, Volume 191, Issue 4, pp 945–956 | Cite as

Predator identity dominates non-consumptive effects in a disease-impacted rocky shore food web

  • Kindall A. MurieEmail author
  • Paul E. Bourdeau
Community ecology – original research


Predicting the effects of predator diversity loss on food webs is challenging, because predators can both consume and induce behavioral responses in their prey (i.e., non-consumptive effects or NCEs). Studies manipulating predator diversity and investigating NCEs are rare, especially in marine systems. Recently, a severe outbreak of sea star wasting syndrome (SSWS) on the west coast of North America resulted in unprecedented declines of the sea star Pisaster ochraceus. We investigated the consequences of Pisaster loss on an abundant grazer, the black turban snail Tegula funebralis, through NCEs. We combined a laboratory experiment and field surveys to examine the importance of identity vs. diversity in a predator assemblage (Pisaster, crabs, and octopuses) on Tegula behavior, feeding, and growth. Laboratory and field results indicated that predator identity, not diversity, drives Tegula behavior and causes NCEs. Mesocosm treatments with Pisaster caused greater NCEs on Tegula than assemblages without Pisaster. Tegula’s distribution in the field, which is driven primarily by anti-predator behavior, was strongly associated only with Pisaster abundance, and not with the abundance of crabs, octopuses, and other predatory sea stars (Leptasterias spp.). We conclude that Pisaster primarily drives Tegula vertical distribution and may be having strong NCEs on Tegula on northern California rocky shores. Furthermore, predator diversity in northern California does not provide functional redundancy, in terms of NCEs on Tegula, to buffer the system from Pisaster loss. Thus, predator-induced vertical distributions and grazing suppression may not be maintained in areas where Pisaster populations are reduced or slow to recover from SSWS.


Anti-predator behavior Intertidal zonation Keystone intimidator Multiple predators Predator–prey interactions Sea star wasting syndrome TMIIs Trophic cascade 



We thank the director and staff at TML for logistical support, and T. Burns, T. Flagor, J. Gravelle, L. McIntire, and R. Vadas-Williams for help with the experiment. S. Morgan, D. Burkepile, and three anonymous reviewers provided constructive criticism on the manuscript. Organisms were collected under CDFW SCP #10571. Funding was provided by an Oliphant Scholarship and a Humboldt MSCI Undergraduate Student Research Award to KAM. PEB acknowledges support from CSU-COAST. This is a contribution of Humboldt State University’s Telonicher Marine Laboratory and the Humboldt Marine and Coastal Sciences Institute.

Author contribution statement

KAM and PEB conceived the project. KAM collected and analyzed the data. KAM and PEB wrote the manuscript.

Supplementary material

442_2019_4548_MOESM1_ESM.docx (162 kb)
Supplementary material 1 (DOCX 162 kb)


  1. Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134. CrossRefGoogle Scholar
  2. Bourdeau PE (2010) Cue reliability, risk sensitivity and inducible morphological defense in a marine snail. Oecologia 162:987–994. CrossRefPubMedGoogle Scholar
  3. Bruno JF, O’Connor MI (2005) Cascading effects of predator diversity and omnivory in a marine food web. Ecol Lett 8:1048–1056. CrossRefGoogle Scholar
  4. Burnaford JL (2004) Habitat modification and refuge from sublethal stress drive a marine plant–herbivore association. Ecology 85:2837–2849. CrossRefGoogle Scholar
  5. Byrnes J, Stachowicz JJ, Hultgren KM, Hughes AR, Olyarnik SV, Thornber CS (2006) Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour. Ecol Lett 9:61–71. CrossRefPubMedGoogle Scholar
  6. Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O’connor MI, Gonzalez A (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592CrossRefGoogle Scholar
  7. Doering PH, Phillips DW (1983) Maintenance of the shore-level size gradient in the marine snail Tegula funebralis (A. Adams): importance of behavioral responses to light and sea star predators. J Exp Mar Biol Ecol 67:159–173. CrossRefGoogle Scholar
  8. Duffy JE (2003) Biodiversity loss, trophic skew and ecosystem functioning. Ecol Lett 6:680–687. CrossRefGoogle Scholar
  9. Duffy JE, Cardinale BJ, France KE, McIntyre PB, Thébault E, Loreau M (2007) The functional role of biodiversity in ecosystems: incorporating trophic complexity. Ecol Lett 10:522–538. CrossRefPubMedGoogle Scholar
  10. Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction vulnerability in marine populations. Fish Fish 4:25–64. CrossRefGoogle Scholar
  11. Dulvy NK, Freckleton RP, Polunin NV (2004) Coral reef cascades and the indirect effects of predator removal by exploitation. Ecol Lett 7:410–416. CrossRefGoogle Scholar
  12. Estes JA, Palmisano JF (1974) Sea otters: their role in structuring nearshore communities. Science 185:1058–1060. CrossRefPubMedGoogle Scholar
  13. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fawcett MH (1984) Local and latitudinal variation in predation on an herbivorous marine snail. Ecology 65:1214–1230. CrossRefGoogle Scholar
  15. Finke DL, Denno RF (2005) Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades. Ecol Lett 8:1299–1306. CrossRefGoogle Scholar
  16. Gamfeldt L, Lefcheck JS, Byrnes JE, Cardinale BJ, Duffy JE, Griffin JN (2015) Marine biodiversity and ecosystem functioning: what’s known and what’s next? Oikos 124:252–265. CrossRefGoogle Scholar
  17. Geller JB (1982) Chemically mediated avoidance response of a gastropod, Tegula funebralis (A. Adams), to a predatory crab, Cancer antennarius (Stimpson). J Exp Mar Biol Ecol 65:19–27. CrossRefGoogle Scholar
  18. Gosnell JS, Gaines SD (2012) Keystone intimidators in the intertidal: non-consumptive effects of a keystone sea star regulate feeding and growth in whelks. Mar Ecol Prog Ser 450:107–114. CrossRefGoogle Scholar
  19. Gravem SA, Morgan SG (2016) Prey state alters trait-mediated indirect interactions in rocky tide pools. Funct Ecol 30:1574–1582. CrossRefGoogle Scholar
  20. Gravem SA, Morgan SG (2017) Shifts in intertidal zonation and refuge use by prey after mass mortalities of two predators. Ecology 98:1006–1015. CrossRefPubMedGoogle Scholar
  21. Gruner DS, Smith JE, Seabloom EW, Sandin SA, Ngai JT, Hillebrand H, Harpole WS, Elser JJ, Cleland EE, Bracken ME, Borer ET (2008) A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol Lett 11:740–755. CrossRefPubMedGoogle Scholar
  22. Harrison PA, Berry PM, Simpson G, Haslett JR, Blicharska M, Bucur M, Dunford R, Egoh B, Gacia-Llorente M, Geamănă N, Geertsema W (2014) Linkages between biodiversity attributes and ecosystem services: a systematic review. Ecosyst Ser 9:191–203. CrossRefGoogle Scholar
  23. Hewson I, Button JB, Gudenkauf BM, Miner B, Newton AL, Gaydos JK, Wynne J, Groves CL, Hendler G, Murray M, Fradkin S (2014) Densovirus associated with sea-star wasting disease and mass mortality. Proc Natl Acad Sci 111:17278–17283. CrossRefPubMedGoogle Scholar
  24. Hughes BB (2010) Variable effects of a kelp foundation species on rocky intertidal diversity and species interactions in central California. J Exp Mar Biol Ecol 393:90–99. CrossRefGoogle Scholar
  25. Hull WW, Bourdeau PE (2017) Can crabs kill like a keystone predator? A field-test of the effects of crab predation on mussel mortality on a northeast Pacific rocky shore. PLoS One 12:e0183064. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Ives AR, Cardinale BJ, Snyder WE (2005) A synthesis of subdisciplines: predator–prey interactions, and biodiversity and ecosystem functioning. Ecol Lett 8:102–116. CrossRefGoogle Scholar
  27. Jackson JB, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637. CrossRefPubMedGoogle Scholar
  28. Katano I, Doi H, Eriksson BK, Hillebrand H (2015) A cross-system meta-analysis reveals coupled predation effects on prey biomass and diversity. Oikos 124:1427–1435. CrossRefGoogle Scholar
  29. Mach ME, Bourdeau PE (2011) To flee or not to flee? Risk assessment by a marine snail in multiple cue environments. J Exp Mar Biol Ecol 409:166–171. CrossRefGoogle Scholar
  30. Markowitz DV (1980) Predator influence on shore-level size gradients in Tegula funebralis (A. Adams). J Exp Mar Biol Ecol 45:1–13. CrossRefGoogle Scholar
  31. Menge BA, Berlow EL, Blanchette CA, Navarrete SA, Yamada SB (1994) The keystone species concept: variation in interaction strength in a rocky intertidal habitat. Ecol Monogr 64:249–286. CrossRefGoogle Scholar
  32. Menge BA, Cerny-Chipman EB, Johnson A, Sullivan J, Gravem S, Chan F (2016) Sea star wasting disease in the keystone predator Pisaster ochraceus in Oregon: insights into differential population impacts, recovery, predation rate, and temperature effects from long-term research. PLoS One. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Micheli F, Halpern BS (2005) Low functional redundancy in coastal marine assemblages. Ecol Lett 8:391–400. CrossRefGoogle Scholar
  34. Miner CM, Burnaford JL, Ambrose RF, Antrim L, Bohlmann H, Blanchette CA, Engle JM, Fradkin SC, Gaddam R, Harley CD, Miner BG (2018) Large-scale impacts of sea star wasting disease (SSWD) on intertidal sea stars and implications for recovery. PLoS One. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Morgan SG, Gravem SA, Lipus AC, Grabiel M, Miner BG (2016) Trait-mediated indirect interactions among residents of rocky shore tidepools. Mar Ecol Prog Ser 552:31–46. CrossRefGoogle Scholar
  36. Nielsen KJ (2001) Bottom-up and top-down forces in tide pools: test of a food chain model in an intertidal community. Ecol Monogr 71:187–217.;2 CrossRefGoogle Scholar
  37. Otto SB, Berlow EL, Rank NE, Smiley J, Brose U (2008) Predator diversity and identity drive interaction strength and trophic cascades in a food web. Ecology 89:134–144. CrossRefPubMedGoogle Scholar
  38. Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75. CrossRefGoogle Scholar
  39. Paine RT (1969) The Pisaster–Tegula interaction: prey patches, predator food preference, and intertidal community structure. Ecology 50:950–961. CrossRefGoogle Scholar
  40. Paine RT (1971) Energy flow in a natural population of the herbivorous gastropod Tegula funebralis. Limnol Oceanogr 16:86–98. CrossRefGoogle Scholar
  41. Peacor SD, Werner EE (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proc Natl Acad Sci 98:3904–3908. CrossRefPubMedGoogle Scholar
  42. Peckarsky BL, Abrams PA, Bolnick DI, Dill LM, Grabowski JH, Luttbeg B, Orrock JL, Peacor SD, Preisser EL, Schmitz OJ, Trussell GC (2008) Revisiting the classics: considering nonconsumptive effects in textbook examples of predator–prey interactions. Ecology 89:2416–2425. CrossRefPubMedGoogle Scholar
  43. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509. CrossRefGoogle Scholar
  44. Preisser EL, Orrock JL, Schmitz OJ (2007) Predator hunting mode and habitat domain alter nonconsumptive effects in predator–prey interactions. Ecology 88:2744–2751. CrossRefPubMedGoogle Scholar
  45. Pruitt JN, Stachowicz JJ, Sih A (2011) Behavioral types of predator and prey jointly determine prey survival: potential implications for the maintenance of within-species behavioral variation. Am Nat 179:217–227. CrossRefPubMedGoogle Scholar
  46. Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319:952–954. CrossRefPubMedGoogle Scholar
  47. Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399.;2 CrossRefGoogle Scholar
  48. Sih A, Wooster DE (1994) Prey behavior, prey dispersal, and predator impacts on stream prey. Ecology 75:1199–1207. CrossRefGoogle Scholar
  49. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355. CrossRefPubMedGoogle Scholar
  50. Stafford ES, Tyler CL, Leighton LR (2015) Gastropod shell repair tracks predator abundance. Mar Ecol 36:1176–1184. CrossRefGoogle Scholar
  51. Steinberg PD (1985) Feeding preferences of Tegula funebralis and chemical defenses of marine brown algae. Ecol Monogr 55:333–349. CrossRefGoogle Scholar
  52. Straub CS, Snyder WE (2006) Species identity dominates the relationship between predator biodiversity and herbivore suppression. Ecology 87:277–282. CrossRefPubMedGoogle Scholar
  53. Trussell GC, Ewanchuk PJ, Bertness MD (2003) Trait-mediated effects in rocky intertidal food chains: Predator risk cues alter prey feeding rates. Ecology 84:629–640.;2 CrossRefGoogle Scholar
  54. Tyler CL, Stafford ES, Leighton LR (2015) The utility of wax replicas as a measure of crab attack frequency in the rocky intertidal. J Mar Biol Assoc UK 95:361–369. CrossRefGoogle Scholar
  55. Van Alstyne KL, McCarthy JJ III, Hustead CL, Duggins DO (1999) Geographic variation in polyphenolic levels of Northeastern Pacific kelps and rockweeds. Mar Biol 133:371–379. CrossRefGoogle Scholar
  56. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology. 84:1083–1100.;2 CrossRefGoogle Scholar
  57. Worm B, Sandow M, Oschlies A, Lotze HK, Myers RA (2005) Global patterns of predator diversity in the open oceans. Science 309:1365–1369. CrossRefPubMedGoogle Scholar
  58. Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JB, Lotze HK, Micheli F, Palumbi SR, Sala E (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790. CrossRefPubMedGoogle Scholar
  59. Yarnall JL (1964) The responses of Tegula funebralis to starfishes and predatory snails (Mollusca: gastropoda). Veliger 6:56–58Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Telonicher Marine LaboratoryHumboldt State UniversityTrinidadUSA
  2. 2.Department of Biological SciencesHumboldt State UniversityArcataUSA

Personalised recommendations