Meiofauna versus macrofauna as a food resource in a tropical intertidal mudflat
Tóm tắt
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.
Tài liệu tham khảo
Aarnio K, Bonsdorff E (1993) Seasonal variation in abundance and diet of the sand goby Pomatoschistus minutus (Pallas) in a northern Baltic Archipelago. Ophelia 37:19–30
Alheit J, Scheibel A (1982) Benthic harpacticoids as a food source for fish. Mar Biol 70:141–147
Aller RC, Aller JY (1992) Meiofauna and solute transport in marine muds. Limnol Oceanogr 37:1018–1033
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 80:207–219
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 222:219–238
Bell SS, Coull BC (1978) Field evidence that shrimp predation regulates meiofauna. Oecologia 35:141–148
Bonaglia S, Nascimento FJA, Bartoli M, Klawonn I, Brüchert V (2014) Meiofauna increases bacterial denitrification in marine sediments. Nat Commun 5:5133
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 108:55–68
Carpenter SR, Chisholm SW, Krebs CJ, Schindler DW, Wright RF (1995) Ecosystem experiments. Science 269:324–327
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 503:72–79
Coull BC (1990) Are members of the meiofauna food for higher trophic levels? Trans Am Microsc Soc 109:233–246
Coull BC (1999) Role of meiofauna in estuarine soft bottom habitats. Aust J Ecol 24:327–331
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 85:355–373
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 152:339–350
de Morais T, Bodiou JY (1984) Predation on meiofauna by juvenile fish in a Western Mediterranean flatfish nursery ground. Mar Biol 82:209–215
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 465:53–67
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–S63
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 115:41–53
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 110:39–47
Elana U (2017) Projet de parc solaire de la Sarcelle sur la commune de Mana (Guyane). SUEZ
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 120:416–426
Feller RJ (2006) Weak meiofaunal trophic linkages in Crangon crangon and Carcinus maenas. J Exp Mar Biol Ecol 330:274–283
Fitzhugh GR, Fleeger JW (1985) Goby (Pisces: Gobiidae) interactions with meiofauna and small macrofauna. Bull Mar Sci 36:436–444
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, Ames
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 357:20–34
Fry B (2006) Stable isotope ecology. Springer, New-York
Gee JM (1987) Impact of epibenthic predators on estuarine intertidal harpacticoid copepod populations. Mar Biol 96:497–510
Gee JM (1989) An ecological economic review of meiofauna as food for fish. Zool J Limn Soc 96:243–261
Gibbons MJ (1988) Impact of predation by juvenile Clinus superciliosus on phytal meiofauna: are fish important as predators? Mar Ecol Prog Ser 45:13–22
Gibson RN (2003) Go with the flow: tidal migration in marine animals. Hydrobiologia 503:153–161
Giere O (2009) Meiobenthology: the microscopic motile fauna of aquatic sediments. Springer, Berlin
Gregg CS, Fleeger JW (1998) Grass shrimp Palaemonetes pugio predation on sediment- and stem-dwelling meiofauna: field and laboratory experiments. Mar Ecol Prog Ser 175:77–86
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 2:329–335
Hall SJ, Raffaelli D, Turell WR (1990) Predator-caging experiments in marine systems: a reexamination of their value. Am Nat 136:657–672
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 44:753–771
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 191:223–238
Hindley JPR, Alexander CG (1978) Structure and function of the chelate pereiopods of the banana prawn Penaeus merquiensis. Mar Biol 48:153–160
Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398
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 248:105–119
Jonge VND, Bouwman L (1977) A simple density separation technique for quantitative isolation of meiobenthos using the colloidal silica Ludox TM. Mar Biol 42:143–148
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 40:1159–1170
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 52:319–324
Kneib RT (1985) Predation and disturbance by grass shrimp, Palaemonaetes pugio, Holthuis, in soft-substratum invertebrate benthic assemblages. J Exp Mar Biol Ecol 93:91–102
Kovačić M, la Mesa M (2008) Feeding ecology of De Buen’s goby Buenia affinis, in the Kvarner area (Adriatic Sea). Vie Milieu 58:249–256
Krebs JR (1978) Optimal foraging: decision rules for predators. In: Krebs JR, Davies NB (eds) Behavioural ecology, an evolutionary approach. Blackwell, Oxford
Leduc D, Probert PK, Duncan A (2009) A multi-method approach for identifying meiofaunal trophic connections. Mar Ecol Prog Ser 383:95–111
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:e12495
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 70:23–31
Li J, Vincx M, Herman PMJ (1996) A model of nematode dynamics in the Westerschelde Estuary. Ecol Model 90:271–284
Lipcius RN, Hines AH (1986) Variable functional responses of a marine predator in dissimilar homogeneous microhabitats. Ecology 67:1361–1371
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:e00100
McCall JN, Fleeger JW (1995) Predation by juvenile fish on hyperbenthic meiofauna: a review with data on post-larval Leiostomus xanthurus. Vie Milieu 45:61–73
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 45:1224–1234
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 234:127–137
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 109–152
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 236:23–29
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 48:1841–1853
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 31:95–106
O’Gorman EJ, Enright RA, Emmerson MC (2008) Predator diversity enhances secondary production and decrease likelihood of trophic cascades. Oecologia 158:557–567
Ólafsson E (2003) Do macrofauna structure meiofauna assemblages in marine soft-bottoms? Vie Milieu 53:249–265
Ólafsson E, Elmgren R, Papakosta O (1993) Effects of the deposit-feeding benthic bivalve Macoma balthica on meiobenthos. Oecologia 93:457–462
Pascal PY, Fleeger JW (2013) Diverse dietary responses by saltmarsh consumers to chronic nutrient enrichment. Estuar Coast 36:1115–1124
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 60:151–156
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 355:18–26
Pascal PY, Dupuy C, Richard P, Rzeznik-Orignac J, Niquil N (2008c) Bacterivory of a mudflat nematode community under different environmental conditions. Mar Biol 154:671–682
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 54:1048–1059
Peters RH (1983) The ecological implication of body size. Cambridge University Press, Cambridge
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 15:159–168
Reise K (1978) Experiments on epibenthic predation in the Wadden Sea. Helgol Wiss Meeresunters 31:55–101
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 10:136–140
Scherer B, Reise K (1981) Significant predation on micro- and macrobenthos by the crab Carcinus maenas L. in the Wadden Sea Kieler Meeresforsch, pp 490–500
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 72:59–67
Schratzberger M, Ingels J (2018) Meiofauna matters: the role of meiofauna in benthic ecosystems. J Exp Mar Biol Ecol 502:12–25
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 181:227–236
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 67:203–218
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 31:151–166
Serrano A (2012) Changes in gut evacuation time for larval mud crab, Scylla serrata (Crustacea: Portunidae) fed artificial or live food. AACL Bioflux 5:240–248
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 165:1–21
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 51:2349–2359