Habitat fragmentation differentially affects trophic levels and alters behavior in a multi-trophic marine system


Seagrass, an important subtidal marine ecosystem, is being lost at a rate of 110 km2 year−1, leading to fragmented seagrass seascapes. Habitat fragmentation is predicted to affect trophic levels differently, with higher trophic levels being more sensitive, stressing the importance of a multi-trophic perspective. Utilizing the trophic relationship between the blue crab (Callinectes sapidus) and hard clam (Mercenaria mercenaria), where adult blue crabs prey on juvenile blue crabs, and juvenile blue crabs prey on small hard clams, we examined whether predation rates, abundance, and behavior of predators and prey differed between continuous and fragmented seagrass in a multi-trophic context at two sites in Barnegat Bay, NJ. We tested the hypothesis that fragmented habitats would differentially affect trophic levels within a tri-trophic system, and our results supported this hypothesis. Densities of adult blue crabs were higher in fragmented than continuous habitats. Densities of juvenile blue crabs, the primary predator of hard clams, were lower in fragmented habitats than continuous, potentially due to increased predation by adult blue crabs. Clams experienced lower predation and burrowed to a shallower depth in fragmented habitats than in continuous habitat, likely due in part to the low densities of juvenile blue crabs, their primary predator. Our results suggest that while trophic levels are differentially affected, the impact of habitat fragmentation may be stronger on intermediate rather than top trophic levels in some marine systems.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. Airoldi L, Balata D, Beck MW (2008) The gray zone: relationships between habitat loss and marine diversity and their applications in conservation. J Exp Mar Biol Ecol 366:8–15

  2. Arnold WS (1984) The effects of prey size, predator size, and sediment composition on the rate of predation of the blue crab, Callinectes sapidus rathbun, on the hard clam, Mercenaria mercenaria (Linné). J Exp Mar Biol Ecol 80:207–219

  3. Beck MW, Heck Jr KL, Able KW, Childers DL, Eggleston DB, Gillanders BM, Orth RJ (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates: a better understanding of the habitats that serve as nurseries for marine species and the factors that create site-specific variability in nursery quality will improve conservation and management of these areas. Bioscience 51:633–641

  4. Bernot RJ, Turner AM (2001) Predator identity and trait-mediated indirect effects in a littoral food web. Oecologia 129:139–146

  5. Bologna PAX, Heck KL (1999) Differential predation and growth rates of bay scallops within a seagrass habitat. J Exp Mar Biol Ecol 239:299–314

  6. Boström C, Jackson EL, Simenstad CA (2006) Seagrass landscapes and their effects on associated fauna: a review. Estuar Coast Shelf Sci 68:383–403

  7. Brückmann SV, Krauss J, van Achterberg C, Steffan-Dewenter I (2011) The impact of habitat fragmentation on trophic interactions of the monophagous butterfly Polyommatus coridon. J Insect Conserv 15:707–714

  8. Burkholder DA, Heithaus MR, Fourqurean JW, Wirsing A, Dill LM (2013) Patterns of top-down control in a seagrass ecosystem: could a roving apex predator induce a behaviour-mediated trophic cascade? J Anim Ecol 82:1192–1202

  9. Canion CR, Heck Jr KL (2009) Effect of habitat complexity on predation success: re-evaluating the current paradigm in seagrass beds. Mar Ecol Prog Ser 393:37–46

  10. Carroll J, Furman BT, Tettelbach ST, Peterson BJ (2012) Balancing the edge effects budget: bay scallop settlement and loss along a seagrass edge. Ecology 93:1637–1647

  11. Casini M, Blenckner T, Möllmann C, Gårdmark A, Lindegren M, Llope M, Kornilovs G, Plikshs M, Stenseth NC (2012) Predator transitory spillover induces trophic cascades in ecological sinks. Proc Natl Acad Sci USA 109:8185–8189

  12. Christian RR, Luczkovich JJ (1999) Organizing and understanding a winter’s seagrass foodweb network through effective trophic levels. Ecol Model 117:99–124

  13. Costanza R, d’Arge R, Limburg K, Grasso M, de Groot R, Faber S, O’Neill RV, Van den Belt M, Paruelo J, Raskin RG, Hannon B (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

  14. Crist TO, Pradhan-Devare SV, Summerville KS (2006) Spatial variation in insect community and species responses to habitat loss and plant community composition. Oecologia 147:510–521

  15. Davies KF, Margules CR, Lawrence JF (2000) Which traits of species predict population declines in experimental forest fragments. Ecology 81:1450–1461

  16. Didham RK, Lawton JH, Hammond PM, Eggleton P (1998) Trophic structure stability and extinction dynamics of beetles (Coleoptera) in tropical forest fragments. Philos Trans R Soc Lond B Biol Sci 353:437–451

  17. Dill LM, Heithaus MR, Walters CJ (2003) Behaviorally mediated indirect interactions in marine communities and their conservation implications. Ecology 84:1151–1157

  18. Dittel AI, Hines AH, Ruiz GM, Ruffin KK (1995) Effects of shallow water refuge on behavior and density-dependent mortality of juvenile blue crabs in Chesapeake Bay. Bull Mar Sci 57:902–916

  19. Duffy JE (2003) Biodiversity loss, trophic skew and ecosystem functioning. Ecol Lett 6:680–687

  20. Duffy JE, Richardson PJ, Canuel EA (2003) Grazer diversity effects on ecosystem functioning in seagrass beds. Ecol Lett 6:637–645

  21. Dyer LA, Letourneau D (2003) Top-down and bottom-up diversity cascades in detrital vs. living food webs. Ecol Lett 6:60–68

  22. Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JB, Marquis RJ (2011) Trophic downgrading of planet Earth. Science 333:301–306

  23. Eversole AG (1987) Species Profiles: Life Histories and Environmental Requirements of Coastal Fishes and Invertebrates (South Atlantic) Hard Clam. Clemson University, Clemson

  24. Fagan WF, Cantrell RS, Cosner C (1999) How habitat edges change species interactions. Am Nat 153:165–182

  25. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

  26. Flynn AM, Smee DL (2010) Behavioral plasticity of the soft-shell clam, Mya arenaria (L.), in the presence of predators increases survival in the field. J Exp Mar Biol Ecol 383:32–38

  27. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596

  28. Heck KL, Thoman TA (1981) Experiments on predator–prey interactions in vegetated aquatic habitats. J Exp Mar Biol Ecol 53:125–134

  29. Heck KL, Hays G, Orth RJ (2003) Critical evaluation of the nursery role hypothesis for seagrass meadows. Mar Ecol Prog Ser 253:123–136

  30. Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210

  31. Hemminga MA, Duarte CM (2000) Seagrass ecology. Cambridge University Press, Cambridge

  32. Hines AH, Ruiz GM (1995) Temporal variation in juvenile blue crab mortality: nearshore shallows and cannibalism in Chesapeake Bay. Bull Mar Sci 57:884–901

  33. Hines AH, Wolcott TG, González-Gurriarán E, González-Escalante JL, Freire J (1995) Movement patterns and migrations in crabs: telemetry of juvenile and adult behaviour in Callinectes sapidus and Maja squinado. J Mar Biol Assoc UK 75:27–42

  34. Hovel KA (2003) Habitat fragmentation in marine landscapes: relative effects of habitat cover and configuration on juvenile crab survival in California and North Carolina seagrass beds. Biol Conserv 110(3):401–412

  35. Hovel KA, Fonseca MS (2005) Influence of seagrass landscape structure on the juvenile blue crab habitat-survival function. Mar Ecol Prog Ser 300:179–191

  36. Hovel KA, Lipcius RN (2001) Habitat fragmentation in a seagrass landscape: patch size and complexity control blue crab survival. Ecology 82:1814–1829

  37. Hovel KA, Lipcius RN (2002) Effects of seagrass habitat fragmentation on juvenile blue crab survival and abundance. J Exp Mar Biol Ecol 271:75–98

  38. Hovel KA, Regan HM (2008) Using an individual-based model to examine the roles of habitat fragmentation and behavior on predator–prey relationships in seagrass landscapes. Landsc Ecol 23:75–89

  39. Irlandi EA (1994) Large-and small-scale effects of habitat structure on rates of predation: how percent coverage of seagrass affects rates of predation and siphon nipping on an infaunal bivalve. Oecologia 98:176–183

  40. Irlandi EA (1997) Seagrass patch size and survivorship of an infaunal bivalve. Oikos 78:511–518

  41. Johnson MW, Heck KL (2006) Seagrass patch characteristics alter direct and indirect interactions in a tritrophic estuarine food web. Estuar Coasts 29:499–510

  42. Kareiva P (1987) Habitat fragmentation and the stability of predator–prey interactions. Nature 326:388–390

  43. Kennish MJ, Haag SM, Sakowicz GP (2009) Assessment of eutrophication in the Barnegat Bay-Little Egg Harbor system: use of SAV biotic indicators of estuarine condition. N J Environ Digit Lib. doi:10.7282/T3Z60NVX

  44. Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020

  45. Krauss J, Bommarco R, Guardiola M, Heikkinen RK, Helm A, Kuussaari M, Lindborg R (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol Lett 13:597–605

  46. Layman CA, Quattrochi JP, Peyer CM, Allgeier JE (2007) Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol Lett 10:937–944

  47. Ljungberg P, Hasper TB, Nilsson PA, Persson A (2013) Effects of small-scale habitat fragmentation on predator–prey interactions in a temperate sea grass system. Mar Biol 160:667–675

  48. Macreadie PI, Hindell JS, Jenkins GP, Connolly RM, Keough MJ (2009) Fish responses to experimental fragmentation of seagrass habitat. Conserv Biol 23:644–652

  49. Macreadie PI, Geraldi NR, Peterson CH (2012) Preference for feeding at habitat edges declines among juvenile blue crabs as oyster reef patchiness increases and predation risk grows. Mar Ecol Prog Ser 466:145–153

  50. Martinson HM, Fagan WF, Denno RF (2012) Critical patch sizes for food-web modules. Ecology 93:1779–1786

  51. Millennium Ecosystem Assessment (2005) Ecosystems and human well-being. World Resources Institute, Washington

  52. Moksnes PO, Lipcius RN, Pihl L, van Montfrans J (1997) Cannibal–prey dynamics in young juveniles and postlarvae of the blue crab. J Exp Mar Biol Ecol 215:157–187

  53. New York State Department of Environmental Conservation (2009) Final report of the New York State seagrass taskforce: recommendations to the New York State Governor and legislature

  54. Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996

  55. Paine RT (2002) Trophic control of production in a rocky intertidal community. Science 296:736–739

  56. Peterson BJ, Thompson KR, Cowan JH, Heck KL (2001) Comparison of predation pressure in temperate and subtropical seagrass habitats based on chronographic tethering. Mar Ecol Prog Ser 224:77–85

  57. Ramach S, Darnell MZ, Avissar N, Rittschof D (2009) Habitat use and population dynamics of blue crabs, Callinectes sapidus, in a high-salinity embayment. J Shellfish Res 28:635–640

  58. Ries L, Fletcher Jr RJ, Battin J, Sisk TD (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu Rev Ecol Evol Syst 35:491–522

  59. Roberts D, Rittschof D, Gerhart DJ, Schmidt AR, Hill LG (1989) Vertical migration of the clam Mercenaria mercenaria (L.) (Mollusca: Bivalvia): environmental correlates and ecological significance. J Exp Mar Biol Ecol 126:271–280

  60. Roslin T, Várkonyi G, Koponen M, Vikberg V, Nieminen M (2014) Species–area relationships across four trophic levels–decreasing island size truncates food chains. Ecography 37:443–453

  61. SAS Institute (2000) JMP®, Version 11, 1989–2007. SAS Institute Inc., Cary

  62. Scoffin TP (1970) The trapping and binding of subtidal carbonate sediments by marine vegetation in Bimini lagoon, Bahamas. J Sediment Res 40:249–273

  63. Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD, BS Halpern (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791

  64. Shurin JB, Gruner DS, Hillebrand H (2006) All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc R Soc B 273:1–9

  65. Speir H (1999) A review of predation on blue crabs in Chesapeake Bay. Maryland Department of Natural Resources, Annapolis

  66. Tait KJ, Hovel KA (2012) Do predation risk and food availability modify prey and mesopredator microhabitat selection in eelgrass (Zostera marina) habitat? J Exp Mar Biol Ecol 426:60–67

  67. Tapia-Lewin S, Pardo LM (2014) Field assessment of the predation risk-food availability trade-off in crab megalopae settlement. PLoS One 9:e95335

  68. Tigas LA, Van Vuren DH, Sauvajot RM (2002) Behavioral responses of bobcats and coyotes to habitat fragmentation and corridors in an urban environment. Biol Conserv 108:299–306

  69. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845

  70. Tscharntke T, Brandl R (2004) Plant-insect interactions in fragmented landscapes. Annu Rev Entomol 49:405–430

  71. Valladares G, Salvo A, Cagnolo L (2006) Habitat fragmentation effects on trophic processes of insect-plant food webs. Conserv Biol 20:212–217

  72. van Nouhuys S (2005) Effects of habitat fragmentation at different trophic levels in insect communities. Ann Zool Fenn 42:433–447

  73. Waycott M, Duarte CM, Carruthers TJ, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci USA 106:12377–12381

  74. Wimp GM, Murphy SM, Lewis D, Ries L (2011) Do edge responses cascade up or down a multi-trophic food web? Ecol Lett 14:863–870

  75. Zabel J, Tscharntke T (1998) Does fragmentation of Urtica habitats affect phytophagous and predatory insects differentially. Oecologia 116:419–425

Download references


We thank K. Bezik, C. Hines, R. Kwait, J. Linnell, D. Lopez, and B. Smith for laboratory and field assistance, K. Bezik for video analysis, Island Beach State Park, NJ for accommodating our research, Parsons Seafood Inc. for donating hard clam seed, and E. Cordes, M. Russell, and R. Sanders for useful feedback during the development of the project and manuscript. This study was supported by a Temple University Fellowship, and the National Science Foundation Division of Ocean Sciences Grants 1225583 and 1434528.

Author contribution statement

EWR and ALF conceived and designed the experiments. EWR performed the experiments and analyzed the data. EWR and ALF wrote the manuscript.

Author information

Correspondence to Elizabeth Rielly-Carroll.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interest.

Additional information

Communicated by Joel Trexler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (MPG 25236 kb). Video of blue crab foraging on prey item in continuous seagrass.

Supplementary material 1 (MPG 25236 kb). Video of blue crab foraging on prey item in continuous seagrass.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rielly-Carroll, E., Freestone, A.L. Habitat fragmentation differentially affects trophic levels and alters behavior in a multi-trophic marine system. Oecologia 183, 899–908 (2017).

Download citation


  • Habitat loss
  • Seagrass
  • Blue crabs
  • Fragmentation
  • Food webs