Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-22T23:31:58.415Z Has data issue: false hasContentIssue false
  • English
  • Français

Community-wide stable isotope analysis reveals two distinct trophic groups in a service-providing carabid community

Published online by Cambridge University Press:  15 June 2017

S. Kamenova ,
C. Leroux ,
S.E. Polin  and
M. Plantegenest
S. Kamenova*
Affiliation:
Centre d'Etudes Biologiques de Chizé, 79360 Villiers-en-Bois, France UMR 1349 Institut de Génétique, Environnement et Protection des Plantes, 35042 Rennes, France
C. Leroux
Affiliation:
Station Biologique de Roscoff, Place Georges Teissier 29680 Roscoff, France
S.E. Polin
Affiliation:
UMR 1349 Institut de Génétique, Environnement et Protection des Plantes, 35042 Rennes, France
M. Plantegenest
Affiliation:
UMR 1349 Institut de Génétique, Environnement et Protection des Plantes, 35042 Rennes, France
*
*Author for correspondence Phone: +33 (0)2 23 48 50 00 Fax: +33 (0)2 23 48 55 10 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Disentangling trophic interactions among species is important for elucidating mechanisms underlying ecosystem functioning and services. Carabid beetles are an important guild of predators that may regulate pest populations in arable landscapes, but their generalist feeding behavior hinders predictions about their actual contribution to pest control. In order to assess carabids’ potential for pest control, we simultaneously analyzed the carbon and nitrogen stable isotope ratios of a community of 45 co-occurring species in wheat and oilseed rape fields. With the expectation to identify distinct trophic groups based on the mean and the variance of carabid isotopic signatures, we observed a high degree of overlap in trophic positions between species. However, we also observed that species could be successfully categorized into two groups according to whether or not their carbon signatures varied independently from variations in the crop baseline. We interpret these results as differential primary resource uptake or by differential mobility aptitude in foraging. Accordingly, we propose that the isotopic signal can inform us on the presence/absence of links between generalist predators and cultivated plants through the trophic networks they belong to, and consequently on their potential role as pest natural enemies. We therefore suggest the complementarity of stable isotope analysis for obtaining a time-integrated assessment of carabid trophic behavior that may be combined with more direct molecular diet analysis allowing the simultaneous quantification of specific trophic links within agricultural landscapes.

Keywords

δ13Cδ15Ntrophic interactionsecosystem servicesagroecosystemsbiodiversitypest controlground beetles
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 1 , February 2018 , pp. 130 - 139
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agustí, N., Shayler, S.P., Harwood, J.D., Vaughan, I.P., Sunderland, K.D. & Symondson, W.O.C. (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Molecular Ecology 12, 3467–3475.CrossRefGoogle ScholarPubMed
Bell, J.R., Andrew King, R., Bohan, D.A. & Symondson, W.O.C. (2010) Spatial co-occurrence networks predict the feeding histories of polyphagous arthropod predators at field scales. Ecography 33, 64–72.CrossRefGoogle Scholar
Bennett, P.M. & Hobson, K.A. (2009) Trophic structure of a boreal forest arthropod community revealed by stable isotope (d13C, d15N) analyses. Entomological Science 12, 17–24.CrossRefGoogle Scholar
Bilde, T. & Toft, S. (1998) Quantifying food limitation of arthropod predators in the field. Oecologia 115, 54–58.CrossRefGoogle ScholarPubMed
Bohan, D.A., Bohan, A.C., Glen, D.M., Symondson, W.O.C., Wiltshire, C.W. & Hughes, L. (2000) Spatial dynamics of predation by carabid beetles on slugs. Journal of Animal Ecology 69, 367–379.CrossRefGoogle Scholar
Bohan, D.A., Boursault, A., Brooks, D.R. & Petit, S. (2011) National-scale regulation of the weed seedbank by carabid predators. Journal of Applied Ecology 48, 888–898.CrossRefGoogle Scholar
Bohan, D.A., Raybould, A., Mulder, C., Woodward, G., Tamaddoni-Nezhad, A., Blüthgen, N., Pocock, M.J.O., Muggleton, S., Evans, D.M., Astegiano, J., Massol, F., Loeuille, N., Petit, S. & Macfadyen, S. (2013) Networking agroecology: integrating the diversity of agroecosystem interactions. Advances in Ecological Research 49, 1–67.CrossRefGoogle Scholar
Bommarco, R., Firle, S.O. & Ekbom, B. (2007) Outbreak suppression by predators depends on spatial distribution of prey. Ecological Modelling 201, 163–170.CrossRefGoogle Scholar
Boreau de Roincé, C., Lavigne, C., Ricard, J.-M., Franck, P., Bouvier, J.-C., Garcin, A. & Symondson, W.O.C. (2012) Predation by generalist predators on the codling moth versus a closely-related emerging pest the oriental fruit moth: a molecular analysis. Journal of Applied Entomology 14, 260–269.Google Scholar
Cardinale, B.J., Harvey, C.T., Gross, K. & Ives, A.R. (2003) Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecology Letters 6, 857–865.CrossRefGoogle Scholar
Clare, E.L. (2014) Molecular detection of trophic interactions: emerging trends, distinct advantages, significant considerations and conservation applications. Evolutionary Applications 7, 1144–1157.CrossRefGoogle ScholarPubMed
Cucherousset, J. & Villéger, S. (2015) Quantifying the multiple facets of isotopic diversity: new metrics for stable isotope ecology. Ecological Indicators 56, 152–160.CrossRefGoogle Scholar
Davey, J.S., Vaughan, I.P., Andrew King, R., Bell, J.R., Bohan, D.A., Bruford, M.W., Holland, J.M. & Symondson, W.O.C. (2013) Intraguild predation in winter wheat: prey choice by a common epigeal carabid consuming spiders. Journal of Applied Ecology 50, 271–279.CrossRefGoogle Scholar
DeNiro, M.J. & Epstein, S. (1978) Influence of diet on distribution of carbon isotopes in animals. Geochimica and Cosmochimica Acta 42, 495–506.CrossRefGoogle Scholar
DeNiro, M.J. & Epstein, S. (1981) Influence of diet on the distribution of carbon isotopes in animals. Geochimica and Cosmochimica Acta 45, 341–351.CrossRefGoogle Scholar
Eggers, T. & Jones, T.H. (2000) You are what you eat… or are you? Trends in Ecology and Evolution 15, 265–266.CrossRefGoogle ScholarPubMed
Ehleringer, J.R. & Rundel, P.W. (1988) Stable isotopes: history and units. pp. 1–15 in Rundel, P.W., Ehleringer, J.R. & Nagy, K.A. (Eds) Stable Isotopes in Ecological Research. Ecological Studies Series. New York, Springer-Verlag.Google Scholar
Eitzinger, B. & Traugott, M. (2011) Which prey sustains cold-adapted invertebrate generalist predators in arable land? Examining prey choices by molecular gut-content analysis: prey of cold-adapted predators. Journal of Applied Ecology 48, 591–599.CrossRefGoogle Scholar
Fahrig, L., Baudry, J., Brotons, L., Burel, F.G., Crist, T.O., Fuller, R.J., Sirami, C., Siriwardena, G.M. & Martin, J.-L. (2010) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecology Letters 14, 101–112.CrossRefGoogle ScholarPubMed
Finke, D.L. & Denno, R.F. (2005) Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades. Ecology Letters 8, 1299–1306.CrossRefGoogle Scholar
Foltan, P., Sheppard, S., Konvicka, M. & Symondson, W.O.C. (2005) The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR. Molecular Ecology 14, 4147–4158.CrossRefGoogle ScholarPubMed
Forsythe, T.G. (1982) Feeding mechanisms of certain ground beetles (Coleoptera: Carabidae). Coleopterist Bulletin 36, 26–73.Google Scholar
Forsythe, T.G. (1983) Mouthparts and feeding of certain ground beetles (Coleoptera: Carabidae). Zoological Journal of the Linnean Society 79, 319–376.CrossRefGoogle Scholar
Gannes, L.Z., Martínez del Rio, C. & Koch, P. (1998) Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comparative Biochemistry and Physiology 119, 725–737.CrossRefGoogle ScholarPubMed
Girard, J., Baril, A., Mineau, P. & Fahrig, L. (2011) Carbon and nitrogen stable isotope ratios differ among invertebrates from field crops, forage crops, and non-cropped land uses. Ecoscience 18, 98–109.CrossRefGoogle Scholar
Goldschmidt, H. & Toft, S. (1997) Variable degrees of granivory and phytophagy in insectivorous carabid beetles. Pedobiologia 41, 521–525.CrossRefGoogle Scholar
Heidemann, K., Scheu, S., Ruess, L. & Maraun, M. (2011) Molecular detection of nematode predation and scavenging in oribatid mites: laboratory and field experiments. Soil Biology and Biochemistry 43, 2229–2236.CrossRefGoogle Scholar
Hengeveld, R. (1980) Polyphagy, oligophagy and food specialization in ground beetles (Coleoptera, Carabidae). Netherlands Journal of Zoology 30, 564–584.CrossRefGoogle Scholar
Hintzpeter, U. & Bauer, T. (1986) The antennal setal trap of the Ground beetle Loricera pilicornis: a specialization for feeding on Collembola. Journal of Zoology 208, 615–630.CrossRefGoogle Scholar
Holland, J.M., Thomas, C.F.G., Birkett, T., Southway, S. & Oaten, H. (2005) Farm-scale spatiotemporal dynamics of predatory beetles in arable crops. Journal of Applied Ecology 42, 1140–1152.CrossRefGoogle Scholar
Honek, A., Martinkova, Z. & Jarosik, V. (2003) Ground beetles (Carabidae) as seed predators. European Journal of Entomology 100, 531–544.CrossRefGoogle Scholar
Honek, A., Martinkova, Z., Saska, P. & Pekar, S. (2007) Size and taxonomic constraints determine the seed preferences of Carabidae (Coleoptera). Basic and Applied Ecology 8, 343–353.CrossRefGoogle Scholar
Hooper, D.U., Chapin, F.S. III, Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, D.M., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setälä, H., Symstad, A.J., Vandermeer, J. & Wardle, D.A. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3–35.CrossRefGoogle Scholar
Ikeda, H., Kubota, K., Kagawa, A. & Sota, T. (2010) Diverse diet compositions among harpaline ground beetle species revealed by mixing model analyses of stable isotope ratios. Ecological Entomology 35, 307–316.CrossRefGoogle Scholar
Johnson, K.H., Vogt, K.A., Clark, H.J., Schmitz, O.J. & Vogt, D.J. (1996) Biodiversity and the productivity and stability of ecosystems. Trends in Ecology & Evolution 11, 372–377.CrossRefGoogle ScholarPubMed
Johnson, N.E. & Cameron, R.S. (1969) Phytophagous ground beetles. Annals of the Entomological Society of America 62, 909–914.CrossRefGoogle Scholar
Jonason, D., Smith, H., Bengtsson, J. & Birkhofer, K. (2013) Landscape simplification promotes weed seed predation by carabid beetles (Coleoptera: Carabidae). Landscape Ecolology 28, 487–494.CrossRefGoogle Scholar
Juen, A. & Traugott, M. (2005) Detecting predation and scavenging by DNA gut-content analysis: a case study using a soil insect predator-prey system. Oecologia 142, 344–352.CrossRefGoogle ScholarPubMed
Kamenova, S., Tougéron, K., Cateine, M., Marie, A. & Plantegenest, M. (2015) Behaviour-driven micro-scale niche differentiation in carabid beetles. Entomologia Experimentalis et Applicata 155, 39–46.CrossRefGoogle Scholar
King, R.A., Vaughan, I.P., Bell, J.R., Bohan, D.A. & Symondson, W.O.C. (2010) Prey choice by carabid beetles feeding on an earthworm community analysed using species-and lineage-specific PCR primers. Molecular Ecology 19, 1721–1732.CrossRefGoogle Scholar
Kromp, B. (1999) Carabid beetles in sustainable agriculture: a review on pest control efficacy cultivation impact and enhancement. Agriculture, Ecosystems and Environment 74, 187–228.CrossRefGoogle Scholar
Kulkarni, S., Dosdall, L.M., Willenborg, C.J. (2015) The role of ground beetles (Coleoptera: Carabidae) in weed seed consumption: a review. Weed Science 63, 355–376.CrossRefGoogle Scholar
Laparie, M., Larvor, V., Frenot, Y., Renault, D. (2012) Starvation resistance and effects of diet on energy reserves in a predatory ground beetle (Merizodus soledadinus; Carabidae) invading the Kerguelen Islands. Comparative Biochemistry and Physiology 161, 122–129.CrossRefGoogle Scholar
Larochelle, A. (1990) The Food of Carabid Beetles. Canada, Fabreries Supplement.Google Scholar
Layman, C.A., Arrington, D.A., Montaña, C.G., Post, D.M. (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88, 42–48.CrossRefGoogle ScholarPubMed
Letourneau, D.K., Jedlicka, J.A., Bothwell, S.G. & Moreno, C.R. (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annual Review of Ecology, Evolution, and Systematics 40, 573–592.CrossRefGoogle Scholar
Loreau, M. (2000) Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91, 3–17.CrossRefGoogle Scholar
Losey, J.E. & Denno, R.F. (1998) Positive predator-predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79, 2143–2152.Google Scholar
Lövei, G.L. & Sunderland, K.D. (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annual Review of Entomology 41, 231–256.CrossRefGoogle ScholarPubMed
Makarov, K., Matalin, A., Goncharov, A. & Tiunov, A. (2013) Report on XVIth European Carabidologists Meeting, September 22–27, 2013, Prague, Czech.Google Scholar
Marrec, R., Badenhausser, I., Bretagnolle, V., Börger, L., Roncoroni, M., Guillon, N. & Gauffre, B. (2015) Crop succession and habitat preferences drive the distribution and abundance of carabid beetles in an agricultural landscape. Agriculture, Ecosystems & Environment 199, 282–289.CrossRefGoogle Scholar
Marshall, E.J.P., Brown, V.K., Boatman, N.D., Lutman, P.J.W., Squire, G.R. & Ward, L.K. (2003) The role of weeds in supporting biological diversity within crop fields. Weed Research 43, 77–89.CrossRefGoogle Scholar
Martínez del Rio, C., Wolf, N., Carleton, S.A. & Gannes, L.Z. (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews 84, 91–111.CrossRefGoogle Scholar
Mollot, G., Duyck, P.-F., Lefeuvre, P., Lescourret, F., Martin, J.-F., Piry, S., Canard, E. & Tixier, P. (2014) Cover cropping alters the diet of arthropods in a banana plantation: a metabarcoding approach. PLoS ONE 9, e93740.CrossRefGoogle Scholar
Montoya, J.M., Rodríguez, M.A. & Hawkins, B.A. (2003) Food web complexity and higher-level ecosystem services. Ecology Letters 6, 587–593.CrossRefGoogle Scholar
Okuzaki, Y., Tayasu, I., Okuda, N. & Sota, T. (2010) Stable isotope analysis indicates trophic differences among forest floor carabids in Japan. Entomologia Experimentalis et Applicata 135, 263–270.CrossRefGoogle Scholar
Parnell, A.C., Phillips, D.L., Bearhop, S., Semmens, B.X., Ward, E.J., Moore, J.W., Jackson, A.L., Grey, J., Kelly, D.J., Inger, R. (2013) Bayesian stable isotope mixing models. Environmetrics 24, 387–399.CrossRefGoogle Scholar
Peralta, G., Frost, C.M., Rand, T.A., Didham, R.K. & Tylianakis, J.M. (2014) Complementarity and redundancy of interactions enhance attack rates and spatial stability in host–parasitoid food webs. Ecology 95, 1888–1896.CrossRefGoogle ScholarPubMed
Peterson, B.J. & Fry, B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecological Systems 18, 293–320.CrossRefGoogle Scholar
Pocock, M.J.O., Evans, D.M. & Memmott, J. (2012) The robustness and restoration of a network of ecological networks. Science 335, 973–977.CrossRefGoogle ScholarPubMed
Pompanon, F., Deagle, B.E., Symondson, W.O.C., Brown, D.S., Jarman, S.N. & Taberlet, P. (2012) Who is eating what: diet assessment using Next Generation Sequencing. Molecular Ecology 21, 1931–1950.CrossRefGoogle ScholarPubMed
Puech, C., Poggi, S., Baudry, J. & Aviron, S. (2015) Do farming practices affect natural enemies at the landscape scale? Landscape Ecology 30, 125–140.CrossRefGoogle Scholar
R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at http://www.R-project.org/.Google Scholar
Roger, J.-L., Jambon, O. & Bouger, G. (2012) Clé de Détermination des Carabidés Paysages agricoles du Nord Ouest de la France. https://osur.univ-rennes1.fr/za-armorique/news/cle-de-determination-des-carabidae-des-paysages-agricoles-du-nord-ouest-de-la-france.html Google Scholar
Rosenheim, J.A. (1998) Higher-order predators and the regulation of insect herbivore populations. Annual Review of Entomology 43, 421–447.CrossRefGoogle ScholarPubMed
Rouabah, A., Lasserre-Joulin, F., Amiaud, B. & Plantureux, S. (2014) Emergent effects of ground beetles size diversity on the strength of prey suppression: ground beetle size diversity and pest control. Ecological Entomology 39, 47–57.CrossRefGoogle Scholar
Rusch, A., Birkhofer, K., Bommarco, R., Smith, H.G. & Ekbom, B. (2015) Predator body sizes and habitat preferences predict predation rates in an agroecosystem. Basic and Applied Ecology 16, 250–259.CrossRefGoogle Scholar
Saska, P. (2005) Contrary food requirements of the larvae of two Curtonotus (Coleoptera: Carabidae: Amara) species. Annals of Applied Biology 147, 139–144.CrossRefGoogle Scholar
Saska, P. & Honek, A. (2004) Development of the beetle parasitoids, Brachinus explodens and B. crepitans (Coleoptera: Carabidae). Journal of Zoology 262, 29–36.CrossRefGoogle Scholar
Saska, P. & Honek, A. (2008) Synchronization of a Coleopteran Parasitoid, Brachinus spp. (Coleoptera: Carabidae), and its host. Annals of the Entomological Society of America 101, 533–538.CrossRefGoogle Scholar
Snyder, W.E., Snyder, G.B., Finke, D.L. & Straub, C.S. (2006) Predator biodiversity strengthens herbivore suppression. Ecology Letters 9, 789–796.CrossRefGoogle ScholarPubMed
Staudacher, K., Jonsson, M. & Traugott, M. (2016) Diagnostic PCR assays to unravel food web interactions in cereal crops with focus on biological control of aphids. Journal of Pest Science 89, 281–293.CrossRefGoogle ScholarPubMed
Straub, C.S., Finke, D.L. & Snyder, W.E. (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biological Control 45, 225–237.CrossRefGoogle Scholar
Sunderland, K.D. (1975) The diet of some predatory arthropods in cereal crops. Journal of Applied Ecology 12, 507–515.CrossRefGoogle Scholar
Symondson, W.O.C. (2002) Molecular identification of prey in predator diets. Molecular Ecology 11, 627–641.CrossRefGoogle ScholarPubMed
Thiele, H.U. (1977) Carabid Beetles in Their Environments. pp. 1–369. Berlin/Heidelberg, Springer.CrossRefGoogle Scholar
Thompson, R.M., Brose, U., Dunne, J.A., Hall, R.O., Hladyz, S., Kitching, R.L., Martinez, N.D., Rantala, H., Romanuk, T.N., Stouffer, D.B. & Tylianakis, J.M. (2012) Food webs: reconciling the structure and function of biodiversity. Trends in Ecology & Evolution 27, 689–697.CrossRefGoogle ScholarPubMed
Tixier, P., Dagneaux, D., Mollot, G., Vinatier, F. & Duyck, P.-F. (2013) Weeds mediate the level of intraguild predation in arthropod food webs. Journal of Applied Entomology 137, 702–710.CrossRefGoogle Scholar
Trichard, A., Alignier, A., Biju-Duval, L. & Petit, S. (2013) The relative effects of local management and landscape context on weed seed predation and carabid functional groups. Basic and Applied Ecology 14, 235–245.CrossRefGoogle Scholar
Vacher, C., Tamaddoni-Nezhad, A., Kamenova, S., Peyrard, N., Moalic, Y., Sabbadin, R., Schwaller, L., Chiquet, J., Smith, M.A., Vallance, J., Fievet, V., Jakuschkin, B. & Bohan, D.A. (2016) Learning ecological networks from next-generation sequencing data. pp. 1–39 in Woodward, G. & Bohan, D. (Eds) Advances in Ecological Research. Cambridge, MA, Elsevier Academic Press.Google Scholar
Von Berg, K., Traugott, M. & Scheu, S. (2012) Scavenging and active predation in generalist predators: a mesocosm study employing DNA-based gut content analysis. Pedobiologia 55, 1–5.CrossRefGoogle Scholar
Wallinger, C., Staudacher, K., Schallhart, N., Peter, E., Dresch, P., Juen, A., Traugott, M. (2013) The effect of plant identity and the level of plant decay on molecular gut content analysis in a herbivorous soil insect. Molecular Ecology Resources 13, 75–83.CrossRefGoogle Scholar
Wallinger, C., Sint, D., Baier, F., Schmid, C., Mayer, R. & Traugot, M. (2015) Detection of seed DNA in regurgitates of granivorous carabid beetles. Bulletin of Entomological Research 105, 728–35.CrossRefGoogle ScholarPubMed
Young, O.P. (1984) Utilization of dead insects on the soil surface in row crop situations. Environmental Entomology 13, 1346–1351.CrossRefGoogle Scholar
Young, O.P. (2005) Laboratory predation and scavenging of three ground beetle (Carabidae) species from the U.S.A. on Fall Armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) larvae. Entomological News 116, 347–352.Google Scholar
Zalewski, M., Dudek, D., Tiunov, A., Godeau, J.-F., Okuzaki, Y., Ikeda, H., Sienkiewicz, P. & Ulrich, W. (2014) High niche overlap in stable isotope space of ground beetles. Annales Zoologici Fennici 51, 301–312.CrossRefGoogle Scholar
Supplementary material: File

Kamenova supplementary material S1

Supplementary Table

Download Kamenova supplementary material S1(File)
File 88.2 KB
Supplementary material: PDF

Kamenova supplementary material S2

Supplementary Figure

Download Kamenova supplementary material S2(PDF)
PDF 19.2 KB
Supplementary material: PDF

Kamenova supplementary material S3

Supplementary Figure

Download Kamenova supplementary material S3(PDF)
PDF 19.2 KB