Advertisement

Nutrient Dynamics in Decomposing Dead Wood in the Context of Wood Eater Requirements: The Ecological Stoichiometry of Saproxylophagous Insects

  • Michał Filipiak
Chapter
Part of the Zoological Monographs book series (ZM, volume 1)

Abstract

Dead wood is rich in sugars and can serve as an energy source when digested, but it lacks other nutrients, preventing the growth, development, and maturation of saproxylophages (saproxylic organisms that consume dead wood at any stage of decomposition). Split into atoms, sugars only serve as a source of carbon, hydrogen, and oxygen, thereby providing insufficient nutrition for saproxylophages and for their digestive tract symbionts, despite the ability of certain symbionts to assimilate nitrogen directly from the air. Ecological stoichiometry framework was applied to understand how nutritional scarcity shapes saproxylophage-dead wood interactions. Dead wood is 1–3 orders of magnitude inadequate in biologically essential elements (N, P, K, Na, Mg, Zn, and Cu), compared to requirements of its consumers, preventing the production of necessary organic compounds, thus limiting saproxylophages’ growth, development, and maintenance. However, the wood is nutritionally unstable. During decomposition, concentrations of the biologically essential elements increase promoting saproxylophage development. Three mechanisms contribute to the nutrient dynamics in dead wood: (1) C loss, which increases the concentration of other essential elements, (2) N fixation by prokaryotes, and (3) fungal transport of outside nutrients. Prokaryotic N fixation partially mitigates the limitations on saproxylophages by the scarcity of N, often the most limiting nutrient, but co-limitation by seven elements (N, P, K, Na, Mg, Zn, and Cu) may occur. Fungal transport can shape nutrient dynamics early in wood decay, rearranging extremely scarce nutritional composition of dead wood environment during its initial stage of decomposition and assisting saproxylophage growth and development. This transport considerably alters the relative and total amounts of non-C elements, mitigating also nutritional constraints experienced by saproxylophages inhabiting such nutritionally enriched wood during later stages of decomposition. Additionally, C losses during later decomposition stages may further change non-C element concentrations beyond fungal enrichment. More detailed studies of the short-term nutrient dynamics in dead wood relative to the nutritional requirements of saproxylophages are needed to understand decomposition process and nutrient cycling in ecosystems. These studies should include a wide array of elements that may be limiting for saproxylophages (e.g., P, Na, K, Mg, Zn, and Cu in addition to commonly studied N). Studies on nutrient dynamics in dead wood should discuss obtained data in the context of nutritional needs of saproxylophages. To allow for this, data on multielemental ecological stoichiometry of saproxylophages of various taxa, inhabiting different wood species in various geographical locations, are needed.

Notes

Acknowledgments

I am indebted to Michael Ulyshen, Zuzanna Świątek, and the anonymous reviewers for their constructive comments that greatly improved an earlier version of this manuscript. I also thank Maciej Filipiak for his help creating the graphics. English language editing was performed by American Journal Experts (AJE.com).

This study was supported by the Polish Ministry of Science and Higher Education (Grant No. DS/WBiNoZ/INoŚ/DS 761) and the National Science Centre of Poland (Grant No. DEC 2013/11/N/NZ8/00929).

References

  1. Aho PE (1974) Distribution, enumeration, and identification of nitrogen-fixing bacteria associated with decay in living White Fir trees. Phytopathology 64:1413–1420.  https://doi.org/10.1094/Phyto-64-1413CrossRefGoogle Scholar
  2. Atkinson CL, Capps KA, Rugenski AT, Vanni MJ (2016) Consumer-driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems. Biol Rev.  https://doi.org/10.1111/brv.12318
  3. Baldrian P (2017) Forest microbiome: diversity, complexity and dynamics. FEMS Microbiol Rev 41:109–130.  https://doi.org/10.1093/femsre/fuw040CrossRefPubMedGoogle Scholar
  4. Becker G (1965) Versuche über den Einfluss von braunfaulepilzen auf Wahl und Ausnutzung der holznährung durch Termiten. Mater Organ 1:95–156Google Scholar
  5. Bignell DE, Roisin Y, Lo N (eds) (2011) Biology of termites: a modern synthesis. Springer Netherlands, DordrechtGoogle Scholar
  6. Boddy L, Watkinson SC (1995) Wood decomposition, higher fungi, and their role in nutrient redistribution. Can J Bot 73:1377–1383.  https://doi.org/10.1139/b95-400CrossRefGoogle Scholar
  7. Bouchard P, Grebennikov VV, Smith ABT, Douglas H (2009) Biodiversity of Coleoptera. In: Foottit RG, Adler PH (eds) Insect biodiversity: science and society. Wiley-Blackwell, Oxford, UK, pp 265–301CrossRefGoogle Scholar
  8. Bridges JR (1981) Nitrogen-fixing bacteria associated with bark beetles. Microb Ecol 7:131–137.  https://doi.org/10.1007/BF02032495CrossRefPubMedGoogle Scholar
  9. Burford EP, Fomina M, Gadd GM (2003) Fungal involvement in bioweathering and biotransformation of rocks and minerals. Miner Mag 67:1127–1155.  https://doi.org/10.1180/0026461036760154CrossRefGoogle Scholar
  10. Cairney JWG (2005) Basidiomycete mycelia in forest soils: dimensions, dynamics and roles in nutrient distribution. Mycol Res 109:7–20.  https://doi.org/10.1017/S0953756204001753CrossRefPubMedGoogle Scholar
  11. Čapek P, Kotas P, Manzoni S, Šantrůčková H (2016) Drivers of phosphorus limitation across soil microbial communities. Funct Ecol 30:1705–1713.  https://doi.org/10.1111/1365-2435.12650CrossRefGoogle Scholar
  12. Chen Y, Forschler BT (2016) Elemental concentrations in the frass of saproxylic insects suggest a role in micronutrient cycling. Ecosphere 7:e01300.  https://doi.org/10.1002/ecs2.1300CrossRefGoogle Scholar
  13. Cherif M (2012) Biological stoichiometry: the elements at the heart of biological interactions. In: Innocenti A (ed) Stoichiometry and research-the importance of quantity in biomedicine. InTech, Rijeka, pp 357–376Google Scholar
  14. Cherif M, Loreau M (2013) Plant-herbivore-decomposer stoichiometric mismatches and nutrient cycling in ecosystems. Proc Biol Sci 280:20122453.  https://doi.org/10.1098/rspb.2012.2453CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cherif M, Faithfull C, Guo J, Meunier CL, Sitters J, Uszko W, Rivera Vasconcelos F (2017) An operational framework for the advancement of a molecule-to-biosphere stoichiometry theory. Front Mar Sci 4:1–16.  https://doi.org/10.3389/fmars.2017.00286CrossRefGoogle Scholar
  16. Clinton PW, Buchanan PK, Wilkie JP, Smaill SJ, Kimberley MO (2009) Decomposition of Nothofagus wood in vitro and nutrient mobilization by fungi. Can J For Res 39:2193–2202.  https://doi.org/10.1139/X09-134CrossRefGoogle Scholar
  17. Clymans W, Conley DJ, Battles JJ, Frings PJ, Koppers MM, Likens GE, Johnson CE (2016) Silica uptake and release in live and decaying biomass in a northern hardwood forest. Ecology 97:3044–3057.  https://doi.org/10.1002/ecy.1542CrossRefPubMedGoogle Scholar
  18. Cohen AC (2003) Insect diets: science and technology. CRC, New YorkCrossRefGoogle Scholar
  19. Cowling EB, Merrill W (1966) Nitrogen in wood and its role in wood deterioration. Can J Bot 44:1539–1554.  https://doi.org/10.1139/b66-167CrossRefGoogle Scholar
  20. Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, Alma A, Sacchi L, Bourtzis K, Mandrioli M, Cherif A, Bandi C, Daffonchio D (2010) Acetic acid bacteria, newly emerging symbionts of insects. Appl Environ Microbiol 76:6963–6970.  https://doi.org/10.1128/AEM.01336-10CrossRefPubMedPubMedCentralGoogle Scholar
  21. Danger M, Arce Funck JA, Devin S, Heberle J, Felten V (2013) Phosphorus content in detritus controls life-history traits of a detritivore. Funct Ecol 27:807–815.  https://doi.org/10.1111/1365-2435.12079CrossRefGoogle Scholar
  22. Denno RF, Fagan WF (2003) Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology 84:2522–2531.  https://doi.org/10.1890/02-0370CrossRefGoogle Scholar
  23. Dighton J (2003) Fungi in ecosystem processes, 2nd edn. CRC, New YorkCrossRefGoogle Scholar
  24. Dighton J (2007) Nutrient cycling by saprotrophic fungi in terrestrial habitats. In: Kubicek CP, Druzhinina IS (eds) Environmental and microbial relationships. Springer, Berlin, pp 287–300Google Scholar
  25. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49:71–92.  https://doi.org/10.1146/annurev.ento.49.061802.123416CrossRefPubMedPubMedCentralGoogle Scholar
  26. Dodds KJ, Graber C, Stephen FM (2001) Facultative intraguild predation by larval Cerambycidae (Coleoptera) on bark beetle larvae (Coleoptera: Scolytidae). Environ Entomol 30:17–22.  https://doi.org/10.1603/0046-225X-30.1.17CrossRefGoogle Scholar
  27. Doi H, Cherif M, Iwabuchi T, Katano I, Stegen JC, Striebel M (2010) Integrating elements and energy through the metabolic dependencies of gross growth efficiency and the threshold elemental ratio. Oikos 119:752–765.  https://doi.org/10.1111/j.1600-0706.2009.18540.xCrossRefGoogle Scholar
  28. Dominik J, Starzyk JR (2004) Owady uszkadzające drewno (Wood damaging insects). PWRiL, WarsawGoogle Scholar
  29. Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23:38–47.  https://doi.org/10.1111/j.1365-2435.2008.01442.xCrossRefGoogle Scholar
  30. Elser JJ, Hamilton A (2007) Stoichiometry and the new biology: the future is now. PLoS Biol 5:e181.  https://doi.org/10.1371/journal.pbio.0050181CrossRefPubMedPubMedCentralGoogle Scholar
  31. Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–751.  https://doi.org/10.1890/0012-9658(1999)080[0735,TSOCDN]2.0.CO;2CrossRefGoogle Scholar
  32. Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N:P stoichiometry. BioScience 46:674–684.  https://doi.org/10.2307/1312897CrossRefGoogle Scholar
  33. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LW (2000a) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550.  https://doi.org/10.1046/j.1461-0248.2000.00185.xCrossRefGoogle Scholar
  34. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000b) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580.  https://doi.org/10.1038/35046058CrossRefPubMedGoogle Scholar
  35. Evans-White MA, Halvorson HM (2017) Comparing the ecological stoichiometry in green and brown food webs – a review and meta-analysis of freshwater food webs. Front Microbiol 8:1–14.  https://doi.org/10.3389/fmicb.2017.01184CrossRefGoogle Scholar
  36. Fagan WF, Denno RF (2004) Stoichiometry of actual vs. potential predator-prey interactions: insights into nitrogen limitation for arthropod predators. Ecol Lett 7:876–883.  https://doi.org/10.1111/j.1461-0248.2004.00641.xCrossRefGoogle Scholar
  37. Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ (2002) Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat 160:784–802.  https://doi.org/10.1086/343879CrossRefPubMedGoogle Scholar
  38. Filipiak M (2016) Pollen stoichiometry may influence detrital terrestrial and aquatic food webs. Front Ecol Evol 4:1–8.  https://doi.org/10.3389/fevo.2016.00138CrossRefGoogle Scholar
  39. Filipiak M, Weiner J (2014) How to make a beetle out of wood: multi-elemental stoichiometry of wood decay, xylophagy and fungivory. PLoS One 9:e115104.  https://doi.org/10.1371/journal.pone.0115104CrossRefPubMedPubMedCentralGoogle Scholar
  40. Filipiak M, Weiner J (2017a) Nutritional dynamics during the development of xylophagous beetles related to changes in the stoichiometry of 11 elements. Physiol Entomol 42:73–84.  https://doi.org/10.1111/phen.12168CrossRefGoogle Scholar
  41. Filipiak M, Weiner J (2017b) Plant-insect interactions: the role of ecological stoichiometry. Acta Agrobot 70:1–16.  https://doi.org/10.5586/aa.1710CrossRefGoogle Scholar
  42. Filipiak M, Sobczyk Ł, Weiner J (2016) Fungal transformation of tree stumps into a suitable resource for xylophagous beetles via changes in elemental ratios. Insects 7:13.  https://doi.org/10.3390/insects7020013CrossRefPubMedCentralGoogle Scholar
  43. Filipiak M, Kuszewska K, Asselman M, Denisow B, Stawiarz E, Woyciechowski M, Weiner J (2017) Ecological stoichiometry of the honeybee: pollen diversity and adequate species composition are needed to mitigate limitations imposed on the growth and development of bees by pollen quality. PLoS One 12(8):e0183236.  https://doi.org/10.1371/journal.pone.0183236CrossRefPubMedPubMedCentralGoogle Scholar
  44. Foster JR, Lang GE (1982) Decomposition of red spruce and balsam fir boles in the White Mountains of New Hampshire. Can J For Res 12:617–626.  https://doi.org/10.1139/x82-094CrossRefGoogle Scholar
  45. Fraústo da Silva JJR, Williams RJP (2001) The biological chemistry of the elements. The inorganic chemistry of life, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  46. Frost PC, Benstead JP, Cross WF, Hillebrand H, Larson JH, Xenopoulos MA, Yoshida T (2006) Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol Lett 9:774–779.  https://doi.org/10.1111/j.1461-0248.2006.00919.xCrossRefPubMedGoogle Scholar
  47. Fukasawa Y, Komagata Y, Kawakami S (2017) Nutrient mobilization by plasmodium of myxomycete Physarum rigidum in deadwood. Fungal Ecol 29:42–44.  https://doi.org/10.1016/j.funeco.2017.05.005CrossRefGoogle Scholar
  48. Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49.  https://doi.org/10.1016/j.mycres.2006.12.001CrossRefPubMedGoogle Scholar
  49. Gadd GM (2017a) The geomycology of elemental cycling and transformations in the environment. Microbiol Spectr 5:1–16.  https://doi.org/10.1128/microbiolspec.FUNK-0010-2016CrossRefGoogle Scholar
  50. Gadd GM (2017b) Geomycology: geoactive fungal roles in the biosphere. In: John J, White JF (eds) The fungal community. Mycology. CRC, Boca Raton, pp 119–136CrossRefGoogle Scholar
  51. Gadd GM, Rhee YJ, Stephenson K, Wei Z (2012) Geomycology: metals, actinides and biominerals. Environ Microbiol Rep 4:270–296.  https://doi.org/10.1111/j.1758-2229.2011.00283.xCrossRefPubMedGoogle Scholar
  52. Galbraith ED, Martiny AC (2015) A simple nutrient-dependence mechanism for predicting the stoichiometry of marine ecosystems. Proc Natl Acad Sci USA 112:8199–8204.  https://doi.org/10.1073/pnas.1423917112CrossRefPubMedPubMedCentralGoogle Scholar
  53. Gentry JB, Whitford WG (1982) The relationship between wood litter infall and relative abundance and feeding activity of subterranean termites Reticulitermes spp. in three southeastern coastal plain habitats. Oecologia 54:63–67.  https://doi.org/10.1007/BF00541109CrossRefPubMedGoogle Scholar
  54. Gonzalez AL, Dezérald O, Marquet PA, Romero GQ, Srivastaba DS (2017) The multidimensional stoichiometric niche. Front Ecol Evol.  https://doi.org/10.3389/fevo.2017.00110
  55. Grier CC (1978) A Tsuga heterophylla-Picea sitchensis ecosystem of coastal Oregon: decomposition and nutrient balances of fallen logs. Can J For Res 8:198–206.  https://doi.org/10.1139/x78-031CrossRefGoogle Scholar
  56. Grove SJ (2002) Saproxylic insect ecology and the sustainable management of forests. Annu Rev Ecol Syst 33:1–23.  https://doi.org/10.1146/annurev.ecolsys.33.010802.150507CrossRefGoogle Scholar
  57. Haack RA, Slansky FJ (1987) Nutritional ecology of wood feeding Coleoptera, Lepidoptera and Hymenoptera. In: Rodriguez JG, Slansky F (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, pp 449–486Google Scholar
  58. Hanula JL (1996) Relationship of wood-feeding insects and coarse woody debris. In: Forest Service, Southeastern Forest Experiment Station (eds) Biodiversity and coarse woody debris in Southern Forests. Department of Agriculture, US, Washington, DC, pp 55–81Google Scholar
  59. Harmon ME, Franklin JF, Swanson FJ, Sollins P, Gregory SV, Lattin JD, Anderson NH, Cline SP, Aumen NG, Sedell JR, Lienkaemper GW, Cromack K, Cummins KW (1986) Ecology of coarse woody debris in temperate ecosystems. Adv Ecol Res 15:133–302.  https://doi.org/10.1016/S0065-2504(08)60121-XCrossRefGoogle Scholar
  60. Hendee EC (1935) The role of fungi in the diet of the common damp-wood termite, Zootermopsis angusticollis. Hilgardia 9:499–525.  https://doi.org/10.3733/hilg.v09n10p499CrossRefGoogle Scholar
  61. Hessen DO, Elser JJ, Sterner RW, Urabe J (2013) Ecological stoichiometry: an elementary approach using basic principles. Limnol Oceanogr 58:2219–2236.  https://doi.org/10.4319/lo.2013.58.6.2219CrossRefGoogle Scholar
  62. Higashi M, Abe T, Burns TP (1992) Carbon-nitrogen balance and termite ecology. Proc R Soc Lond B Biol Sci 249:303–308.  https://doi.org/10.1098/rspb.1992.0119CrossRefGoogle Scholar
  63. Jeyasingh PD, Goos JM, Thompson SK, Godwin CM, Cotner JB (2017) Ecological stoichiometry beyond Redfield: an ionomic perspective on elemental homeostasis. Front Microbiol 8:(722).  https://doi.org/10.3389/fmicb.2017.00722
  64. Johnson CE, Siccama TG, Denny EG, Koppers MM, Vogt DJ (2014) In situ decomposition of northern hardwood tree boles: decay rates and nutrient dynamics in wood and bark. Can J For Res 44:1515–1524.  https://doi.org/10.1139/cjfr-2014-0221CrossRefGoogle Scholar
  65. Johnston SR, Boddy L, Weightman AJ (2016) Bacteria in decomposing wood and their interactions with wood-decay fungi. FEMS Microbiol Ecol 92:fiw179.  https://doi.org/10.1093/femsec/fiw179CrossRefPubMedGoogle Scholar
  66. Kaspari M, Powers JS (2016) Biogeochemistry and geographical ecology: embracing all twenty-five elements required to build organisms. Am Nat 188(Suppl 1):S62–SS73.  https://doi.org/10.1086/687576CrossRefPubMedGoogle Scholar
  67. Kaspari M, Yanoviak SP (2008) Biogeography of litter depth in tropical forests: evaluating the phosphorus growth rate hypothesis. Funct Ecol 22:919–923.  https://doi.org/10.1111/j.1365-2435.2008.01447.xCrossRefGoogle Scholar
  68. Kaspari M, Bujan J, Weiser MD, Ning D, Michaletz ST, Zhili H, Enquist BJ, Waide RB, Zhou J, Turner BL, Wright SJ (2017a) Biogeochemistry drives diversity in the prokaryotes, fungi, and invertebrates of a Panama forest. Ecology 98:2019–2028.  https://doi.org/10.1002/ecy.1895CrossRefPubMedGoogle Scholar
  69. Kaspari M, Roeder KA, Benson B, Weiser MD, Sanders NJ (2017b) Sodium co-limits and catalyzes macronutrients in a prairie food web. Ecology 98:315–320.  https://doi.org/10.1002/ecy.1677CrossRefPubMedGoogle Scholar
  70. Klausmeier CA, Litchman E, Daufresne T, Levin SA (2008) Phytoplankton stoichiometry. Ecol Res 23:479–485.  https://doi.org/10.1007/s11284-008-0470-8CrossRefGoogle Scholar
  71. Klironomos JN, Hart MM (2001) Food-web dynamics. animal nitrogen swap for plant carbon. Nature 410:651–652.  https://doi.org/10.1038/35070643CrossRefPubMedGoogle Scholar
  72. Kneip C, Lockhart P, Voss C, Maier UG (2007) Nitrogen fixation in eukaryotes – new models for symbiosis. BMC Evol Biol 7:55.  https://doi.org/10.1186/1471-2148-7-55CrossRefPubMedPubMedCentralGoogle Scholar
  73. Köster K, Metslaid M, Engelhart J, Köster E (2015) Dead wood basic density, and the concentration of carbon and nitrogen for main tree species in managed hemiboreal forests. For Ecol Manage 354:35–42.  https://doi.org/10.1016/j.foreco.2015.06.039CrossRefGoogle Scholar
  74. Kovoor J (1964) Modifications chimiques provoquées par un termitide Microcerotermes edentatus dans du bois de peuplier sain ou partiellement dégradé par des champignons. Bull Biol Fr Belg 98:491–509Google Scholar
  75. Laiho R, Prescott CE (2004) Decay and nutrient dynamics of coarse woody debris in northern coniferous forests: a synthesis. Can J For Res 34:763–777.  https://doi.org/10.1139/x03-241CrossRefGoogle Scholar
  76. Lambert RL, Lang GE, Reiners WA (1980) Loss of mass and chemical change in decaying boles of a subalpine balsam fir forest. Ecology 61:1460–1473.  https://doi.org/10.2307/1939054CrossRefGoogle Scholar
  77. Landvik M, Niemelä P, Roslin T (2016) Mother knows the best mould: an essential role for non-wood dietary components in the life cycle of a saproxylic scarab beetle. Oecologia 182:163–175.  https://doi.org/10.1007/s00442-016-3661-yCrossRefPubMedGoogle Scholar
  78. Lemoine NP, Giery ST, Burkepile DE (2014) Differing nutritional constraints of consumers across ecosystems. Oecologia 174:1367–1376.  https://doi.org/10.1007/s00442-013-2860-zCrossRefPubMedGoogle Scholar
  79. Li Z, Liu L, Chen J, Teng HH (2016) Cellular dissolution at hypha- and spore-mineral interfaces revealing unrecognized mechanisms and scales of fungal weathering. Geology 44:319–322.  https://doi.org/10.1130/G37561.1CrossRefGoogle Scholar
  80. Lilburn TG, Kim KS, Ostrom NE, Byzek KR, Leadbetter JR, Breznak JA (2001) Nitrogen fixation by symbiotic and free-living spirochetes. Science 292:2495–2498.  https://doi.org/10.1126/science.1060281CrossRefPubMedGoogle Scholar
  81. Liu D, Keiblinger KM, Leitner S, Mentler A, Zechmeister-Boltenstern S (2016) Is there a convergence of deciduous leaf litter stoichiometry, biochemistry and microbial population during decay? Geoderma 272:93–100.  https://doi.org/10.1016/j.geoderma.2016.03.005CrossRefGoogle Scholar
  82. Ljungdahl LG, Eriksson KE (1985) Ecology of microbial cellulose degradation. In: Marshall KC (ed) Advances in microbial ecology, vol 8. Springer US, New York, NY, pp 237–299CrossRefGoogle Scholar
  83. Lodge DJ (1987) Nutrient concentrations, percentage moisture and density of field-collected fungal mycelia. Soil Biol Biochem 19:727–733.  https://doi.org/10.1016/0038-0717(87)90055-1CrossRefGoogle Scholar
  84. Mansour K (1934) On the digestion of wood by insects. J Exp Biol 11:243–256Google Scholar
  85. Marleau JN, Guichard F, Loreau M (2015) Emergence of nutrient co-limitation through movement in stoichiometric meta-ecosystems. Ecol Lett 18:1163–1173.  https://doi.org/10.1111/ele.12495CrossRefPubMedGoogle Scholar
  86. Martin MM (1983) Cellulose digestion in insects. Comp Biochem Physiol A Physiol 75:313–324.  https://doi.org/10.1016/0300-9629(83)90088-9CrossRefGoogle Scholar
  87. Martin MM, Jones CG, Bernays EA (1991) The evolution of cellulose digestion in insects [and discussion]. Philos Trans R Soc Lond B Biol Sci 333:281–288.  https://doi.org/10.1098/rstb.1991.0078CrossRefGoogle Scholar
  88. Martinson HM, Schneider K, Gilbert J, Hines JE, Hambäck PA, Fagan WF (2008) Detritivory: stoichiometry of a neglected trophic level. Ecol Res 23:487–491.  https://doi.org/10.1007/s11284-008-0471-7CrossRefGoogle Scholar
  89. Meerts P (2002) Mineral nutrient concentrations in sapwood and heartwood: a literature review. Ann For Sci 59:713–722.  https://doi.org/10.1051/forest:2002059CrossRefGoogle Scholar
  90. Meunier CL, Boersma M, El-Sabaawi R, Halvorson HM, Herstoff EM, Van de Waal DB, Vogt RJ, Litchman E (2017) From elements to function: toward unifying ecological stoichiometry and trait-based ecology. Front Environ Sci 5:1–10.  https://doi.org/10.3389/fenvs.2017.00018CrossRefGoogle Scholar
  91. Moe SJ, Stelzer RS, Forman MR, Harpole WS, Daufresne T, Yoshida T (2005) Recent advances in ecological stoichiometry: insights for population and community ecology. Oikos 109:29–39.  https://doi.org/10.1111/j.0030-1299.2005.14056.xCrossRefGoogle Scholar
  92. Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 5:22.  https://doi.org/10.3389/fmicb.2014.00022CrossRefPubMedPubMedCentralGoogle Scholar
  93. Nadeau P, Thibault M, Horgan FG, Michaud J, Gandiaga F, Comeau C, Moreau G (2015) Decaying matters: Coleoptera involved in heterotrophic systems. In: Stack C (ed) Beetles: biodiversity, ecology and role in the environment. Nova Science, New York, pp 123–174Google Scholar
  94. Nardi JB, Mackie RI, Dawson JO (2002) Could microbial symbionts of arthropod guts contribute significantly to nitrogen fixation in terrestrial ecosystems? J Insect Physiol 48:751–763.  https://doi.org/10.1016/S0022-1910(02)00105-1CrossRefPubMedGoogle Scholar
  95. Palviainen M, Finér L (2015) Decomposition and nutrient release from Norway spruce coarse roots and stumps – a 40-year chronosequence study. For Ecol Manage 358:1–11.  https://doi.org/10.1016/j.foreco.2015.08.036CrossRefGoogle Scholar
  96. Palviainen M, Finér L, Laiho R, Shorohova E, Kapitsa E, Vanha-Majamaa I (2010a) Carbon and nitrogen release from decomposing Scots pine, Norway spruce and silver birch stumps. For Ecol Manage 259:390–398.  https://doi.org/10.1016/j.foreco.2009.10.034CrossRefGoogle Scholar
  97. Palviainen M, Finér L, Laiho R, Shorohova E, Kapitsa E, Vanha-Majamaa I (2010b) Phosphorus and base cation accumulation and release patterns in decomposing Scots pine, Norway spruce and silver birch stumps. For Ecol Manage 260:1478–1489.  https://doi.org/10.1016/j.foreco.2010.07.046CrossRefGoogle Scholar
  98. Parkin EA (1940) The digestive enzymes of some wood-boring beetle larvae. J Exp Biol 17:364–377Google Scholar
  99. Pearson M, Laiho R, Penttilä T (2017) Decay of Scots pine coarse woody debris in boreal peatland forests: mass loss and nutrient dynamics. For Ecol Manage 401:304–318.  https://doi.org/10.1016/j.foreco.2017.07.021CrossRefGoogle Scholar
  100. Pettersen RC (1984) The chemical composition of wood. In: Rowell R (ed) The chemistry of solid wood. American Chemical Society, Washington, DC, pp 57–126CrossRefGoogle Scholar
  101. Pinkalski C, Damgaard C, Jensen K-MV, Peng R, Offenberg J (2015) Quantification of ant manure deposition in a tropical agroecosystem: implications for host plant nitrogen acquisition. Ecosystems 18:1373–1382.  https://doi.org/10.1007/s10021-015-9906-5CrossRefGoogle Scholar
  102. Pinto-Tomás AA, Anderson MA, Suen G, Stevenson DM, Chu FST, Cleland WW, Weimer PJ, Currie CR (2009) Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326:1120–1123.  https://doi.org/10.1126/science.1173036CrossRefPubMedGoogle Scholar
  103. Pokarzhevskii AD, van Straalen NM, Zaboev DP, Zaitsev AS (2003) Microbial links and element flows in nested detrital food-webs. Pedobiologia 47:213–224.  https://doi.org/10.1078/0031-4056-00185CrossRefGoogle Scholar
  104. Preston CM, Trofymow JA, Niu J, Fyfe CA (1998) PMAS-NMR spectroscopy and chemical analysis of coarse woody debris in coastal forests of Vancouver Island. For Ecol Manage 111:51–68.  https://doi.org/10.1016/S0378-1127(98)00307-7CrossRefGoogle Scholar
  105. Preston CM, Nault JR, Trofymow JA, Smyth C (2009) Chemical changes during 6 years of decomposition of 11 litters in some Canadian Forest sites. Part 1. Elemental composition, tannins, phenolics, and proximate fractions. Ecosystems 12:1053–1077.  https://doi.org/10.1007/s10021-009-9266-0CrossRefGoogle Scholar
  106. Purahong W, Wubet T, Lentendu G, Schloter M, Pecyna MJ, Kapturska D, Hofrichter M, Krüger D, Buscot F (2016) Life in leaf litter: novel insights into community dynamics of bacteria and fungi during litter decomposition. Mol Ecol 25:4059–4074.  https://doi.org/10.1111/mec.13739CrossRefPubMedGoogle Scholar
  107. Ragland KW, Aerts DJ, Baker AJ (1991) Properties of wood for combustion analysis. Bioresour Technol 37:161–168.  https://doi.org/10.1016/0960-8524(91)90205-XCrossRefGoogle Scholar
  108. Reiners WA (1986) Complementary models for ecosystems. Am Nat 127:59–73.  https://doi.org/10.1086/284467CrossRefGoogle Scholar
  109. Rinne KT, Rajala T, Peltoniemi K, Chen J, Smolander A, Mäkipää R (2017) Treseder K (ed.) Accumulation rates and sources of external nitrogen in decaying wood in a Norway spruce dominated forest. Funct Ecol 31:530–541.  https://doi.org/10.1111/1365-2435.12734CrossRefGoogle Scholar
  110. Roskoski JP (1980) Nitrogen fixation in hardwood forests of the northeastern United States. Plant Soil 54:33–44.  https://doi.org/10.1007/BF02181997CrossRefGoogle Scholar
  111. Sánchez A, Micó E, Galante E, Juárez M (2017) Chemical transformation of quercus wood by Cetonia larvae (Coleoptera: Cetoniidae): an improvement of carbon and nitrogen available in saproxylic environments. Eur J Soil Biol 78:57–65.  https://doi.org/10.1016/j.ejsobi.2016.12.003CrossRefGoogle Scholar
  112. Sardans J, Rivas-Ubach A, Peñuelas J (2012) The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organismic lifestyle and ecosystem structure and function: a review and perspectives. Biogeochemistry 111:1–39. doi: https://doi.org/10.1007/s10533-011-9640-9CrossRefGoogle Scholar
  113. Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ (2003) Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett 6:96–101.  https://doi.org/10.1046/j.1461-0248.2003.00409.xCrossRefGoogle Scholar
  114. Schneider K, Kay AD, Fagan WF (2010) Adaptation to a limiting environment: the phosphorus content of terrestrial cave arthropods. Ecol Res 25:565–577.  https://doi.org/10.1007/s11284-009-0686-2CrossRefGoogle Scholar
  115. Seibold S, Bässler C, Baldrian P, Thorn S, Müller J, Gossner MM (2014) Wood resource and not fungi attract early-successional saproxylic species of Heteroptera - an experimental approach. Insect Conserv Divers 7:533–542.  https://doi.org/10.1111/icad.12076CrossRefGoogle Scholar
  116. Sitters J, Bakker ES, Veldhuis MP, Veen GF, Olde Venterink H, Vanni MJ (2017) The stoichiometry of nutrient release by terrestrial herbivores and its ecosystem consequences. Front Earth Sci 5:1–8.  https://doi.org/10.3389/feart.2017.00032CrossRefGoogle Scholar
  117. Slansky F, Rodriguez JG (1987) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New YorkGoogle Scholar
  118. Smythe RV, Carter FL, Baxter CC (1971) Influence of wood decay on feeding and survival of the eastern subterranean termite, Reticulitermes flavipes (Isoptera: Rhinotermitidae). Ann Entomol Soc Am 64:59–62.  https://doi.org/10.1093/aesa/64.1.59CrossRefGoogle Scholar
  119. Soper RS, Olson RE (1963) Survey of biota associated with Monochamus (Coleoptera: Cerambycidae) in Maine. Can Entomol 95:83–95.  https://doi.org/10.4039/Ent9583-1CrossRefGoogle Scholar
  120. Spano SD, Jurgensen MF, Larsen MJ, Harvey AE (1982) Nitrogen-fixing bacteria in Douglas-fir residue decayed by Fomitopsis pinicola. Plant Soil 68:117–123.  https://doi.org/10.1007/BF02374731CrossRefGoogle Scholar
  121. Sperfeld E, Halvorson HM, Malishev M, Clissold FJ, Wagner ND (2016a) Woodstoich III: integrating tools of nutritional geometry and ecological stoichiometry to advance nutrient budgeting and the prediction of consumer-driven nutrient recycling. Oikos 125:1539–1553.  https://doi.org/10.1111/oik.03529CrossRefGoogle Scholar
  122. Sperfeld E, Raubenheimer D, Wacker A (2016b) Bridging factorial and gradient concepts of resource co-limitation: towards a general framework applied to consumers. Ecol Lett 19:201–215.  https://doi.org/10.1111/ele.12554CrossRefPubMedGoogle Scholar
  123. Sperfeld E, Wagner ND, Halvorson HM, Malishev M, Raubenheimer D (2017) Bridging ecological stoichiometry and nutritional geometry with homeostasis concepts and integrative models of organism nutrition. Funct Ecol 31:286–296.  https://doi.org/10.1111/1365-2435.12707CrossRefGoogle Scholar
  124. Stark N (1972) Nutrient cycling pathways and litter fungi. BioScience 22:355–360.  https://doi.org/10.2307/1296341CrossRefGoogle Scholar
  125. Stenlid J, Penttilä R, Dahlberg A (2008) Wood-decay basidiomycetes in boreal forests: distribution and community development. In: Boddy L, Frankland JC, van West P (eds) British Mycological Society symposia series, vol 28. Academic Press, London, pp 239–262Google Scholar
  126. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton University, Princeton, NJGoogle Scholar
  127. Sterner RW, Hessen DO (1994) Algal nutrient limitation and the nutrition of aquatic herbivores. Annu Rev Ecol Syst 25:1–29.  https://doi.org/10.1146/annurev.es.25.110194.000245CrossRefGoogle Scholar
  128. Stokland JN, Siitonen J, Jonsson GB (2012) Biodiversity in dead wood. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  129. Strukelj M, Brais S, Mazerolle MJ, Paré D, Drapeau P (2017) Decomposition patterns of foliar litter and deadwood in managed and unmanaged stands: a 13-year experiment in boreal mixedwoods. Ecosystems:1–17.  https://doi.org/10.1007/s10021-017-0135-y
  130. Swanson EM, Espeset A, Mikati I, Bolduc I, Kulhanek R, White WA, Kenzie S, Snell-Rood EC (2016) Nutrition shapes life-history evolution across species. Proc Biol Sci 283(1834).  https://doi.org/10.1098/rspb.2015.2764CrossRefPubMedGoogle Scholar
  131. Swift MJ (1977) The ecology of wood decomposition. Sci Prog 64:175–199Google Scholar
  132. Swift MJ, Boddy L (1984) Animal-microbial interactions in wood decomposition. In: Anderson JM, Rayner ADM, Walton DWH (eds) Invertebrate-microbe interactions. Cambridge University Press, Cambridge, pp 89–131Google Scholar
  133. Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. University of California Press, Berkeley, CAGoogle Scholar
  134. Täyasu I, Sugimoto A, Wada E, Abe T (1994) Xylophagous termites depending on atmospheric nitrogen. Naturwissenschaften 81:229–231.  https://doi.org/10.1007/BF01138550CrossRefGoogle Scholar
  135. Thorne BL, Kimsey RB (1983) Attraction of neotropical Nasutitermes termites to carrion. Biotropica 15:295–296.  https://doi.org/10.2307/2387656CrossRefGoogle Scholar
  136. Ulyshen MD (2015) Insect-mediated nitrogen dynamics in decomposing wood. Ecol Entomol 40:97–112.  https://doi.org/10.1111/een.12176CrossRefGoogle Scholar
  137. Ulyshen MD (2016) Wood decomposition as influenced by invertebrates. Biol Rev 91:70–85.  https://doi.org/10.1111/brv.12158CrossRefPubMedPubMedCentralGoogle Scholar
  138. Ulyshen MD, Wagner TL (2013) Quantifying arthropod contributions to wood decay. Methods Ecol Evol 4:345–352.  https://doi.org/10.1111/2041-210x.12012CrossRefGoogle Scholar
  139. Urabe J, Watanabe Y (1992) Possibility of N or P limitation for planktonic cladocerans: an experimental test. Limnol Oceanogr 37:244–251.  https://doi.org/10.4319/lo.1992.37.2.0244CrossRefGoogle Scholar
  140. Varm A, Kolli BK, Paul J, Saxena S, König H (1994) Lignocellulose degradation by microorganisms from termite hills and termite guts: a survey on the present state of art. FEMS Microbiol Rev 15:9–28. doi: https://doi.org/10.1111/j.1574-6976.1994.tb00120.xCrossRefGoogle Scholar
  141. Vega FE, Blackwell M (2005) Insect-fungal associations: ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  142. Vinet L, Zhedanov A (2010) A “missing” family of classical orthogonal polynomials. Biology of termites: a modern synthesis. In: Bignell D, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, pp 439–475.  https://doi.org/10.1007/978-90-481-3977-4_16CrossRefGoogle Scholar
  143. Walczyńska A (2010) Is wood safe for its inhabitants? Bull Entomol Res 100(4):461–465.  https://doi.org/10.1017/S0007485309990514CrossRefPubMedGoogle Scholar
  144. Walczyńska A, Kapusta P (2017) Microclimate buffering of winter temperatures by pine stumps in a temperate forest. Clim Dyn 48(5–6):1953–1961.  https://doi.org/10.1007/s00382-016-3184-6CrossRefGoogle Scholar
  145. Wallace HR (1953) The ecology of the insect fauna of pine stumps. J Anim Ecol 22:154.  https://doi.org/10.2307/1698CrossRefGoogle Scholar
  146. Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632.  https://doi.org/10.1146/annurev-ento-112408-085319CrossRefPubMedPubMedCentralGoogle Scholar
  147. Watkinson SC, Bebber D, Darrah P et al (2006) The role of wood decay fungi in the carbon and nitrogen dynamics of the forest floor. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, Cambridge, pp 151–181CrossRefGoogle Scholar
  148. Wells JM, Boddy L (1995) Phosphorus translocation by saprotrophic basidiomycete mycelial cord systems on the floor of a mixed deciduous woodland. Mycol Res 99:977–980.  https://doi.org/10.1016/S0953-7562(09)80759-4CrossRefGoogle Scholar
  149. Wells JM, Hughes C, Boddy L (1990) The fate of soil-derived phosphorus in mycelial cord systems of Phanerochaete Velutina and Phallus impudicus. New Phytol 114:595–606.  https://doi.org/10.1111/j.1469-8137.1990.tb00430.xCrossRefGoogle Scholar
  150. Welti N, Striebel M, Ulseth AJ, Cross WF, DeVilbiss S, Glibert PM, Guo L, Hirst AG, Hood J, Kominoski JS, MacNeill KL, Mehring AS, Welter JR, Hillebrand H (2017) Bridging food webs, ecosystem metabolism, and biogeochemistry using ecological stoichiometry theory. Front Microbiol 8:1298.  https://doi.org/10.3389/fmicb.2017.01298CrossRefPubMedPubMedCentralGoogle Scholar
  151. Wilder SM, Jeyasingh PD (2016) Merging elemental and macronutrient approaches for a comprehensive study of energy and nutrient flows. J Anim Ecol 85:1427–1430.  https://doi.org/10.1111/1365-2656.12573CrossRefPubMedGoogle Scholar
  152. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar
  153. Wirtz KW, Kerimoglu O (2016) Autotrophic stoichiometry emerging from optimality and variable co-limitation. Front Ecol Evol 4.  https://doi.org/10.3389/fevo.2016.00131
  154. Yuan J, Hou L, Wei X, Shang Z, Cheng F, Zhang S (2017) Decay and nutrient dynamics of coarse woody debris in the Qinling Mountains, China. PLoS One 12:e0175203.  https://doi.org/10.1371/journal.pone.0175203CrossRefPubMedPubMedCentralGoogle Scholar
  155. Zhang J, Elser JJ (2017) Carbon:nitrogen:phosphorus stoichiometry in fungi: a meta-analysis. Front Microbiol 8:1281.  https://doi.org/10.3389/fmicb.2017.01281CrossRefPubMedPubMedCentralGoogle Scholar
  156. Zhang C, Jansen M, De Meester L, Stoks R (2016) Energy storage and fecundity explain deviations from ecological stoichiometry predictions under global warming and size-selective predation. J Anim Ecol 85:1431–1441.  https://doi.org/10.1111/1365-2656.12531CrossRefPubMedGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection.  2018

Authors and Affiliations

  • Michał Filipiak
    • 1
  1. 1.Institute of Environmental SciencesJagiellonian UniversityKrakówPoland

Personalised recommendations