Heat Stress in the Intertidal: Comparing Survival and Growth of an Invasive and Native Mussel Under a Variety of Thermal Conditions

Summary Coping with environmental stress may involve combinations of behavioral and physiological responses. We examined potential interactions between adult mussels’ simple behavioral repertoire – opening/closing of the shell valves – and thermal stress physiology in common-gardened individuals of three Mytilus congeners found on the West Coast of North America, two of which are native species (M. californianus and M. trossulus) and one an invasive from the Mediterranean (M. galloprovincialis). We first continuously monitored valve behavior over three consecutive days on which body temperatures were gradually increased, either in air or in seawater. A temperature threshold effect was evident between 25°C and 33°C in several behavioral measures. Mussels tended to spend much less time with the valves in a sealed position following exposure to 33°C body temperature, especially when exposed in air. This behavior could not be explained by decreases in adductor muscle glycogen (stores of this metabolic fuel actually increased in some scenarios), impacts of forced valve sealing on long-term survival (none observed in a second experiment), or loss of contractile function in the adductor muscles (individuals exhibited as many or more valve adduction movements following elevated body temperature as in controls). We hypothesize that this reduced propensity to seal the valves following thermal extremes represents avoidance of hypoxia-reoxygenation cycles and concomitant oxidative stress. We further conjecture that prolonged valve gaping following episodes of elevated body temperature may have important ecological consequences by affecting species interactions. We then examined survival over a 90-d period following exposure to elevated body temperature and/or emersion, observing ongoing mortality throughout this monitoring period. Survival varied significantly among species (M. trossulus had lowest survival) and among experimental contexts (survival was lowest after experiencing elevated body temperature in seawater). Surprisingly, we observed no cumulative impact on survival of three days relative to one day of exposure to elevated body temperature. The delayed mortality and context-specific outcomes we observed have important implications for design of future experiments and for interpretation of field distribution patterns of these species. Ultimately, variation in the catalog of physiological and behavioral capacities among closely related or sympatric species is likely to complicate prediction of the ecological consequences of global change and species invasions.

Section: Discussionsupporting

confidence: 91%

Behavior and survival ofMytiluscongeners following episodes of elevated body temperature in air and seawater

Dowd

Somero

2012

“…4; supplementary material Table S2). This fits with a growing body of research showing that invasive species are often more thermally tolerant than related noninvasive species (Schneider, 2008;Sorte et al, 2010a;Lenz et al, 2011;Lockwood and Somero, 2011;Zerebecki and Sorte, 2011). A recent meta-analysis concluded that, in aquatic environments, invasive species performed significantly better at increased temperatures than did co-occurring native species (Sorte et al, 2013).…”

Section: Discussion Eurythermalitysupporting

confidence: 79%

Master of all trades: thermal acclimation and adaptation of cardiac function in a broadly distributed marine invasive species, the European green crab,Carcinus maenas

Tepolt

Somero

2014

128

126

As global warming accelerates, there is increasing concern about how ecosystems may change as a result of species loss and replacement. Here, we examined the thermal physiology of the European green crab (Carcinus maenas Linnaeus 1758), a globally invasive species, along three parallel thermal gradients in its native and invasive ranges. At each site, we assessed cardiac physiology to determine heat and cold tolerance and acclimatory plasticity. We found that, overall, the species is highly tolerant of both heat and cold, and that it survives higher temperatures than co-occurring native marine crustaceans. Further, we found that both heat and cold tolerance are plastic in response to short-term acclimation (18-31 days at either 5 or 25°C). Comparing patterns within ranges, we found latitudinal gradients in thermal tolerance in the native European range and in the invasive range in eastern North America. This pattern is strongest in the native range, and likely evolved there. Because of a complicated invasion history, the latitudinal pattern in the eastern North American invasive range may be due either to rapid adaptation post-invasion or to adaptive differences between the ancestral populations that founded the invasion. Overall, the broad thermal tolerance ranges of green crabs, which may facilitate invasion of novel habitats, derive from high inherent eurythermality and acclimatory plasticity and potentially adaptive differentiation among populations. The highly flexible physiology that results from these capacities may represent the hallmark of a successful invasive species, and may provide a model for success in a changing world. KEY WORDS: Acclimatory plasticity, Cardiac physiology, Local adaptation, Species invasion, Thermal tolerance INTRODUCTIONEnvironmental temperature exerts a pervasive influence on the physiology of ectothermic animals, from the level of molecular processes to that of broad-scale biogeographic patterning (Hochachka and Somero, 2002). As global temperatures rise, there is increasing concern about the ability of ectothermic animals to survive in their warming environments, and considerable effort is being expended to identify the physiological traits that may be of greatest importance in adapting to rising temperatures and to learn how these traits differ among species (Somero, 2010).One aspect of success in a changed thermal environment comprises a combination of broad intrinsic tolerance of acute changes in temperature and a high capacity for acclimatization (phenotypic 'plasticity') during extended exposure to a new thermal regime (Simons, 2011;Healy and Schulte, 2012). These two abilities may largely govern how eurythermal an ectothermic species is, and thus help determine its chances for success in a warming world, particularly over short time scales. RESEARCH ARTICLEStanfordBecause maintenance of broad thermal tolerance may be metabolically costly and, indeed, unnecessary for animals inhabiting narrow thermal niches, ectothermic species range from extreme eurytherms to na...

“…Based on their natural distribution, the Eastern Pacific M. trossulus seem to prefer colder temperatures and tolerate lower salinity levels, whereas the Mediterranean M. galloprovincialis is a warm-water species that prefers high salinity levels (Seed, 1992). Measurements of growth, heart rate and survival generally confirm these interspecific differences (Braby and Somero, 2006b;Schneider, 2008). One hypothesis for the underlying mechanistic differences is that M. trossulus may achieve tolerance to lower salinities by closing their shells, as indicated by a drop in heart rate (Braby and Somero, 2006b).…”

Section: Introductionmentioning

confidence: 66%

Proteomics of hyposaline stress in blue mussel congeners (genusMytilus): implications for biogeographic range limits in response to climate change

Tomanek

Zuzow

Hitt

et al. 2012

SUMMARYClimate change is affecting speciesʼ physiology, pushing environmental tolerance limits and shifting distribution ranges. In addition to temperature and ocean acidification, increasing levels of hyposaline stress due to extreme precipitation events and freshwater runoff may be driving some of the reported recent range shifts in marine organisms. Using two-dimensional gel electrophoresis and tandem mass spectrometry, we characterized the proteomic responses of the cold-adapted blue mussel Mytilus trossulus, a native to the Pacific coast of North America, and the warm-adapted M. galloprovincialis, a Mediterranean invader that has replaced the native from the southern part of its range, but may be limited from expanding north due to hyposaline stress. After exposing laboratory-acclimated mussels for 4h to two different experimental treatments of hyposaline conditions and one control treatment (24.5, 29.8 and 35.0psu, respectively) followed by a 0 and 24h recovery at ambient salinity (35psu), we detected changes in the abundance of molecular chaperones of the endoplasmic reticulum (ER), indicating protein unfolding, during stress exposure. Other common responses included changes in small GTPases of the Ras superfamily during recovery, which suggests a role for vesicle transport, and cytoskeletal adjustments associated with cell volume, as indicated by cytoskeletal elements such as actin, tubulin, intermediate filaments and several actin-binding regulatory proteins. Changes of proteins involved in energy metabolism and scavenging of reactive oxygen species suggest a reduction in overall energy metabolism during recovery. Principal component analyses of protein abundances suggest that M. trossulus is able to respond to a greater hyposaline challenge (24.5psu) than M. galloprovincialis (29.8psu), as shown by changing abundances of proteins involved in protein chaperoning, vesicle transport, cytoskeletal adjustments by actin-regulatory proteins, energy metabolism and oxidative stress. While proteins involved in energy metabolism were lower in M. trossulus during recovery from hyposaline stress, M. galloprovincialis showed higher abundances of those proteins at 29.8psu, suggesting an energetic constraint in the invader but not the native congener. Both species showed lower levels of oxidative stress proteins during recovery. In addition, oxidative stress proteins associated with protein synthesis and folding in the ER showed lower levels during recovery in M. galloprovincialis, in parallel with ER chaperones, indicating a reduction in protein synthesis. These differences may enable the native M. trossulus to cope with greater hyposaline stress in the northern part of its range, as well as to outcompete M. galloprovincialis in the southern part of M. trossulusʼ range, thereby preventing M. galloprovincialis from expanding further north. Supplementary material available online at