Biological Invasions

, Volume 3, Issue 2, pp 137–149 | Cite as

Invasion of a Reef-builder Polychaete: Direct and Indirect Impacts on the Native Benthic Community Structure

  • Evangelina Schwindt
  • Alejandro Bortolus
  • Oscar Osvaldo Iribarne
Article

Abstract

In this work, we evaluate the effect of the introduced reef-building polychaete Ficopomatus enigmaticus on the benthic community and on sediment characteristics of a southwestern Atlantic coastal lagoon. When reefs were experimentally added, density of the native crab Cyrtograpsus angulatus dramatically increased in a short time period. After reefs and crabs were experimentally transplanted as a unit, they decreased the density of the free-living soft-bottom polychaetes Heteromastus similis and Laeonereis acuta. Exclusion/inclusion caging experiments showed that Cyrtograpsus negatively affect the density of soft-bottom polychaetes (H. similis, L. acuta, Nephtys fluviatilis) and ostracodes. Our results showed that this effect is much higher in areas populated by reefs because of the increased density of crabs that find shelter under the reefs. Thus, reefs have a cascading effect on the native benthic community within the areas colonized by them. Analysis of crab stomach contents indicated that crabs feed on a wide variety of prey, including infaunal organisms, small gastropods and also algae. When reefs and crabs were experimentally added, the amount of bivalve shells on superficial sediments increased. Our results suggest that this bivalve shell accumulation and sediment composition are due to the reworking activity of Cyrtograpsus in the sediment where they dig burrows. The invasive habits of Ficopomatus may be favoring crabs to have a major effect on the integrity of the native community in the lagoon. Ficopomatus should be considered a bioengineer organism by creating and regulating refuge for other species, altering the interactions between preexistent species and also by changing the physical factors of the invaded environment.

crabs ecosystem engineer exotic species Ficopomatus polychaete predation reef 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bertness MD (1985) Fiddler crab regulation of Spartina alterniflora production on aNewEngland salt marsh. Ecology 66: 1042-1055Google Scholar
  2. Bertness MD (1999) The Ecology of Atlantic Shorelines. Sinauer Associates, Sunderland, Massachusetts, 417 ppGoogle Scholar
  3. Bianchi CN andMorri C (1996) Ficopomatus ‘reefs’ in the Po River Delta (Northern Adriatic): their constructional dynamics, biology, and influences on the brackish-water biota. P.S.Z.N.I: Marine Ecology 17: 51-66Google Scholar
  4. Bortolus A andIribarne O (1999) Effects of the SW Atlantic burrowing crab Chasmagnathus granulata on a Spartina salt marsh. Marine Ecology Progress Series 178: 79-88Google Scholar
  5. Bortolus A,Iribarne O andMartínez MM (1998) Relationship between waterfowl and seagrass Ruppia maritima in a southwestern Atlantic coastal lagoon. Estuaries 21: 710-717Google Scholar
  6. Botto F andIribarne O (1999) Effect of the burrowing crab Chasmagnathus granulata (Dana) on the benthic community of a SW Atlantic coastal lagoon. Journal of Experimental Marine Biology and Ecology 241: 263-284Google Scholar
  7. Botto F andIribarne O (2000) Contrasting effects of two burrowing crabs (Chasmagnathus granulata and Uca uruguayensis) on sediment composition and transport in estuarine environments. Estuarine Coastal and Shelf Science 51: 141-151Google Scholar
  8. Capehart AA andHackney CT (1989) The potential role of roots and rhizomes in structuring salt-marsh benthic communities. Estuaries 12: 119-122Google Scholar
  9. Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biological Conservation 78: 97-106Google Scholar
  10. Carlton JT,Thompson JK,Schemel LE andNichols FH (1990) Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. I. Introduction and dispersal. Marine Ecology Progress Series 66: 81-94Google Scholar
  11. Carver RE (1971) Procedures in Sedimentary Petrology. Wiley Interscience, New York, 653 ppGoogle Scholar
  12. Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Marine Ecology Progress Series 162: 137-152Google Scholar
  13. Crooks JA andKhim HS (1999) Architectural vs. biological effects of a habitat-altering, exotic mussel, Musculista senhousia. Journal of Experimental Marine Biology and Ecology 240: 53-75Google Scholar
  14. Dahlgren CP,Posey MH andHulbert AW (1999) The effects of bioturbation on the infaunal community adjacent to an offshore hardbottom reef. Bulletin of Marine Science 64: 21-34Google Scholar
  15. Day JW,Hall CAS,Kemp WM andYañez Arancibia A (1989) Estuarine Ecology. John Wiley & Sons, New York, 558 ppGoogle Scholar
  16. Diaz RJ andRosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanography Marine Biology: An Annual Review 33: 245-303Google Scholar
  17. Eckman JE (1983) Hydrodynamic processes affecting benthic recruitment. Limnology and Oceanography 28: 241-257Google Scholar
  18. Eckman JE,Nowell ARM andJumars PA (1981) Sediment destabilization by animal tubes. Journal of Marine Research 39: 361-374Google Scholar
  19. Fasano JL,Hernández MA,Isla FI andSchnack EJ (1982) Aspectos evolutivos y ambientales de la laguna Mar Chiquita (Provincia de Buenos Aires, Argentina). Oceanologica Acta N?SP: 285-292Google Scholar
  20. Fauvel P (1923) Un nouveau serpulien d'eau saumatre Mercierella n.g. enigmatica n. sp. Bulletin de la Société Zoologique de France 46: 424-430Google Scholar
  21. Fonseca MS andCahalan JA (1992) A preliminary evaluation of wave attenuation by four species of seagrasses. Estuarine Coastal and Shelf Science 35: 565-576Google Scholar
  22. Gherardi F andCassidy PM (1994) Sabellarian tubes as the housing of the hermit crab Discorsopagurus schmitti. Canadian Journal of Zoology 72: 526-532Google Scholar
  23. Gray JS (1981) The Ecology of Marine Sediments. An Introduction to the Structure and Function of Benthic Communities. Cambridge University Press, Cambridge, London, 185 ppGoogle Scholar
  24. Haines JL andMaurer D (1980) Quantitative faunal associates with the serpulid polychaete Hydroides dianthus. Marine Biology 56: 43-47Google Scholar
  25. Hall SJ (1994) Physical disturbance and marine benthic communities: life in unconsolidated sediment. Oceanography Marine Biology: An Annual Review 32: 179-239Google Scholar
  26. Herman PMJ,Middelburg JJ,Van De Koppel J andHeip CHR (1999) Ecology of estuarine macrobenthos. In: Nedwell DB andRaffaelli DG ( eds) Advances in Ecological Research, pp 195-240. Academic Press, LondonGoogle Scholar
  27. Iribarne O,Bortolus A andBotto F (1997) Between-habitats differences in burrow characteristics and trophic modes in the south western Atlantic burrowing crab Chasmagnathus granulata. Marine Ecology Progress Series 155: 137-145Google Scholar
  28. Isla FI (1997) Seasonal behavior of Mar Chiquita tidal inlet in relation to adjacent beaches, Argentina. Journal of Coastal Research 13: 1221-1232Google Scholar
  29. Jones CG,Lawton JH andShachak M (1994) Organisms as ecosystems engineers. Oikos 69: 373-386Google Scholar
  30. Jones CG,Lawton JH andShachak M (1997) Positive and negative effects of organisms as physical engineers. Ecology 78: 1946-1957Google Scholar
  31. Kittelson PM andBoyd MJ (1997) Mechanism of expansion for an introduced species of cordgrass Spartina densiflora, in Humboldt Bay, California. Estuaries 20: 770-778Google Scholar
  32. Lenihan HS (1999) Physical-biological coupling on oyster reefs: how habitat structure influences individual performance. Ecological Monographs 69: 251-275Google Scholar
  33. Levin LA (1991) Interactions between metazoan and large, agglutinating protozoans: implications for the community structure of deep-sea benthos. American Zoologist 31: 886-900Google Scholar
  34. Levinton JS (1989) Deposit feeding on coastal oceanography. In: Lopez G,Taghon G andLevinton J (eds) Ecology of Marine Deposit Feeders. Lectures Notes on Coastal and Estuarine Studies, pp 1-23. Springer-Verlag, New York, 322 ppGoogle Scholar
  35. Lipcius RN andHines AH (1986) Variable functional responses of a marine predator in dissimilar homogeneous microhabitats. Ecology 67: 1361-1371Google Scholar
  36. Luppi T andBas C (2000) Papel de los arrecifes del poliqueto introducido Ficopomatus enigmaticus (Polychaeta, Serpulidae) en el reclutamiento de Cyrtograpsus angulatus (Brachyura, Grapsidae), en la laguna costera Mar Chiquita, Argentina. IV Jornadas Nacionales de Ciencias del Mar, Puerto Madryn, ArgentinaGoogle Scholar
  37. Manly BFJ (1997) Randomization, Bootstrap and Monte Carlo Methods in Biology. Chapman & Hall, London, 399 ppGoogle Scholar
  38. Miller DC andJumars PA (1986) Pellet accumulation, sediment supply, and crowding as determinants of surface deposit-feeding rate in Pseudopolydora kempi japonica Imajima & Hartman (Polychaeta: Spionidae). Journal of Experimental Marine Biology and Ecology 99: 1-17Google Scholar
  39. Netto SA andLana PC (1994) Effects of sediment disturbance on the structure of benthic fauna in a subtropical tidal creek of southeastern Brazil. Marine Ecology Progress Series 106: 239-247Google Scholar
  40. Nowell ARM andJumars P (1984) Flow environments of aquatic benthos. Annual Review of Ecology and Systematics 15: 303-328Google Scholar
  41. Obenat SM andPezzani SE (1994) Life cycle and population structure of the polychaete Ficopomatus enigmaticus (Serpulidae) in Mar Chiquita Coastal Lagoon, Argentina. Estuaries 17: 263-270Google Scholar
  42. ólafsson EB,Peterson CH andAmbrose WG Jr (1994) Does recruitment limitation structure populations and communities of macroinvertebrates in marine soft-sediments: the relative significance of pre-and post-settlement processes. Oceanography Marine Biology: An Annual Review 32: 65-109Google Scholar
  43. Olivier SR,Escofet A,Penchaszadeh P andOrensanz JM (1972) Estudios ecológicos de la región estuarial de Mar Chiquita (Buenos Aires, Argentina). ll. Relaciones tróficas interespecíficas. Anales de la Sociedad Científica Argentina 194: 89-104Google Scholar
  44. Orth RJ,Heck KL Jr andvan Montfrans J (1984) Faunal communities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries 7: 339-350Google Scholar
  45. Ruiz GM,Carlton JT,Grosholz ED andHines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. American Zoologist 37: 621-632Google Scholar
  46. Scholten M andRozema J (1990) The competitive ability of Spartina anglica on Dutch salt marshes. In: Gray AJ andBenham PEM (eds) Spartina anglica a Research Review. Institute of Terrestrial Ecology, Natural Environmental Research Council, LondonGoogle Scholar
  47. Schwindt E (2001) Efectos de una especie exótica formadora de arrecifes Ficopomatus enigmaticus en la laguna costera Mar Chiquita. Doctoral Thesis. Departamento de Biología, Universidad Nacional de Mar del Plata, Argentina, 145 ppGoogle Scholar
  48. Schwindt E andIribarne O (1998) Reef of Ficopomatus enigmaticus (Polychaeta; Serpulidae) in the Mar Chiquita coastal lagoon, Argentina. Bollet´i de la Societat d'Hist`oria Natural de les Balears 41: 35-40Google Scholar
  49. Schwindt E andIribarne O (2000) Settlement sites, survival and effects on benthos of an introduced reef-building polychaete in a SWAtlantic coastal lagoon. Bulletin of Marine Science 67: 73-82Google Scholar
  50. Snelgrove PVR andButman CA (1994) Animal-sediment relationship revisited: cause versus effect. Oceanography Marine Biology: An Annual Review 32: 111-177Google Scholar
  51. Spivak E,Anger K,Luppi T,Bas CT andIsmael D (1994) Distribution and habitat preferences of two grapsid crab species in Mar Chiquita Lagoon (Province of Buenos Aires, Argentina). Helgoländer Meeresunter 48: 59-78Google Scholar
  52. Strayer DL (1999) Effects of alien species on freshwater mollusks in North America. Journal of North American Benthological Society 18: 74-98Google Scholar
  53. Ten Hove HA andWeerdenburg JCA (1978) A generic revision of the brackish-water serpulid Ficopomatus Southern 1921 (Polychaeta: Serpulidae), including Mercierella Fauvel 1923, Sphaeropomatus Treadwell 1934, Mercierellopsis Rioja 1954, and Neopomatus Pillai 1960. Biological Bulletin 154: 96-120Google Scholar
  54. Valiela I (1995) Marine Ecological Processes. Springer-Verlag, New York, 686 ppGoogle Scholar
  55. Virnstein RW (1979) Predation on estuarine infauna: response patterns of component species. Estuaries 2: 69-86Google Scholar
  56. Vitousek PM (1990) Biological invasions and ecosystem processes: toward an integration of population biology and ecosystem studies. Oikos 57: 7-13Google Scholar
  57. Wilson WH Jr (1979) Community structure and species diversity of the sedimentary reefs constructed by Petaloproctus socialis (Polychaeta: Maldanidae). Journal of Marine Research 37: 623-641Google Scholar
  58. Wood R (1999) Reef Evolution. Oxford University Press, New York, 414 ppGoogle Scholar
  59. Zar JH (1984) Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, New Jersey, 718 ppGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Evangelina Schwindt
    • 1
  • Alejandro Bortolus
    • 1
  • Oscar Osvaldo Iribarne
    • 1
  1. 1.Laboratorio de Ecología (FCEyN)Universidad Nacional de Mar del PlataArgentina; Comisión de Investigaciones Científicas (CIC); Author for correspondence (e-mail

Personalised recommendations