Abstract
The role of multi-species benthic diatom films (BDF) in the settlement of late pediveliger larvae of the bivalve Macoma balthica was investigated in still-water bioassays and multiple choice flume experiments. Axenic diatom cultures that were isolated from a tidal mudflat inhabited by M. balthica were selected to develop BDF sediment treatments characterized by a different community structure, biomass, and amount of extracellular polymeric substances (EPS). Control sediments had no added diatoms. Although all larvae settled and initiated burrowing within the first minute after their addition in still water, regardless of treatment, only 48–52% had completely penetrated the high diatom biomass treatments after 5 min, while on average 80 and 69% of the larvae had settled and burrowed into the control sediments and BDF with a low diatom biomass (<3.5 μg Chl a g−1 dry sediment), respectively. The percentage of larvae settling and burrowing into the sediment was negatively correlated with the concentration of Chl a and EPS of the BDF. This suggests higher physical resistance to bivalve penetration by the BDF with higher diatom biomass and more associated sugar and protein compounds. The larval settlement rate in annular flume experiments at flow velocities of 5 and 15 cm s−1 was distinctly lower compared to the still-water assays. Only 4.6–5.8% of the larvae were recovered from BDF and control sediments after 3 h. Nonetheless, a clear settlement preference was observed for BDF in the flume experiments; i.e., larvae settled significantly more in BDF compared to control sediments irrespective of flow speed. Comparison with the settlement of polystyrene mimics and freeze-killed larvae led to the conclusion that active selection, active secondary dispersal and, at low flow velocities (5 cm s−1), passive adhesion to the sediment are important mechanisms determining the settlement of M. balthica larvae in estuarine biofilms.
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References
Bao WY, Satuito CG, Yank JL, Kitamura H (2007) Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis in response to biofilms. Mar Biol 150:565–574
Beukema JJ (1976) Biomass and species richness of the macrobenthic animals living on tidal flats of the Dutch Wadden Sea. Neth J Sea Res 10:236–261
Beukema JJ, Devlas 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 52:193–200
Bocher P, Piersma T, Dekinga A, Kraan C, Yates MG, Guyot T, Folmer EO, Radenac G (2007) Site- and species-specific distribution patterns of mollusks at five intertidal soft-sediment areas in northwest Europe during a single winter. Mar Biol 151:577–594
Bos OG (2005) Recruitment variation of Macoma balthica (L.) is there a role for larval food limitation? PhD thesis, Groningen University
Bos OG, Phillipart CJM, Cadée GC, Van der Meer J (2006) Recruitment variation in Macoma balthica: a laboratory examination of the match/mismatch hypothesis. Mar Ecol Prog Ser 320:207–214
Butman CA (1987) Larval settlement of soft-sediment invertebrates: the spatial scales of pattern explained by active habitat selection and the emerging role of hydrodynamical processes. Oceanogr Mar Biol Annu Rev 25:113–165
Caddy JF (1967) Maturation of gametes and spawning in Macoma balthica (L). Can J Zool 45:955–965
Chiu JMY, Thiyagarajan V, Pechenik JA, Hung OS, Qian PY (2007) Influence of bacteria and diatoms in biofilms on metamorphosis of the marine slipper limpet Crepidula onyx. Mar Biol 151:1417–1431
Dahms HU, Dobretsov S, Qian PY (2004) The effect of bacterial and diatom biofilms on the settlement of the bryozoan Bugula neritina. J Exp Mar Biol Ecol 313:191–209
De Boer PL (1981) Mechanical effects of microorganisms on intertidal bedform migration. Sedimentology 28:129–132
de Brouwer JFC, Stal LJ (2001) Short-term dynamics in microphytobenthos distribution and associated extracellular carbohydrates in surface sediments of an intertidal mudflat. Mar Ecol Prog Ser 218:33–44
Decho AW (2000) Microbial biofilms in intertidal systems: an overview. Cont Shelf Res 20:1257–1273
de Jong DJ, de Jonge VN (1995) Dynamics and distribution of microphytobenthic chlorophyll a in the Western Scheldt estuary (SW Netherlands). Hydrobiologia 311:21–30
Dobretsov S, Qian PY (2006) Facilitation and inhibition of larval attachment of the bryozoan Bugula neritina in association with mono-species and multi-species biofilms. J Exp Mar Biol Ecol 333:263–274
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Calorimetric method for determination of sugar and related substances. Anal Chem 28:350–356
Dworjanyn SA, Pirozzi I (2008) Induction of settlement in the sea urchin Tripneustes gratilla by macroalgae, biofilms and conspecifics: a role for bacteria? Aquaculture 274:268–274
Engstrom SJ, Marinelli RL (2005) Recruitment responses of benthic infauna to manipulated sediment geochemical properties in natural flows. J Mar Res 63:407–436
Esser F, Winterberg M, Sebesvari Z, Harder T (2008) Effects of halogenated metabolites from infaunal polychaetes on larval settlement of the spionid polychaete Streblospio benedicti. Mar Ecol Prog Ser 355:161–172
Forster RM, Creach V, Sabbe K, Vyverman W, Stal LJ (2006) Biodiversity–ecosystem function relationship in microphytobenthic diatoms of the Westerschelde estuary. Mar Ecol Prog Ser 311:191–201
Grassle JP, Butman CA, Mills SW (1992) Active habitat selection by Capitella sp. 1 larvae. II. Multiple choice experiments in still water and flume flows. J Mar Res 50:717–743
Gross TF, Werner FE, Eckman JE (1992) Numerical modelling of larval settlement in turbulent bottom boundary layers. J Mar Res 50:611–642
Guillard RL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith LW, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York
Harder T, Lam C, Qian PY (2002) Induction of larval settlement in the polychaete Hydroides elegans by marine biofilms: an investigation of monospecific diatom films as settlement cues. Mar Ecol Prog Ser 229:105–112
Hiddink JG (2003) Modelling the adaptive value of intertidal migration and nursery use in the bivalve Macoma balthica. Mar Ecol Prog Ser 252:173–185
Hiddink JG, Kock RP, Wolff WJ (2002a) Active pelagic migrations of the bivalve Macoma balthica are dangerous. Mar Biol 140:1149–1156
Hiddink JG, Marijnssen SAE, Troost K, Wolff WJ (2002b) Predation on 0-group and older classes of the bivalve Macoma balthica: interaction of size selection and intertidal distribution of epibenthic predators. J Exp Mar Biol Ecol 269:223–248
Hiddink JG, ter Hofstede R, Wolff WJ (2002c) Predation of intertidal infauna on juveniles of the bivalve Macoma balthica. J Sea Res 47:141–159
Hills JM, Thomason JC, Milligan JL, Richardson M (1998) Do barnacle larvae respond to multiple settlement cues over a range of spatial scales? Hydrobiologia 175(376):101–111
Honkoop PJC, Luttikhuizen PC, Piersma T (1999) Experimentally extending the spawning season of a marine bivalve using temperature change and fluoxetine as synergistic triggers. Mar Ecol Prog Ser 180:297–300
Hulscher JB (1982) The oystercatcher Haematopus ostralegus as a predator of the bivalve Macoma balthica in the Dutch Wadden Sea. Ardea 70:89–152
Jonsson PR, Andre C, Lindegarth M (1991) Swimming behavior of marine bivalve larvae in a flume boundary layer flow: evidence for near-bottom confinement. Mar Ecol Prog Ser 79:67–76
Jonsson PR, Berntsson KM, Larsson AI (2004) Linking larval supply to recruitment: flow-mediated control of initial adhesion of barnacle larvae. Ecology 85:2850–2859
Jouuchi T, Satuito CG, Kitamura H (2007) Sugar compound products of the periphytic diatom Navicula ramosissima induce larval settlement in the barnacle, Amphibalanus amphitrite. Mar Biol 152:1065–1076
Keough MJ, Raimondi PT (1995) Responses of settling invertebrate larvae to bioorganic films: effects of different types of films. J Exp Mar Biol Ecol 185:235–253
Lam C, Harder T, Qian PY (2003) Induction of larval settlement in the polychaete Hydroides elegans by surface-associated settlement cues of marine benthic diatoms. Mar Ecol Prog Ser 263:83–92
Lam C, Harder T, Qian PY (2005) Induction of larval settlement in the polychaete Hydroides elegans by extracellular polymers of benthic diatoms. Mar Ecol Prog Ser 286:145–154
Lindegarth M, Jonsson PR (1991) Fluorescent microparticles: a new way of visualizing sedimentation and larval settlement. Limnol Oceanogr 36:1471–1476
MacIntyre HL, Geider RJ, Miller DC (1996) Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow water marine habitats. I. Distribution, abundance and primary production. Estuaries 19:186–201
Marinelli RL, Williams TJ (2003) Evidence for density-dependent effects of infauna on sediment biogeochemistry and benthic–pelagic coupling in nearshore systems. Estuar Coast Shelf Sci 57:179–192
Marinelli RL, Woodin SA (2002) Experimental evidence for linkages between infaunal recruitment, disturbance, and sediment surface chemistry. Limnol Oceanogr 47:221–229
Marinelli RL, Woodin SA (2004) Disturbance and recruitment: a test of solute and substrate specificity using Mercenaria mercenaria and Capitella sp. 1. Mar Ecol Prog Ser 269:209–221
Martini IP, Morrison RIG (1987) Regional distribution of Macoma balthica and Hydrobia minuta on the sub-Arctic coasts of Hudson Bay and James Bay, Ontario, Canada. Estuar Coast Shelf Sci 24:47–68
Moens T, Verbeeck L, de Maeyer A, Swings J, Vincx M (1999) Selective attraction of marine bacterivorous nematodes to their bacterial food. Mar Ecol Prog Ser 176:165–178
Montserrat F, Van Colen C, Degraer S, Ysebaert T, Herman PMJ (2008) Benthic community-mediated sediment dynamics. Mar Ecol Prog Ser 372:43–59
Nikula R, Strelkov P, Väinola R (2007) Diversity and trans-Arctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia: Tellinidae). Evolution 61:928–941
Olivier F, Desroy N, Retière C (1996) Habitat selection and adult-recruit interactions in Pectinaria koreni (Malmgren) (Annelide: Polychaeta) post-larval populations: results of flume experiments. J Sea Res 36:217–226
Olivier F, Tremblay R, Bourget E, Rittschof D (2000) Barnacle settlement: field experiments on the influence of larval supply, tidal level, biofilm quality and age on Balanus amphitrite cyprids. Mar Ecol Prog Ser 199:185–204
Patil JS, Anil AC (2005) Influence of diatom exopolymers and biofilms on metamorphosis in the barnacle Balanus amphitrite. Mar Ecol Prog Ser 301:231–245
Pawlik JF (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol Annu Rev 30:274–278
Pawlik JR, Butman CA (1993) Settlement of a marine tube worm as a function of current velocity: interacting effects of hydrodynamics and behavior. Limnol Oceanogr 38:1730–1740
Pawlik JR, Butman CA, Starczak VR (1991) Hydrodynamic facilitation of gregarious settlement of a reef-building tube worm. Science 251:421–424
Pineda J, Reyns NB, Starczak VR (2009) Complexity and simplification in understanding recruitment in benthic populations. Popul Ecol 51:17–32
Qian PY, Lau SCK, Dahms HU, Dobretsov S, Harder T (2007) Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture. Mar Biotechnol 9:399–410
Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Reading CJ (1979) Changes in the downshore distribution of Macoma balthica (L) in relation to shell length. Estuar Coast Mar Sci 8:1–13
Rossi F, Herman PMJ, Middelburg JJ (2004) Interspecific and intraspecific variation of delta C13 and delta N15 in deposit- and suspension-feeding bivalves (Macoma balthica and Cerastoderma edule): evidence of ontogenetic changes in feeding mode of Macoma balthica. Limnol Oceanogr 49:408–414
Sabbe K, Vyverman W (1991) Distribution of benthic diatom assemblages in the Westerschelde (Zeeland, The Netherlands). Belg J Bot 124:91–101
Sebesvari Z, Esser F, Harder T (2006) Sediment-associated cues for larval settlement of the infaunal spionid polychaetes Polydora cornuta and Streblospio benedicti. J Exp Mar Biol Ecol 337:109–120
Snelgrove PVR, Grassle JP, Butman CA (1998) Sediment choice by settling larvae of the bivalve, Spisula solidissima (Dillwyn), in flow and still water. J Exp Mar Biol Ecol 231:171–190
Snelgrove PVR, Grant J, Pilditch CA (1999) Habitat selection and adult–larvae interactions in settling larvae of soft-shell clam Mya arenaria. Mar Ecol Prog Ser 182:149–159
Snelgrove PVR, Grassle JP, Zimmer CA (2001) Adult macrofauna effects on Capitella sp. I larval settlement: a laboratory flume study. J Mar Res 59:657–674
Sokal RR, Rohlf FJ (1995) Biometry. WH Freeman, New York
Tankersley RA, Welch JM, Forward RD (2002) Settlement times of blue crab (Callinectes sapidus) megalopae during flood-tide transport. Mar Biol 141:863–875
Tolhurst TJ, Black KS, Shayler SA, Mather S, Black I, Baker K, Paterson DM (1999) Measuring the in situ erosion shear stress of intertidal sediments with the Cohesive Strength Meter (CSM). Estuar Coast Shelf Sci 49:281–294
Turner EJ, Zimmer-Faust RK, Palmer MA, Luckenbach M, Pentcheff ND (1994) Settlement of oyster (Crassostrea virginica) larvae: effects of water flow and a water-soluble chemical cue. Limnol Oceanogr 39:1579–1593
Väinola R (2003) Repeated trans-Arctic invasions in littoral bivalves: molecular zoogeography of the Macoma balthica complex. Mar Biol 143:935–946
Van Colen C, Monsterrat F, Vincx M, Herman PMJ, Ysebaert T, Degraer S (2008) Macrobenthic recovery from hypoxia in an estuarine tidal mudflat. Mar Ecol Prog Ser 372:31–42
Van Colen C, Snoeck F, Struyf K, Vincx M, Degraer S (2009) Macrobenthic community structure and distribution in the Zwin nature reserve (Belgium and the Netherlands). J Mar Biol Assoc UK 89:431–438
Van der Meer J, Beukema JJ, Dekker R (2003) Large spatial variability in lifetime egg production in an intertidal Baltic tellin (Macoma balthica) population. Helgol Mar Res 56:274–278
Whitlatch RB, Lohrer AM, Thrush SF (2001) Scale-dependent recovery of the benthos: effects of larval and post-larval life stages. In: Aller JY, Woodin SA, Aller RC (eds) Organism–sediment interactions. University of South Carolina Press, USA, pp 181–197
Widdows J, Brinsley MD, Bowley N, Barrett C (1998) A benthic annular flume for in situ measurement of suspension feeding/biodeposition rates and erosion potential of intertidal cohesive sediments. Estuar Coast Shelf Sci 46:27–38
Wieczorek SK, Clare AS, Todd CD (1995) Inhibitory and facilitatory effects of microbial films on settlement of Balanus amphitrite larvae. Mar Ecol Prog Ser 119:221–228
Woodin SA, Marinelli RL, Lincoln DE (1993) Allelochemical inhibition of recruitment in a sedimentary assemblage. J Chem Ecol 19:517–530
Woodin SA, Lindsay SM, Wethey DS (1995) Process-specific recruitment cues in marine sedimentary systems. Biol Bull 189:49–58
Woodin SA, Marinelli RL, Lindsay SM (1998) Process-specific cues for recruitment in sedimentary environments: geochemical signals? J Mar Res 56:535–558
Ysebaert T, Herman PMJ, Meire P, Craeymeersch J, Verbeek H, Heip CHR (2003) Large-scale spatial patterns in estuaries: estuarine macrobenthic communities in the Schelde estuary, NW Europe. Estuar Coast Shelf Sci 57:335–355
Zardus JD, Nedved BT, Huang Y, Tran C, Hadfield MG (2008) Microbial biofilms facilitate adhesion in biofouling invertebrates. Biol Bull 214:91–98
Zwarts L, Blomert AM (1992) Why knot Calidris canutus take medium-sized Macoma balthica when 6 prey species are available? Mar Ecol Prog Ser 83:113–128
Acknowledgments
This research was supported by the Institute for the Promotion of Innovation through Science and Technology in Flanders, Belgium (IWT Vlaanderen). We would like to thank John Widdows and Peter Herman for their comments on the flume and experimental design, Tjeerd Bouma for his help with the ADV measurements, Jurgen Verstraeten and Yves Israël for construction of the annular flume, and Giovanni A.P. Dos Santos, Tatiana Maria, and Katia Guilini for their aid on bacterial quantification. Annick Verween, Annick Van Kenhove, Danielle Schram, Annelien Rigaux, and Dirk Van Gansbeke are acknowledged for their assistance during processing of the samples and maintenance of the larval cultures. The comments of three anonymous referees substantially improved the manuscript. This paper contributes to the Ghent University BBSea Project (GOA 01600705) and the EU Network of Excellence Marbef (GOCE-CT-2003-505446, contribution nr. 9035). This is NIOO-KNAW publication nr. 4553.
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Van Colen, C., Lenoir, J., De Backer, A. et al. Settlement of Macoma balthica larvae in response to benthic diatom films. Mar Biol 156, 2161–2171 (2009). https://doi.org/10.1007/s00227-009-1246-6
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DOI: https://doi.org/10.1007/s00227-009-1246-6