Читать книгу Marine Mussels - Elizabeth Gosling - Страница 43

Most marine bivalves live within a temperature range from −3 to 44°C (Vernberg & Vernberg 1972). Within this range, the degree of temperature tolerance is species‐specific, and within individual species early embryos and larva have a narrower temperature tolerance than adults (see Chapter 5). In addition, the temperature required for spawning is invariably higher than the minimum temperature required for growth. All of these factors set limits on the natural distribution of individual species on both regional and local scales. A few relevant examples from marine mussels will elucidate this.

As described earlier, the distribution of M. edulis on the Atlantic coast of North America extends from the Canadian Maritimes southward to Cape Hatteras in North Carolina, the historical southern limit for this species. It is believed that the northward‐moving warm water Gulf Stream meets the southward‐moving cold Labrador Current in the region of Cape Hatteras (35.25 °N), thus providing a temperature barrier for the distribution and survival of mussel larvae south of this point. Field experimental data, combined with a modelling approach, indicate that the southern limit of M. edulis is mediated by intolerance to high summer temperatures (Jones et al. 2009). Since 1960, seasonal air and water temperatures have increased along the eastern US seaboard, and south of Lewes, Delaware (38.8 °N) summer sea surface temperature (SST) increases have exceeded the upper lethal limits (32 °C) of M. edulis (Jones et al. 2010), resulting in geographic contraction of the southern, equatorward range edge of M. edulis, shifting it approximately 350 km north of the previous limit at Cape Hatteras. At the southern part of the range, high water and air temperatures cause mass mortality events, while along the more northerly portion mortality is caused by high temperatures during aerial exposure. Ultimately, water temperatures in excess of thermal tolerances have caused contraction of the mussel’s biogeographic range.

Two Mytilus conspecifics, M. trossulus and M. galloprovincialis, co‐occur on the West Coast of the United States, and both have exhibited changes in biogeographic ranges over several decades. The range of M. trossulus once extended from Baja California north to Alaska. However, when the Mediterranean mussel, M. galloprovincialis, was introduced into southern California in the first half of the 20th century, the invasive mussel was able to completely displace the native M. trossulus throughout the southern portion of its range. Fields et al. (2006) investigated whether biochemical adaptation to temperature might potentially play a role in invasion success. An examination of cytosolic malate dehydrogenase (cMDH), an enzyme known to exhibit distinct patterns of temperature adaptation in kinetic properties, showed that a minor change in structure permits M. galloprovincialis cMDH to function at warmer temperatures and may be a part of a broad suite of molecular adaptations that has allowed this species to displace its congener throughout the warmer part of M. trossulus’ original range in North America, and also in Japan. In a subsequent study, Lockwood & Somero (2011a) analysed a variety of physiological, biochemical and molecular systems, including cardiac function, enzymatic activity and gene expression, in the same two species. In all comparisons, M. galloprovincialis was more warm‐adapted than M. trossulus. Higher activities of enzymes involved in ATP generation show that the native M. trossulus is better adapted to colder conditions than M. galloprovincialis. The higher thermal tolerance of the invasive species is likely due in part to its enhanced ability to induce changes in the expression of particular genes and proteins in response to acute heat stress. Taken together, these data predict that M. galloprovincialis will continue to be the dominant blue mussel species along the warmer range of the California Current,² yet its northward spread is limited. In support of this, Hilbish et al. (2010) reported that from 1995 to 1999 the poleward movement of M. galloprovincialis showed a reversal concomitant with a cooling phase of the Pacific Decadal Oscillation (PDO),³ an important driver of climate. M. galloprovincialis has declined in abundance over the northern third of its geographic range (~540 km), and has become rare or absent across the northern 200 km of the range it previously colonised during its initial invasion. The distribution of the native species M. trossulus has, however, remained unchanged over the same time period. The difference in SST between warm and cold phases of the PDO is small (~1 °C), but Hilbish et al. (2010) deduced that even this minor decrease during the cold phase of the PDO might be enough to retard larval development in M. galloprovincialis, such that recruitment is handicapped in northern waters.

The Asian green mussel, P. viridis, has been introduced into coastal waters of Florida; it was also reported in coastal Georgia in 2003 and has spread as far north as South Carolina (Benson 2019). Its current distribution is assumed to be limited by low temperatures during winter. To test this, Urian et al. (2011) analysed lethal and sublethal effects of cold water and air temperatures in two size classes of the mussel from Florida in an effort to determine the effects of current and forecasted temperatures on the potential for range expansion. Mussels were exposed to water temperatures of 14, 10, 7 and 3 °C for up to 30 days, or to air temperatures of 14, 7, 0 and −10 °C for two hours. Mortality was significantly increased at all water and air temperatures ≤14 °C. No differences in mortality rates were observed between small (15–45 mm) and large (75–105 mm) size classes except after exposure to 7 °C air, in which small mussels had higher mortality. The temperature threshold for survival in this population appears to be between 10 and 14 °C, suggesting that under present conditions P. viridis may already be at the northern edge of its potential range in the United States, unless with global climate change northerly flowing currents permit range expansion beyond the coastal waters of South Carolina.

Beside rising air and water temperatures, global climate change may also entail increases in precipitation, and estuarine species in particular may be exposed to increasing hypoosmotic stress due to decreasing salinities impacting on species’ distribution ranges (Somero 2012). Indeed, increased precipitation leading to reduced salinity in estuarine habitats may in some cases be more important in governing local distributions than changes in temperatures (Somero 2012; Braby & Somero 2006a,b). The open ocean has surface salinities between 33 and 37 psu, with an average of 35 psu. In contrast, estuaries and bays are subject to pronounced salinity fluctuations because of evaporation, rainfall and inflow from rivers. Many mussels, in particular Mytilus spp., are euryhaline (i.e. they can tolerate an extremely wide range of salinity, 4–40 psu, in their natural environment). In the northern Baltic, M. trossulus is living at the margin of its salinity tolerance (4.5 psu), and although dwarfed by the low‐salinity conditions, the species is very abundant in this area (Westerbom et al. 2002; see Chapter 7 for salinity tolerance values in marine mussels).

Tomanek et al. (2012) examined the proteomic responses to hyposaline stress in M. trossulus and M. galloprovincialis, whose ranges overlap on the west coast of N. America (see earlier). Mussels were exposed to short time periods (4 hr) of hyposaline stress, followed by a recovery period to mimic conditions typical for bays and coastal areas experiencing heavy freshwater input, with a quick return to full salinity with incoming tides and mixing with full‐strength seawater. The differences in protein abundances in gill tissue suggested that M. trossulus was able to respond to a greater hyposaline challenge (24.5 psu) than M. galloprovincialis (29.8 psu). These differences, in a scenario of reduced coastal salinities, may enable M. trossulus to cope with greater hyposaline stress and outcompete M. galloprovincialis in the southern part of the M. trossulus range, thereby preventing M. galloprovincialis from expanding northward. Interestingly, Lockwood & Somero (2011b), in a transcriptomic analysis of gill tissue of Mytilus specimens from the same experiment (but limited to 29.8 and 35.0 psu), found no major differences in salinity stress tolerance between the two congeners at the level of transcriptional regulation.

P. viridis and Mytella charruana are two species of non‐native marine mussels that have recently invaded Florida, United States; as they are now well established, they are potential causes of concern along SE‐US coasts. Both species have been documented on intertidal oyster reefs in Florida (Spinuzzi et al. 2013), where they have a negative impact on the commercially important eastern oyster Crassostrea virginica (Yuan et al. 2016a). The simultaneous effects of salinity and temperature on the two species were investigated to get a better understanding of their respective invasion potentials (Yuan et al. 2016b). Survival at three salinity ranges (5–9, 20–22.5 and 35–40 psu) in both cold and warm water was estimated for juveniles and adults of both species. Yuan et al. (2016b) found that P. viridis can survive at a wide range of temperatures (9–35 °C) when the salinity is 35–37 psu, but as salinity decreases, the thermal survival range for P. viridis becomes narrower. The data for M. charruana indicate that juvenile and adult individuals can survive at a wide range of salinities (5–40 psu) at 20 °C, but the salinity tolerance range narrows as the temperature decreases or increases. Also, temperature rapidly impacts survival of both species (within hours), while salinity impacts are more gradual (days to weeks). As the species are tolerant of many salinity–temperature combinations found in SE‐US, they should be able to both persist in their present invaded range and expand into new estuaries and bays along the Atlantic coastline of Florida and west within the Gulf of Mexico. Freezing weather, however, could impede expansions into colder waters. Given that both species have a detrimental effect on C. virginica and possibly on many other native species, the abiotic variables could be used to help predict successful introductions and future biogeographic expansions.

In 2004, Berge et al. (2005) were the first to report the presence of settled mussels (M. edulis), for the first time since the age of the Vikings (793–1066 AD), in the high Arctic Archipelago of Svalbard – a Norwegian archipelago between mainland Norway and the North Pole. Their data indicated that most mussels settled at a single site as spat in 2002 and that larvae were transported by the West Spitsbergen Current northward from the Norwegian coast to Svalbard the same year. The extension of the mussel’s distribution range was made possible by the unusually high northward mass transport of warm Atlantic water resulting in elevated sea surface temperatures in the North Atlantic and along the west coast of Svalbard. This was suggested to be a one‐time event as all mussels were of similar age. Recently, Leopold et al. (2019) carried out a detailed field survey with scientific divers to map the Mytilus spp. distribution along the west coast of Svalbard, with a focus on the west coast of Spitsbergen, the largest island of the Svalbard archipelago, where strong Atlantification (transition from cold, fresh Arctic waters to a warm, salty Atlantic regime) has been documented over the last few decades. Low densities (<0.5 individuals m⁻²) of live Mytilus were recorded at 21 locations on the west coast of Svalbard and Spitsbergen. Using genetic markers, the authors found that these were mainly M. edulis, although some samples were classified as M. galloprovincalis or as hybrids of both M. edulis/M. galloprovincalis and M. edulis/M. trossulus. However, Leopold et al. (2019) regarded the three species as one complex, referring to them as ‘Mytilus spp.’ throughout their publication. The oldest mussel collected settled around the year 2000, indicating, despite low mussel densities at all sites, that settlement of blue mussels is a recurring event, with evidence of recruitment every year since 2000. The presence of Mytilus on Svalbard is the probable outcome of at least two distinct dispersal vectors: natural larval advection⁴ by ocean currents and human introduction by ship traffic. Based on the estimated year of settlement of mussels found in non‐harbour locations, Leopold et al. (2019) concluded that the settlement of Mytilus spp. is an annual event, rather than the unique one suggested by Berge et al. (2005), which implies that current environmental conditions are favourable for continued persistence of Svalbard’s Mytilus spp. populations.

The coast of South Africa comprises three broad biogeographic regions: the cool‐temperate western coast, the warm‐temperate southern coast and the subtropical eastern coast; these are aligned with two globally important currents and characterised by a clear decrease of upwelling intensity and frequency and by primary production from west to east (McQuaid et al. 2015 and references therein). The two currents are the upwelling‐driven Benguela Current (BC) on the southwestern coast and the warm, temperate Agulhas Current (AC), which follows the eastern and southern coasts (Figure 3.3). Upwelling is believed to have strong effects on the advection of larvae between coastal waters and the intertidal. In southern Africa, the indigenous mussel, P. perna, dominates the subtropical and warm‐temperate bioregions from central Mozambique to the Cape of Good Hope, west of Cape Agulhas on the southwest coast of S. Africa. The species is absent from there to central Namibia due to the cold, upwelling waters of the Benguela system – a distributional gap of more than 1000 km. From there, P. perna extends northward along the west coast of Africa to the Mediterranean Sea, as far as the Gulf of Tunis (Van Erkom Schurink & Griffiths 1990; Zardi et al. 2015). The invasive M. galloprovincialis is considered to have arrived on the western coast of South Africa via shipping in the 1970s (Grant & Cherry 1985). The species subsequently spread both north and south, with its northerly spread being more rapid under the influence of the north‐flowing BC, which flows from the Cape of Good Hope to Lüderitz, after which it is deflected away from the coast to the northwest. The northern limit of M. galloprovincialis on the west coast is in central Namibia, where conditions may represent the limit of the species’ temperature tolerance (Zardi et al. 2007a). The second distributional limit for M. galloprovincialis occurs on the SE southern African coast. There, the warm AC, which flows to the southwest, diverges away from the coast, thereby reducing SST significantly. And because warm waters tend to have fewer nutrients than cold waters, the distributional limits of M. galloprovincialis may also be affected by unfavourable trophic conditions beyond these boundaries, in addition to prohibitive thermal conditions (Assis et al. 2015).

Figure 3.3 Map of the Benguela Current region bordering Namibia and South Africa, showing the 500 m depth contour (dashed line) and the approximate locations of the Lüderitz upwelling cell (which separates the northern and southern Benguela Current subsystems) and the Agulhas Current.

Source: From Roux et al. (2013). Reproduced with permission from the Bulletin of Marine Science.

There is increasing modelling and experimental evidence that pronounced alterations to oceanographic features (dominant currents and upwelling systems) due to climatic change are rearranging species’ distributions globally (Lourenço et al. 2017). Researchers at the University of Miami found that the Indian Ocean’s warm Agulhas Current is getting wider rather than strengthening (Beal & Elipot 2016). Their findings, which have important implications for global climate change, suggest that intensifying winds in the region may be increasing the turbulence of the current, rather than increasing its flow rate. In the case of the Benguela Current, global climate change has led to a rise in the temperature of this cold current. Not only has there been a rise in water temperature, but the water has become increasingly saline (Global Climate 2019). An El Niño⁵ effect has already been detected. The outcome of these changes from the Benguela El Niño is expected to have a dramatic effect on marine life on the southwest coast of Africa. How exactly it will impact global distributions of marine mussels remains to be seen.