Vol. 367: 185–192, 2008 MARINE ECOLOGY PROGRESS SERIES Published September 11 doi: 10.3354/meps07450 Mar Ecol Prog Ser Mobile ‘reefs’ in the northeastern Gulf of California: aggregations of black murex snails Hexaplex nigritus as habitat for invertebrates Rebecca Prescott1, 2,*, Richard Cudney-Bueno1, 3 1School of Natural Resources, University of Arizona, Biosciences East, Room 325, Tucson, Arizona 85721, USA 2University of Hawaii, Kewalo Marine Laboratory, 41 Ahui Street, Honolulu, Hawaii 96813, USA 3Institute of Marine Science, University of California at Santa Cruz, 100 Schaffer Road, Santa Cruz, California 95060, USA ABSTRACT: We documented positive interactions created by aggregations of black murex snail Hexaplex nigritus that support an epifaunal community annually. We examined abundance, species richness, and species composition of epifauna associated with aggregations, sampling snails from 12 aggregations and collecting epifauna from snails. We estimated 49 100 organisms (±7400) within a 25 m2 area of an aggregation, many of which were juvenile invertebrates, and 193 species (95% CI 178–224) representing at least 7 trophic guilds. Epifauna occur on H. nigritus because shell structure provides benthic habitat heterogeneity, although biological characteristics of this foundation species may influence the associated composition of epifauna. To test this hypothesis, we anchored artificial reefs constructed of black murex shells and compared epifaunal communities that developed on them to those on aggregations. Abundance of epifauna was not different between aggregations and artificial reefs (p = 0.4); however, species composition was different (p = 0.005, R = 0.7). Epifaunal communities of aggregations had higher numbers of filter feeders and grazers than artificial reefs. Black murex snails illustrate that mobile benthic organisms can function as a foundation species and that biological characteristics of a foundation species may influence the associated composition of species. This system is ephemeral in nature, and epifauna that occur each spring and summer on snails may vary considerably. Loss of large H. nigritus aggregations has been documented due to overfishing, and declines in black murex populations result in the loss of a benthic substrate. KEY WORDS: Benthic diversity · Biogenic reefs · Black murex · Hexaplex nigritus · Epifauna · Gulf of California · Foundation species · Habitat modifier Resale or republication not permitted without written consent of the publisher INTRODUCTION and raising benthic organisms into the water column (Duggins et al. 1990, Irlandi & Peterson 1991, Harvey Many marine benthic communities are generated by et al. 1993). These foundation species can transform a habitat-modifying species or foundation species (Day- 2-dimensional landscape into a complex 3-dimensional ton 1972, Bruno & Bertness 2001), which create spatial landscape (Bruno & Bertness 2001) and increase spe- refuge from environmental stress and predation simply cies richness on a local scale (Heck & Wetstone 1977, by their presence (Dayton 1975, Bruno & Bertness Thompson et al. 1996). 2001). Foundation species such as kelps, corals, and In the benthic environment of the northeastern Gulf oysters can facilitate communities by providing a site of California, strips of rocky reef are a limited substrate of attachment for sessile organisms (Witman 1985, for rocky reef invertebrates and fish and are separated Duggins et al. 1990) and enhancing propagule supply by vast sandy plains. Consequently, as in other loca- or retention (Carr 1989). They can also increase food tions, it is thought that there is intense competition for supply to associated organisms by altering water flow space on these hard substrates (Dayton 1971, Jackson *Email: [email protected] © Inter-Research 2008 · www.int-res.com 186 Mar Ecol Prog Ser 367: 185–192, 2008 1977). However, from April to August, the amount of In the present study, we documented the mobile and hard substrate available at certain locations increases sedentary invertebrate epifaunal community associ- as large aggregations of hundreds to thousands of ated with breeding aggregations of Hexaplex nigritus. black murex snails (Hexaplex nigritus = Muricanthus Specifically, we estimated epifaunal abundance and nigritus) gather on sandy bottoms some distance from species richness, and we assessed variation in species rocky reefs (Fig. 1). composition of epifauna on snails from aggregations at Hexaplex nigritus, a predatory snail and Gulf of Cali- different sites. We also evaluated factors that influ- fornia endemic, aggregates to breed; females lay egg enced abundance of epifauna on snails, including site, capsules on the shells of other conspecifics, and 1 snail number of egg capsules on the shell, and the time of can carry several hundred egg capsules on its shell year when snails were collected. Finally, we evaluated (Cudney-Bueno et al. in press). Aggregations vary in whether epifaunal organisms use black murex simply size and number of snails by location and over the because they provide benthic structure, and whether course of the aggregation. Snails are typically found on biological and behavioral characteristics associated the surface of the seafloor during warm-water months, with living snails, such as movement, influence com- and bury themselves into sediments during cold-water munity composition. To evaluate these hypotheses, we months (Cudney-Bueno et al. in press). They have well- constructed and anchored artificial reefs made of H. developed varices, which create ridges and spines nigritus shells. We then compared the epifaunal com- across the shell, giving it a complex shape. Although munity that developed on artificial reefs to epifaunal these snails are mobile, Olabarria (2000) found that communities of aggregations. If relatively similar epi- they function as habitat for a diverse mollusk epibiont faunal abundance and species composition developed community. When the snails aggregate, they increase on artificial reefs as on aggregations, then this would benthic habitat complexity over a large area and likely suggest that H. nigritus simply provides habitat het- influence local hydrodynamic processes, much like ses- erogeneity, and biological characteristics of live snails sile reef structures do (Lenihan 1999, Monismith 2007). do not influence epifaunal communities. Since the early 1990s, commercial divers have heavily harvested snails for their meat, shells, and opercula dur- ing aggregation periods (Cudney-Bueno 2000). Harvest- MATERIALS AND METHODS ing has resulted in the fishery’s rapid decline, prompting community-based resource management, including sea- Study sites. Breeding aggregations of black murex son closures and harvest refugia (Cudney-Bueno 2007). were sampled along the northeastern coast of the Gulf Loss of large snail aggregations has been documented of California from 4 subtidal sites: La Cholla, Sandy, Las (Cudney-Bueno et al. in press), and declines in black Conchas, and Los Tanques (Fig. 2). La Cholla’s benthic murex populations may result in the loss of a benthic topography has many flat rocky reefs (tepetates), with a substrate and a settlement substrate (Prescott et al. depth of 20 to 25 m. Sandy has rubble substrates with 2007). basalt and granite boulders near shore. Las Conchas and Los Tanques have isolated te- petates separated by fine grain sands. Sandy, Las Conchas, and Los Tanques range from 10 to 15 m in depth; how- ever, all sites vary in depth and currents because of extremely large tides (maxi- mum annual change in water height is 8 m; Thomson et al. 2000). The annual sea-surface temperatures range from <10°C to >32°C (Thomson et al. 2000). Aggregation measurements and col- lection of snails. We located and sam- pled 12 aggregations during May, June, and July of 2003 and 2004 with the assistance of commercial divers. We marked the center of each aggregation with PVC pipe and an underwater buoy. We measured the size of each ag- Fig. 1. Hexaplex nigritus. Beginning of an aggregation (individuals have egg gregation by recording 1 length mea- capsules on shells), depth of 10 m (photo by Doug Moon) surement and 2 width measurements, Prescott & Cudney-Bueno: Epifauna of black murex aggregations 187 also rinsed over sieves. We then care- fully examined the snails for organisms that were still present on shells by searching between egg capsules and on exposed surfaces of the shell. We preserved mobile epifauna from each snail (n = 295 snails; 1 sample = 1 snail) in individual jars containing 70% alco- hol. Epifauna were selected for identi- fication and abundance estimation by dividing the contents of a sample into 4 quadrants in a 10 cm diameter Petri dish, and randomly selecting all organ- isms within 1 quadrant. We then counted and identified epifauna in the subsample to the lowest taxonomic level possible, grouping morphologi- cally similar organisms. Counts of epi- fauna from subsamples were multi- plied by 4 to estimate a total count of organisms per snail. For 50 samples, we counted all organisms in the sam- ple, and compared these counts to our abundance estimates from subsam- Fig. 2. Northeastern coast of the Gulf of California with 4 sites where snail ples. All abundance estimates given in aggregations were sampled the results are based on subsample cal- culations. Voucher specimens of epi- as width varied considerably along the length of each fauna were placed in the University of Arizona’s Inver- aggregation. We then averaged the