Advertisement

Marine Biology

, Volume 159, Issue 10, pp 2359–2365 | Cite as

Avoidance of feeding opportunities by the whelk Buccinanops globulosum in the presence of damaged conspecifics

  • Pedro DaleoEmail author
  • Juan Alberti
  • Maria Soledad Avaca
  • Maite Narvarte
  • Paulina Martinetto
  • Oscar Iribarne
Original Paper

Abstract

Feeding decisions under predation risk can be a key in the life of scavenger organisms, and tuned recognition of predation alarm cues and flexibility in the response are fundamental. The effect of injured conspecifics on the response behavior of the whelk Buccinanops globulosum to feeding opportunities was experimentally evaluated in a Patagonian Bay (40°45′S, 64°56′W, Argentina) in September 2010. The effect of sex, size, body condition, or starvation on anti-predatory behavior was assessed. The number of B. globulosum feeding on carrion was reduced by half when damaged conspecifics were present. Smaller, lighter, and starved individuals responded less to the presence of damaged conspecifics. These results indicate that, under natural conditions, feeding avoidance after detecting damaged conspecifics is a common and important anti-predatory strategy of B. globulosum and show that morphology and starvation are significant factors in the context of the trade-off between feeding and avoiding predation risk.

Keywords

Predation Risk Shell Length Shell Width Shell Weight Shell Hardness 
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.

Notes

Acknowledgments

We thank Dr. J.P. Grassle and two anonymous referees for valuable comments in the manuscript. This project was supported by grants from the Universidad Nacional de Mar del Plata, the Fundación Antorchas, CONICET and ANPCyT (all granted to O.I.) and PICT CONAE-CONICET 04/2010 (granted to M.N.). M.S.A was supported by a Postdoctoral scholarship from CONICET (Argentina).

References

  1. Alexander JE Jr, Covich AP (1991) Predation risk and avoidance behavior in two freshwater snails. Biol Bull 180:387–393CrossRefGoogle Scholar
  2. Avaca MS (2011) Estudio comparativo de la estructura demográfica y de las características biológicas del caracol Buccinanops globulosus en los golfos norpatagónicos. Tesis Doctoral de la Universidad Nacional del Sur, UNS, Bahía BlancaGoogle Scholar
  3. Avaca MS, Narvarte M, Martín PR (2010) Description of the radula of Buccinanops globulosum (Neogastropoda, Nassaridae), and an assessment of its variability in Patagonian gulfs. Malacologia 53:175–184CrossRefGoogle Scholar
  4. Blum MS (1969) Alarm pheromones. Annu Rev Entomol 14:57–80CrossRefGoogle Scholar
  5. Bordeau PE (2010) An inducible morphological defense is a passive by-product of behaviour in a marine snail. Proc R Soc B 277:455–462CrossRefGoogle Scholar
  6. Britton JC, Morton B (1994) Marine carrion and scavengers. Oceanogr Mar Biol Annu Rev 32:369–434Google Scholar
  7. Brookers JI, Rochette R (2007) Mechanisms of plastic phenotypic response: predator-induced shell thickening in the intertidal gastropod Littorina obtusata. J Evol Biol 20:1015–1027CrossRefGoogle Scholar
  8. Brown GE, Adrian JC, Naderi NT, Harvey MC, Kelly JM (2003) Nitrogen oxides elicit antipredator responses in juvenile channel catfish, but not in convict cichlids or rainbow trout: conservation of the ostariophysan alarm pheromone. J Chem Ecol 29:1781–1796CrossRefGoogle Scholar
  9. Chivers DP, Smith RJF (1998) Chemical alarm signaling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5:338–352Google Scholar
  10. 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 92:135–142CrossRefGoogle Scholar
  11. Cotton PA, Rundle SD, Smith KE (2004) Trait compensation in marine gastropods: shell shape, avoidance behavior, and susceptibility to predation. Ecology 85:1581–1584CrossRefGoogle Scholar
  12. Crowl TA, Covich AP (1990) Predator-induced life-history shifts in a freshwater snail. Science 247:949–951CrossRefGoogle Scholar
  13. Cuthill IC, Houston AI (1997) Managing time and energy. In: Krebs JR, Davies NB Jr (eds) Behavioural ecology: an evolutionary approach. Blackwell, OxfordGoogle Scholar
  14. Daleo P, Escapa M, Isacch JP, Ribeiro P, Iribarne O (2005) Trophic facilitation by the oystercatcher Haematopus palliatus Temminick on the scavenger snail Buccinanops globulosum Kiener in a Patagonian bay. J Exp Mar Biol Ecol 325:27–34CrossRefGoogle Scholar
  15. Daleo P, Silliman B, Alberti J, Escapa M, Canepuccia A, Peña N, Iribarne O (2009) Grazer facilitation of fungal infection and the control of plant growth in south-western Atlantic salt marshes. J Ecol 97:781–787CrossRefGoogle Scholar
  16. Davenport J, Moore PG (2002) Behavioural responses of the netted dogwhelk Nassarius reticulatus to olfactory signals derived from conspecifics and nonconspecific carrion. J Mar Biol Assess UK 82:967–969CrossRefGoogle Scholar
  17. Dewitt TJ, Sih A, Hucko JA (1999) Trait compensation and cospecialization in a freshwater snail: size, shape and antipredator behaviour. Anim Behav 58:397–407CrossRefGoogle Scholar
  18. Ferner MC, Smee DL, Chang Y (2005) Cannibalistic crabs respond to the scent of injured conspecifics: danger or dinner? Mar Ecol Prog Ser 300:193–200CrossRefGoogle Scholar
  19. Garcia GO, Isacch JP, Gomes Laich A, Albano M, Favero M, Cardoni DA, Luppi T, Iribarne O (2010) Foraging behaviour and diet of the American oystercatcher in a Patagonian intertidal area affected by nutrient loading. Emu 110:146–154CrossRefGoogle Scholar
  20. González PM, Piersma T, Verkuil Y (1996) Food, feeding, and refuelling of Red Knots during northward migration at San Antonio Oeste, Río Negro, Argentina. J Field Ornithol 67:575–591Google Scholar
  21. Hartman EJ, Abrahams MV (2000) Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proc Roy Soc B 267:571–575CrossRefGoogle Scholar
  22. Iribarne OO (1990) Use of shelter by the small Patagonian octopus Octopus tehuelchus: availability, selection and effects on fecundity. Mar Ecol Prog Ser 66:251–258CrossRefGoogle Scholar
  23. Isacch JP, Costa CBS, Rodrıguez-Gallego L, Conde D, Escapa M, Gagliardini DA, Iribarne OO (2006) Distribution of saltmarsh plant communities associated with environmental factors along a latitudinal gradient in the south-west Atlantic coast. J Biogeogr 33:888–900CrossRefGoogle Scholar
  24. Jacobsen HP, Stabell OB (2004) Antipredator behaviour mediated by chemical cues: the role of conspecific alarm signalling and predator labelling in the avoidance response of a marine gastropod. Oikos 104:43–50CrossRefGoogle Scholar
  25. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  26. 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
  27. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  28. Magurran AE, Irving PW, Henderson PA (1996) Is there a fish alarm pheromone? A wild study and critique. Proc Roy Soc B 229:1551–1556CrossRefGoogle Scholar
  29. McCormick MI, Larson JK (2007) Field verification of the use of chemical alarm cues in a coral reef fish. Coral Reefs 26:571–576CrossRefGoogle Scholar
  30. McKillup SC, Butler AJ (1979) Modification of egg production and packaging in response of food availability by Nassarius pauperatus. Oecologia 43:222–231CrossRefGoogle Scholar
  31. McKillup SC, McKillup RV (1994) The decision to feed by a scavenger in relation to the risks of predation and starvation. Oecologia 97:41–48CrossRefGoogle Scholar
  32. McKillup SC, McKillup RV (1997) The effect of supplemental feeding on the growth of an intertidal scavenger. Mar Ecol Prog Ser 148:109–114CrossRefGoogle Scholar
  33. Morton B, Chan K (1999) Hunger rapidly overrides the risk of predation in the subtidal scavenger Nassarius siquijorensis (Gastropoda: nassariidae): an energy budget and a comparison with the intertidal Nassarius festivus in Hong Kong. J Exp Mar Biol Ecol 240:213–228CrossRefGoogle Scholar
  34. Morton B, Jones DS (2003) The dietary preferences of a suite of carrion-scavenging gastropods (Nassariidae, Buccinidae) in Princess Royal Harbour, Albany, Western Australia. J Moll Stud 69:151–156CrossRefGoogle Scholar
  35. Narvarte M, Willers V, Avaca S, Echave ME (2008) Population structure of the snail Buccinanops globulosum (Prosobranchia, Nassariidae) in San Matías Gulf, Patagonia Argentina: isolated enclaves? J Sea Res 60:144–150CrossRefGoogle Scholar
  36. Pfeiffer W (1977) Distribution of fright reaction and alarm substance cells in fishes. Copeia 1977:653–665CrossRefGoogle Scholar
  37. Rochette R, Himmelman JH (1996) Does vulnerability influence trade-offs made by whelks between predation risk and feeding opportunities? Anim Behav 52:783–794CrossRefGoogle Scholar
  38. Rochette R, Tétreault F, Himmelman JH (2001) Aggregation of whelks, Buccinum undatum, near feeding predators: the role of reproductive requirements. Anim Behav 61:31–41CrossRefGoogle Scholar
  39. Rundle SD, Brönmark C (2001) Inter- and intraspecific trait compensation of defence mechanisms in freshwater snails. Proc Roy Soc Lon B 268:1463–1468CrossRefGoogle Scholar
  40. Rundle SD, Spicer JI, Coleman RA, Vasper J, Soane J (2004) Environmental calcium modifies induced defenses in snails. Proc Roy Soc Lond B 271:S67–S70CrossRefGoogle Scholar
  41. Scarabino V (1977) Moluscos del Golfo San Matías (Prov. de Río Negro, Rca. Argentina). Inventario y claves para su identificación. Comunic Soc Malacol Uruguay 4:177–297Google Scholar
  42. Schoeppner NM, Relyea RA (2005) Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defenses. Ecol Lett 8:505–512CrossRefGoogle Scholar
  43. Soto RE, Castilla JC, Bozinovic F (2005) The impact of physiological demands on foraging decisions under predation risk: a test with the whelk Acanthina monodon. Ethology 111:1044–1049CrossRefGoogle Scholar
  44. Spitze K (1992) Predator-mediated plasticity of prey life history and morphology: Chaoborus americanus predation on Daphnia pulex. Am Nat 139:229–247CrossRefGoogle Scholar
  45. Trussell GC (1996) Phenotypic plasticity in an intertidal snail: the role of a common crab predator. Evolution 50:448–454CrossRefGoogle Scholar
  46. Trussell GC, Nicklin MO (2002) Cue sensitivity, inducible defense, and trade-offs in a marine snail. Ecology 83:1635–1647CrossRefGoogle Scholar
  47. Trussell CC, Smith LD (2000) Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proc Natl Acad Sci USA 97:2123–2127CrossRefGoogle Scholar
  48. Turner AM (2008) Predator diet and prey behaviour: freshwater snail discriminate among closely related prey in a predator’s diet. Anim Behav 76:1211–1217CrossRefGoogle Scholar
  49. Wisenden BD, Vollbrecht KA, Brown JL (2004) Is there a fish alarm cue? Affirming evidence from a wild study. Anim Behav 67:59–67CrossRefGoogle Scholar
  50. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Pedro Daleo
    • 1
    • 2
    Email author
  • Juan Alberti
    • 1
    • 2
  • Maria Soledad Avaca
    • 2
    • 3
  • Maite Narvarte
    • 2
    • 3
  • Paulina Martinetto
    • 1
    • 2
  • Oscar Iribarne
    • 1
    • 2
  1. 1.Lab. Ecología, Dpto. Biología, Facultad de Ciencias Exactas y Naturales, Instituto de Investigaciones Marinas y Costeras (IIMyC), CONICET–UNMDPUniversidad Nacional de Mar del PlataMar del PlataArgentina
  2. 2.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos AiresArgentina
  3. 3.Instituto de Biología Marina y Pesquera Almirante StorniSan Antonio OesteArgentina

Personalised recommendations