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Stoichiometry, growth, and fecundity responses to nutrient enrichment by invertebrate grazers in sub-tropical turtle grass (Thalassia testudinum) meadows

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Abstract

Although the effectiveness of herbivores in mitigating the effects of nutrient enrichment is well documented, few studies have examined the effects of nutrient enrichment on components of consumer fitness. Enclosures were deployed in shallow turtle grass (Thalassia testudinum) beds in Florida Bay, Florida in fall 2003, spring 2004, and fall 2004 to measure the effects of nitrogen and phosphorous enrichment on the growth, fecundity, and stoichiometry of three invertebrate epiphyte grazers commonly associated with T. testudinum. The gastropod Turbo castanea exhibited significantly greater wet weight gain and lower C:P and N:P in enriched than in ambient treatments. Although nutrient enrichment did not have any significant effects on the growth of caridean shrimp (treatment consisted of several different caridean shrimp species), their C:N was significantly lower in enriched treatments. The final size and stoichiometry of the hermit crab Paguristes tortugae was not significantly affected by nutrient enrichment, nor did nutrient enrichment significantly affect the fecundity of P. tortugae, the only grazer in which gravid individuals or egg masses were present. Our study demonstrated that nutrient enrichment of primary producers can positively affect the growth of marine invertebrate grazers and alter their stoichiometry; however, these effects were species-specific and may be dependent upon the life stage, specific diets, and/or compensatory feeding habits of the grazers.

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References

  • Armitage AR, Frankovich TA, Heck KL, Fourqurean JW (2005) Experimental nutrient enrichment causes complex changes in seagrass, microalgae, and macroalgae community structure in Florida Bay. Estuaries 28:422–434. doi:10.1007/BF02693924

    Article  Google Scholar 

  • Atkinson MJ, Smith SV (1983) C:N:P ratios of benthic marine plants. Limnol Oceanogr 28:568–574

    Article  CAS  Google Scholar 

  • Baggett LP, Heck KL, Frankovich TA, Armitage AR, Fourqurean JW (2010) Nutrient enrichment, grazer identity and their effects on epiphytic algal assemblages: field experiments in sub-tropical turtle grass (Thalassia testudinum) meadows. Mar Ecol Prog Ser 406:33–45. doi:10.3354/meps08533

    Article  CAS  Google Scholar 

  • Bauer RT, Van Hoy R (1996) Variation in sexual systems (protandry, gonochorism) and reproductive biology among three species of the shrimp genus Thor (Decapoda: Caridea). Bull Mar Sci 59:53–73

    Google Scholar 

  • Boersma M, Kreutzer C (2002) Life at the edge: is food quality really of minor importance at low quantities? Ecology 83:2552–2561

    Article  Google Scholar 

  • Boesch DF (2002) Challenges and opportunities for science in reducing nutrient over-enrichment of coastal ecosystems. Estuaries 26:886–900

    Article  Google Scholar 

  • Bonnet D, Carlotti F (2001) Development and egg production in Centropages typicus (Copepoda: Calanoidea) fed different food types: a laboratory study. Mar Ecol Prog Ser 224:133–148

    Article  Google Scholar 

  • Bowman MF, Chambers PA, Schindler DW (2005) Changes in stoichiometric constraints on epilithon and benthic macroinvertebrates in response to slight nutrient enrichment of mountain rivers. Freshw Biol 50:1836–1852. doi:10.1111/j.1365-2427.2005.01454.x

    Article  CAS  Google Scholar 

  • Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139. doi:10.1890/0012-9658(2006)87[3128:HVNCOM]2.0.CO;2

    Article  Google Scholar 

  • Clark DR (2001) Growth rate relationships to physiological indices of nutrient status in marine diatoms. J Phycol 37:249–256. doi:10.1046/j.1529-8817.2001.037002249.x

    Article  CAS  Google Scholar 

  • Cross WF, Benstead JP, Rosemond AD, Wallace JB (2003) Consumer-resource stoichiometry in detritus-based streams. Ecol Lett 6:721–732. doi:10.1046/j.1461-0248.2003.00481.x

    Article  Google Scholar 

  • Cruz-Rivera E, Hay M (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81:201–219. doi:10.1890/0012-9658(2000)081[0201:CQRQFC]2.0.CO;2

    Article  Google Scholar 

  • Cruz-Rivera E, Hay M (2003) Prey nutritional value quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol Monogr 73:483–506. doi:10.1890/0012-9615(2003)073[0483:PNQIWC]2.0.CO;2

    Article  Google Scholar 

  • Deegan LA (2002) Lessons learned: the effects of nutrient enrichment on the support of nekton by seagrass and salt marsh ecosystems. Estuaries 25:727–742

    Article  CAS  Google Scholar 

  • Deegan LA, Wright A, Ayvazian SG, Finn JT, Golden H, Rand Merson R, Harrison J (2002) Nitrogen loading alters seagrass ecosystem structure and support of higher trophic levels. Aquat Conserv Mar Freshw Ecosyst 12:193–212

    Article  Google Scholar 

  • Duarte CM (2002) The future of seagrass meadows. Environ Conserv 29:192–206

    Article  Google Scholar 

  • Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–751. doi:10.1890/0012-9658(1999)080[0735:TSOCDN]2.0.CO;2

    Article  Google Scholar 

  • Elser JJ, Frost P, Kyle M, Urabe J, Andersen T (2002) Effects of light and nutrients on plankton stoichiometry and biomass in a P-limited lake. Hydrobiologia 481:101–112. doi:10.1023/A:1021217221004

    Article  Google Scholar 

  • Færøvig PJ, Hessen DO (2003) Allocation strategies in crustacean stoichiometry: the potential role of phosphorous in the limitation of reproduction. Freshw Biol 48:1782–1792. doi:10.1046/j.1365-2427.2003.01128.x

    Article  Google Scholar 

  • Ferrao-Filho AS, Tessier AJ, DeMott WR (2007) Sensitivity of herbivorous zooplankton to phosphorous-deficient diets: testing stoichiometric theory and the growth rate hypothesis. Limnol Oceanogr 52:407–415

    Article  CAS  Google Scholar 

  • Fink P, von Elhert E (2006) Physiological responses to stoichiometric constraints: nutrient limitation and compensatory feeding in a freshwater snail. Oikos 115:484–494

    Article  CAS  Google Scholar 

  • Foster GG, Hodgson AN, Balarin M (1999) Effect of diet on the growth rate and reproductive fitness of Turbo sarmaticus (Mollusca: Vetigastropoda: Turbinidae). Mar Biol 134:307–315. doi:10.1007/s002270050548

    Article  Google Scholar 

  • Fourqurean JW, Robblee MB (1999) Florida Bay: a history of recent ecological changes. Estuaries 22:345–357. doi:10.2307/1353203

    Article  CAS  Google Scholar 

  • Fourqurean JW, Zieman JC (2002) Nutrient content of the seagrass Thalassia testudinum reveals regional patterns of relative availability of nitrogen and phosphorus in the Florida Keys USA. Biogeochemistry 61:229–245. doi:10.1023/A:1020293503405

    Article  CAS  Google Scholar 

  • Fourqurean JW, Zieman JC, Powell GVN (1992) Phosphorous 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 

  • Frankovich TA, Zieman JC (2005) A temporal investigation of grazer dynamics, nutrients, seagrass leaf productivity, and epiphyte standing stock. Estuaries 28:41–52. doi:10.1007/BF02732752

    Article  Google Scholar 

  • Gil M, Armitage AR, Fourqurean JW (2006) Nutrient impacts on epifaunal density and species composition in a subtropical seagrass bed. Hydrobiologia 569:437–447. doi:10.1007/s10750-006-0147-7

    Article  CAS  Google Scholar 

  • Gurevitch J, Morrow LL, Wallace A, Walsh JS (1992) A meta-analysis of competition in field experiments. Am Nat 140:539–572

    Article  Google Scholar 

  • Hazlett BA (1981) The behavioral ecology of hermit crabs. Annu Rev Ecol Syst 12:1–22

    Article  Google Scholar 

  • Heck KL, Valentine JF (2007) The primacy of top-down effects in shallow benthic ecosystems. Estuaries Coasts 30:371–381. doi:10.1007/BF02819384

    Article  Google Scholar 

  • Heck KL Jr, Valentine JF, Pennock JR, Chaplin G, Spitzer PM (2006) Effects of nutrient enrichment and grazing on shoalgrass (Halodule wrightii) and its epiphytes: results of a field experiment. Mar Ecol Prog Ser 326:145–156

    Article  CAS  Google Scholar 

  • Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064. doi:10.1890/0012-9658(2002)083[1052:NEIPOA]2.0.CO;2

    Article  Google Scholar 

  • Hessen DO, Færøvig PJ, Andersen T (2002) Light, nutrients, and P:C ratios in algae: grazer performance related to food quality and quantity. Ecology 83:1886–1898. doi:10.1890/0012-9658(2002)083[1886:LNAPCR]2.0.CO;2

    Article  Google Scholar 

  • Holmquist JG, Powell GVN, Sogard SM (1989) Decapod and stomatopod assemblages on a system of seagrass-covered mud banks in Florida Bay. Mar Biol 100:473–483. doi:10.1007/BF00394824

    Article  Google Scholar 

  • Huberty AF, Denno RF (2006) Consequences of nitrogen and phosphorous limitation for the performance of two planthoppers with divergent life-history strategies. Oecologia 149:444–455. doi:10.1007/s00442-006-0462-8

    Article  Google Scholar 

  • Kraufvelin P, Salovius S, Christie H, Moy FE, Karez R, Pedersen MF (2006) Eutrophication-induced changes in benthic algae affect the behavior and fitness of the marine amphipod Gammarus locusta. Aquat Bot 84:199–209. doi:10.1016/j.aquabot.2005.08.008

    Article  Google Scholar 

  • Lapointe BE, O’Connell J (1989) Nutrient-enhanced growth of Cladophora prolifera in Harrington Sound, Bermuda: eutrophication of a confined, phosphorus-limited marine ecosystem. Est Coast Shelf Sci 28:347–360

    Article  CAS  Google Scholar 

  • Liess A, Hillebrand H (2006) Role of nutrient supply in grazer-periphyton interactions: reciprocal influences of periphyton and grazer nutrient stoichiometry. J N Am Benthol Soc 25:632–642

    Article  Google Scholar 

  • McGlathery KJ (2001) Macroalgal blooms contribute to the decline of seagrass in nutrient-enriched coastal waters. J Phycol 37:453–456

    Article  Google Scholar 

  • Nixon SW, Oviatt C, Frithsen J, Sullivan B (1986) Nutrients and productivity of estuaries and coastal marine ecosystems. J Limnol Soc S Afr 12:43–71. doi:10(1080/03779688),1986,9639398

    CAS  Google Scholar 

  • Orth RJ, van Montfrans J (1987) Utilization of a seagrass meadow and tidal marsh creek by blue crabs Callinectes sapidus. 1. Seasonal and annual variations in abundance with emphasis on post-settlement juveniles. Mar Ecol Prog Ser 41:283–294

    Article  Google Scholar 

  • Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL Jr, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S, Short FT, Waycott M, Williams SL (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996. doi:10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2

    Article  Google Scholar 

  • Petersen D, Laterveer M, Schumacher H (2005) Spatial and temporal variation in larval settlement of reefbuilding corals in mariculture. Aquaculture 249:317–327. doi:10.1016/j.aquaculture.2005.04.048

    Article  Google Scholar 

  • Quiñones-Rivera ZJ, Fleeger JW (2005) The grazing effects of grass shrimp, Palaemonetes pugio, on epiphytic microalgae associated with Spartina alterniflora. Estuaries 28:274–285. doi:10.1007/BF02732861

    Article  Google Scholar 

  • Robblee MB, Daniels A (2003) Fish and shrimp in relation to seagrass habitat change in Johnson Key Basin, western Florida Bay (1985–1995) in joint conference on the science and restoration of the Greater Everglades and Florida Bay ecosystem. National Oceanographic and Atmospheric Administration, Miami, pp 230–232

    Google Scholar 

  • Romero J, Lee K-S, Pérez M, Mateo MA, Alcoverro T (2006) Nutrient dynamics in seagrass ecosystems. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 227–254

    Chapter  Google Scholar 

  • Ruesink JL (2000) Intertidal mesograzers in field microcosms; linking laboratory feeding rates to community dynamics. J Exp Mar Biol Ecol 248:163–176. doi:10.1016/S0022-0981(00)00170-2

    Article  Google Scholar 

  • Russell-Hunter WD (1970) Aquatic productivity: an introduction to some basic aspects of biological oceanography and limnology. The Macmillan Company, New York

    Google Scholar 

  • Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ (2003) Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett 6:96–101. doi:10.1046/j.1461-0248.2003.00409.x

    Article  Google Scholar 

  • Sharp JH (1974) Improved analysis for ‘particulate’ organic carbon and nitrogen from seawater. Limnol Oceanogr 19:984–989

    Article  CAS  Google Scholar 

  • Singer GA, Battin TJ (2007) Anthropogenic subsidies alter stream consumer-resource stoichiometry, biodiversity, and food chains. Ecol Appl 17:376–389. doi:10.1890/06-0229

    Article  Google Scholar 

  • Solorzano L, Sharp JH (1980) Determination of total dissolved phosphorus and particulate phosphorus in natural waters. Limnol Oceanogr 25:754–758

    Article  CAS  Google Scholar 

  • Stelzer RS, Lamberti GA (2002) Ecological stoichiometry in running waters: periphyton chemical composition and snail growth. Ecology 83:1039–1051. doi:10.1890/0012-9658(2002)083[1039:ESIRWP]2.0.CO;2

    Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Tewfik A, Rasmussen JB, McCann KS (2007) Simplification of seagrass food webs across a gradient of nutrient enrichment. Can J Fish Aquat Sci 64:956–967

    Article  Google Scholar 

  • Tomasko DA, Lapointe BE (1991) Productivity and biomass of Thalassia testudinum as related to water column nutrient availability and epiphyte levels: field observations and experimental studies. Mar Ecol Prog Ser 75:9–17

    Article  Google Scholar 

  • Tomasko DA, Dawes CJ, Hall MO (1996) The effects of anthropogenic nutrient enrichment on turtle grass (Thalassia testudinum) in Sarasota Bay, Florida. Estuaries Coasts 19:448–456

    Article  Google Scholar 

  • Valiela I (1995) Marine ecological processes, 2nd edn. Springer, New York

    Google Scholar 

  • Van Nieuwerburgh L, Wänstrand I, Snoeijs P (2004) Growth and C:N:P ratios in copepods grazing on N- or Si-limited phytoplankton blooms. Hydrobiologia 514:57–72. doi:10.1023/B:hydr.0000018206.02271.2b

    Article  Google Scholar 

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Acknowledgments

This research was made possible by grants from the Alabama Center for Estuarine Studies (ACES Project # R-83065101-3-05), the Everglades National Park under cooperative agreement 1443CA528001022, and the Florida Coastal Everglades Long Term Ecological Research Program funded by the US National Science Foundation (Cooperative Agreement # DEB-9910514). D. Morrison and B. Perry facilitated permit issuance and the use of ENP facilities. We are grateful to the following people for their hard work and assistance with the field experiments: From the DISL: R. Adams, D. Booth, D. Byron, B. Furman, J. Koeppel, L. Kramer, K. Merkins, R. Shiplett, T. Spitzer, C. Steeves, and K. Young. From Florida International University: B. Dewsbury, C. Furst, M. Gil, S. Ruiz, T. Thyberg, and P. William. We thank L. Linn of DISL for her assistance with elemental analysis, and S. Bosarge of DISL for creating Fig. 1. This is the contribution number 408 from the Dauphin Island Sea Laboratory and 569 from the Southeast Environmental Research Center at Florida International University.

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Correspondence to Lesley P. Baggett.

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Communicated by F. Bulleri.

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Baggett, L.P., Heck, K.L., Frankovich, T.A. et al. Stoichiometry, growth, and fecundity responses to nutrient enrichment by invertebrate grazers in sub-tropical turtle grass (Thalassia testudinum) meadows. Mar Biol 160, 169–180 (2013). https://doi.org/10.1007/s00227-012-2075-6

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