Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Should I stay or should I go: predator- and conspecific-induced hatching in a marine snail

  • 306 Accesses

  • 28 Citations

Abstract

Predator-induced hatching plasticity has been demonstrated in many species of amphibians. However, animals from other clades (e.g., marine species of molluscs and annelids) also place their embryos in capsules or gelatinous masses and might also exhibit hatching plasticity to predators. To date there is no evidence of predator-induced hatching plasticity from any marine species or a major clade of bilateria animals, the Lophotrochozoa. We studied predator-induced hatching plasticity of Nucella lamellosa, a carnivorous marine snail that deposits embryos in capsules. We used two experiments to investigate the effects of two types of predator, crabs and isopods, on developing embryos. In the first experiment, we quantified proportion of hatched embryos from capsules through time exposed to water-borne chemicals of crabs and isopods. Crabs delayed time-to-hatching, and the effects of predators were additive. In the second experiment, we quantified proportion of hatched embryos from capsules through time, developmental stage, and size of embryos in capsules exposed to water-borne chemicals of crabs and conspecifics. With this experiment, we wanted to answer: (1) whether a delay in hatching corresponded to embryos developing slower, and (2) whether the general products of metabolic waste from organisms can delay hatching. We unexpectedly observed that adult conspecific snails accelerated hatching but not developmental rate—the few past studies on the effects of conspecifics have all demonstrated that conspecifics delay time-to-hatching and rate of development. The results were also inconsistent with metabolic waste in general causing a delay in hatching, although the effect of conspecifics does weaken this inference. This study demonstrates that predators delay time-to-hatching in a marine mollusc, and suggests that predator-induced hatching plasticity is widespread among animals and likely evolved multiple times within the bilateria. In addition, conspecifics accelerated time-to-hatching in a marine mollusc, which suggests that conspecifics, like predators, might commonly influence when embryos hatch.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Beladjal L, Kierckens K, Mertens J (2007) Pheromones inhibit the hatching of diapausing Anostraca (Crustacea: Branchiopoda). Anim Biol 57:1–9

  2. Benoît HP, Pepin P, Brown JA (2000) Patterns of metamorphic age and length in marine fishes, from individuals to taxa. Can J Zool 57:856–869

  3. Blaustein L (1997) Non-consumptive effects of larval Salamandra on crustacean prey: can eggs detect predators? Oecologia 110:212–217

  4. Bolker BM (2008) Ecological models and data in R. Princeton University Press, Princeton

  5. Chivers DP, Kiesecker JM, Marco A, DeVito J, Anderson MT, Blaustein AR (2001) Predator-induced life history changes in amphibians: egg predation induces hatching. Oikos 92:135–142

  6. Collin R (2004) Phylogenetic effects, the loss of complex characters, and the evolution of development in calypteraeid gastropods. Evolution 58:1488–1502

  7. Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a freshwater snail. Science 247:949–951

  8. De Roeck ERM, Artois T, Brendonck L (2005) Consumptive and non-consumptive effects of turbellarian (Mesostoma sp.) predation on anostracans. Hydrobiologia 542:103–111

  9. Goddard JHR (2004) Developmental mode in benthic opisthobranch molluscs from the northeast Pacific Ocean: feeding in a sea of plenty. Can J Zool 82:1954–1968

  10. Havenhand JN (1993) Egg to juvenile period, generation time, and the evolution of larval types in marine invertebrates. Mar Ecol Prog Ser 97:247–260

  11. Hawkins LE, Hutchinson S (1988) Egg capsule structure and hatching mechanism of Ocenebra erinacea (L.) (Prosobranchia: Muricidae). J Exp Mar Biol Ecol 119:269–283

  12. Hentschel BT (1999) Complex life cycles in a variable environment: predicting when the timing of metamorphosis shifts from resource dependent to developmentally fixed. Am Nat 154:549–558

  13. Ireland DH, Wirsing AJ, Murray DL (2007) Phenotypically plastic responses of green frog embryos to conflicting predation risk. Oecologia 152:162–168

  14. Jägersten G (1972) Evolution of metazoan life cycle. Academic Press, New York

  15. Johnson JB, Saenz D, Adams CK, Conner RN (2003) The influence of predator threat on the timing of a life-history switch point: predator-induced hatching in the southern leopard frog (Rana sphenocephala). Can J Zool 81:1608–1613

  16. Kaha D, Berman Y, Bar-El T (1988) Maternal inhibition of hatching at high population densities in Tigriopus japonicus (Copepoda, Crustacea). Biol Bull 174:139–144

  17. Krug PJ (2009) Not my “type”: larval dispersal dimorphisms and bet-hedging in opisthobranch life histories. Biol Bull 216:355–372

  18. Kusch RC, Chivers DP (2004) The effects of crayfish predation on phenotypic and life-history variation in fathead minnows. Can J Zool 82:917–921

  19. Laurila A, Pakkasmaa S, Crochet P-A, Merilä J (2002) Predator-induced plasticity in early life history and morphology in two anuran amphibians. Oecologia 132:524–530

  20. Levin LA (1984) Life history and dispersal patterns in a dense infaunal polychaete assemblage: community structure and response to disturbance. Ecology 65:1185–1200

  21. Levitan DR (2000) Optimal egg size in marine invertebrates: theory and phylogenetic analysis of the critical relationship between egg size and development in echinoids. Am Nat 156:175–192

  22. Li D (2002) Hatching responses of subsocial spitting spiders to predation risk. Proc R Soc Lond B 269:2155–2161

  23. Livdahl TP, Koenekoop RK, Futterweit SG (1984) The complex hatching response of Aedes eggs to larval density. Ecol Entomol 9:437–442

  24. Ludwig D, Rowe L (1990) Life-history strategies for energy gain and predator avoidance under time constraints. Am Nat 135:686–707

  25. McEdward LR, Miner BG (2001) Larval and life-cycle patterns in echinoderms. Can J Zool 79:1125–1170

  26. Moore RD, Newton B, Sih A (1996) Delayed hatching as a response of streamside salamander eggs to chemical cues from predatory sunfish. Oikos 77:331–335

  27. Newman RA (1992) Adaptive plasticity in amphibian metamorphosis. Bioscience 42:671–678

  28. Nussbaum RA, Schultz DL (1989) Coevolution of parental care and egg size. Am Nat 133:591–603

  29. Pearce CM, Scheibling RE (1990) Induction of settlement and metamorphosis in the sand dollar Echinarachnius parma: evidence for an adult-associated factor. Mar Biol 107:363–369

  30. Pechenik JA (1975) The escape of veligers from the egg capsules of Nassarius obsoletus and Nassarius trivittatus (Gastropoda, Prosobranchia). Biol Bull 149:580–589

  31. Pechenik JA (1986) The encapsulation of eggs and embryos by molluscs: an overview. Am Malacol Bull 4:165–172

  32. Pechenik JA (1990) Delayed metamorphosis by larval of benthic marine invertebrates: does it occur? Is there a price to pay? Ophelia 32:63–94

  33. Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297

  34. Peckarsky BL, Taylor BW, McIntosh AR, McPeek MA, Lytle DA (2001) Variation in mayfly size at metamorphosis as a developmental response to risk of predation. Ecology 82:740–757

  35. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, New York

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

  37. Rapoport HS, Shadwick RE (2002) Mechanical characterization of an unusual elastic biomaterial from the egg capsules of marine snails (Busycon spp.). Biomacromolecules 3:42–50

  38. Rapoport HS, Shadwick RE (2007) Reversibly labile, sclerotization-induced elastic properties in a keratin anolog from marine snails: whelk egg capsule biopolymer (WECB). J Exp Biol 210:12–26

  39. Rawlings TA (1990) Associations between egg capsule morphology and predation among populations of the marine gastropod, Nucella emarginata. Biol Bull 179:312–325

  40. Reznick DN (1990) Plasticity in age and size at maturity in male guppies (Poecilia retculata): an experimental evaluation of alternative models of development. J Evol Biol 3:185–203

  41. Roff DA (2002) Life history evolution. Sinauer, Sunderland

  42. Rousset V, Pleijel F, Rouse GW, Erséus C, Siddall ME (2007) A molecular phylogeny of annelids. Cladistics 23:41–63

  43. Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427

  44. Saenz D, Johnson JB, Adams CK, Dayton GH (2003) Accelerated hatching of southern leopard frog (Rana sphenocephala) eggs in response to the presence of a crayfish (Procambarus nigrocinctus) predator. Copeia 2003:646–649

  45. Sargent RC, Taylor PD, Gross MR (1987) Care and evolution of egg size in fishes. Am Nat 129:32–46

  46. Schalk G, Forbes MR, Weatherhead PJ (2002) Developmental plasticity and growth rates of green frog (Rana clamitans) embryos and tadpoles in relation to a leech (Macrobdella decora) predator. Copeia 2009:445–449

  47. Scheltema RS (1971) Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine gastropods. Biol Bull 140:284–322

  48. Schoeppner NM, Relyea RA (2009) When should prey respond to consumed heterospecifics? Testing hypotheses of perceived risk. Copeia 2009:190–194

  49. Shine R (1978) Propagule size and parental care: the “safe harbor” hypothesis. J Theor Biol 75:417–424

  50. Sih A, Moore RD (1993) Delayed hatching of salamander eggs in response to enhanced larval predation risk. Am Nat 142:947–960

  51. Spight TM, Emlen J (1976) Clutch sizes of two marine snails with a changing food supply. Ecology 57:1162–1178

  52. Strathmann RR (1978) The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894–906

  53. Strathmann MF (1987) Reproduction and development of marine invertebrates of the Northern Pacific Coast. University of Washington Press, Seattle

  54. Sullivan CH, Bonar DB (1985) Hatching of Ilyanassa obsoleta embryos: degradation of the egg capsule plug in the absence of detectable proteolysis of the the major plug proteins. Biol Bull 169:365–376

  55. Sullivan CH, Maugel TK (1984) Formation, organization, and composition of the egg capsule of the marine gastropod, Ilyanassa obsoleta. Biol Bull 167:378–389

  56. Vance RR (1973) On reproductive strategies in marine benthic invertebrates. Am Nat 107:339–352

  57. Vonesh JR, Bolker BM (2005) Compensatory larval responses shift trade-offs associated with predator-induced hatching plasticity. Ecology 86:1580–1591

  58. Voronezhskaya EE, Khabarova MY, Nezlin LP (2004) Apical sensory neurones mediate developmental retardation induced by conspecific environmental stimuli in freshwater pulmonate snails. Development 131:3671–3680

  59. Warkentin KM (1995) Adaptive plasticity in hatching age: a response to predation risk trade-offs. Proc Natl Acad Sci USA 92:3507–3510

  60. Warkentin KM (2005) How do embryos assess risk? Vibrational cues in predator-induced hatching of red-eyed treefrogs. Anim Behav 70:59–71

  61. Warkentin KM (2007) Oxygen, gills, and embryo behavior: mechanisms of adaptive plasticity in hatching. Comp Biochem Physiol A 148:720–731

  62. Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341

  63. Wilbur HM (1997) Experimental ecology of food webs: complex systems in temporary ponds. Ecology 78:2279–2302

Download references

Acknowledgments

We thank R. Price and E. Wackenhut for assisting us with experiments, D. E. Schneider for sharing his wisdom, and two reviewers for their thoughtful reviews that improved this manuscript.

Author information

Correspondence to Benjamin G. Miner.

Additional information

Communicated by Steven Kohler.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Miner, B.G., Donovan, D.A. & Andrews, K.E. Should I stay or should I go: predator- and conspecific-induced hatching in a marine snail. Oecologia 163, 69–78 (2010). https://doi.org/10.1007/s00442-010-1570-z

Download citation

Keywords

  • Hemigrapsus oregonensis
  • Idotea
  • Larva
  • Life history
  • Nucella lamellosa