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Food habits of the farmer damselfish Stegastes nigricans inferred by stomach content, stable isotope, and fatty acid composition analyses

Abstract

The territorial damselfish, Stegastes nigricans, maintains algal farms by excluding invading herbivores and weeding unpalatable algae from its territories. In Okinawa, Japan, S. nigricans farms are exclusively dominated by Polysiphonia sp., a highly digestible filamentous rhodophyte. This study was aimed at determining the diet of S. nigricans in Okinawa and its dependency on these almost-monoculture algal farms based on stomach content and chemical analyses. Stomach content analyses revealed that all available food items in the algal farms (i.e., algae, benthic animal inhabitants, trapped detritus) were contained in fish stomachs, but amorphous organic matter accounted for 68% of the contents. Therefore, carbon and nitrogen stable isotope ratios and fatty acid (FA) compositions were analyzed to trace items actually assimilated in their bodies. Stable isotope analyses showed that benthic animals were an important food source even for this farmer fish. Two essential fatty acids (EFAs), 20:4n6 and 20:5n3, which are produced only by rhodophytes among available food items, were rich in the muscle tissue of S. nigricans as well as in algal mats and detritus, suggesting that algal mats contribute EFAs to S. nigricans directly and indirectly through the food web. In conclusion, S. nigricans ingested algal mats, detritus, and benthic animals maintained within its farm. Algae and detritus were original sources of EFAs, and benthic animals, which were much more abundant in the farms than in outside territories, provided a nitrogen-rich dietary source for the fish.

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References

  1. Adams T, Sterner R (2000) The effect of dietary nitrogen content on trophic level 15N enrichment. Limnol Oceanogr 45:601–607

  2. Barnes C, Sweeting CJ, Jennings S, Barry JT, Pollunin NVC (2007) Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Funct Ecol 21:356–362

  3. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

  4. Branch GM, Harris JM, Parkins C, Bustamante RH, Eekhout S (1992) Algal ‘gardening’ by grazers: a comparison of the ecological effects of territorial fish and limpets. In: John DM, Hawkins SJ, Price JH (eds) Plant–animal interactions in the marine benthos. Clarendon Press, Oxford, pp 405–423

  5. Cabana G, Rasmussen JB (1994) Modelling food chain structure and contaminant bioaccumulation using stable isotopes. Nature 372:255–257

  6. Ceccarelli DM, Jones GP, McCook LJ (2001) Territorial damselfishes as determinants of the structure of benthic communities on coral reefs. Oceanogr Mar Biol Annu Rev 39:355–389

  7. Chakrabarti I, Gani MA, Chaki KK, Sur R, Misra KK (1995) Digestive enzymes in 11 freshwater teleost fish species in relation to food habit and niche segregation. Comp Biochem Physiol A 112:167–177

  8. Clements KD, Raubenheimer D, Choat JH (2009) Nutritional ecology of marine herbivorous fishes: ten years on. Funct Ecol 23:79–92

  9. Cleveland A, Montgomery WL (2003) Gut characteristics and assimilation efficiencies in two species of herbivorous damselfishes (Pomamcentridae: Stegastes dorsopunicans and S. planifrons). Mar Biol 142:35–44

  10. Coull BC (1999) Role of meiofauna in estuarine soft-bottom habitats. Aust J Ecol 24:327–343

  11. Crossman D, Choat J, Clements K (2005) Nutritional ecology of nominally herbivorous fishes on coral reefs. Mar Ecol Prog Ser 296:129–142

  12. Dalsgaard J, John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340

  13. Feller RJ, Taghon GL, Gallagher ED, Kenny GE, Jumars PA (1979) Immunological methods for food web analysis in a soft-bottom benthic community. Mar Biol 54:61–74

  14. Hata H, Kato M (2002) Weeding by the herbivorous damselfish Stegastes nigricans in nearly monocultural algae farms. Mar Ecol Prog Ser 237:227–231

  15. Hata H, Kato M (2003) Demise of monocultural algal-farms by exclusion of territorial damselfish. Mar Ecol Prog Ser 263:159–167

  16. Hata H, Kato M (2004) Monoculture and mixed-species algal farms on a coral reef are maintained through intensive and extensive management by damselfishes. J Exp Mar Biol Ecol 313:285–296

  17. Hata H, Kato M (2006) A novel obligate cultivation mutualism between damselfish and Polysiphonia algae. Biol Lett 2:593–596

  18. Hata H, Nishihira M (2002) Territorial damselfish enhances multi-species co-existence of foraminifera mediated by biotic habitat structuring. J Exp Mar Biol Ecol 270:215–240

  19. Hata H, Watanabe K, Kato M (2010) Geographic variation in the damselfish-red alga cultivation mutualism in the Indo-West Pacific. BMC Evol Biol 10:185

  20. Hiatt RW, Strasburg DW (1960) Ecological relationships of the fish fauna on coral reefs of the Marshall Islands. Ecol Monogr 30:65–127

  21. Hoey A, Bellwood D (2010) Damselfish territories as a refuge for macroalgae on coral reefs. Coral Reefs 29:107–118

  22. Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol Annu Rev 27:167–272

  23. Jones GP, Santana L, McCook LJ, McCormick MI (2006) Resource use and impact of three herbivorous damselfishes on coral reef communities. Mar Ecol Prog Ser 328:215–224

  24. Karino K, Nakazono A (1993) Reproductive behavior of the territorial herbivore Stegastes nigricans (Pisces: Pomacentridae) in relation to colony formation. J Ethol 11:99–110

  25. Khotimchenko SV, Vaskovsky VE (1990) Distribution of C20 polyenoic fatty acids in red macrophytic algae. Bot Mar 33:525–528

  26. Khotimchenko SV, Vaskovsky VE, Titlyanova TV (2002) Fatty acids of marine algae from the Pacific coast of North California. Bot Mar 45:17–22

  27. Kuo SR, Shao KT (1991) Feeding habits of damselfishes (Pomacentridae) from the southern part of Taiwan. J Fish Soc Taiwan 18:165–176

  28. Letourneur Y, Galzin R, Harmelin-Vivien M (1997) Temporal variations in the diet of the damselfish Stegastes nigricans (Lacepède) on a Réunion fringing reef. J Exp Mar Biol Ecol 217:1–18

  29. Lison de Loma T, Ballesteros E (2002) Microspatial variability inside epilithic algal communities within territories of the damselfish Stegastes nigricans at La Reunion (Indian Ocean). Bot Mar 45:316–323

  30. Lobel PS (1980) Herbivory by damselfishes and their role in coral reef community ecology. Bull Mar Sci 30:273–289

  31. Mattson WJ Jr (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161

  32. Menzel DW (1959) Utilization of algae for growth by the angelfish, Holacanthus bermudensis. ICES J Mar Sci 24:308–313

  33. Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine and aquatic food webs. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental science. Blackwell, Oxford, pp 138–157

  34. Mill AC, Pinnegar JK, Polunin NVC (2007) Explaining isotope trophic-step fractionation: why herbivorous fish are different. Funct Ecol 21:1137–1145

  35. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140

  36. Montgomery WL, Gerking SD (1980) Marine macroalgae as foods for fishes: an evaluation of potential food quality. Environ Biol Fish 5:143–153

  37. Munro C (2005) Diving systems. In: Eleftheriou A, Mclntyre A (eds) Methods for the study of marine benthos. Blackwell, Oxford, pp 112–159

  38. Napolitano GE, Pollero RJ, Gayoso AM, Macdonald BA, Thompson RJ (1997) Fatty acids as trophic markers of phytoplankton blooms in the Bahia Blanca estuary (Buenos Aires, Argentina) and in Trinity Bay (Newfoundland, Canada). Biochem Syst Ecol 25:739-755

  39. Pecquerie L, Nisbet RM, Fablet R, Lorrain A, Kooijman SALM (2010) The impact of metabolism on stable isotope dynamics: a theoretical framework. Phil Trans R Soc B 365:3455–3468

  40. Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125

  41. Raubenheimer D, Zemke-White WL, Phillips RJ, Clements KD (2005) Algal macronutrients and food selection by the omnivorous marine fish Girella tricuspidata. Ecology 86:2601–2610

  42. Robertson DR, Polunin NVC (1981) Coexistence: symbiotic sharing of feeding territories and algal food by some coral reef fishes from the Western Indian ocean. Mar Biol 62:185–195

  43. Saliot A, Laureillard J, Scribe P, Sicre MA (1991) Evolutionary trends in the lipid biomarker approach for investigating the biogeochemistry of organic matter in the marine environment. Mar Chem 36:233–248

  44. Sano M, Shimizu M, Nose Y (1984) Food habits of teleostean reef fishes in Okinawa Island, southern Japan. University of Tokyo Press, Tokyo

  45. Sargent JR, Parkes RJ, Mueller-Harvey I, Henderson RJ (1987) Lipid biomarkers in marine ecology. In: Sleigh MA (ed) Microbes in the sea. Ellis Horwood, West Sussex, pp 119–138

  46. Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199

  47. Shansudin L, Yusof M, Azis A, Shukri Y (1997) The potential of certain indigenous copepod species as live food for commercial fish larval rearing. Aquaculture 151:351–356

  48. Southgate PC, Kavanagh K (1999) The effect of dietary n-3 highly unsaturated fatty acids on growth, survival and biochemical composition of the coral reef damselfish Acanthochromis polyacanthus. Aquat Living Resour 12:31–36

  49. Sweeting CJ, Barry JT, Polunin NVC, Jennings S (2007) Effects of body size and environment on diet-tissue δ13C fractionation in fishes. J Exp Mar Biol Ecol 352:165–176

  50. Toledo JD, Golez MS, Doi M, Ohno A (1999) Use of copepod nauplii during early feeding stage of grouper Epinephelus coioides. Fish Sci 65:390–397

  51. Tsuchiya M, Nadaoka K, Kayanne H, Yamano H (eds) (2004) Coral reefs of Japan. Ministry of the Environment, Tokyo

  52. Umezawa Y, Miyajima T, Yamamuro M, Kayanne H, Koike I (2002) Fine-scale mapping of land-derived nitrogen in coral reefs by δ15N in macroalgae. Limnol Oceanogr 47:1405–1416

  53. Umezawa Y, Miyajima T, Tanaka Y, Koike I, Hayashibara T (2007) Variation in internal δ15N and δ13C distribution in the brown macroalgae Padina australis growing in subtropical oligotrophic waters. J Phycol 43:437–448

  54. Umezawa Y, Komatsu T, Yamamuro M, Koike I (2009) Physical and topographic factors affecting suspended particulate matter composition in a shallow tropical estuary. Mar Environ Res 68:59–70

  55. Vaskovsky VE, Khotimchenko SV, Xia B, Hefang L (1996) Polar lipids and fatty acids of some marine macrophytes from the Yellow Sea. Phytochemistry 42:1347–1356

  56. Watanabe T, Kitajima C, Fujita S (1983) Nutritional values of live organisms used in Japan for mass propagation of fish: a review. Aquaculture 34:115–143

  57. Wilson S (2002) Nutritional value of detritus and algae in blenny territories on the Great Barrier Reef. J Exp Mar Biol Ecol 271:155–169

  58. Wilson S, Bellwood DR (1997) Cryptic dietary components of territorial damselfishes (Pomacentridae, Labroidei). Mar Ecol Prog Ser 153:299–310

  59. Wilson SK, Burns K, Codi S (2001) Sources of dietary lipids in the coral reef blenny Salarias patzneri. Mar Ecol Prog Ser 222:291–296

  60. Wilson SK, Bellwood DR, Choat JH, Furnas MJ (2003) Detritus in the epilithic algal matrix and its use by coral reef fishes. Oceanogr Mar Biol Annu Rev 41:279–309

  61. Zeller DC (1988) Short-term effects of territoriality of a tropical damselfish and experimental exclusion of large fishes on invertebrates in algal turfs. Mar Ecol Prog Ser 44:85–93

  62. Zemke-White WL, Clements KD, Harris PJ (1999) Acid lysis of macroalgae by marine herbivorous fishes: myth or digestive mechanism? J Exp Mar Biol Ecol 233:95–113

  63. Zemke-White WL, Clements KD, Harris PJ (2000) Acid lysis of macroalgae by marine herbivorous fishes: effects of acid pH on cell wall porosity. J Exp Mar Biol Ecol 245:57–68

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Acknowledgments

The authors deeply appreciate two anonymous reviewers to improve this manuscript much. We are grateful to International Coral Reef Research and Monitoring Center, and WWF Japan Coral Reef Conservation and Research Center in Ishigaki Island. We also thank P.L. Mfilinge (the Ryukyu University), Y. Yamada (Kitazato University), K. Suetsugu and T. Miyajima (University of the Tokyo), K. Fukuoka (Seikai National Fisheries Research Institute), T. Miller and J. Shibata (Ehime University) for helping analyses, identification, stimulating discussions on the data, and preparing manuscript. This study is supported by JSPS (Japan Society for the Promotion of Science) Research Fellowship for Young Scientist.

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Correspondence to Hiroki Hata.

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Hata, H., Umezawa, Y. Food habits of the farmer damselfish Stegastes nigricans inferred by stomach content, stable isotope, and fatty acid composition analyses. Ecol Res 26, 809–818 (2011). https://doi.org/10.1007/s11284-011-0840-5

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Keywords

  • Coral reef
  • Fatty acid composition
  • Herbivory
  • Stable isotope analysis
  • Stomach contents