Saturday, December 22, 2018

Exploring the dark food web? Start with molluscs first.

Parasites with complex life cycles, such as the ubiquitous digenetic trematodes, exploit different hosts for different reasons (i.e. asexual reproduction in a molluscan intermediate host and sexual reproduction in a vertebrate definitive host). At the same time, for transmission between different hosts, trematodes exploit trophic interactions between these hosts. Parasites with complex life cycles are hidden hitchhikers in food webs, creating an unseen web of interactions – what we might call the ‘dark food web’ (well, that’s what I like to call it because it sounds rad and you know, up with the times).

Parasites are consumers and constitute a large amount of biomass in communities (Kuris et al., 2008). There are a number of really great papers on the importance of incorporating parasites into food webs. For a start see Thompson et al. (2005), Lafferty et al. (2006, 2008) and the references within those papers. Furthermore, parasites are not only consumers, but are also predated upon (think gnathiid isopods and cleaner wrasse). Digenetic trematodes have a free-living larval stage, called a cercaria, which seeks to infect the next host in the digenean’s complex life-cycle. Cercariae are produced from asexual colonies residing in infected molluscs, and thousands of cercariae can emerge from an infected mollusc each day. In many communities a large proportion of the molluscs are infected with trematodes, so you can imagine that there are a lot of cercariae being pumped into the world’s ecosystems daily. This represents a huge, and mostly unstudied, path of energy flow in food webs (Thieltges et al. 2008; Morley, 2012).

Clearly incorporating parasites into food webs has great promise for understanding how complex ecological communities function. However, progress is generally hindered by a lack of knowledge of parasite life cycles. Most larval parasites are difficult to identify to species on the basis of morphology alone and in many cases these larval stages may only be identifiable to family (common for trematode cercaria). Thus traditional methods for elucidating life-cycles are slow and difficult. This process can be sped up significantly however, by using molecular barcodes to connect various life-cycle stages. I have done this twice previously (see this post and this post) – and in my recent(ish) paper I focused on molecularly characterising a whole community of trematodes parasitising a single species of gastropod on the Great Barrier Reef : 

Huston, D.C., Cutmore, S.C., and Cribb, T.H. 2018. Molecular systematics of the digenean community parasitising the cerithiid gastropod Clypeomorus batillariaeformis Habe & Kusage on the Great Barrier Reef. Parasitology international 67 (2018): 722735.

It took me over 3 years to collect all the data (mostly working on the side while I was on Heron Island for other reasons). Fortunately, I had a head start on this particular project because of the work of Cannon (1978), who had previously morphologically characterised most of the cercariae which I sequenced in my study. Although I didn’t find all the cercariae that Cannon (1978) described, I found two which he had not, showing a shift in the community structure over time. The new tally of digeneans which utilise Clypeomorus batillariaeformis on the Great Barrier Reef stands at 14! That is a large diversity and volume of cercariae being pumped into the waters of the Great Barrier Reef.

Although the morphology of the cercariae typically tell us what family they belong to, molecular data takes us a step further. Phylogenetic placements for cercariae can tell us what sorts of definitive hosts we ought to expect each cercariae ultimately aims to end up in, and from that we might infer what the transfer mechanisms might be. For example, in my study we found three species of the heterophyid genus Galactosomum. With that knowledge we know that the definitive hosts ought to be birds, and because all three of these species of Galactosomum had large, visually conspicuous cercariae we can infer that the second intermediate hosts are likely surface feeding fishes.

Characterising whole communities of digeneans from molluscs with molecules seems a great way to advance our understanding of food-web dynamics and build on our understanding of trematode-mollusc evolutionary interactions. Thus, when setting out to explore the dark food web, start with the snails first.


Cannon, L.R.G. (1978). Marine cercariae from the gastropod Cerithium moniliferum Kiener at Heron Island, Great Barrier Reef. Proceedings of the Royal Society of Queensland 89, 45–57.

Kuris, A.M., Hechinger, R.F., Shaw, J.C., Whitney, K.L., Aguirre-Macedo, L., Boch, C.A., Dobson, A.P., Dunham, E.J., Fredensborg, B.L., & Huspeni, T.C. (2008). Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515.

Lafferty, K.D., Allesina, S., Arim, M., Briggs, C.J., De Leo, G., Dobson, A.P., Dunne, J.A., Johnson, P.T.J., Kuris, A.M., & Marcogliese, D.J. (2008). Parasites in food webs: the ultimate missing links. Ecology letters 11, 533–546.

Lafferty, K.D., Dobson, A.P., & Kuris, A.M. (2006). Parasites dominate food web links. Proceedings of the National Academy of Sciences 103, 11211–11216.

Morley, N. (2012). Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 7-19.

Thieltges, D.W., de Montaudouin, X., Fredensborg, B., Jensen, K.T., Koprivnikar, J., & Poulin, R. (2008). Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Marine Ecology Progress Series 372, 147-155.

Thompson, R.M., Mouritsen, K.N., & Poulin, R. (2005). Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. Journal of Animal Ecology 74, 77-85.

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