Sex-specific facilitation and reproduction of the gynodioecious cushion plant Arenaria polytrichoides on the Himalaya-Hengduan mountains, SW China

doi:10.1016/j.pld.2023.07.002

Abstract

Abstract: When benefiting other beneficiaries, cushion plants may reciprocally receive feedback effects. The feedback effects on different sex morphs, however, remains unclear. In this study, taking the gynodioecious Arenaria polytrichiodes as a model species, we aimed to assess the sex-specific facilitation intensity of cushion plant by measuring the beneficiary cover ratio, and to assess the potential costs in cushion reproductive functions by measuring the flower and fruit cover ratios. The total beneficiary cover ratio was similar between females and hermaphrodites. Females produced much less flowers but more fruits than hermaphrodites. These results suggested that females and hermaphrodites possess similar facilitation intensity, and female cushion A. polytrichoides may allocate more resources saved from pollen production to seed production, while hermaphrodites possibly allocate more resources to pollen production hence reducing seed production. The surface areas covered by beneficiaries produced less flowers and fruits than areas without beneficiaries. In addition, strong negative correlations between beneficiary cover and flower cover were detected for both females and hermaphrodites, but the correlation strength were similar for these two sex morphs. However, the correlation between beneficiary cover and fruit cover was only significantly negative for females, suggesting that beneficiary plants negatively affect fruit reproduction of females while have neutral effects on hermaphrodites. All the results suggest that to facilitate other beneficiaries can induce reproductive costs on cushion A. polytrichoides, with females possibly suffering greater cost than hermaphrodites. Such differentiation in reproductive costs between sex morphs, in long-term perspective, may imply sex imbalance in population dynamics.

Key words: Facilitation intensity, Feedback effect, Sex-specific facilitation, Nurse plant, Population dynamics, Reproductive function

Xufang Chen, Yazhou Zhang, Lishen Qian, Renyu Zhou, Hang Sun, Jianguo Chen. Sex-specific facilitation and reproduction of the gynodioecious cushion plant Arenaria polytrichoides on the Himalaya-Hengduan mountains, SW China[J]. Plant Diversity, 2024, 46(02): 247-255.

References

[1] Alatalo, J.M., Little, C.J. 2014. Simulated global change:contrasting short and medium term growth and reproductive responses of a common alpine/Arctic cushion plant to experimental warming and nutrient enhancement. SpringerPlus 3, 157.
[2] Antonsson, H., Bjork, R.G., Molau, U. 2009. Nurse plant effect of the cushion plant Silene acaulis (L.) Jacq. in an alpine environment in the subarctic Scandes, Sweden. Plant Ecol. Divers. 2, 17-25.
[3] Aubert, S., Boucher, F., Lavergne, S., et al., 2014. 1914-2014:a revised worldwide catalogue of cushion plants 100 years after Hauri and Schroter. Alpine Bot. 124, 59-70.
[4] Badano, E.I., Marquet, P.A., 2008. Ecosystem engineering affects ecosystem functioning in high-Andean landscapes. Oecologia 155, 821-829.
[5] 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, 369-385.
[6] Benedict, J.B., 1989. Use of Silene acaulis for dating:the relationship of cushion diameter to age. Arct. Alp. Res. 21, 91-96.
[7] Bertness, M.D., Callaway, R., 1994. Positive interactions in communities. Trends Ecol. Evol. 9, 191-193.
[8] Bruno, J., Kennedy, C., 2000. Patch-size dependent habitat modification and facilitation on New England cobble beaches bySpartina alterniflora. Oecologia 122, 98-108.
[9] Buckley, N.E., Avila-Saka,r G., 2013. Reproduction, growth, and defense trade-offs vary with gender and reproductive allocation in Ilex glabra (Aquifoliaceae). Am. J. Bot. 100, 357-364.
[10] Callaway, R.M., 2007. Positive Interactions and Interdependence in Plant Communities. Berlin (Germany):Springer.
[11] Callaway, R.M., Brooker, R.W., Choler, P., et al., 2002. Positive interactions among alpine plants increase with stress. Nature 417, 844-848.
[12] Callaway, R.M., Pugnaire, F.I., 1999. Facilitation in plant communities. In:Pugnaire, F. & Valladares, F. (eds.) Handbook of Functional Plant Ecology, pp. 623-648. Dekker, New York, NY.
[13] Cavieres, L., Arroyo, M.T.K., Penaloza, A., et al., 2002. Nurse effect of Bolax gummifera cushion plants in the alpine vegetation of the Chilean Patagonian Andes. J. Veg. Sci. 13, 547-554.
[14] Cavieres, L.A., Badano, E.I., 2009. Do facilitative interactions increase species richness at the entire community level? J. Ecol. 97, 1181-1191.
[15] 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. Arctic Antarct. Alpine Res. 39, 229-236.
[16] Charlesworth, D., Morgan, M.T., 1991. Allocation of resources to sex functions in flowering plants. Trans. R. Soc. B-Biol. Sci. 332, 91-102.
[17] Chen, J.G., Chen, X.F., Qian, L.S., et al., 2023. Degeneration of foundation cushion species induced by ecological constraints can cause massive changes in alpine plant communities. Sci. China Life Sci. (accepted).
[18] Chen, J.G., He, X.F., Wang, S.W., et al., 2019. Cushion and shrub ecosystem engineers contribute differently to diversity and functions in alpine ecosystems. J. Veg. Sci. 30, 362-374.
[19] Chen, J.G., Li, Y.B., Yang, Y., et al., 2017a. How cushion communities are maintained in alpine ecosystems:a review and case study on alpine cushion plant reproduction. Plant Diversity 39, 221-228.
[20] Chen, J.G., Niu, Y., Li, Z.M., et al., 2017b. Sex allocation in gynodioecious Cyananthus delavayi differs between gender morphs and soil quality. Plant Reprod. 30, 107-117.
[21] Chen, J.G., Niu, Y., Yang, Y., et al., 2016. Sexual allocation in the gynodioecious species Cyananthus macrocalyx (Campanulaceae) at high elevations in the Sino-Himalaya Mountains. Alpine Bot. 126, 49-57.
[22] Chen, J.G., Schob, C., Zhou, Z., et al., 2015a. Cushion plants can have a positive effect on diversity at high elevations in the Himalayan Hengduan Mountains. J. Veg. Sci. 26, 768-777.
[23] Chen, J.G., Yang, Y., Stocklin, J., et al., 2015b. 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, 199-120.
[24] Chen, J.G., Yang, Y., Wang, S.W., et al., 2020. Recruitment of the high elevation cushion plant Arenaria polytrichoides is limited by competition thus threaten by currently established vegetation. J. Systemat. Evol. 58, 58-69.
[25] Chen, J.G., Zhang, Y.Z., Zhang, H.R., et al., 2021. The positive effects of the alpine cushion plant Arenaria polytrichoides on insect dynamics are determined by both physical and biotic factors. Sci. Total Environ. 762, 143091.
[26] Cranston, B.H., Callaway, R.M., Monks, A., et al., 2012. Gender and abiotic stress affect community-scale intensity of facilitation and its costs. J. Ecol. 100, 915-922.
[27] 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, 642-650.
[28] Forbis, T.A., Doak, D.F., 2004. Seedling establishment and life history trade-offs in alpine plants. Am. J. Bot. 91, 1147-1153.
[29] Gavini, S.S., Ezcurra, C., Aizen, M.A., 2020. Patch-level facilitation fosters high-Andean plant diversity at regional scales. J. Veg. Sci. 31, 1133-1143.
[30] Haddad, N.M., Crutsinger, G.M., Gross, K., et al., 2009. Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol. Lett. 12, 1029-1039.
[31] Harrell, J.F., 2023. Hmisc:Harrell Miscellaneous. R Package Version 5.0-1, <https://CRAN.R-project.org/package=Hmisc>.
[32] Kikvidze, Z., Brooker, R.W., Butterfield, B.J., et al., 2015. The effects of foundation species on community assembly:a global study on alpine cushion plant communities. Ecology 96, 2064-2069.
[33] Kjaer, U., Olsen, S.L., Klanderud, K., 2018. Shift from facilitative to neutral interactions by the cushion plant Silene acaulis along a primary succession gradient. J. Veg. Sci. 29, 42-51.
[34] Korner, C., 2003. Alpine Plant Life:Functional Plant Ecology of High Mountain Ecosystems. New York:Springer-Verlag Berlin Heideberg.
[35] Liu, Z.Y., Michalet, R., Wang, C.Y., et al., 2023. Contrasting effects of two phenotypes of an alpine cushion plant on understory species drive community assembly. Sci. Total Environ. 859, 160154.
[36] Lortie, C.J., Reid, A.M., 2012. Reciprocal gender effects of a keystone alpine plant species on other plants, pollinators, and arthropods. Botany 90, 273-282.
[37] Maestre, F.T., Callaway, R.M., Valladares, F., et al., 2009. Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J. Ecol. 97, 199-205.
[38] Michalet, R., Schob, C., Xiao, S., et al., 2016. Beneficiary feedback effects on alpine cushion benefactors become more negative with increasing cover of graminoids and in dry conditions. Funct. Ecol. 30, 79-87.
[39] Molau, U., 1997. Age-related growth and reproduction in Diapensia lapponica, an arctic-alpine cushion plant. Nord. J. Bot. 17, 225-234.
[40] 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.
[41] Molina-Montenegro, M.A., Oses, R., Torres-Diaz C., et al., 2015. Fungal endophytes associated with roots of nurse cushion species have positive effects on native and invasive beneficiary plants in an alpine ecosystem. Perspect. Plant Ecol. Evol. Systemat. 17, 218-226.
[42] Montesinos, D., Verdu, M., Garcia-Fayos, P., 2007. Moms are better nurses than dads:sex biased self-facilitation in a dioecious Juniperus tree. J. Veg. Sci. 18, 271-280.
[43] 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, 784-793.
[44] Nunez, C.I., Aizen, M.A., Ezcurra, C., 1999. Species associations and nurse plant effects in patches of high-Andean vegetation. J. Veg. Sci. 10, 357-364.
[45] Pugnaire, F.I., Zhang, L., Li, R.C., et al., 2015. No evidence of facilitation collapse in the Tibetan plateau. J. Veg. Sci. 26, 233-242.
[46] R Core Team, 2022. Nlme:Linear and Nonlinear Mixed Effects Models. R Package Version 3.1-160. https://CRAN.R-project.org/package=nlme.
[47] Raath-Kruger, M.J., Schob, C., McGeoch, M.A., et al., 2023. Long-term spatially-replicated data show no physical cost to a benefactor species in a facilitative plant-plant interaction. Oikos 4, e09617.
[48] Ramirez, L.A., Rada, F., Llambi, L.D., 2015. Linking patterns and processes through ecosystem engineering:effects of shrubs on microhabitat and water status of associated plants in the high tropical Andes. Plant Ecol. 216, 213-225.
[49] Reekie, E.G., Bazzaz, F.A., 2005. Reproductive Allocation in Plants. USA:Elsevier Academic Press.
[50] Rich, M.E., Gough, L., Boelman, N.T., 2013. Arctic arthropod assemblages in habitats of differing shrub dominance. Ecography 36, 994-1003.
[51] Ridenour, W.M., Callaway, R.M., Cavieres, L.A., 2012. Parasitism by Cuscuta chilensis and gender affect how the nurse cushion Laretia acaulis increases diversity in Andean alpine communities. J. Veg. Sci. 25, 1474-1483.
[52] Rodriguez-Echeverria, S., Lozano, Y.M., Bardgett, R.D., 2016. Influence of soil microbiota in nurse plant systems. Funct. Ecol. 30, 30-40.
[53] 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, 724-736.
[54] Schob, C., Armas, C., Pugnaire, F.I., 2013. Direct and indirect interactions co-determine species composition in nurse plant systems. Oikos 122, 1371-1379.
[55] Schob, C., Callaway, R.M., Anthelme, F., et al., 2014a. The context dependence of beneficiary feedback effects on benefactors in plant facilitation. New Phytol. 204, 386-396.
[56] Schob, C., Michalet, R., Cavieres, L.A., et al., 2014b. A global analysis of bidirectional interactions in alpine plant communities shows facilitators experiencing strong reciprocal fitness costs. New Phytol. 202, 95-105.
[57] Schob, C., Prieto, I., Armas, C., et al., 2014c. Consequences of facilitation:one plant's benefit is another plant's cost. Funct. Ecol. 28, 500-508.
[58] Sebastien, L., Julie, J., Francois, H., 2008. FactoMineR:an R package for multivariate analysis. J. Stat. Software 25, 1-18.
[59] Tewksbury, J., Lloyd, J. 2001. Positive interactions under nurse-plants:spatial scale, stress gradients and benefactor size. Oecologia 127, 425-434.
[60] Verdu, M., Villar-Salvador, P., Garcia-Fayos, P., 2004. Sex effects on the post-facilitation performance of two dioecious Juniperus species. Funct. Ecol. 18, 87-93.
[61] Weiner, J., 2004. Allocation, plasticity and allometry in plants. Perspect. Plant Ecol. Evol. Systemat. 6, 207-215.
[62] Wickham, H., 2016. ggplot2:Elegant Graphics for Data Analysis. Springer-Verlag New York.
[63] Wiesmair, M., Otte, A., Waldhardt, R. 2017. Relationships between plant diversity, vegetation cover, and site conditions:implications for grassland conservation in the Greater Caucasus. Biodivers. Conserv. 26, 273-291.
[64] Williams, C.F., Kuchenreuther, M.A., Drew, A., 2000. Floral dimorphism, pollination, and self-fertilization in gynodioecious Geranium richardsonii (Geraniaceae). Am. J. Bot. 87, 661-669.
[65] Yang, Y., Chen, J.G., Schob, 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. 8, 465.
[66] 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, 1048-1057.
[67] Zhang, Y.Z., Wang, S.W., He, X.F., et al. 2020. Altitudinal variation in flowering area and position and their ecological significances of an alpine cushion Arenaria polytrichoides, a gynodioecious herb. Chinese J. Plant Ecol. 44, 1154-1163.
[68] Zhao, R., An, L., 2021. Plant size of the alpine cushion Thylacospermum caespitosum affects soil amelioration at different elevations. Plant Ecol. 222, 323-335.