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Ecosystems

, Volume 22, Issue 4, pp 796–804 | Cite as

Land–Ocean Connectivity Through Subsidies of Terrestrially Derived Organic Matter to a Nearshore Marine Consumer

  • Daniel GormanEmail author
  • Marinella Pucci
  • Lucy S. H. Soares
  • Alexander Turra
  • Thomas A. Schlacher
Article

Abstract

Land–ocean coupling in the form of riverine inputs of terrestrial matter can constitute an energetic subsidy to food webs in nearshore coastal areas. In regions with distinctly seasonal rainfall patterns, the strength and spatial footprint of any terrestrial signal in receiving marine food webs is predicted to mirror seasonal changes in fluvial forcing. Here, we test this prediction in a subtropical bay by isotopically (δ13C and δ15N) characterizing the main primary producers and reconstructing (using a Bayesian stable isotope mixing model) their contributions to the diet of thinstripe hermit crabs (Clibanarius vittatus). Seasonal rainfall flushed terrestrial carbon out of coastal watersheds, and this material made a sizable (up to 28%) contribution to the diet of marine consumers, in addition to mangroves, seagrass and algae. Our isotope model indicates that inputs of terrestrial grasses and other littoral vegetation were 15% greater as a result of increased fluvial forcing. In addition, the spatial footprint of the terrestrial signal in marine consumers propagated more widely throughout the bay during high-rainfall periods. Given the widespread conversion of natural watershed habitats for agriculture and urban development, understanding the nature, temporal dynamics and strength of such land–ocean coupling will become increasingly important.

Keywords

terrestrial input δ13δ15hermit crabs spatial variability Brazil 

Notes

Acknowledgements

This research was funded by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) through the BIOTA-Araçá Project (2011/50317-5) and scholarship grants to DG (2013/07576-5; 2018/06162-6) and MP (2012/09937-2). Isotopic analysis was done at the University of California, Davis.

Supplementary material

10021_2018_303_MOESM1_ESM.doc (48 kb)
Supplementary material 1 (DOC 48 kb)

References

  1. Abrantes K, Sheaves M. 2008. Incorporation of terrestrial wetland material into aquatic food webs in a tropical estuarine wetland. Estuar Coast Shelf Sci 80:401–12.CrossRefGoogle Scholar
  2. Amaral ACZ, Migotto AE, Turra A, Schaeffer-Novelli Y. 2010. Araçá: biodiversity, impacts and threats. Biota Neotrop 10:219–64.CrossRefGoogle Scholar
  3. Amaral ACZ, Corte GN, Rosa JS, Denadai MR, Colling LA, Borzone C, Veloso V, Omena EP, Zalmon IR, Rocha-Barreira CD, de Souza JRB, da Rosa LC, de Almeida TCM. 2016. Brazilian sandy beaches: characteristics, ecosystem services, impacts, knowledge and priorities. Braz J Oceanogr 64:11.CrossRefGoogle Scholar
  4. Anderson WB, Wait DA, Stapp P. 2008. Resources from another place and time: responses to pulses in a spatially subsidized system. Ecology 89:660–70.CrossRefPubMedGoogle Scholar
  5. Atwood TB, Wiegner TN, MacKenzie RA. 2012. Effects of hydrological forcing on the structure of a tropical estuarine food web. Oikos 121:277–89.CrossRefGoogle Scholar
  6. Augusto FG, Tassoni M, Ferreira A, Pereira AL, de Camargo PB, Martinelli LA. 2015. Land use change in the Atlantic Forest affects carbon and nitrogen sources of streams as revealed by the isotopic composition of terrestrial invertebrates. Biota Neotrop 15:8.CrossRefGoogle Scholar
  7. Aveytua-Alcazar L, Camacho-Ibar VF, Souza AJ, Allen JI, Torres R. 2008. Modelling Zostera marina and Ulva spp. in a coastal lagoon. Ecol Model 218:354–66.CrossRefGoogle Scholar
  8. Carrilho C. 2015. Identificação e valoração econômica e sociocultural dos serviços ecossistêmicos da Baía do Araçá - São Sebastião, SP, Brasil. Programa de Pós-Graduação em Ciência Ambiental, Instituto de Energia e Ambiente: Universidade de São Paulo, p170Google Scholar
  9. Choi TS, Kim JH, Kim KY. 2001. Seasonal changes in the abundance of Ulva mats on a rocky intertidal zone of the southern coast of Korea. Algae 16:337–41.Google Scholar
  10. Connolly RM, Schlacher TA. 2013. Sample acidification significantly alters stable isotope ratios of sulfur in aquatic plants and animals. Mar Ecol Prog Ser 493:1–8.CrossRefGoogle Scholar
  11. Connolly RM, Waltham NJ. 2015. Spatial analysis of carbon isotopes reveals seagrass contribution to fishery food web. Ecosphere 6:12.CrossRefGoogle Scholar
  12. Connolly RM, Schlacher TA, Gaston TF. 2009. Stable isotope evidence for trophic subsidy of coastal benthic fisheries by river discharge plumes off small estuaries. Mar Biol Res 5:164–71.CrossRefGoogle Scholar
  13. Connolly RM, Gorman D, Hindell JS, Kildea TN, Schlacher TA. 2013. High congruence of isotope sewage signals in multiple marine taxa. Mar Pollut Bull 71:152–8.CrossRefPubMedGoogle Scholar
  14. Dias E, Morais P, Cotter AM, Antunes C, Hoffman JC. 2016. Estuarine consumers utilize marine, estuarine and terrestrial organic matter and provide connectivity among these food webs. Mar Ecol Prog Ser 554:21–34.CrossRefGoogle Scholar
  15. Garcia AF, Bueno M, Leite FPP. 2016. The Bostrychietum community of pneumatophores in Araca Bay: an analysis of the diversity of macrofauna. J Mar Biol Assoc UK 96:1617–24.CrossRefGoogle Scholar
  16. Giannini MFC, Ciotti AM. 2016. Parameterization of natural phytoplankton photo-physiology: effects of cell size and nutrient concentration. Limnol Oceanogr 61:1495–512.CrossRefGoogle Scholar
  17. Goni MA, Ruttenberg KC, Eglinton TI. 1997. Source and contribution of terrigenous organic carbon to surface sediments in the Gulf of Mexico. Nature 389:275–8.CrossRefGoogle Scholar
  18. Gorman D, Russell BD, Connell SD. 2009. Land-to-sea connectivity: linking human-derived terrestrial subsidies to subtidal habitat change on open rocky coasts. Ecol Appl 19:1114–26.CrossRefPubMedGoogle Scholar
  19. Gorman D, Sikinger CE, Turra A. 2015. Spatial and temporal variation in the predation risk for hermit crabs in a subtropical bay. J Exp Mar Biol Ecol 462:98–104.CrossRefGoogle Scholar
  20. Gorman D, Turra A, Bergstrom ER, Horta PA. 2016. Population expansion of a tropical seagrass (Halophila decipiens) in the southwest Atlantic (Brazil). Aquat Bot 132:30–6.CrossRefGoogle Scholar
  21. Gorman D, Corte G, Checon HH, Amaral ACZ, Turra A. 2017a. Benthic sensitivity index (SI) for multiple-use areas: an informative tool for coastal and marine spatial planning. Ecol Indic 82:23–31.CrossRefGoogle Scholar
  22. Gorman D, Turra A, Connolly RM, Olds AD, Schlacher TA. 2017b. Monitoring nitrogen pollution in seasonally-pulsed coastal waters requires judicious choice of indicator species. Mar Pollut Bull 122:149–55.CrossRefPubMedGoogle Scholar
  23. Gorman D, Ragagnin MN, Turra A. 2018. Assessing the resilience of hermit crabs to extrinsic and intrinsic environmental change. Estuar Coast Shelf Sci 214:25–30.CrossRefGoogle Scholar
  24. Laidre ME. 2013. Foraging across ecosystems: diet diversity and social foraging spanning aquatic and terrestrial ecosystems by an invertebrate. Mar Ecol Evol Perspect 34:80–9.CrossRefGoogle Scholar
  25. Lartigue J, Fontanella FM, Cebrian J, Arbaczauskas S. 2003. Evidence that ultraviolet radiation may depress short-term photosynthetic rates of intertidal Ulva lactuca and consumption by a generalist feeder (Clibanarius vittatus). Gulf Mex Sci 21:71–8.Google Scholar
  26. Marczak LB, Thompson RM, Richardson JS. 2007. Meta-analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88:140–8.CrossRefPubMedGoogle Scholar
  27. Marin X. 2013. ggmcmc: graphical tools for analyzing Markov Chain Monte Carlo simulations from Bayesian inference.Google Scholar
  28. Mellbrand K, Lavery PS, Hyndes G, Hamback PA. 2011. Linking Land and sea: different pathways for marine subsidies. Ecosystems 14:732–44.CrossRefGoogle Scholar
  29. Montes E, Thunell R, Muller-Karger FE, Lorenzoni L, Tappa E, Troccoli L, Astor Y, Varela R. 2013. Sources of delta N-15 variability in sinking particulate nitrogen in the Cariaco Basin, Venezuela. Deep Sea Res Part II Top Stud Oceanogr 93:96–107.CrossRefGoogle Scholar
  30. Neto JAB, Barreto CF, da Silva MAM, Smith BJ, McAllister JJ, Vilela CG. 2013. Nearshore sedimentation as a record of landuse change and erosion: Jurujuba Sound, Niteroi, SE Brazil. Ocean Coast Manag 77:31–9.CrossRefGoogle Scholar
  31. Phillips DL, Gregg JW. 2001. Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–9.CrossRefPubMedGoogle Scholar
  32. Plucênio RM, Dechoum M, Castellani TT. 2013. Invasão Biológica em Restinga: O Estudo de caso de Terminalia catappa L. (Combretaceae). Número Temático: Diagnóstico e Controle de Espécies Exóticas Invasoras em Áreas Protegidas: Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio).Google Scholar
  33. Polis GA, Hurd SD. 1996. Linking marine and terrestrial food webs: allochthonous input from the ocean supports high secondary productivity on small islands and coastal land communities. Am Nat 147:396–423.CrossRefGoogle Scholar
  34. Polis GA, Anderson WB, Holt RD. 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316.CrossRefGoogle Scholar
  35. Ren JS, Barr NG, Scheuer K, Schiel DR, Zeldis J. 2014. A dynamic growth model of macroalgae: application in an estuary recovering from treated wastewater and earthquake-driven eutrophication. Estuar Coast Shelf Sci 148:59–69.CrossRefGoogle Scholar
  36. Sant’Anna BS, dos Santos DM, Sandron DC, de Souza SC, de Marchi MRR, Zara FJ, Turra A. 2012. Hermit crabs as bioindicators of recent tributyltin (TBT) contamination. Ecol Indic 14:184–8.CrossRefGoogle Scholar
  37. Sarma VVSS, Gupta SNM, Babu PVR, Acharya T, Harikrishnachari N, Vishnuvardhan K, Rao NS, Reddy NPC, Sarma VV, Sadhuram Y, Murty TVR, Kumar MD. 2009. Influence of river discharge on plankton metabolic rates in the tropical monsoon driven Godavari estuary, India. Estuar Coast Shelf Sci 85:515–24.CrossRefGoogle Scholar
  38. Schlacher TA, Connolly RM. 2009. Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches. Ecosystems 12:311–21.CrossRefGoogle Scholar
  39. Schlacher TA, Connolly RM. 2014. Effects of acid treatment on carbon and nitrogen stable isotope ratios in ecological samples: a review and synthesis. Methods Ecol Evol 5:541–50.CrossRefGoogle Scholar
  40. Schlacher TA, Skillington AJ, Connolly RM, Robinson W, Gaston TF. 2008. Coupling between marine plankton and freshwater flow in the plumes off a small estuary. Int Rev Hydrobiol 93:641–58.CrossRefGoogle Scholar
  41. Schmidt F, Hinrichs KU, Elvert M. 2010. Sources, transport, and partitioning of organic matter at a highly dynamic continental margin. Mar Chem 118:37–55.CrossRefGoogle Scholar
  42. Semmens B, Stock B, Jackson A, Ward E, Parnell A, Phillips D, Inger R, Bearhop S. in prep. MixSIAR: a new generation of Bayesian mixing model.Google Scholar
  43. Soares L, Arantes L, Pucci M. 2018. Food web of a subtropical tidal flat, Atlantic Southwestern: Temporal and spatial variability of the primary organic sources. Ocean Coast Manag.  https://doi.org/10.1016/j.ocecoaman.2018.01.035.CrossRefGoogle Scholar
  44. Steinarsdottir MB, Ingolfsson A, Olafsson E. 2009. Trophic relationships on a fucoid shore in south-western Iceland as revealed by stable isotope analyses, laboratory experiments, field observations and gut analyses. J Sea Res 61:206–15.CrossRefGoogle Scholar
  45. Turra A, Denadai MR. 2003. Daily activity of four tropical intertidal hermit crabs from southeastern Brazil. Braz J Biol 63:537–44.CrossRefPubMedGoogle Scholar
  46. Turra A, Leite FPP. 2000. Population biology and growth of three sympatric species of intertidal hermit crabs in south-eastern Brazil. J Mar Biol Assoc UK 80:1061–9.CrossRefGoogle Scholar
  47. Vander Zanden MJ, Vadeboncoeur Y. 2002. Fishes as integrators of benthic and pelagic food webs in lakes. Ecology 83:2152–61.CrossRefGoogle Scholar
  48. Vanderklift MA, Ponsard S. 2003. Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–82.CrossRefGoogle Scholar
  49. Williams AB. 1984. Shrimps, lobsters, and crabs of the Atlantic Coast of the Eastern United States, Maine to Florida. California: Smithsonian Institution Press. p 550.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto OceanográficoUniversity of São PauloSão PauloBrazil
  2. 2.Center for Marine Biology (CEBIMar)University of São PauloSão SebastiãoBrazil
  3. 3.School of Science and EngineeringUniversity of the Sunshine CoastQueenslandAustralia

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