Articles

How cushion communities are maintained in alpine ecosystems:A review and case study on alpine cushion plant reproduction

  • Jianguo Chen ,
  • Yanbo Li ,
  • Yang Yang ,
  • Hang Sun
Expand
  • a Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan, China;
    b University of Chinese Academy of Sciences, Beijing 100049, China

Received date: 2017-03-30

  Revised date: 2017-07-18

  Online published: 2021-11-05

Supported by

This work was supported by grants from the National Key Research and Development Program of China (grant no. 2017YFC0505200), the Major Program of National Natural Science Foundation of China (grant no. 31590823) to H Sun, the Natural Science Foundation of China (Grant no. 31500185 to JG Chen, 31470321 to Y Yang).

Abstract

Cushion species occur in nearly all alpine environments worldwide. In past decades, the adaptive and ecosystem-engineering roles of such highly specialized life forms have been well studied. However, the adaptive strategies responsible for cushion species reproductive success and maintenance in severe alpine habitats remain largely unclear. In this study, we reviewed the current understanding of reproductive strategies and population persistence in alpine cushion species. We then present a preliminary case study on the sexual reproduction of Arenaria polytrichoides (Caryophyllaceae), a typical cushion species inhabiting high elevations of the Himalaya Hengduan Mountains, which is a hotspot for diversification of cushion species. Finally, we highlight the limitations of our current understanding of alpine cushion species reproduction and propose future directions for study.

Cite this article

Jianguo Chen , Yanbo Li , Yang Yang , Hang Sun . How cushion communities are maintained in alpine ecosystems:A review and case study on alpine cushion plant reproduction[J]. Plant Diversity, 2017 , 39(04) : 221 -228 . DOI: 10.1016/j.pld.2017.07.002

References

Agakhanyantz, O.E., Lopatin, I.K., 1978. Main characteristics of the ecosystems of the Pamirs, USSR. Arct. Alp. Res. 10 (2), 397-407.
Alatalo, J.M., Molau, U., 1995. Effect of altitude on the sex ratio in populations of Silene acaulis (Caryophyllaceae). Nord. J. Bot. 15 (3), 251-256.
Alatalo, J.M., Molau, U., 2001. Pollen viability and limitation of seed production in a population of the circumpolar cushion plant, Silene acaulis (Caryophyllaceae).Nord. J. Bot. 21 (4), 365-372.
Arnan, X., Escola, A., Rodrigo, A., et al., 2014. Female reproductive success in gynodioecious Thymus vulgaris:pollen versus nutrient limitation and pollinator foraging behaviour. Bot. J. Linn. Soc. 175 (3), 395-408.
Arroyo, M.T.K., Primack, R., Armesto, J., 1982. Community studies in pollination ecology in the high temperate Andes of central Chile.1. Pollination mechanisms and altitudinal variation. Am. J. Bot. 69 (1), 82-97.
Ashman, T.L., 1994. Reproductive allocation in hermaphrodite and female plants of Sidalcea oreganas sp. spicata (Malvaceae) using 4 currencies. Am. J. Bot. 81 (4), 433-438.
Ashman, T.L., 2006. The evolution of separate sexes:a focus on the ecological context. In:Harder, L.D., Barrett, S.C.H. (Eds.), Ecology and Evolution of Flowers.Oxford University Press, Oxford, pp. 204-219.
Aubert, S., Boucher, F., Lavergne, S., et al., 2014. 1914-2014:a revised worldwide catalogue of cushion plants 100 years after Hauri and Schroter. Alp. Bot. 124 (1), 59-70.
Badano, E.I., Cavieres, L.A., 2006a. Ecosystem engineering across ecosystems:do engineer species sharing common features have generalized or idiosyncratic effects on species diversity? J. Biogeogr. 33 (2), 304-313.
Badano, E.I., Cavieres, L.A., 2006b. Impacts of ecosystem engineers on community attributes:effects of cushion plants at different elevations of the Chilean Andes.Divers. Distrib. 12 (4), 388-396.
Badano, E.I., Jones, C.G., Cavieres, L.A., et al., 2006. Assessing impacts of ecosystem engineers on community organization:a general approach illustrated by effects of a high-Andean cushion plant. Oikos 115 (2), 369-385.
Benedict, J.B., 1989. Use of Silene acaulis for dating:the relationship of cushion diameter to age. Arct. Alp. Res. 21 (1), 91-96.
Bliss, L.C., 1971. Arctic and alpine plant life cycles. Annu. Rev. Ecol. Syst. 2 (2), 405-438.
Boucher, F.C., Lavergne, S., Basile, M., et al., 2016. Evolution and biogeography of the cushion life form in angiosperms. PPEES 20, 22-31.
Callaway, R.M., Walker, L.R., 1997. Competition and facilitation:a synthetic approach to interactions in plant communities. Ecology 78 (7), 1958-1965.
Carroll, S.B., Delph, L.F., 1996. The effects of gender and plant architecture on allocation to flowers in dioecious Silene latifolia (Caryophyllaceae). Int. J. Plant. Sci. 157 (4), 493-500.
Case, A.L., Ashman, T.L., 2005. Sex-specific physiology and its implications for the cost of reproduction. In:Reekie, E., Bazzaz, F.A. (Eds.), Reproductive Allocation in Plants. Elsevier Academic Press, UK, pp. 126-154.
Cavieres, L.A., Arroyo, M.T.K., Molina-Montenegro, M., et al., 2002. Nurse effect of Bolax gummigera (Apiaceae) cushion plants in the alpine vegetation of the Chilean Patagonian Andes. J. Veg. Sci. 13 (4), 547-554.
Cavieres, L.A., Badano, E.I., 2009. Do facilitative interactions increase species richness at the entire community level? J. Ecol. 97 (6), 1181-1191.
Cavieres, L.A., Badano, E.I., Sierra-Almeida, A., et al., 2007. Microclimatic modifications of cushion plants and their consequences for seedling survival of native and non-native herbaceous species in the high Andes of central Chile. Arct.Antarct. Alp. Res. 39 (2), 229-236.
Cavieres, L.A., Brooker, R.W., Butterfield, B.J., et al., 2014. Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecol. Lett. 17(2), 193-202.
Cavieres, L.A., Hernandez-Fuentes, C., Sierra-Almeida, A., et al., 2016. Facilitation among plants as an insurance policy for diversity in alpine communities. Funct.Ecol. 30 (1), 52-59.
Cavieres, L.A., Quiroz, C.L., Molina-Montenegro, M.A., 2008. Facilitation of the nonnative Taraxacum officinale by native nurse cushion species in the high Andes of central Chile:are there differences between nurses? Funct. Ecol. 22 (1), 148-156.
Charlesworth, B., Charlesworth, D., 1978. A model for the evolution of dioecy and gynodioecy. Am. Nat. 112 (988), 975-997.
Charlesworth, D., Morgan, M.T., 1991. Allocation of resources to sex functions in flowering plants. Trans. R. Soc. B-Biol. Sci. 332 (1262), 91-102.
Chen, J.G., Niu, Y., Yang, Y., et al., 2016. Sexual allocation in the gynodioecious species Cyananthus macrocalyx (Campanulaceae) at high elevations in the SinoHimalaya Mountains. Alp. Bot. 126 (1), 49-57.
Chen, J.G., Niu, Y., Li, Z.M., et al., 2017. Sex allocation in gynodioecious Cyananthus delavayi differs between gender morphs and soil quality. Plant Reprod. 30, 107-117.
Chen, J.G., Schöb, C., Zhou, Z., et al., 2015. Cushion plants can have a positive effect on diversity at high elevations in the Himalayan Hengduan Mountains. J. Veg.Sci. 26 (4), 768-777.
Chen, J.G., Yang, Y., Stöcklin, J., et al., 2014. Soil nutrient availability determines the facilitative effects of cushion plants on other plants species at high elevations in the South-Eastern Himalayas. Plant Ecol. Divers 8 (2), 199-210.
Cranston, B.H., Monks, A., Whigham, P.A., et al., 2015. Variation and response to experimental warming in a New Zealand cushion plant species. Austral Ecol. 40(6), 642-650.
Delph, L.F., 1990. Sex ratio variation in the gynodioecious shrub Hebe strictissima(Scrophulariaceae). Evolution 44 (1), 134-142.
Delph, L.F., Bailey, M.F., Marr, D.L., 1999. Seed provisioning in gynodioecious Silene acaulis (Caryophyllaceae). Am. J. Bot. 86 (1), 140-144.
Delph, L.F., Carroll, S.B., 2001. Factors affecting relative seed fitness and female frequency in a gynodioecious species, Silene acaulis. Evol. Ecol. Res. 3 (4), 487-505.
Dufay, M., Lahiani, E., Brachi, B., 2010. Gender variation and inbreeding depression in gynodioecious-gynomonoecious Silene nutans (Caryophyllaceae). Int. J. Plant Sci. 171 (1), 53-62.
Ehrlén, J., Lehtilä, K., 2002. How perennial are perennial plants? Oikos 98 (98), 308-322.
Fine, P.V.A., Ree, R.H., 2006. Evidence for a time-integrated species-area effect on the latitudinal gradient in tree diversity. Am. Nat. 168 (6), 796-804.
Forbis, T.A., Doak, D.F., 2004. Seedling establishment and life history trade-offs in alpine plants. Am. J. Bot. 91 (7), 1147-1153.
GarcíaeCamacho, R., Totland, Ø., 2009. Pollen limitation in the alpine:a metaanalysis. Arct. Antarct. Alp. Res. 41 (103), 103-111.
Gibson, N., 1990. The environments and primary production of cushion species at Mt Field and Mt Wellington, Tasmania. Aust. J. Bot. 38 (3), 229-243.
Gugerli, F., 1998. Effect of elevation on sexual reproduction in alpine populations of Saxifraga oppositifolia (Saxifragaceae). Oecologia 114 (1), 60-66.
Hermanutz, L.A., Innes, D.J., 1994. Gender variation in Silene acaulis (Caryophyllaceae). Plant Syst. Evol. 191 (1-2), 69-81.
Kleier, C., Rundel, P.W., 2004. Microsite requirements, population structure and growth of the cushion plant Azorella compacta in the tropical Chilean Andes.Austral Ecol. 29 (4), 461-470.
Kleier, C., Trenary, T., Graham, E.A., et al., 2015. Size class structure, growth rates, and orientation of the central Andean cushion Azorella compacta. PeerJ 3, e843.
Klimes, L., Klimesova, J., Hendriks, R., et al., 1997. Clonal plant architecture:a comparative analysis of form and function. In:de Kroon, J.V.G.E.H. (Ed.), The Ecology and Evolution of Clonal Plants. Backhuys Publishers, Leiden, The Netherlands, pp. 1-29.
Körner, C., 2003. Alpine Plant Life, second ed. Springer, Berlin, DE.
Körner, C., Paulsen, J., 2009. Exploring and explaining mountain biodiversity. In:Spehn, E.M., Korner, C. (Eds.), Data Mining for Global Trends in Mountain Biodiversity. CRC Press, Boca Raton, Florida, USA, pp. 1-10.
le Roux, P.C., McGeoch, M.A., 2004. The use of size as an estimator of age in the subantarctic cushion plant, Azorella selago (Apiaceae). Arct. Antarct. Alp. Res. 36(4), 509-517.
Li, B.S., Wang, J.T., Li, S.Y., 1987. The floristic features and geographic distribution of the cushion plant in Xizang. Mt. Res. 5 (1), 14-20.
Lloyd, D.G., 1976. The transmission of genes via pollen and ovules in gynodioecious angiosperms. Theor. Pop. Biol. 9 (3), 299-316.
Lortie, C.J., Reid, A.M., 2012. Reciprocal gender effects of a keystone alpine plant species on other plants, pollinators, and arthropods. Botany-Botanique 90 (4), 273-282.
Lundbye, H., Johansson, D.K., Andersen, M.R., et al., 2012. The effect of a seedsucking bug on seed germination of an arctic cushion plant. Ecoscience 19(3), 209-212.
Mackay, A., 2008. Climate change 2007:impacts, adaptation and vulnerability.Contribution of working group Ⅱ to the fourth assessment report of the intergovernmental panel on climate change. J. Environ. Qual. 37 (6), 2407.
Maurice, S., Desfeux, C., Mignot, A., et al., 1998. Is Silene acaulis (Caryophyllaceae) a trioecious species? Reproductive biology of two subspecies. Can. J. Bot. 76 (3), 478-485.
Mccarthy, D.P., 1992. Dating with cushion plants e establishment of a Silene acaulis growth curve in the Canadian Rockies. Arct. Alp. Res. 24 (1), 50-55.
Medan, D., Montaldo, N.H., Devoto, M., et al., 2002. Plant-pollinator relationships at two altitudes in the Andes of Mendoza, Argentina. Arct. Antarct. Alp. Res. 34 (3), 233-241.
Méndez, E., 2011. Growth and covering of Azorella monantha Clos (Apiaceae) in the high central Andes of Mendoza, Argentina. Rev. Fac.Cien. Agrar. 43 (1), 219-229.
Milla, R., Gimenez-Benavides, L., Escudero, A., et al., 2009. Intra-and interspecific performance in growth and reproduction increase with altitude:a case study with two Saxifraga species from Northern Spain. Funct. Ecol. 23 (1), 111-118.
Molau, U., 1997. Age-related growth and reproduction in Diapensia lapponica, an arctic-alpine cushion plant. Nord. J. Bot. 17 (3), 225-234.
Molenda, O., Reid, A., Lortie, C.J., 2012. The alpine cushion plant Silene acaulis as foundation species:a bug's-eye view to facilitation and microclimate. PLoS One 7, e37223.
Molina-Montenegro, M.A., Badano, E.I., Cavieres, L.A., 2006. Cushion plants as microclimatic shelters for two ladybird beetles species in alpine zone of central Chile. Arct. Antarct. Alp. Res. 38 (2), 224-227.
Morris, W., Doak, D., 1998. Life history of the long-lived gynodioecious cushion plant Silene acaulis (Caryophyllaceae), inferred from size-based population projection matrices. Am. J. Bot. 85 (6), 784-793.
Peng, D.L., Zhang, Z.Q., Xu, B., et al., 2012. Patterns of flower morphology and sexual systems in the subnival belt of the Hengduan Mountains, SW China. Alp. Bot. 122 (2), 65-73.
Philipp, M., Böcher, J., Mattson, O., et al., 1990. A quantitative approach to the sexual reproductive biology and population structure in some arctic flowering plants:Dryas integrifolia, Silene acaulis and Ranunculus nivalis. Medd. Grønl. Biosci. 34, 3-60.
Ramsey, M., Vaughton, G., Peakall, R., 2006. Does inbreeding avoidance maintain gender dimorphism in Wurmbea dioica (Colchicaceae)? J. Evol. Biol. 19 (5), 1497-1506.
Reid, A.M., Lortie, C.J., 2012. Cushion plants are foundation species with positive effects extending to higher trophic levels. Ecosphere 3 (11), 96.
Roy, J., Albert, C.H., Ibanez, S., et al., 2013. Microbes on the cliff:alpine cushion plants structure bacterial and fungal communities. Front. Microbiol. 4 (64), 1-14.
Sakai, A.K., Weller, S.G., Chen, M.L., et al., 1997. Evolution of gynodioecy and maintenance of females:the role of inbreeding depression, outcrossing rates, and resource allocation in Schiedea adamantis (Caryophyllaceae). Evolution 51(3), 724-736.
Schöb, C., Butter field, B.J., Pugnaire, F.I., 2012. Foundation species influence traitbased community assembly. New Phytol. 196 (3), 824-834.
Sieber, Y., Holderegger, R., Waser, N.M., et al., 2011. Do alpine plants facilitate each other's pollination? Experiments at a small spatial scale. Acta Oecol. Int. J. Ecol. 37 (4), 369-374.
Shykoff, J.A., 1988. Maintenance of gynodioecy in Silene acaulis (Caryophyllaceae):stage-specific fecundity and viability selection. Am. J. Bot. 75 (6), 844-850.
Shykoff, J.A., 1992. Sex polymorphism in Silene acaulis (Caryophyllaceae) and the possible role of sexual selection in maintaining females. Am. J. Bot. 79 (2), 138-143.
Williams, C.F., Kuchenreuther, M.A., Drew, A., 2000. Floral dimorphism, pollination, and self-fertilization in gynodioecious Geranium richardsonii (Geraniaceae). Am.J. Bot. 87 (5), 661-669.
Wirth, L.R., Graf, R., Gugerli, F., et al., 2010a. Between-year variation in seed weights across altitudes in the high-alpine plant Eritrichium nanum. Plant Ecol. 207 (2), 227-231.
Wirth, L.R., Graf, R., Gugerli, F., et al., 2010b. Lower selfing rate at higher altitudes in the alpine plant Eritrichium nanum (Boraginaceae). Am. J. Bot. 97 (5), 899-901.
Wirth, L.R., Waser, N.M., Graf, R., et al., 2011. Effects of floral neighborhood on seed set and degree of outbreeding in a high-alpine cushion plant. Oecologia 167 (2), 427-434.
Yang, Y., Chen, J.G., Schöb, C., et al., 2017. Size-mediated interaction between a cushion species and other non-cushion species at high elevations of the Hengduan Mountains, SW China. Front. Plant Sci. http://dx.doi.org/10.3389/fpls.2017.00465online.
Yang, Y., Niu, Y., Cavieres, L.A., et al., 2010. Positive associations between the cushion plant Arenaria polytrichoides (Caryophyllaceae) and other alpine plant species increase with altitude in the Sino-Himalayas. J. Veg. Sci. 21 (6), 1048-1057.
Zhang, R.Z., Zheng, D., Yang, Q.Y., et al., 1997. Physical Geography of Hengduan Mountains. Science Press, Beijing, China.
Zoller, H., Lenzin, H., Erhardt, A., 2002. Pollination and breeding system of Eritrichium nanum (Boraginaceae). Plant Syst. Evol. 233 (1), 1-14.
Zoller, H., Lenzin, H., Rusterholz, H.P., et al., 2005. Increasing population density and seed production with altitude in Eritrichium nanum (Boraginaceae) e an arctic alpine obligatory seeder. Arct. Antarct. Alp. Res. 37 (1), 41-48.
Outlines

/