BULLETIN OF MARINE SCIENCE, 58(1): 1-8, 1996 PREY SELECTION BY THE SOUTH AFRICAN CAPE ROCK LOBSTER JASUS LALANDI/: ECOLOGICAL AND PHYSIOLOGICAL APPROACHES A. Barkai, C. L. Davis and S. Tugwell ABSTRACT Certain aspects of the foraging behavior of the Cape Rock Lobster, Jasus lalandii, were investigated to determine whether this animal selects prey or merely feeds randomly on a variety of prey items in proportion to their abundance. We also investigated the lobsters' ability to digest unusual food items, e.g., sponges and seaweeds, which are sometimes found in large quantities in their gut. The study combined field observations with analyses of gut contents and digestive enzyme activity. The results suggest that Jasus lalandii is primarily a carnivore with limited ability to digest plant tissue. Preferred foods are black and ribbed mussels (Charamytilus meridianalis and Aulacamya ater correspondingly), and a large variety of marine arthropods; activities of protease and chitinase are strong. Seaweeds are probably only incidentally caught by lobsters. They are only sporadically found in lobster guts. More- over, neither laminarinase nor alginase activity, which is essential for the digestion of plant tissue, was detected. It is possible, however, that Jasus lalandii extracts some starches from marine plants as amylase activity in their gut is strong. The most significant finding of this study is the ability of lobsters to feed on and digest sponges. This is evidenced by large quantities of sponge in certain lobster guts and strong activity of the protease gelatinase (which breaks down the sponge collagen skeleton). The Cape Rock Lobster, Jasus lalandii (Milne Edwards), is an important sub- tidal predator along the west coast of South Africa (Heydorn, 1969; Newman and Pollock, 1974; Pollock, 1979, 1982, 1986; Barkai and Branch, 1988a, 1988b, 1988c; Barkai and McQuaid, 1988). These animals substantially modify subtidal benthic communities and, when present in large numbers, may eliminate most of their benthic prey (Barkai and Branch, 1988c). Barkai and Branch (1988b) found that dense populations of rock lobsters can sustain high growth rates at high densities even when the standing stock of conventionally recognised prey species falls below the minimal energy requirements of the lobsters. In their study of a high-density population of lobsters near Malgas Island, Saldanha Bay (Fig. I), Barkai and Branch (I 988b ) noted that during the summer lobsters often scratched the substrata. They ascertained that the energetic requirements of the lobsters were met by the consumption of newly settled species such as barnacles and mussels. During the winter, when recruitment of prey was low, the rate of cannibalism among lobsters was high and their selection of prey centered on unorthodox spe- cies such as the mysid Mysidopsis schultzei. Barkai and Branch (1988b) concluded that the Cape Rock Lobster is an opportunistic predator and scavenger. The guts of the Cape Rock Lobster often contain fragments of sponge and sea weed, and it is unclear whether these items are selectively or incidentally con- sumed (Heydorn, 1969; Newman and Pollock, 1974; Pollock et aI., 1982; Barkai and Branch, 1988b). It is also unknown whether lobsters are capable of digesting and assimilating sponge and plant tissue. These questions are of great ecophysi- ological interest since both sponges and seaweed are often very abundant in lob- ster grounds and might constitute another important, yet unrecognised, source of energy for lobsters. Two methods were selected to address these questions. The first method utilised an analytical approach to potential food items, based on the "availability versus 2 BULLETIN OF MARINE SCIENCE. VOL. 58. NO. I. 1996 Durban t South Africa N Port Elizabeth Cape Agulhas Figure I. Map of the sampling areas and the sampling sites in each area (site numbers in parentheses as presented in Table 2). usage" analysis developed by Johnson (1980). The second method tested the activity of various digestive enzymes in the digestive fluids of the rock lobsters. The enzymes selected for this analysis (Table 1) were those necessary for the break-down of the component polymers characteristic of various potential lobster prey (i.e., chitin, starch, laminarin, alginates and proteins). Table 1. List of five digestive enzymes for which the digestive fluid of the rock lobster Jasus lalandii was tested. Column 2 lists the different types of substrates that were used in the assays, expressed as weight of substrate per volume (WN) of phosphate buffer (PB). The third column lists the equivalent end products which were used to draw up the standard curve. The last column provides the method used for the analysis, with the literature source in parentheses. Enzyme Substrate (WN in PB) Standard curve Method (References) Chitinase Approx. 20 mg·ml-I N-acetyl glucosamine (Monreal and Reese, 1969) chitin* Amylase 1.0% starch Glucose Nelson Somogyi (Nelson, 1952) Laminarinase 0.1 % laminarin Glucose Nelson Somogyi (Nelson, 1952) Alginase 0.4% alginate Malon-dialdehyde Thiobarbituric acid (Jacober et aI., 1980) Protease a) 0.5% azocaseint Azocasein spectrophotometric (Long et aI., 1981) b) I% gelatine:!: Gelatine plate I 0.2% agar (Cowan and Steel, 1970) *' Chitin slurry was prepared from powdered crab shell as described by Reichenbach and Dworkin (t 981). t Awcasein substrate made up in O.2M Tris-HCI. pH 7.8. :I:Agar plate assay involves monitoring zones of activity around wells cut in agar filled with "enzyme", BARKA! ET AL.: ROCK LOBSTER PREY SELECTION 3 MATERIALS AND METHODS Sampling of the Benthos.- Twenty-eight sites along the South African and Namibian west coasts (Fig. 1) were sampled to obtain comparative data on the standing stocks of potential benthic prey and the gut contents of the lobsters. Sites were selected according to their accessibility to divers operating from the shore. In most cases, there was no prior knowledge of the composition of the benthos. Benthic species abundance was estimated as mean percent coverage from six 50 cm X 50 cm quadrats. Replication of samples was achieved by the haphazard positioning of quadrats on the sea floor after "blind diving" for not less than 30 sec between each of the replicates. Kelp abundance was assessed by estimating the percent coverage of holdfasts in each quadrat using a 50 cm X 50 cm three-sided quadrat. Rock lobster densities were estimated from six replicate belt-transects in which all animals within I m of a lO-m weighted rope were counted (20 m2 per replicate). Analysis of Gut Contents.-Samples of gut contents were taken from at least ]5 rock lobsters of similar size (90 mm to ]00 mm carapace length) that were caught at each of the 28 sites mentioned above. The proventriculus of each lobster was removed and the contents examincd microscopicaHy and identified to the level of species where possible. The relative abundance of each item was estimated from its contribution to the total volume of each gut (P, expressed as a percentage). This value was then multiplied by the estimated fullness of the gut (F, ranked from I to 10), summed for all guts, divided by the total relative value of all items from all the gut contents of the sample, and expressed as a percentage (IPiFilIPijFij)1100 (Shepherd, ]973). Comparison of Prey Availability Versus Usage.-The methods and computer program of Johnson (1980) were used to determine whether lobsters consume ("usage") their prey according to its relative abundance ("availability"), or whether they select prey items regardless of their relative abundance. To simplify the analysis, these methods were only applied to the seven most common benthic groups that were found in the lobster guts. These included the black mussel Choromytilus meridionalis, the ribbed mussel Aulacomya ater, barnacles (mostly Notomegabalanus algicola), the sea-urchins Pare- chinus angulosus, sponges, kelp and other seaweed. The availability of these groups were determined at each site and ranked according to their average percent coverage. The usage of these groups by rock lobsters was determined from gut contents and ranked according to the relative proportions present in the gut. Hotelling's T2 test (multivariate t-test; see Harris, 1985) was used to test whether the prey groups are consumed with equal intensity. Waller and Duncan's (1969) multiple comparisons test was then used to declare significant differences between preferences of the lobsters for the various prey groups. In this regard the term "preference" should be treated with caution since the lobsters were not free to choose from different, equally available, prey species. Therefore, in this study, we use the term "preferred food items" to refer to those species which on a relative scale occur in larger quantities in the lobster gut, compared to their proportional abundance in the benthos. Lobster Digestive Enzyme Activity.-Eight lobsters were caught at Oudekraal on the west coast of the Cape Peninsula in South Africa (Fig. I). Each animal was immediately transported to the laboratory and placed in an ice-cold sea water slush until all tactile response had ceased. The animals were then dissected and digestive fluid was collected in Pasteur pipettes from the hepatopancreatic caeca at a point immediately proximal to their junction with the gut. Extracts of several milliliters of fluid were obtained from each animal in this manner. Each extract was diluted in phosphate buffer (67 mM with ]50 mM NaCl, pH 6.8). All substrates were also dissolved in phosphate buffer of the same specifi- cations. Enzyme activity was determined by measuring the rate of end-product formation in spectro- photometric assays (Table I). Standard curves for the end-product of each of the enzymes, excluding protease, were performed. Protein concentration of the digestive fluids was determined using the Folin- Lowry method (Lowry et aI., ]951) with bovine serum albumin as a standard. The rate of enzyme activity for each of the enzymes was expressed as the amount of product formed per hour per milligram of protein present in the digestive fluids.