Predicting the Growth of Vibrio parahaemolyticus in Oysters under Varying Ambient Temperature.

Temperature is a critical factor that influences the proliferation of pathogens in hosts. One example of this is the human pathogen Vibrio parahaemolyticus (V. parahaemolyticus) in oysters. Here, a continuous time model was developed for predicting the growth of Vibrio parahaemolyticus in oysters under varying ambient temperature. The model was fit and evaluated against data from previous experiments. Once evaluated, the V. parahaemolyticus dynamics in oysters were estimated at different post-harvest varying temperature scenarios affected by water and air temperature and different ice treatment timing. The model performed adequately under varying temperature, reflecting that (i) increasing temperature, particularly in hot summers, favors a rapid V. parahaemolyticus growth in oysters, resulting in a very high risk of gastroenteritis in humans after consumption of a serving of raw oysters, (ii) pathogen inactivation due to day/night oscillations and, more evidently, due to ice treatments, and (iii) ice treatment is much more effective, limiting the risk of illness when applied immediately onboard compared to dockside. The model resulted in being a promising tool for improving the understanding of the V. parahaemolyticus-oyster system and supporting studies on the public health impact of pathogenic V. parahaemolyticus associated with raw oyster consumption. Although robust validation of the model predictions is needed, the initial results and evaluation showed the potential of the model to be easily modified to match similar systems where the temperature is a critical factor shaping the proliferation of pathogens in hosts.

Understanding Crassostrea virginica tolerance of Perkinsus marinus through global gene expression analysis.

Disease tolerance, a host's ability to limit damage from a given parasite burden, is quantified by the relationship between pathogen load and host survival or reproduction. Dermo disease, caused by the protozoan parasite P. marinus, negatively impacts survival in both wild and cultured eastern oyster (C. virginica) populations. Resistance to P. marinus has been the focus of previous studies, but tolerance also has important consequences for disease management in cultured and wild populations. In this study we measured dermo tolerance and evaluated global expression patterns of two sensitive and two tolerant eastern oyster families experimentally challenged with distinct doses of P. marinus (0, 106, 107, and 108 parasite spores per gram wet weight, n = 3-5 individuals per family per dose). Weighted Gene Correlation Network Analysis (WGCNA) identified several modules correlated with increasing parasite dose/infection intensity, as well as phenotype. Modules positively correlated with dose included transcripts and enriched GO terms related to hemocyte activation and cell cycle activity. Additionally, these modules included G-protein coupled receptor, toll-like receptor, and tumor necrosis factor pathways, which are important for immune effector molecule and apoptosis activation. Increased metabolic activity was also positively correlated with treatment. The module negatively correlated with infection intensity was enriched with GO terms associated with normal cellular activity and growth, indicating a trade-off with increased immune response. The module positively correlated with the tolerant phenotype was enriched for transcripts associated with "programmed cell death" and contained a large number of tripartite motif-containing proteins. Differential expression analysis was also performed on the 108 dosed group using the most sensitive family as the comparison reference. Results were consistent with the network analysis, but signals for "programmed cell death" and serine protease inhibitors were stronger in one tolerant family than the other, suggesting that there are multiple avenues for disease tolerance. These results provide new insight for defining dermo response traits and have important implications for applying selective breeding for disease management.

Vibrio vulnificus and Vibrio parahaemolyticus in Oysters under Low Tidal Range Conditions: Is Seawater Analysis Useful for Risk Assessment?

Human-pathogenic Vibrio bacteria are acquired by oysters through filtering seawater, however, the relationships between levels of these bacteria in measured in oysters and overlying waters are inconsistent across regions. The reasons for these discrepancies are unclear hindering our ability to assess if -or when- seawater samples can be used as a proxy for oysters to assess risk. We investigated whether concentrations of total and human pathogenic Vibrio vulnificus (vvhA and pilF genes) and Vibrio parahaemolyticus (tlh, tdh and trh genes) measured in seawater reflect concentrations of these bacteria in oysters (Crassostrea virginica) cultured within the US lower Chesapeake Bay region. We measured Vibrio spp. concentrations using an MPN-qPCR approach and analyzed the data using structural equation modeling (SEM). We found seawater concentrations of these bacteria to predictably respond to temperature and salinity over chlorophyll a, pheophytin or turbidity. We also inferred from the SEM results that Vibrio concentrations in seawater strongly predict their respective concentrations in oysters. We hypothesize that such seawater-oyster coupling can be observed in regions of low tidal range. Due to the ease of sampling and processing of seawater samples compared to oyster samples, we suggest that under low tidal range conditions, seawater samples can foster increased spatial and temporal coverage and complement data associated with oyster samples.

Evaluation of six methods for external attachment of electronic tags to fish: assessment of tag retention, growth and fish welfare.

External attachment of electronic tags has been increasingly used in fish studies. Many researchers have used ad hoc attachment methods and provided little or no validation for the assumption that tagging itself does not bias animal behaviour or survival. The authors compared six previously published methods for externally attaching acoustic transmitters to fish in a tank holding experiment with black sea bass Centropristis striata (L.). They tracked tag retention, fish growth and external trauma (as a measure of fish welfare) for 60 days. For each of these metrics, the results showed a wide range of responses among tagging treatments. A simple attachment method using a spaghetti tag passed through the dorsal musculature of the fish and tied to the end cap of the transmitter emerged as the preferred option based on high retention, no impact on growth and relatively low detriment to fish welfare. Future field studies using external electronic tagging should consider tag-related effects that could compromise results when selecting a method for tag attachment.

Modeling Pathogen Dispersal in Marine Fish and Shellfish.

In marine ecosystems, oceanographic processes often govern host contacts with infectious agents. Consequently, many approaches developed to quantify pathogen dispersal in terrestrial ecosystems have limited use in the marine context. Recent applications in marine disease modeling demonstrate that physical oceanographic models coupled with biological models of infectious agents can characterize dispersal networks of pathogens in marine ecosystems. Biophysical modeling has been used over the past two decades to model larval dispersion but has only recently been utilized in marine epidemiology. In this review, we describe how biophysical models function and how they can be used to measure connectivity of infectious agents between sites, test hypotheses regarding pathogen dispersal, and quantify patterns of pathogen spread, focusing on fish and shellfish pathogens.

Quality of a fished resource: Assessing spatial and temporal dynamics.

Understanding spatio-temporal variability in the demography of harvested species is essential to improve sustainability, especially if there is large geographic variation in demography. Reproductive patterns commonly vary spatially, which is particularly important for management of "roe"-based fisheries, since profits depend on both the number and reproductive condition of individuals. The red sea urchin, Mesocentrotus franciscanus, is harvested in California for its roe (gonad), which is sold to domestic and international sushi markets. The primary driver of price within this multi-million-dollar industry is gonad quality. A relatively simple measure of the fraction of the body mass that is gonad, the gonadosomatic index (GSI), provides important insight into the ecological and environmental factors associated with variability in reproductive quality, and hence value within the industry. We identified the seasonality of the reproductive cycle and determined whether it varied within a heavily fished region. We found that fishermen were predictable both temporally and spatially in collecting urchins according to the reproductive dynamics of urchins. We demonstrated the use of red sea urchin GSI as a simple, quantitative tool to predict quality, effort, landings, price, and value of the fishery. We found that current management is not effectively realizing some objectives for the southern California fishery, since the reproductive cycle does not match the cycle in northern California, where these management guidelines were originally shaped. Although regulations may not be meeting initial management goals, the scheme may in fact provide conservation benefits by curtailing effort during part of the high-quality fishing season right before spawning.

Fishing diseased abalone to promote yield and conservation.

Past theoretical models suggest fishing disease-impacted stocks can reduce parasite transmission, but this is a good management strategy only when the exploitation required to reduce transmission does not overfish the stock. We applied this concept to a red abalone fishery so impacted by an infectious disease (withering syndrome) that stock densities plummeted and managers closed the fishery. In addition to the non-selective fishing strategy considered by past disease-fishing models, we modelled targeting (culling) infected individuals, which is plausible in red abalone because modern diagnostic tools can determine infection without harming landed abalone and the diagnostic cost is minor relative to the catch value. The non-selective abalone fishing required to eradicate parasites exceeded thresholds for abalone sustainability, but targeting infected abalone allowed the fishery to generate yield and reduce parasite prevalence while maintaining stock densities at or above the densities attainable if the population was closed to fishing. The effect was strong enough that stock and yield increased even when the catch was one-third uninfected abalone. These results could apply to other fisheries as the diagnostic costs decline relative to catch value.

Mapping Physiological Suitability Limits for Malaria in Africa Under Climate Change.

We mapped current and future temperature suitability for malaria transmission in Africa using a published model that incorporates nonlinear physiological responses to temperature of the mosquito vector Anopheles gambiae and the malaria parasite Plasmodium falciparum. We found that a larger area of Africa currently experiences the ideal temperature for transmission than previously supposed. Under future climate projections, we predicted a modest increase in the overall area suitable for malaria transmission, but a net decrease in the most suitable area. Combined with human population density projections, our maps suggest that areas with temperatures suitable for year-round, highest-risk transmission will shift from coastal West Africa to the Albertine Rift between the Democratic Republic of Congo and Uganda, whereas areas with seasonal transmission suitability will shift toward sub-Saharan coastal areas. Mapping temperature suitability places important bounds on malaria transmissibility and, along with local level demographic, socioeconomic, and ecological factors, can indicate where resources may be best spent on malaria control.

Understanding uncertainty in temperature effects on vector-borne disease: a Bayesian approach.

Extrinsic environmental factors influence the distribution and population dynamics of many organisms, including insects that are of concern for human health and agriculture. This is particularly true for vector-borne infectious diseases like malaria, which is a major source of morbidity and mortality in humans. Understanding the mechanistic links between environment and population processes for these diseases is key to predicting the consequences of climate change on transmission and for developing effective interventions. An important measure of the intensity of disease transmission is the reproductive number R0. However, understanding the mechanisms linking R0 and temperature, an environmental factor driving disease risk, can be challenging because the data available for parameterization are often poor. To address this, we show how a Bayesian approach can help identify critical uncertainties in components of R0 and how this uncertainty is propagated into the estimate of R0. Most notably, we find that different parameters dominate the uncertainty at different temperature regimes: bite rate from 15 degrees C to 25 degrees C; fecundity across all temperatures, but especially approximately 25-32 degrees C; mortality from 20 degrees C to 30 degrees C; parasite development rate at degrees 15-16 degrees C and again at approximately 33-35 degrees C. Focusing empirical studies on these parameters and corresponding temperature ranges would be the most efficient way to improve estimates of R0. While we focus on malaria, our methods apply to improving process-based models more generally, including epidemiological, physiological niche, and species distribution models.

Parasite transmission through suspension feeding.

Suspension-feeding bivalve molluscs are confronted with a wide range of materials in the benthic marine environment. These materials include various sized plankton and the organic material derived from it, macroalgae, detritus and a diversity of microbial parasites that have adapted life stages to survive in the water column. For bivalve parasites to infect hosts though, they must first survive and remain infectious in the water column to make initial contact with hosts, and once in contact, enter and overcome elaborate pathways for particle sorting and selection. Even past these defenses, bivalve parasites are challenged with efficient systems of mechanical and chemical digestion and highly evolved systems of innate immunity. Here we review how bivalve parasites evade these hurdles to complete their life cycles and establish within bivalve hosts. We broadly cover significant viral, bacterial, and protozoan parasites of marine bivalve molluscs, and illustrate the emergent properties of these host-parasite systems where parasite transmission occurs through suspension feeding.

Abalone farm discharges the withering syndrome pathogen into the wild.

An intracellular bacterium Candidatus Xenohaliotis californiensis, also called Withering-Syndrome Rickettsia-Like Organism (WS-RLO), is the cause of mass mortalities that are the chief reason for endangerment of black abalone (Haliotis cracherodii). Using a real-time PCR assay, we found that a shore-based abalone farm (AF) in Santa Barbara, CA, USA discharged WS-RLO DNA into the ocean. Several other shore-based AFs discharge effluent into critical habitat for black abalone in California and this might affect the recovery of wild black abalone. Existing regulatory frameworks exist that could help protect wild species from pathogens released from shore-based aquaculture.

Combined analyses of kinship and FST suggest potential drivers of chaotic genetic patchiness in high gene-flow populations.

We combine kinship estimates with traditional F-statistics to explain contemporary drivers of population genetic differentiation despite high gene flow. We investigate range-wide population genetic structure of the California spiny (or red rock) lobster (Panulirus interruptus) and find slight, but significant global population differentiation in mtDNA (ΦST = 0.006, P = 0.001; D(est_Chao) = 0.025) and seven nuclear microsatellites (F(ST) = 0.004, P < 0.001; D(est_Chao) = 0.03), despite the species' 240- to 330-day pelagic larval duration. Significant population structure does not correlate with distance between sampling locations, and pairwise FST between adjacent sites often exceeds that among geographically distant locations. This result would typically be interpreted as unexplainable, chaotic genetic patchiness. However, kinship levels differ significantly among sites (pseudo-F(16,988) = 1.39, P = 0.001), and ten of 17 sample sites have significantly greater numbers of kin than expected by chance (P < 0.05). Moreover, a higher proportion of kin within sites strongly correlates with greater genetic differentiation among sites (D(est_Chao), R(2) = 0.66, P < 0.005). Sites with elevated mean kinship were geographically proximate to regions of high upwelling intensity (R(2) = 0.41, P = 0.0009). These results indicate that P. interruptus does not maintain a single homogenous population, despite extreme dispersal potential. Instead, these lobsters appear to either have substantial localized recruitment or maintain planktonic larval cohesiveness whereby siblings more likely settle together than disperse across sites. More broadly, our results contribute to a growing number of studies showing that low F(ST) and high family structure across populations can coexist, illuminating the foundations of cryptic genetic patterns and the nature of marine dispersal.

Variable intertidal temperature explains why disease endangers black abalone.

Epidemiological theory suggests that pathogens will not cause host extinctions because agents of disease should fade out when the host population is driven below a threshold density. Nevertheless, infectious diseases have threatened species with extinction on local scales by maintaining high incidence and the ability to spread efficiently even as host populations decline. Intertidal black abalone (Haliotis cracherodii), but not other abalone species, went extinct locally throughout much of southern California following the emergence of a Rickettsiales-like pathogen in the mid-1980s. The rickettsial disease, a condition known as withering syndrome (WS), and associated mortality occur at elevated water temperatures. We measured abalone body temperatures in the field and experimentally manipulated intertidal environmental conditions in the laboratory, testing the influence of mean temperature and daily temperature variability on key epizootiological processes of WS. Daily temperature variability increased the susceptibility of black abalone to infection, but disease expression occurred only at warm water temperatures and was independent of temperature variability. These results imply that high thermal variation of the marine intertidal zone allows the pathogen to readily infect black abalone, but infected individuals remain asymptomatic until water temperatures periodically exceed thresholds modulating WS. Mass mortalities can therefore occur before pathogen transmission is limited by density-dependent factors.

Optimal temperature for malaria transmission is dramatically lower than previously predicted.

The ecology of mosquito vectors and malaria parasites affect the incidence, seasonal transmission and geographical range of malaria. Most malaria models to date assume constant or linear responses of mosquito and parasite life-history traits to temperature, predicting optimal transmission at 31 °C. These models are at odds with field observations of transmission dating back nearly a century. We build a model with more realistic ecological assumptions about the thermal physiology of insects. Our model, which includes empirically derived nonlinear thermal responses, predicts optimal malaria transmission at 25 °C (6 °C lower than previous models). Moreover, the model predicts that transmission decreases dramatically at temperatures > 28 °C, altering predictions about how climate change will affect malaria. A large data set on malaria transmission risk in Africa validates both the 25 °C optimum and the decline above 28 °C. Using these more accurate nonlinear thermal-response models will aid in understanding the effects of current and future temperature regimes on disease transmission.

Utilizing spatial demographic and life history variation to optimize sustainable yield of a temperate sex-changing fish.

Fish populations vary geographically in demography and life history due to environmental and ecological processes and in response to exploitation. However, population dynamic models and stock assessments, used to manage fisheries, rarely explicitly incorporate spatial variation to inform management decisions. Here, we describe extensive geographic variation in several demographic and life history characteristics (e.g., size structure, growth, survivorship, maturation, and sex change) of California sheephead (Semicossyphus pulcher), a temperate rocky reef fish targeted by recreational and commercial fisheries. Fish were sampled from nine locations throughout southern California in 2007-2008. We developed a dynamic size and age-structured model, parameterized separately for each location, to assess the potential cost or benefit in terms of fisheries yield and conservation objectives of changing minimum size limits and/or fishing mortality rates (compared to the status quo). Results indicate that managing populations individually, with location-specific regulations, could increase yield by over 26% while maintaining conservative levels of spawning biomass. While this local management approach would be challenging to implement in practice, we found statistically similar increases in yield could be achieved by dividing southern California into two separate management regions, reflecting geographic similarities in demography. To maximize yield, size limits should be increased by 90 mm in the northern region and held at current levels in the south. We also found that managing the fishery as one single stock (the status quo), but with a size limit 50 mm greater than the current regulations, could increase overall fishery yield by 15%. Increases in size limits are predicted to enhance fishery yield and may also have important ecological consequences for the predatory role of sheephead in kelp forests. This framework for incorporating demographic variation into fisheries models can be exported generally to other species and may aid in identifying the appropriate spatial scales for fisheries management.