Intrataxonomic differences in terms of angiosperm suitability for herbivorous insects stem from variables such as plant structure, palatability, and chemistry. It has not yet been elucidated whether these differences also occur in terms of the bryophyte's suitability to bryophages. Hypnum cupressiforme Hedw. is a morphologically variable moss species frequently inhabited or fed by insects. In this investigation, we offered five morphotypes of H. cupressiforme to two bryophagous species of Byrrhidae (Coleoptera) to reveal whether the intrataxonomic variability affects beetles' preferences. The morphotypes were offered with preserved and removed spatial structures. There were no significant differences in morphotype preferences when spatial structures were preserved, although during the daytime, the beetles moved from the flat morphotype to the usual and turgid morphotypes. The beetles preferred the turgid morphotype when the spatial structures were removed. The results suggest that the spatial structure variations in the H. cupressiforme complex are accompanied by different chemical, physiological, or microscopic morphological profiles that are recognized by the bryophagous insects. Phylogenetic and epigenetic analyses can reveal multiple differences within the H. cupressiforme complex. Their interconnection with information about the preferences of bryophagous insects can help us to elucidate which of these differences are ecologically relevant.

Department of Biology and Ecology Institute of Environmental Technologies Faculty of Science University of Ostrava Chittussiho 10 710 00 Ostrava Czech Republic

Heyrovsky High School of Chemistry Středoškolská 2854 1 700 30 Ostrava Czech Republic

See more in PubMed

Basset Y. Local Communities of Arboreal Herbivores in Papua New Guinea: Predictors of Insect Variables. Ecology. 1996;77:1906–1919. doi: 10.2307/2265794. DOI

Videla M., Valladares G., Salvo A. A Tritrophic Analysis of Host Preference and Performance in a Polyphagous Leafminer. Entomol. Exp. Appl. 2006;121:105–114. doi: 10.1111/j.1570-8703.2006.00448.x. DOI

Wiklund C., Friberg M. The Evolutionary Ecology of Generalization: Among-Year Variation in Host Plant Use and Offspring Survival in a Butterfly. Ecology. 2009;90:3406–3417. doi: 10.1890/08-1138.1. PubMed DOI

Whitham T.G., Gehring C.A., Lamit L.J., Wojtowicz T., Evans L.M., Keith A.R., Smith D.S. Community Specificity: Life and Afterlife Effects of Genes. Trends Plant Sci. 2012;17:271–281. doi: 10.1016/j.tplants.2012.01.005. PubMed DOI

Maddox G.D., Root R.B. Structure of the Encounter between Goldenrod (Solidago altissima) and Its Diverse Insect Fauna. Ecology. 1990;71:2115–2124. doi: 10.2307/1938625. DOI

Agrawal A.A. Plant Defense and Density Dependence in the Population Growth of Herbivores. Am. Nat. 2004;164:113–120. doi: 10.1086/420980. PubMed DOI

Utsumi S., Nakamura M., Ohgushi T. Community Consequences of Herbivore-Induced Bottom–up Trophic Cascades: The Importance of Resource Heterogeneity. J. Anim. Ecol. 2009;78:953–963. doi: 10.1111/j.1365-2656.2009.01570.x. PubMed DOI

Meloni F., Lopes N.P., Varanda E.M. The Relationship between Leaf Nitrogen, Nitrogen Metabolites and Herbivory in Two Species of Nyctaginaceae from the Brazilian Cerrado. Environ. Exp. Bot. 2012;75:268–276. doi: 10.1016/j.envexpbot.2011.07.010. DOI

Sosnovsky Y. Sucking Herbivore Assemblage Composition on Greenhouse Ficus Correlates with Host Plant Leaf Architecture. Arthropod Plant Interact. 2016;10:55–69. doi: 10.1007/s11829-015-9408-6. DOI

Linhart Y.B., Grant M.C. Evolutionary Significance of Local Genetic Differentiation in Plants. Annu. Rev. Ecol. Syst. 1996;27:237–277. doi: 10.1146/annurev.ecolsys.27.1.237. DOI

Parker M.A. Disease Impact and Local Genetic Diversity in the Clonal Plant Podophyllum peltatum. Evolution. 1989;43:540–547. doi: 10.1111/j.1558-5646.1989.tb04250.x. PubMed DOI

Fritz R.S., Simms E.L. Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press; Chicago, IL, USA: 1992.

Michalakis Y., Sheppard A.W., Noel V., Olivieri I. Population Structure of a Herbivorous Insect and Its Host Plant on a Microgeographic Scale. Evolution. 1993;47:1611–1616. doi: 10.1111/j.1558-5646.1993.tb02180.x. PubMed DOI

De Vries J., Evers J.B., Poelman E.H. Dynamic Plant–Plant–Herbivore Interactions Govern Plant Growth–Defence Integration. Trends Plant Sci. 2017;22:329–337. doi: 10.1016/j.tplants.2016.12.006. PubMed DOI

Scriber M.J. Latitudinal and Local Geographic Mosaics in Host Plant Preferences as Shaped by Thermal Units and Voltinism in Papilio spp. (Lepidoptera) Eur. J. Entomol. 2002;99:225. doi: 10.14411/eje.2002.032. DOI

Scriber M.J., Lederhouse R.C. The Thermal Environment as a Resource Dictating Geographic Patterns of Feeding Specialization of Insect Herbivores. In: Hunter M.R., Ohgushi T., Price P.W., editors. Effects of Resource Distribution on Animal-Plant Interactions. Academic Press; New York, NY, USA: 1992. pp. 429–466.

Cronin J.T., Abrahamson W.G., Craig T.P. Temporal Variation in Herbivore Host-Plant Preference and Performance: Constraints on Host-Plant Adaptation. Oikos. 2001;93:312–320. doi: 10.1034/j.1600-0706.2001.930214.x. DOI

Frahm J.P. A Preliminary Study of the Infraspecific Taxa of Hypnum cupressiforme in Europe. Arch. Bryol. 2009;40:1–10.

Ando H. Hypnum cupressiforme Hedw. and Its Close Allies in Europe. Abstr. Bot. 1985;9:11–18.

Ando H. Studies on the Genus Hypnum (VI) Hikobia. 1989;10:269–291.

Schlesak S., Hedenäs L., Nebel M., Quandt D. Cleaning a Taxonomic Dustbin: Placing the European Hypnum Species in a Phylogenetic Context! Bryophyte Divers. Evol. 2018;40:37–54. doi: 10.11646/bde.40.2.3. DOI

Kučera J., Kuznetsova O.I., Manukjanová A., Ignatov M.S. A Phylogenetic Revision of the Genus Hypnum: Towards Completion. TAXON. 2019;68:628–660. doi: 10.1002/tax.12095. DOI

Horning D.S., Schuster R.O., Grigarick A.A. Tardigrada of New Zealand. N. Z. J. Zool. 1978;5:185–280. doi: 10.1080/03014223.1978.10428316. DOI

Božanić B., Hradílek Z., Machač O., Pižl V., Št’áhlavskỳ F., Tufová J., Véle A., Tuf I.H. Factors Affecting Invertebrate Assemblages in Bryophytes of the Litovelské Luhy National Nature Reserve, Czech Republic. Acta Zool. Bulg. 2013;65:197–206.

Lazarova S., Peneva V., Penev L. Nematode Assemblages from the Moss Hypnum cupressiforme Hedw. Growing on Different Substrates in a Balkanic Durmast Oak Forest (Quercus dalechampii Ten.) on Mount Vitosha, Bulgaria. Nematology. 2000;2:263–272.

Varga J. Analysis of the Bryofauna of Some Moss Species. Sci. Bull. Uzhhorod Univ. Ser. Biol. 2008;23:264–265.

Hallas T.E. Interstitial Water and Tardigrada in a Moss Cushion. Ann. Zool. Fenn. 1975;12:255–259.

Degma P., Simurka M., Gulánová S. Community Structure and Ecological Macrodistribution of Moss-Dwelling Water Bears (Tardigrada) in Central European Oak-Hornbeam Forests (SW Slovakia) Ekológia. 2005;24:59.

Degma P., Katina S., Sabatovičová L. Horizontal Distribution of Moisture and Tardigrada in a Single Moss Cushion. J. Zool. Syst. Evol. Res. 2011;49:71–77. doi: 10.1111/j.1439-0469.2010.00602.x. DOI

Dunk K. Lebensraum Moospolster. Mikrokosmos. 1979;68:125–131.

Traser G., Szűcs P., Winkler D. Collembola Diversity of Moss Habitats in the Sopron Region, NW-Hungary. Acta Silv. Lignaria Hung. 2006;2:69–80.

Hajer J., Malý J., Hrubá L., Řeháková D. Egg Sac Silk of Theridiosoma gemmosum (Araneae: Theridiosomatidae) J. Morphol. 2009;270:1269–1283. doi: 10.1002/jmor.10757. PubMed DOI

Lungu-Constantineanu C.Ş., Constantineanu R. New Data on Ichneumonid Hibernation (Hymenoptera: Ichneumonidae) in the Bârnova Forest Massif (Iaşi County, Romania) Romanian J. Biol. 2014;59:11–16.

Verdcourt B. A Note on the Food of Acridium Geoff. (Orthopt.) Entomol. Mon. Mag. 1947;83:190.

Konstantinov A., Chamorro M.L., Prathapan K.D., Ge S.-Q., Yang X.-K. Moss-Inhabiting Flea Beetles (Coleoptera: Chrysomelidae: Galerucinae: Alticini) with Description of a New Genus from Cangshan, China. J. Nat. Hist. 2013;47:2459–2477. doi: 10.1080/00222933.2012.763068. DOI

Boukal M. Brouci Čeledi Haliplidae (Plavčíkovití) Střední Evropy; Brouci Čeledi Byrrhidae (Vyklenulcovití) Střední Evropy. Academia; Prague, Czech: 2017.

Pyszko P., Plášek V., Drozd P. Don’t Eat Where You Sleep: Unexpected Diversity of Food Web for Beetles Feeding on Mosses. Insect Conserv. Divers. 2020 doi: 10.1111/icad.12453. DOI

Gerson U. Moss-Arthropod Associations. The Bryologist. 1969;72:495–500. doi: 10.1639/0007-2745(1969)72[495:MA]2.0.CO;2. DOI

Rutten A.L.M. The Genus Bryotropha in the Netherlands (Lepidoptera: Gelechiidae) Ned. Faun. Meded. 1999;9:79–102.

Slamka F. Pyraloidea (Lepidoptera) of Central Europe: Identification, Distribution, Habitat, Biology. František Slamka; Bratislava, Slovakia: 2010.

Faber J., Ma W.C. Observations on Seasonal Dynamics in Diet Composition of the Field Vole, Microtus agrestis, with Some Methodological Remarks. Acta Theriol. 1986;31:479–490. doi: 10.4098/AT.arch.86-43. DOI

Heinken T., Rohner M.-S., Hoppert M. Red Wood Ants (Formica rufa Group) Disperse Bryophyte and Lichen Fragments on a Local Scale. Nova Hedw. 2007;131:147–163.

Van Laar V., Dirkse G.M. Bladmossen En Korstmossen Als Nestmateriaal van Kleine Zoogdiersoorten. Buxbaumiella. 2010;85:36–41.

Hříbek M. The Use Species of Moss (Bryophyta Sp.) in the Building of Nests the Great Tits (Parus major L., 1758) and Blue Tit (Parus caeruleus L., 1758) Zprávy Morav. Ornitol. Sdruž. 1985;43:39–45.

Wesolowski T., Wierzcholska S. Tits as Bryologists: Patterns of Bryophyte Use in Nests of Three Species Cohabiting a Primeval Forest. J. Ornithol. 2018;159:733–745. doi: 10.1007/s10336-018-1535-2. DOI

Alpert P. Microtopography as Habitat Structure for Mosses on Rocks. In: Bell S.S., McCoy E.D., Mushinsky H.R., editors. Habitat Structure: The Physical Arrangement of Objects in Space. Springer; Dordrecht, The Netherlands: 1991. pp. 120–140. (Population and Community Biology Series).

Kinchin I.M. An Introduction to the Invertebrate Microfauna Associated with Mosses and Lichens, with Observations from Maritime Lichens on the West Coast of the British Isles. Microscopy. 1992;36:721–731.

Brusven M.A., Meehan W.R., Biggam R.C. The Role of Aquatic Moss on Community Composition and Drift of Fish-Food Organisms. Hydrobiologia. 1990;196:39–50. doi: 10.1007/BF00008891. DOI

Smith R.M., Young M.R., Marquiss M. Bryophyte Use by an Insect Herbivore: Does the Crane-Fly Tipula montana Select Food to Maximise Growth? Ecol. Entomol. 2001;26:83–90. doi: 10.1046/j.1365-2311.2001.00297.x. DOI

Hodgetts N.G., Söderström L., Blockeel T.L., Caspari S., Ignatov M.S., Konstantinova N.A., Lockhart N., Papp B., Schröck C., Sim-Sim M., et al. An Annotated Checklist of Bryophytes of Europe, Macaronesia and Cyprus. J. Bryol. 2020;42:1–116. doi: 10.1080/03736687.2019.1694329. DOI

Yan J. Geepack: Yet Another Package for Generalized Estimating Equations. R-News. 2002;2:12–14.

Yan J., Fine J. Estimating Equations for Association Structures. Stat. Med. 2004;23:859–874. doi: 10.1002/sim.1650. PubMed DOI

Halekoh U., Højsgaard S., Yan J. The R Package Geepack for Generalized Estimating Equations. J. Stat. Softw. 2006;15:1–11. doi: 10.18637/jss.v015.i02. DOI

Thall P.F., Vail S.C. Some Covariance Models for Longitudinal Count Data with Overdispersion. Biometrics. 1990:657–671. doi: 10.2307/2532086. PubMed DOI

Pan W. Akaike’s Information Criterion in Generalized Estimating Equations. Biometrics. 2001;57:120–125. doi: 10.1111/j.0006-341X.2001.00120.x. PubMed DOI

Hin L.-Y., Wang Y.-G. Working-Correlation-Structure Identification in Generalized Estimating Equations. Stat. Med. 2009;28:642–658. doi: 10.1002/sim.3489. PubMed DOI

Morales M. [(accessed on 28 February 2021)];Sciplot: Scientific Graphing Functions for Factorial Designs. 2020 R Package Version 1.2-0. Available online: https://CRAN.R-project.org/package=sciplot.

Cleveland W.S., Grosse E., Shyu W.M. In: Local Regression Models. Chapter 8 in Statistical Models in S. Chambers J.M., Hastie T.J., editors. Routledge; Boca Raton, FL, USA: 1992. p. 624.

Kočárek P., Grucmanová Š., Filipcová Z., Bradová L., Plášek V., Holuša J. Bryophagy in the Groundhopper Tetrix ceperoi (Orthoptera: Tetrigidae): Analysis of Alimentary Tract Contents. Scripra Fac. Rerum Nat. Univ. Ostrav. 2008;186:348–352.

Mattson W.J., Haack R.A. The Role of Drought Stress in Provoking Outbreaks of Phytophagous Insects. Insect Outbreaks. 1987:365–407. doi: 10.1016/b978-0-12-078148-5.50019-1. DOI

Larsson S. Stressful Times for the Plant Stress: Insect Performance Hypothesis. Oikos. 1989:277–283. doi: 10.2307/3565348. DOI

Glime J.M. Bryophytes as Homes for Stream Insects. Hikobia. 1994;11:483–498.

Haines W.P., Renwick J.A.A. Bryophytes as Food: Comparative Consumption and Utilization of Mosses by a Generalist Insect Herbivore. Entomol. Exp. Appl. 2009;133:296–306. doi: 10.1111/j.1570-7458.2009.00929.x. DOI

Henrikson B.-I. Sphagnum Mosses as a Microhabitat for Invertebrates in Acidified Lakes and the Colour Adaptation and Substrate Preference in Leucorrhinia dubia (Odonata, Anisoptera) Ecography. 1993;16:143–153. doi: 10.1111/j.1600-0587.1993.tb00066.x. DOI

Merrifield K., Ingham R.E. Nematodes and Other Aquatic Invertebrates in Eurhynchium oreganum from Mary’s Peak, Oregon Coast Range. Bryol. 1998;101:505–511. doi: 10.1639/0007-2745(1998)101[505:NAOAII]2.0.CO;2. DOI

Penny N.D. A Systematic Study of the Family Boreidae (Mecoptera) [New Taxa, North America] Univ. Kans. Sci. Bull. USA. 1977;51:141–217.

Rice S.K., Collins D., Anderson A.M. Functional Significance of Variation in Bryophyte Canopy Structure. Am. J. Bot. 2001;88:1568–1576. doi: 10.2307/3558400. PubMed DOI

Caldwell M.M., Flint S.D. Stratospheric Ozone Reduction, Solar UV-B Radiation and Terrestrial Ecosystems. Clim. Chang. 1994;28:375–394. doi: 10.1007/BF01104080. DOI

Filella I., Peñuelas J. Altitudinal Differences in UV Absorbance, UV Reflectance and Related Morphological Traits of Quercus ilex and Rhododendron ferrugineum in the Mediterranean Region. Plant Ecol. 1999;145:157–165. doi: 10.1023/A:1009826803540. DOI

Hultine K.R., Marshall J.D. Altitude Trends in Conifer Leaf Morphology and Stable Carbon Isotope Composition. Oecologia. 2000;123:32–40. doi: 10.1007/s004420050986. PubMed DOI

Caldwell M.M., Bornman J.F., Ballaré C.L., Flint S.D., Kulandaivelu G. Terrestrial Ecosystems, Increased Solar Ultraviolet Radiation, and Interactions with Other Climate Change Factors. Photochem. Photobiol. Sci. 2007;6:252–266. doi: 10.1039/b700019g. PubMed DOI

Gehrke C. Impacts of Enhanced Ultraviolet-B Radiation on Mosses in a Subarctic Heath Ecosystem. Ecology. 1999;80:1844–1851. doi: 10.1890/0012-9658(1999)080[1844:IOEUBR]2.0.CO;2. DOI

Rozema J., Björn L.O., Bornman J.F., Gaberščik A., Häder D.-P., Trošt T., Germ M., Klisch M., Gröniger A., Sinha R.P., et al. The Role of UV-B Radiation in Aquatic and Terrestrial Ecosystems—an Experimental and Functional Analysis of the Evolution of UV-Absorbing Compounds. J. Photochem. Photobiol. B. 2002;66:2–12. doi: 10.1016/S1011-1344(01)00269-X. PubMed DOI

Robinson S.A., Turnbull J.D., Lovelock C.E. Impact of Changes in Natural Ultraviolet Radiation on Pigment Composition, Physiological and Morphological Characteristics of the Antarctic Moss, Grimmia antarctici. Glob. Chang. Biol. 2005;11:476–489. doi: 10.1111/j.1365-2486.2005.00911.x. DOI

Rozema J., Boelen P., Solheim B., Zielke M., Buskens A., Doorenbosch M., Fijn R., Herder J., Callaghan T., Björn L.O., et al. Stratospheric Ozone Depletion: High Arctic Tundra Plant Growth on Svalbard is Not Affected by Enhanced UV-B after 7 Years of UV-B Supplementation in the Field. In: Rozema J., Aerts R., Cornelissen H., editors. Plants and Climate Change. Springer; Dordrecht, The Netherlands: 2006. pp. 121–136. Tasks for Vegetation Science.

Hudaib M., Aburjai T. Volatile Components of Thymus vulgaris L. from Wild-Growing and Cultivated Plants in Jordan. Flavour Fragr. J. 2007;22:322–327. doi: 10.1002/ffj.1800. DOI

Bozoudi D., Claps S., Abraham E.M., Parissi Z.M., Litopoulou-Tzanetaki E. Volatile Organic Compounds of Mountainous Plant Species and the Produced Milk as Affected by Altitude in Greece: A Preliminary Study. Int. J. Dairy Technol. 2019;72:159–164. doi: 10.1111/1471-0307.12573. DOI

Üçüncü O., Cansu T.B., Özdemïr T., Karaoğlu Ş.A., Yayli N. Chemical Composition and Antimicrobial Activity of the Essential Oils of Mosses (Tortula muralis Hedw., Homalothecium lutescens (Hedw.) H. Rob., Hypnum cupressiforme Hedw., and Pohlia nutans (Hedw.) Lindb.) from Turkey. Turk. J. Chem. 2010;34:825–834.

Liu X., Zhang G., Jones K.C., Li X., Peng X., Qi S. Compositional Fractionation of Polycyclic Aromatic Hydrocarbons (PAHs) in Mosses (Hypnum plumaeformae WILS.) from the Northern Slope of Nanling Mountains, South China. Atmos. Environ. 2005;39:5490–5499. doi: 10.1016/j.atmosenv.2005.05.048. DOI

Zhang C., Feng Y., Liu Y., Chang H., Li Z., Xue J. Uptake and Translocation of Organic Pollutants in Plants: A Review. J. Integr. Agric. 2017;16:1659–1668. doi: 10.1016/S2095-3119(16)61590-3. DOI

Russel L.K. A New Genus and a New Species of Boreidae from Oregon (Mecoptera) Proc. Ent. Soc. Wash. 1979;82:22–31.

Spagnuolo V., Terracciano S., Cobianchi R.C., Giordano S. Taxonomy of the Hypnum cupressiforme Complex in Italy Based on ITS and TrnL Sequences and ISSR Markers. J. Bryol. 2008;30:283–289. doi: 10.1179/174328208X300750. DOI

Kuřavová K., Hajduková L., Kočárek P. Age-Related Mandible Abrasion in the Groundhopper Tetrix tenuicornis (Tetrigidae, Orthoptera) Arthropod Struct. Dev. 2014;43:187–192. doi: 10.1016/j.asd.2014.02.002. PubMed DOI

Schoonhoven L.M., Jermy T., Van Loon J.J.A. Insect-Plant Biology. Springer; Berlin/Heidelberg, Germany: 1998. Host-Plant Selection: How to Find a Host Plant; pp. 121–153.

Sardans J., Peñuelas J. Drought Changes Nutrient Sources, Content and Stoichiometry in the Bryophyte Hypnum cupressiforme Hedw. Growing in a Mediterranean Forest. J. Bryol. 2008;30:59–65. doi: 10.1179/174328208X281987. DOI

Van Hoof L., Vanden Berghe D.A., Petit E., Vlietinck A.J. Antimicrobial and Antiviral Screening of Bryophyta. Fitoterapia. 1981;52:223–229.

Abay G., Karakoç Ö.C., Tüfekçi A.R., Koldaş S., Demirtas I. Insecticidal Activity of Hypnum cupressiforme (Bryophyta) against Sitophilus granarius (Coleoptera: Curculionidae) J. Stored Prod. Res. 2012;51:6–10. doi: 10.1016/j.jspr.2012.05.005. DOI

Asakawa Y. Biologically Active Compounds from Bryophytes. Pure Appl. Chem. 2007;79:557–580. doi: 10.1351/pac200779040557. DOI

Acosta-Mercado D., Cancel-Morales N., Chinea J.D., Santos-Flores C.J., De Jesús I.S. Could the Canopy Structure of Bryophytes Serve as an Indicator of Microbial Biodiversity? A Test for Testate Amoebae and Microcrustaceans from a Subtropical Cloud Forest in Dominican Republic. Microb. Ecol. 2012;64:200–213. doi: 10.1007/s00248-011-0004-8. PubMed DOI

Pyszko P., Šigut M., Kostovčík M., Drozd P., Hulcr J. High-Diversity Microbiomes in the Guts of Bryophagous Beetles (Coleoptera: Byrrhidae) Eur. J. Entomol. 2019;116:432–441. doi: 10.14411/eje.2019.044. DOI

Pyszko P., Višňovská D., Drgová M., Šigut M., Drozd P. Effect of Bacterial and Fungal Microbiota Removal on the Survival and Development of Bryophagous Beetles. Environ. Entomol. 2020;49:902–911. doi: 10.1093/ee/nvaa060. PubMed DOI

Alonso C., Ramos-Cruz D., Becker C. The Role of Plant Epigenetics in Biotic Interactions. New Phytol. 2019;221:731–737. doi: 10.1111/nph.15408. PubMed DOI PMC

Pikaard C.S., Mittelsten Scheid O. Epigenetic Regulation in Plants. Cold Spring Harb. Perspect. Biol. 2014;6 doi: 10.1101/cshperspect.a019315. PubMed DOI PMC

Non-Random Distribution of Boreus hyemalis Among Bryophyte Hosts: Evidence from Field and Laboratory Tests