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): 722–735.
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.
References
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.
