Herbivoria en Peces

Herbivory in Tropical Reef Fish

Herbivores are essential in maintaining ecosystem health, particularly in tropical reef systems. Coral reefs are facing many challenges (global warming, coral diseases and predation, etc.) that may upset the natural balance of these ecosystems. Therefore it is important for us to understand the dynamics of these systems, even down to the fundamental level of intestinal microbes and their role in digestion in herbivores. A thorough knowledge of these complex interactions may help us identify and control critical factors that threaten these ecosystems.

Herbivory on Coral Reefs

Algea on Reef

Herbivores are an important part of coral reef ecosystems. They help to maintain the balance between corals and macroalgae on reefs. Macroalgae are extraordinarily fast growers and are generally less sensitive to changes in environmental factors, such as temperature and sedimentation, than coral species. For these reasons macroalgae have the potential to out-compete corals. However, consumption of macroalgae by herbivores limits their density, thus maintaining a healthy competition between the two groups. Reefs that lack the appropriate number of herbivores suffer greatly due to an overgrowth of algae. One of the most well known cases of overgrowth occurred in the Caribbean after a previously unseen disease virtually killed off the herbivorous sea urchin Diadema antillarum [1].

Diadema antillarum

The mass decimation of this urchin caused an ecological collapse of Caribbean reefs, with macroalgae becoming dominant over coral species. This ecological shift has had a negative effect on the diversity and composition of Caribbean reef assemblages. This unfortunate event in the Caribbean demonstrates that herbivores and their ecological function are extremely important to the health of coral reefs around the globe.

On coral reefs, there are both invertebrate and vertebrate herbivores. Invertebrate herbivores include urchins (see above), crabs, limpets, chitons, and polychaete worms. Prominent vertebrate herbivores can be reef fishes, sea turtles, and dugongs [2].

Primary Producers- Algae on Coral Reefs

Phytoplankton

Coral reef ecosystems rely heavily on primary producers. Terrestrial primary producers are well known to us, they are green plants. Primary producers are often the ·first step· in the food chain; they take inorganic carbon from the atmosphere (carbon dioxide) and fix it into organic carbon molecules (carbohydrates), subsequently transporting it into the food web when the algae are consumed by herbivores.

In the marine environment, the most significant primary producers are large, plant-like macroalgae and microscopic phytoplankton. Both serve as food sources for a variety of marine organisms. Marine herbivores feed on different types of large, fleshy macroalgae (red, green, and brown), which are distinguished from each other by their different photosynthetic pigments. Planktivores or filter-feeders feed on free-floating phytoplankton.

Reef fishes are diverse and commonly have bright and attractive color patterns. This vibrancy makes them appealing objects of amusement and observation. Recently they have even become part of pop culture; we are now familiar with some of them as Nemo (Clownfish, Amphiprion species), Dory (blue tang/palette surgeonfish, Paracanthurus hepatus), Gill (Moorish Idol, Zanclidae species), etc.

Most reef fishes are of the large and diverse Order of bony fishes, the Perciformes, and are distributed in many of the suborders. Most notably, they are found in the Labroids, Blennoids, Gobioids, Percoids, and Acanthuroids. The table below lists some of the commonly recognized reef fishes.

Digestion in Herbivorous Reef Fishes

Pharyngeal teeth

Most algae (like terrestrial plants) have complex polysaccharide cell walls which must be broken down after consumption so the fish can access their nutrients. In herbivorous fishes this can be achieved by mechanical, chemical, or enzymatic means [3]. Mechanical breakdown of the cell wall can be performed using a pharyngeal mill or gizzard-like stomach, both of which grind and shred algal cells, an action that is analogous to our own chewing. Chemical digestion is attained using acid lysis of the cells in the stomach. Finally, enzymatic digestion of algal cells is most likely accomplished by microbial fermentation; enzymes produced by microorganisms inhabiting the gastrointestinal tract can breakdown the otherwise unusable polysaccharides and convert them to organic molecules that the fish can absorb and utilize.

The Role of Microbes in the Digestion in Reef Fishes

There is increasing evidence for the contribution of intestinal microbes (and their enzymes) to the digestion of algae in herbivorous reef fishes. Microbial fermentation has been detected using short-chain fatty acid (SCFA) analyses in the intestines of a variety of species of tropical herbivorous fishes, including many Epulopiscium-harboring Acanthurids [4],[5]. SCFAs are products of microbial fermentation and are thought to contribute to the nutrition of some herbivorous fishes. A more direct study of the intestinal microbiota of the herbivorous king angelfish (Family: Pomacanthidae) demonstrated that a variety of gut microorganisms could be cultured from angelfish intestinal contents, and some of these microbes were able to grow on components of algal cell walls (cellulose, agar, and alginic acid)[6]. The Angert lab's own work on the bacterial community in the gut of Naso tonganus (Bulbnose Unicornfish) has yielded gene sequences from bacteria that are closely related to Clostridium spp., Bacteroidetes, and Verrucomicrobia.

Acanthuridae

Naso literatus, Orangespine

Epulopiscium species are found in the gut of come Acanthuridae, a family of tropical reef fishes that include surgeonfishes/tangs (Acanthurinae), unicornfishes (Nasinae), and sawtails (Prionurinae). Most Acanthurids are common on reefs in the Indo-Pacific Ocean, though some are found in tropical and subtropical areas around the world. This Family is distinguished by spines on the caudal peduncle (the base of the tail fin), which are used for defense or during aggressive behavior.

Acanthurus lineatus, Lined Surgeonfish

Many Acanthurids are conspicuous herbivores on the reef. They are often seen traveling in schools or small groups, deftly grazing on the substrate. They are found in shallow water where they can target the algae that thrive on hard surfaces like rock and coral rubble. Most Acanthurid species are primarily herbivorous, feeding on reef macroalgae, though some are planktivores or detritivores [11].

Epulopiscium's Role

The prevalence of Epulopiscium species in herbivorous Acanthurid intestinal tracts suggests a role in digestion, though the exact nature of the symbiosis remains unknown. Epulopiscium's kinship with other bacterial species that are obligate intestinal inhabitants and/or active in fermentation supports the hypothesis that Epulopiscium species may contribute to the intestinal break down of food. Epulopiscium spp. are related to Clostridium species, which are intestinal inhabitants of a variety of organisms (including, but not limited to, humans [7], pigs [8], freshwater fishes [9], subtropical marine fishes [10], and chickens [11]). Many Clostridium spp. can breakdown complex polysaccharides and ferment sugars. Even some clostridia isolated from the human gut have the ability to break down laminaran, a component of brown algae [12]. Epulopiscium are also very closely related to Metabacterium polyspora, an intestinal symbiont of guinea pigs and other rodents [13].

Initial results from the whole-genome sequencing of Epulopiscium have substantiated the idea that they function in the breakdown of polysaccharides and fermentation of sugars in Acanthurid intestinal tracts. Further study of Epulopiscium and its genetic potential will hopefully elucidate the spirit of this particular fish-microbe interaction.

References

  1. Knowlton, N. 2001. Sea urchin recovery from mass mortality: New hope for Caribbean coral reefs? Proceedings of the National Academy of Sciences 98(9): 4822-48244
  2. Hay, M.E. 1997. The ecology and evolution of seaweed-herbivore interactions on coral reefs. Coral Reefs 16(Supp.1): S67-S76
  3. Choat, J.H. and K.D. Clements 1998. Vertebrate Herbivores in Marine and Terrestrial Environments: A Nutritional Ecology Perspective. Annual Review of Ecological Systems 29: 375-403
  4. Clements, K.D. and J.H. Choat. 1995. Fermentation in Tropical Marine Herbivorous Fishes. Physiological Zoology 68(3): 355-378
  5. Choat, J.H., K.D. Clements, and W.D. Robbins. 2002. The trophic status of herbivorous fishes on coral reefs: 1. Dietary Analyses. Marine Biology 140:613-623
  6. Martinez-Diaz, S.F. and H. Perez-Espana. 1999. Feasible mechanisms for algal digestion in the king angelfish. Journal of Fish Biology 55: 692-703
  7. Kuiter, Rudie H. and Helmut Debelius. 2001. Surgeonfishes, Rabbitfishes, and their Relatives: A comprehensive guide to Acanthuroidei. TMC Publishing: Chorleywood, UK. 18
  8. Lay, C., L. Rigottier-Gois, K. Holmstrøm, M. Rajilic, E. E. Vaughan, W. M. de Vos, M.D. Collins, R. Thiel, P. Namsolleck, M. Blaut, and J. Doré. 2005. Colonic microbiota signatures across five northern European countries. Applied and Environmental Microbiology 71(7): 4153-4155
  9. Reid, C.A., K. Hillman, C. Henderson, and H. Glass. 1996. Fermentation of native and processed starches by the porcine caecal anaerobe Clostridium butyricum. Journal of Applied Bacteriology 80(2): 191-198
  10. Sugita, H., J. Kawasaki, and Y. Deguchi. 1997. Production of amylase by the intestinal microflora in cultured freshwater fish. Letters in Applied Microbiology 24(2):105-108
  11. Moran, D., S.J. Turner and K.D. Clements. 2005. Ontogenetic development of the gastrointestinal microbiota in the marine herbivorous fish Kyphosus sydneyanus. Microbial Ecology 49(4): 590-597
  12. Amit-Romach, E., D. Sklan, and Z. Uni. 2004. Microflora ecology of the chicken intestine using 16S ribosomal DNA primers. Poultry Science 83(7): 1093-1098
  13. Fujii, T., T. Kuda, K. Saheki, and M. Okuzumi. 1992. Fermentation of water-soluble polysaccharides of brown-algae by human intestinal bacteria invitro. Nippon Suison Gakkaishi 58 (1): 147-152

Pictures

Further Useful References and Links

  • Clements, K.D. 1997. Fermentation and gastrointestinal microorganisms in fishes. In: Gastrointestinal microbiology. Vol. 1: Gastrointestinal ecosystems and fermentations (eds. R.I. Mackie and B.A. White). Chapman and Hall, New York, pp. 156-198
  • Crossman, D.J., J.H. Choat, and K.D. Clements. 2005. Nutritional ecology of nominally herbivorous fishes on coral reefs. Marine Ecology Progress Series 296: 129-142
  • Kendall Clements· Research Group
  • Moran, D., S.J. Turner, and K.D. Clements. 2005. Ontogenetic development of the gastrointestinal microbiota in the marine herbivorous fish Kyphosus sydneyanus. Microbial Ecology 49(4): 590-597
  • Sale, P. (ed.) 1991. The ecology of fishes on coral reefs. Academic Press, San Diego.
  • Kuiter, Rudie H. and Helmut Debelius. 2001. Surgeonfishes, Rabbitfishes, and their Relatives: A comprehensive guide to Acanthuroidei. TMC Publishing: Chorleywood, UK. 18
  • Angert, E.R., A.E. Brooks, and N.R. Pace. 1996. Phylogenetic analysis of Metabacterium polyspora: clues to the evolutionary origin of the daughter cell production in Epulopiscium species, the largest bacteria. Journal of Bacteriology 178(5): 1451-1456