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Diet, Food Preference, and Algal Availability for Fishes and Crabs on Intertidal Reef Communities in Southern California

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Diet, Food Preference, and Algal Availability for Fishes and Crabs on Intertidal Reef Communities in Southern California Environmental Biology of Fishes 37: 75-95,1993. 0 1993 Kluwer Academic Publishers. Printed in the Netherlands. Diet, food preference, and algal availability for fishes and crabs on intertidal reef communities in southern California James P. Barry’ & Michael J. Ehret* A-001 Scripps Institution of Oceanography, La Jolla, CA 92093, U.S.A. ‘Present address: Monterey Bay Aquarium Research Institute, 160 Central Ave., Pacific Grove, CA 93950, U.S.A. 2 Present address: Biology Department, Old Dominion University, Norfolk, VA 23507, U.S. A. Received 18.9.1991 Accepted 3.9.1992 Key words: Herbivory, Kyphosidae, Girella, Hermosilla, Pachygrapsus, Community structure, Foraging, Chemical ecology Synopsis Herbivory by wide-ranging fishes is common over tropical reefs, but rare in temperate latitudes where the effects of herbivorous fishes are thought to be minimal. Along the west coast of North America, herbivory by fishes on nearshore reefs is largely restricted to a few members of the Kyphosidae, distributed south of Pt. Conception. This paper presents information on natural diets and results from feeding choice experiments for two abundant kyphosids from intertidal habitats in San Diego, California - Girella nigricans and Hermosilla azurea, and similar data for the lined shore crab, Pachygrapsus crassipes, which also forages over intertidal reefs. These results are compared with the availability of algae in intertidal habitats measured during summer and winter, on both disturbed and undisturbed habitats. The diets of juveniles of G. nigricans and H. azurea collected from nearshore habitats were dominated by animal prey (mainly amphipods), but adults of these fishes, and P. crassipes, consumed algae nearly exclusively, with 26,10, and 14 taxa of algae identified from G. nigricans, H. azurea, and P. crassipes, respectively. Algae with sheet-like morphologies (e.g. Ulva sp., Enteromorpha sp., members of the Delesseriaceae) were the principal algae in the diets of the fishes, and calcareous algae (e.g. Corallina sp., Lithothrix aspergillum) and sheet-like algae (Enteromorpha sp.) comprised the greatest identifiable portion of the shore crab’s diet. Feeding choice experiments indicated that the fishes preferred filamentous algae (e.g. Centroceras clavulatum, Polysiphonia sp., Chon- dria californica) and sheet-like algae (e.g. Enteromorpha sp., Ulva sp., Cryptopleura crispa) over other algal morphologies, whereas the shore crab chose jointed calcareous algae (e.g. Lithothrix aspergillum, Corallina vancouveriensis, Jania sp.) most frequently. The diets and preferences for algae by the fishes were generally most similar to the assemblage of algae available in early successional (disturbed) habitats during summer when sheet-like and filamentous algae are abundant. The shore crab exhibited the opposite trend with a diet more similar to late successional (undisturbed) habitats. Introduction Ogden & Lobe1 1978, Gaines & Lubchenco 1982, Carpenter 1986, Horn 1989) herbivory by highly Compared to tropical reefs where grazing by fishes mobile fishes and decapods is apparently ineffec- limits the distribution of algae (Randall 1961,1965, tive in controlling the distribution of algae on in- 76 tertidal and shallow subtidal reefs in temperate (Mediulunu culiforniensis, Scorpidinae) potentially latitudes. The presence of extensive turfs of macro- affect algal communities on shallow reefs. Girellu algae in low intertidal and shallow subtidal zones, nigricuns recruit to intertidal pools as small juve- low diversity and abundance of highly mobile herb- niles, and move to subtidal nearshore habitats as ivores, and assumed indigestibility of algae by tem- adults (Norris 1963, Feder et al. 1974). Hermosillu perate fishes has led to the consensus that herb- azureu are also abundant in intertidal pools as juve- ivory by fishes does not control the structure of niles (Barry personal observation) and are restrict- algal communities in shallow marine habitats of ed to shallow inshore waters (Feder et al. 1974). temperate latitudes. However, the effects of herb- Both species, and to a lesser extent Mediulunu ivory by fishes and decapod crustaceans on the culiforniensis, forage in monospecific or mixed structure of algal communities, as well as diet, di- schools over the intertidal reefs (DeMartini 1981, gestive physiology, and feeding preference for vari- Barry 1988, personal observation). ous macroalgae, have received little attention and Detailed studies of diets and prey preferences of are poorly documented in temperate latitudes these herbivores in southern California should in- (Dayton 1975, Horn 1989, but see Sousa 1979). dicate the potential for control of algal community The diverse families of herbivorous and omnivo- structure by herbivory. Kyphosids are omnivorous, rous fishes that forage actively in groups over trop- with varying degrees of herbivory (Quast 1968, ical reefs (e.g. Acanthuridae, Siganidae, Sparidae, Feder et al. 1974, Bray & Ebeling 1975, Hobson & Kyphosidae; Hiatt & Strasburg 1960, Randall Chess 1976, Laur & Ebeling 1983). However, even 1967) are largely absent in temperate latitudes though algae were the dominant component of where wide ranging herbivorous fishes are rela- some species’ diets, Quast (1968) and others tively rare (Horn 1989). In contrast to the effects of (Mitchell 1953, Burge & Schultz 1973, Wheeler fishes in tropical latitudes, echinoderms and mol- 1980) assumed that algae were consumed inciden- lusts have been implicated as the major herbivores tally and were unimportant, relative to animal prey in temperate habitats (Gaines & Lubchenco 1982, due to the apparent lack of cellulolytic enzymes or Schiel & Foster 1986, see review by Horn 1989). gut symbionts for cellulose digestion (Stickney & North of Pt. Conception along the western coast of Shumway 1974). More recent studies have shown North America the most abundant herbivorous that two members of the Kyphosidae in the south- fishes belonging to the reclusive Stichaeidae (Esch- ern hemisphere (Kyphosus cornelii and K. syd- meyer et al. 1983) and the majority of roving fishes neyunus) are capable of fermentive digestion of are carnivores and omnivores (e.g. Embiotocidae) marine algae (Rimmer & Wiebe 1987). A third that forage over beds of macroalgal turf and con- kyphosid from Australia Gireflu tricuspidutu, is sume mainly small crustaceans and polychaetes known to assimilate radioactive carbon from 14C (Quast 1968, Bray & Ebeling 1975, Hobson & labelled protoplasts and cell walls of the green alga, Chess 1976, Laur & Ebeling 1983). The southern Enteromorphu sp. (Anderson 1987). Owing to its California bight, however, includes a transitional taxonomic affinity and similar feeding modes, G. fish fauna derived from both tropical and temper- nigricuns is likely to have similar physiological ca- ate zones (Eschmeyer et al. 1983), and it is here pabilities. that the effects of herbivory by fishes on the struc- Several species of crabs also occur in intertidal ture of temperate algal communities should be evi- and shallow subtidal habitats of California. The dent. lined shore crab, Puchygrupsus crussipes, has im- This transition zone includes three predomin- portant effects on the structure of high intertidal antly herbivorous species of fish from three sub- communities (Robles & Cubit 1981, Robles 1982, families of the Kyphosidae (Eschmeyer 1990). Be- Shanks & Wright 1986) and potentially affects cause they are common in inshore habitats, zebra- lower zones as well. The shore crab is common perch (Hermosiflu aturea, Kyphosinae) , opaleye throughout temperate latitudes of the north Pacific (Girella nigricans, Girellinae) , and halfmoon and is most abundant near refuge crevices from the 77 middle to upper intertidal (Morris et al. 1980). It is inant species on rocky substrata. This assemblage largely herbivorous (Bovbjerg 1946, Hiatt 1948, of epilithic algae, and particularly members of the Sousa 1979), but will also take animal prey when Corallinaceae, provide a substratum (anchor spe- available. cies, sensu Stewart 1982) occupied by several com- Preferences for particular species of macroalgae mon epiphytic species of seasonal or perennial al- are little known for temperate herbivores, but are gae. Ulva sp., Enteromorpha sp., Binghamia for- important in identifying the effects of herbivory on kii, and other rapidly recruiting species are com- the structure of the algal communities. Opaleye are mon on newly created bare space, particularly thought to graze preferentially the red alga, Gigur- during spring and summer. The surfgrasses, Phyl- tina canaliculata, in subtidal kelp beds near Santa lospadix sp. are conspicuously dominant in the low- Barbara, California, such that cover of G. canalic- er intertidal, but are restricted from shallower por- ulata increases within fish exclusion cages (Foster tions of intertidal reefs by desiccation (Stewart 1975). Pachygrapsus crassipes has been shown to 1988,1989, Barry 1988, unpublished data). Anchor consume the chlorophyte, Ulva, preferentially species and epiphytes also are damaged by des- over several other species of red and brown algae, iccation events when dry desert winds and warm and to increase the rate of succession in the algal temperatures coincide with extreme low tides that community on intertidal boulders (Sousa 1979). occur during afternoon hours from fall to spring In this paper, we describe diets of two, dominant (Emerson & Zedler 1978, Littler 1980, Gunnill herbivorous fishes (G. nigricuns and Hermosillu 1985,
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