Abstract
Meiofaunal organisms are diverse, and so is their diet comprising bacteria, fungi, micro-algae, flagellates, ciliates, and other meiofauna. Studies have inferred diet from correlative evidences, observations of feeding or gut contents. Incubation experiments have also helped to link meiofauna’s role to microbially mediated ecosystem processes, reporting in most cases beneficial effects on microbial activity. Nevertheless, our knowledge of meiofauna’s trophic ecology still lags far behind that of other aquatic fauna (i.e. zooplankton, macroinvertebrates, vertebrates), probably because the small-size and the cryptic nature of the meiofauna becomes an issue when it comes to detect their isotopic or lipid composition. Here, we provide a critical review of diverse methodologies used while examining meiofaunal diets. Observation of feeding, incubation experiments, gut content analyses, calorimetry, stable isotopic and fatty acid analyses are very helpful and some modifications of standard materials and methods can help reduce the time-consuming sorting of individuals. Other analytic tools used by microbial ecologists like compound-specific stable isotopic analysis, DNA-stable isotopic probing, confocal laser scanning microscopy, coherent anti-stokes Raman spectrometry and nanoscale secondary ion mass spectrometry have the potential to unravel hidden trophic channels between meiofauna and microbes.
Similar content being viewed by others
References
Akoto, L., F. Stellaard, H. Irth, R. J. J. Vreuls & R. Pel, 2008. Improved fatty acid detection in micro-algae and aquatic meiofauna species using direct thermal desorption interface combined with comprehensive gas chromatography-time-of-flight mass spectrometry. Journal of Chromatography A 1186: 254–261.
Arts, M. T., M. T. Brett & M. Kainz, 2009. Lipids in Aquatic Ecosystems. Springer, New York.
Bec, A., M.-E. Perga, A. Koussoroplis, G. Bardoux, C. Desvilettes, G. Bourdier & A. Mariotti, 2011. Assessing the reliability of fatty acid–specific stable isotope analysis for trophic studies. Methods in Ecology and Evolution 2: 651–659.
Bell, M. V. & D. R. Tocher, 2009. Biosynthesis of Polyunsaturated Fatty Acids in Aquatic Ecosystems: General Pathways and New Directions Lipids in Aquatic Ecosystems. Springer, New York: 211–236.
Bell, S. S., 1988. Experimental techniques. In Higgins, R. P. & H. Thiel (eds), Introduction to the Study of Meiofauna. Smithsonian Institution Press, Washington, DC: 169–180.
Bergtold, M., V. Gunther & W. Traunspurger, 2005. Is there competition among ciliates and nematodes? Freshwater Biology 50: 1351–1359.
Bonaglia, S., F. J. A. Nascimento & M. Bartoli, 2014. Meiofauna increases bacterial denitrification in marine sediments. Nature Communications 5: 5133.
Borchardt, M. A. & T. L. Bott, 1995. Meiofaunal grazing of bacteria and algae in a Piedmont stream. Journal of the North American Benthological Society 14: 278–298.
Boschker, H. T. S., W. De Graaf, M. Köster, L.-A. Meyer-Reil & T. E. Cappenberg, 2001. Bacterial populations and processes involved in acetate and propionate consumption in anoxic brackish sediment. FEMS Microbiology Ecology 35: 97–103.
Braeckman, U., P. Provoost, K. Sabbe, K. Soetaert, J. J. Middelburg, M. Vincx & J. Vanaverbeke, 2015. Temporal dynamics in a shallow coastal benthic food web: insights from fatty acid biomarkers and their stable isotopes. Marine Environmental Research 108: 55–68.
Braeckman, U., F. Janssen, G. Lavik, M. Elvert, H. Marchant, C. Buckner, C. Bienhold & F. Wenzhöfer, 2018. Carbon and nitrogen turnover in the Arctic deep sea: in situ benthic community response to diatom and coccolithophorid phytodetritus. Biogeosciences 15: 6537–6557.
Buffan-Dubau, E. & K. R. Carman, 2000. Diel feeding behavior of meiofauna and their relationships with microalgal resources. Limnology and Oceanography 45: 381–395.
Buffan-Dubau, E., R. de Wit & J. Castel, 1996. Feeding selectivity of the harpacticoid copepod Canuella perplexa in benthic muddy environments demonstrated by HPLC analyses of chlorin and carotenoid pigments. Marine Ecology Progress Series 137: 71–82.
Burnett, C. M. L. & J. L. Grobe, 2013. Direct calorimetry identifies deficiencies in respirometry for the determination of resting metabolic rate in C57Bl/6 and FVB mice. American Journal of Physiology 305: 916–924.
Caramujo, M. J., H. T. Boschker & W. Admiraal, 2008. Fatty acid profiles of algae mark the development and composition of harpacticoid copepods. Freshwater Biology 53: 77.
Carman, K. R. & B. Fry, 2002. Small-sample methods for δ13C and δ15 N analysis of the diets of marsh meiofaunal species using natural-abundance and tracer-addition isotope techniques. Marine Ecology Progress Series 240: 85–92.
Cnudde, C., A. Willems, K. Van Hoorde, W. Vyverman, T. Moens & M. De Troch, 2011. Effect of food preservation on the grazing behavior and on the gut flora of the harpacticoid copepod Paramphiascella fulvofasciata. Journal of Experimental Marine Biology and Ecology 407: 63–69.
Cnudde, C., T. Moens, E. Werbrouck, G. Lepoint, D. Van Gansbeke & M. De Troch, 2015. Trophodynamics of estuarine intertidal harpacticoid copepods based on stable isotope composition and fatty acid profiles. Marine Ecology Progress Series 524: 225–239.
Crotty, F. V., S. M. Adl, R. P. Blackshaw & P. J. Murray, 2012. Using stable isotopes to differentiate trophic feeding channels within soil food webs. Journal of Eukaryotic Microbiology 59: 520–526.
Degen, R. & S. Faulwetter, 2019. The arctic traits database—a repository of arctic benthic invertebrate traits. Earth System Science Data 11: 301–322.
De Mesel, I., S. Derycke, T. Moens, K. Van der Gucht, M. Vincx & J. Swings, 2004. Top-down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environmental Microbiology 6: 733–744.
De Mesel, I., S. Derycke, J. Swings, M. Vincx & T. Moens, 2006. Role of nematodes in decomposition processes: does within-trophic group diversity matter? Marine Ecology Progress Series 321: 157–166.
De Troch, M., M. B. Steinarsdottir, V. Chepurnov & E. Olafsson, 2005. Grazing on diatoms by harpacticoid copepods: species-specific density-dependent uptake and microbial gardening. Aquatic Microbial Ecology 39: 135–144.
De Troch, M., C. Cnudde, A. Willems, T. Moens & A. Vanreusel, 2010. Bacterial colonization on fecal pellets of harpacticoid copepods and on their diatom food. Microbial Ecology 60: 581–591.
Deines, P., P. L. Bodelier & G. Eller, 2007a. Methane-derived carbon flows through methane-oxidizing bacteria to higher trophic levels in aquatic systems. Environmental Microbiology 9: 1126–1134.
Deines, P., J. Grey, H.-H. Richnow & G. Eller, 2007b. Linking larval chironomids to methane: seasonal variation of the microbial methane cycle and chironomid δ13C. Aquatic Microbial Ecology 46: 273–282.
Derycke, S., N. De Meester, A. Rigaux, S. Creer, H. Bik, W. K. Thomas & T. Moens, 2016. Coexisting cryptic species of the Litoditis marina complex (Nematoda) show differential resource use and have distinct microbiomes with high intraspecific variability. Molecular Ecology 25: 2093–2110.
D’Hondt, A.-S., W. Stock, L. Blommaert, T. Moens & K. Sabbe, 2018. Nematodes stimulate biomass accumulation in a multispecies diatom biofilm. Marine Environmental Research 140: 78–89.
Doohan, M., 1973. An energy budget for adult Brachionus plicatilis Muller (Rotatoria). Oecologia 13: 351–362.
dos Santos, G. A., S. Derycke, V. G. Genevois, L. C. Coelho, M. T. Correia & T. Moens, 2009. Interactions among bacterial-feeding nematode species at different levels of food availability. Marine Biology 156: 629–640.
Duncan, A., & R. Z. Klekowski, 1975. Parameters of an energy budget. In Grodziński, W., Klekowski, R. Z., & A. Duncan (eds), Methods for Ecological Bioenergetics. IBP Handbook 24, Blackwell Scientific Publishing, Oxford, UK: 97–147.
Duncan, A., F. Schiemer & R. Z. Klekowski, 1974. A preliminary study of feeding rates on bacterial food by adult females of a benthic nematode, Plectus palustris De Man 1880. Polish Archives of Hydrobiology 21: 249–255.
Elton, C. S., 1927. Animal Ecology. The Macmillan Company, London.
Esser, M., 2006. Long-term dynamics of microbial biofilm communities of the river Rhine. PhD Thesis, Universität zu Köln, Germany.
Estifanos, T. K., W. Traunspurger & L. Peters, 2013. Selective feeding in nematodes: a stable isotope analysis of bacteria and algae as food sources for free-living nematodes. Nematology 15: 1–13.
Fonseca, G., D. Fontaneto & M. Di Domenico, 2018. Adressing biodiversity shortfalls in meiofauna. Journal of Experimental Marine Biology and Ecology 502: 26–38.
Fontaneto, D., A. M. Barbosa, H. Segers & M. Pautasso, 2012. The ‘rotiferologist’ effect and other global correlates of species richness in monogonont rotifers. Ecography 35: 174–182.
Fueser, H., N. Majdi, A. Haegerbaeumer, C. Pilger, H. Hachmeister, P. Greife, T. Huser & W. Traunspurger, 2018. Analyzing life-history traits and lipid storage using CARS microscopy for assessing effects of copper on the fitness of Caenorhabditis elegans. Ecotoxicology and Environmental Safety 156: 255–262.
Gansfort, B., J. Uthoff & W. Traunspurger, 2018. Interactions among competing nematode species affect population growth rates. Oecologia 187: 75–84.
Garvey, J. E. & M. R. Whiles, 2017. Trophic Ecology. CRC Press, Boca Raton.
Gaudes, A., I. Muñoz & T. Moens, 2013. Bottom-up effects on freshwater bacterivorous nematode populations: a microcosm approach. Hydrobiologia 707: 159–172.
Gaudes, A., S. Sabater, E. Vilalta & I. Muñoz, 2006. The nematode community in cyanobacterial biofilms in the river Llobregat, Spain. Nematology 8: 909–919.
Giere, O., 2019. Future trend lines in ecological meiobenthos research. In Giere, O. (ed.), Perspectives in Meiobenthology. Springer, New York: 37–49.
Gingold, R., T. Moens & A. Rocha-Olivares, 2013. Assessing the response of nematode communities to climate change-driven warming: a microcosm experiment. PLoS ONE 8: e66653.
Goldfinch, A. C. & K. R. Carman, 2000. Chironomid grazing on benthic microalgae in a Louisiana salt marsh. Estuaries 23: 536–547.
Gravel, D., C. Albouy & W. Thuiller, 2016. The meaning of functional trait composition of food webs for ecosystem functioning. Philosophical Transactions of the Royal Society B: Biological Sciences 371: 20150268.
Guénard, G., P. Legendre & P. Peres-Neto, 2013. Phylogenetic eigenvector maps: a framework to model and predict species traits. Methods in Ecology and Evolution 4: 1120–1131.
Guilini, K., G. Veit-Koehler, M. De Troch, D. Van Gansbeke & A. Vanreusel, 2013. Latitudinal and temporal variability in the community structure and fatty acid composition of deep-sea nematodes in the Southern Ocean. Progress in Oceanography 110: 80–92.
Hägerbäumer, A., S. Höss, P. Heininger & W. Traunspurger, 2015. Experimental studies with nematodes in ecotoxicology: an overview. Journal of Nematology 47: 1–11.
Heidemann, K., S. Scheu, L. Ruess & M. Maraun, 2011. Molecular detection of nematode predation and scavenging in oribatid mites: laboratory and field experiments. Soil Biology and Biochemistry 43: 2229–2236.
Herman, P. M. J. & G. Vranken, 1988. Studies of the life-history and energetics of marine and brackish-water nematodes. II. Production, respiration and food uptake by Monhystera disjuncta. Oecologia 77: 457–463.
Höckelmann, C., T. Moens & F. Jüttner, 2004. Odor compounds from cyanobacterial biofilms acting as attractants and repellents for free-living nematodes. Limnology and Oceanography 49: 1809–1819.
Hohberg, K. & W. Traunspurger, 2005. Predator-prey interaction in soil food web: functional response, size-dependent foraging efficiency, and the influence of soil texture. Biology and Fertility of Soils 41: 419–427.
Hordijk, C. A., I. Burgers, G. J. Phylipsen & T. E. Cappenberg, 1990. Trace determination of lower volatile fatty acids in sediments by gas chromatography with chemically bonded FFAP columns. Journal of Chromatography A 511: 317–323.
Hortal, J., F. de Bello, J. A. F. Diniz-Filho, T. M. Lewinsohn, J. M. Lobo & R. J. Ladle, 2015. Seven shortfalls that beset large-scale knowledge of biodiversity. Annual Reviews of Ecology Evolution and Systematics 46: 523–549.
Hubas, C., C. Sachidhanandam, H. Rybarczyk, H. V. Lubarsky, A. Rigaux, T. Moens & D. M. Paterson, 2010. Bacterivorous nematodes stimulate microbial growth and exopolymer production in marine sediment microcosms. Marine Ecology Progress Series 419: 85–94.
Jakob, E. M., S. D. Marshall & G. W. Uetz, 1996. Estimating fitness: a comparison of body condition indices. Oikos 77: 61–67.
Jardim, L., L. M. Bini, J. A. F. Diniz-Filho & F. Villalobos, 2016. Challenging the Raunkiaeran shortfall and the consequences of using imputed databases. BioRxiv. https://doi.org/10.1101/081778.
Jehmlich, N., C. Vogt, V. Lünsmann, H. H. Richnow & M. von Bergen, 2016. Protein-SIP in environmental studies. Current Opinion in Biotechnology 41: 26–33.
Johnson, S. N., D. B. Read & P. J. Gregory, 2004. Tracking larval insect movement within soil using high resolution X-ray microtomography. Ecological Entomology 29: 117–122.
Kathol, M., H. Norf, H. Arndt & M. Weitere, 2009. Effects of temperature increase on the grazing of planktonic bacteria by biofilm-dwelling consumers. Aquatic Microbial Ecology 55: 65–79.
Kazemi-Dinan, A., F. Schroeder, L. Peters, N. Majdi & W. Traunspurger, 2014. The effect of trophic state and depth on periphytic nematode communities in lakes. Limnologica 44: 49–57.
King, R. A., D. S. Read, M. Traugott & W. O. C. Symondson, 2008. Molecular analysis of predation: a review of best practice for DNA-based approaches. Molecular Ecology 17: 947–963.
Kohzu, A., C. Kato, T. Iwata, D. Kishi, M. Murakami, S. Nakano & E. Wada, 2004. Stream food web fueled by methane-derived carbon. Aquatic Microbial Ecology 36: 189–194.
Kreuzinger-Janik, B., S. Kruscha, N. Majdi & W. Traunspurger, 2018. Flatworms like it round: nematode consumption by Planaria torva (Müller 1774) and Polycelis tenuis (Iijima 1884). Hydrobiologia 819: 231–242.
Kreuzinger-Janik, B., H. Brüchner-Hüttemann & W. Traunspurger, 2019. Effect of prey size and structural complexity on the functional response in a nematode-nematode system. Scientific Reports 9: 5696.
Kydd, J., H. Rajakaruna, E. Briski & S. Bailey, 2018. Examination of a high resolution laser optical plankton counter and FlowCAM for measuring plankton concentration and size. Journal of Sea Research 133: 2–10.
Langel, R. & J. Dyckmans, 2014. Combined 13C and 15 N isotope analysis on small samples using a near-conventional elemental analyzer/isotope ratio mass spectrometer setup. Rapid Communications in Mass Spectrometry 28: 1019–1022.
Leduc, D. & P. K. Probert, 2009. The effect of bacterivorous nematodes on detritus in- corporation by macrofaunal detritivores: a study using stable isotope and fatty acid analyses. Journal of Experimental Marine Biology and Ecology 371: 130–139.
Liu, Y., N. Majdi, M. Tackx, A. Dauta, M. Gérino, F. Julien & E. Buffan-Dubau, 2015. Short-term effects of nutrient enrichment on river biofilm: NO3- uptake rate and response of meiofauna. Hydrobiologia 744: 165–175.
Liu, Y., K. Dedieu, J.-M. Sánchez-Pérez, B. Montuelle, E. Buffan-Dubau, F. Julien, F. Azémar, S. Sauvage, P. Marmonier & J. Yao, 2017. Role of biodiversity in the biogeochemical processes at the water-sediment interface of macroporous river bed: an experimental approach. Ecological Engineering 103: 385–393.
Lubzens, E., A. Marko & A. Tietz, 1985. De novo synthesis of fatty acids in the rotifer, Brachionus plicatilis. Aquaculture 47: 27–37.
Lucas, A. & J. J. Watson, 2002. Bioenergetics of aquatic animals. CRC Press, Boca Raton: 169.
Lueders, T., B. Wagner, P. Claus & M. W. Friedrich, 2004. Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environmental Microbiology 6: 60–72.
Lueders, T., M. G. Dumont, L. Bradford & M. Manefield, 2016. RNA-stable isotope probing: from carbon flow within key microbiota to targeted transcriptomes. Current Opinion in Biotechnology 41: 83–89.
Maghsoud, H., A. Weiss, J. P. S. Smith, M. K. Litvaitis & S. R. Fegley, 2014. Diagnostic PCR can be used to illuminate meiofaunal diets and trophic relationships. Invertebrate Biology 133: 121–127.
Maboreke, H., V. Bartel, R. Seiml-Buchinger & L. Ruess, 2018. Micro-food web structure shapes rhizosphere microbial communities and growth in Oak. Diversity 10: 15.
Majdi, N. & W. Traunspurger, 2015. Free-living nematodes in the freshwater food web: a review. Journal of Nematology 47: 28–44.
Majdi, N. & W. Traunspurger, 2017. Leaf fall affects the isotopic niches of meiofauna and macrofauna in a stream food web. Food Webs 10: 5–14.
Majdi, N., B. Mialet, S. Boyer, M. Tackx, J. Leflaive, S. Boulêtreau, L. Ten-Hage, F. Julien, R. Fernandez & E. Buffan-Dubau, 2012a. The relationship between epilithic biofilm stability and its associated meiofauna under two patterns of flood disturbance. Freshwater Science 31: 38–50.
Majdi, N., M. Tackx & E. Buffan-Dubau, 2012b. Trophic positionning and microphytobenthic carbon uptake of biofilm-dwelling meiofauna in a temperate river. Freshwater Biology 57: 1180–1190.
Majdi, N., M. Tackx, W. Traunspurger & E. Buffan-Dubau, 2012c. Feeding of biofilm-dwelling nematodes examined using HPLC-analysis of gut pigment contents. Hydrobiologia 680: 219–232.
Majdi, N., I. Threis & W. Traunspurger, 2016. It’s the little things that count: meiofaunal density and production in the sediment of two headwater streams: Meiofauna in Streams. Limnology and Oceanography 62: 151–163.
Majdi, N., N. Hette-Tronquart, E. Auclair, A. Bec, T. Chouvelon, B. Cognie, M. Danger, P. Decottignies, A. Dessier, C. Desvilettes, S. Dubois, C. Dupuy, C. Fritsch, C. Gaucherel, M. Hedde, F. Jabot, S. Lefebvre, M. P. Marzloff, B. Pey, N. Peyrard, T. Powolny, R. Sabbadin, E. Thébault & M.-E. Perga, 2018. There’s no harm in having too much: a comprehensive toolbox of methods in trophic ecology. Food Webs 17: e00100.
Majdi, N., W. Traunspurger, H. Fueser, B. Gansfort, P. Laffaille & A. Maire, 2019. Effects of a broad range of experimental temperatures on the population growth and body-size of five species of free-living nematodes. Journal of Thermal Biology 80: 21–36.
Malte, C. L., S. Nørgaard & T. Wang, 2016. Closed system respirometry may underestimate tissue gas exchange and bias the respiratory exchange ratio (RER). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 192: 17–27.
Mathieu, M., J. Leflaive, L. Ten-Hage, R. de Wit & E. Buffan-Dubau, 2007. Free-living nematodes affect oxygen turnover of artificial diatom biofilms. Aquatic Microbial Ecology 49: 281–291.
Melody, C., B. Griffiths, J. Dyckmans & O. Schmidt, 2016. Stable isotope analysis (δ13C and δ15 N) of soil nematodes from four feeding groups. PeerJ 4: e2372.
Mialet, B., N. Majdi, M. Tackx, F. Azémar & E. Buffan-Dubau, 2013. Selective feeding of Bdelloid rotifers in river biofilms. PLoS One 8: e75352.
Middelburg, J. J., C. Barranguet, H. T. S. Boschker, P. M. J. Herman, T. Moens & C. H. R. Heip, 2000. The fate of intertidal microphytobenthos carbon: an in situ 13C-labeling study. Limnology and Oceanography 45: 1224–1234.
Moens, T. & M. Vincx, 1997. Observations on the feeding ecology of estuarine nematodes. Journal of the Marine Biological Association of the UK 77: 211–227.
Moens, T., G. A. P. dos Santos, F. Thompson, J. Swings, V. Fonsêca-Genevois, M. Vincx & I. De Mesel, 2005. Do nematode mucus secretions affect bacterial growth? Aquatic Microbial Ecology 40: 77–83.
Moens, T., A.-M. Vafeiadou, E. De Geyter, P. Vanormelingen, K. Sabbe & M. De Troch, 2013. Diatom feeding across trophic guilds in tidal flat nematodes, and the importance of diatom cell size. Journal of Sea Research 92: 125–133.
Mohr, S. & R. Adrian, 2000. Functional responses of the rotifers Brachionus calyciflorus and Brachionus rubens feeding on armored and unarmored ciliates. Limnology and Oceanography 45: 1175–1179.
Musat, N., F. Musat, P. K. Weber & J. Pett-Ridge, 2016. Tracking microbial interactions with NanoSIMS. Current Opinion in Biotechnology 41: 114–121.
Muschiol, D. & W. Traunspurger, 2007. Life cycle and calculation of the intrinsic rate of natural increase of two bacterivorous nematodes, Panagrolaimus sp and Poikilolaimus sp from chemoautotrophic Movile Cave, Romania. Nematology 9: 271–284.
Muschiol, D., M. Markovic, I. Threis & W. Traunspurger, 2008. Predatory copepods can control nematode populations: a functional-response experiment with Eucyclops subterraneus and bacterivorous nematodes. Fundamental and Applied Limnology 172: 317–324.
Nascimento, F. J. A., J. Näslund & R. Elmgren, 2012. Meiofauna enhances organic matter mineralization in soft sediment ecosystems. Limnology and Oceanography 57: 338–346.
Nejstgaard, J. C., M. E. Frischer, C. L. Raule, R. Gruebel, K. E. Kohlberg & P. G. Verity, 2003. Molecular detection of algal prey in copepod guts and fecal pellets. Limnology and Oceanography: Methods 1: 29–38.
Nejstgaard, J. C., M. E. Frischer, P. Simonelli, C. Troedsson, M. Brakel, F. Adiyaman, A. F. Sazhin & L. F. Artigas, 2008. Quantitative PCR to estimate copepod feeding. Marine Biology 153: 565–577.
Neu, T. R. & J. R. Lawrence, 2015. Innovative techniques, sensors, and approaches for imaging biofilms at different scales. Trends in Microbiology 23: 233–242.
Neufeld, J. D., M. Wagner & J. C. Murrell, 2007. Who eats what, where and when? Isotope-labelling experiments are coming of age. The ISME Journal 1: 103.
Neury-Ormanni, J., J. Vedrenne, M. Wagner, G. Jan & S. Morin, 2019. Micro-meiofauna morphofunctional traits linked to trophic activity. Hydrobiologia. https://doi.org/10.1007/s10750-019-04120-0.
Pausch, J., S. Hofmann, A. Scharroba, Y. Kuzyakov & L. Ruess, 2016. Fluxes of root-derived carbon into the nematode micro-food web of an arable soil. Food Webs 9: 32–38.
Perlmutter, D. G. & J. L. Meyer, 1991. The impact of a stream-dwelling harpacticoid copepod upon detritally associated bacteria. Ecology 72: 2170–2180.
Peters, L. & W. Traunspurger, 2005. Species distribution of free-living nematodes and other meiofauna in littoral periphyton communities of lakes. Nematology 7: 267–280.
Peters, L., H. Hillebrand & W. Traunspurger, 2007. Spatial variation of grazer effects on epilithic meiofauna and algae. Journal of the North American Benthological Society 26: 78–91.
Ptatscheck, C., B. Kreuzinger-Janik, H. Putzki & W. Traunspurger, 2015. Insights into the importance of nematode prey for chironomid larvae. Hydrobiologia 757: 143–153.
Ptatscheck, C., H. Putzki & W. Traunspurger, 2017. Impact of deposit-feeding chironomid larvae (Chironomus riparius) on meiofauna and protozoans. Freshwater Science 36: 796–804.
Radajewski, S., P. Ineson, N. R. Parekh & J. C. Murrell, 2000. Stable-isotope probing as a tool in microbial ecology. Nature 403: 646.
Raubenheimer, D., S. J. Simpson & D. Mayntz, 2009. Nutrition, ecology and nutritional ecology: toward an integrated framework. Functional Ecology 23: 4–16.
Reiss, J. & J. M. Schmid-Araya, 2008. Existing in plenty: abundance, biomass and diversity of ciliates and meiofauna in small streams. Freshwater Biology 53: 652–658.
Reiss, J. & J. M. Schmid-Araya, 2011. Feeding response of a benthic copepod to ciliate prey type, prey concentration and habitat complexity. Freshwater Biology 56: 1519–1530.
Riemann, F. & E. Helmke, 2002. Symbiotic relations of sediment-agglutinating nematodes and bacteria in detrital habitats: the enzyme-sharing concept. Marine Ecology 23: 93–113.
Ristau, K., M. Faupel & W. Traunspurger, 2012. The effects of nutrient enrichment on a freshwater meiofaunal assemblage. Freshwater Biology 57: 824–834.
Ristau, K., N. Spann & W. Traunspurger, 2015. Species and trait compositions of freshwater nematodes as indicative descriptors of lake eutrophication. Ecological Indicators 53: 196–205.
Robertson, J. R. & G. W. Salt, 1981. Responses in growth mortality, and reproduction to variable food levels by the rotifer, Asplanchna girodi. Ecology 62: 1585–1596.
Rossel, S. & P. Martínez Arbizu, 2018. Automatic specimen identification of Harpacticoids (Crustacea:Copepoda) using Random Forest and MALDI-TOF mass spectra, including a post hoc test for false positive discovery. Methods in Ecology and Evolution 9: 1421–1434.
Rossel, S. & P. Martínez Arbizu, 2019. Revealing higher than expected diversity of Harpacticoida (Crustacea:Copepoda) in the North Sea using MALDI-TOF MS and molecular barcoding. Scientific Reports 9: 9182.
Rothstein, M. & P. Götz, 1968. Biosynthesis of fatty acids in the free-living nematode, Turbatrix aceti. Archives of Biochemistry and Biophysics 126: 131–140.
Rubin, D., 1976. Inference and missing data. Biometrika 63: 581–592.
Ruiz, T., A. Bec, M. Danger, A.-M. Koussoroplis, J.-P. Aguer, J.-P. Morel & N. Morel-Desrosiers, 2018. A microcalorimetric approach for investigating stoichiometric constraints on the standard metabolic rate of a small invertebrate. Ecology Letters 21: 1714–1722.
Rzeznik-Orignac, J., A. Puisay, E. Derelle, E. Peru, N. Le Bris & P. E. Galand, 2018. Co-occurring nematodes and bacteria in submarine canyon sediments. PeerJ 6: e5396.
Schenck, J. & D. Fontaneto, 2019. Biodiversity analyses in freshwater meiofauna through DNA sequence data. Hydrobiologia. https://doi.org/10.1007/s10750-019-04067-2.
Schiemer, F., 1982. Food dependence and energetics of freeliving Nematodes. Oecologia 54: 108–121.
Schiemer, F. & A. Duncan, 1974. The oxygen consumption of a freshwater benthic nematode, Tobrilus gracilis (Bastian). Oecologia 15: 121–126.
Schiemer, F., A. Duncan & R. Z. Klekowski, 1980. A bioenergetic study of a benthic nematode, Plectus palustris de Man 1880, throughout its life cycle. Oecologia 44: 205–212.
Schmid, P. E. & J. M. Schmid-Araya, 1997. Predation on meiobenthic assemblages: resource use of a tanypod guild (Chironomidae, Diptera) in a gravel stream. Freshwater Biology 38: 67–91.
Schmid, P. E. & J. M. Schmid-Araya, 2002. Trophic relationships in temporary and permanent freshwater meiofauna. In Rundle, S. D., A. L. Robertson & J. M. Schmid-Araya (eds), Freshwater meiofauna biology and ecology. Backhuys Publishers, Leiden: 295–320.
Schmid-Araya, J. M. & P. E. Schmid, 1995. Preliminary results on diet of stream invertebrate species: the meiofaunal assemblages. Jahresbericht der Biologischen Station Lunz 15: 23–31.
Schmid-Araya, J. M., A. G. Hildrew, A. Robertson, P. E. Schmid & J. Winterbottom, 2002a. The importance of meiofauna in food webs: evidence from an acid stream. Ecology 83: 1271–1285.
Schmid-Araya, J. M., P. E. Schmid, A. Robertson, J. Winterbottom, C. Gjerløv & A. G. Hildrew, 2002b. Connectance in stream food webs. Journal of Animal Ecology 71: 1056–1062.
Schmid-Araya, J. M., P. E. Schmid, S. P. Tod & G. F. Esteban, 2016. Trophic positioning of meiofauna revealed by stable isotopes and food web analyses. Ecology 97: 3099–3109.
Schroeder, F., D. Muschiol & W. Traunspurger, 2010. Fluctuating food availability may permit coexistence in bacterivorous nematodes. Fundamental and Applied Limnology 178: 59–66.
Schroeder, F., W. Traunspurger, K. Pettersson & L. Peters, 2012. Temporal changes in periphytic meiofauna in lakes of different trophic states. Journal of Limnology 71: 216–227.
Sieriebriennikov, B., H. Ferris & R. G. de Goede, 2014. NINJA: an automated calculation system for nematode-based biological monitoring. European Journal of Soil Biology 61: 90–93.
Taylor, W. D., 1980. Observations on the feeding and growth of the predacious oligochaete Chaetogaster langi on ciliated protozoa. Transactions of the American Microscopical Society 99: 360–368.
Traunspurger, W., 1997. Bathymetric, seasonal and vertical distribution of feeding-types of nematodes in an oligotrophic lake. Vie et Milieu 47: 1–7.
Traunspurger, W., M. Bergtold & W. Goedkoop, 1997. The effects of nematodes on bacterial activity and abundance in a freshwater sediment. Oecologia 112: 118–122.
Traunspurger, W., S. Höss, A. Witthöft-Mühlmann, M. Wessels & H. Güde, 2012. Meiobenthic community patterns of oligotrophic and deep Lake Constance in relation to water depth and nutrients. Fundamental and Applied Limnology 180: 233–248.
Traunspurger, W., B. Wilden & N. Majdi, 2019. An overview of meiofaunal and nematode distribution in lake ecosystems differing in their trophic state. Hydrobiologia. https://doi.org/10.1007/s10750-019-04092-1.
Vafeiadou, A.-M., P. Materatski, H. Adão, M. De Troch & T. Moens, 2014. Resource utilization and trophic position of nematodes and harpacticoid copepods in and adjacent to Zostera noltii beds. Biogeosciences 11: 4001–4014.
Van Gaever, S., L. Moodley, F. Pasotti, M. Houtekamer, J. J. Middelburg, R. Danovaro & A. Vanreusel, 2009. Trophic specialisation of metazoan meiofauna at the Håkon Mosby Mud Volcano: fatty acid biomarker isotope evidence. Marine Biology 156: 1289–1296.
Van Oevelen, D., L. Moodley, K. Soetaert & J. J. Middelburg, 2006. The trophic significance of bacterial carbon in a marine intertidal sediment: results of an in situ stable isotope labeling study. Limnology and Oceanography 51: 2349–2359.
Vecchi, M., I. L. Newton, M. Cesari, L. Rebecchi & R. Guidetti, 2018. The microbial community of tardigrades: environmental influence and species specificity of microbiome structure and composition. Microbial Ecology 76: 467–481.
Vestheim, H., B. Edvardsen & S. Kaartvedt, 2005. Assessing feeding of a carnivorous copepod using species-specific PCR. Marine Biology 147: 381–385.
Vidakovic, J., G. Palijan & D. Cerba, 2011. Relationship between nematode community and biomass and composition of periphyton developing on artificial substrates in floodplain lake. Polish Journal of Ecology 59: 577–588.
Volland, J.-M., A. Schintlmeister, H. Zambalos, S. Reipert, P. Mozetič, S. Espada-Hinojosa, V. Turk, M. Wagner & M. Bright, 2018. NanoSIMS and tissue autoradiography reveal symbiont carbon fixation and organic carbon transfer to giant ciliate host. The ISME Journal 12: 714.
Walsberg, G. E. & T. C. Hoffman, 2005. Direct calorimetry reveals large errors in respirometric estimates of energy expenditure. Journal of Experimental Biology 208: 1035–1043.
Watts, J. L. & J. Browse, 1999. Isolation and characterization of a Δ5-fatty acid desaturase from caenorhabditis elegans. Archives of Biochemistry and Biophysics 362: 175–182.
Weber, S. & W. Traunspurger, 2013. Food choice of two bacteria-feeding nematode species dependent on food source, food density and interspecific competition. Nematology 15: 291–301.
Wegener, G., M. Y. Kellermann & M. Elvert, 2016. Tracking activity and function of microorganisms by stable isotope probing of membrane lipids. Current Opinion in Biotechnology 41: 43–52.
Weitere, M., M. Erken, N. Majdi, H. Arndt, H. Norf, M. Reinshagen, W. Traunspurger, A. Walterscheid & J. K. Wey, 2018. The food web perspective on aquatic biofilms. Ecological Monographs 88: 543–559.
Wieser, W., 1953. Die Beziehung zwischen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden marinen Nernatode. Arkiv für Zoologie 439–484.
Wilden, B., N. Majdi, U. Kuhlicke, T. R. Neu & W. Traunspurger, 2019. Flatworm mucus as the base of a food web. BMC Ecology 19: 15.
Witte, U., F. Wenzhöfer, S. Sommer, A. Boetius, P. Heinz, N. Aberle, M. Sand, A. Cremer, W.-R. Abraham, B. B. Jørgensen & O. Pfannkuche, 2003. In situ experimental evidence of the fate of a phytodetritus pulse at the abyssal sea floor. Nature 424: 763–766.
Wu, X., T. Campinas Bezerra, D. Van Gansbeke & T. Moens, 2019. Natural stable isotope ratios and fatty acid profiles of estuarine tidal flat nematodes reveal very limited niche overlap among co-occurring species. PeerJ 7: e7864.
Yeates, G. W., T. d Bongers, R. G. M. De Goede, D. W. Freckman, & S. S. Georgieva, 1993. Feeding habits in soil nematode families and genera—an outline for soil ecologists. Journal of Nematology 25: 315–331.
Acknowledgements
We are grateful to Diego Fontaneto and Sidinei Magela Thomaz for their support and confidence allowing us to compile a special volume on freshwater meiofauna. We thank Peter E. Schmid and two anonymous reviewers for their helpful comments on a previous version of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Guest editors: Nabil Majdi, Jenny M. Schmid-Araya & Walter Traunspurger/Patterns and Processes of Meiofauna in Freshwater Ecosystems
Rights and permissions
About this article
Cite this article
Majdi, N., Schmid-Araya, J.M. & Traunspurger, W. Examining the diet of meiofauna: a critical review of methodologies. Hydrobiologia 847, 2737–2754 (2020). https://doi.org/10.1007/s10750-019-04150-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-019-04150-8