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

Abstract

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...

RAD sequencing reveals genomewide divergence between independent invasions of the European green crab (Carcinus maenas) in the Northwest Atlantic

“…In fact, it may be necessary to consider these crabs as two distinct ecotypes across their invasive range due to their potential adaptations to different thermal regimes and behavioral differences (Rossong et al., 2012) to implement more effective management strategies. Green crab show different thermal tolerances between lineages (Tepolt & Somero, 2014) and adaptive differences in the native range likely facilitated the invasion success and subsequent range expansion in North America (Roman, 2006). However, to date green crab in Atlantic Canada have been treated as a single species and population for risk assessment and habitat suitability modeling (Therriault, Herborg, Locke, & McKindsey, 2008).…”

Selection for upper thermal tolerance in rainbow trout (Oncorhynchus mykissWalbaum)

“…The approaches used here stem from the pioneering physiological studies of thermal performance in fishes by Dr Fred Fry (1947) and the more recent concept of 'oxygen-and capacity-limited thermal tolerance ' (Pörtner and Knust, 2007;Pörtner and Farrell, 2008), as well as the recent finding that rate transition temperatures for heart rate reveal much about the upper thermal tolerance that governs the biogeographical distribution of a species (Tepolt and Somero, 2014). Indeed, recent physiological studies of thermal optima in fish range from warm water temperature species such as coral reef fishes (Nilsson et al, 2009) and Danio (Sidhu et al, 2014), through several temperate salmonid species (Casselman et al, 2012;Anttila et al, 2014;Chen et al, 2013;Verhille et al, 2013) and goldfish, Carassius auratus (Ferreira et al, 2014), to polar species such as the Antarctic nototheniid fish Pagothenia borchgrevinki (Franklin et al, 2007) and Arctic cod, Boreogadus saida (Drost et al, 2014).…”

Adaptation in marine invasion: a genetic perspective

“…However, recent physiological research supports the local adaptation hypothesis, finding that crabs from Portugal were more heat-and less coldtolerant than crabs from Norway. This pattern was recapitulated in the east coast range, where crabs from Newfoundland (derived in part from the second invasion) were more cold-and less heat-tolerant than crabs from New Jersey (derived entirely from the initial invasion) (Tepolt and Somero 2014). Taken together, the physiological, biogeographic, and genetic evidence all suggest that local adaptation may have played a critical role in the establishment and spread of green crabs along the east coast.…”

“…However, evidence for thermal adaptation is not limited to species, like these, with little to no time spent in a pelagic larval stage. The mud crab Rhithropanopaeus harrisii showed thermal differences in larval development between populations (Laughlin and French 1989), and the high-gene flow European green crab Carcinus maenas differed in its adult cardiac response to temperature across multiple populations (Tepolt and Somero 2014). There is also evidence for thermal adaptation in the snails Littorina littorea and L. saxatilis and the oyster Crassostrea virginica (Dittman 1997;Dittman et al 1998;Sokolova and Pörtner 2001;Sorte et al 2011).…”