[en] Deadwood stores about 8% of global carbon stock and its decomposition is a key factor in forest ecosystems. Deadwood-associated (saproxylic) organisms constitute a food web that sustains a substantial part of biodiversity globally. After fungi, saproxylic beetles are the most prominent agents of structural deadwood decomposition in forests. They are often classified according to their presumed linkto the deadwood decomposition gradient, generally as feeding on fresh wood, decayed wood, fungi or as predators. These classifications are, however, based on ecomorphological characters (e.g., trophic morphology, habitat use) while information on their diet is globally limited. Carbon (δ13C) and nitrogen (δ15N) stable isotope ratios represent potential useful tracers to improve knowledge on the trophic ecology of this model group and the whole decomposition food web. We performed stable isotope analysis on 121 beetle species (530 samples) from a mixed-deciduous forest in Central Europe in order to (1) characterize drivers of saproxylic beetles’ isotopic variability with respect to potential food sources along the wood decomposition gradient and in relation to the potentially key intrinsic factors such as phylogeny and body size, and (2) to assess how isotope information matches with two trophic guild classifications based on ecomorphological characters which are commonly used in ecological studies. The analysis revealed a clear pattern of δ13C increase and simultaneous C:N ratio decrease across potential food sources along the gradient from fresh to decayed deadwood and fungi. Beetle phylogeny and body size explained a significant part of their isotope variability, with values of δ13C being lower in smaller species. After filtering out these effects, the δ13C values reflected the position of beetle species on the decomposition gradient only loosely. Fungi-feeding guild had higher δ13C values than the guilds dependent on fresher deadwood, but otherwise the guilds were indistinguishable. Deadwood consumers did not differ from predators. The isotopic niches of different feeding guilds largely overlapped, and the large observed variation suggests that not only fungi feeders but species from most guilds may depend considerably on fungi and that mixed trophic strategies may be more common in the decomposition food web than currently acknowledged.
Research Center/Unit :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Environmental sciences & ecology Entomology & pest control Zoology
Author, co-author :
Kozel, Petr; Biology Centre of the Czech Academy of Sciences, Czech Republic > Institute of Entomology
Lejeune, Benjamin ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Écologie et de Conservation des Amphibiens (LECA)
Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Ecologie trophique et isotopique ; F.R.S.-FNRS - Fonds de la Recherche Scientifique
Drag, Lukas; Biology Centre of the Czech Academy of Sciences > Institute of Entomology
Cizek, Lukas; Biology Centre of the Czech Academy of Sciences > Institute of Entomology,
Sebek, Pavel; Biology Centre of the Czech Academy of Sciences, Czech Republic > Institute of Entomology
Language :
English
Title :
Stable isotopes of saproxylic beetles reveal low differences among trophic guilds and suggest a high dependence on fungi
Publication date :
22 February 2025
Journal title :
Ecological Monographs
ISSN :
0012-9615
Publisher :
Wiley-Blackwell, United States
Volume :
95
Issue :
1
Pages :
e70002
Peer reviewed :
Peer Reviewed verified by ORBi
Development Goals :
15. Life on land
Funding number :
GAJU 038/2019/P
Funding text :
projects GAJU 011/2019/P and GAJU 038/2019/P provided by the Grant Agency of the University of South Bohemia, Czech Republic
Adams, M. O., C. L. Seifert, L. Lehner, C. Truxa, W. Wanek, and K. Fiedler. 2016. “Stable Isotope Signatures Reflect Dietary Diversity in European Forest Moths.” Frontiers in Zoology 13: 1–10.
Allgeier, J. E., B. C. Weeks, K. S. Munsterman, N. Wale, S. J. Wenger, V. Parravicini, N. M. D. Schiettekatte, S. Villéger, and D. E. Burkepile. 2021. “Phylogenetic Conservatism Drives Nutrient Dynamics of Coral Reef Fishes.” Nature Communications 12(1): 5432.
Biedermann, P. H. W., and F. E. Vega. 2020. “Ecology and Evolution of Insect–Fungus Mutualisms.” Annual Review of Entomology 65: 22.1–22.25.
Bílý, S. 1990. “Cucujus cinnaberinus Scopoli, 1763, Cucujidae.” In Beetles, edited by Anonymous, 142–143. Prague: Artia.
Birkemoe, T., R. M. Jacobsen, A. Sverdrup-Thygeson, and P. H. W. Biedermann. 2018. “Insect-Fungus Interactions in Dead Wood Systems.” In Saproxylic Insects. Diversity, Ecology and Conservation, edited by M. D. Ulyshen, 377–427. Cham: Springer International Publishing. https://doi.org/10.1007/978-3-319-75937-1_12.
Bluhm, C., S. Scheu, and M. Maraun. 2015. “Oribatid Mite Communities on the Bark of Dead Wood Vary with Log Type, Surrounding Forest and Regional Factors.” Applied Soil Ecology 89: 102–112.
Blüthgen, N., G. Gebauer, and K. Fiedler. 2003. “Disentangling a Rainforest Food Web Using Stable Isotopes: Dietary Diversity in a Species-Rich Ant Community.” Oecologia 137(3): 426–435.
Bonacci, T., M. Rovito, J. Horák, and P. Brandmayr. 2020. “Artificial Feeding and Laboratory Rearing of Endangered Saproxylic Beetles as a Tool for Insect Conservation.” Journal of Insect Science 20(5): 20.
Bouget, C., H. Brustel, and L. M. Nageleisen. 2005. “Nomenclature des Groupes Écologiques D'insectes Liés au Bois: Synthèse et Mise au Point Sémantique.” Comptes Rendus Biologies 328: 936–948.
Bouget, C., H. Brustel, T. Noblecourt, and P. Zagatti. 2019. Les Coléoptères Saproxyliques de France: Catalogue Écologique Illustré 744. Paris: Muséum National d'Histoire Naturelle.
Bouget, C., H. Brustel, and P. Zagatti. 2008. “The French Information System on Saproxylic Beetle Ecology (FRISBEE): An Ecological and Taxonomical Database to Help with the Assessment of Forest Conservation Status.” Revue d'Écologie (La Terre et la Vie) 10: 33–36.
Bourguignon, T., J. Šobotník, G. Lepoint, J. M. Martin, and Y. Roisin. 2009. “Niche Differentiation among Neotropical Soldierless Soil-Feeding Termites Revealed by Stable Isotope Ratios.” Soil Biology and Biochemistry 41(10): 2038–2043.
Bourguignon, T., J. A. N. Šobotník, G. Lepoint, J. M. Martin, O. J. Hardy, A. Dejean, and Y. Roisin. 2011. “Feeding Ecology and Phylogenetic Structure of a Complex Neotropical Termite Assemblage, Revealed by Nitrogen Stable Isotope Ratios.” Ecological Entomology 36(2): 261–269.
Brooks, J. L., and S. I. Dodson. 1965. “Predation, Body Size, and Composition of Plankton: The Effect of a Marine Planktivore on Lake Plankton Illustrates Theory of Size, Competition, and Predation.” Science 150(3692): 28–35.
Brustel, H. 2004. “Coléoptères Saproxyliques et Valeur Biologique des Forêts Françaises [Saproxylic Beetles and Biological Value of FRENCH Forests].” PhD thesis, National Forest Office. 301 p.
Burner, R. C., L. Drag, J. G. Stephan, T. Birkemoe, R. Wetherbee, J. Muller, J. Siitonen, et al. 2022. “Functional Structure of European Forest Beetle Communities Is Enhanced by Rare Species.” Biological Conservation 267: 109491.
Burner, R. C., J. G. Stephan, L. Drag, T. Birkemoe, J. Muller, T. Snäll, O. Ovaskainen, et al. 2021. “Traits Mediate Niches and Co-Occurrences of Forest Beetles in Ways that Differ among Bioclimatic Regions.” Journal of Biogeography 48(12): 3145–3157.
Ceja-Navarro, J. A., U. Karaoz, M. Bill, Z. Hao, R. A. White, III, A. Arellano, L. Ramanculova, et al. 2019. “Gut Anatomical Properties and Microbial Functional Assembly Promote Lignocellulose Deconstruction and Colony Subsistence of a Wood-Feeding Beetle.” Nature Microbiology 4(5): 864–875.
Cognato, A. I., J. Hulcr, S. A. Dole, and B. H. Jordal. 2011. “Phylogeny of Haplo–Diploid, Fungus-Growing Ambrosia Beetles (Curculionidae: Scolytinae: Xyleborini) Inferred from Molecular and Morphological Data.” Zoologica Scripta 40(2): 174–186.
Colman, D. R., E. C. Toolson, and C. D. Takacs-Vesbach. 2012. “Do Diet and Taxonomy Influence Insect Gut Bacterial Communities?” Molecular Ecology 21(20): 5124–5137.
Cullen, L. E., and C. MacFarlane. 2005. “Comparison of Cellulose Extraction Methods for Analysis of Stable Isotope Ratios of Carbon and Oxygen in Plant Material.” Tree Physiology 25(5): 563–569.
Dodds, K. J., C. Graber, and F. M. Stephen. 2001. “Facultative Intraguild Predation by Larval Cerambycidae (Coleoptera) on Bark Beetle Larvae (Coleoptera: Scolytidae).” Environmental Entomology 30(1): 17–22.
Drag, L., R. C. Burner, J. G. Stephan, T. Birkemoe, I. Doerfler, M. M. Gossner, P. Magdon, et al. 2023. “High-Resolution 3D Forest Structure Explains Ecomorphological Trait Variation in Assemblages of Saproxylic Beetles.” Functional Ecology 37(1): 150–161.
Eberl, F., M. Fernandez de Bobadilla, M. Reichelt, A. Hammerbacher, J. Gershenzon, and S. B. Unsicker. 2020. “Herbivory Meets Fungivory: Insect Herbivores Feed on Plant Pathogenic Fungi for Their Own Benefit.” Ecology Letters 23(7): 1073–1084.
Elser, J. J., W. F. Fagan, R. F. Denno, D. R. Dobberfuhl, A. Folarin, A. Huberty, S. Interlandi, et al. 2000. “Nutritional Constraints in Terrestrial and Freshwater Food Webs.” Nature 408(6812): 578–580.
Falqueto, S. A., J. R. de Sousa, R. C. da Silva, G. F. da Silva, D. G. Pinheiro, and M. A. Soares. 2022. “Larval Gut Microbiome of Pelidnota luridipes (Coleoptera: Scarabaeidae): High Bacterial Diversity, Different Metabolic Profiles on Gut Chambers and Species with Probiotic Potential.” World Journal of Microbiology and Biotechnology 38(11): 210.
Filipiak, M. 2018. “Nutrient Dynamics in Decomposing Dead Wood in the Context of Wood Eater Requirements: The Ecological Stoichiometry of Saproxylophagous Insects.” In Saproxylic Insects. Diversity, Ecology and Conservation, edited by M. D. Ulyshen, 429–469. Cham: Springer International Publishing. https://doi.org/10.1007/978-3-319-75937-1_13.
Filipiak, M., Ł. Sobczyk, and J. Weiner. 2016. “Fungal Transformation of Tree Stumps into a Suitable Resource for Xylophagous Beetles Via Changes in Elemental Ratios.” Insects 7(2): 13. https://doi.org/10.3390/insects7020013.
Filipiak, M., and J. Weiner. 2014. “How to Make a Beetle out of Wood: Multi-Elemental Stoichiometry of Wood Decay, Xylophagy and Fungivory.” PLoS One 9(12): e115104.
Filipiak, M., and J. Weiner. 2017. “Nutritional Dynamics during the Development of Xylophagous Beetles Related to Changes in the Stoichiometry of 11 Elements.” Physiological Entomology 42(1): 73–84. https://doi.org/10.1111/phen.12168.
Fridman, J., and M. Walheim. 2000. “Amount, Structure, and Dynamics of Dead Wood on Managed Forestland in Sweden.” Forest Ecology and Management 131(1–3): 23–36.
Gallardo, P., and A. M. Cárdenas. 2016. “Long-Term Monitoring of Saproxylic Beetles from Mediterranean Oak Forests: An Approach to the Larval Biology of the Most Representative Species.” Journal of Insect Conservation 20(6): 999–1009.
Gessler, A., J. P. Ferrio, R. Hommel, K. Treydte, R. A. Werner, and R. K. Monson. 2014. “Stable Isotopes in Tree Rings: Towards a Mechanistic Understanding of Isotope Fractionation and Mixing Processes from the Leaves to the Wood.” Tree Physiology 34(8): 796–818.
Gimmel, M. L., and M. L. Ferro. 2018. “General Overview of Saproxylic Coleoptera.” In Saproxylic Insects. Zoological Monographs, Vol. 1, edited by M. Ulyshen. Cham: Springer. https://doi.org/10.1007/978-3-319-75937-1_2.
Gouix, N., J. Mertlik, A. Jarzabek-Müller, T. Németh, and H. Brustel. 2012. “Known Status of the Endangered Western Palaearctic Violet Click Beetle (Limoniscus violaceus) (Coleoptera).” Journal of Natural History 46: 769–802. https://doi.org/10.1080/00222933.2011.651639.
Gratton, C., and A. E. Forbes. 2006. “Changes in δ13C Stable Isotopes in Multiple Tissues of Insect Predators Fed Isotopically Distinct Prey.” Oecologia 147: 615–624.
Grove, S. J. 2002. “Saproxylic Insect Ecology and the Sustainable Management of Forests.” Annual Review of Ecology and Systematics 33(1): 1–23.
Grundler, M. R., E. R. Pianka, N. Pelegrin, M. A. Cowan, and D. L. Rabosky. 2017. “Stable Isotope Ecology of a Hyper-Diverse Community of Scincid Lizards from Arid Australia.” PLoS One 12(2): e0172879.
Hagen, E. M., K. E. McCluney, K. A. Wyant, C. U. Soykan, A. C. Keller, K. C. Luttermoser, E. J. Holmes, J. C. Moore, and J. L. Sabo. 2012. “A Meta-Analysis of the Effects of Detritus on Primary Producers and Consumers in Marine, Freshwater, and Terrestrial Ecosystems.” Oikos 121(10): 1507–1515.
Hagge, J., J. Müller, T. Birkemoe, J. Buse, M. M. Gossner, A. Gruppe, C. Heibl, et al. 2021. “What Does a Threatened Saproxylic Beetle Look like? Modelling Extinction Risk Using a New Morphological Trait Database.” The Journal of Animal Ecology 90(8): 1934–1947.
Harrington, T. C. 2005. “Ecology and Evolution of Mycophagous Bark Beetles and their Fungal Partners.” In Insect-Fungal Associations: Ecology and Evolution, edited by F. E. Vega and M. Blackwell, 257–291. Oxford: Oxford University Press.
Harvey, D. J., and A. C. Gange. 2003. “The Private Life of the Stag Beetle.” The Bulletin of the Amateur Entomologists' Society 62: 240–244.
Heethoff, M., and S. Scheu. 2016. “Reliability of Isotopic Fractionation (Δ15N, Δ13C) for the Delimitation of Trophic Levels of Oribatid Mites: Diet Strongly Affects Δ13C but Not Δ15N.” Soil Biology and Biochemistry 101: 124–129.
Hellemans, S., J. Šobotník, G. Lepoint, M. Mihaljevič, Y. Roisin, and T. Bourguignon. 2022. “Termite Dispersal Is Influenced by their Diet.” Proceedings of the Royal Society B 289(1975): 20220246.
Hope Jahren, A. 2004. “The Carbon Stable Isotope Composition of Pollen.” Review of Palaeobotany and Palynology 132(3–4): 291–313.
Hothorn, T., F. Bretz, P. Westfall, R. M. Heiberger, A. Schuetzenmeister, S. Scheibe, and M. T. Hothorn. 2016. Package ‘multcomp’. Simultaneous Inference in General Parametric Models. Vienna: Project for Statistical Computing.
Hunt, T., J. Bergsten, Z. Levkanicova, A. Papadopoulou, O. S. John, R. Wild, P. M. Hammond, et al. 2007. “A Comprehensive Phylogeny of Beetles Reveals the Evolutionary Origins of a Superradiation.” Science 318(5858): 1913–1916.
Hůrka, K. 2017. Beetles of the Czech and Slovak Republics 1–390. Zlín: Kabourek.
Hyodo, F. 2015. “Use of Stable Carbon and Nitrogen Isotopes in Insect Trophic Ecology.” Entomological Science 18(3): 295–312.
Hyodo, F., T. Matsumoto, Y. Takematsu, and T. Itioka. 2015. “Dependence of Diverse Consumers on Detritus in a Tropical Rain Forest Food Web as Revealed by Radiocarbon Analysis.” Functional Ecology 29(3): 423–429.
Ikeda, H., K. Kubota, T. Kagaya, and T. Abe. 2006. “Niche Differentiation of Burying Beetles (Coleoptera: Silphidae: Nicrophorinae) in Carcass Use in Relation to Body Size: Estimation from Stable Isotope Analysis.” Applied Entomology and Zoology 41(4): 561–564.
Jabot, F., C. Giraldo, S. Lefebvre, and S. Dubois. 2017. “Are Food Web Structures Well Represented in Isotopic Spaces?” Functional Ecology 31(10): 1975–1984. https://doi.org/10.1111/1365-2435.12895.
Jackson, A. L., R. Inger, A. C. Parnell, and S. Bearhop. 2011. “Comparing Isotopic Niche Widths among and within Communities: SIBER–Stable Isotope Bayesian Ellipses in R.” Journal of Animal Ecology 80(3): 595–602.
Jacobsen, R. M., H. Kauserud, A. Sverdrup-Thygeson, M. M. Bjorbækmo, and T. Birkemoe. 2017. “Wood-Inhabiting Insects Can Function as Targeted Vectors for Decomposer Fungi.” Fungal Ecology 29: 76–84.
Johnston, S. R., L. Boddy, and A. J. Weightman. 2016. “Bacteria in Decomposing Wood and their Interactions with Wood-Decay Fungi.” FEMS Microbiology Ecology 92(11): fiw179.
Jonsson, B. G., and N. Kruys. 2001. Ecology of Woody Debris in Boreal Forest. Oxford: Blackwell Publishing.
Keeling, C. I., M. M. Yuen, N. Y. Liao, T. Roderick Docking, S. K. Chan, G. A. Taylor, D. L. Palmquist, et al. 2013. “Draft Genome of the Mountain Pine Beetle, Dendroctonus ponderosae Hopkins, a Major Forest Pest.” Genome Biology 14: 1–20.
Köhler, F. 2000. Totholzkäfer in Naturwaldzellen des nördlichen Rheinlands 352. Recklinghausen: Landesanstalt für Ökologie, Bodenordnung und Forsten/Landesamt für Agrarordnung NRW, LÖBF-Schriftereihe, Band 18.
Kozel, P., B. Lejeune, G. Lepoint, L. Drag, L. Cizek, and P. Sebek. 2025. “Kozel_et_al_Stable Isotopes of Saproxylic Beetles_data.” figshare. Dataset. https://doi.org/10.6084/m9.figshare.28172060.v1.
Kozel, P., P. Sebek, M. Platek, J. Benes, M. Zapletal, M. Dvorsky, V. Lanta, et al. 2021. “Connectivity and Succession of Open Structures as a Key to Sustaining Light-Demanding Biodiversity in Deciduous Forests.” Journal of Applied Ecology 58(12): 2951–2961.
Kukor, J. J., and M. M. Martin. 1983. “Acquisition of Digestive Enzymes by Siricid Woodwasps from their Fungal Symbiont.” Science 220(4602): 1161–1163. https://doi.org/10.1126/science.220.4602.1161.
Kupferschmid Albisetti, A. D., P. Brang, W. Schönenberger, and H. Bugmann. 2003. “Decay of Picea abies Snag Stands on Steep Mountain Slopes.” The Forestry Chronicle 79(2): 247–252.
Larsen, T., M. Ventura, K. Maraldo, X. Triadó-Margarit, E. O. Casamayor, Y. V. Wang, N. Andersen, and D. M. O'Brien. 2016. “The Dominant Detritus-Feeding Invertebrate in Arctic Peat Soils Derives Its Essential Amino Acids from Gut Symbionts.” Journal of Animal Ecology 85(5): 1275–1285.
Layman, C. A., D. A. Arrington, C. G. Montaña, and D. M. Post. 2007. “Can Stable Isotope Ratios Provide for Community-Wide Measures of Trophic Structure?” Ecology 88: 42–48.
Lehenberger, M., N. Foh, A. Göttlein, D. Six, and P. H. Biedermann. 2021. “Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched with Biologically Important Elements.” Frontiers in Microbiology 12: 664542.
Lejeune, B., L. Bissey, E. A. Didaskalou, N. Sturaro, G. Lepoint, and M. Denoël. 2021. “Progenesis as an Intrinsic Factor of Ecological Opportunity in a Polyphenic Amphibian.” Functional Ecology 35(2): 546–560.
Lejeune, B., N. Sturaro, G. Lepoint, and M. Denoël. 2018. “Facultative Paedomorphosis as a Mechanism Promoting Intraspecific Niche Differentiation.” Oikos 127: 427–439.
Leschen, R. A. B., and R. G. Beutel. 2014. Handbook of Zoology: Arthropoda: Insecta: Coleoptera, Beetles. Morphology and Systematics (Phytophaga), Vol. 3. Berlin: De Gruyter.
Lustenhouwer, N., D. S. Maynard, M. A. Bradford, D. L. Lindner, B. Oberle, A. E. Zanne, and T. W. Crowther. 2020. “A Trait-Based Understanding of Wood Decomposition by Fungi.” Proceedings of the National Academy of Sciences of the United States of America 117(21): 11551–11558.
Malloch, D., and M. Blackwell. 1993. “Dispersal Biology of the Ophiostomatoid Fungi.” In Ceratocystes and Ophiostoma: Taxonomy, Ecology and Pathogenicity, edited by M. J. Wingfield, K. A. Seifert and J. F. Webber, 195–206. St. Paul, MN: APS Press.
Mayers, C. G., T. C. Harrington, and P. H. W. Biedermann. 2022. “Mycangia Define the Diverse Ambrosia Beetle–Fungus Symbioses.” In The Convergent Evolution of Agriculture in Humans and Insects 105–142. Cambridge: The MIT Press.
McCutchan, J. H., Jr., W. M. Lewis, Jr., C. Kendall, and C. C. McGrath. 2003. “Variation in Trophic Shift for Stable Isotope Ratios of Carbon, Nitrogen, and Sulfur.” Oikos 102(2): 378–390.
McKenna, D. D., E. D. Scully, Y. Pauchet, K. Hoover, R. Kirsch, S. M. Geib, R. F. Mitchell, et al. 2016. “Genome of the Asian Longhorned Beetle (Anoplophora glabripennis), a Globally Significant Invasive Species, Reveals Key Functional and Evolutionary Innovations at the Beetle–Plant Interface.” Genome Biology 17(1): 227.
Micó, E., P. Ramilo, S. Thorn, J. Müller, E. Galante, and C. P. Carmona. 2020. “Contrasting Functional Structure of Saproxylic Beetle Assemblages Associated to Different Microhabitats.” Scientific Reports 10(1): 1–11.
Moore, J. C., E. L. Berlow, D. C. Coleman, P. C. de Ruiter, Q. Dong, A. Hastings, N. C. Johnson, et al. 2004. “Detritus, Trophic Dynamics and Biodiversity.” Ecology Letters 7(7): 584–600.
Mooshammer, M., W. Wanek, S. Zechmeister-Boltenstern, and A. A. Richter. 2014. “Stoichiometric Imbalances between Terrestrial Decomposer Communities and their Resources: Mechanisms and Implications of Microbial Adaptations to their Resources.” Frontiers in Microbiology 5: 22.
Müller, D. W. H., D. Codron, C. Meloro, A. Munn, A. Schwarm, J. Hummel, and M. Clauss. 2013. “Assessing the Jarman–Bell Principle: Scaling of Intake, Digestibility, Retention Time and Gut Fill with Body Mass in Mammalian Herbivores.” Comparative Biochemistry and Physiology Part A 164(1): 129–140. https://doi.org/10.1016/j.cbpa.2012.09.018.
Newsome, S. D., C. Martinez del Rio, S. Bearhop, and D. L. Phillips. 2007. “A Niche for Isotope Ecology.” Frontiers in Ecology and the Environment 5: 429–436. https://doi.org/10.1890/060150.01.
Novák, V. 2014. Beetles of the Family Tenebrionidae of Central Europe. Praha: Academia.
Owen-Smith, R. N. 1988. Megaherbivores. The Influence of Very Large Body Size on Ecology, Cambridge Studies in Ecology. Cambridge: Cambridge University Press.
Pan, Y., R. A. Birdsey, J. Fang, R. Houghton, P. E.Kauppi, W. A.Kurz, O. Phillips, et al. 2011. “A Large and Persistent Carbon Sink in the World’s Forests.” Science 333(6045): 988–993.
Paradis, E., and K. Schliep. 2019. “Ape 5.0: An Environment for Modern Phylogenetics and Evolutionary Analyses in R.” Bioinformatics 35(3): 526–528.
Pérez-Sánchez, D., E. Galante, and E. Micó. 2020. “Functional and Taxonomic Beta Diversity of Saproxylic Beetles in Mediterranean Forests: On What Factors Do They Depend?” Environmental Entomology 49(3): 615–626.
Pichler, V., M. Homolak, W. Skierucha, M. Pichlerova, D. Ramirez, J. Gregor, and P. Jaloviar. 2012. “Variability of Moisture in Coarse Woody Debris from Several Ecologically Important Tree Species of the Temperate Zone of Europe.” Ecohydrology 5(4): 424–434.
Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, and R Core Team. 2020. “nlme: Linear and Nonlinear Mixed Effects Models.” R Package Version 3.1-145.
Polis, G. A., and D. R. Strong. 1996. “Food Web Complexity and Community Dynamics.” The American Naturalist 147(5): 813–846.
Pollierer, M. M., T. Larsen, A. Potapov, A. Brückner, M. Heethoff, J. Dyckmans, and S. Scheu. 2019. “Compound-Specific Isotope Analysis of Amino Acids as a New Tool to Uncover Trophic Chains in Soil Food Webs.” Ecological Monographs 89(4): e01384.
Pollierer, M. M., and S. Scheu. 2021. “Stable Isotopes of Amino Acids Indicate that Soil Decomposer Microarthropods Predominantly Feed on Saprotrophic Fungi.” Ecosphere 12: e03425.
Post, D. M. 2002. “Using Stable Isotopes to Estimate Trophic Position: Models, Methods, and Assumptions.” Ecology 83(3): 703–718.
Potapov, A. A., E. E. Semenina, A. Y. Korotkevich, N. A. Kuznetsova, and A. V. Tiunov. 2016. “Connecting Taxonomy and Ecology: Trophic Niches of Collembolans as Related to Taxonomic Identity and Life Forms.” Soil Biology and Biochemistry 101: 20–31.
Potapov, A. M., S. Scheu, and A. V. Tiunov. 2019. “Trophic Consistency of Supraspecific Taxa in Below-Ground Invertebrate Communities: Comparison across Lineages and Taxonomic Ranks.” Functional Ecology 33(6): 1172–1183.
Potapov, A. M., A. V. Tiunov, and S. Scheu. 2019. “Uncovering Trophic Positions and Food Resources of Soil Animals Using Bulk Natural Stable Isotope Composition.” Biological Reviews 94(1): 37–59.
Přikryl, Z. B., M. Turčáni, and J. Horák. 2012. “Sharing the Same Space: Foraging Behaviour of Saproxylic Beetles in Relation to Dietary Components of Morphologically Similar Larvae.” Ecological Entomology 37(2): 117–123.
R Core Team. 2021. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.
Schallhart, N., C. Wallinger, A. Juen, and M. Traugott. 2009. “Dispersal Abilities of Adult Click Beetles in Arable Land Revealed by Analysis of Carbon Stable Isotopes.” Agricultural and Forest Entomology 11(3): 333–339.
Scheu, S., and M. Falca. 2000. “The Soil Food Web of Two Beech Forests (Fagus sylvatica) of Contrasting Humus Type: Stable Isotope Analysis of a Macro-and a Mesofauna-Dominated Community.” Oecologia 123: 285–296.
Seibold, S., R. Brandl, J. Buse, T. Hothorn, J. Schmidl, S. Thorn, and J. Müller. 2015. “Association of Extinction Risk of Saproxylic Beetles with Ecological Degradation of Forests in Europe.” Conservation Biology 29(2): 382–390.
Seibold, S., J. Müller, S. Allner, M. Willner, P. Baldrian, M. D. Ulyshen, R. Brandl, C. Bässler, J. Hagge, and O. Mitesser. 2022. “Quantifying Wood Decomposition by Insects and Fungi Using Computed Tomography Scanning and Machine Learning.” Scientific Reports 12(1): 1–12.
Seibold, S., W. Rammer, T. Hothorn, R. Seidl, M. D. Ulyshen, J. Lorz, M. W. Cadotte, et al. 2021. “The Contribution of Insects to Global Forest Deadwood Decomposition.” Nature 597(7874): 77–81.
Six, D. L., and J. J. Elser. 2020. “Mutualism Is Not Restricted to Tree-Killing Bark Beetles and Fungi: The Ecological Stoichiometry of Secondary Bark Beetles, Fungi, and a Scavenger.” Ecological Entomology 45(5): 1134–1145.
Skelton, J., A.Loyd,J. A. Smith, R. A. Blanchette, B. W. Held, andJ. Hulcr. 2020. “Fungal Symbionts of Bark and Ambrosia Beetles Can Suppress Decomposition of Pine Sapwood by Competing with Wood-Decay Fungi.” Fungal Ecology 45: 100926.
Sláma, M. E. F. 1998. Longhorn Beetles—Cerambycidae of the Czech Republic and Slovak Republic (Beetles-Coleoptera). Krhanice: Author.
Steffan, S. A., Y. Chikaraishi, C. R. Currie, H. Horn, H. R. Gaines-Day, J. N. Pauli, J. E. Zalapa, and N. Ohkouchi. 2015. “Microbes Are Trophic Analogs of Animals.” Proceedings of the National Academy of Sciences of the United States of America 112(49): 15119–15124.
Steffan, S. A., Y. Chikaraishi, P. S. Dharampal, J. N. Pauli, C. Guédot, and N. Ohkouchi. 2017. “Unpacking Brown Food-Webs: Animal Trophic Identity Reflects Rampant Microbivory.” Ecology and Evolution 7(10): 3532–3541.
Stokland, J. N., J. Siitonen, and B. G. Jonsson. 2012. Biodiversity in Deadwood. Cambridge: Cambridge University Press.
Tallamy, D. W., and J. D. Pesek. 1996. “Carbon Isotopic Signatures of Elytra Reflect Larval Diet in Luperine Rootworms (Coleoptera: Chrysomelidae).” Environmental Entomology 25(5): 1167–1172.
Tanahashi, M., and C. J. Hawes. 2016. “The Presence of a Mycangium in European Sinodendron cylindricum (Coleoptera: Lucanidae) and the Associated Yeast Symbionts.” Journal of Insect Science 16(1): 76.
Tanahashi, M., K. Kubota, N. Matsushita, and K. Togashi. 2010. “Discovery of Mycangia and the Associated Xylose-Fermenting Yeasts in Stag Beetles (Coleoptera: Lucanidae).” Naturwissenschaften 97(3): 311–317.
Tanahashi, M., N. Matsushita, and K. Togashi. 2009. “Are Stag Beetles Fungivorous?” Journal of Insect Physiology 55(11): 983–988.
Tayasu, I., F. Hyodo, T. Abe, T. Inoue, and A. V. Spain. 2002. “Nitrogen and Carbon Stable Isotope Ratios in the Sympatric Australian Termites, Amitermes laurensis and Drepanotermes rubriceps (Isoptera: Termitidae) in Relation to Their Feeding Habits and the Quality of their Food Materials.” Soil Biology and Biochemistry 34(3): 297–301.
Tedersoo, L., T. Naadel, M. Bahram, K. Pritsch, F. Buegger, M. Leal, U. Kõljalg, and K. Põldmaa. 2012. “Enzymatic Activities and Stable Isotope Patterns of Ectomycorrhizal Fungi in Relation to Phylogeny and Exploration Types in an Afrotropical Rain Forest.” New Phytologist 195(4): 832–843.
Thompson, B. M., J. Bodart, C. McEwen, and D. S. Gruner. 2014. “Adaptations for Symbiont-Mediated External Digestion in Sirex noctilio (Hymenoptera: Siricidae).” Annals of the Entomological Society of America 107(2): 453–460.
Tiunov, A. V. 2007. “Stable Isotopes of Carbon and Nitrogen in Soil Ecological Studies.” Biology Bulletin 34: 395–407.
Tuo, B., Y.-K. Hu, R. S. P. van Logtestijn, J. Zuo, L. Goudzwaard, M. M. Hefting, M. P. Berg, and J. H. C. Cornelissen. 2024. “Facilitation: Isotopic Evidence that Wood-Boring Beetles Drive the Trophic Diversity of Secondary Decomposers.” Soil Biology and Biochemistry 192: 109353.
Ulyshen, M. D. 2015. “Insect-Mediated Nitrogen Dynamics in Decomposing Wood.” Ecological Entomology 40: 97–112.
Ulyshen, M. D., ed. 2018. Saproxylic Insects: Diversity, Ecology and Conservation. Heidelberg: Springer.
Vega, F. E., and P. F. Dowd. 2005. “The Role of Yeasts as Insect Endosymbionts.” In Insect-Fungal Associations: Ecology and Evolution 211–243. New York: Oxford University Press.
Ware, V. L., and F. M. Stephen. 2006. “Facultative Intraguild Predation of Red Oak Borer Larvae (Coleoptera: Cerambycidae).” Environmental Entomology 35(2): 443–447. https://doi.org/10.1603/0046-225X-35.2.443.
Whitehead, P. F. 2003. “Current knowledge of the Violet Click Beetle Limoniscus violaceus (P. W. J. Müller. 1821) (Col., Elateridae) in Britain.” In Proceedings of the Second Pan-European Conference on Saproxylic Beetles, 57–65. Royal Holloway: People's Trust for Endangered Species, University of London.
Zhang, J., and J. J. Elser. 2017. “Carbon: Nitrogen: Phosphorus Stoichiometry in Fungi: A Meta-Analysis.” Frontiers in Microbiology 8: 1281.