Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail—from small to large scale

Shorebird abundance and spatial distribution of larval trematodes in the New Zealand mudsnail, Zeacumantus subcarinatus, were investigated in soft-sediment intertidal bays within Otago Harbour, South Island, New Zealand. In a small-scale study, recruitment of trematodes to caged sentinel snails and the prevalence of infection in free-living snails were examined across a grid of fifteen 50·25 m plots arranged in a representative area of an intertidal bay, in relation to within-plot shorebird abundance (definitive hosts) and tidal height. In a large-scale study, natural spatial variation of larval trematodes in Z. subcarinatus was examined across 12 bays in relation to local abundance of shorebirds. Our results revealed that trematode prevalence in snails was positively correlated with bird abundance across bays (R=0.503, P=0.006). In contrast, despite a difference in bird abundance between tidal heights, there was no evidence that trematode prevalence reflected the spatial distribution of birds in the small-scale study, suggesting that factors related to differences in submersion time may override the differential input of trematode eggs from birds. Introduction An increasing number of studies are focussing on explaining spatial variation in animal community structure and species richness (Blanchard and Bourget 1999; Grey 2002; Ricklefs 2004). Previously, parasitism was an overlooked biotic parameter, but its impact on host ecology is now widely accepted and has more recently been recognised as an important factor in the structure of animal communities and food webs (Minchella and Scott 1991; Mouritsen and Poulin 2002; Thompson et al. 2005). The spatial distribution of parasites is known to vary greatly between host populations (Esch and Fernandez 1993; Poulin 1998). To integrate the effect of parasites into current community structure models, it is important to understand the mechanisms underlying their recruitment into host populations. Larval trematodes in intertidal snails are classical examples of parasites with a heterogeneous spatial variation among hosts (Curtis and Hurd 1983; Poulin and Mouritsen 2003; Fredensborg et al. 2005). For many intertidal trematodes, the life cycle includes a snail first intermediate host, a second intermediate crustacean or mollusc host, and a bird definitive host. Sexual reproduction takes place inside the gastrointestinal tract of the bird host, and trematode eggs are passed out into the external environment with the faeces of the bird. Snails subsequently get infected either by accidentally ingesting a trematode egg when feeding non-selectively on the sediment or when they are penetrated by miracidia hatched from trematode eggs. The impact of trematodes on intermediate host ecology and community structure is well documented in the intertidal ecosystem (Sousa 1991; Thomas et al. 1997; Mouritsen and Poulin 2002). However, we currently do not understand how to predict and explain spatial heterogeneity in the impact of trematodes on benthic animal communities (Poulin and Mouritsen 2003). The high mobility of birds compared to the other hosts in the trematode life cycle makes birds the main Communicated by G.F. Humphrey, Sydney B. L. Fredensborg (&) Marine Science Institute, Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA 93106-9610, USA E-mail: [email protected] Fax: +1-805-8938062 K. N. Mouritsen Department of Marine Ecology, Institute of Biological Sciences, Aarhus University, Finlandsgade 14, 8200, Aarhus N, Denmark R. Poulin Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand Marine Biology (2006) 149: 275–283 DOI 10.1007/s00227-005-0184-1 dispersal agents of trematodes. The spatial distribution of bird definitive hosts is therefore naturally assumed to be responsible for the often highly heterogeneous spatial infection pattern of larval trematodes in their first intermediate hosts. In spite of this logical assumption, evidence is mostly circumstantial or indirect and based on few observational data on bird abundance (Matthews et al. 1985; Bustnes and Galaktionov 1999; Marcogliese et al. 2001; Skirnisson et al. 2004). Of the studies where bird abundance has been monitored, contrasting results have been obtained (Smith 2001; Kube et al. 2002; Latham and Poulin 2003; Hechinger and Lafferty 2005). The problems of relating bird abundance to trematode prevalence in snails are several. Most importantly, bird distribution is often highly variable in time and space, and transmission of trematode eggs from birds to snails is consequently difficult to predict at the scale at which snails are sampled. Hence, studies on large-scale patterns in trematode infection in Hydrobia spp. and on the similarly transmitted acanthocephalan parasites in shore crabs failed to demonstrate a significant relationship between parasite abundance in first intermediate hosts and the abundance of birds (Fredensborg 2001; Kube et al. 2002; Latham and Poulin 2003). In these studies, the variation in bird numbers over time was considerable within study areas. On the other hand, Smith (2001) found in a small-scale study that the recruitment of larval trematodes to the snail, Cerithidea scalariformis, was significantly related to the density of perches in a mangrove swamp used by wading birds. Further, in that study, a very predictable distribution of birds was observed due to their regular use of the same perches for roosting. Secondly, because trematode eggs can survive for extended periods of time in the external environment (McKindsey and McLaughlin 1993; Galaktionov and Dobrovolskij 2003), tidal currents, osmotic stress and desiccation may influence the distribution and survival of trematode eggs and thus affect the spatial distribution of trematodes in snails. While secondary dispersal of trematode eggs is likely to be of different importance at different spatial scales, virtually nothing is known about the fate of trematode eggs in the external environment. Finally, snail dispersal can also affect the spatial distribution of larval trematodes. This is especially relevant on a very local scale if infected snails have a different migration pattern to uninfected conspecifics (Miller and Poulin 2001), but is possibly also relevant on a regional scale for snail species utilising floating of adults as a means of dispersal. In this study, we investigated the low-tide spatial distribution of shorebirds in relation to the spatial variation of larval trematodes in the snail host, Zeacumantus subcarinatus. Bird abundance and spatial heterogeneity of larval trematodes in snails were measured at two different spatial scales: within an intertidal bay, and among intertidal bays within the same ecosystem. A repeatability analysis was performed at both spatial scales to test the predictability of the pattern of bird distribution within the study areas. Submersion time was included in the small-scale study, to evaluate the importance of tidal height to the availability of trematode eggs to snails. The results obtained at the two different spatial scales are discussed in relation to the habitat use of shorebird definitive hosts. Materials and methods Zeacumantus subcarinatus and its trematode parasites The New Zealand mudsnail, Z. subcarinatus, is a common inhabitant of soft-sediment intertidal mud flats in New Zealand, where it mainly feeds on epipelic and epiphytic diatoms. Data on laboratory-reared Z. subcarinatus and field observations reveal that this species has direct development (i.e. crawl-away larvae) (Fredensborg and Poulin 2005), and that reproduction takes place once a year during the Austral spring and summer from late October to February (B. Fredensborg, unpublished data). Based on size-frequency data from the study area, Z. subcarinatus has a lifespan of at least 5–6 years and reaches a maximum size of about 20 mm (B. Fredensborg, unpublished data). Z. subcarinatus is known to be the first intermediate host to five trematode species within the study area (Otago Harbour, New Zealand). The most common trematode is the recently discovered microphallid, Maritrema novaezealandensis (Martorelli et al. 2004; Fredensborg et al. 2005), which accounts for about 60% of all observed infections. A philophthalmid and the echinostomatid, Acanthoparyphium sp., are also relatively common while a heterophyid and Microphallus sp. are only rarely observed. The second intermediate host differs between species; however, they all utilise birds as the definitive hosts (Fig. 1). Transmission of trematode eggs to snails in all species except the philophthalmid occurs via the faeces of an infected bird. The philophthalmid differs from the others by occupying the eye of birds, and its eggs are released in the bird’s lacrimal secretions (Kearn 1998). Eggs of M. novaezealandensis and Microphallus sp. need to be ingested by a snail to hatch, while eggs of the other species hatch into miracidia larvae in the external environment and actively search for a snail. Due to ethical constraints, many bird species have not been confirmed as definitive hosts for trematodes via dissections, and little is therefore known about the importance of different bird species as definitive hosts for individual trematode species. Consequently, all data on trematode prevalence were pooled across trematode species prior to analysis.