Parasitism can influence the intertidal zonation of non-host organisms

Zonation of organisms in soft-bottom intertidal habitats is mainly a consequence of the tidal sorting of the substrate and how benthic organisms respond to it, with predation and competition also playing a role. Although parasites are ubiquitous in these habitats and known agents of community structure, their impact on zonation is rarely considered. Here, using observational and experimental data, we show that parasitism of the cockle Austrovenus stutchburyi by echinostome trematodes has both direct and indirect effects on the zonation of four other animals associated with cockles on a New Zealand tidal flat. The trematodes encyst in the foot of cockles, leaving heavily infected cockles unable to bury and lying exposed on the sediment surface. Whereas cockle density peaks in the mid intertidal zone, both infection intensity by trematodes and density of surfaced cockles increase linearly towards the shore; this influences the vertical zonation of animals attaching to or feeding on cockles. First, the relative abundance of the whelk Cominella glandiformis increase exponentially shoreward, as does its rate of predation on cockles; the effect of the parasite on the cockles’ burying ability has thus shifted the peak abundance of whelk predators towards the upper tidal level, away from peak cockle densities. Second, the density of the anemone Anthopleura aureoradiata, corrected for the availability of its cockle substrate, peaks in the lower intertidal zone, although a transplantation experiment revealed that anemones can survive higher up the shore if attached to buried cockles. Anemones on exposed cockles are susceptible to desiccation, and thus again the parasiteinduced surfacing of cockles at higher tidal levels plays a role by decreasing substrate availability for anemones. Third, densities of the limpet Notoacmea helmsi increase rapidly toward higher tidal levels, where limpets graze the surfaces of empty cockle shells or live surfaced cockles. The availability of both substrates used by limpets is influenced either directly (surfaced cockles) or indirectly (empty shells, via whelk predation) by parasitism. Fourth, the fish Notolabrus celidotus feeds on cockles by cropping their foot. Although the lower intertidal is submerged for longer and cockle densities peak in the mid intertidal, the frequency of foot-cropping by fish peaks in the upper tidal levels, where parasitism maintains a high density of surfaced cockles. Our results are the first demonstration that parasitism of a key species can influence the zonation of non-host organisms, a phenomenon likely to occur in other systems.