Fishing pressure and habitat degradation are severe and pervasive threats to coastal marine ecosystems. Both are known to impact the dynamics of host movement, aggregation, nutrition, and mortality, and therefore the transmission of disease. The role of fishing pressure in facilitating the emergence and spread of diseases in marine systems is poorly understood, although circumstantial evidence suggests that overexploitation has contributed to the emergence of disease in several marine fisheries. In this research, scientists from Virginia Institute of Marine Sciences and from Old Dominion University will investigate how fishing pressure and declining water quality combine with the hydrography of small coastal estuaries on the Delmarva peninsula to promote outbreaks of a pathogenic parasite, Hematodinium, in blue crabs. Overlying seasonal outbreaks of the disease is an intensive fishery for the blue crab, which alters the population structure of the host by removing the more disease-resistant adults. Thus, the fishery increases the relative number of susceptible individuals both directly, by removing adults, and indirectly by releasing juveniles from density-dependent cannibalism. Potentially counter-balancing these anthropogenically-induced effects are the rapid growth rate of the blue crab, a seasonal nadir in infection dynamics, and an ontogenetic shift in host susceptibility to infection that may constrain transmission of the disease. Over five years of work, the research will; assess the prevalence and spatial distribution of Hematodinium infections in juvenile and adult blue crabs in relation to the topology of coastal bays on the Delmarva Peninsula; determine the effect of the blue crab fishery on the population structure of healthy and diseased blue crabs; determine how environmental factors affect infections in blue crabs and how they affect the life history and spread of the pathogen; clarify the modes of transmission in the life history of the parasite and their efficiencies in relation to host factors; model the underlying mechanisms that control the spread of disease and predict outbreaks in relation to changes in fishing pressure and environmental stressors. In terms of broader impacts, the disease causes significant annual losses to national and international crustacean fisheries. This study will produce an epidemiological model capable of integrating local environmental change and fishing pressure with disease dynamics with broad application to several finfish and shellfish populations. The PIs will continue their strong involvement with mentoring of undergraduates, graduate students, and postdoctoral fellows in this project, including participation in NSF REU programs at VIMS and ODU. Three outreach programs will include an annual meeting with fishermen, resource managers and environmental stewards, an outreach program in local high schools, and development of a website on Hematodinium.

Project Report

Fishing pressure and habitat degradation are severe and pervasive threats to marine ecosystems. Both impact the dynamics of host movement, aggregation, nutrition, and mortality, and therefore the transmission of disease. We investigated how fishing pressure combined with the physiography of small coastal estuaries facilitates outbreaks of a pathogen in blue crabs, Callinectes sapidus. Outbreaks of the parasitic dinoflagellate Hematodinium perezi are associated with high salinity, shallow lagoons along the eastern seaboard of the USA. Physical features entrain water masses within these systems and amplify the spread of the pathogen leading to outbreaks of the parasite in blue crabs. Overlying this is an intensive fishery for the blue crab, which alters the population structure of the host, essentially removing the more disease-resistant adults. Thus, the fishery may increases the relative number of susceptible individuals both directly, by removing adults, and indirectly by releasing juveniles from density-dependent cannibalism. Countering these effects are the rapid growth rate of the blue crab, a seasonal nadir in infection dynamics, and an ontogenetic shift in host susceptibility. The objectives were: (I) to assess the prevalence and spatial distribution of Hematodinium infections in juvenile and adult blue crabs in relation to the topology of coastal bays on the Delmarva Peninsula; (II) to determine the effect of the blue crab fishery on the population structure of healthy and diseased blue crabs; (III) to determine how environmental factors affect infections in blue crabs and how they affect the life history and spread of the pathogen; (IV) to clarify the modes of transmission in the life history of the parasite and their efficiencies in relation to host factors; and (V) to model the underlying mechanisms that control the spread of disease and predict outbreaks in relation to changes in fishing pressure and environmental stressors. Species of Hematodinium cause significant annual losses to several important crustacean fisheries. Prevalence levels of H. perezi may approach 100% during outbreaks in populations of the blue crab, and infections are typically fatal. Based on molecular evidence the species in blue crabs was identified as H. perezi genotype III (Small et al. 2012). Sequence studies indicate H. perezi infects blue crabs and many alternate hosts, including amphipods, and other crab species, from Virginia to Texas (Pagenkopp Lohan et al. 2012b, 2013). A quantitative PCR assay was developed to quantify dinospores in water samples (Li et al. 2009). Dinospores were shown to live less than 7 days. Infections can occur in crabs at low salinities, but dinospores do not thrive at <20 psu (Coffey et al. 2012). Microsatellite markers showed that the parasite had a high diversity in the crab population, infections were haploid, and 50% of the infections had multiple strains of the parasite (Pagenkopp Lohan et al. 2012, 2013). The life cycle of H. perezi was described from in vitro cultures (Li et al. 2011a). This represents a breakthrough and allows for additional studies on the parasite. Cultures show variability in asexual growth, variations in the type of dinospores produced, and the presence of a multi-nucleate schizont-like stage. Transmission of H. perezi remains a key component to resolve. Production of dinospores during periods of host molting is suggestive of transmission through an infectious spore (Li et al. in prep.). Prevalence increases 30-40 days after peaks in pubertal molting (Shields et al. in prep.). A technique was developed for exposing juvenile crabs to pathogens and assessing infectivity. None of the exposed crabs obtained demonstrable infections via histology, and only a few were faintly positive by PCR (Dolan et al. in prep.). While the results were equivocal, the approach shows great promise. The parasite is not transmitted via cannibalism or scavenging (Li et al. 2011b). Field studies showed that during autumnal peaks in prevalence, dinospore densities can be high in water samples, approaching 100% occurrence with densities ranging from 1-100+ parasites/L (Li et al. in prep.). Dinospore densities were associated with the endemicity of the parasite in crabs in relation to physiographical features, particularly residence time of small bays on the Eastern Shore. Entrained water masses constrained by physiographic features within the coastal systems retain the infectious stages of the pathogen during periods of host recruitment; thus contributing to the rapid amplification of the pathogen and disease outbreaks in blue crabs (Shields et al. 2012). While environmental forcing accounts for much of the variability in recruitment of marine animals, disease-related mortality may be a factor in the stasis of the blue crab population in Chesapeake Bay. This grant led to 15 peer-reviewed publications, 22 presentations at scientific meetings, and 10 invited presentations, with additional papers and activities in various stages of production. The educational component comprised 5 graduate students (2 MS, 3 PhD.), 4 postdocs, 1 visiting researcher, and 6 undergraduates, including 6 women and 2 international students. More info: www.vims.edu/research/departments/eaah/programs/crustacean/research/index.php References: www.vims.edu/~jeff/pubs.htm

Agency
National Science Foundation (NSF)
Institute
Division of Ocean Sciences (OCE)
Type
Standard Grant (Standard)
Application #
0723662
Program Officer
Michael Lesser
Project Start
Project End
Budget Start
2007-08-01
Budget End
2013-07-31
Support Year
Fiscal Year
2007
Total Cost
$2,110,161
Indirect Cost
Name
College of William & Mary Virginia Institute of Marine Science
Department
Type
DUNS #
City
Gloucester Point
State
VA
Country
United States
Zip Code
23062