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Global change stressors alter resources and shift plant interactions from facilitation to competition over time
Christina Alba
Agronomy Department, University of Florida, McCarty Hall B, Gainesville, Florida, 32611 USA
Research and Conservation Department, Denver Botanic Gardens, 909 York Street, Denver, Colorado, 80206 USA
Search for more papers by this authorCatherine Fahey
School of Natural Resources and Environment, University of Florida, 103 Black Hall, Gainesville, Florida, 32611 USA
Biology Department, Algoma University, 1520 Queen Street East, Sault Ste. Marie, Ontario, P6A 2G4 Canada
Search for more papers by this authorCorresponding Author
S. Luke Flory
Agronomy Department, University of Florida, McCarty Hall B, Gainesville, Florida, 32611 USA
Corresponding Author. E-mail: [email protected]Search for more papers by this authorChristina Alba
Agronomy Department, University of Florida, McCarty Hall B, Gainesville, Florida, 32611 USA
Research and Conservation Department, Denver Botanic Gardens, 909 York Street, Denver, Colorado, 80206 USA
Search for more papers by this authorCatherine Fahey
School of Natural Resources and Environment, University of Florida, 103 Black Hall, Gainesville, Florida, 32611 USA
Biology Department, Algoma University, 1520 Queen Street East, Sault Ste. Marie, Ontario, P6A 2G4 Canada
Search for more papers by this authorCorresponding Author
S. Luke Flory
Agronomy Department, University of Florida, McCarty Hall B, Gainesville, Florida, 32611 USA
Corresponding Author. E-mail: [email protected]Search for more papers by this authorAbstract
Global change stressors such as drought and plant invasion can affect ecosystem structure and function via mediation of resource availability and plant competition outcomes. Yet, it remains uncertain how native plants respond to drought stress that co-occurs with potentially novel resource conditions created by a nonnative invader. Further, there is likely to be temporal variation in competition outcomes between native and nonnative plant species depending on which resources are most limiting at a given time. Interacting stressors coupled with temporal variation make it difficult to predict how global change will impact native plant communities. To address this knowledge gap, we conducted a 5-yr factorial field experiment to quantify how simulated drought, plant invasion (by cogongrass, Imperata cylindrica), and these stressors combined, affected resource availability (soil moisture and light) and competition dynamics between the invader and native longleaf pine (Pinus palustris), a foundation species in southeast U.S. forests. Drought and invasion mediated the survival and performance of pine seedlings in temporally dynamic and unexpected ways. Drought and invasion alone each significantly reduced pine seedling survival. However, when the stressors occurred together, the invader offset drought stress for pine seedlings by maintaining high levels of soil moisture, humidity, and shade compared to uninvaded vegetation. This facilitative effect was pronounced for 2 yr, yet shifted to strong competitive exclusion as the invasion progressed and the limiting resource switched from soil moisture to light. After 3 yr, pine tree survival was low except for pines growing with uninvaded vegetation under ambient precipitation conditions. After 5 yr, pines experiencing a single stressor were taller and had greater height to diameter ratios than pines under no stress or both stressors. This outcome revealed a filtering effect where poorly performing trees were culled under stressful conditions, especially when pines were growing with the invader. Together, these results demonstrate that although drought and invasion suppressed a foundation tree species, the invader temporarily moderated stressful drought conditions, and at least some trees were able to survive despite increasingly strong competition. Such unpredictable effects of interacting global change stressors on native plant species highlight the need for additional long-term studies.
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Literature Cited
- Alavalapati, J. R. R., G. A. Stainback, and D. R. Carter. 2002. Restoration of the longleaf pine ecosystem on private lands in the US South: An ecological economic analysis. Ecological Economics 40: 411–419.
- Alba, C., J. E. NeSmith, C. Fahey, C. Angelini, and S. L. Flory. 2017. Methods to test the interactive effects of drought and plant invasion on ecosystem structure and function using complementary common garden and field experiments. Ecology and Evolution 7: 1442–1452.
- Allen, C. D., and D. D. Breshears. 1998. Drought-induced shift of a forest-woodland ecotone: Rapid landscape response to climate variation. Proceedings of the National Academy of Sciences USA 95: 14839–14842.
- Allen, C. D., et al. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259: 660–684.
- Armas, C., and F. I. Pugnaire. 2005. Plant interactions govern population dynamics in a semi-arid plant community. Journal of Ecology 93: 978–989.
- Bertness, M. D., and R. Callaway. 1994. Positive interactions in communities. Trends in Ecology and Evolution 9: 187–191.
- Bradley, B. A., D. S. Wilcove, and M. Oppenheimer. 2010. Climate change increases risk of plant invasion in the Eastern United States. Biological Invasions 12: 1855–1872.
- Breshears, D. D., et al. 2005. Regional vegetation die-off in response to global-change-type drought. Proceedings of the National Academy of Sciences USA 102: 15144–15148.
- Brewer, S. 2008. Declines in plant species richness and endemic plant species in longleaf pine savannas invaded by Imperata cylindrica. Biological Invasions 10: 1257–1264.
- Brooker, R. W. 2006. Plant – plant interactions and environmental change. New Phytologist 171: 271–284.
- Brooker, R. W., and T. V. Callaghan. 1998. The balance between positive and negative plant interactions and its gradients: A model. Oikos 81: 196–207.
- Brooker, R. W., et al. 2008. Facilitation in plant communities: The past, the present, and the future. Journal of Ecology 96: 18–34.
- Butterfield, B. J., J. B. Bradford, C. Armas, I. Prieto, and F. I. Pugnaire. 2016. Does the stress-gradient hypothesis hold water? Disentangling spatial and temporal variation in plant effects on soil moisture in dryland systems. Functional Ecology 30: 10–19.
- Caldeira, M. C., X. Lecomte, T. S. David, J. G. Pinto, M. N. Bugalho, and C. Werner. 2015. Synergy of extreme drought and shrub invasion reduce ecosystem functioning and resilience in water-limited climates. Scientific Reports 5: 1–9.
- Callaway, R. M., W. M. Ridenour, T. Laboski, T. Weir, and J. M. Vivanco. 2005. Natural selection for resistance to the allelopathic effects of invasive plants. Journal of Ecology 93(3): 576–583.
- Cavieres, L. A., C. L. Quiroz, M. A. Molina-Montenegro, A. A. Muñoz, and A. Pauchard. 2005. Nurse effect of the native cushion plant Azorella monantha on the invasive non-native Taraxacum officinale in the high-Andes of central Chile. Perspectives in Plant Ecology, Evolution and Systematics 7: 217–226.
- Côté, I. M., E. S. Darling, and C. J. Brown. 2016. Interactions among ecosystem stressors and their importance in conservation. Proceedings of the Royal Society B 283: 20152592.
- Craine, J. M., and R. Dybzinski. 2013. Mechanisms of plant competition for nutrients, water and light. Functional Ecology 27: 833–840.
- Daneshgar, P., S. Jose, A. Collins, and C. Ramsey. 2008. Cogongrass (Imperata cylindrica), an alien invasive grass, reduces survival and productivity of an establishing pine forest. Forest Science 54: 579–587.
- D'Antonio, C. D., and S. L. Flory. 2017. Long-term dynamics and impacts of plant invasions. Journal of Ecology 105: 1459–1461.
- Darling, E. S., and I. M. Côté. 2008. Quantifying the evidence for ecological synergies. Ecology Letters 11: 1278–1286.
- Davidson, A. M., M. Jennions, and A. B. Nicotra. 2011. Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecology Letters 14: 419–431.
- Diez, J. M., et al. 2012. Will extreme climatic events facilitate biological invasions? Frontiers in Ecology and the Environment 10: 249–257.
- Dozier, H., J. E. Gaffney, S. K. Mcdonald, E. R. R. L. Johnson, and D. G. Shilling. 1998. Cogongrass in the United States: History, ecology, impacts, and management. Weed Technology 12: 737–743.
- Espigares, T., A. López-Pintor, and J. M. Rey Benayas. 2004. Is the interaction between Retama sphaerocarpa and its understorey herbaceous vegetation always reciprocally positive? Competition-facilitation shift during Retama establishment. Acta Oecologica 26: 121–128.
- Estrada, J. A., and S. L. Flory. 2015. Cogongrass (Imperata cylindrica) invasions in the US: Mechanisms, impacts, and threats to biodiversity. Global Ecology and Conservation 3: 1–10.
- Fahey, C., C. Angelini, and S. L. Flory. 2018. Grass invasion and drought interact to alter the diversity and structure of native plant communities. Ecology 99: 2692–2702.
- Fang, Y., and L. Xiong. 2015. General mechanisms of drought response and their application in drought resistance improvement in plants. Cell and Molecular Life Sciences 72: 673–689.
- Farrior, C. E., et al. 2013. Resource limitation in a competitive context determines complex plant responses to experimental resource additions. Ecology 94: 2505–2517.
- Flory, S. L., and J. T. Bauer. 2014. Experimental evidence for indirect facilitation among invasive plants. Journal of Ecology 102: 12–18.
- Frost, C. C. 1993. Four centuries of changing landscape patterns in the longleaf pine ecosystem. Pages 17–43 in Proceedings of the Tall Timbers fire ecology conference, 18.
- Funk, J. L., and P. M. Vitousek. 2007. Resource-use efficiency and plant invasion in low-resource systems. Nature 446: 1079–1081.
- Gioria, M., and B. Osborne. 2014. Resource competition in plant invasions: Emerging patterns and research needs. Frontiers in Plant Science 5: 1–21.
- Goergen, E. M., E. A. Leger, and E. K. Espeland. 2011. Native perennial grasses show evolutionary response to Bromus tectorum (cheatgrass) invasion. PLoS ONE 6: e18145.
- Grant, K., J. Kreyling, H. Heilmeier, C. Beierkuhnlein, and A. Jentsch. 2014. Extreme weather events and plant-plant interactions: Shifts between competition and facilitation among grassland species in the face of drought and heavy rainfall. Ecological Research 29: 991–1001.
- He, Q., M. Bertness, and A. Altieri. 2013. Global shifts towards positive species interactions with increasing environmental stress. Ecology Letters 16: 695–706.
- Henderson, J. P., and H. D. Grissino-Mayer. 2009. Climate-tree growth relationships of longleaf pine (Pinus palustris Mill.) in the Southeastern Coastal Plain, USA. Dendrochronologia 27: 31–43.
- Holzmueller, E. J., and S. Jose. 2011. Invasion success of cogongrass, an alien C4 perennial grass, in the southeastern United States: Exploration of the ecological basis. Biological Invasions 13: 435–442.
- IPCC. 2014. Climate change 2014 synthesis report. Contribution of Working Groups I, II, and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva, Switzerland.
- Jactel, H., J. Petit, M. L. Desprez-Loustau, S. Delzon, D. Piou, A. Battisti, and J. Koricheva. 2012. Drought effects on damage by forest insects and pathogens: A meta-analysis. Global Change Biology 18: 267–276.
- Kane, J. M., K. A. Meinhardt, T. Chang, B. L. Cardall, R. Michalet, and T. G. Whitham. 2011. Drought-induced mortality of a foundation species (Juniperus monosperma) promotes positive afterlife effects in understory vegetation. Plant Ecology 212: 733–741.
- Kelly, A. E., and M. L. Goulden. 2008. Rapid shifts in plant distribution with recent climate change. Proceedings of the National Academy of Sciences USA 105: 11823–11826.
- Kottek, M., J. Grieser, C. Beck, B. Rudolf, and F. Rubel. 2006. World map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift 15: 259–263.
- Lau, J. A. 2006. Evolutionary responses of native plants to novel community members. Evolution 60(1): 56–63.
- Loudermilk, E. L., J. K. Hiers, S. Pokswinski, J. J. O'Brien, A. Barnett, and R. J. Mitchell. 2016. The path back: Oaks (Quercus spp.) facilitate longleaf pine (Pinus palustris) seedling establishment in xeric sites. Ecosphere 7: 1–14.
- Maestre, F. T., S. Bautista, and J. Cortina. 2003. Positive, negative, and net effects in grass-shrub interactions in Mediterranean semiarid grasslands. Ecology 84: 3186–3197.
- Maron, J. L., and P. G. Connors. 1996. A native nitrogen-fixing shrub facilitates weed invasion. Oecologia 105: 302–312.
- McDowell, N., et al. 2008. Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytologist 178: 719–739.
- McGuire, J. P., R. J. Mitchell, E. B. Moser, S. D. Pecot, D. H. Gjerstad, and C. W. Hedman. 2001. Gaps in a gappy forest: Plant resources, longleaf pine regeneration, and understory response to tree removal in longleaf pine savannas. Canadian Journal of Forest Research 31: 765–778.
- McIntire, E. J. B., and A. Fajardo. 2014. Facilitation as a ubiquitous driver of biodiversity. New Phytologist 201: 403–416.
- Mealor, B. A., and A. L. Hild. 2007. Post-invasion evolution of native plant populations: A test of biological resilience. Oikos 116: 1493–1500.
- Myers, J. A., and K. E. Harms. 2009. Seed arrival, ecological filters, and plant species richness: A meta-analysis. Ecology Letters 12: 1250–1260.
- Nepstad, D. C. 2002. The effects of partial throughfall exclusion on canopy processes, aboveground production, and biogeochemistry of an Amazon forest. Journal of Geophysical Research 107: 1–18.
- NeSmith, J. E., C. Alba, and S. L. Flory. 2018. Experimental drought and plant invasion additively suppress primary pine species of southeastern US forests. Forest Ecology and Management 411: 158–165.
- Paterno, G. B., J. A. Siqueira Filho, and G. Ganade. 2016. Species-specific facilitation, ontogenetic shifts and consequences for plant community succession. Journal of Vegetation Science 27: 606–615.
- Pearson, D. E., Y. K. Ortega, and J. L. Maron. 2017. The tortoise and the hare: Reducing resource availability shifts competitive balance between plant species. Journal of Ecology 105: 999–1009.
- Ploughe, L. W., E. M. Jacobs, G. S. Frank, S. M. Greenler, M. D. Smith, and J. S. Dukes. 2019. Community response to extreme drought (CRED): A framework for drought-induced shifts in plant – plant interactions. New Phytologist 222: 52–69.
- R Core Team. 2019. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.URL https://www.R-project.org/.
- Richards, C. L., O. Bossdorf, N. Z. Muth, J. Gurevitch, and M. Pigliucci. 2006. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9: 981–993.
- Rodriguez, L. F. 2006. Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biological Invasions 8: 927–939.
- Simberloff, D., D. Schmitz, and T. Brown, editors. 1997. Strangers in paradise: impact and management of nonindigenous species in Florida. Island Press, Washington, D.C., USA.
- Smith, M. D. 2011. The ecological role of climate extremes: Current understanding and future prospects. Journal of Ecology 99: 651–655.
- Strauss, S. Y., J. A. Lau, and S. P. Carroll. 2006. Evolutionary responses of natives to introduced species: What do introductions tell us about natural communities? Ecology Letters 9: 357–374.
- Sui, Z., Z. F. Fan, M. K. Crosby, and X. G. Fan. 2015. Distribution of longleaf pine in the southeastern United States and its association with climatic conditions. Volume 203. General Technical Report Southern Research Station, USDA Forest Service, Asheville, NC: 227–232.
- Thibault, K. M., and J. H. Brown. 2008. Impact of an extreme climatic event on community assembly. Proceedings of the National Academy of Sciences USA 105: 3410–3415.
- Thuiller, W., D. M. Richardson, and G. F. Midgley. 2007. Will climate change promote alien plant invasions? Biological Invasions 193: 197–211.
- Tilman, D. 2004. Niche tradeoffs, neutrality, and community structure: A stochastic theory of resource competition, invasion, and community assembly. Proceedings of the National Academy of Sciences USA 101: 10854–10861.
- Trinder, C. J., R. W. Brooker, and D. Robinson. 2013. Plant ecology's guilty little secret: Understanding the dynamics of plant competition. Functional Ecology 27: 918–929.
- van Kleunen, M., W. Dawson, F. Essl, and J. Pergl. 2015. Global exchange and accumulation of non-native plants. Nature 525: 100–104.
- Vitousek, P. M., C. M. D'Antonio, L. L. Loope, M. Rejmanek, and R. Westbrooks. 1997. Introduced species: A significant component of human-caused global change. New Zealand Journal of Ecology 21: 1–16.
- Vose, J. M., J. S. Clark, C. H. Luce, and T. Patel-Weynand. 2016. Effects of drought on forests and rangelands in the United States: A comprehensive science synthesis. Volume 93, pp. 1–289. Forest Service General Technical Report. US Department of Agriculture, Forest Service, Washington Office, Washington, DC.
- Walther, G., E. Post, P. Convey, A. Menzel, C. Parmesan, T. J. C. Beebee, J. Fromentin, O. Hoegh-Guldberg, and F. Bairlein. 2002. Ecological responses to recent climate change. Nature 416: 389–395.
- Wang, H., R. Fu, A. Kumar, and W. Li. 2010. Intensification of summer rainfall variability in the southeastern United States during recent decades. Journal of Hydrometeorology 11: 1007–1018.
- Weltzin, J. F., R. T. Belote, and N. J. Sanders. 2003. Biological invaders in a greenhouse world: Will elevated CO2 fuel plant invasions? Frontiers in Ecology and the Environment 1: 146–153.
- Wright, A., S. Schnitzer, and P. Reich. 2014. Living close to your neighbors: The importance of both competition and facilitation in plant communities. Ecology 95: 2213–2223.
- Wright, A., S. A. Schnitzer, and P. B. Reich. 2015. Daily environmental conditions determine the competition–facilitation balance for plant water status. Journal of Ecology 103: 648–656.
- Zaal, K., L. Khetsuriani, D. Kikodze, and R. Callaway. 2006. Seasonal shifts in competition and facilitation in subalpine plant communities of the central Caucasus. Journal of Vegetation Science 17: 77–82.
- Zhou, Y., C. J. Lambrides, and S. Fukai. 2014. Drought resistance and soil water extraction of a perennial C 4 grass: Contributions of root and rhizome traits. Functional Plant Biology 41: 505–519.