Abstract
Accurate prediction of the biodiversity–ecosystem functioning relationship requires adequate understanding of the interactions among species in a community. Effects of species diversity on ecosystem functioning are usually considered more pronounced with increasing functional dissimilarity, although species within functional groups may also perform non-identical functions and interact with each other. Here we present results of a laboratory experimental study aimed at elucidating whether interspecific interactions among species within a single nematode trophic group, bacterivores, (1) affect population development and community structure, and (2) depend on food availability. We studied the population growth of Rhabditis (Pellioditis) marina, a rhabditid nematode known to favour very high food densities when in monoculture, and of Diplolaimelloides meyli and D. oschei, congeneric Monhysteridae known to perform better in monocultures at intermediate food availability. Both Diplolaimelloides species showed significantly different patterns of food-density dependence in combination culture compared to monoculture. At very high food availability, the rhabditid nematode facilitated growth of both monhysterid species, probably as a result of down-regulation of bacterial density. At the lowest food availabilities, the presence of even low numbers of monhysterid nematodes lead to exclusion of the rhabditid, which at such low food availability has a very inefficient food uptake. At intermediate food availabilities, abundances of both Diplolaimelloides species were strongly depressed in the combination culture, as a result of food depletion by the rhabditid, indirect inhibitory interactions between the two congeneric species, or both. The complexity of the species interactions render predictions on the outcome and functional consequences of changes in within-trophic-group diversity highly problematic.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alkemade R, Wielemaker A, De Jong SA, Sandee AJJ (1992) Experimental evidence for the role of bioturbation by the marine nematode Diplolaimella dievengatensis in stimulating the mineralization of Spartina anglica leaves. Mar Ecol Prog Ser 90:149–155. doi:https://doi.org/10.3354/meps090149
Alkemade R, Wielemaker A, Hemminga MA (1993) Correlation between nematode abundance and decomposition rate of Spartina anglica leaves. Mar Ecol Prog Ser 99:293–300. doi:https://doi.org/10.3354/meps099293
Aller RC, Aller JY (1992) Meiofauna and solute transport in marine muds. Limnol Oceanogr 37:1018–1033
Arroyo NL, Aarnio K, Ólafsson E (2007) Interactions between two closely related phytal harpacticoid copepods, asymmetric positive and negative effects. J Exp Mar Biol Ecol 3:219–227. doi:https://doi.org/10.1016/j.jembe.2006.10.032
Blanc C, Sy M, Djizal D, Brauman A, Normand P, Villenave C (2006) Nutrition on bacteria by bacterial-feeding nematodes and consequences on the structure of soil bacterial community. Eur J Soil Biol 42:570–578. doi:https://doi.org/10.1016/j.ejsobi.2006.06.003
Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19. doi:https://doi.org/10.1007/BF00324627
Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10:239–251. doi:https://doi.org/10.1016/S0929-1393(98)00123-1
Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14:224–228. doi:https://doi.org/10.1016/S0169-5347(98)01583-3
Bongers T, Alkemade R, Yeates GW (1991) Interpretation of disturbance-induced maturity decrease in marine nematode assemblages by means of the Maturity Index. Mar Ecol Prog Ser 76:135–142. doi:https://doi.org/10.3354/meps076135
Cardinale BJ, Palmer MA, Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 24:426–429. doi:https://doi.org/10.1038/415426a
Chandler GT, Fleeger JW (1987) Facilitative and inhibitory interactions among estuarine meiobenthic harpacticoid copepods. Ecology 68:1906–1919. doi:https://doi.org/10.2307/1939882
Chapin FS III, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277:500–504. doi:https://doi.org/10.1126/science.277.5325.500
Charnov EL, Bull J (1977) When is sex environmentally determined? Nature 266:828–830. doi:https://doi.org/10.1038/266828a0
Debenham NJ, Lambshead PJD, Ferrero TJ, Smith CR (2004) The impact of whale falls on nematode abundance in the deep sea. Deep Sea Res Part I Oceanogr Res Pap 51:701–706. doi:https://doi.org/10.1016/j.dsr.2004.02.004
De Mesel I, Derycke S, Swings J, Vincx M, Moens T (2003) Influence of bacterivorous nematodes on the decomposition of cordgrass. J Exp Mar Biol Ecol 296:227–242. doi:https://doi.org/10.1016/S0022-0981(03)00338-1
De Mesel I, Derycke S, Moens T, Van der Gucht K, Vincx M, Swings J (2004) Top-down impact of bacterivorous nematodes on the bacterial community structure: a microcosm study. Environ Microbiol 6:733–744. doi:https://doi.org/10.1111/j.1462-2920.2004.00610.x
De Mesel I, Derycke S, Swings J, Vincx M, Moens T (2006) Role of nematodes in decomposition processes: does within-trophic group diversity matter? Mar Ecol Prog Ser 321:157–166. doi:https://doi.org/10.3354/meps321157
Derycke S, Remerie T, Vierstraete A, Backeljau T, Vanfleteren J, Vincx M, Moens T (2005) Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Mar Ecol Prog Ser 300:91–103. doi:https://doi.org/10.3354/meps300091
Derycke S, Backeljau T, Vlaeminck C, Vierstraete A, Vanfleteren J, Vincx M, Moens T (2006) Seasonal dynamics of population genetic structure in cryptic taxa of the Pellioditis marina complex (Nematoda: Rhabditida). Genetica 128:307–321. doi:https://doi.org/10.1007/s10709-006-6944-0
Derycke S, Van Vynckt R, Vanoverbeke J, Vincx M, Moens T (2007) Colonization patterns of Nematoda on decomposing algae in the estuarine environment: community assembly and genetic structure of the dominant species Pellioditis marina. Limnol Oceanogr 52:992–1001
Dietrich B, Wehner R (2003) Sympatry and allopatry in two desert ant sister species: how do Cataglyphis bicolor and C. savignyi coexist? Oecologia 136:63–72. doi:https://doi.org/10.1007/s00442-003-1245-0
dos Santos GAP, Derycke S, Fonsêca-Genevois VG, Coelho LCBB, Correia MTS, Moens T (2008) Differential effects of food availability on population growth and fitness of three species of estuarine, bacterial-feeding nematodes. J Exp Mar Biol Ecol 355:27–40. doi:https://doi.org/10.1016/j.jembe.2007.11.015
Emmerson MC, Solan M, Emes C, Paterson DM, Raffaelli DG (2001) Consistent patterns and the idiosyncratic effects of biodiversity in marine ecosystems. Nature 411:73–77. doi:https://doi.org/10.1038/35075055
Ettema CH (1998) Soil nematode diversity: species coexistence and ecosystem function. J Nematol 30:159–169
Ferris H, Matute MM (2003) Structural and functional succession in the nematode fauna of a soil food web. Appl Soil Ecol 23:93–110. doi:https://doi.org/10.1016/S0929-1393(03)00044-1
Ferris H, Eyre M, Venette RC, Lau SS (1996) Population energetics of bacterial-feeding nematodes: stage-specific development and fecundity rates. Soil Biol Biochem 28:271–280. doi:https://doi.org/10.1016/0038-0717(95)00127-1
Ferris H, Venette RC, Lau SS (1997) Population energetics of bacterial-feeding nematodes: carbon and nitrogen budgets. Soil Biol Biochem 29:1183–1194. doi:https://doi.org/10.1016/S0038-0717(97)00035-7
Ferris H, Bongers T, de Goede RGM (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13–29. doi:https://doi.org/10.1016/S0929-1393(01)00152-4
Fonseca G, Vanreusel A, Decraemer W (2006) Taxonomy and biogeography of Molgolaimus Ditlevsen, 1921 (Nematoda: Chromadoria) with reference to the origins of deep-sea nematodes. Antarct Sci 18:23–50. doi:https://doi.org/10.1017/S0954102006000034
Fridley JD (2001) The influence of species diversity on ecosystem productivity: how, where, and why? Oikos 93:514–526. doi:https://doi.org/10.1034/j.1600-0706.2001.930318.x
Fu S, Ferris H, Brown D, Plant R (2005) Does the positive feedback effect of nematodes on the biomass and activity of their bacteria prey vary with nematode species and population size? Soil Biol Biochem 37:1979–1987. doi:https://doi.org/10.1016/j.soilbio.2005.01.018
Grewal PS, Lewis EE, Venkatachari S (1999) Allelopathy: a possible mechanism of suppression of plant-parasitic nematodes by entomopathogenic nematodes. Nematology 1:735–743. doi:https://doi.org/10.1163/156854199508766
Heemsbergen DA, Berg MP, Loreau M, Van Hal JR, Faber JH, Verhoef HA (2004) Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science 306:1019–1020. doi:https://doi.org/10.1126/science.1101865
Heip C, Vincx M, Vranken G (1985) The ecology of marine nematodes. Oceanogr Mar Biol Annu Rev 23:399–489
Ilieva-Makulec K (2001) A comparative study of the life strategies of two bacterial-feeding nematodes under laboratory conditions. III. Influence of the initial nematode density on the interactions of Acrobeloides nanus (De Man 1880) Anderson and Dolichorhabditis dolichura (Schneider 1866) Andrassy 1983 in mixed cultures. Pol J Ecol 49:137–144
Johnson KH, Vogt KA, Clark HJ, Schmitz OJ, Vogt DJ (1996) Biodiversity and the productivity and stability of ecosystems. Trends Ecol Evol 11:372–377. doi:https://doi.org/10.1016/0169-5347(96)10040-9
Jonsson M, Malmqvist B (2003) Mechanisms behind positive diversity effects on ecosystem functioning: testing the facilitation and interference hypotheses. Oecologia 134:554–559
Kokko H, Rankin DJ (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philos Trans R Soc Lond B 361:319–334. doi:https://doi.org/10.1098/rstb.2005.1784
Köster M, Meyer-Reil LA (2001) Characterization of carbon and microbial biomass pools in shallow water coastal sediments of the southern Baltic Sea (Nordrügensche Bodden). Mar Ecol Prog Ser 214:25–41. doi:https://doi.org/10.3354/meps214025
Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808. doi:https://doi.org/10.1126/science.1064088
Mikola J (1998) Effects of microbivore species composition and basal resource enrichment on trophic-level biomasses in an experimental microbial-based soil food web. Oecologia 117:396–403. doi:https://doi.org/10.1007/s004420050673
Moens T, Vincx M (1997) Observations on the feeding ecology of estuarine nematodes. J Mar Biol Assoc UK 77:211–227
Moens T, Vincx M (1998) On the cultivation of free-living marine and estuarine nematodes. Helgolander Meeresunters 52:115–139. doi:https://doi.org/10.1007/BF02908742
Moens T, Vincx M (2000a) Temperature and salinity constraints on the life cycle of two brackish-water nematode species. J Exp Mar Biol Ecol 243:115–135. doi:https://doi.org/10.1016/S0022-0981(99)00113-6
Moens T, Vincx M (2000b) Temperature, salinity and food thresholds in two brackish-water bacterivorous nematode species: assessing niches from food absorption and respiration experiments. J Exp Mar Biol Ecol 243:137–154. doi:https://doi.org/10.1016/S0022-0981(99)00114-8
Moens T, Vierstraete A, Vincx M (1996) Life strategies in two bacterivorous marine nematodes: preliminary results. PSZN I Mar Ecol 17:509–518. doi:https://doi.org/10.1111/j.1439-0485.1996.tb00524.x
Moens T, Verbeeck L, de Maeyer A, Swings J, Vincx M (1999a) Selective attraction of marine bacterivorous nematodes to their bacterial food. Mar Ecol Prog Ser 176:165–178. doi:https://doi.org/10.3354/meps176165
Moens T, Verbeeck L, Vincx M (1999b) Preservation and incubation time-induced bias in tracer-aided grazing studies on meiofauna. Mar Biol (Berl) 133:69–77. doi:https://doi.org/10.1007/s002270050444
Moens T, Yeates GW, De Ley P (2004) Use of carbon and energy sources by nematodes. Nematol Monogr Perspect 2:529–545
Moens T, dos Santos GAP, Thompson F, Swings J, Fonsêca-Genevois V, Vincx M, De Mesel I (2005) Do nematode mucus secretions affect bacterial growth? Aquat Microb Ecol 40:77–83. doi:https://doi.org/10.3354/ame040077
Naeem S (1998) Species redundancy and ecosystem reliability. Conserv Biol 12:39–45. doi:https://doi.org/10.1046/j.1523-1739.1998.96379.x
Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579. doi:https://doi.org/10.1046/j.1461-0248.2003.00471.x
Pfennig DW, Murphy PJ (2002) How fluctuating competition and phenotypic plasticity mediate species divergence. Evolution 56:1217–1228
Postma-Blaauw MB, de Vries FT, de Goede RGM, Bloem J, Faber JH, Brussaard L (2005) Within-trophic group interactions of bacterivorous nematode species and their effects on the bacterial community and nitrogen mineralization. Oecologia 142:428–439. doi:https://doi.org/10.1007/s00442-004-1741-x
Schiemer F (1982a) Food dependence and energetics of free-living nematodes. I. Respiration, growth and reproduction of Caenorhabditis briggsae (Nematoda) at different levels of food supply. Oecologia 54:108–121. doi:https://doi.org/10.1007/BF00541117
Schiemer F (1982b) Food dependence and energetics of free-living nematodes. II. Life history parameters of Caenorhabditis briggsae (Nematoda) at different levels of food supply. Oecologia 54:122–128. doi:https://doi.org/10.1007/BF00541118
Schratzberger M, Warr K, Rogers SI (2007) Functional diversity of nematode communities in the southwestern North Sea. Mar Environ Res 63:368–389. doi:https://doi.org/10.1016/j.marenvres.2006.10.006
Sokal RR, Rohlf FJ (2001) Biometry, 3rd edn. WH Freeman, New York
Tietjen JH, Lee JJ, Rullman J, Greengart A, Trompeter J (1970) Gnotobiotic culture and physiological ecology of the marine nematode Rhabditis marina Bastian. Limnol Oceanogr 15:535–543
Titelman J, Varpe Ø, Eliassen S, Fiksen Ø (2007) Copepod mating: chance or choice? J Plankton Res 29:1023–1030. doi:https://doi.org/10.1093/plankt/fbm076
Van Duyl FC, Kop AJ (1994) Bacterial production in North-Sea sediments—clues to seasonal and spatial variations. Mar Biol (Berl) 120:323–337. doi:https://doi.org/10.1007/BF00349694
Venette RC, Ferris H (1998) Influence of bacterial type and density on population growth of bacterial-feeding nematodes. Soil Biol Biochem 30:949–960. doi:https://doi.org/10.1016/S0038-0717(97)00176-4
Vranken G, Heip C (1983) Calculation of the intrinsic rate of natural increase, rm, with Rhabditis marina Bastian 1865 (Nematoda). Nematologica 29:468–477
Walker BH (1992) Biodiversity and ecological redundancy. Conserv Biol 6:18–23. doi:https://doi.org/10.1046/j.1523-1739.1992.610018.x
Wall D, Moore JC (1999) Interactions underground. Bioscience 49:109–117. doi:https://doi.org/10.2307/1313536
Warwick RM (1987) Meiofauna: their role in marine detrital systems. In: Moriarty DJW, Pullin RSV (eds) Detritus and microbial ecology in aquaculture. ICLARM conference proceedings 14. International Center for Living Aquatic Resources Management, Manila, pp 282–295
Wieser W (1953) Die Beziehung zwishen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden marinen Nematoden. Ark Zool 4:439–484
Yeates GW, Bongers T, de Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in nematode families and genera—a guide for soil ecologists. J Nematol 25:315–331
Acknowledgments
This work was financially supported by a CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) grant to the first author, and by Ghent University through BOF projects 0110600002 and 01GZ0705. S.D. and T.M. are postdoctoral fellows with the Flemish Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S.D. Connell.
Rights and permissions
About this article
Cite this article
dos Santos, G.A.P., Derycke, S., Genevois, V.G.F. et al. Interactions among bacterial-feeding nematode species at different levels of food availability. Mar Biol 156, 629–640 (2009). https://doi.org/10.1007/s00227-008-1114-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-008-1114-9