Skip to main content

Advertisement

Log in

Why run and hide when you can divide? Evidence for larval cloning and reduced larval size as an adaptive inducible defense

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Predator-induced cloning (asexual reproduction), with reduced size as consequence of cloning, suggests a novel adaptation to the threat of predation. Although cloning is a common reproductive strategy of many plants and animals, cloning in response to stimuli from predators has, at present, been documented only in the larvae (plutei) of the sand dollar, Dendraster excentricus. Other studies report larval cloning in echinoderms under optimal conditions of food and temperature. A burst of asexuality should be favored when environmental conditions are conducive to growth, but it is less clear that cloning is advantageous when conditions indicate risk from predators. This study tested the hypothesis that the small size of predator-induced clones reduces vulnerability during encounters with planktivorous fish. Successful cloning was inferred from an increase in larval density, a reduction in larval size and stage, and some direct observations of budding. All clones were smaller than uncloned sibling larvae, suggesting an advantage against visual predators. Pair-wise predation trials demonstrated that planktivorous fish ate more uncloned sibling plutei than small clones. These results offer a new ecological context for asexual reproduction: rapid size reduction as a defense. If the identifiable cues for cloning in echinoderm larvae (food and predators) are linked in nature, then larval cloning may be a response to a single ecological scenario rather than two separate and unrelated conditions.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen JD (2008) Size-selective predation on marine invertebrate larvae. Biological Bulletin 214

  • Balser EJ (1998) Cloning by ophiuroid echinoderm larvae. Biol Bull 194:187–193

    Article  Google Scholar 

  • Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Ann Rev Ecol Evol Syst 35:651–673

    Article  Google Scholar 

  • Bergkvist J, Selander E, Pavia H (2008) Induction of toxin production in dinoflagellates: the grazer makes a difference. Oecologia 156:147–154

    Article  PubMed  Google Scholar 

  • Bollens SM, Frost BW, Thoreson DS, Watts SJ (1992) Diel vertical migration in zooplankton—field evidence in support of the predator avoidance hypothesis. Hydrobiologia 234:33–39

    Google Scholar 

  • Bosch I, Rivkin RB, Alexander SP (1989) Asexual reproduction by oceanic planktotrophic echinoderm larvae. Nature 337:169–170

    Article  Google Scholar 

  • Bronmark C, Miner JG (1992) Predator-induced phenotypical change in body morphology in crucian carp. Science 258:1348–1350

    Article  PubMed  CAS  Google Scholar 

  • Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35

    Article  PubMed  CAS  Google Scholar 

  • Chen MS (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114

    Article  CAS  Google Scholar 

  • Craig SF, Slobodkin LB, Wray GA, Biermann CH (1997) The ‘paradox’ of polyembryony: a review of the cases and a hypothesis for its evolution. Evol Ecol 11:127–143

    Article  Google Scholar 

  • Cronin G, Hay ME (1996) Induction of seaweed chemical defense by amphipod grazing. Ecology 77:2287–2301

    Article  Google Scholar 

  • De Robertis A, Jaffe JS, Ohman MD (2000) Size-dependent visual predation risk and the timing of vertical migration in zooplankton. Limnol Oceanogr 45

  • DeMeester L, Dawidowicz P, van Gool E, Loose CJ (1999) Predator-induced behavior of zooplankton: Depth selection behavior and diel vertical migration. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 160–176

    Google Scholar 

  • Eaves AA, Palmer AR (2003) Widespread cloning in echinoderm larvae. Nature 425:146

    Article  PubMed  CAS  Google Scholar 

  • Folt CL, Burns CW (1999) Biological drivers of zooplankton patchiness. Trends Ecol Evol 14:300–305

    Article  PubMed  Google Scholar 

  • Forward RB, Rittschof D (1999) Brine shrimp larval photoresponses involved in diel vertical migration: activation by fish mucus and modified amino sugars. Limnol Oceanogr 44:1904–1916

    CAS  Google Scholar 

  • Forward RB, Rittschof D (2000) Alteration of photoresponses involved in diel vertical migration of a crab larva by fish mucus and degradation products of mucopolysaccharides. J Exp Mar Biol Ecol 245:277–292

    Article  PubMed  CAS  Google Scholar 

  • Genin A, Jaffe JS, Reef R, Franks PJS (2005) Swimming against the flow: a mechanism of zooplankton aggregation. Science 308:860–862

    Article  PubMed  Google Scholar 

  • Gill AB, Hart PJB (1998) Stomach capacity as a directing factor in prey size selection of three-spined stickleback. J Fish Biol 53:897–900

    Article  Google Scholar 

  • Grünbaum D (2001) Predicting availability to consumers of spatially and temporally variable resources. Hydrobiologia 480:175–191

    Article  Google Scholar 

  • Harvell CD (1986) The ecology and evolution of inducible defenses in a marine bryozoan. Am Nat 128:810–823

    Article  Google Scholar 

  • Highsmith RC (1982) Induced settlement and metamorphosis of sand dollar (Dendraster excentricus) larvae in predator-free sites: adult sand dollar beds. Ecology 63:329–337

    Article  Google Scholar 

  • Iglesias C, Mazzeo N, Goyenola G, Fosalba C, De Mello FT, Garcia S, Jeppesen E (2008) Field and experimental evidence of the effect of Jenynsia multidentata, a small omnivorous-planktivorous fish, on the size distribution of zooplankton in subtropical lakes. Freshw Biol 53:1797–1807

    Article  Google Scholar 

  • Jaeckle WB (1994) Multiple-modes of asexual reproduction by tropical and subtropical sea star larvae—an unusual adaptation for genet dispersal and survival. Biol Bull 186:62–71

    Article  Google Scholar 

  • Jang MH, Ha K, Joo G, Takamura N (2003) Toxic production of cyanobacteria is increased by exposure to zooplankton. Freshw Biol 48:1540–1550

    Article  Google Scholar 

  • Knott KE, Balser EJ, Jaeckle WB, Wray GA (2003) Identification of asteroid genera with species capable of larval cloning. Biol Bull 204:246–255

    Article  PubMed  CAS  Google Scholar 

  • Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton

    Google Scholar 

  • Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Marshall DJ, Keough MJ (2008) The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol 53:1–60

    Article  Google Scholar 

  • McCollum SA, Leimberger JD (1997) Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109:615–621

    Article  Google Scholar 

  • McDonald K, Vaughn D (2010) An abrupt change in food environment induces cloning in Dendraster excentricus plutei. Biol Bull (in press)

  • Menden-Deuer S (2006) Individual foraging behaviors and population distributions of planktonic predators to phytoplankton thin layers. Limnol Oceanogr 45:569–579

    Article  Google Scholar 

  • Menden-Deuer S (2008) Spatial and temporal characteristics of plankton-rich layers in a shallow, temperate fjord. Mar Ecol Prog Ser 355:21–30

    Article  Google Scholar 

  • Metaxas A (2001) Behaviour in flow: perspectives on the distribution and dispersion of meroplanktonic larvae in the water column. Can J Fish Aquat Sci 58:86–98

    Article  Google Scholar 

  • Metaxas A, Young CM (1998) Response of echinoid larvae to food patches of different algal densities. Mar Biol 130:433–445

    Article  Google Scholar 

  • Miner BG (2004) Evolution of feeding structure plasticity in marine invertebrate larvae: a possible trade-off between arm length and stomach size. J Exp Mar Biol Ecol 315:117–125

    Article  Google Scholar 

  • O’Brien WJ (1979) The predator-prey interaction of planktivorous fish and zooplankton. Am Sci 67:572–581

    Google Scholar 

  • Padilla DK, Adolph SC (1996) Plastic inducible morphologies are not always adaptive: the importance of time delays in a stochastic environment. Evol Ecol 10:456

    Article  Google Scholar 

  • Palmer AR (1990) Effect of crab effluent and scent of damaged conspecifics on feeding, growth, and shell morphology of the Atlantic dogwhelk Nucella lapillus. Hydrobiologia 193:155–182

    Article  Google Scholar 

  • Pennington JT, Rumrill SS, Chia FS (1986) Stage specific predation upon embryos and larvae of the Pacific sand dollar, Dendraster excentricus, by 11 species of common zooplankton predators. Bull Mar Sci 39:234–240

    Google Scholar 

  • Ruehl CB, DeWitt TJ (2005) Trophic plasticity and fine-grained resource variation in populations of western mosquitofish, Gambusia affinis. Evol Ecol Res 7:801–819

    Google Scholar 

  • Schabetsberger R, Luger MS, Drozdowski G, Jagsch A (2009) Only the small survive: monitoring long-term changes in the zooplankton community of an Alpine lake after fish introduction. Biol Invasions 11:1335–1345

    Article  Google Scholar 

  • Selander E, Thor P, Toth GB, Pavia H (2006) Copepods induce paralytic shellfish toxin production in marine dinoflagellates. Proc R Soc Lond 273:1673–1680

    Article  CAS  Google Scholar 

  • Seuront L, Schmitt F, Lagadeuc Y (2001) Turbulence intermittency, small-scale phytoplankton patchiness and encounter rates in the plankton: where do we go from here? Deep Sea Res 48:1199–1215

    Article  Google Scholar 

  • Sewell MA, Cameron MJ, McArdle B (2004) Developmental plasticity in larval development in the echinometrid sea urchin Evechinus chloroticus with varying food ration. J Exp Mar Biol Ecol 309:219–237

    Article  Google Scholar 

  • Sih A (2004) A behavioral ecological view of phenotypic plasticity. In: Dewitt TJ, Scheiner SM (eds) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, New York, pp 112–125

    Google Scholar 

  • Strathmann RR (1971) The behavior of planktotrophic echinoderm larvae: mechanisms, regulation, and rates of suspension feeding. J Exp Mar Biol Ecol 6:109–160

    Article  Google Scholar 

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

    Google Scholar 

  • Strathmann RR (1996) Are planktonic larvae of marine benthic invertebrates too scarce to compete within species? Oceanol Acta 19:399–407

    Google Scholar 

  • Strathmann RR, Fenaux L, Strathmann MF (1992) Heterochronic developmental plasticity in larval sea urchins and its implications for evolution of nonfeeding larvae. Evolution 46:972–986

    Article  Google Scholar 

  • Suchman CL, Sullivan BK (2000) Effect of prey size on vulnerability of copepods to predation by scyphomedusae Aurelia aurita and Cyanea sp. J Plankton Res 22:2289–2306

    Article  Google Scholar 

  • Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defenses. Princeton University Press, Princeton

    Google Scholar 

  • Trussell GC (1996) Phenotypic plasticity in an intertidal snail: the role of a common crab predator. Evolution 50:448–454

    Article  Google Scholar 

  • Van Der Stap I, Vos M, Verschoor AM, Helmsing NR, Mooij WM (2007) Induced defenses in herbivores and plants differentially modulate a trophic cascade. Ecology 88:2474–2481

    Article  PubMed  Google Scholar 

  • Van Donk E (2007) Chemical information transfer in freshwater plankton. Ecol Inf 2:112–120

    Article  Google Scholar 

  • Vaughn D (2007) Predator-induced morphological defenses in marine zooplankton: a larval case study. Ecology 88:1030–1039

    Article  PubMed  Google Scholar 

  • Vaughn D (2009) Predator-induced larval cloning in the sand dollar Dendraster excentricus: might mothers matter? Biol Bull 217:103–114

    PubMed  Google Scholar 

  • Vaughn D, Strathmann RR (2008) Predators induce cloning in echinoderm larvae. Science 319:1503

    Article  PubMed  CAS  Google Scholar 

  • Vickery MCL, McClintock JB (1998) Regeneration in metazoan larvae. Nature 394:140

    Article  CAS  Google Scholar 

  • Vickery MS, McClintock JB (2000) Effects of food concentration and availability on the incidence of cloning in planktotrophic larvae of the sea star Pisaster ochraceus. Biol Bull 199:298–304

    Article  PubMed  CAS  Google Scholar 

  • Vos M, Verschoor AM, Kooi BW, Wackers FL, DeAngelis DL, Mooij WM (2004) Inducible defenses and trophic structure. Ecology 85:2783–2794

    Article  Google Scholar 

  • Vos M, Vet LEM, Wackers FL, Middleburg JJ, van der Putten WH, Mooji WM, Heip CHR, Van Donk E (2006) Infochemicals structure marine, terrestrial and freshwater food webs: implications for ecological informatics. Ecol Inf 1:23–32

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Werner EE, Hall DJ (1974) Optimal foraging and the size selection of prey by bluegill sunfish (Lepomis macrochirus). Ecology 55:1042–1052

    Article  Google Scholar 

  • Woodson CB, McManus MA (2007) Foraging behavior can influence dispersal of marine organisms. Limnol Oceanogr 52:2701–2709

    Google Scholar 

  • Woodson CB, Webster DR, Weissburg MJ, Yen J (2005) Response of copepods to physical gradients associated with structure in the ocean. Limnol Oceanogr 50:1552–1564

    Article  Google Scholar 

Download references

Acknowledgments

NSF grant OCE0623102 to R. R. Strathmann, the Friday Harbor Laboratories, and the ARCS Foundation supported this study. I thank R. R. Strathmann, M. F. Strathmann, E. Dusek, R. Kodner, and K. Vaughn for advice and assistance and two anonymous reviewers for comments that improved the manuscript. I also thank P. Kitaeff and the 2008 class in Functional Morphology and Ecology of Marine Fishes at the FHL for collection of the predatory fish used in this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dawn Vaughn.

Additional information

Communicated by U. Sommer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vaughn, D. Why run and hide when you can divide? Evidence for larval cloning and reduced larval size as an adaptive inducible defense. Mar Biol 157, 1301–1312 (2010). https://doi.org/10.1007/s00227-010-1410-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-010-1410-z

Keywords

Navigation