Detritus as food for sediment-grazing fishes on coral reefs

Abstract

Sediment-grazing fishes from the families Acanthuridae (surgeonfishes) and Scaridae (parrotfishes) are abundant on coral reefs and are generally thought to receive nutrition from the digestion and assimilation of turf algae. However, recent publications have suggested that these fishes do not target algae per se but feed principally on protein-rich detritus associated with the algae. Therefore the primary aim of this thesis was to examine the contribution of detritus to the nutrition of these fishes. There were three main components to this work: (l) to determine which methodologies of protein measurement are most appropriate for samples derived from algae; (2) to assess the nutritional value of detritus and algae from turf or epilithic algal communities (EAC) on coral reefs upon which sediment grazing fishes feed; and (3) to investigate the trophic status of sediment-grazing fishes through a nutritional comparison with algivorous, omnivorous and planktivorous coral reef fishes. The first aspect of this study involved comparing different techniques for the estimation of protein in algal derived samples. Gut fluid from the temperate marine herbivorous fish Kyphosus sydneyanus was chosen as a model system. There were two components to this work: (l) to compare the ability of spectrophotometric methods to estimate protein in gut fluid; and (2) to determine the effect of freezing on the extraction of gut fluid from the digesta samples for the measurement of total protein amino acids (TAA). The Bradford, Lowry, deoxycholate/trichloroacetic acid (DOC/TCA) Lowry and the bicinchoninic acid (BCA) spectrophotometric protein assays were compared for their ability to estimate protein in gut fluid, and were validated with protein determined by quantitative amino acid analysis using an automated procedure. The spectrophotometric assays all gave differing estimates of protein content and none correlated well with quantitative amino acid analysis. The Lowry and BCA methods gave similar estimates of protein, which were higher than those measured in the same samples by amino acid analysis. Both the DOC/TCA Lowry and the Bradford assay substantially underestimated protein in pooled gut fluid. These results indicated the unreliability of spectrophotometric protein assays in samples containing algal compounds. Two methods of extracting gut fluid were compared: (l) method A, which involved removing the gut fluid from the digesta immediately post capture; and (2) method B, in which samples of digesta were frozen and gut fluid removed later. The fluid from method B gave significantly higher levels of TAA in some gut segments. Freeze-thawing of digesta in method B was thought to be the basis of the increased TAA. This finding suggests that method A more accurately reflects in vivo gut fluid conditions and thus provides the better methodology to compare the ability of fish species at extracting TAA from dietary material. The above results highlight that the estimation of protein can be affected by methodology and by sample composition, and shows that methods must be optimized for a particular application. Algal turf assemblages of the northern Great Barrier Reef, Australia, were sampled to determine the nutritional value of detritus and algae as food sources for sediment-grazing fishes. Samples were collected with a suction apparatus across an exposure gradient from (l) the reef crest at highly exposed outer barrier reefs, (2) the reef crest of moderately exposed mid-shelf reefs, and (3) the reef slope of sheltered mid-shelf reefs. The biomass of algae and detritus decreased from sheltered mid-shelf reefs to moderately exposed mid-shelf reefs to highly exposed outer barrier reefs. This decrease was significant only for detritus (P < 0.005). Wave energies were calculated across the exposure gradient with the wave model, WAMGBR. Detrital mass was inversely correlated with predicted wave energies and fitted a polynomial relationship (P < 0.001) that explained 52.8 % of the variation. A similar relationship was also found between algal mass and wave energy (P < 0.001), but this only explained 30.0 %o of the variation. The nutritional value of samples in protein amino acids and starch was assessed. The amino acid composition of detritus and algae was similar and not considered nutritionally different. However, the concentration of TAA was significantly (P< 0.001) higher in detritus (21.2 ± 2.0 mg g-1) than in algae (11.8 ± 1.0 mg g-1).Starch content was significantly (P<0.05) higher in algae (7.7 ± 0.9 mg g-1) than in detritus (6.0 ± 1.0 mg g-1). These results demonstrate that detritus is a potentially valuable food source to sediment-grazing fishes on coral reefs. The trophic status of sediment-grazing fishes was examined through a nutritional comparison with algivorous, omnivorous and planktivorous coral reef fishes from the families Acanthuridae (surgeonfishes), Kyphosidae (drummers) and Scaridae (parrotfishes). This involved, (l) calculating the assimilation efficiencies for TAA, carbohydrate and lipid, and (2) measuring the TAA in gut fluid along the intestinal tract in study fishes. Assimilation efficiencies were determined by measuring the nutrients in stomach contents and feces and using ash as an indigestible marker to determine amount of nutrients assimilated. Samples for the above analysis were obtained from fish speared in the vicinity of Lizard Island, Great Barrier Reef, Australia. To examine which macronutrients were important to the different trophic groups assimilation data were expressed as the proportion each nutrient made up of the summed nutrient assimilation. For most species the proportions of TAA, carbohydrate and lipid that were assimilated were similar to the proportions of these nutrients in the diet. The carnivorous acanthurid Naso hexacanthus assimilated a high proportion of TAA (0.73), a moderate proportion of lipid (0.23) and a low proportion of carbohydrate (0.05). The omnivorous acanthurids Naso tonganus and Naso vlamingii assimilated moderate proportions of TAA (0.44-0.5) and carbohydrate (0.44-0.-5), and a lower proportion of lipid (0.17-0.22). The algivorous species Kyphosus cinerascens, Kyphosus vaigiensis and Naso unicornis assimilated a low proportion of TAA (0.14-0.19) and lipid (0.08-0.15), but a high proportion of carbohydrate (0.65-0.77) while the algivorous fish Acanthurus lineatus assimilated a moderate proportion of TAA (0.43) and carbohydrate (0.42), and a low proportion of lipid (0.15). The sediment-grazing scarids Chlorurus microrhinos, Scarus frenatus and S. schlegeli assimilated a high proportion of amino acids (0.59-0.68), a low proportion of carbohydrate (0.05-0.1l) and moderate proportion of lipid (0.24-0.3) and were distinct from algivores examined. The gut segment with the highest or peak TAA concentrations in the gut fluid followed a similar trend across species as the assimilation proportions for TAA. The carnivorous species Acanthurus mata and N. hexacanthus had a high peak concentration of TAA (27.3-28.9 mg ml-1), which was in contrast to the low peak concentration of TAA (4.4- 12.5 mg ml-1) of the algivorous species K. cinerascens, K. vaigiensis and N. unicornis. The omnivores N. tonganus and N. vlamingii had intermediate peak concentrations of TAA (12.8 -19.6 mg ml-l), and the herbivorous fish A. lineatus had moderately high peak TAA (25.1 mg ml-l). The sediment-grazing fishes which included the searids C. microrhinos, S, frenatus and S. schlegeli and the acanthurids Acanthurus olivaceus and Ctenochaetus striatus had the highest peak TAA concentrations in gut fluid (29.3 – 51.6 mg ml-1). These results suggest that sediment-grazing fishes digest and assimilate dietary material high in TAA and low in carbohydrate. In contrast, most algivorous fishes examined assimilated a high proportion of carbohydrate and low proportion of TAA. The above results indicate that there are major differences in the food resources targeted by sediment-grazing and algivorous fishes on coral reefs. Algivorous fishes appear to consume and assimilate dietary material high in carbohydrate, which is consistent with a diet of algae. However, sediment-grazing fishes digest and assimilate dietary material high in TAA and low in carbohydrate that is not consistent with a diet of algae. This supports the hypothesis that sediment-grazing fishes do not feed on turf algae but target protein-rich detritus.