Contrasting complexity of adjacent habitats influences the strength of cascading predatory effects

Abstract

Although cascading effects of top predators can help structure communities, their influence may vary across habitats that differentially protect prey. Therefore, to understand how and to what degree habitat complexity can affect trophic interactions in adjacent habitats, we used a combination of a broad regional-scale survey, manipulative field trials, and an outdoor mesocosm experiment to quantify predator–prey interaction strengths across four trophic levels. Within estuaries of the southeastern USA, bonnethead sharks (Sphyrna tiburo) hunt blue crabs on mudflats and adjacent oyster reefs, two habitats with vastly different aboveground structure. Using 12-h tethering trials of blue crabs we quantified habitat-dependent loss rates of 37% on reefs and 78% on mudflats. We hypothesized that the sharks’ predatory effects on blue crabs would cascade down to release a lower-level mud crab predator, which subsequently would increase juvenile oyster mortality, but that the cascade strength would be habitat-dependent. We experimentally manipulated predator combinations in split-plot mesocosms containing reef and mudflat habitats, and quantified oyster mortality. Bonnetheads exerted strong consumptive and non-consumptive effects on blue crabs, which ceased eating oysters in the sharks’ presence. However, mud crabs, regardless of shark and blue crab presence, continued to consume oysters, especially within the structural refuge of the reef where they kept oyster mortality high. Thus, bonnetheads indirectly boosted oyster survival, but only on the mudflat where mud crabs were less active. Our work demonstrates how structural differences in adjacent habitats can moderate trophic cascades, particularly when mesopredators exhibit differential use of structure and different sensitivities to top predators.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Belcher CN, Jennings CA (2009) Use of a fishery-independent trawl survey to evaluate distribution patterns of subadult sharks in Georgia. Mar Coast Fish 1:218–229

    Article  Google Scholar 

  2. Bishop MJ, Byers JE (2015) Predation risk predicts use of a novel habitat. Oikos 124:1225–1231

    Article  Google Scholar 

  3. Borer ET et al (2005) What determines the strength of a trophic cascade? Ecology 86:528–537

    Article  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. Byers JE et al (2015) Geographic variation in intertidal oyster reef properties and the influence of tidal prism. Limnol Oceanogr 60:1051–1063

    Article  Google Scholar 

  6. Carpenter SR et al (1987) Regulation of lake primary productivity by food web structure. Ecology 68:1863–1876

    Article  Google Scholar 

  7. Carr LA, Boyer KE (2014) Variation at multiple trophic levels mediates a novel seagrass–grazer interaction. Mar Ecol Prog Ser 508:117–128

    Article  Google Scholar 

  8. Catano LB et al (2016) Reefscapes of fear: predation risk and reef heterogeneity interact to shape herbivore foraging behaviour. J Anim Ecol 85:146–156

    Article  PubMed  Google Scholar 

  9. Cohen JE, Pimm SL, Yodzis P, Saldana J (1993) Body sizes of animal predators and animal prey in food webs. J Anim Ecol 62:67–78

    Article  Google Scholar 

  10. 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 

  11. DeLong JP et al (2015) The body size dependence of trophic cascades. Am Nat 185:354–366

    Article  PubMed  Google Scholar 

  12. Driggers WB et al (2014) Site fidelity of migratory bonnethead sharks Sphyrna tiburo (L. 1758) to specific estuaries in South Carolina, USA. J Exp Mar Biol Ecol 459:61–69

    Article  Google Scholar 

  13. Eggleston DB (1990) Foraging behavior of the blue crab, Callinectes sapidus, on juvenile oysters, Crassostrea virginica—effects of prey density and size. Bull Mar Sci 46:62–82

    Google Scholar 

  14. Estes JA, Duggins DO (1995) Sea otters and kelp forests in Alaska—generality and variation in a community ecological paradigm. Ecol Monogr 65:75–100

    Article  Google Scholar 

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

    Article  Google Scholar 

  16. Farji-Brener AG, Barrantes G, Ruggiero A (2004) Environmental rugosity, body size and access to food: a test of the size-grain hypothesis in tropical litter ants. Oikos 104:165–171

    Article  Google Scholar 

  17. Ferner MC, Smee DL, Weissburg MJ (2009) Habitat complexity alters lethal and non-lethal olfactory interactions between predators and prey. Mar Ecol Prog Ser 374:13–22

    Article  Google Scholar 

  18. Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071

    PubMed  Google Scholar 

  19. Finke DL, Denno RF (2002) Intraguild predation diminished in complex-structured vegetation: implications for prey suppression. Ecology 83:643–652

    Article  Google Scholar 

  20. Finke DL, Denno RF (2006) Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades. Oecologia 149:265–275

    Article  PubMed  Google Scholar 

  21. Gehman AM, Grabowski JH, Hughes AR, Kimbro DL, Piehler MF, Byers JE (2017) Predators, environment and host characteristics influence the probability of infection by an invasive castrating parasite. Oecologia 183:139–149

    Article  PubMed  Google Scholar 

  22. Grabowski JH (2004) Habitat complexity disrupts predator–prey interactions but not the trophic cascade on oyster reefs. Ecology 85:995–1004

    Article  Google Scholar 

  23. Grabowski JH, Kimbro DL (2005) Predator—avoidance behavior extends trophic cascades to refuge habitats. Ecology 86:1312–1319

    Article  Google Scholar 

  24. Grabowski JH, Powers SP (2004) Habitat complexity mitigates trophic transfer on oyster reefs. Mar Ecol Prog Ser 277:291–295

    Article  Google Scholar 

  25. Grabowski JH, Hughes AR, Kimbro DL (2008) Habitat complexity influences cascading effects of multiple predators. Ecology 89:3413–3422

    Article  PubMed  Google Scholar 

  26. Griffen BD, Byers JE (2006) Partitioning mechanisms of predator interference in different habitats. Oecologia 146:608–614

    Article  PubMed  Google Scholar 

  27. Harding JM, Mann R (2010) Observations of distribution, size, and sex ratio of mature blue crabs, Callinectes sapidus, from a Chesapeake Bay tributary in relation to oyster habitat and environmental factors. Bull Mar Sci 86:75–91

    Google Scholar 

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

    Article  Google Scholar 

  29. Heithaus MR, Wirsing AJ, Burkholder D, Thomson J, Dill LM (2009) Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics. J Anim Ecol 78:556–562

    Article  PubMed  Google Scholar 

  30. Heithaus MR, Wirsing AJ, Dill LM (2012) The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem. Mar Freshw Res 63:1039–1050

    Article  Google Scholar 

  31. Hill JM, Weissburg MJ (2013) Habitat complexity and predator size mediate interactions between intraguild blue crab predators and mud crab prey in oyster reefs. Mar Ecol Prog Ser 488:209–219

    Article  Google Scholar 

  32. Humphries AT, La Peyre MK, Kimball ME, Rozas LP (2011) Testing the effect of habitat structure and complexity on nekton assemblages using experimental oyster reefs. J Exp Mar Biol Ecol 409:172–179

    Article  Google Scholar 

  33. Kimbro DL, Byers JE, Grabowski JH, Hughes AR, Piehler MF (2014) The biogeography of trophic cascades on US oyster reefs. Ecol Lett 17:845–854

    Article  PubMed  Google Scholar 

  34. Lenihan HS, Peterson CH (1998) How habitat degradation through fishery disturbance enhances impacts of hypoxia on oyster reefs. Ecol Appl 8:128–140

    Article  Google Scholar 

  35. Lenihan HS, Peterson CH, Byers JE, Grabowski JH, Thayer GW, Colby DR (2001) Cascading of habitat degradation: oyster reefs invaded by refugee fishes escaping stress. Ecol Appl 11:764–782

    Article  Google Scholar 

  36. Lessa RP, Almeida Z (1998) Feeding habits of the bonnethead shark, Sphyrna tiburo, from northern Brazil. Cybium 22:383–394

    Google Scholar 

  37. McClanahan TR, Muthiga NA (2016) Geographic extent and variation of a coral reef trophic cascade. Ecology 97:1862–1872

    CAS  Article  PubMed  Google Scholar 

  38. Micheli F (1997) Effects of predator foraging behavior on patterns of prey mortality in marine soft bottoms. Ecol Monogr 67:203–224

    Article  Google Scholar 

  39. Nakao S, Miyasaka H, Kuhara N (1999) Terrestrial-aquatic linkages: riparian arthropod inputs alter trophic cascades in a stream food web. Ecology 80:2435–2441

    Google Scholar 

  40. Pace ML, Cole JJ, Carpenter SR, Kitchell JF (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488

    CAS  Article  PubMed  Google Scholar 

  41. Peckarsky BL, McIntosh AR, Alvarez M, Moslemi JM (2013) Nutrient limitation controls the strength of behavioral trophic cascades in high elevation streams. Ecosphere 4:110. doi:10.1890/ES13.00084.1

    Article  Google Scholar 

  42. Peterson CH, Black R (1994) An experimentalists challenge—when artifacts of intervention interact with treatments. Mar Ecol Prog Ser 111:289–297

    Article  Google Scholar 

  43. Polis GA, Hurd SD (1996) Allochthonous input across habitats, subsidized consumers, and apparent trophic cascades: examples from the ocean-land interface. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamics. Chapman and Hall, New York, pp 275–285

    Google Scholar 

  44. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Google Scholar 

  45. Schmitz OJ, Beckerman AP, OBrien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399

    Article  Google Scholar 

  46. Shurin JB et al (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791

    Article  Google Scholar 

  47. Smee DL, Ferner MC, Weissburg MJ (2008) Alteration of sensory abilities regulates the spatial scale of nonlethal predator effects. Oecologia 156:399–409

    Article  PubMed  Google Scholar 

  48. Soluk DA (1993) Multiple predator effects—predicting combined functional-response of stream fish and invertebrate predators. Ecology 74:219–225

    Article  Google Scholar 

  49. Strong DR (1992) Are trophic cascades all wet—differentiation and donor-control in speciose ecosystems. Ecology 73:747–754

    Article  Google Scholar 

  50. Thorpe T, Jensen CF, Moser ML (2004) Relative abundance and reproductive characteristics of sharks in southeastern North Carolina coastal waters. Bull Mar Sci 74:3–20

    Google Scholar 

  51. Trussell GC, Ewanchuk PJ, Matassa CM (2006) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–1252

    Article  PubMed  Google Scholar 

  52. Tscharntke T, Rand TA, Bianchi FJJA (2005) The landscape context of trophic interactions: insect spillover across the crop-noncrop interface. Ann Zool Fenn 42:421–432

    Google Scholar 

  53. Ulrich GF, Jones CM, Driggers WB III, Drymon JM, Oakley D, Riley C (2007) Habitat utilization, relative abundance, and seasonality of sharks in the estuarine and nearshore waters of South Carolina. In: McCandless CT, Kohler NE, Pratt HLJ (eds) Shark nursery grounds of the Gulf of Mexico and East Coast Waters of the United States. American Fisheries Society Symposium, vol 50. Bethesda, Maryland, pp 125–139. ISBN: 978-1-888569-81-0

  54. Vance-Chalcraft HD, Soluk DA (2005) Multiple predator effects result in risk reduction for prey across multiple prey densities. Oecologia 144:472–480

    Article  PubMed  Google Scholar 

  55. Weissburg MJ, Zimmerfaust RK (1993) Life and death in moving fluids—hydrodynamic effects on chemosensory-mediated predation. Ecology 74:1428–1443

    Article  Google Scholar 

  56. Wellnitz T (2014) Can current velocity mediate trophic cascades in a mountain stream? Freshw Biol 59:2245–2255

    Article  Google Scholar 

  57. Wilson ML, Weissburg MJ (2013) Biotic structure indirectly affects associated prey in a predator-specific manner via changes in the sensory environment. Oecologia 171:427–438

    Article  PubMed  Google Scholar 

  58. Wu XW, Griffin JN, Sun SC (2014) Cascading effects of predator–detritivore interactions depend on environmental context in a Tibetan alpine meadow. J Anim Ecol 83:546–556

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank J. DeVore, R. Smith, M. Walker, H. Weiskel and C. Yeager for field assistance and. J. Grabowski, R. Hughes, D. Kimbro, and M. Piehler for consultation and input. We are grateful to the staff at the Skidaway Institute of Oceanography for their support. Our work was supported by NSF-OCE-0961853 (Directorate for Geosciences). The study and procedures were approved by the UGA Institutional Animal Care and Use Committee.

Data accessibility

Data from this work is archived in Dryad Digital Repository. doi:10.5061/dryad.429t4.

Author information

Affiliations

Authors

Contributions

JB obtained funding and conceived the experiments. ZH and JM performed the experiments. JB analyzed the data. JB and ZH wrote the manuscript; JM provided editorial advice.

Corresponding author

Correspondence to James E. Byers.

Additional information

Communicated by Jeremy Long.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 718 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Byers, J.E., Holmes, Z.C. & Malek, J.C. Contrasting complexity of adjacent habitats influences the strength of cascading predatory effects. Oecologia 185, 107–117 (2017). https://doi.org/10.1007/s00442-017-3928-y

Download citation

Keywords

  • Ecotones
  • Edge effects
  • Intraguild predation
  • Trait-mediated indirect effects
  • Trophic interactions