Differential Algal Consumption by Three Species of <I>Fissurella</I

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Differential Algal Consumption by Three Species of <I>Fissurella</I BULLETIN OF MARINE SCIENCE. 46(3): 735-748.1990 DIFFERENTIAL ALGAL CONSUMPTION BY THREE SPECIES OF FISSURELLA(MOLLUSCA:GASTROPODA)AT ISLA DE MARGARITA, VENEZUELA Craig J. Franz ABSTRACT Visual observations and gut analyses were used to determine types of food ingested by Fissurella nimbosa (Linnaeus, 1758), F. nodosa (Born, 1778), and F. barbadensis (Gmelin, 1791) at Isla de Margarita, Venezuela. Although these animals have a wide variety of algal sources from which to select and on which they appear to feed in an opportunistic fashion, specific food preferences exist. Fissurella nodosa prefers encrusting microalgae and diatoms; F. nimbosa ingests laminar sheets of predominantly brown algae; F. barbadensis feeds on a wide variety of algae but often selects coralline algae of which it ingests entire branches. In zones of overlap, it is hypothesized that competition for food among Fissurella species is minimal due to resource allocation through food preference. Laboratory experiments indicate that all three congeners can ingest a greater variety of algal types than they normally consume in the field. Differential food consumption indicates significantly more elaborate niche par- titioning among tropical intertidal Fissure/la than was previously known. Studies of comparative feeding among congeneric predators may provide insight into the manner by which organisms partition their environment. This partitioning may be achieved through spatial segregation, temporal allocation, or dietary pref- erence. In situations of spatial overlap and temporal feeding similarity, a unique opportunity exists to evaluate the way in which food preferences may help establish an individual's niche. In these circumstances, dietary studies of co-occurring congeners provides information concerning the partitioning of community food resources. Many prosobranch groups utilize benthic algae as a food source (Fretter and Graham, 1962; Sutherland, 1970; Lubchenco, 1978; Underwood, 1980; Bosman and Hockey, 1988). Although competition and physical factors may regulate the vertical distribution of algae in the intertidal zone, grazing may be equally im- portant (Hawkins and Hartnoll, 1983). Most limpets are classified as generalist feeders which utilize available microflora and detritus (Graham, 1955; Purchon, 1968; Branch, 1981); nevertheless, some limpets eat macroa1gae (Eaton, 1968; Goss-Custard et al., 1979). Feeding preferences oflimpets may differ considerably, and these differences can exist even among congeners. For example, Lottia (=Ac- maea) limatula Carpenter, 1864 feeds mostly on the encrusting red and coralline algae Hildenbrandia, Peyssonellia, Lithophyllum and Lithothamnion (Eaton, 1968), whereas a sympatric congener, Lottia (=Acmaea) pelta Rathke, 1833, feeds on numerous macroscopic frond algae such as Rhodoglossum affine Harvey, Pelvetia !astigata J. Agardh and Egregia menziesii Turner (Craig, 1968). Only a few studies have included the feeding habits of species in the genus Fissurella Bruguiere, 1789; existing information for this group is incomplete and confusing. Kohn (1983) stated that fissurellids are mainly predators which graze on sessile invertebrates. However, Ward (1966) found that F. barbadensis in Barbados commonly ingests cyanobacteria [blue-green algae], including Lyngbya, Oscillatoria, Phormidium and Anacystis, and green algae such as Chlorochytrium, Ulothrix, Cladophora and Precursaria. Castilla (1981) reported that several species of Chilean Fissurella feed on benthic algae, but did not identify these algae. One 735 736 BULLETIN OF MARINE SCIENCE, VOL. 46, NO.3, 1990 Chilean species, F. pieta lata Sowerby, 1835, has been reported as feeding noc- turnally on Iridaea and Viva (Moreno and Jaramillo, 1983; Jara and Moreno, 1984; Moreno et aI., 1984), Bretos (1978) reported that the Chilean species, F. erassa Lamarck, 1822, feeds mainly on Viva and Enteromorpha, but Santelices and Correa (1985) found only trace amounts of Enteromorpha in the gut of that species. Nevertheless, they found 11 different species of macroalgae in the stom- achs of F. erassa, while its co-occurring cogener, F. limbata Sowerby, 1835, consumed 17 different algal species. Although direct observation of an organism's feeding excursion is an excellent way to monitor food preferences, some animals may feed while concealed under protective coverings (e.g., chitons), along hazardous gradients (e.g., wave-impacted barnacles), during incommodious times (e.g., irregular noctural feeders) or in remote areas (e.g., burrowing bivalves). Several of these conditions complicate food preference studies in fissurellids. Under circumstances where direct moni- toring of feeding can be conducted only incompletely, gut analyses may be used to determine which foods are consumed. The growth and development of a marine community along a Caribbean in- tertidal zone is a dynamic process involving complicated and intricate interre- lations between herbivores and their algal prey, This paper reports on studies which illustrate important differences exhibited by three congeneric fissurellids, both in their natural feeding preferences and in ingestion of algal types outside their normal diet. METHODS Fissurella nodosa, F. nimbosa and F. barbadensis were collected intermittently from Manzanillo, Pampatar and Punta Angel at Isla de Margarita, Venezuela, between October 1986 and August 1987. These collection sites were located at the eastern and northern coasts of the island where considerable wave activity is present and where subtidal shelves are easily accessible (Fig. I). These sites additionally were selected because all three Fissurella species were abundantly present; this permitted intensive sampling without serious disruption of local populations. Visual observations of feeding behavior were conducted during both day and night. To determine food resource availability to the limpets, algal samples from the study sites were collected and identified. Voucher specimens for many of the algae have been deposited in the mac- roalgae collection in the Estacion de Investigaciones Marinas de Margarita (EDIMAR) at Punta de Piedras, Isla de Margarita. Algae were considered to be within the feeding range of any given limpet if they were not more than 0.5 m from that limpet. Loose macroalgae that washed into the sites were not included in this survey. When recording the type of food consumed by each species, Fissurella were collected along their full tidal range and, when possible, large and small animals of each sex were included. Because Fissurella feed at different times (Franz, 1988), collections were made during the feeding periods of each species and dissections were performed immediately. Approximately 50 samples of each species were collected for gut analysis. The animals were placed dorsal side down on dissection trays and examinations were performed as follows: the foot was removed by a ventral incision beginning at the left edge of the nuchal cavity, continuing marginally around the semicircular shell muscle, and terminating at the right nuchal cavity edge. Upon removal of the foot, an incision in the intestinal wall was initiated at the junction of the intestine and the stomach; the dissection continued longitudinally along the central axis of the stomach extending anteriorly to the esophageal opening. The gut contents were extracted by pipette (and sometimes forceps) and were placed on microscope slides for subsequent identification under compound and dissecting microscopes. Identifiable algal pieces were permanently mounted on microscope slides with Keiser's solution (50 ml distilled H20, 50 ml glycerine, 8 gm gelatin, 0.02 mg phenol). In the laboratory at EDIMAR, the limpets were exposed to a variety of different algae to determine whether they would eat algae which exists outside their normal feeding range and/or algae which was not found in gut samples but occurred within their feeding range. To test feeding capabilities, each of the three limpet species from the Pampatar site were placed in containers with a single species of algae. Twelve limpets of each species were used for each alga presented. Animals were collected during early morning and subsequently were inspected for collection-related injury to the foot or mantle; FRANZ: ALGAL CONSUMPTION BY FISSURELLA 737 ... 'i i' ISLA DE MARGARITA v' I -GULF OF MEXICO 2" •••0 12' 75' 72' ... ..' ... eo' Figure 1. Map of the Caribbean region, showing the location ofIsla de Margarita, Venezuela. Inset: Map of Isla de Margarita showing the collection stations at Punta Angel (I), Pampatar (2) and Man- zanillo (3). damaged animals were eliminated from the experiment. Each species was separated into three sub- merged 10 cm' 20 cm· 30 cm plastic boxes into which had been placed ad libitum rations of algae which abundantly covered the bottom of the box. This technique was based on observations by Vadas (1985) who reported that ad libitum amounts of algae permit maximum feeding rates to be achieved for most macroalgae grazers. The open-grid construction of the boxes allowed ample water flow but prohibited algal and limpet exit. The animals were removed after 24 h, and dissections were performed immediately. The gut contents were examined using the method described above. All experiments were conducted at ambient temperatures in aquaria with fresh seawater. The water was exchanged midway through the experiment. Due to their well-fitted sculpture and strong adhesion to a home scar, it was difficult in some cases to remove the limpets
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