Thermal constraints for range expansion of the invasive green mussel, Perna viridis, in the southeastern United States

Temperature is often thought to be the predominant factor determining the geographic distribution of marine invertebrates (Hutchins, ’47; Seed, ’76; Hicks and McMahon, 2002). For tropical and sub-tropical species, it is predominantly cold winter temperatures that act as a limiting factor. Cold temperatures have been shown to increase mortality in a number of marine invertebrates, including the mollusks Crepidula fornicata (Thieltges et al., 2004) and Perna perna (Hicks and McMahon, 2002). Although cold-induced mortality may determine the absolute limits of a species potential range, typically species have a broad range of temperatures acceptable for survival (Delgado and Camacho, 2007). But even environmental stressors at nonlethal, yet extreme temperatures, can induce a stress response that may reduce long-term survival (Seed, ’76; Krebs and Feder, ’97; Krebs and Feder, ’98; Beukema et al., 2009), growth (Feder et al., ’92), and/or reproductive success (Krebs and Loeschcke, ’94). Therefore, both the lethal and sub-lethal effects of temperature are likely to play a pivotal role in defining the observable patterns of species distribution. Here the Asian green mussel, P. viridis, was used as a model to study the effects of cold temperatures on geographic distribution and range expansion. P. viridis is native to the Indo-Pacific region (Sidall, ’80; Rajagopal et al., 2006), but in recent years, green mussels have been introduced to coastal waters of North America, South America, and the Caribbean (Agard et al., ’92; Rylander et al., ’96; Benson et al., 2001; Ingrao et al., 2001). Green mussels were first discovered in the United States as a fouling organism on the intake pipes of a power plant in Tampa Bay, FL in August 1999 (Benson et al., 2001). Since that time, they have also spread along parts of the Gulf coast and have been discovered on the east coast of the US in northern Florida and parts of Georgia (Power et al., 2004). The green mussel's potential impact on local ecosystems and native species is not yet fully understood; however, high densities have been reported to foul power plant intake pipes, ship hulls, and structures such as bridge pilings and are therefore likely to have an economic impact (Benson et al., 2001). The US Army Corp of Engineers has estimated that zebra and quagga mussels, which foul similar structures, cause up to $1 billion per year in damage and control costs. It has also been suggested that P. viridis may displace native species such as the oyster Crassostrea virginica (Baker and Benson, 2002). Green mussels have become successful invaders in many locales due in part to their tolerance for environmental extremes (Rajagopal et al., 2006). For example, green mussels in the Indo-Pacific region experience an average annual water temperature range between 12 and 32°C (Rajagopal et al., 2006), with an optimal range between 26 and 32°C (Power, 2004). Previous experiments have shown that green mussels have a 50% mortality rate after 2-week exposures to water temperatures of 10 and 35°C (Sivalingam, ’77). Water quality monitoring data from the Guana Tolomato Matanzas National Estuarine Research Reserve (GTMNERR) in St. Augustine, FL reports an average winter water temperature of 13.9°C, suggesting that local populations of green mussels may experience water temperatures well below their optimal range during winter months. In addition, intertidal green mussels in the southeastern United States may also be vulnerable to periods of acute stress from cold air when low spring tides correspond with sub-freezing overnight temperatures. During these periods, air temperatures are often substantially lower than the ambient water temperature. Therefore, chronic exposure to cold air and water temperatures is expected to limit the ability of P. viridis to expand its geographic range further north along the Atlantic coast of the United States. Most studies on temperature tolerance in marine mollusks have focused on the critical temperature at which adult survival is no longer possible. More subtle sub-lethal effects that have been shown include reduction in growth and reproductive output in Mytilus galloprovincialis and P. canaliculus (Petes et al., 2007). Analysis of heat-shock protein (Hsp) induction can be a good model to monitor sub-lethal stress upon an organism (Dalhoff, 2004). Heat shock proteins (Hsp) are a highly conserved class of molecular chaperone that are up-regulated during periods of stress to repair damaged and denatured proteins (Lindquist and Craig, ’88; Hendrick and Hartl, ’93; Parsell and Lindquist, ’93; Feder and Hofman, ’99; Gonzalez-Riopedre et al., 2007). Heat shock protein induction due to temperature stress has been documented in numerous bivalve species, including Mytilus spp. (Buckley et al., 2001), Dreissena polymorpha (Singer et al., 2005), and C. gigas (Hamdoun et al., 2003); however, long-term effects on longevity and fecundity have not been widely studied in these species. Induced expression of heat shock proteins has been shown to decrease the larvae to adult survival rate (Krebs and Feder, ’97), reduce fecundity (Krebs and Loeschcke, ’94), and lower growth rates (Feder et al., ’92) in Drosophila melanogaster. Although induced stress responses may increase survival in the short term, the costs may have long-term consequences on the potential for population growth and range expansion (Krebs and Feder, ’97). As temperature is likely to be among the most important factors determining the potential for range expansion of tropical exotic species, this study was designed to examine the effects of lethal and sub-lethal cold stress on two different size/age classes of the Asian green mussel, P. viridis. Based on volumetric difference, it is expected that larger mussels may exhibit a slower/reduced response to the effects of cold stress during aerial exposure due to a greater thermal inertia. Furthermore, subtidal mussels that have survived a previous winter may also be more likely to survive subsequent cold stress associated with low winter water temperatures. If there is differential survival with respect to size in cold conditions, the ultimate geographical distribution will be determined by the point at which young of the year can no longer survive the winter. In addition, heat shock protein expression was used as an indicator of physiological stress to examine sub-lethal effects of exposure to cold water and air temperatures.