The epizootics in eastern oysters, Crassostrea virginica, of haplosporidiosis or “MSX” disease caused by Haplosporidium nelsoni, and perkinsosis or “dermo” disease caused by Perkinsus marinus, were two of the most significant marine disease events of the last century. Haplosporidium nelsoni, a protozoan parasite native to Asian populations of the Pacific oyster Crassostrea gigas, emerged in Delaware Bay in 1957 and Chesapeake Bay in 1959 (Andrews 1962; Haskin, Stauber, and Mackin 1966), and in the decades that followed caused major mortality events from the Mid-Atlantic region of the USA to Atlantic Canada. Perkinsus marinus is a native pathogen, also a protozoan, that had always been present in southern US (and Mexican) Atlantic and Gulf waters as far north as the Chesapeake Bay region; it dramatically intensified in its activity and impacts in the mid-1980s, however, causing reduction and loss of oyster populations from the Chesapeake Bay region north to the New England region of the USA as it expanded its range rapidly northward (Burreson and Andrews 1988; Ford 1996).
The ecological and economic damage caused by the depletion of oyster resources, disease compounding the effects of more than a century of over-harvesting, produced substantial despair with regard to the future prospects for improvement in C. virginica resources. C. Ronald Franks, the Secretary of Natural Resources of the Chesapeake Bay region state of Maryland, USA, included the following words in a statement to the Sub-Committee on Fisheries Conservation, Wildlife and Oceans, of the Committee on Resources, US House of Representatives (October 14, 2003, Annapolis, Maryland, USA; serial no. 108-67):
The oyster diseases Dermo and MSX are a dominant influence, and unless they are substantially controlled–and no evidence suggests that they can be–the trend and the outlook for the native oyster [i.e., C. virginica] is bleak. There is little reason for optimism and even less evidence that we are making any progress in defeating these oyster diseases.
As early as the 1980s, serious consideration was given to introducing C. gigas to the Chesapeake Bay, and the states of Maryland and Virginia with the US Army Corps of Engineers came very close to introducing Asian oyster species Crassostrea ariakensis to the Chesapeake Bay in the early 2000s (National Research Council 2004). Around the same time introduction of C. ariakensis was being explored, “terraforming” of Chesapeake Bay with disease-resistant, hatchery produced, domesticated lines of native C. virginica to “genetically rehabilitate” flawed natural populations was also proposed (Allen, Brumbaugh, and Schulte 2003). That these potential inventions were appealing to proponents reflected a deep lack of optimism that C. virginica populations would ever begin to recover naturally, and this lack of optimism was, at least on the surface, not unfounded: after a half-century of exposure to H. nelsoni, and perhaps centuries, if not millennia, of exposure to P. marinus, oyster resources were in a worse state than ever. On what basis should there be any hope for improvement by natural processes?
The recent revelation that the 1980s intensification of P. marinus was due to the emergence and rapid dispersal of a hypervirulent P. marinus phenotype, which hypothetically arose due to alteration of the adaptive landscape for P. marinus through the earlier anthropogenic introduction of H. nelsoni (Carnegie et al. 2021), brings new perspective to much of this history of oyster diseases. There are important implications for our understanding of the trajectory of C. virginica resources; for approaches to their management and restoration; and beyond the C. virginica-P. marinus system, for understanding diseases of important marine resource species world-wide. I describe some of these implications in the paragraphs below.
First, the nadir for C. virginica is not exactly what we thought it was. The status of the C. virginica -P. marinus relationship between the mid-1980s and the early 2000s did not represent a continuing and deepening failure of the host in its interaction with a long-established pathogen, an assumption behind both the non-native oyster introduction and genetic rehabilitation paradigms that were presented as solutions for the “oyster problem”. Rather, it reflected an entirely new interaction between the oyster host and a pathogen that had changed dramatically in its engagement with the host: shortening its life cycle, infecting different tissues, and generally attacking its host far more intensely, and killing its host far more quickly, than it ever had in the past (Carnegie et al. 2021). Clear signs of any evolutionary response by C. virginica to this continuing parasitic challenge were absent in those years. Furthermore, physical modeling suggesting lower salinity areas of low infection by both H. nelsoni and P. marinus were key sources of oyster larval recruitment (North et al. 2008) reinforced earlier suggestions that resistance would be unlikely to develop because of the dominant contributions of low salinity oyster populations with no exposure or adaptation to diseases to reproduction in these systems. We now realise from analyses drawing on long-term monitoring that resistance to H. nelsoni was becoming established by the 1990s, if not earlier, even in higher salinity areas of Chesapeake Bay (Carnegie and Burreson 2011), as it had before in Delaware Bay (Haskin and Ford 1979). But for P. marinus, time, and oyster generations (an oyster generation conceivably being two years) (Hedgecock 1994), would need to pass before an adaptative response to hypervirulent P. marinus could develop and become widely manifest.
Second, the improvements in oyster populations in recent years should be viewed as at least potentially reflecting resistance and/or tolerance evolution with regard to P. marinus compounding the positive effects of increasing resistance to H. nelsoni—an adaptive response beginning to be expressed. We know precisely from oyster adaptation to H. nelsoni that oyster populations are not functioning in a way that precludes resistance (or tolerance) evolution against P. marinus. It is not only oysters in low salinity, disease-free areas that are reproducing; oysters in higher salinity, disease-intense waters must be reproducing as well (Carnegie and Burreson 2011), and selection should favor those capable of living longer, to greater fecundities, with more opportunities in living longer to pass on genes underlying resistance. Annual surveys indicate that oyster abundance indeed is increasing region-wide (e.g., Maryland Department of Natural Resources 2018; Southworth and Mann 2021). While this increase is popularly attributed to success in oyster restoration, particularly the adoption of very large projects conducted at the scale of small tributaries as a preferred strategy, it difficult to imagine a relatively small number of even large restoration projects driving an oyster increase at the vast 300-km scale of the Chesapeake Bay estuary. Other evidence points directly to oyster adaptation, including decreases in oyster mortality despite continued intense P. marinus infection pressure that are evident in the long-term monitoring data (e.g., Southworth and Mann 2021), and indications of increased gonadal area indices and oocyte densities in P. marinus- and H. nelsoni-endemic oyster populations in the Virginia part of Chesapeake Bay beginning around 2003 (Huey 2018). With such signs of oyster adaptation emerging, resource managers should strive to harness this adaptation to greatest effect. Incorporating sanctuaries from harvest, for example, into management paradigms to promote continued adaptation on the part of the oyster should be part of this. However, we should also reconsider the scale of oyster restoration: not just focusing large-scale efforts on a few tributaries at a time, but engaging communities to expand restoration activity as broadly as possible to harness oyster adaptation across the full spatial and geographic extent at which it is occurring.
Finally, the C. virginica-H. nelsoni-P. marinus system highlights the importance of long-term monitoring for understanding ecological and evolutionary dynamics in all our disease systems as they play out over decades. This is a point that was made earlier in another, recent forum, the ICES Workshop on Emerging Mollusc Pathogens (ICES 2019), but it deserves mention here too as an area warranting priority attention. Without long-term perspective on key disease metrics such as prevalence and intensity profiles over some degree of space, it is impossible to ascertain patterns of change that could be relevant to control of important diseases. Without additional perspective on relevant host and environmental factors that may be important, such as host abundance or density or demographics, and water temperature, salinity, and so on, it may be difficult to interpret, and construct hypothesis concerning, epizootiological patterns that may emerge. Yet the lesson of the oyster disease system in the eastern USA is that these relationships are dynamic, and important changes may be occurring that we should understand if we are to successfully manage aquatic diseases as effectively as we must. While it is just not feasible to collect highly granular data across all our important host-pathogen systems wherever they occur, we might envision identifying networks of key populations or sites that can be more intensively evaluated over time; partnering more effectively with fisheries agencies and other resource managers and with commercial interests to pursue and integrate key perspective on host populations; and integrating environmental data collection with oceanographic and meteorological observations at different scales to allow for modelling of system function under changing climate. This will allow the relative roles of environmental drivers of change to be better understood, providing an important backdrop against which evolutionary dynamics might be inferred.
As aquaculture in particular grows in importance as a source of sustenance for growing human populations, and as global change including to marine and freshwater aquatic environments intensifies, we are not expanding efforts fast enough to understand disease dynamics in cultured and wild systems under this dynamic change. In fact, disease surveillance often has eroded relative to activity in the past. The case study of P. marinus and H. nelsoni in C. virginica is useful in underscoring the importance of intensive and long-term disease surveillance, and in providing a template for how we may similarly view other systems.
Acknowledgements
The author is most grateful to the organisers of the EAFP’s 20th International Conference on Diseases of Fish and Shellfish for the invitation to give this presentation.