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Sublethal effects on reproduction in native fauna: are females more vulnerable to biological invasion?

Abstract

Although invasive species are a major threat to survivorship of native species, we know little about their sublethal effects. In soft-sediment marine systems, mat-forming invasive species often have positive effects, facilitating recruitment and enhancing the diversity and abundance of native invertebrates. However, because mat-forming invasive species change the habitat in which they invade, and benthic invertebrates are sensitive to environmental disturbance, important sublethal effects on native species may exist. Using a model marine system we show that the widespread mat-forming invasive alga Caulerpa taxifolia (Vahl) C. Agardh has strong negative effects on the reproductive traits of a native bivalve Anadara trapezia (Deshayes, 1840) (e.g. timing of reproductive development and spawning, and follicle and gamete production) even though the invader has positive effects on recruitment. Moreover, gender specific responses occurred and indicated that females were more susceptible to invasion than males. Our results indicate that sublethal effects of an invasive species on reproductive traits will have severe consequences for fitness of the native species.

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References

  1. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with imageJ. Biophotonics Int 11:36–42

  2. Allen BJ, Williams SL (2003) Native eelgrass Zostera marina controls growth and reproduction of an invasive mussel through food limitation. Mar Ecol Prog Ser 254:57–67

  3. Bayne BL, Holland DL, Moore MN, Lowe DM, Widdows J (1978) Further studies on the effects of stress in the adult on the eggs of Mytilus edulis. J Mar Biolog Assoc UK 58:825–841

  4. Bayne BL, Salkeld PN, Worrall CM (1983) Reproductive effort and value in different populations of the marine mussel, Mytilus edulis. Oecologia 59:18–26

  5. Bellan-Santini D, Arnaud PM, Bellan G, Verlaque M (1996) The influence of the introduced alga, Caulerpa taxifolia, on the biodiversity of the Mediterranean marine biota. J Mar Biolog Assoc UK 76:235–237

  6. Bolam SG, Fernandes TF (2002) The effects of macroalgal cover on the spatial distribution of macrobenthic invertebrates: the effect of macroalgal morphology. Hydrobiologia 475–476:437–448

  7. Brody MS, Edgar MH, Lawlor LR (1983) A cost of reproduction in a terrestrial isopod. Evolution 37:653–655

  8. Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinuaer, Sunderland, pp 201–218

  9. Carmichael RH, Shriver AC, Valiela I (2004) Changes in shell and soft tissue growth, tissue composition, and survival of quahogs, Mercenaria mercenaria, and softshell clams, Mya arenaria, in response to eutrophic-driven changes in food supply and habitat. J Exp Mar Biol Ecol 313:75–104

  10. Ceccherelli G, Cinelli F (1999) Effects of Posidonia oceania canopy on Caulerpa taxifolia size in a northwestern Mediterranean bay. J Exp Mar Biol Ecol 240:19–36

  11. Chisholm JRM, Moulin P (2003) Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta). Limnol Oceanogr 48:797–794

  12. Creese RG, Davies AR, Glasby TM (2004) Eradicating and preventing the spread of the invasive alga Caulerpa taxifolia in NSW. NSW Fish Final Rep, Ser 64, p 110

  13. Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser 162:137–152

  14. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166

  15. D’Antonio CM, Mahall BE (1991) Root profiles and competition between the invasive exotic perennial, Carpobrotus edulis, and two native shrub species in California coastal scrub. Am J Bot 78:885–894

  16. Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar Biol Annu Rev 33:345–303

  17. Elkin EM, Reid ML (2005) Low energy reserves and energy allocation decisions affect reproduction by mountain pine beetles, Dendroctonus ponderosae. Funct Ecol 19:102–109

  18. Equihua M, Usher MB (1993) Impact of carpets of the invasive moss Campylopus introflexus on Calluna vulgaris regeneration. J Ecol 81:359–365

  19. Eversole AG (1989) Gametogenesis and spawning in North American clam populations: implications for culture. In: Manzi JJ, Castagna M (eds) Developments in aquaculture and fisheries science, Clam Mariculture in North America, vol 19. Elsevier, Amsterdam, pp 75–109

  20. George SB, Fenaux L, Lawrence JM (1991) The effect of food ration on the quality of eggs of Luidia clathrata (Say) (Echinodermata: Asteroidea). Invertebr Reprod Dev 20:237–242

  21. Ghislen MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208

  22. Gribben PE, Wright JT (2006) Invasive seaweed enhances recruitment of a native bivalve: roles of refuge from predation and habitat choice. Mar Ecol Prog Ser (in press)

  23. Gribben PE, Helson J, Jeffs AG (2004) Reproductive cycle of the New Zealand geoduck, Panopea zelandica, in two North Island populations. Veliger 47:59–71

  24. Hadfield AJ, Anderson DT (1988) Reproductive cycles of the bivalve molluscs Anadara trapezia (Deshayes), Venerupis crenata Lamarck and Anomia descripta Iredale in the Sydney region. Aust J Mar Freshw Res 39:649–660

  25. Harvey M, Vincent B (1989) Spatial and temporal variations of the reproduction cycle and energy allocation of the bivalve Macoma balthica (L.) on a tidal flat. J Exp Mar Biol Ecol 129:199–217

  26. Jaeckle WB (1995) Variation in size, energy content, and biochemical composition of invertebrate eggs: correlates of the mode of larval development. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC, Boca Raton, pp 49–78

  27. Jones ZF, Bock CE (2005) The Botteri’s sparrow and exotic Arizona grasslands: an ecological trap or habitat regained? Condor 107:731–741

  28. Jousson O, Pawlowski J, Zaninetti L, Zechman FW, Dini F, Di Guiseppe G, Woodfield R, Millar AJK, Meinesz A (2000) Invasive alga reaches California. Nature 408:157–158

  29. Keck RT, Maurer D, Lind H (1975) A comparative study of the hard clam gonad development cycle. Biol Bull 148:243–258

  30. Koops MA, Hutchings JA, Adams BK (2003) Environmental predictability and the cost of imperfect information: influences on offspring size variability. Evol Ecol Res 5:29–42

  31. Lenihan HS, Micheli F (2001) Soft sediment communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinuaer, Sunderland, pp 253–288

  32. Levi F, Francour P (2004) Behavioural response of Mullus surmuletus to habitat modification by the invasive macroalga Caulerpa taxifolia. J Fish Biol 64:55–64

  33. Levine JM, Vilá M, D’Antonio CM, Dukes JF, Grigulis K, Lavorel S (2002) Mechanisms underlying the impacts of exotic plant invasion. Proc R Soc Lond B 270:775–881

  34. Levitan DR (1991) Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. Biol Bull 181:261–268

  35. Levitan DR (1995) The ecology of fertilization in free-spawning invertebrates. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC, Boca Raton, pp 123–156

  36. Longepierre S, Robert A, Levi F, Francour P (2005) How an invasive alga species (Caulerpa taxifolia) induces changes in foraging strategies of the benthivorous fish Mullus surmuletus in coastal Mediterranean ecosystems. Biodivers Conserv 14:365–376

  37. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

  38. Mackie GL (1984) Bivalves. In: Tompa AS, Verdonk NH, van den Biggelaar JAM (eds) Reproduction, vol 7. Academic, New York, pp 351–418

  39. Marshall DJ, Keough MJ (2003) Variation in the dispersal potential of non-feeding larvae: the desperate larva hypothesis and larval size. Mar Ecol Prog Ser 255:145–153

  40. Meinesz A, Benishou L, Blacher J, Komatsu T, Lemee R, Molenaar H, Mari X (1995) The introduced green alga Caulerpa taxifolia in the Mediterranean sea. Bot Mar 38:499–508

  41. McGinley MA, Temme DH, Geber MA (1987) Parental investment in offspring in variable environments: theoretical and empirical considerations. Am Nat 130:370–398

  42. Moran AL, Emlet RB (2001) Offspring size and performance in variable environments: field studies on a marine snail. Ecology 82:1597–1612

  43. Neira C, Levin LA, Grosholz ED (2005) Benthic macrofaunal communities of three sites in San Francisco Bay invaded by hybrid Spartina, with comparison to uninvaded habitats. Mar Ecol Prog Ser 292:111–126

  44. Oliver J, Babcock R (1992) Aspects of the fertilization ecology of broadcast spawning corals: sperm dilution effects and in situ measurements of fertilization. Biol Bull 183:409–418

  45. Pennington JT (1985) The ecology of fertilization of echinoid eggs: the consequence of sperm dilution, adult aggregation, and synchronous spawning. Biol Bull 169:417–430

  46. Peterson CH, Kennicutt MC, Green RH, Harper DE Jr, Powell EN, Roscigno PF (1996) Ecological consequences of environmental perturbations associated with offshore hydrocarbon production: a perspective on long-term exposure in the Gulf of Mexico. Can J Fish Aquat Sci 53:2637–2654

  47. Posey MH (1988) Community changes associated with the spread of an introduced seagrass, Zostera japonica. Ecology 69:974–983

  48. Remes V (2003) Effects of exotic habitat on nesting success, territory density, and settlement patterns in the Blackcap (Sylvia atricapilla). Conser Biol 17:1127–1133

  49. Schlaepfer MA, Sherman PW, Blossey B, Runge MC (2005) Introduced species as evolutionary traps. Ecol Lett 8:241–246

  50. Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506

  51. Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

  52. Thompson RJ (1982) The relationship between food ration and reproductive effort in the green sea urchin, Strongylocentrotus droebachiensis. Oecologia 56:50–57

  53. Wonham MJ, O’Connor M, Harley CDG (2005) Positive effects of a dominant invader on introduced and native mudflat species. Mar Ecol Prog Ser 289:109–116

  54. Wright JT (2005) Differences between native and invasive Caulerpa taxifolia: a link between asexual fragmentation and abundance in invasive populations. Mar Biol 147:559–569

  55. Wright WG (1988) Sex change in the Mollusca. Trends Ecol Evol 3:137–140

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Acknowledgements

Thanks to Dr. Steve Bonser who provided valuable comments on an earlier draft of the manuscript. We also thank Louise MacKenzie for her valuable assistance with the collection of animals and video image analysis, and the histological unit, School of Medicine, University of New South Wales, for processing samples.

Author information

Correspondence to Paul E. Gribben.

Additional information

Communicated by Martin Attrill

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Gribben, P.E., Wright, J.T. Sublethal effects on reproduction in native fauna: are females more vulnerable to biological invasion?. Oecologia 149, 352 (2006). https://doi.org/10.1007/s00442-006-0452-x

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Keywords

  • Caulerpa taxifolia
  • Invasion biology
  • Life history
  • Reproductive traits
  • Sex ratios