Mutualism And Coral Persistence: The Role Of Herbivore Resistance To Algal Chemical Defense - Statistical Data Included

Ecology, Sept, 1999 by John J. Stachowicz, Mark E. Hay

INTRODUCTION

Recent experimental investigations of positive interactions such as commensalism and facilitation demonstrate that they are predictable forces capable of shaping community structure and composition (Bertness and Callaway 1994, Bertness and Leonard 1997, Callaway and Walker 1997, Holmgren et al. 1997). In habitats with extreme physical (Bertness and Hacker 1994) or biotic (Atsatt and O'Dowd 1976, Hay 1986, Littler et al. 1986, Pfister and Hay 1988, Stachowicz and Hay 1996) stresses, species resistant to these stresses modify the local environment, allowing the persistence of less tolerant species and enhancing species diversity (Hacker and Gaines 1997). In contrast to this growing appreciation for the role of these one-way positive interactions in structuring ecological communities, mutualisms are still regularly portrayed as little more than natural history curiosities (but see Regal 1977, Vance 1978, Witman 1987). Thus, despite an impressive amount of amassed information about some mutualisms and their direct consequences for the participants (see reviews by Boucher et al. 1982, Addicott 1984, Boucher 1985, Bronstein 1994), there is still little rigorous empirical evidence for the broader role of mutualism in ecological communities.

Tropical reef-building corals and their endosymbiotic dinoflagellates are one of the most often cited examples of the importance of mutualism to community structure and function. This association provides reef corals with the bulk of their dietary requirements (Muscatine and Porter 1977, Davies 1991), enhancing calcification rates and reef accretion. Other less-obvious, but critically important, mutualisms between corals or calcified seaweeds (coralline algae) and mobile invertebrates have been reported; in these interactions, low-mobility invertebrates gain food or shelter from the host, while enhancing host fitness by discouraging predators (Glynn 1983, 1987)or removing competitors (Steneck 1982, Coen 1988, Littler et al. 1995, Stachowicz and Hay 1996). Such studies have rarely addressed the broader implications of these associations, but where they have, these mutualisms have been shown to facilitate the production of biogenic structure (Littler et al. 1995), which can have important community and ecosystem level consequences (Lawton and Jones 1995, Jones et al. 1997).

Positive interactions between corals and herbivores are at least partially responsible for the restriction of most corals to tropical environments (Johannes et al. 1983, Miller 1998). Although temperature may play an indirect role, many temperate and subarctic habitats support corals (Cerame-Vivas and Gray 1966, Squires and Keyes 1967, Jacques et al. 1983, Schumaker and Zibrowius 1985, Ruppert and Fox 1988), and some tropical species occur where temperatures decline to 10 [degrees] C or lower for certain months of the year (MacIntyre and Pilkey 1969, Ruppert and Fox 1988). Intolerance to cold is, therefore, not an insurmountable physical barrier. In well-lit habitats, corals are slow growing relative to seaweeds, and the persistence of coral reefs appears to be tightly linked to the high abundance of herbivores that prevent seaweed overgrowth of corals (Miller 1998). When herbivorous fishes or sea urchins are naturally or experimentally removed from tropical reefs, seaweed biomass increases dramatically and corals are smothered (Lewis 1986, Hughes 1989, 1994). In contrast, on temperate reefs, herbivorous fishes are less abundant than in the tropics and algal standing stock is typically much higher (Horn 1989, Choat 1991, Ebeling and Hixon 1991). On the temperate reefs investigated here, herbivorous fishes and urchins alter the species composition of the algal community through selective removal of preferred species, but they do not diminish total seaweed biomass (Miller and Hay 1996) and are thus unlikely to mediate coral-algal competition (see reviews in Lubchenco and Gaines 1981, Horn 1989). The dependence of corals on positive interactions with herbivores may thus help explain why corals are generally uncommon in temperate latitudes and why coral abundance is inversely correlated with algal abundance among habitats in temperate regions (Miller and Hay 1996, Miller 1998).

In contrast to this general latitudinal pattern, the coral Oculina arbuscula does co-occur with seaweeds on natural and artificial reefs in North Carolina. Although it forms much denser aggregations in poorly lit habitats where seaweeds are rare or absent, Oculina is a common member of many North Carolina reef communities (McCloskey 1970, Peckol and Searles 1984, Miller and Hay 1996). Oculina is also the only species of coral in this region with a structurally complex branching morphology that provides shelter for a species-rich epifauna. Over 300 species of invertebrates are known to live among the branches of Oculina colonies, and although only a few are obligate coral dwellers, many more are reported to complete much of their life cycle within the coral (McCloskey 1970). In this paper, we investigate the possibility that the success of Oculina on temperate reefs is derived from its ability to harbor symbiotic herbivorous crabs that mediate competition with encroaching seaweeds and invertebrates.