Individuals of Crepidula adunca (Mollusca, Gastropoda) avoid shared doom through host specificity

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Abstract

Individuals of the epibiotic gastropod Crepidula adunca predominantly utilize the gastropod Calliostoma ligatum as their hosts in the San Juan Islands, Washington, rather than exploiting other potential host species. Snails of Margarites pupillus would appear to be particularly good alternate hosts, given their similarities in microhabitat choice, shell shape, and taxonomic closeness with Calliostoma ligatum. However, M. pupillus are almost never utilized as a host by Crepidula adunca. We examined the reasons for host fidelity by Crepidula adunca in the San Juan Islands. The small but voracious sea star Leptasterias hexactis was common across all our intertidal survey sites and consumed significantly more M. pupillus than Calliostoma ligatum in laboratory experiments. Individuals of Calliostoma ligatum stimulated by tube feet from Leptasterias hexactis moved significantly more quickly than non-stimulated individuals, but snails of this species stimulated by Pycnopodia helianthoides did not move at a significantly different rate than non-stimulated snails. There was a significant positive correlation between gastropod size and the rate of movement for Calliostoma ligatum stimulated by Leptasterias hexactis, but this correlation was not significant for non-stimulated individuals. Neither stimulation by asteroids nor gastropod size (whether for stimulated or non-stimulated snails) had a significant effect on the rate of movement for M. pupillus. Thus Calliostoma ligatum, and especially large individuals of this species, react more than M. pupillus to the presence of a common predator (Leptasterias hexactis) in such a way that likely elevates the snails' chance of escape. Finally, we found that Calliostoma ligatum used both chemical and physical defenses to effectively repel attacks by Leptasterias hexactis, while defenses by M. pupillus were less successful. We suggest that epibiotic Crepidula adunca specialize on Calliostoma ligatum in the San Juan Islands because this particular host species is more likely to protect the epibiont from shared doom due to its effective defenses against potential predators.

Highlights

► Crepidula adunca may avoid shared doom by using Calliostoma ligatum as a host. ► Field trials: predators consumed more Margarites pupillus than Calliostoma ligatum. ► Laboratory trials: common predators preferred M. pupillus to Calliostoma ligatum. ► Calliostoma ligatum is faster than M. pupillus when stimulated by Leptasterias hexactis. ► Body size affected speed in Calliostoma ligatum but not in M. pupillus.

Introduction

Residing on the wrong host may leave an associate at risk of death by shared doom (Wahl and Hay, 1995), wherein both the epibiont and host are killed by the host's predator. “One of the greatest hazards in an epibiont's life is the danger of falling victim to predators of the substrate organism” (p. 180 in Wahl, 1989). Even if the epibiont survives direct, immediate mortality caused by the host's predator, the attached organism may eventually die if it cannot readily move to a new suitable host. Therefore, it is often to the epibiont's advantage, especially for one with limited movement, to reside on a host species with a low predation rate and to avoid damaging the host in a manner that would dramatically increase that rate.

Individuals of Crepidula adunca G. B. SOWERBY I, 1825 (Gastropoda, Calyptraeidae) are suspension-feeding snails that engage in long-term epibiotic associations. Adults are sedentary and the epibiont's shell grows to fit the curvature of its host's shell (Hoagland, 1979, Vermeij et al., 1987). Consequently, adult Crepidula adunca are especially vulnerable to predation when dislodged from hosts (Vermeij et al., 1987; Iyengar, personal observation). Thus, the mobile juveniles must choose long-term hosts that minimize their chances of death by shared doom.

In the San Juan Islands, Washington, USA, individuals of Crepidula adunca disproportionately utilize snails of Calliostoma ligatum (GOULD, 1849) as hosts rather than using other species (Vermeij et al., 1987, Iyengar et al., in review). One species that would seem a suitable alternative host is the gastropod Margarites pupillus (GOULD, 1849). Snails of this species are similar in size and shell morphology to Calliostoma ligatum, both species belong to the superfamily Trochoidea (Bouchet and Rocroi, 2005), and M. pupillus can be as prevalent as Calliostoma ligatum at sites on San Juan Island (Iyengar et al., submitted for publication). Even though the two species are often found within a meter of each other, shells of M. pupillus almost never host individuals of Crepidula adunca (Iyengar et al., submitted for publication).

The host fidelity displayed by Crepidula adunca may be to minimize the epibiont's chances of death through shared doom. Calliostoma ligatum is one of the fastest intertidal gastropods in the San Juan Islands, and moves more quickly than M. pupillus in response to the predatory sea star Pisaster ochraceus (BRANDT, 1835) (Miller, 1974). We extended Miller's (1974) previous studies, examining the relative ability of these two snail species to hasten their pace after stimulation by other species of common intertidal asteroid predators and determining the relationship between speed of movement and body size for each gastropod species.

To determine why individuals of Crepidula adunca are restricted to Calliostoma ligatum in their choice of hosts, we examined the potential benefits gained by the epibionts from Calliostoma ligatum compared with M. pupillus. We (1) surveyed local areas to determine the predatory species co-occurring with Crepidula adunca, (2) examined whether predators consume more individuals of M. pupillus than Calliostoma ligatum in laboratory and field experiments, (3) measured movement rates for variously-sized individuals of Calliostoma ligatum and M. pupillus, both when the snails were not stimulated and when they were stimulated by tube feet of predatory sea stars, and (4) investigated whether predator deterrence was due to physical or behavioral defenses of the potential host snails.

Section snippets

Materials and methods

All field surveys and laboratory experiments were conducted June–July 2007 and July–August 2008 on San Juan Island, Washington, USA.

Field surveys of potential predators

Individuals of five species of predators were common in the areas surveyed: the sea stars Leptasterias hexactis and P. ochraceus, the snail Lirabuccinum dirum, and the crabs Cancer oregonensis and Cancer productus. The most common predators on the west side of San Juan Island (Land Bank and Deadman Bay) were individuals of Leptasterias hexactis and Lirabuccinum dirum, while individuals of Leptasterias hexactis and Cancer oregonensis were the most common predators at Colin's Cove (Table 1).

Choice by predators given mobile prey

Discussion

In the San Juan Islands, individuals of Crepidula adunca almost exclusively use the shells of Calliostoma ligatum as hosts; even the alternate host snail M. pupillus is rarely used by these epibionts. The host specificity of Crepidula adunca is likely driven in part by the different selection pressures that predators exert on the potential hosts. Individuals of P. ochraceus and Cancer productus were relatively rare in our intertidal surveys of potential predators, and Cancer oregonensis was

Conclusion

In an effort to explain the strong host fidelity of Crepidula adunca in the San Juan Islands, we undertook a series of experiments to investigate whether snails of Calliostoma ligatum provide benefits to their epibionts that snails of M. pupillus could not. While individuals of both Leptasterias hexactis and Lirabuccinum dirum were common at our study sites, local predation pressure by this latter species is likely low for both Calliostoma ligatum and M. pupillus. On the other hand, asteroids

Acknowledgments

We would like to thank the director and staff of Friday Harbor Laboratories (FHL) for assistance and laboratory space. Funding for this work was generously provided by Muhlenberg College through the Dean's Summer Student Research Grant and Dr. John E. Trainer Scholarship to Herstoff and summer research faculty grants to Iyengar. [SS]

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