Non-linear effects of non-host diversity on the removal of free-living infective stages of parasites.

Among the ecological functions and services of biodiversity is the potential buffering of diseases through dilution effects where increased biodiversity results in a reduction in disease risk for humans and wildlife hosts. Whether such effects are a universal phenomenon is still under intense debate and diversity effects are little studied in cases when non-host organisms remove free-living parasite stages during their transmission from one host to the next by consumption or physical obstruction. Here, we investigated non-host diversity effects on the removal of cercarial stages of trematodes, ubiquitous parasites in aquatic ecosystems. In laboratory experiments using response surface designs, varying both diversity and density at same time, we compared three combinations of two non-hosts at four density levels: predatory crabs that actively remove cercariae from the water column via their mouth parts and gills, filter feeding oysters that passively filter cercariae from the water column while not becoming infected themselves, and seaweed which physically obstructs cercariae. The addition of a second non-host did not generally result in increased parasite removal but neutralised, amplified or reduced the parasite removal exerted by the first non-host, depending on the density and non-host combination. These non-linear non-host diversity effects were probably driven by intra- and interspecific interactions and suggest the need to integrate non-host diversity effects in understanding the links between community diversity and infection risk.

Marine virus predation by non-host organisms.

Viruses are the most abundant biological entities in marine environments, however, despite its potential ecological implications, little is known about virus removal by ambient non-host organisms. Here, we examined the effects of a variety of non-host organisms on the removal of viruses. The marine algal virus PgV-07T (infective to Phaeocystis globosa) can be discriminated from bacteriophages using flow cytometry, facilitating its use as a representative model system. Of all the non-host organisms tested, anemones, polychaete larvae, sea squirts, crabs, cockles, oysters and sponges significantly reduced viral abundance. The latter four species reduced viral abundance the most, by 90, 43, 12 and 98% over 24 h, respectively. Breadcrumb sponges instantly removed viruses at high rates (176 mL h-1 g tissue dry wt-1) which continued over an extended period of time. The variety of non-host organisms capable of reducing viral abundance highlights that viral loss by ambient organisms is an overlooked avenue of viral ecology. Moreover, our finding that temperate sponges have the huge potential for constant and effective removal of viruses from the water column demonstrates that natural viral loss has, thus far, been underestimated.

Consumer and host body size effects on the removal of trematode cercariae by ambient communities.

Parasite transmission can be altered via the removal of parasites by the ambient communities in which parasite-host interactions take place. However, the mechanisms driving parasite removal remain poorly understood. Using marine trematode cercariae as a model system, we investigated the effects of consumer and host body size on parasite removal rates. Laboratory experiments revealed that consumer or host body size significantly affected cercarial removal rates in crabs, oysters and cockles but not in shrimps. In general, cercarial removal rates increased with consumer (crabs and oysters) and host (cockles) body size. For the filter feeding oysters and cockles, the effects probably relate to their feeding activity which is known to correlate with bivalve size. Low infection levels found in cockle hosts suggest that parasite removal by hosts also leads to significant mortality of infective stages. The size effects of crab and shrimp predators on cercarial removal rates were more complex and did not show an expected size match-mismatch between predators and their cercarial prey, suggesting that parasite removal rates in predators are species-specific. We conclude that to have a comprehensive understanding of parasite removal by ambient communities, more research into the various mechanisms of cercarial removal is required.

Effect of dose and frequency of exposure to infectious stages on trematode infection intensity and success in mussels.

Marine parasites such as trematodes often compromise the fitness of their hosts. Such effects are generally considered to be density-dependent, i.e. the greater the infection intensity in the host, the greater the detrimental impact on host fitness. However, the mechanisms determining infection in marine hosts are still poorly understood. Here, we investigated the effect of cercarial dose and exposure frequency (single vs. trickle infections) of a marine trematode parasite, Himasthla elongata (Trematoda: Echinostomatidae), on infection intensity and success in its second intermediate host, the blue mussel Mytilus edulis, an abundant and widely distributed bivalve in European coastal waters. In our laboratory experiment, we tested 4 levels of parasite doses and showed that mussels faced higher parasite infection intensity at higher doses of cercarial exposure and that they acquired more infections when repeatedly exposed to smaller doses compared to a single high dose. However, the infection success of cercariae did not differ among 4 dose levels but was only significantly different between trickle and single exposures. This indicates that cercariae were not subjected to a dose-dependent regulation of their infectivity, suggesting that infection intensity in mussels is largely driven by factors mediating the abundance of infective stages. With the combined investigation of the effect of cercarial dose and exposure frequency at realistic dose levels, our study contributes to our currently very limited understanding of the determinants of infection intensity in marine hosts and highlights the usefulness of experimental studies in advancing our knowledge in this field.

Parasites as prey: the effect of cercarial density and alternative prey on consumption of cercariae by four non-host species.

In parasites with complex life cycles the transmission of free-living infective stages can be influenced by ambient community diversity, in particular via predation. Here, we experimentally investigated whether parasite density and the presence of alternative prey can alter predation rates on free-living cercarial stages of a marine trematode by several non-host predators. All four predator species consumed increasing numbers of cercariae with an increase in cercarial density, indicating that the removal of cercariae by predators is effective over a range of natural densities as well as in the presence of alternative prey for a number of predators typical of marine ecosystems. However, the relative removal rates and the effects of cercarial density and alternative prey differed among predator species. In barnacles and shrimps, significant interactive effects of cercarial density and alternative prey on cercarial predation occurred while in oysters and crabs cercarial removal rates were unaffected by both factors. As changes in cercarial densities directly translate into changes in infection levels in down-stream hosts in this parasite-host system, the observed predator-specific responses suggest that cercarial predation effects on disease risks will depend on the specific species composition of ambient communities and not on non-host biodiversity per se.

The Use of Filter-feeders to Manage Disease in a Changing World.

Rapid environmental change is linked to increases in aquatic disease heightening the need to develop strategies to manage disease. Filter-feeding species are effective biofilters and can naturally mitigate disease risk to humans and wildlife. We review the role of filter-feeders, with an emphasis on bivalves, in altering disease outcomes via augmentation and reduction. Filtration can reduce transmission by removing pathogens from the water column via degradation and release of pathogens in pseudofeces. In other cases, filtration can increase pathogen transmission and disease risk. The effect of filtration on pathogen transmission depends on the selectivity of the filter-feeder, the degree of infectivity by the pathogen, the mechanism(s) of pathogen transmission and the ability of the pathogen to resist degradation. For example, some bacteria and viruses can resist degradation and accumulate within a filter-feeder leading to disease transmission to humans and other wildlife upon ingestion. Since bivalves can concentrate microorganisms, they are also useful as sentinels for the presence of pathogenic microorganisms. While somewhat less studied, other invertebrates, including ascidians and sponges may also provide ecosystem services by altering pathogen transmission. In all scenarios, climate change may affect the potential for filter-feeders to mitigate disease risk. We conclude that an assessment including empirical data and modeling of system-wide impacts should be conducted before selection of filter-feeders to mitigate disease. Such studies should consider physiology of the host and microbe and risk factors for negative impacts including augmentation of other pathogens.

Pathological and physiological effects of nicking on brown crab (Cancer pagurus) in the Irish crustacean fishery.

Nicking is used in fisheries to immobilize claws of brown crab (Cancer pagurus) in order to prevent cannibalism and fighting during storage. Nicking fractures the apodemes creating an open wound and damage to the internal claw tissues, which is the most valuable product of brown crab. In turn, this results in a reduction of quality of product and possibly compromises the host's defence mechanisms to other physiological challenges experienced throughout the post-harvest process. This study assessed the effects of nicking on the physiology and pathology of brown crab from the Irish fishery over 7 days. Results showed significantly elevated levels of muscle necrosis (P=0.005), total pathologies (P=0.022) and encirculating granulocytes in nicked crab compared to non-nicked crab. Mean glucose (212.0 µg/mL±108.4), lactate (36.52 µg/mL±38.74) and RI (11.05n±1.78) levels were higher in nicked crab indicating increased stress levels. Overall, histology results showed a significantly higher (P=0.022) occurrence of pathologies, such as melanised nodules, in nicked animals. In addition to an observed reduction in the quality of claw muscle, nicked crab also showed significantly higher (P=0.005) levels of necrosis in claw muscle. From the results of this study it is recommended that alternative retention methods are used.