Exploring the intricacies of bryophyte reproduction:
life cycles, sexual dynamics, and reproductive strategies
DOI:
https://doi.org/10.35699/2675-5327.2024.48846Keywords:
liverworts, hornworts, mosses, sexual reproduction, asexual reproduction, plant life cycles, plant life strategiesAbstract
This review presents a comprehensive examination of bryophyte reproductive biology, an area pivotal to understanding these unique land plants. We delve into the morphological intricacies of both sexual and asexual reproductive structures in bryophytes, underscoring their integral roles in the life cycles of these organisms. Our discussion encompasses the diverse sexual systems observed in bryophytes, ranging from monoicous to dioicous configurations, and investigates the patterns and ecological consequences of sex ratios, particularly the commonly observed female-biased ratios. In detailing reproductive strategies, the review evaluates the reproductive investments, efforts, and costs associated with these ratios in various species. Such analysis provides insights into the evolutionary and ecological dynamics shaping bryophyte populations. We also highlight the primary types of asexual reproductive structures, such as gemmae and leafy propagula, providing examples that illustrate their importance in bryophyte life strategies, especially in terms of dispersal capabilities and habitat colonization. Furthermore, the review juxtaposes the advantages and disadvantages of sexual and asexual reproduction, considering their implications for the distribution, genetic diversity, and conservation of bryophyte species. This comparison sheds light on the adaptive significance of these reproductive modes in response to environmental pressures and habitat variability. To aid in the understanding of specialized terms and concepts, the review includes a brief glossary of key terminology used in bryophyte reproductive biology. This addition makes the paper accessible to a diverse audience, ranging from academic researchers to students and enthusiasts in the field of botany. Overall, this review offers an insightful and thorough exploration of the reproductive strategies of bryophytes, enhancing our understanding of their complex life cycles and the implications for their survival and proliferation in varied ecosystems.
References
Allen, B.H. & Magill, R.E. (1987) Support of a distinct terminology for bryophyte sexuality. Taxon, 36, 57–58.
Allen, N.S. (1991) A preliminary treatment of the Central American species of Octoblepharum (Musci: Calymperaceae). Tropical Bryology, 4, 85–97.
Alvarenga, L.D.P., Pôrto, K.C. & Zartman, C.E. (2013) Sex ratio, spatial segregation, and fertilization rates of the epiphyllous moss Crossomitrium patrisiae (Brid.) Müll. Hal. in the Brazilian Atlantic rainforest. Journal of Bryology, 35, 88–95.
Alvarenga, L.D.P., Pôrto, K.C. & Silva, M.P.P. (2009) Relations between regional–local habitat loss and metapopulation properties of epiphyllous bryophytes in the Brazilian Atlantic Forest. Biotropica, 41, 682–691.
Anderson, L.E. (1980) Cytology and reproductive biology of mosses. In: Taylor, R.J. & Leviton, A.E. (Eds.), The Mosses of North America. San Francisco, American Association for the Advancement of Science, pp. 37–76.
Benassi M., Stark L.R., Brinda J.C., McLetchie D.N., Bonine M. & Mishler B.D. (2011) Plant size, sex expression and sexual reproduction along an elevation gradient in a desert moss. The Bryologist, 114, 277–288.
Bisang I., Ehrlén J. & Hedenäs L. (2006) Reproductive effort and costs of reproduction do not explain female‐biased sex ratios in the moss Pseudocalliergon trifarium (Amblystegiaceae). American Journal of Botany, 93, 1313–1319.
Bisang I., Ehrlén J., Persson C., Hedenäs L. (2014) Family affiliation, sex ratio and sporophyte frequency in unisexual mosses. Botanical Journal of the Linnean Society, 174, 163–172.
Bisang I., Hedenäs L. (2013) Males are not shy in the wetland moss Drepanocladus lycopodioides. International Journal of Plant Sciences, 174, 733–739.
Bisang I. & Hedenäs L. (2005) Sex ratio patterns in dioicous bryophytes re-visited. Journal of Bryology, 27, 207–219.
Bowker M.A., Stark L.R., McLetchie D.N. & Mishler B.D. (2000) Sex expression, skewed sex ratios, and microhabitat distribution in the dioecious desert moss Syntrichia caninervis (Pottiaceae). American Journal of Botany, 87, 517–526.
Brzyski, J.R., Wade, T. & McLetchie, D.N. (2014) Reproductive allocation between the sexes, across natural and novel habitats, and its impact on genetic diversity. Evolutionary Ecology, 28, 247–261.
Casanova-Katny, A., Torres-Mellado, G.A. & Eppley, S.M. (2016) Reproductive output of mosses under experimental warming on Fildes Peninsula, King George Island, maritime Antarctica. Revista Chilena de Historia Natural, 89. https://doi.org/10.1186/s40693-016-0061-y.
Charlesworth D. & Willis J.H. (2009) The genetics of inbreeding depression. Nature Reviews Genetics, 10, 783–796.
Crandall-Stotler, B., Stotler, R.E. & Long, D.G. (2009) Morphology and classification of the Marchantiophyta. In: Goffinet B., Shaw A.J. (Eds.), Bryophyte Biology. Cambridge, Cambridge University Press, pp. 1–54.
Crawford, M., Jesson, L.K. & Garnock‐Jones, P.J. (2009) Correlated evolution of sexual system and life‐history traits in mosses. Evolution, 63, 1129–1142.
Cronberg, N. (2012) Animal-mediated fertilization in bryophytes–parallel or precursor to insect pollination in angiosperms? Lindbergia, 35, 76–85.
Cronberg, N., Natcheva, R. & Hedlund, K. (2006) Microarthropods mediate sperm transfer in mosses. Science, 313, 1255. https://doi.org/10.1126/science.1128707.
Cruden R.W., Lloyd R.M. (1995) Embryophytes have equivalent sexual phenotypes and breeding systems: why not a common terminology to describe them? American Journal of Botany, 82, 816–825.
Duckett J.G., Ligrone R. (1992) A survey of diaspore liberation mechanisms and germination patterns in mosses. Journal of Bryology, 17, 335–354.
During, H.J. (1979) Life strategies of bryophytes: a preliminary review. Lindbergia, 5, 2–18.
Edwards, S.R. (1978) Protonemal gemmae in Schistostega pennata (Hedw.) Web. et Mohr. Journal of Bryology, 10, 69–72.
Ehrlén, J., Bisang, I. & Hedenäs, L. (2000) Costs of sporophyte production in the moss, Dicranum polysetum. Plant Ecology, 149, 207–217.
Fantecelle, L.B., Bojacá, G.F.P. & Oliveira, B.A., Araújo, C.A.T. & Maciel-Silva, A.S. (2017) Briófitas da Chapada de Canga: diversidade e importância. In: Carmo, F.F., Kamino, L. (eds.) Chapada de Canga. Belo Horizonte, Instituto Prístino, p. 169–195.
Frey, W. & Kürschner, H. (2010) Asexual reproduction, habitat colonization and habitat maintenance in bryophytes. Flora, 206, 173–184.
Gerrienne, P. & Gonez, P. (2011) Early evolution of life cycles in embryophytes: a focus on the fossil evidence of gametophyte/sporophyte size and morphological complexity. Journal of Systematics and Evolution, 49, 1–16.
Glime, J.M. (2017a) Life cycles: surviving change. Chapt. 2-2. In: Bryophyte Ecology. Volume 1. Physiological Ecology. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Available from: http://digitalcommons.mtu.edu/bryophyte-ecology (20 Sep. 2023).
Glime, J.M. (2017b) Adaptive strategies: spore dispersal vectors. Chapt. 4-9. In: Bryophyte Ecology. Volume 1. Physiological Ecology. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Available from: http://digitalcommons.mtu.edu/bryophyte-ecology (20 Sep. 2023).
Glime, J.M. (2017c) Marchantiophyta. In: Bryophyte Ecology. Volume 1. Physiological Ecology. Michigan Technological University and the International Association of Bryologists. Available from: http://digitalcommons.mtu.edu/bryophyte-ecology (20 Sep. 2023).
Glime, J.M. (2017d) Anthocerotophyta. In: Bryophyte Ecology. Volume 1. Physiological Ecology. Michigan Technological University and the International Association of Bryologists. Available from: http://digitalcommons.mtu.edu/bryophyte-ecology (20 Sep. 2023).
Glime, J.M. (2017e) Adaptive strategies: vegetative propagules. In: Bryophyte Ecology. Volume 1. Physiological Ecology. Michigan Technological University and the International Association of Bryologists. Available from: http://digitalcommons.mtu.edu/bryophyte-ecology (20 Sep. 2023).
Glime, J.M. (2017f) Adaptive strategies: vegetative dispersal vectors. In: Bryophyte Ecology. Volume 1. Physiological Ecology. Michigan Technological University and the International Association of Bryologists. Available from: http://digitalcommons.mtu.edu/bryophyte-ecology (20 Sep. 2023).
Glime, J.M. (2017g) Adaptive strategies: vegetative vs sexual diaspores. In: Bryophyte Ecology. Volume 1. Physiological Ecology. Michigan Technological University and the International Association of Bryologists. Available from: http://digitalcommons.mtu.edu/bryophyte-ecology (20 Sep. 2023).
Glime, J.M. & Bisang, I. (2017a) Sexuality: sex ratio and sex expression. In: Bryophyte Ecology, Volume 1. Physiological Ecology. Michigan Technological University and the International Association of Bryologists. Available from: http://digitalcommons.mtu.edu/bryophyte-ecology (20 Sep. 2023).
Glime, J.M. & Bisang, I. (2017b) Sexuality: reproductive barriers and tradeoffs. In: Bryophyte Ecology, Volume 1. Physiological Ecology. Michigan Technological University and the International Association of Bryologists. Available from: http://digitalcommons.mtu.edu/bryophyte-ecology (20 Sep. 2023).
Goffinet, B. & Buck W.R. (2012) The evolution of body form in bryophytes. Annual Plant Reviews, 45, 51–89.
Goffinet, B., Buck, W. & Shaw, A.J. (2009) Morphology and classification of the Bryophyta. In: Goffinet, B. & Shaw, A.J. (Eds.), Bryophyte Biology. Cambridge, Cambridge University Press, pp. 55–138.
Gradstein, S.R., Churchill, S.P. & Salazar-Allen, N. (2001) Guide to the bryophytes of tropical America. Memoirs of the New York Botanical Garden, 86, 1–577.
Gradstein, S.R. & Wilson, R. (2008) Protonemal neoteny in bryophytes. In: Mohamed H., Baki B.B., Nasrulhaq-Boyce A., Lee P.K.Y. (Eds.) Bryology in the New Millennium. Kuala Lumpur, University of Malaya, pp. 1–11.
Gradstein, S.R., Wilson, R., Ilkiu-Borges, A.L. & Heinrichs, J. (2006) Phylogenetic relationships and neotenic evolution of Metzgeriopsis (Lejeuneaceae) based on chloroplast DNA sequences and morphology. Botanical Journal of the Linnean Society, 151, 293–308.
Graham, L.K. & Wilcox, L.W. (2000) The origin of alternation of generations in land plants: a focus on matrotrophy and hexose transport. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 355, 757–767.
Haig, D. (2016) Living together and living apart: the sexual lives of bryophytes. Philosophical Transactions of the Royal Society, 371. https://doi.org/10.1098/rstb.2015.0535
Hallingbäck, T. & Hodgetts, N. (2000) Mosses, Liverworts, and Hornworts. Status Survey and Conservation Action Plan for Bryophytes. Gland, IUCN/SSC Bryophyte Specialist Group.
Hedenäs, L. & Bisang, I. (2011) The overlooked dwarf males in mosses – unique among green land plants. Perspectives in Plant Ecology, Evolution and Systematics, 13, 121–135.
Holá, E., Vesalainen, T., Těšitel, J. & Laaka-Lindberg, S. (2014) Sex ratio, sex-specific pattern in vegetative growth and gemma production in an aquatic liverwort, Scapania undulata (Marchantiophyta: Scapaniaceae). Botanical Journal of the Linnean Society, 175, 229–241.
Horsley, K., Stark, L.R. & McLetchie, D.N. (2011) Does the silver moss Bryum argenteum exhibit sex-specific patterns in vegetative growth rate, asexual fitness or prezygotic reproductive investment? Annals of Botany, 107, 897–907.
Hugonnot, V., Blay, B. & Celle, J. (2014) The male gender as a key for understanding the reproductive biology of Anomobryum concinnatum (Spruce) Lindb. Journal of Bryology, 36, 244–248.
Imura, S. (1994) Vegetative diaspores in Japanese mosses. Journal of the Hattori Botanical Laboratory, 77, 177–232.
Imura, S. & Iwatsuki, Z. (1990) Classification of vegetative diaspores on Japanese mosses. Hikobia, 10, 435–443.
Kimmerer, R.W. (1991a) Reproductive ecology of Tetraphis pellucida. I. Population density and reproductive mode. The Bryologist, 94, 255–260.
Kimmerer, R.W. (1991b) Reproductive ecology of Tetraphis pellucida. II. Differential success of sexual and asexual propagules. The Bryologist, 94, 284–288.
Korpelainen, H. (1998) Labile sex expression in plants. Biological Reviews of the Cambridge Philosophical Society, 73, 157–180.
Laaka-Lindberg, S., Korpelainen, H. & Pohjamo, M. (2003) Dispersal of asexual propagules in bryophytes. Journal of the Hattori Botanical Laboratory, 93, 319–330.
Laenen, B., Machac, A., Gradstein, S.R., Shaw, B., Patiño, J., Désamoré, A., Goffinet, B., Cox, C.J., Shaw, J. & Vanderpoorten, A. (2016a) Geographical range in liverworts: does sex really matter? Journal of Biogeography, 43, 627–635.
Laenen, B., Machac, A., Gradstein, S.R., Shaw, B., Patiño, J., Désamoré, A., Goffinet, B., Cox, C.J., Shaw, A.J. & Vanderpoorten, A. (2016b) Increased diversification rates follow shifts to bisexuality in liverworts. New Phytologist, 210, 1121–1129.
Lewis, L.R., Behling, E., Gousse, H., Qian, E., Elphick, C.S, Lamarre, J., Bêty, J., Liebezeit, J., Rozzi, R. & Goffinet, B. (2014) First evidence of bryophyte diaspores in the plumage of transequatorial migrant birds. PeerJ, 2, e424. https://doi.org/10.7717/peerj.424.
Ligrone, R., Duckett, J.G. & Renzaglia, K.S. (2000) Conducting tissues and phyletic relationships of bryophytes. Philosophical Transactions of the Royal Society, 355, 795–813.
Löbel, S., Snäll, T. & Rydin, H. (2009) Mating system, reproduction mode and diaspore size affect metacommunity diversity. Journal of Ecology, 97, 176–185.
Longton, R.E. (1992) Reproduction and rarity in British mosses. Biological Conservation, 59, 89–98.
Longton, R.E. (2006) Reproductive ecology of bryophytes: what does it tell us about the significance of sexual reproduction? Lindbergia, 31, 16–23.
Longton, R.E. & Schuster, R.M. (1983) Reproduction Biology. In: Schuster R.M. (Eds.), New Manual of Bryology. Nichinan, The Hattori Botanical Laboratory, pp. 386–462.
Maciel-Silva, A.S., Pôrto, K.C. & Simabukuro, E.A. (2006) Morfogênese protonemática de briófitas ocorrentes em Remanescentes de Floresta Atlântica do estado de Pernambuco, Brasil. Boletim do Instituto de Botânica, 18, 213–227.
Maciel-Silva, A.S. (2016) Asexual regeneration and its implications for local bryophyte establishment in a Brazilian tropical rain forest. Botany, 95, 45–52.
Maciel-Silva A.S., Gaspar E.P., Conceição F.P., Santos N.D., Costa D.P. (2016) Reproductive biology of Syzygiella rubricaulis (Nees) Steph. (Adelanthaceae, Marchantiophyta), a liverwort disjunctly distributed in high-altitude Neotropical mountains. Plant Biology, 18, 601–608.
Maciel-Silva, A.S. & Pôrto K.C. (2014) Reproduction in Bryophytes. In: Ramawat K.G., Mérillon J.-M., Shivanna K.R. (Eds.), Reproductive Biology of Plants. New Delhi, CRC Press, pp. 1–20.
Maciel-Silva, A.S. & Valio, I.F.M. (2011) Reproductive phenology of bryophytes in tropical rain forests: the sexes never sleep. The Bryologist, 114, 708–719.
Maciel-Silva, A.S., Valio, I.F.M. & Rydin, H. (2012) Altitude affects the reproductive performance in monoicous and dioicous bryophytes: examples from a Brazilian Atlantic rainforest. AoB plants 2012: pls016. https://doi.org/10.1093/aobpla/pls016.
McDaniel, S.F. & Perroud, P.F. (2012) Invited perspective: bryophytes as models for understanding the evolution of sexual systems. The Bryologist, 115, 1–11.
McLetchie, D.N. (1992) Sex ratio from germination through maturity and its reproductive consequences in the liverwort Sphaerocarpos texanus. Oecologia, 92, 273–278.
McLetchie, D.N. (2001) Sex-specific germination response in the liverwort Sphaerocarpos texanus (Sphaerocarpaceae). The Bryologist, 104, 69–72.
McLetchie, D.N. & Puterbaugh M.N. (2000) Population sex ratios, sex-specific clonal traits and trade-offs among these traits in the liverwort Marchantia inflexa. Oikos, 90, 227–237.
Milne, J. (2001) Reproductive biology of three Australian species of Dicranoloma (Bryopsida, Dicranaceae): sexual reproduction and phenology. The Bryologist, 104, 440–452.
Mishler B.D. (1988) Reproductive ecology of bryophytes. In: Lovett Doust J., Lovett Doust L. (Eds.), Plant reproductive ecology: patterns and strategies. New York, Oxford University Press, pp. 285–306.
Nakamura, K., Hisanaga, T., Fujimoto, K., Nakajima, K. & Wada, H. (2018) Plant-inspired pipettes. Journal of The Royal Society Interface, 15 (140). https://doi.org/10.1098/rsif.2017.0868.
Nehira, K. (1983) Spore germination, protonema development and sporeling development. In: Schuster R.M. (Ed.), New Manual of Bryology. Nichinan, The Hattori Botanical Laboratory, pp. 343–385.
Newton, A.E. & Mishler, B.D. (1994) The evolutionary significance of asexual reproduction in mosses. Journal of the Hattori Botanical Laboratory, 76, 127–145.
Newton, M.E. (1972) Sex-ratio differences in Mnium hornum Hedw. and M. undulatum Sw. in relation to spore germination and vegetative regeneration. Annals of Botany, 36, 163–178.
Norrell, T.E., Jones, K.S., Payton, A.C. & McDaniel, S.F. (2014) Meiotic sex ratio variation in natural populations of Ceratodon purpureus (Ditrichaceae). American Journal of Botany, 101, 1572–1576.
Obeso, J.R. (2002) The costs of reproduction in plants. New Phytologist, 155, 321–348.
Oliveira, S.M. & Pôrto, K.C. (2002) Population profile of Bryum apiculatum Schwaegr. in an Atlantic Forest remnant, Pernambuco, Brazil. Journal of Bryology, 24, 251–252.
Paolillo Jr, D.J. (1979) On the lipids of the sperm masses of three mosses. The Bryologist, 82, 93–96.
Paolillo Jr, D.J. (1981) The swimming sperms of land plants. Bioscience, 31, 367–373.
Parsons, J.G., Cairns, A., Johnson, C.N., Robson, S.K., Shilton, L.A. & Westcott, D.A. (2007) Bryophyte dispersal by flying foxes: a novel discovery. Oecologia, 152, 112–114.
Patiño, J., Bisang, I., Hedenäs, L., Dirkse, G., Bjarnason, Á.H., Ah-Peng, C. & Vanderpoorten, A. (2013) Baker's law and the island syndromes in bryophytes. Journal of Ecology, 101, 1245–1255.
Peñaloza-Bojacá, G.F., Oliveira, B.A., Araújo, C.A.T., Fantecelle, L.B. & Maciel-Silva, A.S. (2018) Bryophyte reproduction on ironstone outcrops: delicate plants in harsh environments. Flora, 238, 155–161.
Pereira, M.R., Dambros, C.S. & Zartman, C.E. (2016) Prezygotic resource-allocation dynamics and reproductive trade-offs in Calymperaceae (Bryophyta). American Journal of Botany, 103, 1838–1846.
Pichonet, A. & Gradstein S.R. (2012) Male dwarfism in the genus Dicranum (Dicranaceae) – a review. Cryptogamie, Bryologie, 33, 299–312.
Pohjamo, M. & Laaka-Lindberg, S. (2004) Demographic population structure of a leafy epixylic hepatic Anastrophyllum hellerianum (Nees ex Lindenb.) R.M. Schust. Plant Ecology, 173, 73–81.
Pohjamo, M., Laaka-Lindberg, S., Ovaskainen, O. & Korpelainen, H. (2006) Dispersal potential of spores and asexual propagules in the epixylic hepatic Anastrophyllum hellerianum. Evolutionary Ecology, 20, 415–430.
Pôrto, K.C., Cavalcanti e Silva, I.C., Reis, L.C., Maciel-Silva, A.S. (2016) Sex ratios and sporophyte production in the moss Bryum argenteum Hedw. on a rock outcrop, north-eastern Brazil. Journal of Bryology, 39, 194–198.
Pressel, S. & Duckett J.G. (2019) Do motile spermatozoids limit the effectiveness of sexual reproduction in bryophytes? Not in the liverwort Marchantia polymorpha. Journal of Systematics and Evolution, 57, 371–381.
Proctor, M.C.F., Oliver, M.J., Wood, A.J., Alpert, P., Stark, L.R., Cleavitt, N.L. & Mishler, B.D. (2007) Desiccation-tolerance in bryophytes: a review. The Bryologist, 110, 595–621.
Qiu, Y.L., Taylor, A.B. & McManus, H.A. (2012) Evolution of the life cycle in land plants. Journal of Systematics and Evolution, 50, 171–194.
Renner, S.S. & Ricklefs, R.E. (1995) Dioecy and its correlates in the flowering plants. American Journal of Botany, 82, 596–606.
Renzaglia, K.S., Schuette, S., Duff, R.J., Ligrone, R., Shaw, R.J., Mishler, B.D. & Duckett, J.G. (2007) Bryophyte phylogeny: Advancing the molecular and morphological frontiers. The Bryologist, 110, 179–213.
Renzaglia K.S., Villarreal J.C. & Duff R.J. (2009) New insights into morphology, anatomy and systematics of hornworts. In: Goffinet B., Shaw A.J. (Eds.), Bryophyte Biology. Cambridge, Cambridge University Press, pp. 139–171.
Reynolds, D.N. (1980) Gamete dispersal in Mnium ciliare. The Bryologist, 83, 73–77.
Rosengren, F. & Cronberg, N. (2014) The adaptive background of nannandry: dwarf male distribution and fertilization in the moss Homalothecium lutescens. Biological Journal of the Linnean Society, 113, 74–84.
Rosenstiel, T.N., Shortlidge, E.E., Melnychenko, A.N., Pankow, J.F. & Eppley, S.M. (2012) Sex-specific volatile compounds influence microarthropod-mediated fertilization of moss. Nature, 489, 431–433.
Rydgren, K., Halvorsen, R. & Cronberg, N. (2010) Infrequent sporophyte production maintains a female-biased sex ratio in the unisexual clonal moss Hylocomium splendens. Journal of Ecology, 98, 1224–1231.
Rydgren, K. & Økland, R.H. (2002) Sex distribution and sporophyte frequency in a population of the clonal moss Hylocomium splendens. Journal of Bryology, 24, 207–214.
Santos, W.L., Alvarenga, L.D.P. & Pôrto, K.C. (2018) Sexual dimorphism, vegetative growth and reproductive investment in the rhizautoicous moss Fissidens flaccidus (Fissidentaceae, Bryopsida). Cryptogamie, Bryologie, 39, 271–281.
Santos, W.L. & Maciel‐Silva, A.S. & Pôrto K.C. (2020) How do sexual expression, reproductive phenology and reproductive success relate to sexual systems in Fissidens Hedw. (Fissidentaceae)? A case study comparing two different sexual systems in mosses. Plant Biology, 22, 573-581.
Santos, W.L., Bordin, J., Pôrto, K.C. & Pinheiro, F. (2023a) Life-history traits and density dependence in metapopulations of a tropical moss: a monoicous species that is almost dioicous. Oecologia, 201, 287-298.
Santos, W.L., Pôrto, K.C., Bordin, J., Pinheiro, F. & Bisang, I. (2023b) The spatial arrangement of sexes is related to reproductive allocation in mosses: a comparative study of reproductive allocation in three different monoicous sexual systems. Annals of Botany, 131, 885-896.
Santos, W.L., Pôrto, K.C., Greenwood, J., Davis, A., Pinheiro, F. & Stark, L.R. (2023c) A comparative study of cultured and field plants provides evidence for the shy male hypothesis in tropical genotypes of Bryum argenteum Hedw. Journal of Bryology, 1-11.
Shaw, J. & Beer, S.C. (1999) Life history variation in gametophyte populations of the moss Ceratodon purpureus (Ditrichaceae). American Journal of Botany, 86, 512–521.
Shaw, A.J. & Gaughan, J.F. (1993) Control of sex ratios in haploid populations of the moss, Ceratodon purpureus. American Journal of Botany, 80, 584–591.
Shimamura, M., Yamaguchi, T. & Deguchi, H. (2008) Airborne sperm of Conocephalum conicum (Conocephalaceae). Journal of Plant Research, 121, 69–71.
Slate, M.L., Rosenstiel, T.N. & Eppley, S.M. (2017) Sex-specific morphological and physiological differences in the moss Ceratodon purpureus (Dicranales). Annals of Botany, 120, 845–854.
Snäll, T., Fogelqvist, J., Ribeiro Jr, P.J. & Lascoux, M. (2004) Spatial genetic structure in two congeneric epiphytes with different dispersal strategies analysed by three different methods. Molecular Ecology, 13, 2109–2119.
Söderström, L. & During, H.J. (2005) Bryophyte rarity viewed from the perspectives of life history strategy and metapopulation dynamics. Journal of Bryology, 27, 261–268.
Solli, I.M.S., Söderström, L., Bakken, S., Flatberg, K.I. & Pedersen, B. (2000) Studies of fertility of Dicranum majus in two populations with contrasted sporophyte production. Journal of Bryology, 22, 3–8.
Stark, L.R. (1983) Reproductive biology of Entodon cladorrhizans (Bryopsida, Entodontaceae). I. Reproductive cycle and frequency of fertilization. Systematic Botany, 8, 381–386.
Stark, L.R. (1997) Phenology and reproductive biology of Syntrichia inermis (Bryopsida, Pottiaceae) in the Mojave Desert. The Bryologist, 100, 13–27.
Stark, L.C., Brinda, J.C. & McLetchie D.N. (2009) An experimental demonstration of the cost of sex and a potential resource limitation on reproduction in the moss Pterygoneurum (Pottiaceae). American Journal of Botany, 96, 1712–1721.
Stark, L.R. & Castetter, R.C. (1995) Phenology of Trichostomum perligulatum (Pottiaceae, Bryopsida) in the Chihuahuan Desert. The Bryologist, 98, 389–397.
Stark, L.R., McLetchie, D.N. & Eppley, S.M. (2010) Sex ratios and the shy male hypothesis in the moss Bryum argenteum (Bryaceae). The Bryologist, 113, 788–798.
Stark, L.R., McLetchie, D.N. & Mishler, B.D. (2005) Sex Expression, plant size, and spatial segregation of the sexes across a stress gradient in the desert moss Syntrichia caninervis. The Bryologist, 108, 183–193.
Stark, L.R., Mishler, B.D. & McLetchie, D.N. (1998) Sex expression and growth rates in natural populations of the desert soil crustal moss Syntrichia caninervis. Journal of Arid Environments, 40, 401–416.
Stark, L.R., Mishler, B.D. & McLetchie, D.N. (2000) The cost of realized sexual reproduction: assessing patterns of reproductive allocation and sporophyte abortion in a desert moss. American Journal of Botany, 87, 1599–1608.
Stark, L.R., McLetchie, D.N. & Roberts, S.P. (2009) Gender differences and a new adult eukaryotic record for upper thermal tolerance in the desert moss Syntrichia caninervis. Journal of Thermal Biology, 34, 131–137.
Taylor, P.J., Eppley, S.M. & Jesson, L.K. (2007) Sporophytic inbreeding depression in mosses occurs in a species with separate sexes but not in a species with combined sexes. American Journal of Botany, 94, 1853–1859.
Une, K. (1985) Sexual dimorphism in the Japanese species of Macromitrium Brid. (Musci; Orthotrichaceae). Journal of the Hattori Botanical Laboratory, 59, 487–513.
Vanderpoorten, A. & Goffinet, B. (2009) Introduction to bryophytes. Cambridge, Cambridge University Press.
Villarreal, J.C. & Renner, S.S. (2013) Correlates of monoicy and dioicy in hornworts, the apparent sister group to vascular plants. BMC Evolutionary Biology, 13. https://doi.org/10.1186/1471-2148-13-239.
Wyatt, R. (1982) Population ecology of bryophytes. Journal of Hattori Botanical Laboratory, 52, 179–198.
Wyatt, R. (1985) Terminology for bryophyte sexuality: toward a unified system. Taxon, 34, 420–425.
Wyatt, R. (1994) Population genetics of bryophytes in relation to their reproductive biology. Journal of Hattori Botanical Laboratory, 76, 147–157.
Zander, R.H. (1984) Bryophyte sexual systems: -oicous versus -oecious. Bryol. Beitraege, 3, 46–51.

Downloads
Published
Issue
Section
License
Copyright (c) 2024 Adaises Simone Maciel da Silva, Kátia Cavalcanti Pôrto

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.