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Trophic ecology of elasmobranch and teleost fishes in a large subtropical seagrass ecosystem (Florida Big Bend) determined by stable isotope analysis

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Abstract

Carbon and nitrogen stable isotope analyses were used to infer relative trophic structure and examine regional variation in trophic dynamics of fishes in the Florida Big Bend, an approximately 300 km stretch of relatively pristine coastline in the eastern Gulf Of Mexico that contains over 250,000 ha of seagrass. The Florida Big Bend is home to a diverse assemblage of fauna; and the ecosystem is regionally important through its support of robust fishing (recreational and commercial) and eco-tourism industries. Stable isotope analyses suggest assemblages of fishes in the Florida Big Bend are trophically diverse, with considerable isotopic overlap across many taxa. Patterns of trophic structure corroborated the results of similar studies of these and related taxa and in other seagrass ecosystems, and there appear to be multiple channels of primary production. Large elasmobranch fishes were most enriched in δ 15N with values well above the teleost fishes sampled, while smaller and demersal elasmobranchs had δ 15N signatures comparable to several species of predatory teleosts. Results of stable isotope analyses suggested high trophic redundancy and overlap in resource use among both teleost and elasmobranch fishes. Comparisons of regional stable isotope values revealed some spatial variability and indicated the southern Big Bend is isotopically distinct, suggesting a distinct regional faunal zone in this region, potentially due to greatly reduced river influence in the southern portion of the system.

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References

  • Ajemian MJ, Powers SP (2012) Habitat-specific feeding by cownose rays (Rhinoptera bonasus) of the northern Gulf of Mexico. Environ Biol Fishes 95:79–97

    Article  Google Scholar 

  • Bethea DM, Buckel JA, Carlson JK (2004) Foraging ecology of the early life stages of four sympatric shark species. Mar Ecol Prog Ser 268:245–264

    Article  Google Scholar 

  • Bethea DM, Carlson JK, Buckel JA, Satterwhite M (2006) Ontogenetic and site-related trends in the diet of the Atlantic sharpnose shark, Rhizoprionodon terraenovae from the northeast Gulf of Mexico. Bull Mar Sci 78:287–307

    Google Scholar 

  • Bethea DM, Hale L, Carlson JK, Cortes E, Manire CA, Gelsleichter J (2007) Geographic and ontogenetic variation in the diet and daily ration of the bonnethead shark, Sphyrna tiburo, from the eastern Gulf of Mexico. Mar Biol 152:1009–1020

    Article  Google Scholar 

  • Bowman RE, Stillwell CE, Michaels WL, Grosslein MD (2000) Food of northwest Atlantic fishes and two common species of squid. NOAA Technical Memorandum NMFS-NE-155

  • Carlisle AB, Litvin SW, Madigan DJ, Lyons K, Bigman JS, Ibarra M, Bizzaro JJ (2017) Interactive effects of urea and lipid content confound stable isotope analysis in elasmobranch fishes. Can J Fish Aquat Sci 74:419–428

    Article  CAS  Google Scholar 

  • Castro JI (1996) Biology of the blacktip shark, Carcharhinus limbatus, off the southeastern United States. Bull Mar Sci 59:508–522

    Google Scholar 

  • Castro JI (2000) The biology of the nurse shark, Ginglymostoma cirratum, off the Florida east coast and Bahama Islands. Environ Biol Fish 58:1–22

    Article  Google Scholar 

  • Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (∆15N and ∆13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453

    Article  CAS  Google Scholar 

  • Chanton JP, Lewis FG (1999) Plankton and dissolved inorganic carbon isotopic composition in a river-dominated estuary: Apalachicola Bay, Florida, U.S.A. Estuaries 22:575–583

    Article  CAS  Google Scholar 

  • Chanton JP, Lewis FG (2002) Examination of coupling between primary and secondary production in a river-dominated estuary: Apalachicola Bay, Florida, U.S.A. Limnol Oceanogr 47:683–697

    Article  Google Scholar 

  • Chasar LC, Chanton JP, Koenig CC, Coleman FC (2005) Evaluating the effect of environmental disturbance on the trophic structure of Florida Bay, U.S.A.: Multiple stable isotope analyses of contemporary and historical specimens. Limnol Oceanogr 50:1059–1072

    Article  CAS  Google Scholar 

  • Collins AB, Heupel MR, Hueter RE, Motta PJ (2007) Hard prey specialist or opportunistic generalists? An examination of the diet of the cownose ray, Rhinoptera bonasus. Mar Freshwater Res 58:135–144

    Article  Google Scholar 

  • Cortes E (1999) Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci 56:707–717

    Article  Google Scholar 

  • Cortes E, Manire CA, Hueter RE (1996) Diet, feeding habits, and diel feeding chronology of the bonnethead shark, Sphyrna tiburo, in southwest Florida. Bull Mar Sci 58:353–367

    Google Scholar 

  • Cummings DO, Buhl J, Lee RW, Simpson SJ, Holmes SP (2012) Estimating niche width using stable isotope s in the face of habitat variability: a modelling case study in the marine environment. Plos One 7:1–14

    Google Scholar 

  • Darnell RM (1961) Trophic spectrum of an estuarine community, based on studies of Lake Pontchartrain, Louisiana. Ecology 42:553–568

    Article  Google Scholar 

  • Davis AM, Blanchette ML, Pusey BJ, Jardine TD, Pearson RG (2012) Gut content and stable isotope analyses provide complementary understanding of ontogenetic dietary shifts and trophic relationships among fishes in a tropical river. Freshw Biol 57:2156–2172

    Article  CAS  Google Scholar 

  • Dawes CJ, Phillips RC, Morrison G (2004) Seagrass Communities of the Gulf Coast of Florida: Status and Ecology. Florida Fish and Wildlife Conservation Commission Fish and Wildlife Research Institute and the Tampa Bay Estuary Program, St. Petersburg (iv + 74 pp)

  • Cocheret de la Moriniere E, Pollux BJA, Nagelkerken I, Hemminga MA, Huiskes AHL, van der Velde G (2003) Ontogenetic dietary changes of coral fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut-content analysis. Mar Ecol Prog Ser 246:279–289

  • Dennis CA, MacNeil MA, Rosati JY, Pitcher TE, Fisk AT (2010) Diet discrimination factors are inversely related to δ15N and δ13C of food for fish under controlled conditions. Rapid Commun Mass Spectrom 24:3515–3520

    Article  CAS  PubMed  Google Scholar 

  • Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Fry B, Macko SA, Zieman JC (1987) Review of stable isotopic investigations of food webs in seagrass meadows. In: Durako MJ, Phillips RC, Lewis RR (eds) Proceedings of a Symposium on Subtropical-Tropical Seagrasses, Southeast United States. Florida Department of Natural Resources, Bureau of Marine Research, St. Petersburg, 117–138 (Florida Mar Resources Publ No. 42)

  • Gilliam D, Sullivan KM (1993) Diet and feeding habits of the southern stingray Dasyatis americana in the central Bahamas. Bull Mar Sci 52:1007–1013

    Google Scholar 

  • Graham BS, Grubbs RD, Holland K, Popp BN (2007) A rapid ontogenetic shift in the diet of yellowfin tuna from Hawaii. Mar Biol 150:647–658

    Article  Google Scholar 

  • Harrell FE Jr. (2014) Hmisc: Harrell miscellaneous. R package version 3.14-3. http://CRAN.R-project.org/package=Hmisc

  • Heithaus MR, Vaudo JJ, Kreicker S, Layman CA, Krutzen M, Burkholder DA, Gastrich K, Bessey C, Sarabia R, Cameron K, Wirsing A, Thomson JA, Dunphy-Daly MM (2013) Apparent resource partitioning and trophic structure of large-bodied marine predators in a relatively pristine seagrass ecosystem. Mar Ecol Prog Ser 481:225–237

    Article  Google Scholar 

  • Hughes AR, Williams SL, Duarte CM, Heck KL, Waycott M (2008) Associations of concern: declining seagrasses and threatened dependent species. Front Ecol Environ 7:242–246

    Article  Google Scholar 

  • Hussey NE, Dudley SFJ, McCarthy ID, Cliff G, Fisk AT (2011) Stable isotope profiles of large marine predators: viable indicators of trophic position, diet, and movement in sharks? Can J Fish Aquat Sci 68:2029–2045

    Article  CAS  Google Scholar 

  • Hussey NE, MacNeil MA, Olin JA, McMeans BC, Kinney MJ, Chapman DD, Fisk AT (2012a) Stable isotopes and elasmobranchs: tissue types, methods, applications, and assumptions. J Fish Biol 80:1449–1484

    Article  CAS  PubMed  Google Scholar 

  • Hussey NE, Olin JA, Kinney MJ, McMeans BC, Fisk AT (2012b) Lipid extraction effects on stable isotope values (δ13C and δ15N) of elasmobranch muscle tissue. J Exp Mar Biol Ecol 434:7–15

    Article  CAS  Google Scholar 

  • Hussey NE, MacNeil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff G, Wintner SP, Fennessy ST, Fisk AT (2014) Rescaling the trophic structure of marine food webs. Ecol Lett 17:239–250

    Article  PubMed  Google Scholar 

  • Jackson EL, Rowden AA, Attrill MJ, Bossey SJ, Jones MB (2001) The importance of seagrass beds as a habitat for fishery species. Oceanogr Mar Biol 39:269–303

    Google Scholar 

  • Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER - stable isotope Bayesian ellipses in R. J Anim Ecol 80:595–602

    Article  PubMed  Google Scholar 

  • Kling GW, Fry B, O’Brien WJ (1992) Stable isotopes and planktonic trophic structure in Arctic lakes. Ecology 73:561–566

    Article  Google Scholar 

  • Layman CA, Arrington DA, Montana CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48

    Article  PubMed  Google Scholar 

  • Link JS, Browman HI (2014) Integrating what? Levels of marine ecosystem-based assessment and management. ICES J Mar Sci 71:1170–1173

    Article  Google Scholar 

  • Livingston RJ (1982) Trophic organization of fishes in a coastal seagrass system. Mar Ecol Prog Ser 7:1–12

    Article  Google Scholar 

  • Livingston RJ, Niu X, Lewis III FG, Woodsum GC (1997) Freshwater input to a Gulf estuary: long-term control of trophic organization. Ecol Appl 7:277–299

  • Matich P, Kiszka JJ, Gastrich KR, Heithaus MR (2017) Trophic redundancy among fishes in an East African nearshore seagrass community inferred from stable-isotope analysis. J Fish Biol 91:490–509

    Article  CAS  PubMed  Google Scholar 

  • McCann KS, Rasmussen JB, Umbanhowar J (2005) The dynamics of spatially coupled food webs. Ecol Lett 8:513–523

    Article  CAS  PubMed  Google Scholar 

  • Moncreiff CA, Sullivan MJ (2002) Tropic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 21:93–106

    Google Scholar 

  • Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470–480

    Article  PubMed  Google Scholar 

  • Nelson J, Chanton J, Coleman F, Koenig C (2011) Patterns of stable carbon turnover in gag, Mycteroperca microlepis, an economically important marine piscivore determined with a non-lethal surgical biopsy procedure. Environ Biol Fish 90:243–252

    Article  Google Scholar 

  • Nelson J, Wilson R, Coleman F, Koenig C, DeVries D, Gardner C, Chanton J (2012) Flux by fin: fish mediated carbon and nutrient flux in the northeastern Gulf of Mexico. Mar Biol 159:365–372

    Article  CAS  Google Scholar 

  • Newsome SD, Martinez C, del Rio S, Bearhop DL, Phillips (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436

    Article  Google Scholar 

  • Nyunja J, Ntiba M, Onyari J, Mavuti K, Soetaert K, Bouillon S (2009) Carbon sources supporting a diverse fish community in a tropical coastal ecosystem (Gazi Bay, Kenya). Estuar Coast Shelf Sci 83(2009):333–341

    Article  CAS  Google Scholar 

  • Olin JA, Hussey NE, Fritts MW, Heupel MR, Simpfendorfer CA, Poulakis GA, Fisk AT (2011) Maternal meddling in neonatal sharks: implications for interpreting stable isotopes for young animals. Rapid Commun Mass Spectrom 25:1008–1016

    Article  CAS  PubMed  Google Scholar 

  • Olin JA, Hussey NE, Grgicak-Mannion A, Fritts MW, Wintner SP, Fisk AT (2013) Variable δ15N diet-tissue discrimination factors among sharks: implications for trophic position, diet and food web models. Plos One 8:1–11

    Article  CAS  Google Scholar 

  • Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, 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

    Article  Google Scholar 

  • Papastamatiou YP, Wetherbee BM, Lowe CG, Crow GL (2006) Distribution and diet of four species of carcharhinid shark in the Hawaiian Islands: evidence for resource partitioning and competitive exclusion. Mar Ecol Prog Ser 320:239–251

    Article  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. Plos One 5:1–5

    Google Scholar 

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

    Article  Google Scholar 

  • Peterson CT, Grubbs RD (2020) Distribution and abdunance of elasmobranchs and large teleost fishes in a subtropical seasgrass ecosystem: community structure along environmental and spatial gradients. Environ Biol Fishes 103:319–338

  • Peterson CT, Grubbs RD, Mickle A (2017) An investigation of effects of the Deepwater Horizon oil spill on coastal fishes in the Florida Big Bend using fishery-independent surveys and stable isotope analysis. Southeast Nat 16:G93–G108

    Article  Google Scholar 

  • Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231

    Article  Google Scholar 

  • Plumlee JD, Wells RDJ (2016) Feeding ecology of three coastal shark species in the northwest Gulf of Mexico. Mar Ecol Prog Ser 550:163–174

    Article  CAS  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (ISBN 3-900051-07-0, http://www.R-project.org/)

  • Radabaugh KR, Hollander DJ, Peebles EB (2013) Seasonal d13C and d15N isoscapes of fish populations along a continental shelf trophic gradient. Cont Shelf Res 68:112–122

    Article  Google Scholar 

  • Rooney N, McCann KS (2012) Integrating food web diversity, structure and stability. Trends Ecol Evol 27:40–46

    Article  PubMed  Google Scholar 

  • Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269

    Article  CAS  PubMed  Google Scholar 

  • Scharf FS, Juanes F, Rountree RA (2000) Predator size - prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic niche-breadth. Mar Ecol Prog Ser 208:229–248

    Article  Google Scholar 

  • Shaw AL, Frazier BS, Kucklick JR, Sancho G (2016) Trophic ecology of a predatory community in a shallow-water, high salinity estuary assessed by stable isotope analysis. Mar Coast Fish 8:46–61

    Article  Google Scholar 

  • Short F, Carruthers T, Dennison W, Waycott M (2007) Global seagrass distribution and diversity: a bioregional model. J Exp Mar Biol Ecol 350:3–20

    Article  Google Scholar 

  • Syvaranta J, Lensu A, Marjomaki TJ, Oksanen S, Jones RI (2013) An empirical evaluation of the utility of convex hull and standard ellipse areas for assessing population niche widths from stable isotope data. Plos One 8:1–8

    Article  CAS  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (1999) Consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395–1404

    Article  Google Scholar 

  • Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet and δ15N enrichment: a meta-analysis. Oecologia 136:169–182

    Article  PubMed  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Fourth Edition. Springer, New York

  • Vonk JA, Christianenm MJA, Stapel J (2008) Redefining the trophic importance of seagrasses for fauna in tropical Indo-Pacific meadows. Estuar Coast Mar Sci 79:653–660

    Article  Google Scholar 

  • Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. PNAS 106:12377–12381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yarbro LA, Carlson PR Jr., (eds) (2016) Seagrass Integrated Mapping and Monitoring Program: Mapping and Monitoring Report No. 2. Fish and Wildlife Research Institute Technical Report TR-17 version 2. vi + 281 p

  • Yarbro LA, Carlson PR Jr, Jones T, Brucker J, Letendre J (2016) Summary report for the southern Big Bend region. pp. 118–131, in L. A. Yarbro and P. R. Carlson Jr., eds. Seagrass Integrated Mapping and Monitoring Report No. 2. Fish and Wildlife Research Institute Technical Report TR-17, version 2. Florida Fish and Wildlife Conservation Commission, St. Petersburg. 281 p. https://doi.org/10.13140/RG.2.2.12366.05445

  • Zieman JC, Zieman RT (1989) The ecology of the seagrass meadows of the west coast of Florida: a community profile. US Fish Wildlife Service Biological Report 85(7.25):155 pp

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Acknowledgements

We would like to acknowledge the many volunteers without whom this work would not be possible, particularly Mariah Pfleger and Travis Richards. We also thank Jeff Chanton and Alex Harper for graciously sharing data with us. We thank the staff at the FSU Coastal and Marine Laboratory, and the National High Magnetic Field Laboratory. Finally, we acknowledge our funding sources: NOAA National Marine Fisheries Service, the Guy Harvey Ocean Foundation, and Florida Sea Grant.

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Correspondence to Cheston T. Peterson.

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Peterson, C.T., Grubbs, R.D. & Mickle, A. Trophic ecology of elasmobranch and teleost fishes in a large subtropical seagrass ecosystem (Florida Big Bend) determined by stable isotope analysis. Environ Biol Fish 103, 683–701 (2020). https://doi.org/10.1007/s10641-020-00976-7

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