Marine Biology

, 164:54 | Cite as

How does a restored oyster reef develop? An assessment based on stable isotopes and community metrics

  • Ryan J. Rezek
  • Benoit Lebreton
  • E. Brendan Roark
  • Terence A. Palmer
  • Jennifer Beseres PollackEmail author
Original paper


Oyster reefs host complex food webs, as their three-dimensional biogenic structure provides habitat for a diverse range of invertebrates and fish. Oyster reefs have suffered severe degradation due to anthropogenic activities. Restoration projects aim to mitigate this habitat loss. We compared the development of a restored subtidal oyster reef to that of a natural reef for 29 months by assessing (1) community metrics (e.g., biomass, diversity), (2) the stable isotope composition of food sources and consumers, and (3) biomass-weighted isotopic diversity indices. A clear shift in restored reef community composition occurred 12–15 months after restoration, moving from a community dominated by opportunistic species to a more diverse and evenly distributed community, similar to that of the natural reef. Consumer stable isotope values indicated that the restored reef community was supported by similar food resources and had similar food chain length as the natural reef community by 5-month post-restoration. However, biomass-weighted isotopic diversity indices indicated that the magnitude of the main trophic pathways and characteristics of food web complexity in the restored reef did not recover to natural reef levels until 12–15 months after construction. The functional recovery of the restored reef community was driven by the homogenization of biomass distribution among trophic compartments as oysters and top predators increasingly colonized the reef. Results indicate that oyster reef restoration can support food web functions like those provided by natural reefs. We also demonstrate the importance of combining food web and community structure information in the study of ecological functioning.


Shell Height Suspension Feeder Oyster Reef Natural Reef Suspend Particulate Organic Matter 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Funding for this project was provided by FishAmerica Foundation and the NOAA Community-Based Restoration Program (Grant No. FAF-11030), the Texas General Land Office Coastal Management Program, and The Ruth Campbell Fellowship at Texas A&M University-Corpus Christi. The authors gratefully acknowledge Patrick Graham, Kevin De Santiago, Eric White, Gaël Guillou, and Dr. Paula Rose for their assistance in the field and the laboratory, Dr. Kim Withers for assistance with species identification, and Dr. Blair Sterba-Boatwright for statistical guidance. We also thank four anonymous reviewers for providing insights and suggestions that greatly improved the quality of this study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2017_3084_MOESM1_ESM.docx (33 kb)
Supplementary material 1 (DOCX 33 KB)
227_2017_3084_MOESM2_ESM.docx (15 kb)
Supplementary material 2 (DOCX 14 KB)


  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi: 10.1046/j.1442-9993.2001.01070.x Google Scholar
  2. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253. doi: 10.1111/j.1541-0420.2005.00440.x CrossRefGoogle Scholar
  3. Armstrong NE (1987) The ecology of open-bay bottoms of Texas: a community profile. Fish and Wildlife Service No. FWS-8, Washington DCGoogle Scholar
  4. Baggett LP, Powers SP, Brumbaugh RD, Coen LD, DeAngelis BM, Greene JK, Hancock BT, Morlock SM, Allen BL, Breitburg DL, Bushek D, Grabowski JH, Grizzle RE, Grosholz ED, La Peyre MK, Luckenbach MW, McGraw KA, Piehler MF, Westby SR, zu Ermgassen PSE (2015) Guidelines for evaluating performance of oyster habitat restoration. Restor Ecol 23:737–745. doi: 10.1111/rec.12262 CrossRefGoogle Scholar
  5. Barillé L, Prou J, Héral M, Razet D (1997) Effects of high natural seston concentrations on the feeding, selection, and absorption of the oyster Crassostrea gigas (Thunberg). J Exp Mar Bio Ecol 212:149–172. doi: 10.1016/S0022-0981(96)02756-6 CrossRefGoogle Scholar
  6. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. doi: 10.18637/jss.v067.i01
  7. Beseres Pollack J, Kim H-C, Morgan EK, Montagna PA (2011) Role of flood disturbance in natural oyster (Crassostrea virginica) population maintenance in an estuary in south Texas, USA. Estuar Coast 34(1):187–197. doi: 10.1007/s12237-010-9338-6 CrossRefGoogle Scholar
  8. Beseres Pollack J, Cleveland A, Palmer TA, Reisinger AS, Montagna PA (2012) A restoration suitability index model for the eastern oyster (Crassostrea virginica) in the Mission-Aransas Estuary, TX, USA. PLoS One 7:e40839. doi: 10.1371/journal.pone.0040839 CrossRefGoogle Scholar
  9. Beseres Pollack J, Yoskowitz D, Kim H-C, Montagna PA (2013) Role and value of nitrogen regulation provided by oysters (Crassostrea virginica) in the Mission-Aransas Estuary, Texas, USA. PLoS One 8:e65314. doi: 10.1371/journal.pone.0065314 CrossRefGoogle Scholar
  10. Blomberg BN (2015) Evaluating success of oyster reef restoration. Dissertation, Texas A&M University, Corpus ChristiGoogle Scholar
  11. Brind’Amour A, Dubois SF (2013) Isotopic diversity indices: how sensitive to food web structure? PLoS One. doi: 10.1371/journal.pone.0084198
  12. Caine EA (1975) Feeding and masticatory structures of selected Anomura (Crustacea). J Exp Mar Bio Ecol 18:277–301. doi: 10.1016/0022-0981(75)90112-4 CrossRefGoogle Scholar
  13. Canty A, Ripley B (2016) Boot: Bootstrap R (S-Plus) functions. R Package version 1.3–18Google Scholar
  14. Cifuentes LA, Sharp JH, Fogel ML (1988) Stable carbon and nitrogen isotope biogeochemistry in the Delaware Estuary. Limnol Oceanogr 33:1102–1115. doi: 10.4319/lo.1988.33.5.1102 CrossRefGoogle Scholar
  15. Clarke KR, Warwick RM (2001) Changes in marine communities: an approach to statistical analysis and interpretation. Plymouth Marine Laboratory, PlymouthGoogle Scholar
  16. Coen LD, Luckenbach MW (2000) Developing success criteria and goals for evaluating oyster reef restoration: ecological function or resource exploitation? Ecol Eng 15:323–343. doi: 10.1016/S0925-8574(00)00084-7 CrossRefGoogle Scholar
  17. Coen L, Luckenbach M, Breitburg D (1999) The role of oyster reefs as essential fish habitat: a review of current knowledge and some new perspectives. Fish Habitat Essent Fish Habitat Rehabil 22:438–454Google Scholar
  18. Colden AM, Fall KA, Cartwright GM, Friedrichs CT (2016) Sediment suspension and deposition across restored oyster reefs of varying orientation to flow: implications for restoration. Estuar Coast 39:1435–1448CrossRefGoogle Scholar
  19. Cucherousset J, Villéger S (2015) Quantifying the multiple facets of isotopic diversity: new metrics for stable isotope ecology. Ecol Indic 56:152–160. doi: 10.1016/j.ecolind.2015.03.032 CrossRefGoogle Scholar
  20. Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655CrossRefGoogle Scholar
  21. Dillon K, Peterson M, May C (2015) Functional equivalence of constructed and natural intertidal eastern oyster reef habitats in a northern Gulf of Mexico estuary. Mar Ecol Prog Ser 528:187–203. doi: 10.3354/meps11269 CrossRefGoogle Scholar
  22. Dinno A (2016) Dunn.test: Dunn’s test of multiple comparisons using rank sums. R package version 1.3.2. Accessed June 2016
  23. Duffy JE (2003) Biodiversity loss, trophic skew and ecosystem functioning. Ecol Lett 6:680–687. doi: 10.1046/j.1461-0248.2003.00494.x
  24. Dunn OJ (1964) Multiple comparisons using rank sums. Technometrics 6:241–252. doi: 10.1080/00401706.1964.10490181 CrossRefGoogle Scholar
  25. Flemer DA, Champ MA (2006) What is the future fate of estuaries given nutrient over-enrichment, freshwater diversion and low flows? Mar Pollut Bull 52:247–258. doi: 10.1016/j.marpolbul.2005.11.027 CrossRefGoogle Scholar
  26. Fry B, Sherr EB (1989) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. In: Stable isotopes in ecological research. Springer, New York, pp 196–229CrossRefGoogle Scholar
  27. Gaston GR, Cleveland CM, Brown SS, Rakocinski CF (1997) Benthic-pelagic coupling in northern Gulf of Mexico estuaries: Do benthos feed directly on phytoplankton? Gulf Res Rep 9:231–237. doi: 10.18785/grr.0904.02 Google Scholar
  28. Glancy TP, Frazer TK, Cichra CE, Lindberg WJ (2003) Comparative patterns of occupancy by decapod crustaceans in seagrass, oyster, and marsh-edge habitats in a Northeast Gulf of Mexico estuary. Estuaries 26:1291–1301. doi: 10.1007/BF02803631 CrossRefGoogle Scholar
  29. Grabowski JH (2004) Habitat complexity disrupts predator–prey interactions but not the trophic cascade on oyster reefs. Ecology 85:995–1004. doi: 10.1890/03-0067 CrossRefGoogle Scholar
  30. Grabowski JH, Powers S (2004) Habitat complexity mitigates trophic transfer on oyster reefs. Mar Ecol Prog Ser 277:291–295. doi: 10.3354/meps277291 CrossRefGoogle Scholar
  31. Grabowski JH, Brumbaugh RD, Conrad RF, Keeler AG, Opaluch JJ, Peterson CH, Piehler MF, Powers SP, Smyth AR (2012) Economic valuation of ecosystem services provided by oyster reefs. Bioscience 62:900–909. doi: 10.1525/bio.2012.62.10.10 CrossRefGoogle Scholar
  32. Graham PM, Palmer TA, Beseres Pollack J (2016) Oyster reef restoration: substrate suitability may depend on specific restoration goals. Restor Ecol. doi: 10.1111/rec.12449 Google Scholar
  33. Gregalis KC, Powers SP, Heck KL (2008) Restoration of oyster reefs along a bio-physical gradient in Mobile Bay, Alabama. J Shellfish Res 27:1163–1169. doi: 10.2983/0730-8000-27.5.1163 CrossRefGoogle Scholar
  34. Griffen BD, Mosblack H (2011) Predicting diet and consumption rate differences between and within species using gut ecomorphology. J Anim Ecol 80:854–863. doi: 10.1111/j.1365-2656.2011.01832.x CrossRefGoogle Scholar
  35. Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910. doi: 10.1046/j.1365-2745.1998.00306.x CrossRefGoogle Scholar
  36. Grizzle RE, Greene JK, Coen LD (2008) Seston removal by natural and constructed intertidal eastern oyster (Crassostrea virginica) reefs: a comparison with previous laboratory studies, and the value of in situ methods. Estuar Coasts 31:1208–1220. doi: 10.1007/s12237-008-9098-8 CrossRefGoogle Scholar
  37. Harding J, Mann R (2001) Oyster reefs as fish habitat: opportunistic use of restored reefs by transient fishes. J Shellfish Res 20:951–959Google Scholar
  38. Hoeinghaus DJ, Zeug SC (2008) Can stable isotope ratios provide for community-wide measures of trophic structure? Comment. Ecology 89:2353–2357. doi: 10.1890/07-1143.1 CrossRefGoogle Scholar
  39. Hoellein TJ, Zarnoch CB, Grizzle RE (2015) Eastern oyster (Crassostrea virginica) filtration, biodeposition, and sediment nitrogen cycling at two oyster reefs with contrasting water quality in Great Bay Estuary (New Hampshire, USA). Biogeochemistry 122:113–129. doi: 10.1007/s10533-014-0034-7 CrossRefGoogle Scholar
  40. Hollebone A, Hay M (2007) Population dynamics of the non-native crab Petrolisthes armatus invading the South Atlantic Bight at densities of thousands m−2. Mar Ecol Prog Ser 336:211–223. doi: 10.3354/meps336211 CrossRefGoogle Scholar
  41. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363. doi: 10.1002/bimj.200810425 CrossRefGoogle Scholar
  42. Humphries AT, La Peyre MK (2015) Oyster reef restoration supports increased nekton biomass and potential commercial fishery value. PeerJ 3:e1111. doi: 10.7717/peerj.1111 CrossRefGoogle Scholar
  43. 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. doi: 10.1111/j.1365-2656.2011.01806.x CrossRefGoogle Scholar
  44. Jackson MC, Donohue I, Jackson AL, Britton RJ, Harper DM, Grey J (2012) Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS One 7:e31757. doi: 10.1371/journal.pone.0031757 CrossRefGoogle Scholar
  45. Johnson KD, Smee DL (2014) Predators influence the tidal distribution of oysters (Crassostrea virginica). Mar Biol 161:1557–1564. doi: 10.1007/s00227-014-2440-8 CrossRefGoogle Scholar
  46. Kang C-K, Park HJ, Choy EJ, Choi K-S, Hwang K, Kim J-B (2015) Linking intertidal and subtidal food webs: consumer-mediated transport of intertidal benthic microalgal carbon. PLoS One 10:e0139802. doi: 10.1371/journal.pone.0139802 CrossRefGoogle Scholar
  47. Kirby MX (2004) Fishing down the coast: historical expansion and collapse of oyster fisheries along continental margins. Proc Natl Acad Sci 101:13096–13099. doi: 10.1073/pnas.0405150101 CrossRefGoogle Scholar
  48. La Peyre MK, Humphries AT, Casas SM, La Peyre JF (2014) Temporal variation in development of ecosystem services from oyster reef restoration. Ecol Eng 63:34–44. doi: 10.1016/j.ecoleng.2013.12.001 CrossRefGoogle Scholar
  49. Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community wide measures of trophic structure? Ecology 88:42–48. doi: 10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2
  50. Lebreton B, Beseres Pollack J, Blomberg B, Palmer TA, Adams L, Guillou G, Montagna PA (2016) Origin, composition and quality of suspended particulate organic matter in relation to freshwater inflow in a South Texas estuary. Estuar Coast Shelf Sci 170:70–82. doi: 10.1016/j.ecss.2015.12.024 CrossRefGoogle Scholar
  51. Lehnert RL, Allen DM (2002) Nekton use of subtidal oyster shell habitat in a Southeastern U.S. estuary. Estuaries 25:1015–1024. doi: 10.1007/BF02691348
  52. Lefebvre S, Marín Leal JC, Dubois S, et al (2009) Seasonal dynamics of trophic relationships among co-occurring suspension-feeders in two shellfish culture dominated ecosystems. Estuar Coast Shelf Sci 82:415–425. doi: 10.1016/j.ecss.2009.02.002
  53. Lotze HK, Lenihan H, Bourque B, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–1809. doi: 10.1126/science.1128035 CrossRefGoogle Scholar
  54. MacIntyre H, Cullen J (1996) Primary production by suspended and benthic microalgae in a turbid estuary: time-scales of variability in San Antonio Bay, Texas. Mar Ecol Prog Ser 145:245–268. doi: 10.3354/meps145245 CrossRefGoogle Scholar
  55. MacIntyre HL, Geider RJ, Miller DC (1996) Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 19:186. doi: 10.2307/1352224 CrossRefGoogle Scholar
  56. Martínez del Río C, Wolf B (2005) Mass-balance models for animal isotopic ecology. Science Publishers, EnfieldGoogle Scholar
  57. McGlaun K, Withers K (2012) Metabolism, consumption rates, and scope for growth of porcelain crab (Petrolisthes galathinus). Gulf Mex Sci 30:1–6Google Scholar
  58. Mooney RF, McClelland JW (2012) Watershed export events and ecosystem responses in the Mission–Aransas National Estuarine Research Reserve, South Texas. Estuar Coasts 35:1468–1485. doi: 10.1007/s12237-012-9537-4 CrossRefGoogle Scholar
  59. Nevins JA, Pollack JB, Stunz GW (2014) Characterizing nekton use of the largest unfished oyster reef in the United States compared with adjacent estuarine habitats. J Shellfish Res 33:227–238. doi: 10.2983/035.033.0122 CrossRefGoogle Scholar
  60. Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23:51–61Google Scholar
  61. NOAA National Estuarine Research Reserve System (NERRS) (2016) System-wide monitoring program. Data accessed from the NOAA NERRS Centralized Data Management Office. Accessed 12 Jan 2016
  62. Nordström MC, Demopoulos AWJ, Whitcraft CR et al (2015) Food web heterogeneity and succession in created saltmarshes. J Appl Ecol 52:1343–1354. doi: 10.1111/1365-2664.12473 CrossRefGoogle Scholar
  63. Oakley JW, Simons J, Stunz GW (2014) Spatial and habitat-mediated food web dynamics in an oyster-dominated estuary. J Shellfish Res 33:841–855. doi: 10.2983/035.033.0319 CrossRefGoogle Scholar
  64. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320. doi: 10.1146/ CrossRefGoogle Scholar
  65. Peterson C, Grabowski J, Powers S (2003) Estimated enhancement of fish production resulting from restoring oyster reef habitat: quantitative valuation. Mar Ecol Prog Ser 264:249–264. doi: 10.3354/meps264249 CrossRefGoogle Scholar
  66. Posey MH, Hines AH (1991) Complex predator-prey interactions within an estuarine benthic community. Ecology 72:2155–2169. doi: 10.2307/1941567 CrossRefGoogle Scholar
  67. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718. doi: 10.2307/3071875 CrossRefGoogle Scholar
  68. Powers S, Peterson C, Grabowski J, Lenihan H (2009) Success of constructed oyster reefs in no-harvest sanctuaries: implications for restoration. Mar Ecol Prog Ser 389:159–170. doi: 10.3354/meps08164
  69. Quan W, Humphries AT, Shi L, Chen Y (2012) Determination of trophic transfer at a created intertidal oyster (Crassostrea ariakensis) reef in the Yangtze River Estuary using stable isotope analyses. Estuar Coasts 35:109–120. doi: 10.1007/s12237-011-9414-6 CrossRefGoogle Scholar
  70. Quillien N, Nordström MC, Schaal G et al (2016) Opportunistic basal resource simplifies food web structure and functioning of a highly dynamic marine environment. J Exp Mar Bio Ecol 477:92–102. doi: 10.1016/j.jembe.2016.01.010 CrossRefGoogle Scholar
  71. R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
  72. Reise K (2002) Sediment mediated species interactions in coastal waters. J Sea Res 48:127–141. doi: 10.1016/S1385-1101(02)00150-8 CrossRefGoogle Scholar
  73. Rigolet C, Thiébaut E, Brind’Amour A, Dubois SF (2015) Investigating isotopic functional indices to reveal changes in the structure and functioning of benthic communities. Funct Ecol 29:1350–1360. doi: 10.1111/1365-2435.12444 CrossRefGoogle Scholar
  74. Riisgård H, Larsen P (2010) Particle capture mechanisms in suspension-feeding invertebrates. Mar Ecol Prog Ser 418:255–293. doi: 10.3354/meps08755 CrossRefGoogle Scholar
  75. Rodney WS, Paynter KT (2006) Comparisons of macrofaunal assemblages on restored and non-restored oyster reefs in mesohaline regions of Chesapeake Bay in Maryland. J Exp Mar Bio Ecol 335:39–51. doi: 10.1016/j.jembe.2006.02.017 CrossRefGoogle Scholar
  76. Rothschild B, Ault J, Goulletquer P, Héral M (1994) Decline of the Chesapeake Bay oyster population: a century of habitat destruction and overfishing. Mar Ecol Prog Ser 111:29–39. doi: 10.3354/meps111029 CrossRefGoogle Scholar
  77. Sagouis A, Cucherousset J, Villéger S, et al. (2015) Non-native species modify the isotopic structure of freshwater fish communities across the globe. Ecography (Cop) 38:979–985. doi: 10.1111/ecog.01348 CrossRefGoogle Scholar
  78. Schulte DM, Burke RP, Lipcius RN (2009) Unprecedented restoration of a native oyster metapopulation. Science 325:1124–1128. doi: 10.1126/science.1176516 CrossRefGoogle Scholar
  79. Shideler GL (1984) Suspended sediment responses in a wind-dominated estuary of the Texas Gulf Coast. J Sediment Petrol 54:731–745. doi: 10.1306/212F84E5-2B24-11D7-8648000102C1865D Google Scholar
  80. Soniat TM, Ray SM, Jeffrey LM (1984) Components of the seston and possible available food for oysters in Galveston Bay, Texas. Contrib Mar Sci 27:127–141Google Scholar
  81. Stunz GW, Minello TJ, Rozas LP (2010) Relative value of oyster reef as habitat for estuarine nekton in Galveston Bay, Texas. Mar Ecol Prog Ser 406:147–159. doi: 10.3354/meps08556 CrossRefGoogle Scholar
  82. Thébault E, Loreau M (2006) The relationship between biodiversity and ecosystem functioning in food webs. Ecol Res 21:17–25. doi: 10.1007/s11284-005-0127-9 CrossRefGoogle Scholar
  83. Tolley SG, Volety AK (2005) The role of oysters in habitat use of oyster reefs by resident fishes and decapod crustaceans. J Shellfish Res 24:1007–1012. doi: 10.2983/0730-8000(2005)24[1007:TROOIH]2.0.CO;2 CrossRefGoogle Scholar
  84. Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066. doi: 10.4319/lo.2001.46.8.2061 CrossRefGoogle Scholar
  85. Yeager LA, Layman CA (2011) Energy flow to two abundant consumers in a subtropical oyster reef food web. Aquat Ecol 45:267–277. doi: 10.1007/s10452-011-9352-1 CrossRefGoogle Scholar
  86. Zimmerman RJ, Minello TJ, Baumer T, Castiglione MC (1989) Oyster reef as habitat for estuarine macrofauna. NOAA technical memorandum, NMFS-SEFC-249Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Ryan J. Rezek
    • 1
  • Benoit Lebreton
    • 2
  • E. Brendan Roark
    • 3
  • Terence A. Palmer
    • 1
  • Jennifer Beseres Pollack
    • 1
  1. 1.Department of Life SciencesTexas A&M University-Corpus ChristiCorpus ChristiUSA
  2. 2.UMR 7266 Littoral Environnement et Sociétés (CNRS-Université de La Rochelle)Institut du Littoral et de l’EnvironnementLa RochelleFrance
  3. 3.Department of GeographyTexas A&M UniversityCollege StationUSA

Personalised recommendations