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442 2006 568 Article-Web 1..11 Oecologia (2007) 151:82–92 DOI 10.1007/s00442-006-0568-z COMMUNITY ECOLOGY Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and Wshes Ryan F. Hechinger · Kevin D. LaVerty · Todd C. Huspeni · Andrew J. Brooks · Armand M. Kuris Received: 16 April 2006 / Accepted: 5 September 2006 / Published online: 6 October 2006 © Springer-Verlag 2006 Abstract Measuring biodiversity is diYcult. This has parasites are functionally coupled with the surrounding led to eVorts to seek taxa whose species richness corre- free-living diversity of vertebrate and invertebrate ani- lates with the species richness of other taxa. Such indi- mals. It has been shown that larval trematodes in snails cator taxa could then reduce the time and cost of correlate positively with bird diversity and abundance. assessing the biodiversity of the more extensive com- Here, we explore whether trematodes also correlate munity. The search for species richness correlations with standard measures of Wshes, and large and small has yielded mixed results, however. This may be pri- benthos, for 32 sites in three wetlands. We found asso- marily because of the lack of functional relationships ciations between trematodes and benthic communities between the taxa studied. Trematode parasites are that were not consistent across wetlands. The associa- highly promising bioindicators. Diverse assemblages of tions were, however, consistently positive for large larval trematode parasites are easily sampled in inter- benthic species richness and density. Some of the con- mediate host snails. Through their life cycles these trasting associations between trematode and benthos may be explained by negative associations between large and small benthos. We found no associations with Wsh communities (probably because of the inadequacy Communicated by Steven Kohler. of standard “snapshot” sampling methods for highly mobile Wshes). The results support further exploration Electronic supplementary material Supplementary material is available in the online version of this article at http://dx.doi.org/ of trematodes as bioindicators of diversity and abun- 10.1007/s00442-006-0568-z and is accessible for authorized users. dance of animal communities. R. F. Hechinger (&) · A. M. Kuris Keywords Cerithidea californica · Indicators · Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Biodiversity · Estuaries · Wetlands CA 93106-9610, USA e-mail: [email protected] Introduction R. F. Hechinger · K. D. LaVerty · T. C. Huspeni · A. J. Brooks · A. M. Kuris Marine Science Institute, University of California, People love shortcuts. Scientists and habitat managers Santa Barbara, CA, USA are not immune to this, particularly given the limited time and resources available to accomplish diYcult K. D. LaVerty US Geological Survey, tasks, for example assessment of biodiversity. In such Western Ecological Research Center, assessments we often want information about multiple Sacramento, CA, USA taxa from several replicated sites. Yet, measuring the biodiversity of entire communities is extremely diYcult T. C. Huspeni Y Department of Biology, University of Wisconsin, or impossible. This di culty has led to a search for indi- Stevens Point, WI, USA cator taxa whose species richness is consistently corre- 123 Oecologia (2007) 151:82–92 83 lated with the species richness of other taxa (Lawton Trematode Xatworm parasites are a particularly et al. 1998; Vessby et al. 2002; Olsgard et al. 2003; Kati promising indicator group (Kuris and LaVerty 1994; et al. 2004). Varied results from this search led Gun- Huspeni and LaVerty 2004; Huspeni et al. 2005), narsson et al. (2004) to suggest focusing on groups of because it is common for many trematode species to organisms that provide habitat or resources for other specialize on the same snail species as Wrst intermedi- groups of organisms. Because these organisms are func- ate host (where they can be eYciently sampled) but to tionally coupled, correlations between the condition diverge in the other hosts they use to complete their (e.g., diversity and abundance) of these groups would life cycles (where they are associated with many spe- tend to be more consistent than those between taxa cies at higher trophic levels) (Fig. 1). In these circum- without such direct connections. But, the problem here stances high species richness of parasites in snail hosts is that the presence of the indicator group (the provid- requires, and thus indicates, the presence of numerous ers of habitat or resources) does not necessitate the other taxa (i.e. the hosts required for other parts of the presence of the groups to be indicated (the users of the life cycles). Further, most trematodes are trophically habitat or resources). The converse situation does not transmitted to Wnal hosts in their life cycles. Thus, not suVer from this weakness, however. Organisms that only do such parasites reXect the presence of surround- obligatorily use other organisms as habitat or resources ing taxa, they are also directly indicative of functioning should be excellent indicators. The indicator groups trophic linkages (Gardner and Campbell 1992; Marco- directly depend on the condition of the groups to be gliese and Cone 1998). indicated. Many parasites have multiple-host life cycles In many aquatic and marine systems birds act as that necessarily link them to several diVerent taxa of important hosts for adult trematodes and are the surrounding animal communities. These sorts of para- sources of the trematode stages that infect snails site may therefore be excellent indicators of other com- (Fig. 1). Hechinger and LaVerty (2005) demonstrated ponents of community structure and function (Gardner positive correlations between the diversity of birds and and Campbell 1992; Marcogliese and Cone 1998). Here, diversity of trematodes infecting snail populations. we explore how an easily sampled community of trema- This pattern probably exists because diVerent trema- tode parasites in snails is associated with more diYcult tode species use diVerent bird species as Wnal hosts. to sample communities of Wshes and benthic inverte- Smith (2001), Hechinger and LaVerty (2005), and Fre- brates. The discovery of relationships between these densborg et al. (2006) also found positive associations parasites and surrounding free-living community com- between the abundance of birds and the prevalence of ponents would strongly support further exploration of trematode parasites in snails. This was expected, these parasites as bioindicators. because birds should transmit more trematodes to Fig. 1 A generalized repre- sentation of the trematode life cycles in our system 123 84 Oecologia (2007) 151:82–92 snails in areas where birds are more common. Trema- crabs. The parasites are trophically transmitted to Wnal todes are good indicators of birds, because accurately host wetland birds when the birds eat second interme- quantifying bird communities on small spatial scales diate hosts (except for one of the trematode species, and long-term scales is diYcult (Hechinger and LaV- which lacks a second intermediate host and the cerca- erty 2005; Huspeni et al. 2005). riae infect birds directly). The trematodes mature in In this study we investigate whether, like birds, local the birds, usually in the digestive tract. Trematode eggs Wsh and benthic invertebrate communities are positively or larvae pass with the birds’ excreta and subsequently associated with local trematode communities in snails. infect snails. Thus, although the 20 species of these This prediction has two general bases (Huspeni et al. trematodes diverge with regard to which hosts they 2005). First, Wshes and benthic invertebrates attract require to complete their life cycles, they all converge birds (Colwell and Landrum 1993; Gawlik 2002), which in populations of the horn snail. Information on which are the sources of the trematode stages that infect second intermediate and bird Wnal hosts are used by snails. Thus, sites with greater species richness and the diVerent trematode species is available elsewhere abundance of Wshes and benthos should have greater (Huspeni and LaVerty 2004; LaVerty et al. 2006). richness and abundance of birds. Consequently, this brings a greater richness and abundance of trematodes Field sampling to infect snails. Second, as mentioned above, diVerent trematode species use diVerent Wshes and benthic inver- We sampled Wsh, benthic invertebrate, and snail trema- tebrates as second intermediate hosts. A diverse and tode assemblages in three California coastal wetlands abundant trematode community in snails does not, (Morro Bay (35.34°N, 120.83°W), Carpinteria Salt therefore, merely reXect, but on some scale requires, Marsh (34.40°N, 119.53°W), and Mugu Lagoon the presence of diverse and abundant Wshes and benthic (34.10°N, 119.10°W)) in the summers of 2001 and 2002. invertebrates. We also predicted, because we assessed We sampled 20 sites in 2001 (four at Morro, eight at benthic invertebrates and Wshes using standard “snap- Carpinteria, and eight at Mugu) and 12 diVerent sites shot” techniques, that trematodes would most strongly in 2002 (four at Morro, three at Carpinteria, and Wve at associate with the more stationary component of the Mugu). Each site was a 20-m stretch of tidal creek run- community—that is, the benthos—rather than the vag- ning through pickleweed (Salicornia virginica) salt ile Wshes. Determining
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