When snails become the living dead: trematode parasites of the mud whelk, Batillaria australis

Emily Williams (Supervisors: Ross Coleman, Fleur Ponton and Ashley Ward)


Background
Larval form of Philophthalmus burrili

A parasite is usually defined as an organism that requires a host for at least one, if not all, of its life stages. These stages are not necessarily all parasitic; they can be a combination of parasitic and free-living. Parasites can have simple or very complex life cycles, can be very host-specific or have a broad range of hosts they are able to use and they come from every Phylum. Most importantly, they require their host for habitat and/or food and are usually detrimental to their host. Endoparasites live inside their host, while ectoparasites live on or use the outside of their hosts.

Intake of different nutrients affects longevity and reproductive success in animals. In terms of parasite-host interactions, virulence can be dependent on food availability. Because of the different trade-offs between the different life-history traits of the host, as well as the importance of nutrition on those traits, we can expect that parasites will modify the feeding behaviour of hosts to increase its own longevity. Changes in nutrient use and composition in parasitised hosts may be a direct effect of parasitism or a result of compensation by the host to limit damage.

When infected with a pathogen, animals can also display a change in immune response. Molluscs and other invertebrates have haemocytes in their haemolymph, as well as prophenoloxidase (ProPO) and phenoloxidase (PO) activity, which act as the cellular and humoral components of the immune system respectively. Fluctuations in these components can be triggered by wounding or infection by parasites and pathogens.

Some of the most common marine parasites are digenetic trematodes (Platyhelminthes: Trematoda: Digenea), which are endoparasitic and occupy vertebrate definitive hosts. The first intermediate hosts are always molluscs, which are host to the larval form of trematodes. These snail hosts are castrated for life by the trematode larvae but not killed, effectively becoming vehicles for the parasite. Trematode parthenitae typically fill the spaces between the gonadal tubules and occasionally take up space in the digestive gland or anterior portion of the body. The study system used in this project is the mud whelk Batillaria australis and the parasitic trematodes that infect it.

Aims
Larval form of unnamed Cyathocotylid 1

There are 6 broad aims of this project: (1) to determine the prevalence and distribution of parasitic trematode species inhabiting B. Australis around Sydney; (2) to see if parasitised snails are larger than non-parasitised snails; (3) to measure the lipid, protein and carbohydrate content of parasitised and non-parasitised snails and then use feeding trials to determine if snails select different diets based on infection status; (4) to determine if parasites induce a change in immune response of snails or if they evade the host’s immune system and how diet might affect this; (5) to look at possible chemical communication between parasitised and non-parasitised snails and if potential hosts can increase their immune response before infection; and (6) to use proteomics to investigate the molecular mechanisms occurring during host-parasite interactions by comparing the proteome of snails infected by different parasites and looking for the evolutionary convergences in the mechanisms occurring during infections.

Importance

Parasites are the most abundant organisms on Earth. There have been some estimates that parasites outnumber non-parasitic organisms by 4 to 1. Every living thing has at least one parasite living in it, though usually many more. There are many parasitic trematodes inhabiting snails that can infect humans and are incredibly damaging. By studying how trematodes affect snails in Australia, we may be able to extend the information to other species that are able to parasitise people.

There are also many problems with parasites in aquaculture or fisheries industries. The oyster industry in NSW has suffered a lot from QX disease, a protest parasite that damages the digestive gland of oysters, causing starvation and mortality. The Georges River alone loses 90% of its rock oysters to QX every year.

Parasites, though usually considered harmful, can be used to benefit ecology in a broader sense. Some parasites are incredibly sensitive to changes in the ecosystem, such as increased levels of chemicals and pollutants. They can be excellent indicators of ecosystem health.

Results

Collections of snails currently come from Narrabeen Lagoon. A large percentage of snails (approximately 31%) are infected with some sort of trematode. I have found the following species of parasitic trematode: Acanthoparyphium spinulosum, Cercaria 1, Cyathocotylid 1, Philophthalmus burrili and Stictodora lari. The unnamed cyathocotylid is the first unreported trematode found in B. Australis in this study.

Size distributions of snails indicate that parasitised snails are generally larger than non-parasitised snails. Trials looking at the lipid and protein concentration in gonads of parasitised (any species of parasite living in the snail) and non-parasitised snails showed that lipid content was greater in the gonads of non-parasitised snails than in parasitised snails. Protein content, however, was greater in the gonads of parasitised snails than in non-parasitised snails.