The Ecological Importance of Horseshoe Crabs in Estuarine and Coastal Communities: A Review and Speculative Summary Mark L. Botton Abstract Beyond their commercial importance for LAL and bait, and their status as a living fossil, it is often asserted that horseshoe crabs play a vital role in the ecology of estuarine and coastal communities. How would the various ecological relationships involving horseshoe crabs be affected if these animals were no longer abundant? Attempts to understand and generalize the ecological importance of horseshoe crabs are hampered by several constraints. We know relatively little about the ecology of juvenile horseshoe crabs. Most ecological studies involving adult Limulus polyphemus have been conducted at only a few locations, while much less is known about the three Indo-Pacific species. Furthermore, we are attempting to infer the ecological importance of a group of animals whose numbers may have already declined significantly (the so-called ‘‘shifting baseline syndrome’’). Horseshoe crab shells serve as substrate for a large number of epibionts, such as barnacles and slipper limpets, but the relationships between these epibionts and horseshoe crabs appear to be facultative, rather than obligatory. Horseshoe crabs are dietary generalists, and adult crabs are ecologically important bivalve predators in some locations. The most notable predator–prey relationship involving horseshoe crabs is the migratory shorebird–horseshoe crab egg interaction in Delaware Bay. After hatching, the first and second instars are eaten by surf zone fishes, hermit crabs, and other predators. Virtually nothing is known about predator–prey relationships involving older juveniles, but adult L. polyphemus are important as food for the endangered loggerhead turtle, especially in the mid-Atlantic region. 1 Introduction As with discussions about the significance of preserving global biodiversity, the rationale for conserving horseshoe crabs is often condensed into monetary terms. On these grounds, the considerable economic value of horseshoe crabs for lysate, M.L. Botton (*) Department of Natural Sciences, Fordham College at Lincoln Center, 113 West 60th Street, New York 10023, USA e-mail: [email protected] J.T. Tanacredi et al. (eds.), Biology and Conservation of Horseshoe Crabs, 45 DOI 10.1007/978-0-387-89959-6_3, Ó Springer ScienceþBusiness Media, LLC 2009 [email protected] 46 M.L. Botton bait, and ecotourism makes a very forceful case for the need for sustainable horse- shoe crab populations (e.g., Berkson and Shuster 1999; Manion et al. 2000). However, just as the preservation of ecological diversity has ecological benefits that are not easy to transpose into dollars, horseshoe crabs may have underappre- ciated roles in the ecosystem that need to be part of the discourse about their value. The objective of this chapter is to review the ecological role of horseshoe crabs in estuarine and coastal environments with the goal of better understanding some of these additional ecological benefits. One way of envisioning the ecological roles (as suggested to me by Jane Brockmann) is to project how the functioning of ecosystems would differ if horseshoe crabs were absent or extremely rare. To accomplish this analysis, I subdivide the ecological role of horseshoe crabs into three parts: the importance of horseshoe crabs as predators, their importance as prey, and their importance as hosts for epibionts. In reviewing the literature, it became clear that there were constraints to the inferences that could be made about the ecological importance of horseshoe crabs. One reason for this is that most of the pertinent studies in the literature have been about L. polyphemus, with far fewer reports about Tachypleus tridentatus, T. gigas, and Carcinoscorpius rotundicauda. Of the ecological studies with L. polyphemus, most have been conducted on populations in the middle Atlantic and southern New England. There is also relatively little published information about the feeding ecology of juvenile horseshoe crabs and virtually nothing about the importance of predation on juveniles. It is worth emphasizing that other aspects of horseshoe crab behavior, such as the correlation between spawning intensity and the lunar and tidal cycle, are highly variable across the species’ range. For example, Barlow et al. (1986) found that spawning intensity in Cape Cod, Massachusetts was timed to coincide with the higher of the two daily high tides and that the highest peaks occurred on the spring tides (near the new moon and full moon). By contrast, in Delaware Bay the spring tide peaks may be disrupted by wind events and/or cold fronts that force the animals offshore until the return of favorable conditions (Shuster and Botton 1985, Smith and Michels 2006), and spawning in the Indian River Lagoon, Florida showed no relationship at all to the lunar cycle (Ehlinger et al. 2003). Given the extreme plasticity in spawning behavior, I would expect that there is geographic variation in feeding behavior and other aspects of the ecology as well. So, there is considerable danger in trying to generalize from the relatively few ecological studies of L. polyphemus in locations such as Delaware Bay and Cape Cod to other portions of its range, much less to the three other species. We are in the somewhat tenuous position of extrapolating the ecological importance of a group of animals whose abundance has already declined substantially, what Pauly (1995) has referred to as the ‘‘shifting baseline syndrome.’’ In other words, we risk misinterpreting the current situation as the norm, when in fact horseshoe crabs may have already been reduced to a small fraction of their historic abundances. For example, peaks in the Delaware Bay population that occurred during the nineteenth century may be imperfectly documented (Shuster 2003), but, in the writer’s opinion, are suggestive of [email protected] A Review and Speculative Summary 47 abundances far greater than any living scientist has witnessed. An even more extreme situation exists with T. tridentatus along the Seto Inland Sea in Japan, which have been reduced over the past century to the extent that some local populations are extinct (Tsuchiya 2009). The shifting baseline concept extends beyond the population level, in that the ecological importance of horseshoe crabs as predators, for example, is related to the collective impact of the population, so simply knowing what individual crabs eat is not enough to deduce the importance of these predators to the community. 2 Horseshoe Crabs as Predators 2.1 Predation by Adults Adult horseshoe crabs are omnivorous, feeding on a wide variety of benthic invertebrates, including bivalves, polychaetes, crustaceans, and gastropods. The functional morphology of feeding and the anatomy and physiology of the digestive system has recently been reviewed by Botton and Shuster (2003), so this contribution emphasizes the ecological importance of horseshoe crab predation on estuarine and coastal benthic communities. L. polyphemus on the mid-Atlantic continental shelf primarily feed on bivalves including blue mussels (Mytilus edulis) and surf clams (Spisula solidissima) (Botton and Haskin 1984; Botton and Ropes 1989). When crabs encounter patches of preferred prey such as thin-shelled bivalves, they may feed extensively, literally packing their guts with shells (Fig. 1). Prey selection has been demonstrated in laboratory feeding experiments (Botton 1984a), where crabs exhibited a clear preference for thin- shelled bivalves (e.g., dwarf surf clams, Mulinia lateralis or soft-shell clams, Mya arenaria) when given a choice between these and thicker shelled species, Fig. 1 A longitudinal section through a horseshoe crab showing the anterior portion of the digestive system (mouth, proventriculus or gizzard, and intestine). Note the presence of broken blue mussel shells (Mytilus edulis) in the intestine. Courtesy of Carl N. Shuster [email protected] 48 M.L. Botton including quahogs (Mercenaria mercenaria) and gem clams (Gemma gemma). Bivalves were the most important macrobenthic prey in the stomachs of adult L. polyphemus feeding on a Delaware Bay tidal flat during the breeding season (Botton 1984a), and this was true as well for T. gigas from India (Debnath et al. 1989). Both of these studies found that many animals contained sand, plant detritus, and minute food items such as Foraminifera and nematodes. Botton and Shuster (2003) suggested that when preferred prey are rare, horseshoe crabs may ingest sediment rather indiscriminately, which would account for the presence of such minutely sized food items. The horseshoe crab digestive system contains the enzyme cellulase (Debnath et al. 1989) demonstrating that the plant detritus may be nutritionally useful. The ecological importance of adult horseshoe crabs as predators has primarily been studied on intertidal sand bars and mud flats during the breeding season. Horseshoe crabs withdraw to these areas after spawning on the beaches at high tide, and while they await the return of the tide, they dig pits in search of food or to avoid desiccation. Predator exclusion techniques (caging experiments) have been used to assess the ecological importance of predation by adult horseshoe crabs in these habitats. The first of these studies was conducted in Massachusetts in response to assertions from commercial fishermen that predation was causing enormous destruction to planted soft-shell clams. Plots that were caged to exclude predators had significantly