Low macroinvertebrate biomass suggests limited food availability for shorebird communities in intertidal areas of the Bijagós archipelago (Guinea-Bissau)

  • Pedro M. Lourenço
  • José P. Granadeiro
  • Teresa Catry
Primary Research Paper


Knowledge of the macrozoobenthic community and its interactions with predators is critical for understanding intertidal ecosystems but this information is still lacking for many tropical sites. We core-sampled three intertidal areas in the Bijagós archipelago, Guinea-Bissau, one of the largest intertidal wetlands in West Africa, to evaluate macroinvertebrate abundance and diversity, investigate ecological variables influencing macroinvertebrate distribution, and estimate food availability for several shorebird species. We found a low macroinvertebrate biomass, which mostly consisted of bivalves and polychaetes. The fiddler crab Afruca tangeri was also among the more abundant species. Both Shannon diversity and rarefied species richness indicate macrozoobenthic communities in the Bijagós have low diversity but there is large variation in species composition among sites. Sediment fine fraction, organic content and distance to the coast were correlated with the abundance of several macroinvertebrate taxa. Harvestable biomass for the shorebird species studied was very low, below the values described for intertidal sites in temperate areas and some other sites in the tropics. Although this fits with low shorebird densities in the Bijagós, it also suggests that wintering shorebird communities must depend on secondary production by macrobenthic invertebrates during the winter, in the same way as has been proposed for other tropical intertidal systems.


Harvestable biomass Macrozoobenthos Mudflats Waders West Africa 



We thank Alfredo da Silva, Aissa Regalla and Quintino Tchantchalam from Instituto da Biodiversidade e Áreas Protegidas (IBAP) for logistical support and permission to work in protected areas in Guinea-Bissau, and Santinho da Silva and other staff from IBAP, as well as Joãozinho Sá and Hamilton Monteiro (Gabinete de Planificação Costeira), for help in fieldwork and logistics. Paulo Catry provided advice on Bijagós during expedition’s preparation. Inês Catry provided invaluable help during field work in the Bijagós and Patricia Pedro helped analysing macroinvertebrate samples in the laboratory. This study was supported by Fundação para a Ciência e Tecnologia (FCT) through a postdoctoral grant to PML (SFRH/BPD/84237/2012) and project IF/00694/2015 granted to TC. Thanks are also due for the financial support to CESAM (UID/AMB/50017 - POCI-01-0145-FEDER-007638), to FCT/MCTES through national funds (PIDDAC), and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020.

Supplementary material

10750_2018_3584_MOESM1_ESM.docx (100 kb)
Supplementary material 1 (DOCX 99 kb)
10750_2018_3584_MOESM2_ESM.docx (13 kb)
Supplementary material 2 (DOCX 12 kb)
10750_2018_3584_MOESM3_ESM.docx (14 kb)
Supplementary material 3 (DOCX 14 kb)


  1. Beukema, J. J. & G. C. Cadée, 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. Limnology and Oceanography 42: 1424–1435.CrossRefGoogle Scholar
  2. Bouillon, S., R. M. Connolly & D. P. Gillikin, 2011. Use of stable isotopes to understand food webs and ecosystem functioning in estuaries. In Wolanski, E. & D. S. McLusky (eds), Treatise on Estuarine and Coastal Science 7. Academic Press, Waltham: 143–173.CrossRefGoogle Scholar
  3. Campredon, P. & P. Catry, 2017. Bijagos Archipelago (Guinea-Bissau). In: Finlayson, C.M., Milton, G.R., Prentice, R. & Davidson, N.C. (eds) The Wetland Book. II. Distribution, Description and Conservation. Springer, Dordrecht.Google Scholar
  4. Colwell, M. A. & S. L. Landrum, 1993. Nonrandom shorebird distribution and fine-scale variation in prey abundance. The Condor 95: 94–103.CrossRefGoogle Scholar
  5. Compton, T. J., S. Holthuijsen, A. Koolhaas, A. Dekinga, J. ten Horn, J. Smith, Y. Galama, M. Brugge, D. van der Wal, J. van der Meer, H. W. van der Veer & T. Piersma, 2013. Distinctly variable mudscapes: distribution gradients of intertidal macrofauna across the Dutch Wadden Sea. Journal of Sea Research 82: 103–116.CrossRefGoogle Scholar
  6. Dauer, D. M., 1993. Biological criteria, environmental health and estuarine macrobenthic community structure. Marine Pollution Bulletin 26: 249–257.CrossRefGoogle Scholar
  7. Dauer, D. M., C. A. Maybury & R. M. Ewing, 1981. Feeding behavior and general ecology of several spionid polychaetes from the Chesapeake Bay. Journal of Experimental Marine Biology and Ecology 54: 21–38.CrossRefGoogle Scholar
  8. Day, J.H. 1967. A monograph on the polychaeta of southern Africa. Trustees of the British Museum (Natural History). Publication No. 656. Trustees of the British Museum, London.Google Scholar
  9. del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. 2013. Handbook of the birds of the world alive. Lynx Edicions. Barcelona, Spain. [available on internet at http://www.hbw.com]. Accessed February 2017.
  10. Delany, S., D. Scott, T. Dodman & D. Stroud, 2009. An atlas of wader populations in Africa and western Eurasia. Wetlands International, Wageningen.Google Scholar
  11. Dittmann, S., 2002. Benthic fauna in tropical tidal flats – a comparative perspective. Wetlands Ecology and Management 10: 189–195.CrossRefGoogle Scholar
  12. Dolbeth, M., M. A. Pardal, A. I. Lillebø, U. Azeiteiro & J. C. Marques, 2003. Short- and long-term effects of eutrophication on the secondary production of an intertidal macrobenthic community. Marine Biology 143: 1229–1238.CrossRefGoogle Scholar
  13. Elliott, M. & A. K. Whitfield, 2011. Challenging paradigms in estuarine ecology and management. Estuarine, Coastal and Shelf Science 94: 306–314.CrossRefGoogle Scholar
  14. Ens, B., M. Klaassen & L. Zwarts, 1993. Flocking and feeding in the fiddler crab (Uca tangeri): prey availability as risk-taking behaviour. Netherlands Journal of Sea Research 31: 477–494.CrossRefGoogle Scholar
  15. Estrella, S. M. & J. A. Masero, 2010. Prey and prey size selection by the Near-Threatened black-tailed godwit foraging in non-tidal areas during migration. Waterbirds 33: 293–299.CrossRefGoogle Scholar
  16. Ferner, M. C. & P. A. Jumars, 1999. Responses of deposit-feeding spionid polychaetes to dissolved chemical cues. Journal of Experimental Marine Biology and Ecology 236: 89–106.CrossRefGoogle Scholar
  17. Finn, P. G., C. P. Catterall & P. V. Driscoll, 2008. Prey versus substrate as determinants of habitat choice in a feeding shorebird. Estuarine Coastal and Shelf Science 80: 381–390.CrossRefGoogle Scholar
  18. Goss-Custar, J. D., A. D. West, M. G. Yates, R. W. G. Caldow, R. A. Stillman, L. Bardsley, J. Castilla, M. Castro, V. Dierschke, S. E. A. Durell, G. Eichhorn, B. J. Ens, K.-M. Exo, P. U. Udayangani-Fernando, P. N. Ferns, P. A. R. Hockey, J. A. Gill, I. Johnstone, B. Kalejta-Summers, J. A. Masero, F. Moreira, R. V. Nagarajan, I. P. F. Owens, C. Pacheco, A. Perez-Hurtado, D. Rogers, G. Scheiffarth, H. Sitters, W. J. Sutherland, P. Triplet, D. H. Worrall, Y. Zharikov, L. Zwarts & R. A. Pettifor, 2006. Intake rates and the functional response in shorebirds (Charadriiformes) eating macro-invertebrates. Biological Reviews 81: 1–29.CrossRefGoogle Scholar
  19. Grioche, A., P. Koubbi & X. Harlay, 1999. Spatial patterns of ichthyoplankton assemblages along the eastern English Channel French coast during spring 1995. Estuarine Coastal and Shelf Science 49: 141–152.CrossRefGoogle Scholar
  20. Hampel, H., M. Elliott & A. Cattrijsse, 2009. Macrofaunal communities in the habitats of intertidal marshes along the salinity gradient of the Schelde estuary. Estuarine, Coastal and Shelf Science 84: 45–53.CrossRefGoogle Scholar
  21. Holland, A. F. & J. M. Dean, 1977. The biology of the stout razor clam Tagelus plebeius: i. Animal-sediment relationships, feeding mechanism, and community biology. Chesapeake Science 18: 58–66.CrossRefGoogle Scholar
  22. Honkoop, P. J. C., E. M. Berghuis, S. Holthuijsen, M. S. S. Lavaleye & T. Piersma, 2008. Molluscan assemblages of seagrass-covered and bare intertidal flats on the Banc d’Arguin, Mauritania, in relation to characteristics of sediment and organic matter. Journal of Sea Research 60: 235–243.CrossRefGoogle Scholar
  23. Hosie, G. W. & T. G. Cochran, 1994. Mesoscale distribution patterns of macrozooplankton communities in Prydz bay, Antarctica - January to February 1991. Marine Ecology Progress Series 106: 21–39.CrossRefGoogle Scholar
  24. Hunt, B. P. V., R. J. Nelson, B. Williams, F. A. McLaughlin, K. V. Young, K. A. Brown, S. Vagle & E. C. Carmack, 2014. Zooplankton community structure and dynamics in the Arctic Canada Basin during a period of intense environmental change (2004–2009). Journal of Geophysical Research: Oceans 119: 2518–2538.Google Scholar
  25. Hurlbert, S. H., 1971. The nonconcept of species diversity: a critique and alternative parameters. Ecology 52: 577–586.CrossRefPubMedGoogle Scholar
  26. Karakassis, I. & A. Eleftheriou, 1997. The continental shelf of Crete: structure of macrobenthic communities. Marine Ecology Progress Series 160: 185–196.CrossRefGoogle Scholar
  27. Karpanty, S., J. D. Fraser, J. Berkson, L. J. Niles, A. Dey & E. P. Smith, 2006. Horseshoe crab eggs determine red knot distribution in Delaware Bay. Journal of Wildlife Management 70: 1704–1710.CrossRefGoogle Scholar
  28. Kelsey, M. G. & M. Hassall, 1989. Patch selection by dunlin on a heterogeneous mudflat. Ornis Scandinavica 20: 250–254.CrossRefGoogle Scholar
  29. Kersten, M. & T. Piersma, 1987. High levels of energy expenditure in shorebirds; metabolic adaptations to an energetically expensive way of life. Ardea 75: 175–187.Google Scholar
  30. Kober, K. 2004. Foraging ecology and habitat use of wading birds and shorebirds in the mangrove ecosystem of the Caéte Bay, Northeast Pará, Brazil. PhD Thesis. University of Bremen, Germany.Google Scholar
  31. Kruscal, J. B. & M. Wish, 1978. Multidimensional Scaling. Sage Publications, Beverly Hills.CrossRefGoogle Scholar
  32. Levin, L. A., D. F. Boesch, A. Covich, C. Dahm, C. Erseus, K. C. Ewel, R. T. Kneib, A. Moldenke, M. A. Palmer, P. Snelgrove, D. Strayer & J. M. Weslaeski, 2001. The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems 4: 430–451.CrossRefGoogle Scholar
  33. Lohrer, A. M., L. D. Chiaroni, J. E. Hewitt & S. F. Thrush, 2008. Biogenic disturbance determines invasion success in a subtidal soft-sediment system. Ecology 89: 1299–1300.CrossRefPubMedGoogle Scholar
  34. Lourenço, P. M., J. P. Granadeiro & J. M. Palmeirim, 2005. Importance of drainage channels for waders foraging on tidal flats: relevance for the management of estuarine wetlands. Journal of Applied Ecology 42: 477–486.CrossRefGoogle Scholar
  35. Lourenço, P. M., J. A. Alves, T. Catry & J. P. Granadeiro, 2015. Foraging ecology of sanderlings Calidris alba wintering in estuarine and non-estuarine intertidal areas. Journal of Sea Research 104: 33–40.CrossRefGoogle Scholar
  36. Lourenço, P. M., T. Catry, R. J. Lopes, T. Piersma & J. P. Granadeiro, 2017a. Invisible trophic links? Quantifying the importance of non-standard food sources for key intertidal avian predators in the Eastern Atlantic. Marine Ecology Progress Series 563: 219–232.CrossRefGoogle Scholar
  37. Lourenço, P. M., T. Catry & J. P. Granadeiro, 2017b. Diet and feeding ecology of the wintering shorebird assemblage in the Bijagós archipelago, Guinea-Bissau. Journal of Sea Research 128: 52–60.CrossRefGoogle Scholar
  38. Manning, R.B. & Holthuis, L.B. 1981. West African Brachyuran crabs (Crustacea: Decapoda). Smithsonian Contributions to Zoology. Number 306. Smithsonian Institution Press, Washington D.C.Google Scholar
  39. Maurer, D. & J. A. Vargas, 1984. Diversity of soft-bottom benthos in a tropical estuary: gulf of Nicoya, Costa Rica. Marine Biology 81: 97–106.CrossRefGoogle Scholar
  40. McLusky, D. S., 1981. The Estuarine Ecosystem. Blackie, Glasgow.Google Scholar
  41. Oksanen, J. 2016. Vegan: an introduction to ordination. [available on internet at https://cran.r-project.org/web/packages/vegan/vignettes/intro-vegan.pdf] (Accessed Nov 2016).
  42. Oliver, P. G. & R. von Cosel, 1992. Taxonomy of West African bivalves IV. Arcidae. Bulletin du Muséum National d’Histoire Naturelle, Paris 14: 293–381.Google Scholar
  43. Pennober, G., 1999. Analyse spatiale de l’environnement côtier de l’archipel des Bijagos (Guinée Bissau). Université de Bretagne Occidentale, Brest, Sciences de l’Homme et Société.Google Scholar
  44. Philippe, A. 2016. Interactions between shorebirds and benthic macrofauna: making small things bigger. PhD thesis. University of La Rochelle, France.Google Scholar
  45. Piersma, T., 1987. Production by intertidal benthic animals and limits to their predation by shorebirds: a heuristic model. Marine Ecology Progress Series 38: 187–196.CrossRefGoogle Scholar
  46. Piersma, T., P. de Goeij & I. Tulp, 1993a. An evaluation of intertidal feeding habitats from a shorebird perspective: towards relevant comparisons between temperate and tropical mudflats. Netherlands Journal of Sea Research 31: 503–512.CrossRefGoogle Scholar
  47. Piersma, T., R. Hoekstra, A. Dekinga, A. Koolhaas, P. Wolf, P. Battley & P. Wiersma, 1993b. Scale and intensity of intertidal habitat use by knots Calidris canutus in the western Wadden Sea in relation to food, friends and foes. Netherlands Journal of Sea Research 31: 331–357.CrossRefGoogle Scholar
  48. Piersma, T., A. Koolhaas, A. Dekinga, J. J. Beukema, R. Dekker & K. Essink, 2001. Long-term indirect effects of mechanical cockle-dredging on intertidal bivalve stocks in the Wadden Sea. Journal of Applied Ecology 38: 976–990.CrossRefGoogle Scholar
  49. Quintino, V., A. M. Rodrigues & F. Gentil, 1989. Assessment of macrozoobenthic communities in the Lagoon of Óbidos, western coast of Portugal. Scientia Marina 53: 645–654.Google Scholar
  50. R Core Team, 2014. R: A Language And Environment For Statistical Computing. R Foundation for Statistical Computing, Vienna.Google Scholar
  51. Raffaelli, D. & S. Hawkins, 1999. Intertidal Ecology, 2nd ed. Kluwer Academic Publishers, Dordrecht.Google Scholar
  52. Ricciardi, A. & E. Bourget, 1999. Global patterns of macroinvertebrate biomass in marine intertidal communities. Marine Ecology Progress Series 185: 21–35.CrossRefGoogle Scholar
  53. Rodrigues, A. M., V. Quintino, L. Sampaio, R. Freitas & R. Neves, 2011. Benthic biodiversity patterns in Ria de Aveiro, Western Portugal: environmental-biological relationships. Estuarine, Coastal and Shelf Science 95: 338–348.CrossRefGoogle Scholar
  54. Salvig, J. C., S. Asbirk, J. P. Kjeldsen & P. A. F. Rasmussen, 1994. Wintering waders in the Bijagós archipelago, Guinea-Bissau 1992–1993. Ardea 82: 137–142.Google Scholar
  55. Sanders, H. L., 1968. Marine benthic diversity: a comparative study. The American Naturalist 102: 243–282.CrossRefGoogle Scholar
  56. Salem, M. V. A., M. van der Geest, T. Piersma, Y. Saoud & J. A. van Gils, 2014. Seasonal changes in mollusc abundance in a tropical intertidal ecosystem, Banc d’Arguin (Mauritania): testing the ‘depletion by shorebirds’ hypothesis. Estuarine, Coast and Shelf Science 136: 26–34.CrossRefGoogle Scholar
  57. Somarakis, S., A. Ramfos, A. Palialexis & V. D. Valavanis, 2011. Contrasting multispecies patterns in larval fish production trace inter-annual variability in oceanographic conditions over the N.E. Aegean Sea continental shelf (Eastern Mediterranean). Hydrobiologia 670: 275–287.CrossRefGoogle Scholar
  58. Taghon, G. L., 1982. Optimal foraging by deposit-feeding invertebrates: roles of particle size and organic coating. Oecologia 52: 295–304.CrossRefPubMedGoogle Scholar
  59. Tantikamton, K., N. Thanee, S. Jitpukdee & M. Potter, 2015. Species diversity and ecological characteristics of benthic macroInvertebrates in the intertidal zone of Satun Province, Thailand and the first record of Petersenaspis sp. International Journal of Advances in Agriculture & Environmental Engineering 2: 23–27.Google Scholar
  60. Thrush, S. F., J. E. Hewitt, A. Norkko, V. J. Cummings & G. A. Funnell, 2003. Macrobenthic recovery processes following catastrophic sedimentation on estuarine sandflats. Ecological Applications 13: 1433–1455.CrossRefGoogle Scholar
  61. Thrush, S. F., J. E. Hewitt, M. Gibbs, C. Lundquist & A. Norkko, 2006. Functional role of large organisms in intertidal communities: community effects and ecosystem function. Ecosystems 9: 1029–1040.CrossRefGoogle Scholar
  62. Tulp, I. & P. de Goeij, 1994. Evaluating wader habitats in Roebuck Bay (north-western Australia) as a springboard for northbound migration in waders, with a focus on great knots. Emu 94: 78–95.CrossRefGoogle Scholar
  63. van de Kam, J., B. Ens, T. Piersma & L. Zwarts, 2004. Shorebirds: An Illustrated Behavioural Ecology. KNNV Publishers, Utrecht.Google Scholar
  64. van der Meer, J., 1991. Exploring macrobenthos–environment relationship by canonical correlation analysis. Journal of Experimental Marine Biology and Ecology 148: 105–120.CrossRefGoogle Scholar
  65. van der Zee, E. M., T. van der Heide, S. Donadi, J. S. Eklöf, B. K. Eriksson, H. Olff, H. W. van der Veer & T. Piersma, 2012. Spatially extended habitat modification by intertidal reef-building bivalves has implications for consumer–resource interactions. Ecosystems 15: 664–673.CrossRefGoogle Scholar
  66. von Cosel, R., 1989. Taxonomy of tropical West African bivalves I. Four new species of eulamellibranchiate bivalves. Bulletin du Muséum National d’Histoire Naturelle, Paris 11: 315–331.Google Scholar
  67. van Roomen, M., S. Nagy, R. Foppen, T. Dodman, G. Citegetse, & A. Ndiaye, 2015. Status of coastal waterbird populations in the East Atlantic Flyway. With special attention to flyway populations making use of the Wadden Sea. Programme Rich Wadden Sea, Leuwarden, The Netherlands; SOVON, Nijmegen, The Netherlands; Wetlands International, Wageningen, Rhe Netherlands; BirdLife International, Cambridge, UK & Common Wadden Sea Secretariat, Wilhelmshaven, Germany.Google Scholar
  68. Wiersma, P. & T. Piersma, 1994. Effects of microhabitat, flocking, climate and migratory goal on energy expenditure in the annual cycle of red knots. Condor 96: 257–279.CrossRefGoogle Scholar
  69. Wolff, W. J. & C. J. Smit, 1990. The Banc d’Arguin, Mauritania, as an environment for coastal birds. Ardea 78: 17–38.Google Scholar
  70. Wolff, W. J., J. van der Land, P. H. Nienhuis & P. A. J. W. de Wilde, 1993. The functioning of the ecosystem of the Banc d’Arguin, Mauritania: a review. Hydrobiologia 258: 211–222.CrossRefGoogle Scholar
  71. Wolfrath, B., 1992. Field experiments on feeding of European fiddler crab Uca tangeri. Marine Ecology Progress Series 90: 39–43.CrossRefGoogle Scholar
  72. Wootton, J. T., 1997. Estimates and tests of per capita interaction strength: diet, abundance, and impact of intertidally foraging birds. Ecological Monographs 67: 45–64.CrossRefGoogle Scholar
  73. Ysebaert, T. J. & P. M. J. Herman, 2002. Spatial and temporal variation in benthic macrofauna and relationships with environmental variables in an estuarine, intertidal soft-sediment environment. Marine Ecology Progress Series 244: 105–124.CrossRefGoogle Scholar
  74. Ysebaert, T. J., P. Meire, P. M. J. Herman & H. Verbeek, 2002. Macrobenthic species response surfaces along estuarine gradients: prediction by logistic regression. Marine Ecology Progress Series 225: 79–95.CrossRefGoogle Scholar
  75. Zabbey, N. & A. Hart, 2014. Spatial variability of macrozoobenthic diversity on tidal flats of the Niger Delta, Nigeria: the role of substratum. African Journal of Aquatic Science 39: 67–76.CrossRefGoogle Scholar
  76. Zwarts, L., 1985. The winter exploitation of fiddler crabs Uca tangeri by waders in Guinea-Bissau. Ardea 73: 3–12.Google Scholar
  77. Zwarts, L. & A.-M. Blomert, 1992. Why knot Calidris canutus take medium-sized Macoma balthica when six prey species are available. Marine Ecology Progress Series 83: 113–128.CrossRefGoogle Scholar
  78. Zwarts, L. & J. H. Wanink, 1993. How the food supply harvestable by waders in the Wadden Sea depends on the variation in energy density, body weight, biomass, burying depth and behaviour of tidal-flat invertebrates. Netherlands Journal of Sea Research 31: 441–476.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Departamento de Biologia Animal, Centro de Estudos do Ambiente e do Mar (CESAM)Faculdade de Ciências da Universidade de LisboaLisbonPortugal

Personalised recommendations