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Utilisation of intertidal mudflats by the Dunlin Calidris alpina in relation to microphytobenthic biofilms

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Abstract

The small-scale spatial distribution of Dunlin Calidris alpina staging and wintering in Bourgneuf Bay (France) was investigated on two different mudflats colonized by either epipsammic- or epipelic-dominated microphytobenthos assemblages. Shorebird counts were conducted monthly at ebb tide from October 2011 to May 2012 and from November 2012 to May 2013. Multiple linear regressions followed by hierarchical partitioning of variance showed that microphytobenthos biomass was not a significant factor to explain Dunlin densities. However, on epipelic-dominated mudflats, Dunlins did not show their typical “tide follower” behaviour and instead significantly selected the highest microphytobenthos biomass zones. The biomass of a gastropod predator of an important local Dunlin prey, Retusa obtusa, was negatively correlated with Dunlin densities. This paper provides new suggestions in the ways that biofilms on mudflats affect small shorebird foraging.

Zusammenfassung

Die Nutzung von Wattflächen durch Alpenstrandläufer Calidris alpina im Hinblick auf mikrophytobenthische Biofilme

Die kleinräumige Verteilung von Alpenstrandläufern Calidris alpina, die in der Bucht von Bourgneuf (Frankreich) rasten und überwintern, wurde auf zwei verschiedenen Wattflächen untersucht, die von Mikrophytobenthosgemeinschaften besiedelt wurden, welche entweder von epipsammischen oder epipelischen Arten dominiert wurden. Watvogelzählungen wurden monatlich bei Ebbe von Oktober 2011 bis Mai 2012 durchgeführt. Multiple lineare Regressionen, gefolgt von der hierarchischen Partitionierung der Varianz, zeigten, dass die Biomasse des Mikrophytobenthos keinen signifikanten Einfluss auf die Dichte der Alpenstrandläufer hatte. Auf von epipelischen Arten dominierten Wattflächen zeigten Alpenstrandläufer jedoch nicht ihr typisches “Gezeitenfolgeverhalten”, sondern wählten stattdessen die Zonen mit der höchsten Mikrophytobenthosbiomasse. Die Biomasse einer Schnecke, die eine wichtige lokale Beute des Alpenstrandläufers frisst (Retusa obtusa), zeigte eine negative Korrelation mit der Alpenstrandläuferdichte. Diese Studie liefert neue Hinweise, dass Biofilme auf Wattflächen das Nahrungsverhalten kleiner Watvögel beeinflussen.

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References

  • Baker MC, Baker AEM (1973) Niche relationships among six species of shorebirds on their wintering and breeding ranges. Ecol Monogr 43:193–212

    Google Scholar 

  • Beninger PG, Elner RW, Morançais M, Decottignies P (2011) Downward trophic shift during breeding migration in the shorebird Calidris mauri (Western Sandpiper). Mar Ecol Prog Ser 428:259–269

    Google Scholar 

  • Berry AJ, Radhakrishnan KV, Coward K (1992) Is seasonal breeding in Retusa obtusa (Montagu) (Gastropoda: Opisthobranchia) merely the consequence of seasonal breeding in its prey, the mudsnail Hydrobia ulvae (Pennant)? J Exp Mar Biol Ecol 159:179–189

    Google Scholar 

  • Bocher P, Drouet S, Mahéo R, Le Drean-Quenec’hdu S, Guyot T, Caillot E (2014) Distribution, phenology and long-term trends of Dunlin Calidris alpina in France. Wader Study Group Bull 121:23–32

  • Burger J (1984) Abiotic factors affecting migrant shorebirds. In: Burger J, Olla BL (eds) Shorebirds: migration and foraging behavior. Plenum, New York, pp 1–72

    Google Scholar 

  • Burger J, Howe MA, Hahn DC, Chase J (1977) Effects of tide cycles on habitat selection and habitat partitioning by migrating shorebirds. Auk 94:743–758

    Google Scholar 

  • Burton PJK (1974) Feeding and the feeding apparatus in waders. British Museum (Natural History), London

  • Burton NHK, Musgrove AJ, Rehfisch MM (2004) Tidal variation in numbers of waterbirds: how frequently should birds be counted to detect change and do low tide counts provide a realistic average? Bird Study 51:48–57

    Google Scholar 

  • Carpentier A, Como S, Dupuy C, Lefrançois C, Feunteun E (2014) Feeding ecology of Liza spp. in a tidal flat: evidence of the importance of primary production (biofilm) and associated meiofauna. J Sea Res 92:86–91

    Google Scholar 

  • Cartaxana P, Jesus B, Brotas V (2003) Pheophorbide and pheophytin a-like pigments as useful markers for intertidal microphytobenthos grazing by Hydrobia ulvae. Estuar Coast Shelf Sci 58:293–297

    CAS  Google Scholar 

  • Colwell MA (1993) Shorebird community patterns in a seasonally dynamic estuary. Condor 95:104–114

    Google Scholar 

  • Davis CA, Smith LM (2001) Foraging strategies and niche dynamics of coexisting shorebirds at stopover sites in the Southern Great Plains. Auk 118:484–495

    Google Scholar 

  • Deceunick B, Mahéo R (2000) Synthèse des dénombrements et analyse des tendances des limicoles hivernant en France 1978–1999. WI/LPO/DNP

  • Decottignies P, Beninger PG, Rincé Y, Robins RJ, Riera P (2007) Exploitation of natural food sources by two sympatric, invasive suspension-feeders, Crassostrea gigas and Crepidula fornicata. Mar Ecol Prog Ser 334:179–192

    CAS  Google Scholar 

  • Delany S, Scott DA, Dodman T, Stroud DA (2009) An atlas of wader populations in Africa and Western Eurasia. Wetlands International and Wader Study Group, Wageningen

    Google Scholar 

  • Dias MP, Granadeiro JP, Martins RC, Palmeirim JM (2006) Estimating the use of tidal flats by waders: inaccuracies due to the response of birds to the tidal cycle. Bird Study 53:32–38

    Google Scholar 

  • Dias MP, Granadeiro JP, Palmeirim JM (2009) Searching behaviour of foraging waders: does feeding success influence their walking? Anim Behav 77:1203–1209

    Google Scholar 

  • Dierschke V, Kube J, Probst S, Brenning U (1999) Feeding ecology of dunlins Calidra alpina staging in the southern Baltic Sea, 1. Habitat use and food selection. J Sea Res 42:49–64

    Google Scholar 

  • Durell D, Le Sea V, Kelly CP (1990) Diets of Dunlin Calidris alpina and Grey Plover Pluvialis squatarola on the Wash as determined by dropping analysis. Bird Study 37:44–47

    Google Scholar 

  • Finn PG, Catterall CP, Driscoll PV (2008) Prey versus substrate as determinants of habitat choice in a feeding shorebird. Estuar Coast Shelf Sci 80:381–390

    Google Scholar 

  • Godet L, Toupoint N, Fournier J, Mao PL, Retière C, Olivier F (2009) Clam farmers and Oystercatchers: effects of the degradation of Lanice conchilega beds by shellfish farming on the spatial distribution of shorebirds. Mar Poll Bull 58:589–595

    CAS  Google Scholar 

  • Granadeiro JP, Dias MP, Martins RC, Palmeirim JM (2006) Variation in numbers and behaviour of waders during the tidal cycle: implications for the use of estuarine sediment flats. Acta Oecol 29:293–300

    Google Scholar 

  • Granadeiro JP, Santos CD, Dias MP, Palmeirim JM (2007) Environmental factors drive habitat partitioning in birds feeding in intertidal flats: implications for conservation. Hydrobiologia 587:291–302

    Google Scholar 

  • Jesus B, Brotas V, Ribeiro L, Mendes CR, Cartaxana P, Paterson DM (2009) Adaptations of microphytobenthos assemblages to sediment type and tidal position. Cont Shelf Res 29:1624–1634

    Google Scholar 

  • Jing Z, Kai J, Xiaojing G, Zhijun M (2007) Food supply in intertidal area for shorebirds during stopover at Chongming Dongtan, China. Acta Ecol Sin 27:2149–2159

    Google Scholar 

  • Kelly JP, Warnock N, Page GW, Weathers WW (2002) Effects of weather on daily body mass regulation in wintering dunlin. J Exp Biol 205:109–120

    PubMed  Google Scholar 

  • Kelsey MG, Hassall M (1989) Patch selection by Dunlin on a heterogeneous mudflat. Ornis Scand 20:250–254

    Google Scholar 

  • Kuwae T, Beninger PG, Decottignies P, Mathot KJ, Lund DR, Elner RW (2008) Biofilm grazing in a higher vertebrate: the Western Sandpiper, Calidris mauri. Ecology 89:599–606

    PubMed  Google Scholar 

  • Kuwae T, Miyoshi E, Sassa S, Watabe Y (2010) Foraging mode shift in varying environmental conditions by dunlin Calidris alpina. Mar Ecol Prog Ser 406:281–289

    Google Scholar 

  • Kuwae T et al (2012) Variable and complex food web structures revealed by exploring missing trophic links between birds and biofilm. Ecol Lett 15:347–356

    PubMed  Google Scholar 

  • Le Dréan-Quénec’hdu S, Mahéo R, Boret P (1995) Mont Saint Michel Bay: spatial distribution of major wader species. Wader Study Group Bull 77:55–61

    Google Scholar 

  • MacNally R (2000) Regression and model-building in conservation biology, biogeography and ecology: the distinction between—and reconciliation of—‘predictive’ and ‘explanatory’ models. Biodivers Conserv 9:655–671

    Google Scholar 

  • Mahéo R, Le Dréan-Quénec’hdu S (2012) Limicoles séjournant en France (Littoral), 35ème contribution française aux dénombrements internationaux des oiseaux d’eau organisés (limicoles côtiers) organisés par Wetlands International. Office National de la Chasse et de la Faune Sauvage, France

    Google Scholar 

  • Mathot KJ, Lund DR, Elner RW (2010) Sediment in stomach contents of Western Sandpipers and Dunlin provide evidence of biofilm feeding. Waterbirds 33:300–306

    Google Scholar 

  • Meire PM, Kuyken E (1984) Relations between the distribution of waders and the intertidal benthic fauna of the Oosterschelde, Netherland. In: Evans PR, Goss-Custard JD, Hale W (eds) Coastal waders and waterfowl in winter. Cambridge University Press, Cambridge, pp 57–68

    Google Scholar 

  • Méléder V, Launeau P, Barillé L, Rincé Y (2003) Cartographie des peuplements du microphytobenthos par télédétection visible-infrarouge dans un écosystème conchylicole. CR Biol 326:377–389

    Google Scholar 

  • Méléder V, Barillé L, Rincé Y, Morançais M, Rosa P, Gaudin P (2005) Spatio-temporal changes in microphytobenthos structure analysed by pigment composition in a macrotidal flat (Bourgneuf Bay, France). Mar Ecol Prog Ser 297:83–99

    Google Scholar 

  • Méléder V, Rincé Y, Barillé L, Gaudin P, Rosa P (2007) Spatiotemporal changes in microphytobenthos assemblages in a macrotidal flat (Bourgneuf Bay, France). J Phycol 43:1177–1190

    Google Scholar 

  • Méléder V, Launeau P, Kazémipour F, Barillé L (2013) Microphytobenthos assessment by hyperspectral remote sensing: the first temporal survey (2002 to 2011). In: 8th EARSeL SIG imaging spectroscopy Workshop, Nantes, France, 8–10 April 2013

  • Moreira F (1997) The importance of shorebirds to energy fluwes in a food web of a south european estuary. Estuar Coast Shelf Sci 44:67–78

    Google Scholar 

  • Moreira F (1999) On the use by birds of intertidal areas of the Tagus estuary: implications for management. Aquat Ecol 33:301–309

    Google Scholar 

  • Mouritsen KN, Jensen KT (1992) Choice of microhabitat in tactile foraging dunlins Calidris alpina: the importance of sediment penetrability. Mar Ecol Prog Ser 85:1–8

    Google Scholar 

  • Nehls G, Tiedemann R (1993) What determines the densities of feeding birds on tidal flats? A case study on dunlin, Calidris alpina, in the Wadden Sea. Neth J Sea Res 31:375–384

    Google Scholar 

  • Piersma T (2012) What is habitat quality? Dissecting a research portfolio on shorebirds. In: Fuller R (ed) Birds and habitat: relationships in changing landscapes. Cambridge University Press, Cambridge, pp 383–407

    Google Scholar 

  • Piersma T, Hoekstra R, Dekinga A, Koolhaas A, Wolf P, Battley PF, Wiersma P (1993) Scale and intensity of intertidal habitat use by knots Calidris canutus in the western Wadden Sea in relation to food, friends and foes. Neth J Sea Res 31:331–357

    Google Scholar 

  • Quaintenne G, van Gils JA, Bocher P, Dekinga A, Piersma T (2011) Scaling up ideals to freedom: are densities of red knots across western Europe consistent with ideal free distribution? Proc R Soc Lond B 278:2728–2736

    Google Scholar 

  • Quinn JT, Hamilton DJ (2012) Variation in diet of Semipalmated Sandpipers (Calidris pusilla) during stopover in the upper Bay of Fundy, Canada. Can J Zool 90:1181–1190

    Google Scholar 

  • Rosa S, Granadeiro JP, Cruz M, Palmeirim JM (2007) Invertebrate prey activity varies along the tidal cycle and depends on sediment drainage: consequences for the foraging behaviour of waders. J Exp Mar Biol Ecol 353:35–44

    Google Scholar 

  • Skagen SK, Oman HD (1996) Dietary flexibility of shorebirds in the Western Hemisphere. Can Field Nat 110:419–444

    Google Scholar 

  • Smit CJ, Piersma T (1989) Numbers, midwinter distribution, and migration of wader populations using the East Atlantic Flyway. In: Boyd H, Pirot J-Y (eds) Flyways and reserve networks for water birds. International Waterfowl Research Bureau, Slimbridge, pp 24–63

    Google Scholar 

  • Tucker CJ (1979) Red and photographic infrared linear combinations for monitoring vegetation. Remote Sens Environ 8:127–150

    Google Scholar 

  • van de Kam J, Ens BJ, Piersma T, Zwarts L (2004) Shorebirds. An illustrated behavioural ecology. KNNV, Utrecht

    Google Scholar 

  • van der Wal D, Herman PMJ, Forster RM, Ysebaert T, Rossi F, Knaeps E, Plancke YMG, Ides SJ (2008) Distribution and dynamics of intertidal macrobenthos predicted from remote sensing: response to microphytobenthos and environment. Mar Ecol Prog Ser 367:57–72

    Google Scholar 

  • van Gils JA, Piersma T (2004) Digestively constrained predators evade the cost of interference competition. J Anim Ecol 73:386–398

    Google Scholar 

  • van Gils JA, de Rooij SR, van Belle J, van der Meer J, Dekinga A, Piersma T, Drent R (2005) Digestive bottleneck affects foraging decisions in red knots Calidris canutus I. Prey choice. J Anim Ecol 74:105–119

    Google Scholar 

  • van Gils JA, Spaans B, Dekinga A, Piersma T (2006) Foraging in a tidally structured environment by red knots (Calidris canutus): ideal, but not free. Ecology 87:1189–1202

    Google Scholar 

  • Yates MG, Goss-Custard JD, McGrorty S, Lakhani KH, Durell D, Le Sea V, Clarke RT, Rispin WE, Moy I, Yates T, Plant RA, Frost AJ (1993) Sediment characteristics, invertebrates densities and shorebird densities on the inner banks of the Wash. J Appl Ecol 30:599–614

    Google Scholar 

  • Zwarts L, Wanink JH (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. Neth J Sea Res 31:441–476

    Google Scholar 

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Acknowledgments

We are grateful to the local authorities (Délégation à la Mer et au Littoral—Direction Départementale des Territoires et de la Mer) that allowed us to carry our study through. The experiments comply with the current French laws. We thank P. Bocher, P. Pineau, N. Lachaussée, G. Quaintenne, C. Parrain, P. Rosa, P. Gaudin, I. Benyoucef, P. Gambin-Pozo, V. Méléder, A. Lerouxel and others for their collaboration during fieldwork and cartography. We extend our sincere thanks to M. Amat, E. De Carheil and B. Jesus for the English revisions.

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Correspondence to Priscilla Decottignies.

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Communicated by F. Bairlein.

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Drouet, S., Turpin, V., Godet, L. et al. Utilisation of intertidal mudflats by the Dunlin Calidris alpina in relation to microphytobenthic biofilms. J Ornithol 156, 75–83 (2015). https://doi.org/10.1007/s10336-014-1133-x

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  • DOI: https://doi.org/10.1007/s10336-014-1133-x

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