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The ecology and evolution of fly dispersed dung mosses (Family Splachnaceae): Manipulating insect behaviour through odour and visual cues

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Abstract

The use of sensory attractants is central to most animal-mediated pollination and seed dispersal interactions. Approximately half the 73 species of mosses’ in the family Splachnaceae are entomophilous (have their spores dispersed by flies) and are coprophilous (grow on feces and carrion). When mature, entomophilous species often produce brightly coloured, scented sporophytes which, for several species, have been shown to attract flies. In a number of cases, sporophyte colours and odours, as well as the flies that visit them, have been shown to be species-specific, suggesting that the mosses co-exist by signal diversification, just as flowering plants are thought to reduce competition for pollinators. Analyses of scent chemistry identified an odour contrast between generations; gametophytes were either unscented or weakly scented in most species, whereas sporophyte odours were universally stronger per unit mass and much more chemically complex. Sporophyte odours of North and South American species sampled were both complex and diverse, with an apparent inverse relationship between the size and showiness of the apophysis and its odour complexity. Furthermore, phylogenetic evidence suggests that fly dispersal of spores through visual and olfactory signals has evolved multiple times in the Splachnaceae and that modifications of sporophyte morphology may have followed, rather than triggered, the transitions to coprophily and entomophily. We review the ecological and evolutionary aspects ofentomophily, with particular emphasis on the chemistry of sporophyte odours and the means by which they mimic decaying organic matter.

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References

  • Anderson, W.R. 1979. Floral conservatism in neotropical Malpighiaceae.Biotropica 11: 219–223.

    Article  Google Scholar 

  • Annentano, T.V. and Caponetti, J.D. 1972. The effect of pH on the growth of protonema ofTetraplodon mnioides and Funaria hygrometrica.The Bryologist 75: 147–153.

    Article  Google Scholar 

  • Bai, X.L. and Tan, B.C. 2000.Tayloria rudimenta (Musci, Splachnaceae), a new speciesfrom Nintgxia Huizu autonomous regionof China.Bryologie 21: 3–5.

    Article  Google Scholar 

  • Banziger, H., Sun, H., and Luo, Y.-B. 2005. Pollination of a slippery lady slipper orchid in south-west China:Cypripedium guttatum (Orchidaceae).Botanical Journal of the Linnean Society 148: 251–264.

    Article  Google Scholar 

  • Bequaert, J. 1921. On the dispersal by flies of the spores of certain mosses of the family Splachnaceae.The Bryologist 24: 1–4.

    Google Scholar 

  • Bickel, D.J. 1985. A revision of the NearcticMedetera (Diptera: Dolichopodidae).U.S. Department of Agriculture. Technical Bulletin 1692: 1–109.

    Google Scholar 

  • Borg-Karlson, A.K., Englund, F.O., and Unelius, C.R. 1994. Dimethyl oligosulphides, major volatiles released fromSauromatum guttatum and Phallus impudicus.Phytochemistry 35: 321–323.

    Article  CAS  Google Scholar 

  • Brotherus, V.F. 1918.Moseniella, un nouveau genre des mousses du Brésil.Arkiv för Botanik utfivet av K. Svenska Vetenskapsakademien 15: 1–3.

    Google Scholar 

  • Brotherus, V.F. 1924. Splachnaceae.Die natürlichen Pflanzenfamilien 10: 333–343.

    Google Scholar 

  • Bryhn, N. 1897. Beobachtungen über das Ausstreuen der Sporen bei den Splachnaceen.Biologisches Centralblatt 17: 48–55.

    Google Scholar 

  • Buchmann, S.L. 1988. The ecology of oil flowers and their bees.Annual Review ofEcology and Systematics 18: 343–369.

    Article  Google Scholar 

  • Cameron, R.G. and Troilo, D. 1982. Fly-mediated spore dispersal inSplachnum ampullaceum (Musci).Michigan Botanist 21: 5965.

    Google Scholar 

  • Cameron, R.G. and Wyatt, R. 1986. Substrate restriction in entomophilous Splachnaceae: role of spore dispersal.The Bryologist 89: 279–284.

    Article  Google Scholar 

  • Cameron, R.G. and Wyatt, R. 1989. Substrate restriction in entomophilous Splachnaceae: II. Effects of hydrogen ion concentration on establishment of gametophytes.The Bryologist 92: 397–404.

    Article  Google Scholar 

  • Crosby, M.R., Magill, R.E., Allen, B., and He, S. 1999. A Checklist of the Mosses.Missouri Botanical Garden.

  • Dafni, A. 1984. Mimicry and deception in pollination.Annual Review ofEcology and Systematics 15: 259–278.

    Article  Google Scholar 

  • Dafni, A., Kevan, P.G., and Husband, B.C., eds. 2005.Practical Pollination Biology. Enviroquest, Cambridge, Canada.

    Google Scholar 

  • Demidova, E.E. and Filin, V.R. 1994. False columella and spore release inTetraplodon angustatus (Hedw.) Bruch et Schimp. in B.S.G. andT. mnioides (Hedw.) Bruch et Schimp. in B.S.G. (Musci. Splachnaceae).Arctoa 3: 1–6.

    Google Scholar 

  • Dobson, H.E.M., Raguso, R.A., Knudsen, J.T., and Ayasse, M. 2005. Scent as an attractant. In:Practical Pollination Biology. Dafni, A., Kevan, P.G., and Husband, B.C., eds. Enviroquest, Cambridge, Canada, pp. 197–230.

    Google Scholar 

  • Dodson, C., Dressler, R., Hills, H., Adams, R., and Williams, N. 1969. Biologically active compounds in orchid fragrances.Science 164: 1243–1249.

    Article  CAS  PubMed  Google Scholar 

  • Donoghue, M.J., Ree, R.H., and Baum, D.A. 1998. Phylogeny and the evolution of flower symmetry in the Asteridae.Trends in Plant Science 3: 311–317.

    Article  Google Scholar 

  • Fife, A. and Goffinet, B. 2003. The identity ofTayloria maidenii.The Bryologist 106: 309–310.

    Article  Google Scholar 

  • Fife, A. and Dalton, J. 2005. A reconsideration ofPleurophascum (Musci: Pleurophascaceae) and specific status for a New Zealand endemic,Pleurophascum ovalifolium stat. et nom. nov.New Zealand Journal of Botany 43: 871–884.

    Article  Google Scholar 

  • Forget, P.M. and Vander Wall, S.B. 2001. Scatter-hoarding rodents and marsupials: convergent evolution on diverging continents.Trends in Ecology & Evolution 16: 65–67.

    Article  Google Scholar 

  • Givnish, T. and Sytsma, K. 1997.Molecular Evolution and Adaptive Radiations. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Goffinet, B., Buck, W.R., Massardo, P., and Rozzi, R. 2006.The Miniature Forests of Cape Horn. Universidad de Magallanes, Punta Arenas, Chile.

    Google Scholar 

  • Goffinet, B. and Shaw, A.J. 2002. Independent ongins of cleistocarpy in the Splachnaceae: analyses of cpDNA sequences reveals polyphyly of the Voitioideae.Systematic Botany 27: 203–208.

    Google Scholar 

  • Goffinet, B., Shaw, A.J., and Cox, C. 2004. Phylogenetic inferences in the dung moss family Splachnaceae from analysis of cpDNA sequence data and implications for the evolution of entomophily.American Journal of Botany 91: 748–759.

    Article  CAS  Google Scholar 

  • Grison-Pigé, L., Hossaert-McKey, M., Greeff, J.M., and Bessiere, J.M. 2002. Fig volatile compounds — a first comparative study.Phytochemistry 61: 61–71.

    Article  PubMed  Google Scholar 

  • Handel, S.N. and Beattie, A.J. 1990. Seed dispersal by ants.Scientific American 262: 76–83.

    Article  Google Scholar 

  • Herrera, C.M. and Pellmyr, O., eds. 2002.Plant-Animal Interactions: An Evolutionary Approach. Blackwell, Oxford

    Google Scholar 

  • Hodges, S.A. 1997. Floral nectar spurs and diversification.International Journal of Plant Science 158: S81-S88.

    Article  Google Scholar 

  • Hughes, L. and Westoby, M. 1992. Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation.Ecology 73: 1285–1299.

    Article  Google Scholar 

  • Janzen, D.H. 1983. Dispersal of seeds by vertebrate guts. In:Coevolution. Futuyrna, D.J. and M. Slatkin, M., eds. Sinauer Associates Inc., Sunderland, pp. 232–262.

    Google Scholar 

  • Jofre, J.P. 2007. Tayloria dubyi: fenología y dispersión de esporas en una especie endemica de musgo de turbera en la Reserva de Biosfera Cabo de Homos.Abstract III Reunión Binacional de Ecología.

  • Johnson, S.D. and Steiner, K.E. 2000. Generalization versus specialization in plant pollination systems.Trends in Ecology & Evolution 15: 140–143.

    Article  Google Scholar 

  • Jürgens, A., Dötterl, S., and Meve, U. 2006. The chemical nature of fetid floral odors in stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae).New Phytologist 172: 452–468.

    Article  PubMed  CAS  Google Scholar 

  • Kaiser, W.M. 1993.The Scent of Orchids: Olfactory and Chemical Investigations. Elsevier, Amsterdam.

    Google Scholar 

  • Keams, C.A. and Inouye, D.W. 1993.Techniques for Pollination Biologists. University of Colorado Press, Boulder, CO.

    Google Scholar 

  • Kevan, P.G. and Baker, H.G. 1983. Insects as flower visitors and pollinators.Annual Review of Ecology and Systematics 28: 407–453.

    Google Scholar 

  • Kite, G.C. 1995. The floral odor ofArum maculatum.Biochemical Systematics and Ecology 23: 452–468.

    Article  Google Scholar 

  • Koponen, A. 1978. The peristome and spores in Splachnaceae and their evolutionary and systematic significance.Bryophytorum Bibliotheca 13: 535–567.

    Google Scholar 

  • Koponen, A. 1979. Entomophily and the classification of the Splachnaceae (Musci).Abstracta Botanica 5 (Supplement): 61.

    Google Scholar 

  • Koponen, A. 1982. The classification of the Splachnaceae.Nova Hedwigia Beiheft 71: 237–245.

    Google Scholar 

  • Koponen, A. 1983. Studies on the generic concept in the classification of the moss family Splachnaceae.Publications from the Department of Botany. University of Helsinki 11: 1–48.

    Google Scholar 

  • Koponen, A. 1990. Entomophily in the Splachnaceae.Botanical Journal of the Linnean Society 104: 115–127.

    Article  Google Scholar 

  • Koponen, A. and Koponen, T. 1977. Evidence of entomophily in Splachnaceae (Bryophyta).Bryophytorum Bibilotheca 13: 569–577.

    Google Scholar 

  • Larson, B.M.H., Kevan, P.G., and Inouye, D.W. 2001. Flies and flowers: taxonomic diversity of anthophiles and pollinators.The Canadian Entomologist 133: 439–465.

    Article  Google Scholar 

  • Levey, D.J., Silva, W.R., and Galetti, M. 2002.Seed Dispersal and Frugivory: Ecology. Evolution. and Conservation. CABI Publishing, Wallingford.

    Google Scholar 

  • Levin, R.A., McDade, L.A., and Raguso, R.A. 2003. The systematic utility of floral and vegetative fragrance in two genera of Nyctaginaceae.Systematic Biology 52: 334–351.

    Article  PubMed  Google Scholar 

  • Li, P., Luo, Y.B., Bernhardt, P., Yang, X.Q., and Kou, Y. 2006. Deceptive pollination of the Lady’s SlipperCypripedium tibeticum (Orchidaceae).Plant Systematics and Evolution 262: 53–63.

    Article  Google Scholar 

  • Marino, P.C. 1988a. Coexistence on divided habitats: mosses in the family Splachnaceae.Annales Zoologici Fennici 25: 89–98.

    Google Scholar 

  • Marino, P.C. 1988b. The North American distribution of the circumboreal species ofSplachnum and Tetraplodon.The Bryologist 91: 161–166.

    Article  Google Scholar 

  • Marino, P.C. 1991a. Competition between mosses (Splachnaceae) in patchy habitats.Journal of Ecology 79: 1031–1046.

    Article  Google Scholar 

  • Marino, P.C. 1991b. Dispersal and coexistence of mosses (Splachnaceae) in patchy habitats.Journal of Ecology 79: 1047–1060.

    Article  Google Scholar 

  • Marino, P.C. 1997. Competition, dispersal and coexistence of Splachnaceae in patchy habitats. In:Advances in Bryology. Longton, R.A., ed. J. Cramer, Berlin.

    Google Scholar 

  • Marino, P.C., Raguso, R.A., and Goffinet, B. In prep. Chemical communication, signal mimicry and exploitation of flies bySplachnum ampullaceum.

  • McAlpine, J.F., Peterson, B.V., Shewell, G.E., Teskey, H.J., Vockeroth, J.R., and Wood, D.M., eds. 1981.Manual of the Nearctic Diptera. Volume 1, 2. Agriculture Canada Monograph.

  • Nathan, R. and Muller-Landau, H.C. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment.Trends in Ecology & Evolution 15: 278–285.

    Article  Google Scholar 

  • Olesen, J.M., Bascornpte, J., Dupont, Y., and Jordano, P. 2007. The modularity of pollination networks.Proceedings National Academy of Science 104: 19891–19896.

    Article  CAS  Google Scholar 

  • Patiño, S., Grace, J., and Bänziger, H. 2000. Endothermy by flowers ofRhizanthes lowii (Rafflesiaceae).Oecologia 124: 149–155.

    Article  Google Scholar 

  • Proctor, M., Yeo, P., and Lack, A. 1996.The Natural History of Pollination. Timber Press, Portland, Oregon.

    Google Scholar 

  • Pyysalo, H., Koponen, A., and Koponen, T. 1978. Studies on entomophily in Splachnaceae (Musci). 1. Volatile compounds in the sporophytes.Annales Botanici Fennici 15: 293–296.

    CAS  Google Scholar 

  • Pyysalo, H., Koponen, A., and Koponen, T. 1983. Studies on entomophily in Splachnaceae (Musci). II. Volatile compounds in the hypophysis.Annales Botanici Fennici 20: 335–338.

    CAS  Google Scholar 

  • Raguso, R.A. 2008. Ecology and evolution of floral fragrances.Annual Review of Ecology, Evolution, and Systematics 39: in press.

  • Raguso, R.A., Levin, R.A., Foose, S.E., Holmberg, M.W., and McDade, L.A. 2003. Fragrance chemistry, nocturnal rhythms and pollination “syndromes” inNicotiana.Phytochemistry 63: 265–284.

    Article  CAS  PubMed  Google Scholar 

  • Raguso, R.A. and Pellmyr, O. 1998. Dynamic headspace analysis of floral volatiles: a comparison of methods.Oikos 81: 238–254.

    Article  CAS  Google Scholar 

  • Roy, B.A. and Raguso, R.A. 1997. Olfactory versus visual cues in a floral mimicry system.Oecologia 109: 1432–1939.

    Article  Google Scholar 

  • Roy, B.A. and Widmer, A. 1999. Floral mimicry: a fascinating yet poorly understood phenomenon.Trends in Plant Science 4: 325–330.

    Article  PubMed  Google Scholar 

  • Rozkosny, R. 1984.The Sciomyzidae (Diptera) of Fennoscandia and Denmark. E.J. Brill/Scandinavian Science Press Ltd., Leiden, Copenhagen.

    Google Scholar 

  • Salzmann, C.C., Brown, A., and Schiestl, F.P. 2006. Floral scent emission and pollination syndromes: evolutionary changes from food to sexual deception.International Journal of Plant Science 167: 1197–1204.

    Article  Google Scholar 

  • Schaefer, H.M., Schaefer, V., and Levey, D.J. 2004. How plantanimal interactions signal new insights in communication.Trends in Ecology & Evolution 19: 577–584.

    Article  Google Scholar 

  • Schiestl, F.P. 2005. On the success of a swindle: pollination by deception in orchids.Naturwissenschaften 92: 1432–1904.

    Article  CAS  Google Scholar 

  • Sleeman, D.P., Jones, P., and Cronin, J.N. 1997. Investigations of an association between the stinkhorn fungus and badger setts.Journal of Natural History 31: 983–992.

    Article  Google Scholar 

  • Sorensen, A.E. 1986. Seed dispersal by adhesion.Annual Review of Ecology and Systematics 17: 443–463.

    Article  Google Scholar 

  • Stebbins, G.L. 1970. Adaptive radiation of reproductive characteristics in angiosperms. I: Pollination mechanisms.Annual Review of Ecology and Systematics 1: 307–326.

    Article  Google Scholar 

  • Stensrnyr, M., Urru, J., Collu, J., Celander, M., Hansson, B.S., and Angioy, A.M. 2002. Rotting smell of dead horse arum florets.Nature 429: 625–626.

    Article  CAS  Google Scholar 

  • Troilo, D. and Cameron, R.G. 1981. Comparative behavior of Pyrellia cyanicolor (Diptera: Muscidae) on the mossSplachnum ampullaceum and on substrates of nutritional value.Great Lakes Entomologist 14: 191–195.

    Google Scholar 

  • Tuno, N. 1998. Spore dispersal ofDictyophora fungi (Phallaceae).Ecological Research 13: 7–15.

    Article  Google Scholar 

  • Ulrich, H. 2005. Predation by adult Dolichopodidae (Diptera): a review of literature with an annotated prey-predator list.Studia Dipterologica 11: 1–60.

    Google Scholar 

  • Vander Wall, S.B., Borchert, M.I., and Gworek, J.R. 2006. Secondary dispersal of bigcone Douglas-fir (Pseudotsuga macrocarpa) seeds.Acta Oecologica 30: 100–106.

    Article  Google Scholar 

  • Vitt, D.H. 1981. Adaptive modes of the moss sporophyte.The Bryologist 84: 166–186.

    Article  Google Scholar 

  • Vitt, D.H. 1984. Classification of the Bryopsida. In:New Manual of Bryology. Vol. 2. Schuster, R.M., ed. Hattori Botanical Laboratory, Nichinan, Japan, pp. 696–759.

    Google Scholar 

  • Wenny, D.G. 2001. Advantages of seed dispersal: a re-evalution of directed dispersal.Evolutionary Ecology Research 3: 51–74.

    Google Scholar 

  • Wenny, D.G. and Levey, D.J. 1998. Directed seed dispersal by bellbirds in a tropical cloud forest.Proceedings National Academy of Science 95: 6204–6207.

    Article  CAS  Google Scholar 

  • Wettstein, F.V. 1921. Splachnaceen Studien. I. Entomophilie und Spaltöffnungsapparat.Oesterreich Botanik Zeitschrift 70: 65–77.

    Article  Google Scholar 

  • Whittle, C.L., Bowyer, R.T., Clausen, T.P., and Duffy, L.K. 2000. Putative pheromones in urine of rutting male moose (Alces alces): Evolution of honest advertisement?Journal of Chemical Ecology 26: 2747–2762.

    Article  CAS  Google Scholar 

  • Zoller, H., Lenzin, H., and Erhardt, A. 2002. Pollination and breeding system ofEritrichium nanum (Boraginaceae).Plant Systematics and Evolution 233: 1–14.

    Article  Google Scholar 

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  1. Department of Biology, Memorial University, AlB 3X9, St. John’s, NL, Canada

    Paul Marino

  2. Department of Neurobiology and Behavior, Seeley G. Mudd Hall, Cornell University, 14853-2702, Ithaca, NY, USA

    Robert Raguso

  3. Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Road, 06269-3043, Storrs, CT, USA

    Bernard Goffinet

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Marino, P., Raguso, R. & Goffinet, B. The ecology and evolution of fly dispersed dung mosses (Family Splachnaceae): Manipulating insect behaviour through odour and visual cues. Symbiosis 47, 61–76 (2009). https://doi.org/10.1007/BF03182289

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