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

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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.

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References

  • Andree SW (1981) Locomotory activity patterns and food items of benthic postlarval spiny lobsters, Panulirus argus. M.S. thesis, Florida State University, Tallahassee

  • Baerlocher F, Newell SY (1994) Phenolics and proteins affecting palatability of Spartina leaves to the gastropod Littoraria irrorata. Mar Ecol 15:65–75

    Article  Google Scholar 

  • 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 56:2181–2185

    Article  Google Scholar 

  • 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 20:743–758

    Article  CAS  Google Scholar 

  • 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 129:119–125

    Article  Google Scholar 

  • Butler IV MJ, Herrnkind WF, Hunt JH (1997) Factors affecting the recruitment of juvenile Caribbean spiny lobsters dwelling in macroalgae. Bull Mar Sci 61:3–19

    Google Scholar 

  • 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 276–301

    Google Scholar 

  • Chiappone M, Sullivan KM (1994a) Ecological structure and dynamics of nearshore hard-bottom communties in the Florida Keys. Bull Mar Sci 54:747–756

    Google Scholar 

  • Chiappone M, Sullivan KM (1994b) Patterns of coral abundance defining nearshore hard-bottom communities of the Florida Keys. Fla Sci 57:108–125

    Google Scholar 

  • Chiappone M (1996) Marine benthic communities of the Florida Keys. In: Site characterization for the Florida Keys National Marine Sanctuary and environs. Farley Court, Zenda

  • Corredor JE, Wilkinson CR, Vincente VP, Morell JM, Otero E (1988) Nitrate release by Caribbean reef sponges. Limnol Oceanogr 33:114–120

    Article  CAS  Google Scholar 

  • 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 48:671–679

    Article  Google Scholar 

  • Croley FC, Dawes CJ (1970) Ecology of the algae of a Florida Key. I. A preliminary checklist, zonation, and seasonality. Bull Mar Sci 20:165–185

    Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • Eggleston DB, Lipcius RN, Grover JJ (1997) Predator and shelter-size effects on coral reef fish and spiny lobster prey. Mar Ecol Prog Ser 149:43–59

    Article  Google Scholar 

  • 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 3–15

    Google Scholar 

  • Erickson KL (1983) Constituents of Laurencia. In: Scheuer (ed) Marine natural products: chemical and biological perspectives, vol 5. Academic, New York, pp 131–257

  • Fenical W (1975) Halogenation in the rhodophyta: a review. J Phycol 11:245–259

    CAS  Google Scholar 

  • 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 67:26–45

    Article  Google Scholar 

  • 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 37:162–171

    Article  CAS  Google Scholar 

  • Fourqurean JW, Robblee MB (1999) Florida Bay: a history of recent ecological changes. Estuaries 22:345–357

    Article  CAS  Google Scholar 

  • Fry B (1984) 13C/12C ratios and the trophic importance of algae in Florida Syringodium filiforme seagrass meadows. Mar Biol 79:11–19

    Article  CAS  Google Scholar 

  • Fry B, Joern A, Parker PL (1978) Grasshopper food web analysis: use of carbon isotope ratios to examine feeding relationships among terrestrial herbivores. Ecology 59:498–506

    Article  Google Scholar 

  • 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 14:389–398

    Article  Google Scholar 

  • Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13–47

    CAS  Google Scholar 

  • Fry B, Virnstein RW (1988) Leaf production and export of the seagrass Syringodium filiforme Kuetz in Indian River Lagoon, Florida. Aquat Bot 30:261–266

    Article  Google Scholar 

  • 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 138:1213–1224

    Article  Google Scholar 

  • Hanisak MD (1992) The importance of macroalgae to the queen conch, Strombus gigas. J Phycol 28:12

    Google Scholar 

  • 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 44:65–77

    Google Scholar 

  • Hay ME, Fenical W, Gustafson K (1987) Chemical defense against diverse coral-reef herbivores. Ecology 68:1581–1591

    Article  CAS  Google Scholar 

  • Hemminga MA, Mateo MA (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298

    Article  Google Scholar 

  • Herrnkind WF, Butler IV MJ, Tankersley RA (1988) The effects of siltation on recruitment of spiny lobsters, Panulirus argus. Fish Bull 86:331–338

    Google Scholar 

  • 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 48:759–769

    Article  Google Scholar 

  • 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 20:31–45

    Google Scholar 

  • Holm RF (1978) The community structure of a tropical marine lagoon. Estuar Coast Shelf Sci 7:329–345

    Google Scholar 

  • 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 177:203–217

    Article  Google Scholar 

  • Josselyn MN (1977) Seasonal changes in the distribution and growth of Laurencia poitei (Rhodophyceae, Ceramiales) in a subtropical lagoon. Aquat Bot 3:217–229

    Article  Google Scholar 

  • Kelly S (2001) Temporal variation in the movement of the spiny lobster, Jasus edwardsii. Mar Freshwat Res 52:323–331

    Article  Google Scholar 

  • 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 220:103–117

    Article  CAS  Google Scholar 

  • Kitting CL, Fry B, Morgan MD (1984) Detection of inconspicious epiphytic algae supporting food webs in seagrass meadows. Oecologia 62:145–149

    Article  Google Scholar 

  • Kwak TJ, Zedler JB (1997) Food web analysis of southern California coastal wetlands using multiple stable isotopes. Oecologia 110:262–277

    Article  Google Scholar 

  • Lajtha K, Michener RH (1994) Stable isotopes in ecology. Blackwell, Oxford

    Google Scholar 

  • LaPointe BE, Tomasko DA, Matzie WR (1994) Eutrophication and trophic state classification of seagrass communities in the Florida Keys. Bull Mar Sci 54:696–717

    Google Scholar 

  • 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 298:275–301

    Article  Google Scholar 

  • 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 136:513–518

    Article  CAS  Google Scholar 

  • 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 130:289–300

    Article  Google Scholar 

  • 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 147:185–205

    Article  Google Scholar 

  • 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 151:115–121

    Article  CAS  Google Scholar 

  • Marx J, Herrnkind W (1985b) Factors regulating microhabitat use by young juvenile spiny lobsters, Panulirus argus: food and shelter. J Crust Biol 5:650–657

    Article  Google Scholar 

  • Mathieson AC, Dawes CJ (1975) Seasonal studies of Florida sublittoral marine algae. Bull Mar Sci 25:46–65

    Google Scholar 

  • McClelland JW, Valiela I (1998) Changes in food web structure under the influence of increased anthropogenic nitrogen inputs to estuaries. Mar Ecol Prog Ser 168:259–271

    Article  CAS  Google Scholar 

  • 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 138–157

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Moncreiff CA, Sullivan MJ (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stabe isotope analysis. Mar Ecol Prog Ser 215:93–106

    Article  CAS  Google Scholar 

  • Opresko DM (1973) Abundance and distribution of shallow-water gorgonians in the area of Miami, Florida. Bull Mar Sci 23:535–557

    Google Scholar 

  • 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: 141–146

    Article  PubMed  CAS  Google Scholar 

  • Page HM (1997) Importance of vascular plant and algal production to macro-invertebrate consumers in a southern California marsh. Estuar Coast Shelf Sci 45:823–834

    Article  Google Scholar 

  • 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 45:705–715

    Article  Google Scholar 

  • Paul VJ, Hay ME (1986) Seaweed susceptibility to herbivory: chemical and morphological correlates. Mar Ecol Prog Ser 33:255–264

    Article  CAS  Google Scholar 

  • Petelle M, Haines B, Haines E (1979) Insect food preferences analyzed using 13C/12C ratios. Oecologia 38:159–166

    Article  Google Scholar 

  • Peterson BJ, Howarth RW, Garritt RH (1986) Sulphur and carbon isotopes as tracers of salt-marsh organic matter flow. Ecology 67:865–874

    Article  CAS  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • Peterson BJ, Fourqurean JW (2001) Large-scale patterns in seagrass (Thalassia testudinum) demographics in south Florida. Limnol Oceanogr 46:1077–1090

    Article  Google Scholar 

  • Phillips DL (2001) Mixing models in analysis of diet using multiple stable isotopes: a critique. Oecologia 127:166–170

    Article  Google Scholar 

  • Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269

    Article  PubMed  Google Scholar 

  • Reiswig HM (1971a) Particle feeding in natural populations of three marine demosponges. Biol Bull 141:568–591

    Article  Google Scholar 

  • 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 176:179–190

    Article  Google Scholar 

  • 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 71:297–299

    Article  Google Scholar 

  • 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 236:241–254

    Article  Google Scholar 

  • Stachowicz JJ, Hay ME (1996) Facultative mutualism between a herbivorous crab and a coralline alga: advantages of eating noxious seaweeds. Oecologia 105:377–387

    Article  Google Scholar 

  • Street GT, Montagna PA, Parker PL (1997) Incorporation of brown tide into an estuarine food web. Mar Ecol Prog Ser 152:67–78

    Article  Google Scholar 

  • Suren AM, Lake PS (1989) Edibility of fresh and decomposing macrophytes to three species of freshwater invertebrate herbivores. Hydrobiologia 178:165–178

    Article  Google Scholar 

  • Thayer GW, Parker PL, LaCroix MW, Fry B (1978) The stable isotope ratio of some components of an eelgrass, Zostera marina, bed. Oecologia 35:1–12

    Article  Google Scholar 

  • 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 23:277–285

    Article  Google Scholar 

  • Wada E, Mizutani H, Minagawa M (1991) The use of stable isotopes for food web analysis. Crit Rev Food Sci Nutr 30:361–371

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson CR (1984) Immunological evidence for the Precambrian origin of bacterial symbiosis in marine sponges. Proc R Soc Lond B 220:509–517

    Article  Google Scholar 

  • Yamamuro M (1999) Importance of epiphytic cyanobacteria as food sources for heterotrophs in a tropical seagrass bed. Coral Reefs 18:263–271

    Article  Google Scholar 

  • 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 21–33

    Google Scholar 

  • 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 69:1111

    Google Scholar 

  • Zieman JC, Fourqurean JW, Iverson RL (1989) Distribution, abundance, and productivity of seagrasses and macroalgae in Florida Bay. Bull Mar Sci 44:292–311

    Google Scholar 

  • Zieman JC, Fourqurean JW, Frankovich TA (1999) Seagrass dieoff in Florida Bay: long term trends in abundance and productivity of turtlegrass, Thalassia testudinum. Estuaries 22:460–470

    Article  Google Scholar 

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Acknowledgements

We are grateful to S. Wainright for consultation in the design of this study and for advice regarding sample selection and preparation. We also thank D.K. Behringer, J.E. Schratweiser, E. Riclet and D.N. Robertson for their assistance in sample collection. Funding for this study was provided by a Florida Sea Grant award (LR-B-38) to M. Butler. Suggestions from reviewers were appreciated and improved the manuscript. All of the experiments performed during this study were in compliance with the laws of the United States of America.

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Correspondence to Mark J. Butler IV.

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Communicated by Jim Ehleringer

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Behringer, D.C., Butler, M.J. Stable isotope analysis of production and trophic relationships in a tropical marine hard-bottom community. Oecologia 148, 334–341 (2006). https://doi.org/10.1007/s00442-006-0360-0

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