Sex ratios of oribatid mite assemblages differ among microhabitats

Authors

  • Katja Wehner Ecological Networks, Technische Univeristät Darmstadt, Schnittspahnstraße 3, 64287 Darmstadt, Germany
  • Micheal Heethoff Ecological Networks, Technische Univeristät Darmstadt, Schnittspahnstraße 3, 64287 Darmstadt, Germany
  • Adrian Brückner Ecological Networks, Technische Univeristät Darmstadt, Schnittspahnstraße 3, 64287 Darmstadt, Germany

Keywords:

Sex ratios, oribatid mites, microhabitats, litter, dead wood, moss, grass sod, lichen, tree bark

Abstract

This study investigates sex ratios of oribatid mite species and oribatid mite assemblages in different forest microhabitats (dead wood, grass sod, moss, lichen litter, tree bark) to identify possible factors driving sex ratio dynamics. We considered 46,320 individuals belonging to 47 species, and analyzed data on numbers of sexual and parthenogenetic species as well as individuals across microhabitats using paired t-tests and generalized linear mixed effect models. Most species (75 %) were sexual, with females comprising 43 % to 89 % of samples. In twelve out of 35 sexual species sex ratios differed significantly among microhabitats, the sex ratio of most species (23) remained constant. Parthenogenetic species of Enarthronota, Mixonomata, Nothrina and Quadroppia quadricarinata comprised of 100 % females, but in Oppiella nova, and Tectocepheus spp. spanandric males were found (1–3 %). Sex ratios of oribatid mite assemblages were generally female-biased and differed significantly among microhabitats. The highest proportions of females were found on tree bark (~ 72 %) and grass sod (~ 69 %) and the lowest were in lichens (~ 53 %). The mechanism of sex determination in oribatid mites and factors influencing the distortion of primary sex ratios are poorly known, so explanations for the observed patterns remain speculative. Since field observations are mostly infeasible, complex long-term laboratory studies on egg deposition, egg development and development of males and females under different conditions in different species are needed.

References

Barton, K. (2017): MuMIn: Multi-Model Inference. – R package version 1.40.0. [https://CRAN.R-project.org/package=MuMIn].

Bates, G., M. Maechler, B. Bolker & S. Walker (2015): Fitting linear mixed-effects models using lme4. – Journal of Statistical Software 67(1):1–48 [doi:10.18637/jss.v067.i01].

Behan-Pelletier, V. M. (2015): Review of sexual dimorphism in brachypyline oribatid mites. – Acarologia 55(2):127–146.

Bell, G. (1982): The Masterpiece of Nature. The Evolution and Genetics of Sexuality. – University of California Press, California.

Bergmann, P. & M. Heethoff (2012): Development of the internal reproductive organs in early nymphal stages of Archegozetes longisetosus Aoki (Acari, Oribatida, Trhypochthoniidae) as obtained by synchrotron X-ray microtomography (SR-µCT) and transmission electron microscopy (TEM). – Soil Organisms 84:459–470.

Bergmann, P., M. Laumann, R. A. Norton & M. Heethoff (2018): Cytological evidence for automictic thelytoky in parthenogenetic oribatid mites (Acari, Oribatida): Synaptonemal complexes confirm meiosis in Archegozetes longisetosus. – Acarologia, accepted.

Charnov, E. L. (1982): The Theory of Sex Allocation. – Princeton University Press, Princeton.

Charnov, E. L., R. L. Los-den Hartogh, W. T. Jones & J. van den Assem (1981): Sex ratio evolution in a variable environment. – Nature 289: 27–33.

Cianciolo, J. M. & R. A. Norton (2006): The ecological distribution of reproductive mode in oribatid mites, as related to biological complexity. – Experimental and Applied Acarology 40: 1–25.

Domes, K., S. Scheu & M. Maraun (2007): Resources and sex: soil re-colonization by sexual and parthenogenetic oribatid mites. – Pedobiologia 51: 1–11.

Ermilov, S. G., M. Łochysńka & Z. Olszanowski (2008): The cultivation and morphology of juvenile stages of two species from the genus Scutovertex (Acari: Oribatida: Scutoverticidae). – Annales Zoologici 58(2): 433–443.

Fisher, R. A. (1930): The Genetical Theory of Natural Selection. – Clarendon Press, Oxford.

Fox, J. (2003): Effect displays in R for generalised linear models. – Journal of Statistical Software 8(15): 1–27 [http://www.jstatsoft.org/v08/i15/].

Fox, J. & S. Weisberg (2011): An {R} Companion to Applied Regression, Second Edition. – Thousand Oaks CA: Sage [http://socserv.socsci.mcmaster.ca/jfox/Books/ Companion].

Frey, D. F. & K. L. H. Leong (1993): Can microhabitat selection or differences in ‘catchability’ explain male-biased sex ratios in overwintering populations of monarch butterflies? – Animal Behaviour 45(5): 1025–1027.

Grandjean, F. (1941): Statistique sexuelle et parthénogenèse chez les Oribates (Acariens). – Comptes Rendus des Seances de l’ Academie des Sciences 212: 463–467.

Hamilton, W. D. (1967): Extraordinary sex ratios. – Science 156(3774): 477–488.

Hartig, F. (2017): DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. R package version 0.1.5. [https://CRAN.R-project.org/ package=DHARMa].

Heethoff, M., P. Bergmann & R. A. Norton (2006): Karyology and sex determination of oribatid mites. – Acarologia 46: 127–131.

Heethoff, M., R. A. Norton, S. Scheu & M. Maraun (2009): Parthenogenesis in oribatid mites (Acari, Oribatida): evolution without sex. in I. Schoen, K. Martens & P. van Dijk, editors. Lost Sex – The Evolutionary Biology of Parthenogenesis. – Springer Press: 241–257.

Hothorn, T., F. Bretz & P. Westfall (2008): Simultaneous inference in general parametric models. – Biometrical Journal 50(3): 346–363.

Hubert, J. (2000): Seasonal changes of abundance, sex ratio and egg production of Scheloribates laevigatus (Acari: Oribatida) in the soil of a meadow in the Czech Republic. – Acta Societatis Zoologicae Bohemicae 64: 37–56.

Kempson, D., M. Llyod & R. Ghelardi (1963): A new extractor for woodland litter. – Pedobiologia 3: 1–21.

Kokko, H. & M. D. Jennions (2008): Parental investment, sexual sexual selection and sex ratios. – Journal of Evolutionary Biology 21(4): 919–948.

Laumann, M., P. Bergmann & M. Heethoff (2008): Some remarks on the cytogenetics of oribatid mites. – Soil Organisms 80: 223–232.

Maraun, M., J. A. Salamon, K. Schneider, M. Schaefer & S. Scheu (2003): Oribatid mite and collembolan diversity, density and community structure in a moder beech forest (Fagus sylvatica): effects of mechanical perturbations. – Soil Biology and Biochemistry 35(10): 1387–1394.

Myers, J. H. (1978): Sex ratio adjustment under food stress: maximization of quality or number of offspring? – The American Naturalist 112(984): 381–388.

Nager, R. G., P. Monaghan, R. Griffiths, D. C. Houston & R. Dawson (1999): Experimental demonstration that offspring sex ratio varies with maternal conditions. – Proceeding of the National Academy of Sciences 96: 570–573.

Nakagawa, S. & H. Schielzeth (2013): A general and simple method for obtaining R^2 from generalized linear mixed-effects models. – Methods in Ecology and Evolution 4: 133–142.

Norton, R. A. & S. C. Palmer (1991): The distribution, mechanisms, and evolutionary significance of parthenogenesis in oribatid mites. In: R. Schuster & P. W. Murphy (eds). – The Acari: Reproduction, Development and Life-History Strategies. – Chapman and Hall, London: 107–136.

Norton, R.A. & V. Behan-Pelletier (2009): Suborder Oribatida. – In: G. W. Krantz & D. E. Walter (eds): A Manual of Acarology. – Third Edition. Lubbock, Texas: Texas Tech University Press: 430–564.

Norton, R. A, P. M. Bonamo, J. D. Grierson & W. A. Shear. (1988): Oribatid mite fossils from terrestrial Devonian deposit near Gilboa, New York. – Journal of Paleontology 62: 259–269.

Norton, R. A., J. B. Kethley, D. E. Johnston & B. M. OConnor. (1993): Phylogenetic perspectives on genetic systems and reproductive modes in mites. In: D. L. Wrensch & M. A. Ebbert (eds): Evolution and Diversity of Sex Ratios. – Chapman and Hall, New York: 8–99.

Palmer, S. C. & R. A. Norton (1992): Genetic diversity in thelytokous oribatid mites (Acari: Acariformes: Oribatida). – Biochemical Systematics and Ecology 20: 219–231.

Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar & R Core Team (2016): Nlme: linear and nonlinear mixed effects models. – R package version 3.1–128, [http://CRAN.R-project.org/package=nlme>].

R Development Core Team (2014): R version 3.0.3. R: A language and environment for statistical computing. – R Foundation for Statistical Computing, Vienna, Austria.

Schaefer, I., R. A. Norton, S. Scheu & M. Maraun (2010): Arthropod colonization of land – Linking molecules and fossils in oribatid mites (Acari, Oribatida). – Molecular Phylogenetics and Evolution 57(1): 113–121.

Schatz, H., V. M. Behan-Pelletier, B. M. OConnor & R. A. Norton (2011): Suborder Oribatida van der Hammen, 1968. In: Z.-Q. Zhang (ed.): Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. – Zootaxa 3148: 141–148.

Shear, W. A., M. Bonamo, J. D. Grierson, W. D. I. Rolfe, E. L. Smith & R. A. Norton (1984): Early land animals in North America: evidence from Devonian age arthropods from Gilboa, New York. – Science 224: 492–494.

Smelansky, I. E. (2006): Some population characteristics of oribatid mites steppes habitats. – Acarina 14(1): 123–130.

Steinberger, Y., J. A. Wallwork & M. Halimi (1990): Sex ratios and egg production of Zygoribatula spp. (Acari, Cryptostigmata) in the Negev Desert of Southern Israel. – Acarologia 31(1): 85–91.

Subías, L. S. (2004, 2017): Listado sistemático, sinonímico y biogeográfico de los ácaros oribátidos (Acariformes, Oribatida) del mundo (1758-2002). – Graellsia 60:3–305. Actualized in February 2017: 1–598 [http://bba.bioucm.es/cont/docs/RO_1.pdf, doi:10.3989/graellsia.2004.v60.iExtra.218].

Taberly, G. (1987): Recherches sur la parthénogenèse thélytoque de deux espèces d`acariens oríbates: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). III. Etude anatomique, histologique et cytologique des femelles parthénogenétiques. – Acarologia 28: 389–403.

Taberly, G. (1988): Recherches sur la parthénogenèse thélythoque de deux espèces d’acariens oribatides: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). IV Observations sur les mâles ataviques. – Acarologia 29: 95–107.

Tràvnìcek, M. (1989): Laboratory cultivation and biology of mites in the family Liacaridae (Acari: Oribatida). – Acta Universitatis Carolinae – Biologica 33: 69–80.

Walter, D.E. & H. C. Proctor (1999): Mites: Ecology, Evolution, and Behaviour. – University of New South Wales Press.

Webb, N. R. & G. W. Elmes (1979): Variations between populations of Steganacarus magnus (Acari; Cryptostigmata) in Great Britain. – Pedobiologia 19: 390–401.

Weeks, A. R., R. Velten & R. Stouthamer (2003): Incidence of a new sex−ratio−distorting endosymbiotic bacterium among arthropods. – Proceedings of the Royal Society of London B 270: 1857–1865.

Weigmann, G. (1975): Labor- und Freilanduntersuchungen zur Generationsdauer von Orbatiden (Acari: Oribatidei). – Pedobiologia 15: 133–148.

Weigmann, G. (2006): Hornmilben (Oribatida). In: Dahl (ed.) – Tierwelt Deutschlands 76. – Goecke and Evers, Keltern.

Wehner, K., S. Scheu & M. Maraun (2014): Resource availability as driving factor of the reproductive mode in soil microarthropods (Acari, Oribatida). – PlosOne 9(8): e104243 [doi:10.1371/journal.pone.0104243].

Wehner, K., R. A. Norton, N. Blüthgen & M. Heethoff (2016): Specialization of oribatid mites to forest microhabitats – the enigmatic role of litter. – Ecosphere 7(3) [doi10.1002/ecs2.1336].

Wrensch, D. L., J. B. Kethley & R. A. Norton (1994): Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalizations on eukaryotes. In: M. A. Houck (ed.): Mites: Ecological and Evolutionary Analysis of Life-history Patterns. – Chapman and Hall, New York: 282–343.

Downloads

Published

2018-04-01

How to Cite

Wehner, K. ., Heethoff, M., & Brückner, A. (2018). Sex ratios of oribatid mite assemblages differ among microhabitats. SOIL ORGANISMS, 90(1), 13–21. Retrieved from https://soil-organisms.org/index.php/SO/article/view/69

Issue

Section

ARTICLES