along the West Coast of the United States (Figure 3.6). Their objective was to test the hypothesis that local modifying factors, such as the timing of low tide in summer, can lead to large‐scale geographic mosaics of body temperature. The results indicated that patterns of body temperature during aerial exposure at low tide varied in physiologically meaningful and often counterintuitive ways, over large sections of the species’ geographic range. An evaluation of spatial correlations among sites to explore how body temperatures change along the latitudinal gradient showed that ‘hot spots’ and ‘cold spots’ exist where temperatures are hotter or colder than expected based on latitude. Four major hot spots and four cold spots were identified along the entire geographic gradient, with at least one hot spot and one cold spot occurring in regions as climatically distinct as Washington/Oregon, Central California and Southern California. This pattern was driven by differences in the timing of low tides among regions. At northern latitudes, low tides in the summer occur at midday and expose intertidal organisms to high aerial temperatures, while at southern sites low tides during summer occur mostly at night and organisms are thus often submerged during hot days. Temporal autocorrelation analysis of year‐to‐year consistency and temporal predictability in the mussel body temperatures revealed that southern mussels experience higher levels of predictability in thermal signals compared to northern animals. Helmuth et al. (2006) also explored the role of wave splash at a subset of sites and found that while average daily temperature extremes varied between sites with different levels of wave splash, yearly extreme temperatures were often similar, as were patterns of predictability. In summary, rather than simple latitudinal gradients, these intertidal mussels experience a complex thermal mosaic, with many potential variables affecting the thermal state of an intertidal organism. The results of this study highlight the importance of quantitatively assessing biogeographic patterns in temperatures and other environmental variables at scales relevant to the organisms themselves and of forecasting the impacts of changes in climate across species ranges.
Figure 3.6 Map of the 10 deployment sites used by Helmuth et al. (2006) along the United States Pacific coast.
Source: From Helmuth et al. (2006). Reproduced with permission from John Wiley and Sons.
Between 1998 and 2016, Helmuth et al. (2016) further deployed biomimetic sensors that approximated the thermal characteristics of intertidal mussels at 71 sites worldwide. Biomimetic loggers (robomussels) were programmed to record at intervals of 10–30 min and were left in the field for periods up to nine months before they were removed for downloading and replaced with another logger. The loggers were used at multiple intertidal elevations to estimate temperatures of the mussels M. californianus (west coast of North America), M. edulis and Geukensia demissa (east coast of North America), M. chilensis (Chile), P. perna (South Africa) and P. canaliculus (New Zealand). Unmodified (‘off‐the‐shelf’) commercial loggers were also deployed on rock surfaces at multiple sites (Australia, Ireland, Mexico, Scotland, United Kingdom, United Staes), which recorded temperatures relevant to barnacles, newly settled mussels and other organisms that are sufficiently small that their temperatures mirror those of the underlying rock. Comparisons against direct measurements of mussel tissue temperature indicated errors of ~2.0–2.5 °C during daily fluctuations that often exceeded 15–20 °C. Geographic patterns in thermal stress, based on biomimetic logger measurements, were generally far more complex than expected, based only on ‘habitat‐level’ measurements of air temperature or SST. This unique data set provides an opportunity to link physiological measurements with spatially‐ and temporally‐explicit field observations of body temperature in intertidal mussels.
In cold conditions, mobile intertidal species can hide in rock crevices or migrate to deeper water to avoid freezing. But sessile bivalves, often exposed to subzero temperatures during winter, do not have such protection. In northeastern Canada, temperatures can drop to −35°C in winter. Mussels (M. trossulus) survive such low temperatures even when their tissue temperatures are as low as −10°C (Williams 1970), with large adults surviving laboratory conditions of −16 °C for 24 hours (Bourget 1983). As much as 60% of their extracellular fluid (ECF) is frozen at this temperature. The unfrozen ECF becomes more concentrated with solutes, and this process draws water by osmosis out of cells, thus lowering the intracellular freezing point. The high osmotic concentration of the ECF places an osmotic stress on the cells that can damage membranes and enzymes. This damage can be minimised through the production of cryoprotectants (e.g. the amino acids glycine, alanine and proline), as well as the end products of anaerobic metabolism (e.g. lactate, succinate and strombine (Loomis et al. 1988; Loomis & Zinser 2001) and glucose (Gionet et al. 2009)). Calcium also acts as a cryoprotectant in the mussel G. demissa by binding to cell membranes and reducing cell damage during freezing, either through physical stabilisation of the membrane against mechanical disruption caused by cell shrinkage or by prevention of the denaturation of membrane compounds (Ansart & Vernon 2003). Another mechanism to avoid intracellular ice formation – an invariably lethal process – is the production of ice‐nucleating proteins, which are secreted into the ECF and act to induce and control extracellular ice formation. These proteins reduce undercooling from the range −15 to −20 °C to the range of −5 to −10 °C. G. demissa is a freeze‐tolerant saltmarsh mussel that is regularly exposed to subzero temperatures for extended periods during low tides. The species’ cold tolerance varies seasonally, ranging from a lower lethal