Marine Biology

, 163:5 | Cite as

A predator has nonconsumptive effects on different life-history stages of a prey

  • Julius A. Ellrich
  • Ricardo A. Scrosati
  • Camilla Bertolini
  • Markus Molis
Original paper


Through a field experiment, we show that a predator has negative nonconsumptive effects (NCEs) on different life-history stages of the same prey species. Shortly before the recruitment season of the barnacle Semibalanus balanoides (May–June), we established experimental cages in rocky intertidal habitats in Nova Scotia, Canada. The cages were used to manipulate the presence and absence of dogwhelks, Nucella lapillus, the main predators of barnacles. At the centre of each cage, we installed a tile where barnacle pelagic larvae could settle and the resulting recruits grow. Mesh prevented caged dogwhelks from accessing the tiles, but allowed waterborne dogwhelk cues to reach the tiles. Results in May indicated that barnacle larvae settled preferentially on tiles from cages without dogwhelks. In November, at the end of the dogwhelk activity period and once the barnacle recruits had grown to adult size, barnacle body mass was lower in the presence of dogwhelks. This limitation may have resulted from a lower barnacle feeding activity with nearby dogwhelks, as found by a previous study. The observed larval and adult responses in barnacles are consistent with attempts to decrease predation risk. November data also indicated that dogwhelk cues limited barnacle reproductive output, a possible consequence of the limited growth of barnacles. Overall, this study suggests that a predator species might influence trait evolution in a prey species through NCEs on different life-history stages.


Predation Risk Prey Species Reproductive Output Lively 1986a Adult Barnacle 
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.



We thank Patrick Comtois for field assistance, Werner Schnepf, Steven MacDonald, and David Risk for laboratory assistance, and two anonymous reviewers for helpful comments on the manuscript. Funds were provided by grants awarded to R. Scrosati by the Canada Research Chairs Program (CRC; Grant Number 210283), the Canada Foundation for Innovation (CFI; Grant Number 202034), and the Natural Sciences and Engineering Research Council (NSERC, Discovery Grant Number 311624) and by Ph.D. scholarships awarded to J. Ellrich by the Stiftung für Kanada-Studien (SKS, Scholarship Number T191/19833) and the German Academic Exchange Service (DAAD, scholarship number D/10/47054). This study is part of the Ph.D. dissertation of J. Ellrich, supervised by R. Scrosati and M. Molis and registered at the University of Bremen, Germany.

Compliance with ethical standards

Conflict of interest

The authors declare to have no conflicts of interest.


  1. Barnes M (1999) The mortality of intertidal cirripedes. Oceanogr Mar Biol Annu Rev 37:153–244Google Scholar
  2. Barnes H, Barnes M (1954) The general biology of Balanus balanus (L.) da Costa. Oikos 5:63–76CrossRefGoogle Scholar
  3. Beermann AJ, Ellrich JA, Molis M, Scrosati RA (2013) Effects of seaweed canopies and adult barnacles on barnacle recruitment: the interplay of positive and negative influences. J Exp Mar Biol Ecol 448:162–170CrossRefGoogle Scholar
  4. Bertness MD (1989) Intraspecific competition and facilitation in a northern acorn barnacle population. Ecology 70:257–268CrossRefGoogle Scholar
  5. Bertness MD, Gaines SD, Stephens EG, Yund PO (1992) Components of recruitment in populations of the acorn barnacle Semibalanus balanoides (Linnaeus). J Exp Mar Biol Ecol 156:199–215CrossRefGoogle Scholar
  6. Bouchard GM, Aiken RB (2012) Latitudinal variation in the reproductive cycle and size of the northern rock barnacle Semibalanus balanoides (L.) (Cirripedia, Archaeobalanidae) in the Bay of Fundy. Crustaceana 85:779–787CrossRefGoogle Scholar
  7. Bousfield EL (1954) The distribution and spawning seasons of barnacles on the Atlantic coast of Canada. Bull Natl Mus Canada 132:112–154Google Scholar
  8. Brönmark C, Hansson LA (2012) Chemical ecology in aquatic systems. Oxford University Press, OxfordCrossRefGoogle Scholar
  9. Buschbaum C (2000) Direct and indirect effects of Littorina littorea (L.) on barnacles growing on mussel beds in the Wadden Sea. Hydrobiologia 440:119–128CrossRefGoogle Scholar
  10. Carriker MR (1981) Shell penetration and feeding in naticacean and muricacean predatory gastropods: a synthesis. Malacologia 20:403–422Google Scholar
  11. Chabot R, Bourget E (1988) Influence of substratum heterogeneity and settled barnacle density on the settlement of cypris larvae. Mar Biol 97:45–56CrossRefGoogle Scholar
  12. Cole SWB, Scrosati RA, Tam JC, Sussmann AV (2011) Regional decoupling between NW Atlantic barnacle recruit and adult density is related to changes in pelagic food supply and benthic disturbance. J Sea Res 65:33–37CrossRefGoogle Scholar
  13. Crisp DJ (1954) The breeding of Balanus porcatus (da Costa) in the Irish Sea. J Mar Biol Assoc UK 33:473–496CrossRefGoogle Scholar
  14. Crisp DJ (1968) Differences between North American and European populations of Balanus balanoides revealed by transplantation. Fish Res Board Canada 25:2633–2641CrossRefGoogle Scholar
  15. Crothers JH (1985) Dog-whelks: an introduction into the biology of Nucella lapillus (L.). Field Stud 6:291–360Google Scholar
  16. Denno RF, Lewis D (2009) Predator–prey interactions. In: Levin SA (ed) The Princeton guide to ecology. Princeton University Press, Princeton, pp 202–212Google Scholar
  17. DFO (2015) Fisheries and Oceans Canada. Oceanography and scientific data branch: database of oceanographic data. Accessed 30 July 2015
  18. Dunkin SB, Hughes RN (1984) Behavioural components of prey selection by dogwhelks, Nucella lapillus (L.), feeding on barnacles, Semibalanus balanoides (L.), in the laboratory. J Exp Mar Biol Ecol 79:91–103CrossRefGoogle Scholar
  19. Ellrich JA, Scrosati RA, Molis M (2015) Predator nonconsumptive effects on prey recruitment weaken with recruit density. Ecology 96:611–616CrossRefGoogle Scholar
  20. Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724CrossRefGoogle Scholar
  21. Hills JM, Thomason JC (2003) The ‘ghost of settlement past’ determines mortality and fecundity in the barnacle Semibalanus balanoides. Oikos 101:529–538CrossRefGoogle Scholar
  22. Holt RD (2009) Predation and community organization. In: Levin SA (ed) The Princeton guide to ecology. Princeton University Press, Princeton, pp 274–281Google Scholar
  23. Hughes RN (1972) Annual production of two Nova Scotian populations of Nucella lapillus (L.). Oecologia 8:356–370CrossRefGoogle Scholar
  24. Hunt HL, Scheibling RE (1998) Effects of whelk (Nucella lapillus (L.)) predation on mussel (Mytilus trossulus (Gould), M. edulis (L.)) assemblages in tidepools and on emergent rock on a wave-exposed rocky shore in Nova Scotia, Canada. J Exp Mar Biol Ecol 226:87–113CrossRefGoogle Scholar
  25. Hurlbert SH, Lombardi CM (2012) Lopsided reasoning on lopsided tests and multiple comparisons. Aust N Z J Stat 54:23–42CrossRefGoogle Scholar
  26. Hurley AC (1973) Fecundity of the acorn barnacle Balanus pacificus: a fugitive species. Limnol Oceanogr 18:386–393CrossRefGoogle Scholar
  27. Jenkins SR, Åberg P, Cervin G, Coleman RA, Delany J, Della Santina P, Hawkins SJ, LaCroix E, Myers AA, Lindegarth M, Power AM, Roberts MF, Hartnoll RG (2000) Spatial and temporal variation in settlement and recruitment of the intertidal barnacle Semibalanus balanoides (L.) (Crustacea: Cirripedia) over a European scale. J Exp Mar Biol Ecol 243:209–225CrossRefGoogle Scholar
  28. Johnson LE, Strathmann RR (1989) Settling barnacle larvae avoid substrata previously occupied by a mobile predator. J Exp Mar Biol Ecol 128:87–103CrossRefGoogle Scholar
  29. Johnston BR, Molis M, Scrosati RA (2012) Predator chemical cues affect prey feeding activity differently in juveniles and adults. Can J Zool 90:128–132CrossRefGoogle Scholar
  30. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Écoscience 5:361–364Google Scholar
  31. Keppel E, Scrosati R (2004) Chemically mediated avoidance of Hemigrapsus nudus (Crustacea) by Littorina scutulata (Gastropoda): effects of species coexistence and variable cues. Anim Behav 68:915–920CrossRefGoogle Scholar
  32. Large SI, Smee DL (2010) Type and nature of cues used by Nucella lapillus to evaluate predation risk. J Exp Mar Biol Ecol 396:10–17CrossRefGoogle Scholar
  33. Large SI, Smee DL, Trussell GC (2011) Environmental conditions influence the frequency of prey responses to predation risk. Mar Ecol Prog Ser 422:41–49CrossRefGoogle Scholar
  34. Lively CM (1986a) Competition, comparative life histories, and maintenance of shell dimorphism in a barnacle. Ecology 67:858–864CrossRefGoogle Scholar
  35. Lively CM (1986b) Predator-induced shell dimorphism in the acorn barnacle Chthamalus anisopoma. Evolution 40:232–242CrossRefGoogle Scholar
  36. Lively CM (1999) Developmental strategies in spatially variable environments: barnacle shell dimorphisms and strategic models of selection. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 245–258Google Scholar
  37. Matassa CM, Trussell GC (2011) Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects. Ecology 92:2258–2266CrossRefGoogle Scholar
  38. Miller LP (2013) The effect of water temperature on drilling and ingestion rates of the dogwhelk Nucella lapillus feeding on Mytilus edulis mussels in the laboratory. Mar Biol 160:1489–1496CrossRefGoogle Scholar
  39. Minchinton TE, Scheibling RE (1991) The influence of larval supply and settlement on the population structure of barnacles. Ecology 72:1867–1879CrossRefGoogle Scholar
  40. Mokady O, Mizrahi L, Perl-Treves R, Achituv Y (2000) The different morphs of Chthamalus anisopoma: a phenotypic response? Direct molecular evidence. J Exp Mar Biol Ecol 243:295–304CrossRefGoogle Scholar
  41. Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405CrossRefGoogle Scholar
  42. Mukherjee S, Heithaus MR, Trexler JC, Ray-Mukherjee J, Vaudo J (2014) Perceived risk of predation affects reproductive life-history traits in Gambusia holbrooki, but not in Heterandria formosa. PLoS One 9:e88832CrossRefGoogle Scholar
  43. Murua J, Burrows MT, Hughes RN, Hawkins SJ, Thompson RC, Jenkins SR (2014) Phenotypic variation in shell form in the intertidal acorn barnacle Chthamalus montagui: distribution, response to predators and life history trade-offs. Mar Biol 161:2609–2619CrossRefGoogle Scholar
  44. NASA (2015) National Aeronautics and Space Administration. Ocean color radiometry online visualization and analysis. Accessed 30 July 2015
  45. Pangle KL, Peacor SD, Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88:402–412CrossRefGoogle Scholar
  46. Peacor S, Werner EE (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proc Nat Acad Sci USA 98:3904–3908CrossRefGoogle Scholar
  47. Peacor SD, Peckarsky BL, Trussell GC, Vonesh JR (2013) Costs of predator-induced phenotypic plasticity: a graphical model for predicting the contribution of nonconsumptive and consumptive effects of predators on prey. Oecologia 171:1–10CrossRefGoogle Scholar
  48. Peckarsky BL, Cowan CA, Penton MA, Anderson C (1993) Sublethal consequences of stream-dwelling predatory stoneflies on mayfly growth and fecundity. Ecology 74:1836–1846CrossRefGoogle Scholar
  49. Peckarsky BL, McIntosh AR, Taylor BW, Dahl J (2002) Predator chemicals induce changes in mayfly life-history traits: a whole-stream manipulation. Ecology 83:612–618CrossRefGoogle Scholar
  50. Pineda J, Riebensahm D, Medeiros-Bergen D (2002) Semibalanus balanoides in winter and spring: larval concentration, settlement, and substrate occupancy. Mar Biol 140:789–800CrossRefGoogle Scholar
  51. Preisser EL, Bolnick DI (2008) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLoS One 3:e2465CrossRefGoogle Scholar
  52. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509CrossRefGoogle Scholar
  53. Quinn GP, Keough MJ (2002) Experimental design and data analyses for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  54. Rainbow PS (1984) An introduction to the biology of British littoral barnacles. Field Stud 6:1–51Google Scholar
  55. Ramírez Llorda E (2002) Fecundity and life strategies in marine invertebrates. Adv Mar Biol 43:87–170CrossRefGoogle Scholar
  56. Scrimgeour GJ, Culp JM (1994) Feeding while evading predators by a lotic mayfly: linking short-term foraging behaviours to long-term fitness consequences. Oecologia 100:128–134CrossRefGoogle Scholar
  57. Scrosati R, Heaven C (2007) Spatial trends in community richness, diversity, and evenness across rocky intertidal environmental stress gradients in eastern Canada. Mar Ecol Prog Ser 342:1–14CrossRefGoogle Scholar
  58. Selden R, Johnson AS, Ellers O (2009) Waterborne cues from crabs induce thicker skeletons, smaller gonads, and size specific changes in growth rate in sea urchins. Mar Biol 156:1057–1071CrossRefGoogle Scholar
  59. Siepielski AM, Wang J, Prince G (2014) Nonconsumptive predator-driven mortality causes natural selection on prey. Evolution 68:696–704CrossRefGoogle Scholar
  60. Smee DL, Weissburg MJ (2006a) Clamming up: environmental forces diminish the perceptive ability of bivalve prey. Ecology 87:1587–1598CrossRefGoogle Scholar
  61. Smee DL, Weissburg MJ (2006b) Hard clams (Mercenaria mercenaria) evaluate predation risk using chemical signals from predators and injured conspecifics. J Chem Ecol 32:605–619CrossRefGoogle Scholar
  62. Strauss SY (2014) Adaptation to the biotic environment. In: Losos JB (ed) The Princeton guide to evolution. Princeton University Press, Princeton, pp 298–303Google Scholar
  63. Tam JC, Scrosati RA (2014) Distribution of cryptic mussel species (Mytilus edulis and M. trossulus) along wave exposure gradients on northwest Atlantic rocky shores. Mar Biol Res 10:51–60CrossRefGoogle Scholar
  64. Tapia-Lewin S, Pardo LM (2014) Field assessment of the predation risk-food availability trade-off in crab megalopae settlement. PLoS One 9:e95335CrossRefGoogle Scholar
  65. Teyssier A, Bestion E, Richard M, Cote J (2014) Partners’ personality types and mate preferences: predation risk matters. Behav Ecol 25:723–733CrossRefGoogle Scholar
  66. Trussell GC, Ewanchuk PJ, Matassa CM (2006) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–1252CrossRefGoogle Scholar
  67. Turner AM (2008) Predator diet and prey behaviour: freshwater snails discriminate among closely related prey in a predator’s diet. Anim Behav 76:1211–1217CrossRefGoogle Scholar
  68. Urban MC, Richardson JL (2015) The evolution of foraging rate across local and geographic gradients in predation risk and competition. Am Nat 186:E16–E32CrossRefGoogle Scholar
  69. Weissburg M, Smee DL, Ferner MC (2014) The sensory ecology of nonconsumptive predator effects. Am Nat 184:141–157CrossRefGoogle Scholar
  70. Welch JM, Rittschof D, Bullock TM, Fordward RB (1997) Effects of chemical cues on settlement behaviour of blue crab Callinectes sapidus postlarvae. Mar Ecol Prog Ser 154:143–153CrossRefGoogle Scholar
  71. Wethey DS (1984) Effects of crowding on fecundity in barnacles: Semibalanus (Balanus) balanoides, Balanus glandula, and Chthamalus dalli. Can J Zool 62:1788–1795CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Julius A. Ellrich
    • 1
  • Ricardo A. Scrosati
    • 1
  • Camilla Bertolini
    • 1
  • Markus Molis
    • 2
  1. 1.Department of BiologySt. Francis Xavier UniversityAntigonishCanada
  2. 2.Alfred Wegener Institute, Helmholtz-Zentrum für Polar- und MeeresforschungBremerhavenGermany

Personalised recommendations