Estuarine, Coastal and Shelf Science (1998) 46, 587–597 The Relationship Between Increasing Sea-surface Temperature and the Northward Spread of Perkinsus marinus (Dermo) Disease Epizootics in Oysters T. Cooka, M. Follia, J. Klinckb, S. Fordc and J. Millera aRutgers University, Institute for Marine and Coastal Sciences, P.O. Box 231, New Brunswick, New Jersey 08903, U.S.A. bCenter for Coastal Physical Oceanography, Crittenton Hall, Old Dominion University, Norfolk, Virginia 23529, U.S.A. cRutgers University, Haskin Shellfish Research Laboratory, 6959 Miller Ave., Port Norris, New Jersey 08345, U.S.A. Received 20 March 1997 and accepted in revised form 25 August 1997 From its initial discovery in the Gulf of Mexico in the late 1940s until 1990, Perkinsus marinus, the parasite responsible for Dermo disease in the eastern oyster, Crassostrea virginica, was rarely found north of Chesapeake Bay. In 1990–92, an apparent range extension of the parasite led to epizootic outbreaks of the disease over a 500 km range north of Chesapeake Bay. One of the hypotheses for the range extension argues that small, undetected numbers of parasites were already present in northern oysters as the result of repeated historical introductions, and that a sharp warming trend in 1990–92 stimulated the disease outbreak. This argument was based on trends in air temperature. The present study examined this hypothesis by analysing water temperatures, rather than air temperatures, for five stations located in areas affected by the recent epizootics. At all five stations, there was a strong increasing trend in winter sea-surface temperature (SST) between 1986 and 1991. At four of the five stations, there was a smaller increasing trend in winter temperatures after 1960. There were no consistent or obvious trends in summer (August) temperatures. In Delaware Bay, which has a 40 year history of monitoring for oyster diseases, occasional findings of P. marinus in oysters were correlated with warming episodes that were especially notable in the winter (February) record. Empirical orthogonal function (EOF) analysis showed that winter temperatures varied consistently at the stations examined and were associated with variations in P. marinus prevalence. Associations using EOF analysis with August temperatures were much weaker. The SST record is consistent with the hypothesis that increasing winter water temperatures have been important in the recent outbreak of P. marinus epizootics in the north-eastern U.S.A. ? 1998 Academic Press Limited Keywords: climatic changes; oyster fisheries; parasitic diseases; temperature; Perkinsus marinus; north-eastern United States Introduction Members of the genus Perkinsus are warm-water parasites that infect a variety of molluscan species Perkinsus marinus is an endoparasite that causes around the world (Perkins, 1993). They are trans- Dermo disease in the eastern oyster, Crassostrea mitted directly from infected to uninfected hosts. virginica (Ford & Tripp, 1996). The parasite was first Perkinsus marinus multiplies at temperatures above discovered in the late 1940s and early 1950s over a 18–20 C, and proliferates most readily at 25 Cor region extending from the Gulf of Mexico along the ) ) higher (Chu, 1996; Ford & Tripp, 1996). Thus, the south-eastern U.S. coast into lower Chesapeake Bay failure of P. marinus to persist in Delaware Bay after (Mackin et al., 1950; Ray, 1954; Andrews & Hewatt, imports of infected oysters ceased was interpreted as 1957). The parasite was also found in Delaware Bay an indication that temperatures were too low to sus- during a period in the mid 1950s when large numbers tain the parasite in that estuary (Ford & Haskin, of seed oysters were being imported from the lower 1982). With the exception of a few isolated findings, Chesapeake Bay where P. marinus was prevalent P. marinus was not detected again in Delaware (Ford, 1996). After an embargo on imported oysters Bay until 1990, although during the late 1980s, the was instituted in 1959, prevalence of the parasite in parasite spread and intensified in Chesapeake Bay Delaware Bay decreased. (Burreson & Ragone Calvo, 1996). In August 1990, cCorresponding author. unusual mortalities of oysters in lower Delaware Bay 0272–7714/98/040587+11 $25.00/0/ec970283 ? 1998 Academic Press Limited 588 T. Cook et al. 42.5 trend in 1990–92 that stimulated a disease outbreak. Boston Ford’s argument was based on trends in air tempera- ture at sites near recent P. marinus epizootics and the observed correlations between air temperature and 4 5 near-shore water temperature (Jeffries & Johnson, 3 Massachusetts 1991 1976; Southward et al., 1988; Ford, unpubl. data). New York City In this paper, long-term sea-surface temperature 40.5 Long Island Sound 1992 (SST) records from five locations in the north-eastern U.S. were used, adjacent to sites where P. marinus has been detected recently, to determine whether the Northern New Jersey coast 1991 range extension of P. marinus is associated with 2 1 climate-related changes in water temperature. Both Atlantic Ocean long-term and short-term changes in the SST record Delaware Bay 1990 100 km were examined. Evidence from both Chesapeake and 38.5 75.5 73.5 71.5 Delaware Bays indicates that high winter tempera- F 1. Map of north-eastern U.S., showing sea-surface tures are more critical to the development or suppres- temperature (SST) stations with dates and locations of new sion of P. marinus epizootics than are high summer Perkinsus marinus observations. 1, Bivalve, NJ; 2, Atlantic temperatures or low winter temperatures (Burreson & City, NJ; 3, Bridgeport, CT; 4, Newport, RI; 5, Woods Ragone Calvo, 1996; Ford, 1996). For this reason, Hole, MA. SST trends for summer and winter seasons were examined separately. signalled a new outbreak of P. marinus infections. Within several months, infection prevalence had reached 90–100%. Equally high prevalences and con- Materials and methods sequent mortalities have occurred since then (Ford, 1996). In 1991 and 1992, additional reports of Five stations from New Jersey to Massachusetts were infected oysters occurred along a 500 km range from chosen to represent SST in the ‘ new ’ P. marinus southern New Jersey to Cape Cod, Massachusetts range (Figure 1, Table 1). Monthly mean water (Figure 1). By 1995, lightly infected oysters were temperatures for each station were obtained from the found as far north as Maine, and heavy infections National Oceanic and Atmospheric Administration were common in Long Island Sound and southern (NOAA), with the exception of Bivalve, NJ record, Massachusetts. which is part of a long-term data set at the Rutgers Hypotheses for the sudden range extension of University Haskin Shellfish Research Laboratory. His- P. marinus include: (1) recent introduction via the torical prevalence records for P. marinus in Delaware transplantation of infected oysters; (2) a change in the Bay were taken from Ford (1996). Each station is genetic structure of host or parasite; and (3) a change assumed to represent the water temperature trends in the environment that favours the parasite. Ford experienced by oysters on nearby growing grounds. (1996) reviewed evidence for and against these hy- For each station, monthly SST figures were potheses and proposed that the phenomenon resulted grouped into three data sets: (1) mean annual tem- from repeated historical introductions of P. marinus peratures based on monthly means for each year; (2) via many routes; survival of small, undetected popu- February values representing the winter temperatures; lations of the parasite in oysters; and a sharp warming and (3) August values representing the summer T 1. Location and length of sea-surface temperature record for each station Station name Location Lat/Long Record length Atlantic City Steel Pier, Atlantic Ocean, Atlantic City, NJ 39*21·3+N74*25·1+W 1950–1991 Bridgeport Tongue Pt Light, Bridgeport Harbor, Bridgeport, CT 41*10·4+N73*10·9+W 1964–1993 Bivalve Haskin Shellfish Research Lab, Maurice River, Bivalve, NJ 39*14·1+N75*01·9+W 1950–1993 Newport Gull Rocks Light, Narragansett Bay, Newport, RI 41*60·3+N71*19·6+W 1955–1994 Woods Hole Great Harbor Light, Buzzards Bay, Woods Hole, MA 41*31·4+N70*40·3+W 1950–1992 Data were acquired from the National Oceanographic and Atmospheric Administration and the Haskin Shellfish Research Laboratory. All temperatures were obtained by the bucket and thermometer method. Sea temperature increase and oyster disease spread 589 temperatures. Each data set was then analysed over obtained from the eigenvectors of the cross correlation three time intervals. The long-term record encom- matrix created from all possible pair-wise combi- passes the entire multidecade data set for each station nations of the input time series (with mean removed). (Table 1). The intermediate record extends from The sum of the eigenvalues is equal to the sum of the 1960 to the end of the data set. The short-term record diagonal terms of the correlation matrix, which is the includes the period from 1986 to 1991. The long- and total variance of the data. Therefore, the eigenvector intermediate-term records were used to document associated with the greatest eigenvalue represents the trends indicative of possible climate change. The largest fraction of the variance in the data. Each of short-term record described temperature change dur- the eigenvectors is then fit to the original data to create ing and just prior to the recent range expansion of the time variation of the given pattern. Thus, EOF P. marinus. Both annual and 5 year running averages analysis identifies variations in contemporaneous data of surface-water temperature were plotted for each sets that occur with a specific temporal pattern. location. The running average was used to remove All of the temperature and P. marinus infection data some of the variability from the monthly SST data and can be represented either as time series or as combi- to facilitate visualization of temperature trends.