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Marine Biology

, 166:144 | Cite as

Meiofauna versus macrofauna as a food resource in a tropical intertidal mudflat

  • Pierre-Yves PascalEmail author
  • Pierrick Bocher
  • Christel Lefrançois
  • Hien T. Nguyen
  • Johan Chevalier
  • Christine Dupuy
Original Paper

Abstract

Evaluations of the functioning of benthic marine food webs could be improved by quantifying organic matter fluxes from the meiofauna to higher trophic levels. In this study, we measured the simultaneous ingestion of meiofauna and macrofauna by common dwellers of a tropical intertidal mudflat on the coast of Amazonia. The meiofauna and macrofauna (tanaid) communities of a tropical intertidal mudflat of French Guiana were separately enriched with 15N and 13C, respectively. The enriched preys were then used as tracers during feeding experiments with common predators of different sizes and feeding mechanisms: a Portunidae crab (Callinectes bocourti), a Penaeidae shrimp (Farfantepenaeus subtilis), and a Gobiidae fish (Gobionellus oceanicus). In feeding experiments with all predators except crabs, feeding rates increased with the availability of meiofauna and macrofauna food sources. The ability of consumers to ingest their food selectively was evaluated by calculating the differences in the ratio of macrofauna to meiofauna between the (1) ingested material and (2) that available in the environment. Larger predators showed a higher degree of preferential macrofauna ingestion than smaller predators, consistent with the optimal foraging theory. For large predators, the meiofauna would be important only during early life or in the absence of large food items.

Notes

Acknowledgements

We would like to thank Antoine Gardel (CNRS Guiana) for technical support in the field, Céline Artero for her help with field work, Jerome Jourde (University of La Rochelle) for identifying C. bocourti and F. subtilis, and three anonymous reviewers for helpful comments. This work received financial support from the CNRS, CNRS Guiana, the University of La Rochelle, and the European Fund for Regional Development (FEDER).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in the study involving animals were in accordance with the ethical standards of French law regarding maintaining animal welfare in research.

References

  1. Aarnio K, Bonsdorff E (1993) Seasonal variation in abundance and diet of the sand goby Pomatoschistus minutus (Pallas) in a northern Baltic Archipelago. Ophelia 37:19–30CrossRefGoogle Scholar
  2. Alheit J, Scheibel A (1982) Benthic harpacticoids as a food source for fish. Mar Biol 70:141–147CrossRefGoogle Scholar
  3. Aller RC, Aller JY (1992) Meiofauna and solute transport in marine muds. Limnol Oceanogr 37:1018–1033CrossRefGoogle Scholar
  4. Arnold WS (1984) The effects of prey size, predator size, and sediment composition on the rate of predation of the blue crab, Callinectes sapidus Rathbun, on the hard clam, Mercenaria mercenaria (Linné). J Exp Mar Biol Ecol 80:207–219CrossRefGoogle Scholar
  5. Austen MC, Widdicombe S (1998) Experimental evidence of effects of the heart urchin Brissopsis lyriferaon-associated subtidal meiobenthic nematode communities. J Exp Mar Biol Ecol 222:219–238CrossRefGoogle Scholar
  6. Bell SS, Coull BC (1978) Field evidence that shrimp predation regulates meiofauna. Oecologia 35:141–148PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bonaglia S, Nascimento FJA, Bartoli M, Klawonn I, Brüchert V (2014) Meiofauna increases bacterial denitrification in marine sediments. Nat Commun 5:5133PubMedPubMedCentralCrossRefGoogle Scholar
  8. Braeckman U, Provoost P, Sabbe K, Soetaert K, Middelburg JJ, Vincx M, Vanaverbeke J (2015) Temporal dynamics in a shallow coastal benthic food web: insights from fatty acid biomarkers and their stable isotopes. Mar Environ Res 108:55–68PubMedCrossRefPubMedCentralGoogle Scholar
  9. Carpenter SR, Chisholm SW, Krebs CJ, Schindler DW, Wright RF (1995) Ecosystem experiments. Science 269:324–327CrossRefGoogle Scholar
  10. Como S, Carpentier A, Rossi F, Dupuy C, Richard P, Feunten E, Lefrancois C (2018) Stable isotope as tracers can reveal resource allocation in juvenile golden gray mullets (Liza aurata, Risso, 1810). J Exp Mar Biol Ecol 503:72–79CrossRefGoogle Scholar
  11. Coull BC (1990) Are members of the meiofauna food for higher trophic levels? Trans Am Microsc Soc 109:233–246CrossRefGoogle Scholar
  12. Coull BC (1999) Role of meiofauna in estuarine soft bottom habitats. Aust J Ecol 24:327–331CrossRefGoogle Scholar
  13. D’Aguillo MC, Harold AS, Darden TL (2014) Diet composition and feeding ecology of the naked goby Gobiosoma bosc (Gobiidae) from four western Atlantic estuaries. J Fish Biol 85:355–373PubMedCrossRefPubMedCentralGoogle Scholar
  14. Danovaro R, Scopa M, Gambi C, Fraschetti S (2007) Trophic importance of subtidal metazoan meiofauna: evidence from in situ exclusion experiments on soft and rocky substrates. Mar Biol 152:339–350CrossRefGoogle Scholar
  15. de Morais T, Bodiou JY (1984) Predation on meiofauna by juvenile fish in a Western Mediterranean flatfish nursery ground. Mar Biol 82:209–215CrossRefGoogle Scholar
  16. De Troch M, Boeckx P, Cnudde C, Van Gansbeke D, Vanreusel A, Vincx M, Caramujo M-J (2012) Bioconversion of fatty acids at the basis of marine food webs: insight from compound-specific stable isotope analysis. Mar Ecol Prog Ser 465:53–67CrossRefGoogle Scholar
  17. Deegan LA, Bowen JL, Drake D, Fleeger JW, Fiedrichs CT, Galván KA, Hobbie JE, Hopkinson CS, Johnson DS, Johnson JM, LeMay LE, Miller E, Peterson BJ, Picard C, Sheldom S, Sutherland M, Vallino J, Warren RS (2007) Susceptibility of salt-marshes to nutrient enrichment and predator removal. Ecol Appl 17:S42–S63CrossRefGoogle Scholar
  18. del Norte-Campos AGC, Temming A (1994) Daily activity, feeding and rations in gobies and brown shrimp in the northern Wadden Sea. Mar Ecol Prog Ser 115:41–53CrossRefGoogle Scholar
  19. Dupuy C, Nguyen TH, Mizrahi D, Jourde J, Bréret M, Agogué H, Beaugeard L, Bocher P (2015) Structure and functional characteristics of the meiofauna community in highly unstable intertidal mudbanks in Suriname and French Guiana (North Atlantic coast of South America). Cont Shelf Res 110:39–47CrossRefGoogle Scholar
  20. Elana U (2017) Projet de parc solaire de la Sarcelle sur la commune de Mana (Guyane). SUEZGoogle Scholar
  21. Fantle MS, Dittel AI, Schwalm SM, Epifanio CE, Fogel ML (1999) A food web analysis of the juvenile blue crab, Callinectes sapidus using stable isotopes in whole animals and individual amino acids. Oecologia 120:416–426CrossRefGoogle Scholar
  22. Feller RJ (2006) Weak meiofaunal trophic linkages in Crangon crangon and Carcinus maenas. J Exp Mar Biol Ecol 330:274–283CrossRefGoogle Scholar
  23. Fitzhugh GR, Fleeger JW (1985) Goby (Pisces: Gobiidae) interactions with meiofauna and small macrofauna. Bull Mar Sci 36:436–444Google Scholar
  24. Fleeger JW (2007) The potential to mass-culture harpacticoid copepods for use as food far larval fish. In: Lee CS, O’Bryen PJ, Marcus NH (eds) Copepods in aquaculture. Blackwell Publishing Professional, AmesGoogle Scholar
  25. Fleeger JW, Johnson DS, Galván KA, Deegan LA (2008) Top-down and bottom-up control of infauna varies across the saltmarsh landscape. J Exp Mar Biol Ecol 357:20–34CrossRefGoogle Scholar
  26. Fry B (2006) Stable isotope ecology. Springer, New-YorkCrossRefGoogle Scholar
  27. Gee JM (1987) Impact of epibenthic predators on estuarine intertidal harpacticoid copepod populations. Mar Biol 96:497–510CrossRefGoogle Scholar
  28. Gee JM (1989) An ecological economic review of meiofauna as food for fish. Zool J Limn Soc 96:243–261CrossRefGoogle Scholar
  29. Gibbons MJ (1988) Impact of predation by juvenile Clinus superciliosus on phytal meiofauna: are fish important as predators? Mar Ecol Prog Ser 45:13–22CrossRefGoogle Scholar
  30. Gibson RN (2003) Go with the flow: tidal migration in marine animals. Hydrobiologia 503:153–161CrossRefGoogle Scholar
  31. Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments. Springer, BerlinGoogle Scholar
  32. Gregg CS, Fleeger JW (1998) Grass shrimp Palaemonetes pugio predation on sediment- and stem-dwelling meiofauna: field and laboratory experiments. Mar Ecol Prog Ser 175:77–86CrossRefGoogle Scholar
  33. Hagerman L, Østrup J (1980) Seasonal and diel activity variations in the shrimp Palaemon adspersus from a Brackish, non-tidal area. Mar Ecol Prog Ser 2:329–335CrossRefGoogle Scholar
  34. Hall SJ, Raffaelli D, Turell WR (1990) Predator-caging experiments in marine systems: a reexamination of their value. Am Nat 136:657–672CrossRefGoogle Scholar
  35. Hamerlynck O, Cattrijsse A (1994) The food of Pomatoschistus minutus (Pisces, Gobiidae) in Belgian coastal waters, and a comparison with the food of its potential competitor P. lozanoi. J Fish Biol 44:753–771CrossRefGoogle Scholar
  36. Henry BA, Jenkins GP (1995) The impact of predation by the girled goby, Nesogobius sp. 1, on abundances of meiofauna and small macrofauna. J Exp Mar Biol Ecol 191:223–238CrossRefGoogle Scholar
  37. Hindley JPR, Alexander CG (1978) Structure and function of the chelate pereiopods of the banana prawn Penaeus merquiensis. Mar Biol 48:153–160CrossRefGoogle Scholar
  38. Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398CrossRefGoogle Scholar
  39. Hoyt M, Fleeger JW, Seibeling R, Feller RJ (2000) Serological estimation of prey-protein gut-residence time and quantification of meal size for grass shrimp consuming meiofaunal copepod. J Exp Mar Biol Ecol 248:105–119PubMedCrossRefPubMedCentralGoogle Scholar
  40. Jonge VND, Bouwman L (1977) A simple density separation technique for quantitative isolation of meiobenthos using the colloidal silica Ludox TM. Mar Biol 42:143–148CrossRefGoogle Scholar
  41. Jourde J, Dupuy C, Nguyen HT, Mizrahi D, da Pracontal N, Bocher P (2017) Low benthic macrofauna diversity in dynamic tropical tidal mudflats: migrating banks on Guiana’s coast, South America. Estuar Coast 40:1159–1170CrossRefGoogle Scholar
  42. Kanou K, Sano M, Kohno H (2005) Ontogenic diet shift, feeding rhythm, and daily ration of juvenile yellowfin goby Acanthogobius flavimanus on a tidal mudflat in the Tama River estuary, central Japan. Ichtyol Res 52:319–324CrossRefGoogle Scholar
  43. Kneib RT (1985) Predation and disturbance by grass shrimp, Palaemonaetes pugio, Holthuis, in soft-substratum invertebrate benthic assemblages. J Exp Mar Biol Ecol 93:91–102CrossRefGoogle Scholar
  44. Kovačić M, la Mesa M (2008) Feeding ecology of De Buen’s goby Buenia affinis, in the Kvarner area (Adriatic Sea). Vie Milieu 58:249–256Google Scholar
  45. Krebs JR (1978) Optimal foraging: decision rules for predators. In: Krebs JR, Davies NB (eds) Behavioural ecology, an evolutionary approach. Blackwell, OxfordGoogle Scholar
  46. Leduc D, Probert PK, Duncan A (2009) A multi-method approach for identifying meiofaunal trophic connections. Mar Ecol Prog Ser 383:95–111CrossRefGoogle Scholar
  47. Legrand E, Martin S, Leroux C, Riera P (2018) Effect of temperature on an algal-grazer trophic transfer: a dual stable isotope (13C,15N) labeling experiment. Mar Ecol 39:e12495CrossRefGoogle Scholar
  48. Leroy F, Riera P, Jeanthon C, Edmond F, Leroux C, Comtet T (2012) Importance of bacterivory and preferential selection toward diatoms in larvae of Crepidula fornicata (L.) assessed by a dual stable isotope (13C,15N) labeling approach. J Sea Res 70:23–31CrossRefGoogle Scholar
  49. Li J, Vincx M, Herman PMJ (1996) A model of nematode dynamics in the Westerschelde Estuary. Ecol Model 90:271–284CrossRefGoogle Scholar
  50. Lipcius RN, Hines AH (1986) Variable functional responses of a marine predator in dissimilar homogeneous microhabitats. Ecology 67:1361–1371CrossRefGoogle Scholar
  51. Majdi N, Hette-Tronquart N, Auclair E, Bec A, Chouvelon T, Cognie B, Danger M, Decottignies P, Dessier A, Desvilettes C, Dubois S, Dupuy C, Fritsch C, Gaucherel C, Hedde M, Jabot F, Lefebvre S, Marzloff MP, Pey B, Peyrard N, Powolny T, Sabbadin R, Thébault E, Perga ME (2018) There’s no harm in having too much: a comprehensive toolbox of methods in trophic ecology. Food Webs 16:e00100CrossRefGoogle Scholar
  52. McCall JN, Fleeger JW (1995) Predation by juvenile fish on hyperbenthic meiofauna: a review with data on post-larval Leiostomus xanthurus. Vie Milieu 45:61–73Google Scholar
  53. Middelburg JJ, Barranguet C, Boschker HTS, Herman PMJ, Moens T, Heip CHR (2000) The fate of intertidal microphytobenthos carbon. An in situ 13C labelling study. Limnol Oceanogr 45:1224–1234CrossRefGoogle Scholar
  54. Moens T, Luyten C, Middelburg JJ, Herman PMJ, Vincx M (2002) Tracing organic matter sources of estuarine tidal flat nematodes with stable carbon isotopes. Mar Ecol Prog Ser 234:127–137CrossRefGoogle Scholar
  55. Moens T, Braeckman U, Derycke S, Fonseca G, Gallucci F, Gingold R, Guilini K, Ingels J, Leduc D, Vanaverbeke J, Van Colen C (2013) Ecology of free-living marine nematode. In: Schmidt-Rhaesa A (ed) Handbook of zoology: gastrotricha, cycloneuralia and gnathifera, Berlin, pp 109–152Google Scholar
  56. Moodley L, Middelburg JJ, Boschker HTS, Duineveld R, Pel R, Herman PMJ, Heip CHR (2002) Bacteria and foraminifera: key players in a short-term deep sea benthic response to phytodetritus. Mar Ecol Prog Ser 236:23–29CrossRefGoogle Scholar
  57. Nguyen HT, Dupuy C, Jourde J, Lefrançois C, Pascal PY, Carpentier A, Chevalier J, Bocher P (2018) Persistent benthic communities in the extreme dynamic intertidal mudflats of Amazonian coast: an overview of the Tanaidacea (Crustacea, Peracarida). Mar Biodiv 48:1841–1853CrossRefGoogle Scholar
  58. Nilsson P, Sundback K, Jonsson B (1993) Effect of the brown shrimp Crangon crangon on endobenthic macrofauna, meiofauna and meiofaunal grazing rates. Neth J Sea Res 31:95–106CrossRefGoogle Scholar
  59. O’Gorman EJ, Enright RA, Emmerson MC (2008) Predator diversity enhances secondary production and decrease likelihood of trophic cascades. Oecologia 158:557–567PubMedCrossRefPubMedCentralGoogle Scholar
  60. Ólafsson E (2003) Do macrofauna structure meiofauna assemblages in marine soft-bottoms? Vie Milieu 53:249–265Google Scholar
  61. Ólafsson E, Elmgren R, Papakosta O (1993) Effects of the deposit-feeding benthic bivalve Macoma balthica on meiobenthos. Oecologia 93:457–462PubMedCrossRefGoogle Scholar
  62. Pascal PY, Fleeger JW (2013) Diverse dietary responses by saltmarsh consumers to chronic nutrient enrichment. Estuar Coast 36:1115–1124CrossRefGoogle Scholar
  63. Pascal PY, Dupuy C, Haubois AG, Richard P, Niquil N (2008a) Influence of environment factors on bacterial ingestion rate of the deposit-feeder Hydrobia ulvae and comparison with meiofauna. J Sea Res 60:151–156CrossRefGoogle Scholar
  64. Pascal PY, Dupuy C, Mallet C, Richard P, Niquil N (2008b) Bacterivory by benthic organism in sediment: quantification using15N-enriched bacteria. J Exp Mar Biol Ecol 355:18–26CrossRefGoogle Scholar
  65. Pascal PY, Dupuy C, Richard P, Rzeznik-Orignac J, Niquil N (2008c) Bacterivory of a mudflat nematode community under different environmental conditions. Mar Biol 154:671–682CrossRefGoogle Scholar
  66. Pascal PY, Dupuy C, Richard P, Mallet C, Armynot du Chatelet E, Niquil N (2009) Seasonal variation in consumption of benthic bacteria by meio- and macrofauna in an intertidal mudflat. Limnol Oceanogr 54:1048–1059CrossRefGoogle Scholar
  67. Peters RH (1983) The ecological implication of body size. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  68. Pihl L, Rosenberg R (1984) Food selection and consumption of the shrimp Crangon crangon in some shallow marine areas in western Sweden. Mar Ecol Prog Ser 15:159–168CrossRefGoogle Scholar
  69. Reise K (1978) Experiments on epibenthic predation in the Wadden Sea. Helgol Wiss Meeresunters 31:55–101CrossRefGoogle Scholar
  70. Ryer CH (1987) Temporal patterns of feeding by blue crabs (Callinectes sapidus) in a tidal-marsh creek and adjacent seagrass meadow in the lower Chesapeake Bay. Estuaries 10:136–140CrossRefGoogle Scholar
  71. Scherer B, Reise K (1981) Significant predation on micro- and macrobenthos by the crab Carcinus maenas L. in the Wadden Sea Kieler Meeresforsch, pp 490–500Google Scholar
  72. Scholz DS, Matthews LL, Feller RJ (1991) Detecting selective digestion of meiobenthic prey in juvenile spot Leiostomus xanthurus (Pisces) using immunoassays. Mar Ecol Prog Ser 72:59–67CrossRefGoogle Scholar
  73. Schratzberger M, Ingels J (2018) Meiofauna matters: the role of meiofauna in benthic ecosystems. J Exp Mar Biol Ecol 502:12–25CrossRefGoogle Scholar
  74. Schratzberger M, Warwick JT (1999) Differential effects of various type of disturbances on the structure of nematode assemblages: an experimental approach. Mar Ecol Prog Ser 181:227–236CrossRefGoogle Scholar
  75. Schückel S, Sell AF, Kihara TC, Koeppen A, Kröncke I, Reiss H (2013) Meiofauna as food source for small-sized demersal fish in the southern North Sea. Helgol Mar Res 67:203–218CrossRefGoogle Scholar
  76. Schwinghamer P, Hargrave BT, Peer D, Hawkins CM (1986) Partitioning of production and respiration among size groups of organisms in an intertidal benthic community. Mar Ecol Prog Ser 31:151–166CrossRefGoogle Scholar
  77. Serrano A (2012) Changes in gut evacuation time for larval mud crab, Scylla serrata (Crustacea: Portunidae) fed artificial or live food. AACL Bioflux 5:240–248Google Scholar
  78. Shaw M, Jenkins GP (1992) Spatial variation in feeding, prey distribution and food limitation of juvenile flounder Rhombosolea tapirina Günther. J Exp Mar Biol Ecol 165:1–21CrossRefGoogle Scholar
  79. van Oevelen D, Moodley L, Soetaert K, Middelburg JJ (2006) The trophic significance of bacterial carbon in a marine intertidal sediment: results of an in situ stable isotope labeling study. Limnol Oceanogr 51:2349–2359CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Pierre-Yves Pascal
    • 1
    Email author
  • Pierrick Bocher
    • 2
  • Christel Lefrançois
    • 2
  • Hien T. Nguyen
    • 2
    • 3
  • Johan Chevalier
    • 4
  • Christine Dupuy
    • 2
  1. 1.Institut de Systématique, Evolution, Biodiversité (ISYEB) UMR 7205, Equipe Biologie de la Mangrove-Université des AntillesPointe-à-PitreFrance
  2. 2.Littoral, Environnement et Sociétés (LIENSs) UMR 7266, CNRS-La Rochelle UniversityLa RochelleFrance
  3. 3.University of Science and Technology of Hanoi (USTH)-Vietnam Academy of Science and Technology (VAST)HanoiViet Nam
  4. 4.Réserve Naturelle Nationale de l’AmanaAwala-YalimapoFrench Guiana

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