Oecologia

, Volume 148, Issue 2, pp 334–341 | Cite as

Stable isotope analysis of production and trophic relationships in a tropical marine hard-bottom community

Community Ecology

Abstract

Seagrasses produce much of the organic carbon in the shallow waters of the Caribbean and it has long been assumed that a substantial portion of this carbon is exported to nearby habitats, contributing substantially to their food webs. In the shallow coastal waters of the Florida Keys (USA), seagrass intersperses with hard-bottom habitat where bushy, red macroalgae are the most prominent primary producers. However, the relative importance of seagrass-derived carbon versus autochthonous algal production or phytoplankton in supporting higher trophic levels within hard-bottom communities has never been investigated. We compared the carbon and nitrogen isotopic values of potential primary producers and representative higher trophic level taxa from hard-bottom sites on the bay-side and ocean-side of the Florida Keys. We also included in our study a set of bay-side sites that experienced significant ecological disturbances over the past decade (e.g., cyanobacteria blooms, seagrass die-off, and sponge die-offs) that may have altered trophic relationships in those regions. We did not detect any differences among regions in the trophic status of hard-bottom taxa that might be associated with ecosystem disturbance. However, our results suggest that autochthonous production of algal detritus is an important source of secondary production in these hard-bottom communities, with seagrass and phytoplankton contributing smaller fractions.

Keywords

Benthic community Laurencia Macroalgae Seagrass Trophic structure 

References

  1. Andree SW (1981) Locomotory activity patterns and food items of benthic postlarval spiny lobsters, Panulirus argus. M.S. thesis, Florida State University, TallahasseeGoogle Scholar
  2. Baerlocher F, Newell SY (1994) Phenolics and proteins affecting palatability of Spartina leaves to the gastropod Littoraria irrorata. Mar Ecol 15:65–75CrossRefGoogle Scholar
  3. Bosely KL, Wainright SC (1999) Effects of preservatives and acidification on the stable isotope ratios (15N:14N, 13C:12C) of two species of marine animals. Can J Fish Aquat Sci 56:2181–2185CrossRefGoogle Scholar
  4. Boyer JN, Fourqurean JW, Jones RD (1997) Spatial characteristics of water quality in Florida Bay and Whitewater Bay by multivariate analyses: zones of similar influence. Estuaries 20:743–758CrossRefGoogle Scholar
  5. Butler IV MJ, Hunt JH, Herrnkind WF, Childress MJ, Bertelsen R, Sharp W, Matthews T, Field JM, Marshall HG (1995) Cascading disturbances in Florida Bay, USA: implications for juvenile spiny lobsters Panulirus argus. Mar Ecol Prog Ser 129:119–125CrossRefGoogle Scholar
  6. Butler IV MJ, Herrnkind WF, Hunt JH (1997) Factors affecting the recruitment of juvenile Caribbean spiny lobsters dwelling in macroalgae. Bull Mar Sci 61:3–19Google Scholar
  7. Butler IV MJ, Herrnkind WF (2000) Puerulus and juvenile ecology. In: Phillips BF, Cobb JS, Kittaka J (eds) Spiny lobster management, 2nd edn. Blackwell, Oxford, pp 276–301Google Scholar
  8. Chiappone M, Sullivan KM (1994a) Ecological structure and dynamics of nearshore hard-bottom communties in the Florida Keys. Bull Mar Sci 54:747–756Google Scholar
  9. Chiappone M, Sullivan KM (1994b) Patterns of coral abundance defining nearshore hard-bottom communities of the Florida Keys. Fla Sci 57:108–125Google Scholar
  10. Chiappone M (1996) Marine benthic communities of the Florida Keys. In: Site characterization for the Florida Keys National Marine Sanctuary and environs. Farley Court, ZendaGoogle Scholar
  11. Corredor JE, Wilkinson CR, Vincente VP, Morell JM, Otero E (1988) Nitrate release by Caribbean reef sponges. Limnol Oceanogr 33:114–120CrossRefGoogle Scholar
  12. Cox C, Hunt JH, Lyons WG, Davis GE (1997) Nocturnal foraging of the Caribbean spiny lobster (Panulirus argus) on offshore reefs of Florida, USA. Mar Freshwat Res 48:671–679CrossRefGoogle Scholar
  13. Croley FC, Dawes CJ (1970) Ecology of the algae of a Florida Key. I. A preliminary checklist, zonation, and seasonality. Bull Mar Sci 20:165–185Google Scholar
  14. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  15. Eggleston DB, Lipcius RN, Grover JJ (1997) Predator and shelter-size effects on coral reef fish and spiny lobster prey. Mar Ecol Prog Ser 149:43–59CrossRefGoogle Scholar
  16. Ehleringer JR, Rundel PW (1989) 1. Stable isotopes: history, units, and instrumentation. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Ecological studies volume 68: stable isotopes in ecological research. Springer, Berlin Heidelberg New York, pp 3–15Google Scholar
  17. Erickson KL (1983) Constituents of Laurencia. In: Scheuer (ed) Marine natural products: chemical and biological perspectives, vol 5. Academic, New York, pp 131–257Google Scholar
  18. Fenical W (1975) Halogenation in the rhodophyta: a review. J Phycol 11:245–259Google Scholar
  19. Field JM, Butler IV MJ (1994) The influence of temperature, salinity, and postlarval transport on the distribution of juvenile spiny lobsters, Panulirus argus (Latreille, 1804), in Florida Bay. Crustaceana 67:26–45CrossRefGoogle Scholar
  20. Fourqurean JW, Zieman JC, Powell GVN (1992) Phosphorus limitation of primary production in Florida Bay: evidence from C:N:P ratios of the dominant seagrass Thalassia testudinum. Limnol Oceanogr 37:162–171CrossRefGoogle Scholar
  21. Fourqurean JW, Robblee MB (1999) Florida Bay: a history of recent ecological changes. Estuaries 22:345–357CrossRefGoogle Scholar
  22. Fry B (1984) 13C/12C ratios and the trophic importance of algae in Florida Syringodium filiforme seagrass meadows. Mar Biol 79:11–19CrossRefGoogle Scholar
  23. Fry B, Joern A, Parker PL (1978) Grasshopper food web analysis: use of carbon isotope ratios to examine feeding relationships among terrestrial herbivores. Ecology 59:498–506CrossRefGoogle Scholar
  24. Fry B, Lutes R, Northam M, Parker PL, Ogden J (1982) A 13C/12C comparison of food webs in Caribbean seagrass meadows and coral reefs. Aquat Bot 14:389–398CrossRefGoogle Scholar
  25. Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13–47Google Scholar
  26. Fry B, Virnstein RW (1988) Leaf production and export of the seagrass Syringodium filiforme Kuetz in Indian River Lagoon, Florida. Aquat Bot 30:261–266CrossRefGoogle Scholar
  27. Granado I, Caballero P (2001) Feeding rates of Littorina striata and Osilinus atratus in relation to nutritional quality and chemical defenses of seaweeds. Mar Biol 138:1213–1224CrossRefGoogle Scholar
  28. Hanisak MD (1992) The importance of macroalgae to the queen conch, Strombus gigas. J Phycol 28:12Google Scholar
  29. Harrigan P, Zieman JC, Macko SA (1989) The base of nutritional support for the gray snapper (Lutjanus griseus): an evaluation based on a combined stomach content and stable isotope analysis. Bull Mar Sci 44:65–77Google Scholar
  30. Hay ME, Fenical W, Gustafson K (1987) Chemical defense against diverse coral-reef herbivores. Ecology 68:1581–1591CrossRefGoogle Scholar
  31. Hemminga MA, Mateo MA (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298CrossRefGoogle Scholar
  32. Herrnkind WF, Butler IV MJ, Tankersley RA (1988) The effects of siltation on recruitment of spiny lobsters, Panulirus argus. Fish Bull 86:331–338Google Scholar
  33. Herrnkind WF, Butler IV MJ, Hunt J, Childress M (1997) The role of physical refugia: implications from a mass sponge die-off in a lobster nursery. Mar Freshwat Res 48:759–769CrossRefGoogle Scholar
  34. Herrnkind WF, Vanderwalker J, Barr L (1975) Population dynamics, ecology and behaviour of spiny lobster, Panulirus argus of St. John, U.S. Virgin Islands: habitation and pattern of movements. Sci Bull Nat Hist Mus Los Angelos Cty 20:31–45Google Scholar
  35. Holm RF (1978) The community structure of a tropical marine lagoon. Estuar Coast Shelf Sci 7:329–345Google Scholar
  36. Isaksson I, Pihl L, Van Montfrans J (1994) Eutrophication-related changes in macrovegetation and foraging of young cod (Gadus morhua L.): a mesocosm experiment. J Exp Mar Biol Ecol 177:203–217CrossRefGoogle Scholar
  37. Josselyn MN (1977) Seasonal changes in the distribution and growth of Laurencia poitei (Rhodophyceae, Ceramiales) in a subtropical lagoon. Aquat Bot 3:217–229CrossRefGoogle Scholar
  38. Kelly S (2001) Temporal variation in the movement of the spiny lobster, Jasus edwardsii. Mar Freshwat Res 52:323–331CrossRefGoogle Scholar
  39. Kharlamenko VI, Kiyashko SI, Imbs AB, Vyshkvartzev DI (2001) Identification of food sources of invertebrates from the seagrass Zostera marina community using carbon and sulphur stable isotope ratios and fatty acid analysis. Mar Ecol Prog Ser 220:103–117CrossRefGoogle Scholar
  40. Kitting CL, Fry B, Morgan MD (1984) Detection of inconspicious epiphytic algae supporting food webs in seagrass meadows. Oecologia 62:145–149CrossRefGoogle Scholar
  41. Kwak TJ, Zedler JB (1997) Food web analysis of southern California coastal wetlands using multiple stable isotopes. Oecologia 110:262–277CrossRefGoogle Scholar
  42. Lajtha K, Michener RH (1994) Stable isotopes in ecology. Blackwell, OxfordGoogle Scholar
  43. LaPointe BE, Tomasko DA, Matzie WR (1994) Eutrophication and trophic state classification of seagrass communities in the Florida Keys. Bull Mar Sci 54:696–717Google Scholar
  44. Lapointe BE, Barile PJ, Yentsch CS, Littler MM, Littler DS, Kakuk B (2004) The relative importance of nutrient enrichment and herbivory on macroalgal communities near Norman’s Pond Cay, Exumas Cays, Bahamas: a “natural” enrichment experiment. J Exp Mar Biol Ecol 298:275–301CrossRefGoogle Scholar
  45. Lepoint G, Nyssen F, Gobert S, Dauby P, Bouquegneau JM (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Mar Biol 136:513–518CrossRefGoogle Scholar
  46. Loneragan NR, Bunn SE, Kellaway DM (1997) Are mangroves and seagrasses sources of organic carbon for penaeid prawns in a tropical Australian estuary? A multiple stable-isotope study. Mar Biol 130:289–300CrossRefGoogle Scholar
  47. MacDiarmid AB, Hickey B, Maller RA (1991) Daily movement patterns of the spiny lobster Jasus edwardsii (Hutton) on a shallow reef in northern New Zealand. J Exp Mar Biol Ecol 147:185–205CrossRefGoogle Scholar
  48. Marguillier S, van der Velde G, Dehairs F, Hemminga MA, Rajagopal S (1997) Trophic relationships in an interlinked mangrove-seagrass ecosystem as traced by δ13C and δ15N. Mar Ecol Prog Ser 151:115–121CrossRefGoogle Scholar
  49. Marx J, Herrnkind W (1985b) Factors regulating microhabitat use by young juvenile spiny lobsters, Panulirus argus: food and shelter. J Crust Biol 5:650–657CrossRefGoogle Scholar
  50. Mathieson AC, Dawes CJ (1975) Seasonal studies of Florida sublittoral marine algae. Bull Mar Sci 25:46–65Google Scholar
  51. McClelland JW, Valiela I (1998) Changes in food web structure under the influence of increased anthropogenic nitrogen inputs to estuaries. Mar Ecol Prog Ser 168:259–271CrossRefGoogle Scholar
  52. Michener RH, Schnell DM (1994) Stable isotope ratios as tracers in marine aquatic food webs. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology. Blackwell, Oxford, pp 138–157Google Scholar
  53. Minagawa M, Wada R (1984) Stepwise enrichment of δ15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim 48:1135–1140CrossRefGoogle Scholar
  54. Moncreiff CA, Sullivan MJ (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stabe isotope analysis. Mar Ecol Prog Ser 215:93–106CrossRefGoogle Scholar
  55. Opresko DM (1973) Abundance and distribution of shallow-water gorgonians in the area of Miami, Florida. Bull Mar Sci 23:535–557Google Scholar
  56. Osinga R, Belarbia EH, Grima EM, Trampera J, Wijffels RH (2003) Progress towards a controlled culture of the marine sponge Pseudosuberites andrewsi in a bioreactor. J Biotechnol 100: 141–146CrossRefPubMedGoogle Scholar
  57. Page HM (1997) Importance of vascular plant and algal production to macro-invertebrate consumers in a southern California marsh. Estuar Coast Shelf Sci 45:823–834CrossRefGoogle Scholar
  58. Paterson AW, Whitfield AK (1997) A stable carbon isotope study of the food-web in a freshwater-deprived South African estuary, with particular emphasis on the ichthyofauna. Estuar Coast Shelf Sci 45:705–715CrossRefGoogle Scholar
  59. Paul VJ, Hay ME (1986) Seaweed susceptibility to herbivory: chemical and morphological correlates. Mar Ecol Prog Ser 33:255–264CrossRefGoogle Scholar
  60. Petelle M, Haines B, Haines E (1979) Insect food preferences analyzed using 13C/12C ratios. Oecologia 38:159–166CrossRefGoogle Scholar
  61. Peterson BJ, Howarth RW, Garritt RH (1986) Sulphur and carbon isotopes as tracers of salt-marsh organic matter flow. Ecology 67:865–874CrossRefGoogle Scholar
  62. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  63. Peterson BJ, Fourqurean JW (2001) Large-scale patterns in seagrass (Thalassia testudinum) demographics in south Florida. Limnol Oceanogr 46:1077–1090CrossRefGoogle Scholar
  64. Phillips DL (2001) Mixing models in analysis of diet using multiple stable isotopes: a critique. Oecologia 127:166–170CrossRefGoogle Scholar
  65. Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269CrossRefPubMedGoogle Scholar
  66. Reiswig HM (1971a) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591CrossRefGoogle Scholar
  67. Ribes R, Coma R, Gili JM (1999) Natural diet and grazing rate of the temperate sponge Dysidea avara (Demospongiae, Dendroceratida) throughout an annual cycle. Mar Ecol Prog Ser 176:179–190CrossRefGoogle Scholar
  68. Robblee MB, Barber TR, Carlson Jr PR, Durako MJ, Fourqurean JW, Muehlstein LK, Porter D, Yarbro LA, Zieman RT, Zieman JC (1991) Mass mortality of the tropical seagrass Thalassia testudinum in Florida Bay (USA). Mar Ecol Prog Ser 71:297–299CrossRefGoogle Scholar
  69. Rogers CN, de Nys R, Steinberg PD (2002) Effects of algal diet on the performance and susceptibility to predation of the sea hare Aplysia parvula. Mar Ecol Prog Ser 236:241–254CrossRefGoogle Scholar
  70. Stachowicz JJ, Hay ME (1996) Facultative mutualism between a herbivorous crab and a coralline alga: advantages of eating noxious seaweeds. Oecologia 105:377–387CrossRefGoogle Scholar
  71. Street GT, Montagna PA, Parker PL (1997) Incorporation of brown tide into an estuarine food web. Mar Ecol Prog Ser 152:67–78CrossRefGoogle Scholar
  72. Suren AM, Lake PS (1989) Edibility of fresh and decomposing macrophytes to three species of freshwater invertebrate herbivores. Hydrobiologia 178:165–178CrossRefGoogle Scholar
  73. Thayer GW, Parker PL, LaCroix MW, Fry B (1978) The stable isotope ratio of some components of an eelgrass, Zostera marina, bed. Oecologia 35:1–12CrossRefGoogle Scholar
  74. Vizzini S, Sarà G, Michener RH, Mazzola A (2002) The role and contribution of the seagrass Posidonia oceanica (L.) Delile organic matter for secondary consumers as revealed by carbon and nitrogen isotope analysis. Acta Oecol 23:277–285CrossRefGoogle Scholar
  75. Wada E, Mizutani H, Minagawa M (1991) The use of stable isotopes for food web analysis. Crit Rev Food Sci Nutr 30:361–371PubMedCrossRefGoogle Scholar
  76. Wilkinson CR (1984) Immunological evidence for the Precambrian origin of bacterial symbiosis in marine sponges. Proc R Soc Lond B 220:509–517CrossRefGoogle Scholar
  77. Yamamuro M (1999) Importance of epiphytic cyanobacteria as food sources for heterotrophs in a tropical seagrass bed. Coral Reefs 18:263–271CrossRefGoogle Scholar
  78. Zieman JC, Thayer GW, Robblee MB, Zieman RT (1979) Production and export of seagrasses from a tropical bay. In: Livingston RJ (ed) Ecological processes in coastal and marine systems. Plenium, New York, pp 21–33Google Scholar
  79. Zieman JC, Fourqurean JW, Robblee M, Durako M, Carlson P, Porter D, Zieman R, Muhlstein L, Powell G (1988) A catastrophic die-off of seagrasses in Florida Bay and Everglades National Park. Trans Am Geophy Union 69:1111Google Scholar
  80. Zieman JC, Fourqurean JW, Iverson RL (1989) Distribution, abundance, and productivity of seagrasses and macroalgae in Florida Bay. Bull Mar Sci 44:292–311Google Scholar
  81. Zieman JC, Fourqurean JW, Frankovich TA (1999) Seagrass dieoff in Florida Bay: long term trends in abundance and productivity of turtlegrass, Thalassia testudinum. Estuaries 22:460–470CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Biological SciencesOld Dominion UniversityNorfolkUSA

Personalised recommendations