Skip to main content

Advertisement

Log in

Temporal variation of Tubularia indivisa (Cnidaria, Tubulariidae) and associated epizoites on artificial habitat communities in the North Sea

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

We have analyzed the composition, diversity, density and biomass of a temporal series of samples taken in a Tubularia indivisa community, which dominates a shipwreck in the North Sea waters (N 51°23′,730–E 02°29′,790, 17 nautical miles from the coast, 30 m depth). This shipwreck has structures emerging up to 8 m above the seabed. Water temperature ranged from 4.2°C in March to 20.3°C in August. Salinity showed few variations around 33.9 psu. Bottom tidal currents followed a semi-diurnal cycle and were preferentially NE oriented with 84% of them in the range 0.25–0.75 m s−1. The mean value for total suspended matter was 6.2 mg l−1 with large variations on a monthly scale. The species richness of samples varied from 15 in October to 42 in August with a mean value of 33 species. Diversity indices were higher during autumn and winter because of the strong dominance of a few crustacean species during the warmer months. The total density of individuals ranged from 6,500 ind m−2 in October to 445,800 ind m−2 in July, most of these individuals belonging to the amphipod species Jassa herdmani. The biomass of the T. indivisa community varied from 9 g AFDW m−2 in October to 1,106 g AFDW m−2 in July, with T. indivisa itself constituting between 59 and 82% of the total biomass. The biomass of T. indivisa was positively correlated with species richness and with the density of 23% of the species identified on this community, suggesting that T. indivisa plays an important structural role in this habitat. This was further confirmed by the number of species associated with T. indivisa which was generally superior to 55% of the sorted species. Multivariate analysis indicated strong differences between spring/summer−autumn/winter assemblages mostly but not solely due to the abundance patterns of species. These findings support the conclusion that shipwrecks in Belgian waters allow the development of assemblages dominated by a high biomass of T. indivisa which in turn provides shelter for high densities and biomass of epizoites. These assemblages will further show large monthly variations in densities and composition due to large variation in T. indivisa biomass under an apparent repetitive annual cycle.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ, Robinson J (2003) Generalized discriminant analysis based on distances. Aust N Z J Stat 45:301–318

    Article  Google Scholar 

  • Bavestrello G, Cerrano C, Cattaneo-Vietti R, Sara M (1996) Relations between Eudendrium glomeratum (Cnidaria, Hydromedusae) and its associated vagile fauna. Sci Mar 60:137–143

    Google Scholar 

  • Baynes TW, Szmant AM (1989) Effects of current on the sessile benthic community structure of an artificial reef. Bull Mar Sci 44:545–566

    Google Scholar 

  • Boero F (1984) The ecology of marine hydroids and effects of environmental factors: a review. Mar Ecol 5:93–118

    Article  Google Scholar 

  • Boero FC, Bouillon J (1993) Zoogeography and life cycle patterns of Mediterranean hydromedusae (Cnidaria). Biol J Linn Soc 48:29–266

    Article  Google Scholar 

  • Boero F, Fresi E (1986) Zonation and evolution of a rocky bottom hydroid community. PSZNI Mar Ecol 7:123–150

    Article  Google Scholar 

  • Boero F, Balduzzi A, Bavestrello G, Caffa B, Vietti RC (1986) Population dynamics of Eudendrium glomeratum (Cnidaria: Anthomedusae) on thePortofino Promontory (Ligurian Sea). Mar Biol 92:81–85

    Article  Google Scholar 

  • Bourget E, Harvey M (1998) Spatial analysis of recruitment of marine invertebrates on arborescent substrata. Biofouling 12:45–55

    Article  Google Scholar 

  • Brey T (1986) Formalin and formaldehyde-depot chemicals: effects on dry weight and ash free dry weight of two marine bivalve species. Meeresforsch 31:52–57

    Google Scholar 

  • Bray JR, Curtis JT (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  • Bulloch DK (1965) The development of the wreck Pinta as a marine habitat. Underw Nat Bull Am Littoral Soc 31:17–32

    Google Scholar 

  • Caine EA (1987) Potential effect of floating dock communities on a South Carolina estuary. J Exp Mar Biol Ecol 108:83–91

    Article  Google Scholar 

  • Caine EA (1998) First case of caprellid amphipod-hydrozoan mutualism. J Crustac Biol 18:317–320

    Article  Google Scholar 

  • Calder DR (1990) Seasonal cycles of activity and inactivity in some hydroids from Virginia and South Carolina. Can J Zool 68:442–450

    Article  Google Scholar 

  • Carpentier A, Vaz S, Martin CS, Coppin F, Dauvin J-C, Desroy N, Dewarumez JM, Eastwood PD, Ernande B, Harrop S, Kemp Z, Koubbi P, Leader-Williams N, Lefèbvre A, Lemoine N, Loots C, Meaden GJ, Ryan N, Walkey M (2005) Eastern Channel habitat atlas for marine resource management (CHARM). Interreg IIIA

  • Claereboudt MR, Bureau D, Cote J, Himmelman JH (1994) Fouling development and its effect on the growth of juvenile giant scallops (Placopecten magellanicus) in suspended culture. Aquaculture 121:327–342

    Article  Google Scholar 

  • Clarke KR (1999) Nonmetric multivariate analysis in community-level ecotoxicology. Environ Toxicol Chem 18:118–127

    Article  CAS  Google Scholar 

  • Clarke KR, Warwick RM (1998) A taxonomic distinctness index and its statistical properties. J Appl Ecol 35:523–531

    Article  Google Scholar 

  • Clarke KR, Warwick RM (2001) A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar Ecol Prog Ser 216:265–278

    Article  Google Scholar 

  • Conlan KE (1989) Delayed reproduction and adult dimorphism in males of the amphipod genus Jassa (Corophioidea: Ischyroceridae): an explanation for systematic confusion. J Crustac Biol 9:601–625

    Article  Google Scholar 

  • Connor DW, Allen JH, Golding N, Howell KL, Lieberknecht LM, Northen KO, Reker JB (2004) The marine habitat classification for Britain and Ireland, Version 04.05, Circalittoral rock section. Joint Nature Conservation Commitee, Peterborough, UK

    Google Scholar 

  • Cornelius PFS (1981) Life cycle, dispersal and distribution among the Hydroida. Por Newsl 2:47–50

    Google Scholar 

  • Costello MJ, Emblow CS, White R (2001) European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification. Patrim Nat 50:1–463

    Google Scholar 

  • Cusson M, Bourget E (2005) Global pattern of macroinvertebrate production in marine benthic habitat. Mar Ecol Prog Ser 297:1–14

    Article  Google Scholar 

  • Dean TA (1981) Structural aspect of sessile invertebrates as organizing forces in an estuarine fouling community. J Exp Mar Biol Ecol 53:163–180

    Article  Google Scholar 

  • Dean TA, Hurd LE (1980) Development in an estuarine fouling community: the influence of early colonists on later arrivals. Oecologia 46:295–301

    Article  CAS  Google Scholar 

  • Degraer S, Vincx M, Meire P, Offringa H (1999) The macrozoobenthos of an important wintering area of the common scoter (Melanitta nigra). J Mar Biol Ass UK 79:243–251

    Article  Google Scholar 

  • Doody JP, Johnston C, Smith B (1993) Directory of the North Sea coastal margin. Joint Nature Conservation Committee, Peterborough, UK

    Google Scholar 

  • Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Eisma D, Kalf J (1987) Distribution, organic content and particle size of suspended matter in the North Sea. Neth J Sea Res 21:265–285

    Article  Google Scholar 

  • Fettweis M, Van den Eynde D (2003) The mud deposits and the high turbidity in the Belgian-Dutch coastal zone, southern bight of the North Sea. Cont Shelf Res 23:669–691

    Article  Google Scholar 

  • Forteath GNR, Picken GB, Ralph R, Williams J (1982) Marine growth studies on the North Sea oil platform Montrose Alpha. Mar Ecol Prog Ser 8:61–68

    Article  Google Scholar 

  • Fraschetti S, Giangrande A, Terlizzi A, Boero F (2003) Pre- and post-settlement events in benthic community dynamics. Oceanol Acta 25:285–296

    Article  Google Scholar 

  • Gaston GR, Bartlett JHW, McAllister AP, Heard RW (1996) Biomass variations of estuarine macrobenthos preserved in ethanol and formalin. Estuaries 19:674–679

    Article  Google Scholar 

  • Genzano GN (1998) Hydroid epizoites on Tubularia crocea and Sertularella mediterranea from the intertidal of Mar del Plata, Argentina. Biol Morya 24:126–129

    Google Scholar 

  • Genzano GN (2001) Associated fauna and sediment trapped by colonies of Tubularia crocea (Cnidaria, Hydrozoa) from the rocky intertidal of Mar del Plata, Argentina. Biociencias 9:105–119

    Google Scholar 

  • Genzano GN (2002) Associations between pycnogonids and hydroids from the Buenos Aires littoral zone, with observations on the semi-parasitic life cycle of Tanystylum orbiculare (Ammotheiidae). Sci Mar 66:83–92

    Article  Google Scholar 

  • Genzano GN, San Martin G (2002) Association between the polychaete Procerastea halleziana (Polychaeta: Syllidae: Autolytinae) and the hydroid Tubularia crocea (Cnidaria: Hydrozoa) from the Mar del Plata intertidal zone, Argentina. Cah Biol Mar 43:165–170

    Google Scholar 

  • Gili JM, Hughes RG (1995) The ecology of marine benthic hydroids. Oceanogr Mar Biol Annu Rev 33:351–426

    Google Scholar 

  • Goss-Cusard S, Jones J, Kitching JA, Norton TA (1979) Tide pools of Carrigathorna and Barloge Creek. Philos Trans R Soc B 287:1–44

    Article  Google Scholar 

  • Guerra-Garcia JM, Corzo J, Garcia-Gomez JC (2002) Clinging behaviour of the Caprellidea (Amphipoda) from the Strait of Gibraltar. Crustac Int J Crustac Res 75:41–50

    Google Scholar 

  • Harvey M, Bourget E, Miron G (1993) Settlement of Iceland scallop Chlamys islandica spat in response to hydroids and filamentous red algae: field observations and laboratory experiments. Mar Ecol Prog Ser 99:283–292

    Article  Google Scholar 

  • Harvey M, Bourget E, Legault C, Ingram RG (1995a) Short-term variations in settlement and early spat mortality of Iceland scallop, Chlamys islandica (O.F. Müller). J Exp Mar Biol Ecol 194:167–187

    Article  Google Scholar 

  • Harvey M, Miron G, Bourget E (1995b Resettlement of Iceland scallop (Chlamys islandica) spat on dead hydroids: Response to chemical cues from the protein-chitinous perisarc and associated microbial film. J Shell Res 14:383–388

    Google Scholar 

  • Harvey M, Bourget E, Gagne N (1997) Spat settlement of the giant scallop, Placopecten magellanicus (Gmelin, 1791), and other bivalve species on artificial filamentous collectors coated with chitinous material. Aquaculture 148:277–298

    Article  Google Scholar 

  • Hughes RG (1983) The life-history of Tubularia indivisa (Hydrozoa: Tubulariidae) with observations on the status of T. ceratogyne. J Mar Biol Assoc UK 63:467–479

    Article  Google Scholar 

  • Jensen A, Collins KJ, Smith P (2000) The Poole Bay artificial reef project. In: Jensen A, Collins KJ, Lockwood APM (eds) Artificial reefs in European Seas, Kluwer, Dordrecht, pp 263–287

    Chapter  Google Scholar 

  • Johannesson K (1988) The paradox of Rockall: why is a brodding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea). Mar Biol 99:507–513

    Article  Google Scholar 

  • Kaandorp JA (1982) Rocky substrate communities of the infralittoral fringe of the Boulonnais coast, NW France: a quantitative survey. Mar Biol 92:255–265

    Article  Google Scholar 

  • Kruskal JB, Wish M (1978) Multidimensional scaling. Sage University Paper series on quantitative applications in the social sciences no 11. Sage, Beverly Hills

    Google Scholar 

  • Lanckneus J, van Lancker V, Moerkerke G, Van den Eynde D, Fettweis M, de Batist M, Jacobs P (2001) Investigation of the natural sand transport on the Belgian continental shelf (BUDGET). Final report. Federal Office for Scientific, Technical and Cultural Affairs (OSTC)

  • Leewis RJ, Hallie F (2000) An artificial reef experiment off the Dutch Coast. In: Jensen A, Collins KJ, Lockwood APM (eds) Artificial reefs in European Seas, Kluwer, Dordrecht, pp 289–306

    Chapter  Google Scholar 

  • Leewis RJ, van Moorsel GWNM, Waardenburg HW (2000) Shipwrecks on the Dutch Continental Shelf as artificial reefs. In: Jensen AC, Collins KJ, Lockwood APM (eds) Artificial reefs in European Seas, Kluwer, Dordrecht, pp 419–434

    Chapter  Google Scholar 

  • Lemire M, Bourget E (1996) Substratum heterogeneity and complexity influence micro-habitat selection of Balanus sp and Tubularia crocea larvae. Mar Ecol Prog Ser 135:77–87

    Article  Google Scholar 

  • Leonhard SB, Pedersen J, Moeslund B (2004) Hard bottom substrate monitoring. Horns Rev Offshore Wind Farm. Annual status report 2003. Bio/consult as, Copenhague, Denmark

  • Lindquist DG, Pietrafesa LJ (1989) Current vortices and fish aggregations: the current field and associated fishes around a tugboat wreck in Onslow Bay, North-Carolina. Bull Mar Sci 44:533–544

    Google Scholar 

  • Luyten PJ, Jones JE, Proctor R, Tabor A, Tette P, Wild-Allen K (1999) COHERENS: a coupled hydrodynamic-ecological model for regional and shelf seas. Users documentation. Report, Management Unit of the Mathematical Models of the North Sea, Brussels

  • Magurran AE (2004) Measuring biological diversity. Blackwell Science, Oxford

    Google Scholar 

  • MarBEF (2004) European marine biodiversity datasets. Available Online at http://www.Marbef Org/Data/Dataset Php

  • Mullineaux LS, Garland ED (1993) Larval recruitment in response to manipulated field flows. Mar Biol 116:667–683

    Article  Google Scholar 

  • Nechad B., De Cauwer V, Park Y, Ruddick K (2003) Suspended particulate matter (SPM) mapping from MERIS imagery. Calibration of a regional algorithm for the Belgian coastal waters. MERIS user workshop, 10–13th November 2003 (Frascati). European Space Agency SP549

  • Nellis P, Bourget E (1996) Influence of physical and chemical factors on settlement and recruitment of the hydroid Tubularia larynx. Mar Ecol Prog Ser 140:123–139

    Article  CAS  Google Scholar 

  • Orlov DVM (1994) Behaviour and settling of actinulae of Tubularia larynx (Leptolida, Tubulariidae). Zool Zh 73:5–11

    Google Scholar 

  • Pakhomov EA (2003) Correction of zooplankton and benthos biomass under-estimations from formaldehyde-preserved samples. Arch Fish Mar Res 50:141–148

    Google Scholar 

  • Petersen KW (1990) Evolution and taxonomy in capitate hydroids and medusae (Cnidaria: Hydrozoa). Zool J Lin Soc Lond 100:101–231

    Article  Google Scholar 

  • Pison V, Ozer J (2003) Operational products and services for the Belgian coastal waters. In: Dalhin H, Flemings NC, Nittis K, Petersson SE (eds) Building the European capacity in operational oceanography. Proceedings of the 3rd international conference on EuroGOOS, Elsevier oceanography, series 69, pp 503–509

  • Pyefinch KA, Downing FS (1949) Notes on the general biology of Tubularia larynx Ellis & Solander. J Mar Biol Assoc UK 28:21–44

    Article  Google Scholar 

  • Robinson M, Tully O (2000) Dynamics of a subtidal population of the porcellanid crab Pisidia longicornis (Decapoda: Crustacea). J Mar Biol Assoc UK 80:75–83

    Article  Google Scholar 

  • Rumohr H, Brey T, Ankar S (1987) A compilation of biometric conversion factor for benthic invertebrates of Baltic Sea. Balt Mar Biol Publ 9:1–56

    Google Scholar 

  • Sampaolo A, Relini G (1994) Coal ash for artificial habitats in Italy. Bull Mar Sci 55:1277–1294

    Google Scholar 

  • Schmidt GH (1983) The hydroid Tubularia larynx causing ‘bloom’ of the ascidians Ciona intestinalis and Ascidiella aspersa. Mar Ecol Prog Ser 12:103–105

    Article  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611

    Article  Google Scholar 

  • Takeuchi I, Hirano R (1995) Clinging behaviour of the epifaunal caprellids (Amphipoda) inhabiting the Sargassum zone on the Pacific coast of Japan, with its evolutionary implications. J Crustac Biol 15:481–492

    Article  Google Scholar 

  • Walters LJ, Wethey DS (1996) Settlement and early post settlement survival of sessile marine invertebrates on topographically complex surfaces: the importance of refuge dimensions and adult morphology. Mar Ecol Prog Ser 137:161–171

    Article  Google Scholar 

  • Wetzel MA, Leuchs H, Koop JHE (2005) Preservation effects on wet weight, dry weight, and ash-free dry weight biomass estimates of four common estuarine macro-invertebrates: no difference between ethanol and formalin. Helgol Meeresunters 59:206–213

    Google Scholar 

  • Whomersley P, Picken GB (2003) Long-term dynamics of fouling communities found on offshore installations in the North Sea. J Mar Biol Assoc UK 83:897–901

    Article  Google Scholar 

  • Woodhead PMJ, Jacobson ME (1985) Epifaunal settlement, the processes of community development and succession over two years on an artificial reef in the New York Bight. Bull Mar Sci 37:364–376

    Google Scholar 

  • Yamashita K, Kawaii S, Nakai M, Fusetani N (2003) Larval behavioral, morphological changes, and nematocyte dynamics during settlement of actinulae of Tubularia mesembryanthemum, Allman 1871 (Hydrozoa : Tubulariidae). Biol Bull 204:256–269

    Article  Google Scholar 

  • Zintzen V, Massin C, Norro A, Mallefet J (2006) Epifaunal inventory of two shipwrecks from the Belgian Continental Shelf. Hydrobiologia 555:207–219

    Article  Google Scholar 

  • Zintzen V, Norro A, Massin C, Mallefet J (2007) Spatial variability of epifaunal communities from artificial habitat: shipwrecks in the Southern Bight of the North Sea. Est Coast Shelf Sci (in press)

Download references

Acknowledgments

The authors wish to thank the crews of the R/V Zeeleeuw and R/V Belgica for their help during the sampling campaigns and to Céline Delforge for the great help during the sorting process. It is also our pleasure to thank all the people who helped collecting the samples: Drs Y. Laitat, A. Simon, D. Delbare, E. Vanden Bergh, T. Schils, Mss C. Delforge and R. Gyssens and Mrs P.B. Demoulin, G. Rooms, D. Marsham, F. Cray, M. Van Espen, Y. Verkemping, M. Backx, J.P. De Blauwe, J. Haelters, F. Hernandez, F. Darchambeau, G. Van Hoydonck, A. Vanhaelen, R. Knuts & P. Van de Steen. Dr Christine Vanderlinden helped with the English. This study has been financially supported by a ‘plan Action II’ grant (contract No. WI/36/C04) from the Belgian Science Policy. The second author is grateful to MUMM BMDC for data, REMSEM group for the availability of satellite data and Model groups for model results availability. His participation to this study has been funded by BEWREMABI project (Belgian Science Policy). We also wish to thank the reviewers for their fruitful remarks which greatly improved the quality of this paper. This research was done within the laws of the country.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vincent Zintzen.

Additional information

Communicated by M. Wahl.

Electronic supplementary material

227_2007_819_MOESM1_ESM.doc

Temporal variation of Tubularia indivisa (Cnidaria, Tubulariidae) and associated epizoites on artificial habitat communities in the North Sea

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zintzen, V., Norro, A., Massin, C. et al. Temporal variation of Tubularia indivisa (Cnidaria, Tubulariidae) and associated epizoites on artificial habitat communities in the North Sea. Mar Biol 153, 405–420 (2008). https://doi.org/10.1007/s00227-007-0819-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-007-0819-5

Keywords

Navigation