Marine Biology

, Volume 152, Issue 6, pp 1271–1282 | Cite as

Habitat related growth and reproductive investment in estuarine waters, illustrated for the tellinid bivalve Macoma balthica (L.) in the western Dutch Wadden Sea

  • Joana F. M. F. CardosoEmail author
  • Johannes IJ. Witte
  • Henk W. van der Veer
Research Article


In estuarine areas, bivalve species can be found in a variety of environments, where they experience large differences in environmental conditions. In the present paper, the importance of different habitats (intertidal, subtidal and adjacent coastal waters) for the persistence of the population was evaluated for the bivalve Macoma balthica (L.) in the western Dutch Wadden Sea estuary. Intra-specific variation in growth and reproductive output were followed during the year and related to local abiotic conditions. Significant differences in growth and reproductive investment were found between locations. Young individuals were mostly found in the intertidal area, where growth in terms of somatic mass was good. These areas were not favourable for adult individuals, since growth in shell length was low and many individuals did not reproduce. In the subtidal, where the highest densities were found, somatic and gonadal mass indices were low. Coastal areas had the lowest densities and showed high growth in terms of shell length and body mass. The habitat with the highest reproductive effort per individual was not the most important habitat in terms of reproductive output due to differences in density and in size of the habitat type. For M. balthica, the subtidal habitat contributed the most to the reproductive output of the western Dutch Wadden Sea population although the highest reproductive output per individual was in the coastal area.


Reproductive Output Shell Length Reproductive Investment Macoma Balthica Subtidal Area 
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.



We thank the crews of RV ‘Navicula’ and RV ‘Stern’ for assistance during sampling. Jan Beukema, Wim Wolff, Jaap van der Meer, Jan Drent, Oscar Bos, Pieter Honkoop, Katja Philippart, Pauline Kamermans and two anonymous reviewers provided critical comments on earlier drafts of the paper. This research was supported by the project ‘Praxis XXI’ MCT—Portugal, grant BD/21799/99 to Joana Cardoso.


  1. Appeldoorn RS (1983) Variation in the growth rate of Mya arenaria and its relationship to the environment as analyzed through Principal Components Analysis and the Omega parameter of the Von Bertalanffy Equation. Fish Bull 81:75–84Google Scholar
  2. Appeldoorn RS (1995) Covariation in life-history parameters of soft-shell clams (Mya arenaria) along a latitudinal gradient. ICES Mar Sci Symp 199:19–25Google Scholar
  3. Armonies W, Hellwig-Armonies M (1992) Passive settlement of Macoma balthica spat on tidal flats of the Wadden Sea and subsequent migration of juveniles. Neth J Sea Res 29:371–378CrossRefGoogle Scholar
  4. Bachelet G (1980) Growth and recruitment of the tellinid bivalve Macoma balthica at the southern limit of its geographical distribution, the Gironde estuary (SW France). Mar Biol 59:105–117CrossRefGoogle Scholar
  5. Bayne BL, Worrall CM (1980) Growth and reproduction of mussels Mytilus edulis from two populations. Mar Biol 3:317–328Google Scholar
  6. Bayne BL, Salkeld PN, Worral CM (1983) Reproductive effort and reproductive value in different populations of Mytilus edulis L. Oecologia 59:18–26CrossRefGoogle Scholar
  7. Beukema JJ (1974a) The efficiency of the Van Veen grab compared with the Reineck box sampler. J Conserv Int Explor Mer 35:319–327CrossRefGoogle Scholar
  8. Beukema JJ (1974b) Seasonal changes in the biomass of the macro-benthos of a tidal flat area in the Dutch Wadden Sea. Neth J Sea Res 8:94–107CrossRefGoogle Scholar
  9. Beukema JJ (1988) An evaluation of the ABC-method (abundance/biomass comparison) as applied to macrozoobenthic communities living on tidal flats in the Dutch Wadden Sea. Mar Biol 99:425–433CrossRefGoogle Scholar
  10. Beukema JJ (1989) Long-term changes in macrozoobenthic abundance on the tidal flats of the western part of the Dutch Wadden Sea. Helgol Meeresunters 43:405–415CrossRefGoogle Scholar
  11. Beukema JJ (1993) Successive changes in distribution patterns as an adaptive strategy in the bivalve Macoma balthica (L) in the Wadden Sea. Helgol Meeresunters 47:287–304CrossRefGoogle Scholar
  12. Beukema JJ, De Bruin W (1977) Seasonal changes in dry weight and chemical composition of the soft parts of the tellinid bivalve Macoma balthica in the Dutch Wadden Sea. Neth J Sea Res 11:42–55CrossRefGoogle Scholar
  13. Beukema JJ, De Vlas J (1989) Tidal-current transport of thread-drifting postlarval juveniles of the bivalve Macoma balthica from the Wadden Sea to the North Sea. Mar Ecol Prog Ser 52:193–200CrossRefGoogle Scholar
  14. Beukema JJ, Meehan BW (1985) Latitudinal variation in linear growth and other shell characteristics of Macoma balthica. Mar Biol 90:27–33CrossRefGoogle Scholar
  15. Beukema JJ, Cadée GC (1997) Local differences in macrozoobenthic response to enhanced food supply caused by mild eutrophication in a Wadden Sea area: Food is only locally a limiting factor. Limnol Oceanogr 42:1424–1435CrossRefGoogle Scholar
  16. Beukema JJ, De Bruin W, Jansen JJM (1978) Biomass and species richness of macrobenthic animals living on tidal flats of Dutch Wadden Sea. Long-term changes during a period of mild winters. Neth J Sea Res 12:58–77CrossRefGoogle Scholar
  17. Beukema JJ, Cadée GC, Dekker R (2002) Zoobenthic biomass limited by phytoplankton abundance: evidence from parallel changes in two long-term data series in, the Wadden Sea. J Sea Res 48:111–125CrossRefGoogle Scholar
  18. Borrero FJ (1987) Tidal height and gametogenesis—reproductive variation among populations of Geukensia demissa. Biol Bull 173:160–168CrossRefGoogle Scholar
  19. Bricelj VM, Epp J, Malouf RE (1987) Intraspecific variation in reproductive and somatic growth cycles of bay scallops Argopecten irradians. Mar Ecol Prog Ser 36:123–137CrossRefGoogle Scholar
  20. Calow P (1979) The cost of reproduction—a physiological approach. Biol Rev 54:23–40CrossRefGoogle Scholar
  21. 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 313:75–104CrossRefGoogle Scholar
  22. Daan R, Mulder M (2002) The macrobenthic fauna in the Dutch sector of the North Sea in 2001 and a comparison with previous data. NIOZ-rapport 2002-1Google Scholar
  23. Daan R, Mulder M (2003) The macrobenthic fauna in the Dutch sector of the North Sea in 2002 and a comparison with previous data. NIOZ-rapport, 2003-5Google Scholar
  24. Daan R, Mulder M (2004) The macrobenthic fauna in the Dutch sector of the North Sea in 2003 and a comparison with previous data. NIOZ-rapport, 2004-4Google Scholar
  25. Dankers N, Beukema JJ (1983) Distributional patterns of macrozoobenthic species in relation to some environmental factors. In: Wolff WJ (ed) Ecology of the Wadden Sea. A.A. Balkema, Rotterdam, pp 69–103Google Scholar
  26. De Montaudouin X (1996) Factors involved in growth plasticity of cockles Cerastoderma edule (L.), identified by field survey and transplant experiments. J Sea Res 36:251–265CrossRefGoogle Scholar
  27. De Wilde PAWJ (1975) Influence of temperature on behaviour, energy metabolism and growth of Macoma balthica (L.). In: Barnes H (ed) 9th European marine biology symposium. Aberdeen University Press, Aberdeen, pp 239–256Google Scholar
  28. Dekinga A, Piersma T (1993) Reconstructing diet composition on the basis of feces in a mollusk-eating wader, the knot Calidris canutus. Bird Study 40:144–156CrossRefGoogle Scholar
  29. Dekker R (1989) The macrozoobenthos of the subtidal western Dutch Wadden Sea. I. Biomass and species richness. Neth J Sea Res 23:57–68CrossRefGoogle Scholar
  30. Dekker R, Waasdorp D (2004) Het macrozoobenthos in de Waddenzee in 2003. NIOZ-rapport, 2004-3Google Scholar
  31. Dekker R, Waasdorp D, Ogilvie JM (2002) Het macrozoobenthos in de Waddenzee in 2001. NIOZ-rapport, 2002-2Google Scholar
  32. Dekker R, Waasdorp D, Ogilvie JM (2003) Het macrozoobenthos in de Waddenzee in 2002. NIOZ-rapport, 2003-1Google Scholar
  33. Delgado M, Camacho AP (2003) A study of gonadal development in Ruditapes decussatus (L.) (Mollusca, Bivalvia), using image analysis techniques: Influence of food ration and energy balance. J Shellfish Res 22:435–441Google Scholar
  34. Drent J (2002) Temperature responses in larvae of Macoma balthica from a northerly and southerly population of the European distribution range. J Exp Mar Biol Ecol 275:117–129CrossRefGoogle Scholar
  35. Drent J (2004) Life history variation of a marine bivalve (Macoma balthica) in a changing world. PhD Thesis, University of Groningen, The NetherlandsGoogle Scholar
  36. Fiori SM, Morsán EM (2004) Age and individual growth of Mesodesma mactroides (Bivalvia) in the southernmost range of its distribution. ICES J Mar Sci 61:1253–1259CrossRefGoogle Scholar
  37. Gilbert MA (1973) Growth rate, longevity and maximum size of Macoma balthica (L.). Biol Bull 145:119–126CrossRefGoogle Scholar
  38. Guevara JM, Niell FX (1989) Growth rates in a continuously immersed population of Cerastoderma edule L. Sci Mar 53:483–489Google Scholar
  39. Günther CP (1991) Settlement of Macoma balthica on an intertidal sandflat in the Wadden Sea. Mar Ecol Prog Ser 76:73–79CrossRefGoogle Scholar
  40. 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 129:199–217CrossRefGoogle Scholar
  41. Heck KL, Coen LD, Wilson DM (2002) Growth of northern [Mercenaria mercenaria (L.)] and southern [M. campechiensis (Gmelin)] quahogs: Influence of seagrasses and latitude. J Shellfish Res 21:635–642Google Scholar
  42. Hiddink JG, Wolff WJ (2002) Changes in distribution and decrease in numbers during migration of the bivalve Macoma balthica. Mar Ecol Prog Ser 233:117–130CrossRefGoogle Scholar
  43. Hiddink JG, Marijnissen SAE, Troost K , Wolff WJ (2002a) Predation on O-group and older year classes of the bivalve Macoma balthica: interaction of size selection and intertidal distribution of epibenthic predators. J Exp Mar Biol Ecol 269:223–248CrossRefGoogle Scholar
  44. Hiddink JG, Ter Hofstede R, Wolff WJ (2002b) Predation of intertidal infauna on juveniles of the bivalve Macoma balthica. J Sea Res 47:141–159CrossRefGoogle Scholar
  45. Holtmann SE, Groenewold A, Schrader KHM, Asjes J, Craeymeersch JA, Duineveld GCA, van Bostelen AJ, van der Meer J (1996) Atlas of the zoobenthos of the Dutch Continental Shelf. Ministry of Transport, Public Works and Water Management, North Sea Directorate, RijswijkGoogle Scholar
  46. Honkoop PJC, Beukema JJ (1997) Loss of body mass in winter in three intertidal bivalve species: an experimental and observational study of the interacting effects between water temperature, feeding time and feeding behaviour. J Exp Mar Biol Ecol 212:277–297CrossRefGoogle Scholar
  47. Honkoop PJC, Van der Meer J (1997) Reproductive output of Macoma balthica populations in relation to winter-temperature and intertidal-height mediated changes of body mass. Mar Ecol Prog Ser 149:155–162CrossRefGoogle Scholar
  48. Hulscher JB (1982) The oystercatcher Haematopus ostralegus as a predator of the bivalve Macoma balthica in the Dutch Wadden Sea. Ardea 70:89–152Google Scholar
  49. Hummel H (1985) An energy budget for a Macoma balthica (Mollusca) population living on a tidal flat in the Dutch Wadden Sea. Neth J Sea Res 19:84–92CrossRefGoogle Scholar
  50. Jensen KT (1992) Macrozoobenthos on an intertidal mudflat in the Danish Wadden Sea—comparisons of surveys made in the 1930s, 1940s and 1980s. Helgol Meeresunters 46:363–376CrossRefGoogle Scholar
  51. Jones DS, Thompson I, Ambrose W (1978) Age and growth rate determinations for Atlantic surf clam Spisula solidissima (Bivalvia, Mactracea), based on internal growth lines in shell cross-sections. Mar Biol 47:63–70CrossRefGoogle Scholar
  52. Kamermans P (1994) Similarity in food source and timing of feeding in deposit-feeding and suspension-feeding bivalves. Mar Ecol Prog Ser 104:63–75CrossRefGoogle Scholar
  53. Lammens JJ (1967) Growth and reproduction in a tidal flat population of Macoma balthica (L.). Neth J Sea Res 3:315–382CrossRefGoogle Scholar
  54. Lodeiros CJ, Himmelman JH (1999) Reproductive cycle of the bivalve Lima scabra (Pterioida: Limidae) and its association with environmental conditions. Rev Biol Trop 47:411–418Google Scholar
  55. MacDonald BA, Thompson RJ (1985a) Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus.1. Growth rates of shell and somatic tissue. Mar Ecol Prog Ser 25:279–294CrossRefGoogle Scholar
  56. MacDonald BA, Thompson RJ (1985b) Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus.2. Reproductive output and total production. Mar Ecol Prog Ser 25:295–303CrossRefGoogle Scholar
  57. MacDonald BA, Thompson RJ (1986) Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus.3. Physiological ecology, the gametogenic cycle and scope for growth. Mar Biol 93:37–48CrossRefGoogle Scholar
  58. MacDonald BA, Bourne NF (1987) Growth, reproductive output and energy partitioning in weathervane scallops, Patinopecten caurinus, from British Columbia. Can J Fish Aquat Sci 44:152–160CrossRefGoogle Scholar
  59. MacDonald BA, Thompson RJ (1988) Intraspecific variation in growth and reproduction in latitudinally differentiated populations of the Giant scallop Placopecten magellanicus (Gmelin). Biol Bull 175:361–371CrossRefGoogle Scholar
  60. MacDonald BA, Thompson RJ, Bayne BL (1987) Influence of temperature and food availability on the ecological energetics of the giant scallop Placopecten magellanicus. 4. Reproductive effort, value and cost. Oecologia 72:550–556CrossRefGoogle Scholar
  61. Navarro JM, Leiva GE, Martinez G, Aguilera C (2000) Interactive effects of diet and temperature on the scope for growth of the scallop Argopecten purpuratus during reproductive conditioning. J Exp Mar Biol Ecol 247:67–83CrossRefGoogle Scholar
  62. Newell CR, Hidu H (1982) The effects of sediment type on growth rate and shell allometry in the soft-shell clam Mya arenaria L. J Exp Mar Biol Ecol 65:285–295CrossRefGoogle Scholar
  63. Nichols FH, Thompson JK (1982) Seasonal growth in the bivalve Macoma balthica near the southern limit of its range. Estuaries 5:110–120CrossRefGoogle Scholar
  64. Page HM, Hubbard DM (1987) Temporal and spatial patterns of growth in mussels Mytilus edulis on an offshore platform: relationships to water temperature and food availability. J Exp Mar Biol Ecol 111:159–179CrossRefGoogle Scholar
  65. Paterson KJ, Schreider MJ, Zimmerman KD (2003) Anthropogenic effects on seston quality and quantity and the growth and survival of Sydney rock oyster (Saccostrea glomerata) in two estuaries in NSW, Australia. Aquaculture 221:407–426CrossRefGoogle Scholar
  66. Roseberry L, Vincent B, Lemaire C (1991) Growth and reproduction of Mya arenaria in their intertidal zone of the Saint Lawrence estuary. Can J Zool 69:724–732CrossRefGoogle Scholar
  67. Sebens KP (1987) The ecology of indeterminate growth in animals. Ann Rev Ecol Syst 18:371–407CrossRefGoogle Scholar
  68. Sinclair M (1988) Marine populations: an essay on population regulation and speciation. Sea Grant Program, Seattle, WashingtonGoogle Scholar
  69. Swennen C, Ching HL (1974) Observations on the trematode Parvatrema affinis, causative agent of crawling tracks of Macoma balthica. Neth J Sea Res 8:108–115CrossRefGoogle Scholar
  70. Thompson JK, Nichols FH (1988) Food availability controls seasonal cycle of growth in Macoma balthica (L.) in San-Francisco Bay, California. J Exp Mar Biol Ecol 116:43–61CrossRefGoogle Scholar
  71. Van der Veer HW, Witte JIJ (1993) The ‘maximum growth/optimal food condition’ hypothesis: a test for 0-group plaice Pleuronectes platessa in the Dutch Wadden Sea. Mar Ecol Prog Ser 101:81–90CrossRefGoogle Scholar
  72. Van der Veer HW, Feller RJ, Weber A, Witte JIJ (1998) Importance of predation by crustaceans upon bivalve spat in the intertidal zone of the Dutch Wadden Sea as revealed by immunological assays of gut content. J Exp Mar Biol Ecol 231:139–157CrossRefGoogle Scholar
  73. Wanink JH, Zwarts L (1993) Environmental effects on the growth rate of intertidal invertebrates and some implications for foraging waders. Neth J Sea Res 31:407–418CrossRefGoogle Scholar
  74. Wilkinson L (1996) SYSTAT: the system for statistics. SYSTAT, Evanston, ILGoogle Scholar
  75. Zwarts L (1991) Seasonal variation in body weight of the bivalves Macoma balthica, Scrobicularia plana, Mya arenaria and Cerastoderma edule in the Dutch Wadden Sea. Neth J Sea Res 28:231–245CrossRefGoogle Scholar
  76. Zwarts L, Blomert AM (1992) Why knot Calidris canutus take medium-sized Macoma balthica when 6 prey species are available. Mar Ecol Prog Ser 83:113–128CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Joana F. M. F. Cardoso
    • 1
    Email author
  • Johannes IJ. Witte
    • 1
  • Henk W. van der Veer
    • 1
  1. 1.Royal Netherlands Institute for Sea ResearchDen Burg TexelThe Netherlands

Personalised recommendations