Algae as food for fishes: a nutritional ecology perspective

Abstract

This thesis examines marine macroalgae (seaweed) as a food source for herbivorous fishes. This is carried out using a nutritional ecology perspective, which focuses on a) details of algal composition, and b) the digestive physiology of the fishes. While this approach has been advocated in the literature, it has received little attention, with much of the current understanding of plant-herbivore interactions in the marine environment being based on the deterrent properties of the algae. This thesis has three main parts. In the first I examine the theory that herbivorous fishes utilise low pH gastric conditions to lyse algal cells thus gaining access to intracellular algal nutrients (acid lysis). Despite limited supporting evidence, acid lysis is widely cited as a digestive mechanism utilised by herbivorous fishes. To examine acid lysis I: a) determined the gastric pH of eight species of marine herbivorous fishes from north-eastern New Zealand, b) treated algae in low pH conditions and measured the ability of digestive enzymes to enter the algal cells, c) utilised Transmission Electron Microscopy (TEM) to determine any large scale structural effects of low pH treatment, and d) examined the effects of low pH treatment on the porosity of algal cell walls. The gastric pH in the fishes ranged from 1.9 - 3.5. At the pH level found in the fish stomachs, seven of the ten algae examined were lysed to an extent that enabled amylolytic enzymes to enter the cells. The results from the remaining three algal species were equivocal, not eliminating the possibility of acid lysis in these algae. The upper limit of pH at which algae were susceptible to acid lysis was lower than found in previous studies. TEM of the acid treated algae showed that low pH treatment lysed the plasma membrane. In untreated algae, the cell-wall pore diameter in Enteromorpha intestinalis, Ulva rigida and Polysiphonia strictissima was less than 8.8 nm, and in Porphyra sp. was less than 7.1 nm. The low pH treatment increased the porosity of the cell walls in all four of these algae to at least 13.5 nm after 20 mins at pH 2.0, and after 60 minutes at either pH 2.5 or pH 3.0. This increase in algal cell-wall porosity would allow molecules similar in size to proteases and α-amylases to pass through the cell walls in under 5 minutes. Thus, the main effects upon algae of the low pH conditions present in the stomach of herbivorous fishes are to a) lyse the cell membrane, and b) increase the porosity of the cell walls. Acid lysis is therefore likely to be an important factor in the digestion of intracellular algal nutrients for any fish that have acidic gastric pH. In the second part of this thesis I assess two ways that algal starches might impact on the diet choices of herbivorous fishes. I first measured seasonal variation in algal starch content and then investigated interspecific differences in starch digestibility. I drew three main conclusions from this study. (1) There were significant seasonal variations in starch content and algae varied in their nutritional value relative to each other on a seasonal basis because of interspecific variation in the pattern of seasonality, e.g. from April to August Ulva rigida had a higher starch content than Caulerpa flexilis, but this pattern was reversed during the rest of the year. (2) There was significant interspecific variation in the susceptibility of algal starches to enzymatic digestion, and these differences could help structure diet choices in marine herbivorous fishes. (3) When determining algal nutritional value one cannot simply measure either total soluble carbohydrates or total storage polysaccharides. Both measures fail to account for differences in the digestibility of storage carbohydrates. In the third part of this thesis I examine the correlation between peak afternoon feeding by herbivorous fishes and diel variation in algal nutritional quality. This involved measuring both algal nutritional components and the ability of the fish to utilise those components. My results demonstrated that a) herbivorous fish can utilise floridoside, the primary photosynthate of many rhodophytes, and b) algae are of higher nutritional value to marine herbivorous fishes in the afternoon than in the morning. These results support the hypothesis that higher fish feeding rates in the afternoons may be viewed as an optimal foraging strategy. In each of the three main parts of this thesis a nutritional ecology perspective is successfully employed, synthesising investigations of both algal components and the digestive physiology of the fishes to further elucidate plant-herbivore interactions in the marine environment.