Climate-change effects on the sex ratio of free-living soil nematodes – perspective and prospect
PERSPECTIVE PAPER
DOI:
https://doi.org/10.25674/so94iss1id174Keywords:
Climate change, human impact, nematode sex ratio, soil biodiversityAbstract
Human-induced global environmental change is predicted to alter the stability and functioning of ecosystems worldwide. Most research in recent decades has focused on studying climate-change effects on aboveground systems, causing a poor understanding of belowground responses. However, gaining knowledge on environmental-change effects on soil biota is of crucial importance, as soil-ecosystem services are indispensable for human well-being and contribute fundamentally to the functioning of terrestrial ecosystems. Nematode communities play a central role in various soil ecosystem processes and are therefore commonly used as biological indicators to assess soil conditions and soil health. While causing overall shifts in community composition patterns, which are most often examined, climate change might also alter nematode population dynamics and the sex ratio (number of males per female). Previous studies on plant-parasitic nematode species suggest that changes to unfavorable environmental conditions trigger reduced development of females and favor sexual rather than parthenogenetic reproduction. Therefore, we are presenting the working hypothesis that predicted climate change causing reduced resource availability and enhanced environmental stress will lead to an increased proportion of males in soil nematode communities. Our systematic literature review revealed that climate- and environmental change effects on the sex ratio of free-living soil nematode populations are inconsistent, but heavily understudied. Data on sex ratios have been treated mostly as additional information, presented without any underlying theory and hypotheses, as well as limited discussion. In this perspective paper, we thus propose that future studies should include clear hypotheses and test if the sex ratio of free-living nematodes increases with climate change due to more stressful environmental conditions and low resource availability. Furthermore, we conclude that experimental studies investigating the specific roles of male and female nematodes are needed to better predict the implications of a changing climate on soil ecosystem functioning.
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References
Adams, B. J., D. H. Wall, U. Gozel, A. R. Dillman, J. M. Chaston & I. D. Hogg (2007): The southernmost worm, Scottnema lindsayae (Nematoda): Diversity, dispersal and ecological stability. – Polar Biology 30: 809–815 [https://doi.org/10.1007/s00300-006-0241-3].
Andriuzzi, W. S. & D. H. Wall (2018). Soil biological responses to, and feedbacks on, trophic rewilding. Philosophical – Transactions of the Royal Society B: Biological Sciences, 373: 20170448 [https://doi.org/10.1098/rstb.2017.0448].
Anjam, M. S., S. J. Shah, C. Matera, E. Różańska, M. Sobczak, S. Siddique & F. M. W. Grundler (2020): Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana. – Plant, Cell & Environment 43: 1160–1174 [https://doi.org/10.1111/pce.13728].
Anwer, M. A., M. S. Anjam, S. J. Shah, M. S. Hasan, A. A. Naz, F. M. W. Grundler & S. Siddique (2018): Genome-wide association study uncovers a novel QTL allele of AtS40-3 that affects the sex ratio of cyst nematodes in Arabidopsis. – Journal of Experimental Botany 69: 1805–1814 [https://doi.org/10.1093/jxb/ery019].
Austin, B. U. R. T., R. Trivers & A. Burt (2009): Genes in conflict: the biology of selfish genetic elements. – Harvard University Press.
Ayres, E., D. H. Wall, B. J. Adams, J. E. Barrett & R. A.Virginia (2007): Unique Similarity of Faunal Communities across Aquatic–Terrestrial Interfaces in a Polar Desert Ecosystem: Soil–Sediment Boundaries and Faunal Community. – Ecosystems 10: 523–535 [https://doi.org/10.1007/s10021-007-9035-x].
Bamforth, S. S., D. H. Wall & R. A. Virginia (2005): Distribution and diversity of soil protozoa in the McMurdo Dry Valleys of Antarctica. – Polar Biology 28: 756–762 [https://doi.org/10.1007/s00300-005-0006-4].
Bardgett, R. D. & W. H. van der Putten (2014): Belowground biodiversity and ecosystem functioning. – Nature 515: 505–511 [https://doi.org/10.1038/nature13855].
Barnett, T. P., J. C. Adam & D. P. Lettenmaier (2005): Potential impacts of a warming climate on water availability in snow-dominated regions. – Nature 438: 303–309 [https://doi.org/10.1038/nature04141].
Bar-On, Y. M., R. Phillips & R. Milo (2018): The biomass distribution on Earth. – Proceedings of the National Academy of Sciences 115: 6506–6511.
Barrett, J. E., R. A. Virginia, D. H. Wall & B. J. Adams (2008): Decline in a dominant invertebrate species contributes to altered carbon cycling in a low-diversity soil ecosystem: CLIMATE-INDUCED DECLINE OF AN INVERTEBRATE SPECIES. – Global Change Biology 14: 1734–1744 [https://doi.org/10.1111/j.1365-2486.2008.01611.x].
Bird, A. F. (1971): Specialized adaptations of nematodes to parasitism. p. 47. – In: B. M. Zuckerman, W. F. Mai & R. A. Rohde (eds): Plant Parasitic Nematodes. Volume II. – Academic Press, New York.
Bird, D. M., V. M. Williamson, P. Abad, J. McCarter, E. G. J. Danchin, P. Castagnone-Sereno & C. H. Opperman (2009): The genomes of root-knot nematodes. – Annual Review of Phytopathology 47: 333–351 [https://doi.org/10.1146/annurev-phyto-080508-081839].
Blankinship, J. C., P. A. Niklaus & B. A. Hungate (2011): A meta-analysis of responses of soil biota to global change. 2 Oecologia 165: 553–565 [https://doi.org/10.1007/s00442-011-1909-0].
Boström, S., O. Holovachov & S. A. Nadler (2011): Description of Scottnema lindsayae Timm, 1971 (Rhabditida: Cephalobidae) from Taylor Valley, Antarctica and its phylogenetic relationship. – Polar Biology 34: 1–12 [https://doi.org/10.1007/s00300-010-0850-8].
Bürger, R. (1999). Evolution of genetic variability and the advantage of sex and recombination in changing environments. – Genetics 153: 1055–1069
Cameron, E. K., I. S. Martins, P. Lavelle, J. Mathieu, L. Tedersoo, M. Bahram, F. Gottschall, C. A. Guerra, J. Hines, G. Patoine & et al. (2019): Global mismatches in aboveground and belowground biodiversity. – Conservation Biology 33: 1187–1192 [https://doi.org/10.1111/cobi.13311].
Castagnone‐Sereno, P. & E. G. J. Danchin (2014): Parasitic success without sex–the nematode experience. – Journal of Evolutionary Biology 27: 1323–1333.
Cesarz, S., M. Ciobanu, A. J. Wright, A. Ebeling, A. Vogel, W. W. Weisser & N. Eisenhauer (2017): Plant species richness sustains higher trophic levels of soil nematode communities after consecutive environmental perturbations. – Oecologia 184: 715–728 [https://doi.org/10.1007/s00442-017-3893-5].
Chahartaghi, M., M. Maraun, S. Scheu & K. Domes (2009): Resource depletion and colonization: a comparison between parthenogenetic and sexual Collembola species. – Pedobiologia 52: 181–189.
Christie, J. R. (1929): Some observations on sex in the Mermithidae. – Journal of Experimental Zoology 53: 59–76 [https://doi.org/10.1002/jez.1400530106].
Cohen, J. M., M. J. Lajeunesse & J. R. Rohr (2018): A global synthesis of animal phenological responses to climate change. – Nature Climate Change 8: 224–228 [https://doi.org/10.1038/s41558-018-0067-3].
Cryan, W. S. & E. L. Hansen (1966): Variation in Sex Ratio of Panagrellus redivivus in Response To Nutritional and Heat Stress. – Nematologica 12: 355–358 [https://doi.org/10.1163/187529266X00824].
Delgado-Baquerizo, M., C. A. Guerra, C. Cano-Díaz, E. Egidi, J.-T. Wang, N. Eisenhauer, B. K. Singh & F. T. Maestre (2020): The proportion of soil-borne pathogens increases with warming at the global scale. – Nature Climate Change 10: 550–554 [https://doi.org/10.1038/s41558-020-0759-3].
Duffy, J. E., Godwin, C. M., & Cardinale, B. J. (2017). Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549: 261–264 [https://doi.org/10.1038/nature23886].
Eisenhauer, N., S. Partsch, D. Parkinson & S. Scheu (2007): Invasion of a deciduous forest by earthworms: Changes in soil chemistry, microflora, microarthropods and vegetation. – Soil Biology and Biochemistry 39: 1099–1110 [https://doi.org/10.1016/j.soilbio.2006.12.019].
Eisenhauer, N., O. Ferlian, D. Craven, J. Hines & M. Jochum (2019): Ecosystem responses to exotic earthworm invasion in northern North American forests. – Research Ideas and Outcomes 5: e34564 [https://doi.org/10.3897/rio.5.e34564].
Eisenhauer, N., V. D. Migunova, M. Ackermann, L. Ruess & S. Scheu (2011): Changes in plant species richness induce functional shifts in soil nematode communities in experimental grassland. – Plos one 6: e24087.
Eisenhauer, N., S. Herrmann, J. Hines, F. Buscot, J. Siebert & M. P. Thakur (2018): The Dark Side of Animal Phenology. Trends in Ecology & Evolution 33: 898–901 [https://doi.org/10.1016/j.tree.2018.09.010].
Eisenhauer, N., T. Dobies, S. Cesarz, S. E. Hobbie, R. J. Meyer, K. Worm & P. B. Reich (2013): Plant diversity effects on soil food webs are stronger than those of elevated CO2 and N deposition in a long-term grassland experiment. – Proceedings of the National Academy of Sciences 110: 6889–6894 [https://doi.org/10.1073/pnas.1217382110].
Eisenhauer, N., F. Buscot, A. Heintz‐Buschart, S. D. Jurburg, K. Küsel, J. Sikorski, H. Vogel & C. A. Guerra (2020): The multidimensionality of soil macroecology. – Global Ecology and Biogeography 30: 4–10 [https://doi.org/10.1111/geb.13211].
Eisenhauer, N., H. Beßler, C. Engels, G. Gleixner, M. Habekost, A. Milcu, S. Partsch, A. C. W. Sabais, C. Scherber, S. Steinbeiss & et al. (2010): Plant diversity effects on soil microorganisms support the singular hypothesis. – Ecology 91: 485–496 [https://doi.org/10.1890/08-2338.1].
Ellenby, C. (1954): Environmental determination of the sex ratio of a plant parasitic nematode. – Nature 174: 1016–1017.
Ferlian, O., S. Cesarz, D. Craven, J. Hines, K. E. Barry, H. Bruelheide, F. Buscot, S. Haider, H. Heklau, S. Herrmann & et al. (2018a): Mycorrhiza in tree diversity–ecosystem function relationships: Conceptual framework and experimental implementation. – Ecosphere 9 [https://doi.org/10.1002/ecs2.2226].
Ferlian, O., N. Eisenhauer, M. Aguirrebengoa, M. Camara, I. Ramirez‐Rojas, F. Santos, K. Tanalgo & M. P. Thakur (2018b): Invasive earthworms erode soil biodiversity: A meta‐analysis. – Journal of Animal Ecology 87: 162–172 [https://doi.org/10.1111/1365-2656.12746].
Ferris, H., T. Bongers & R. G. M. de Goede (2001): A framework for soil food web diagnostics: Extension of the nematode faunal analysis concept. – Applied Soil Ecology 18: 13–29 [https://doi.org/10.1016/S0929-1393(01)00152-4].
Foreman, C. M., C. F. Wolf & J. C. Priscu (2004): Impact of Episodic Warming Events on the Physical, Chemical and Biological Relationships of Lakes in the McMurdo Dry Valleys, Antarctica. – Aquatic Geochemistry 10: 239–268.
Freckman, D. W. & E. P. Caswell (1985): The Ecology of Nematodes in Agroecosystems. – Annual Review of Phytopathology 23: 275–296.
George, P. B. L., D. Lallias, S. Creer, F. M. Seaton, J. G. Kenny, R. M. Eccles, R. I. Griffiths, I. Lebron, B. A. Emmett, D. A. Robinson & D. L. Jones (2019): Divergent national-scale trends of microbial and animal biodiversity revealed across diverse temperate soil ecosystems. – Nature Communications 10: 1107 [https://doi.org/10.1038/s41467-019-09031-1].
Golestaninasab, M., M. Malek, B. Jalali & I. Mobedi (2012): Variation in the sex ratio of Rhabdochona fortunatowi (Spirurida: Rhabdochonidae) in Capoeta capoeta gracilis (Cypriniformes: Cyprinidae), relative to levels of infection, host size and temperature. – Journal of Helminthology 86: 41–45 [https://doi.org/10.1017/S0022149X11000010].
Grundler, F., M. Betka & U. Wyss (1991): Influence of changes in the nurse cell system (syncytium) on sex determination and development of the cyst nematode Heterodera schachtii: Total amounts of proteins and amino acids. – Phytopathology 81: 70–74 [https://doi.org/10.1094/Phyto-81-70].
Guerrero-Ramírez, N. R., D. Craven, P. B. Reich, J. J. Ewel, F. Isbell, J. Koricheva, J. A. Parrotta, H. Auge, H. E. Erickson, D. I. Forrester & et al. (2017): Diversity-dependent temporal divergence of ecosystem functioning in experimental ecosystems. – Nature Ecology & Evolution 1: 1639–1642 [https://doi.org/10.1038/s41559-017-0325-1].
Hansen, E. L., E. J. Buecher & E. A. Yarwood (1972): Sex differentiation of Aphelenchus avenae in axenic culture. – Nematologica 18: 253–260 [https://doi.org/10.1163/187529272X00485].
Hardy, I. C. W. (2002): Sex Ratios: Concepts and Research Methods – Cambridge University Press: 424 pp.
Heethoff, M., R. A. Norton, S. Scheu & M. Maraun (2009): Parthenogenesis in oribatid mites (Acari, Oribatida): evolution without sex. – In: Lost Sex. – Springer, Dordrecht: 241–257.
IPCC (2021): Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. – Cambridge University Press.
IPBES (2019): Global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy – Platform on Biodiversity and Ecosystem Services. IPBES secretariat, Bonn, Germany: 1148 pp. [https://doi.org/10.5281/zenodo.3831673].
Isbell, F., A. Gonzalez, M. Loreau, J. Cowles, S. Díaz, A. Hector, G. M. Mace, D. A. Wardle, M. I. O’Connor, J. E. Duffy, L. A. Turnbull, P. L. Thompson & A. Larigauderie (2017): Linking the influence and dependence of people on biodiversity across scales. – Nature 546: 65–72 [https://doi.org/10.1038/nature22899].
Kahel-Raifer, H. & I. Glazer (2000): Environmental factors affecting sexual differentiation in the entomopathogenic nematode Heterorhabditis bacteriophora. – Journal of Experimental Zoology 287: 158–166.
Kapranas, A., B. Malone, S. Quinn, L. Mc Namara, C. D. Williams, P. O’Tuama, A. Peters & C. T. Griffin (2017): Efficacy of entomopathogenic nematodes for control of large pine weevil, Hylobius abietis: Effects of soil type, pest density and spatial distribution. – Journal of Pest Science 90: 495–505 [https://doi.org/10.1007/s10340-016-0823-y].
Jochum, M., O. Ferlian, M. P. Thakur, M. Ciobanu, B. Klarner, J.-A. Salamon, L. E. Frelich, E. A. Johnson & N. Eisenhauer (2021): Earthworm invasion causes declines across soil fauna size classes and biodiversity facets in northern North American forests. – Oikos 130: 766–780.
Jones, J. T., A. Haegeman, E. G. J. Danchin, H. S. Gaur, J. Helder, M. G. K. Jones, T. Kikuchi, R. Manzanilla-López, J. E. Palomares-Rius, W. M. L. Wesemael & R. N. Perry (2013): Top 10 plant-parasitic nematodes in molecular plant pathology. – Molecular Plant Pathology 14: 946–961 [https://doi.org/10.1111/mpp.12057].
Lange, M., M. Habekost, N. Eisenhauer, C. Roscher, H. Bessler, C. Engels, Y. Oelmann, S. Scheu, W. Wilcke, E.-D. Schulze & G. Gleixner (2014): Biotic and Abiotic Properties Mediating Plant Diversity Effects on Soil Microbial Communities in an Experimental Grassland. – PLoS ONE 9: e96182 [https://doi.org/10.1371/journal.pone.0096182].
Laughlin, C. W., A. S. Williams & J. A. Fox (1969): The Influence of Temperature on Development and Sex Differentiation of Meloidogyne graminis. – Journal of Nematology 1: 212–215.
Lyons, W. B., K. A. Welch, A. E.Carey, P. T. Doran, D. H. Wall, R. A.Virginia, A. G. Fountain, B. M. Csathó & C. M. Tremper (2005): Groundwater seeps in Taylor Valley Antarctica: An example of a subsurface melt event. – Annals of Glaciology 40: 200–206 [https://doi.org/10.3189/172756405781813609].
Maynard Smith, J. (1978): The evolution of sex. – Cambridge University Press.
McClure, M. A. & D. R. Viglierchio (1966): The Influenceof host nutrition and intensity of infection on the sex ratio and development of Meloidogyne incognita in sterile agar cultures of excised cucumber roots. – Nematologica 12: 248–258.
McSorley, R. (2003): Adaptations of nematodes to environmental extremes. – Florida Entomologist 86: 138–142.
Michiels, I. C. & W. Traunspurger (2005): Benthic community patterns and the composition of feeding types and reproductive modes in freshwater nematodes. – Nematology 7: 21–36 [https://doi.org/10.1163/1568541054192234].
Moens, T., A. Vierstraete & M. Vincx (1996): Life Strategies in Two Bacterivorous Marine Nematodes: Preliminary Results. – Marine Ecology 17: 509–518 [https://doi.org/10.1111/j.1439-0485.1996.tb00524.x].
Morran, L. T., B. J. Cappy, J. L. Anderson & P. C. Phillips (2009): Sexual partners for the stressed: facultative outcrossing in the self‐fertilizing nematode Caenorhabditis elegans. – Evolution: International Journal of Organic Evolution 63: 1473–1482.
Mote, P. W., A. F. Hamlet, M. P. Clark & D. P. Lettenmaier (2005): Declining mountain snowpack in Western North America. – Bulletin of the American Meteorological Society 86: 39–50 [https://doi.org/10.1175/BAMS-86-1-39].
Mulder, C. P. H., D. D. Uliassi & D. F. Doak (2001): Physical stress and diversity-productivity relationships: The role of positive interactions. – Proceedings of the National Academy of Sciences 98: 6704–6708 [https://doi.org/10.1073/pnas.111055298].
Müller, J., K. Rehbock & U. Wyss (1981): Growth of Heterodera schachtii with remarks on amounts of food consumed. – Revue de Nematologie 4: 227–234.
Murphy, G. E. P. & T. N. Romanuk (2014): A meta‐analysis of declines in local species richness from human disturbances. Ecology and Evolution 4: 91–103 [https://doi.org/10.1002/ece3.909].
Neher, D. A. (2001): Role of nematodes on soil health and their use as indicators. – Journal of Nematology 33: 161–168.
Orgiazzi, A., R. D. Bardgett & E. Barrios (2016): Global soil biodiversity atlas. – European Commission; CABDirect.
Overhoff, A., D. W. Freckman & R. A. Virginia (1993): Life cycle of the microbivorous Antarctic Dry Valley nematode Scottnema lindsayae (Timm 1971): – Polar Biology 13: 151–156 [https://doi.org/10.1007/BF00238924].
Pen-Mouratov, S., N. Shukurov, J. Yu, S. Rakhmonkulova, O. Kodirov, G. Barness, M. Kersten & Y. Steinberger (2014): Successive development of soil ecosystems at abandoned coal-ash landfills. – Ecotoxicology 23: 880–897 [https://doi.org/10.1007/s10646-014-1227-5].
Pérès, G., D. Cluzeau, S. Menasseri, J. F. Soussana, H. Bessler, C. Engels, M. Habekost, G. Gleixner, A. Weigelt, W. W. Weisser, S. Scheu & N. Eisenhauer (2013): Mechanisms linking plant community properties to soil aggregate stability in an experimental grassland plant diversity gradient. – Plant and Soil 373: 285–299 [https://doi.org/10.1007/s11104-013-1791-0].
Phillips, H. R. P., C. A. Guerra, M. L. C. Bartz, M. J. I. Briones, G. Brown, T. W. Crowther, O. Ferlian, K. B. Gongalsky, J. van den Hoogen, J. Krebs & et al. (2019): Global distribution of earthworm diversity. – Science 366: 480–485 [https://doi.org/10.1126/science.aax4851
Porazinska, D. L., D. H. Wall & R. A. Virginia (2002): Population Age Structure of Nematodes in the Antarctic Dry Valleys: Perspectives on Time, Space, and Habitat Suitability. – Arctic, Antarctic, and Alpine Research 34: 159–168 [https://doi.org/10.1080/15230430.2002.12003480].
Reich, P. B., D. Tilman, F. Isbell, K. Mueller, S. E. Hobbie, D. F. B. Flynn & N. Eisenhauer (2012): Impacts of Biodiversity Loss Escalate Through Time as Redundancy Fades. – Science 336: 589–592 [https://doi.org/10.1126/science.1217909
Roscher, C., J. Schumacher, J. Baade, W. Wilcke, G. Gleixner, W. W. Weisser, B. Schmid & E.-D. Schulze (2004): The role of biodiversity for element cycling and trophic interactions: An experimental approach in a grassland community. – Basic and Applied Ecology 5: 107–121 [https://doi.org/10.1078/1439-1791-00216
Schädler, M., F. Buscot, S. Klotz, T. Teitz, W. Durka, J. Bumberger, I. Merbach, S. G. Michalski, K. Kirsch, P. Remmler, E. Schulz & H. Auge (2019): Investigating the consequences of climate change under different land-use regimes: a novel experimental infrastructure. – Ecosphere 10: e02635.
Scherber, C., N. Eisenhauer, W. W. Weisser, B. Schmid, W. Voigt, M. Fischer, E.-D. Schulze, C. Roscher, A. Weigelt, E. Allan & et al. (2010): Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. – Nature 468: 553–556 [https://doi.org/10.1038/nature09492
Scheu, S. & B. Drossel (2007): Sexual reproduction prevails in a world of structured resources in short supply. – Proceedings of the Royal Society B: Biological Sciences 274: 1225–1231 [https://doi.org/10.1098/rspb.2007.0040].
Schroeder, F., L. Peters & W. Traunspurger (2013): Nematodes in the periphyton of lakes: Variations in diversity, species composition, age structure, and sex ratio. – International Review of Hydrobiology 98: 322–333 [https://doi.org/10.1002/iroh.201301652].
Schwanz, L. E. & A. Georges (2021): Sexual Development and the Environment: Conclusions from 40 Years of Theory. – Sexual Development 15: 7–22 [https://doi.org/10.1159/000515221].
Siebert, J., M. Ciobanu, M. Schädler & N. Eisenhauer (2020): Climate change and land use induce functional shifts in soil nematode communities. – Oecologia 192: 281–294 [https://doi.org/10.1007/s00442-019-04560-4].
Simmons, B. L., D. H. Wall, B. J. Adams, E. Ayres, J. E. Barrett & R. A. Virginia (2009): Long-term experimental warming reduces soil nematode populations in the McMurdo Dry Valleys, Antarctica. – Soil Biology and Biochemistry 41: 2052–2060 [https://doi.org/10.1016/j.soilbio.2009.07.009].
Singh, S. K., M. Hodda, G. J. Ash & N. C. Banks (2013): Plant-parasitic nematodes as invasive species: Characteristics, uncertainty and biosecurity implications. – Annals of Applied Biology 28.
Song, Y., B. Drossel & S. Scheu (2011): Tangled Bank dismissed too early. – Oikos 120: 1601–1607.
Spaak, J. W., J. M. Baert, D. J. Baird, N. Eisenhauer, L. Maltby, F. Pomati, V. Radchuk, J. R. Rohr, P. J. Van den Brink & F. De Laender (2017): Shifts of community composition and population density substantially affect ecosystem function despite invariant richness. – Ecology Letters 20: 1315–1324 [https://doi.org/10.1111/ele.12828].
Stearns, S. C. & R. F. Hoekstra (2005): Evolution, an introduction. – Oxford University Press.
Thakur, M. P., A. Milcu, P. Manning, P. A. Niklaus, C. Roscher, S. Power, P. B. Reich, S. Scheu, D. Tilman, F. Ai & et al. (2015): Plant diversity drives soil microbial biomass carbon in grasslands irrespective of global environmental change factors. – Global Change Biology 21: 4076–4085 [https://doi.org/10.1111/gcb.13011].
Thomas, C. G., G. C. Woodruff & E. S. Haag (2012): Causes and consequences of the evolution of reproductive mode in Caenorhabditis nematodes. – Trends in Genetics 28: 213–220.
Tilman, D., F. Isbell & J. M. Cowles (2014). Biodiversity and Ecosystem Functioning. Annual Review of Ecology, Evolution, and Systematics 45: 471–493 [https://doi.org/10.1146/annurev-ecolsys-120213-091917].
Traunspurger, W. (1998): Distribution and Sex Ratio of Ethmolaimus pratensis De Man, 1880 (Nematoda, Chromadorida) in an Oligotrophic Lake. – Nematologica 44: 391–408 [https://doi.org/10.1163/005525998X00061].
Treonis, A. M., D. H. Wall & R. A. Virginia (1999): Invertebrate Biodiversity in Antarctic Dry Valley Soils and Sediments. – Ecosystems 2: 482–492.
Triantaphyllou, A. C. (1960): Sex determination in Meloidogyne incognita Chitwood, 1949 and intersexuality in M. javanica (Treub, 1985) Chitwood, 1949. – Annales de l’Institut Phytopathologique Benaki 3: 12–31.
Triantaphyllou, A. C. & H. Hirschmann (1964): Reproduction in Plant and Soil Nematodes. – Annual Review of Phytopathology 2: 57–80 [https://doi.org/10.1146/annurev.py.02.090164.000421].
Triantaphyllou, A. C. (1973): Environmental Sex Differentiation of Nematodes in Relation to Pest Management. – Annual Review of Phytopathology 11: 441–462 [https://doi.org/10.1146/annurev.py.11.090173.002301].
Trudgill, D. L. (1967): The Effect of Environment On Sex Determination in Heterodera rostochiensis. – Nematologica 13: 263–272 [https://doi.org/10.1163/187529267X00120
Tyler, J. (1933): Development of the root-knot nematode as affected by temperature. – Hilgardia 7: 389–415 [https://doi.org/10.3733/hilg.v07n10p389].
van den Hoogen, J., S. Geisen, D. Routh, H. Ferris, W. Traunspurger, D. A. Wardle, R. G. M. de Goede, B. J. Adams, W. Ahmad, W. S. Andriuzzi & et al. (2019): Soil nematode abundance and functional group composition at a global scale. – Nature 572: 194–198 [https://doi.org/10.1038/s41586-019-1418-6].
Veresoglou, S. D., J. M. Halley & M. C. Rillig (2015): Extinction risk of soil biota. – Nature Communications 6: 8862 [https://doi.org/10.1038/ncomms9862
Vogel, A., N. Eisenhauer, A. Weigelt & M. Scherer-Lorenzen (2013): Plant diversity does not buffer drought effects on early-stage litter mass loss rates and microbial properties. – Global Change Biology 19: 2795–2803 [https://doi.org/10.1111/gcb.12225].
Wagg, C., S. F. Bender, F. Widmer & M. G. A. van der Heijden (2014): Soil biodiversity and soil community composition determine ecosystem multifunctionality. – Proceedings of the National Academy of Sciences 111: 5266–5270 [https://doi.org/10.1073/pnas.1320054111].
Wall, D. H. (2007): Global change tipping points: Above- and below-ground biotic interactions in a low diversity ecosystem. – Philosophical Transactions of the Royal Society B: Biological Sciences 362: 2291–2306 [https://doi.org/10.1098/rstb.2006.1950].
Wall, J. W., K. R. Skene & R. Neilson (2002): Nematode community and trophic structure along a sand dune succession. – Biology and Fertility of Soils 35: 293–301.
Wall, D. H., R. D. Bardgett, V. Behan-Pelletier, J. E. Herrick, T. H. Jones, K. Ritz, J. Six, D. R. Strong & W. van der Putten (2012): Soil ecology and ecosystem services. – Oxford University Press.
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Soil Organisms is committed to fair open access publishing. All articles are available online without publication fees. Articles published from Vol. 96 No. 3 (2024) onwards are licensed under the Creative Commons Attribution 4.0 International (CC BY 4.0) license. Articles published from Vol. 80 No. 1 through Vol. 96 No. 2 are available under the previous terms, allowing non-commercial, private, and scientific use.
