Abstract
Plant reproduction is highly sensitive to stress from severe weather. While facilitation has been shown to buffer negative impacts along stress gradients, less is known about facilitating plant reproduction in drought periods. Because intensity and frequency of drought are predicted to increase, plant reproductive facilitation has important implications for a species ability to adapt to changes in climate. Our primary study objective is to test if nurse shrubs act as reproductive micro-refugia across soil types, by improving reproductive potential of perennial bunchgrass neighbors subjected to severe drought. To investigate this objective, we designed a fully factored study testing direct interaction between shrub and bunchgrasses in eastern Oregon sagebrush steppe, at two sites with different soil types. The study consisted of six simple effect treatments combining three moisture regimes (moist, ambient, and drought) with two shrub conditions (shrub intact or shrub removed). Our results indicate when facilitation of reproductive potential occurs, it occurs strongly and particularly in drought, consistent with the stress gradient hypothesis (SGH), where several species produced at least 54% more inflorescences in the presence of shrub neighbors. In addition, we found facilitation to be consistent with the SGH at the species level likely reflecting differences in plant strategy and perception of strain, but to follow alternative SGH models more closely at the site level where facilitation declined on the drier soil. Ultimately, our findings highlight the importance of facilitation in improving plant reproductive potential in drought, and support the role of nurse shrubs as micro-refugia in a changing climate.
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References
Adair CE, Reich PB, Trost JJ, Hobbie SE (2011) Elevated CO2 stimulates grassland soil respiration by increasing carbon inputs rather than by enhancing soil moisture. Glob Chang Biol 17:3546–3563
Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1:95–111. https://doi.org/10.1111/j.1752-4571.2007.00013.x
Anderson JT (2016) Plant fitness in a rapidly changing world. New Phytol 210:81–87. https://doi.org/10.1111/nph.13693
Armas C, Rodríguez-Echeverría S, Pugnaire FI (2011) A field test of the stress-gradient hypothesis along an aridity gradient. J Veg Sci 22:818–827
Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–7. http://CRAN.R-project.org/package=lme4. Accessed 1 Sept 2015
Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193. https://doi.org/10.1016/0169-5347(94)90088-4
Butterfield BJ, Bradford JB, Armas C, Prieto I, Pugnaire FI (2016) Does the stress-gradient hypothesis hold water? Disentangling spatial and temporal variation in plant effects on soil moisture in dryland systems. Funct Ecol 30:10–19. https://doi.org/10.1111/1365-2435.12592
Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848. https://doi.org/10.1038/nature00812
Cardon ZG, Stark JM, Herron PM, Rasmussen JA (2013) Sagebrush carrying out hydraulic lift enhances surface soil nitrogen cycling and nitrogen uptake into inflorescences. Proc Natl Acad Sci USA 110:18988–18993. https://doi.org/10.1073/pnas.1311314110
Chesson P, Gebauer RLE, Schwinning S, Huntly N, Wiegand K, Ernest MSK, Sher A, Novoplansky A, Weltzin JF (2004) Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments. Oecologia 141:236–253. https://doi.org/10.1007/s00442-004-1551-1
Choler P, Michalet R, Callaway RM (2001) Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–3308. https://doi.org/10.1890/0012-9658(2001)082%5b3295:FACOGI%5d2.0.CO;2
Christensen NS, Wood AW, Voisin N, Lettenmaier DP, Palmer RN (2004) The effects of climate change on the hydrology and water resources of the Colorado River basin. Clim Change 62:337–363. https://doi.org/10.1023/B:CLIM.0000013684.13621.1f
De Storme N, Geelen D (2014) The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant Cell Environ 37:1–18. https://doi.org/10.1111/pce.12142
Freckleton RP et al (2009) Measuring the importance of competition in plant communities. J Ecol 97:379–384
García-Cervigón AI, Iriondo JM, Linares JC, Olano JM (2016) Disentangling facilitation along the life cycle: impacts of plant-plant interactions at vegetative and reproductive stages in a Mediterranean forb. Front Plant Sci 7:129. https://doi.org/10.3389/fpls.2016.00129
Gasque M, Garciá-Fayos P (2004) Interaction between Stipa tenacissima and Pinus halepensis: consequences for reforestation and the dynamics of grass steppes in semi-arid Mediterranean areas. For Ecol Manage 189:251–261. https://doi.org/10.1016/j.foreco.2003.08.014
Gómez-Aparicio L (2009) The role of plant interactions in the restoration of degraded ecosystems: a meta-analysis across life-forms and ecosystems. J Ecol 97(6):1202–1214
Gray SB, Brady SM (2016) Plant developmental responses to climate change. Dev Biol 419:64–77. https://doi.org/10.1016/j.ydbio.2016.07.023
Grime JP (1979) Plant strategies, vegetation processes and ecosystem properties. Wiley, Chichester
Halpern SL, Adler LS, Wink M (2010) Leaf herbivory and drought stress affect floral attractive and defensive traits in Nicotiana quadrivalvis. Oecologia 163:961–971. https://doi.org/10.1007/s00442-010-1651-z
Harder LD, Prusinkiewicz P (2013) The interplay between inflorescence development and function as the crucible of architectural diversity. Ann Bot 112:1477–1493. https://doi.org/10.1093/aob/mcs252
He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706. https://doi.org/10.1111/ele.12080
Hedhly A, Hormaza JI, Herrero M (2009) Global warming and sexual plant reproduction. Trends Plant Sci 14:30–36. https://doi.org/10.1016/j.tplants.2008.11.001
Holmgren M (2000) Combined effects of shade and drought on tulip poplar seedlings: trade-off in tolerance or facilitation? Oikos 90:67–78. https://doi.org/10.1034/j.1600-0706.2000.900107.x
Holthuijzen MF, Veblen KE (2015) Grass-shrub associations over a precipitation gradient and their implications for restoration in the great basin, USA. PLoS One 10:e0143170. https://doi.org/10.1371/journal.pone.0143170
Horton JL, Hart SC (1998) Hydraulic lift: a potentially important ecosystem process. Trends Ecol Evol 13:232–235. https://doi.org/10.1016/S0169-5347(98)01328-7
Inouye RS (2006) Effects of shrub removal and nitrogen addition on soil moisture in sagebrush steppe. J Arid Environ 65:604–618. https://doi.org/10.1016/j.jaridenv.2005.10.005
IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, New York, NY, 1535 pp
Jones NT, Gilbert B (2016) Biotic forcing: the push-pull of plant ranges. Plant Ecol 217:1331–1344. https://doi.org/10.1007/s11258-016-0603-z
Jump AS, Peñuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8:1010–1020. https://doi.org/10.1111/j.1461-0248.2005.00796.x
Khasanova A, James JJ, Drenovsky RE (2013) Impacts of drought on plant water relations and nitrogen nutrition in dryland perennial grasses. Plant Soil 372:541. https://doi.org/10.1007/s11104-013-747-4
Kawai T, Tokeshi M (2007) Testing the facilitation-competition paradigm under the stress-gradient hypothesis: decoupling multiple stress factors. Proc Biol Sci 274:2503–2508. https://doi.org/10.1098/rspb.2007.0871
Kirchoff BK, Claßen-Bockhoff R (2013) Inflorescences: concepts, function, development and evolution. Ann Bot 112:1471–1476
Kjær U, Olsen SL, 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. https://doi.org/10.1111/jvs.12584
Koyama A, Tsuyuzaki S, Foster B (2013) Facilitation by tussock-forming species on seedling establishment collapses in an extreme drought year in a post-mined peatland. J Veg Sci 24(3):473–483
Lenth RV (2019) emmeans: estimated marginal means, aka least-squares means. R package version 1.3.3
Lentz R, Simonsen G (1986) A detailed soils inventory and associated vegetation of Squaw Butte Range Experiment Station (Special report 760). Oregon State University, Corvallis
Liancourt P, Callaway RM, Michalet R (2005) Stress tolerance and competitive-response ability determine the outcome of biotic interactions. Ecology 86:1611–1618. https://doi.org/10.1890/04-1398
Liancourt P, Le Bagousse-Pinguet Y, Rixen C, Dolezal J (2017) SGH: stress or strain gradient hypothesis? Insights from an elevation gradient on the roof of the world. Ann Bot 120:29–38
Liczner AR, Sotomayor DA, Filazzola A, Lortie CJ (2017) Germination response of desert annuals to shrub facilitation is species specific but not ecotypic. J Plant Ecol 10:364–374. https://doi.org/10.1093/jpe/rtw030
Liston A, Wilson BL, Robinson WA, Doescher PS, Harris NR, Svejcar T (2003) The relative importance of sexual reproduction versus clonal spread in an aridland bunchgrass. Oecologia 137:216–225. https://doi.org/10.1007/s00442-003-1332-2
Loarie SR, Duffy PB, Hamilton H, Asner GP, Field CB, Ackerly DD (2009) The velocity of climate change. Nature 462:1052–1055. https://doi.org/10.1038/nature08649
Loayza AP, Herrera-Madariaga MA, Carvajal DE et al (2017) Conspecific plants are better “nurses” than rocks: consistent results revealing intraspecific facilitation as a process that promotes establishment in a hyper-arid environment. AoB Plants 9:plx056
Maestre FT, Cortina J (2004) Do positive interactions increase with abiotic stress? A test from a semi-arid steppe. Proc Biol Sci 271(Suppl 5):S331–S333. https://doi.org/10.1098/rsbl.2004.0181
Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205
Malkinson D, Tielbörger K (2010) What does the stress-gradient hypothesis predict? Resolving the discrepancies. Oikos 119:1546–1552. https://doi.org/10.1111/j.1600-0706.2010.18375.x
Mann ME, Rahmstorf S, Kornhuber K, Steinman BA, Miller SK, Coumou D (2017) Influence of anthropogenic climate change on planetary wave resonance and extreme weather events. Sci Rep 7:45242. https://doi.org/10.1038/srep45242
McLaughlin BC, Ackerly DD, Klos PZ, Natali J, Dawson TE, Thompson SE (2017) Hydrologic refugia, plants, and climate change. Glob Chang Biol 23:2941–2961. https://doi.org/10.1111/gcb.13629
Medvigy D, Beaulieu C (2012) Trends in daily solar radiation and precipitation coefficients of variation since 1984. J Clim 25:1330–1339. https://doi.org/10.1175/2011JCLI4115.1
Michalet R, Brooker RW, Cavieres LA, Kikvidze Z, Lortie CJ, Pugnaire, Valiente-Banuet A, Callaway RM (2006) Do biotic interactions shape both sides of the humped-back model of species richness in plant communities? Ecol Lett 9(7):767–773
Michalet R, Le Bagousse-Pinguet Y, Maalouf J-P, Lortie CJ (2014) Two alternatives to the stress-gradient hypothesis at the edge of life: the collapse of facilitation and the switch from facilitation to competition. J Veg Sci 25:609–613. https://doi.org/10.1111/jvs.12123
Miriti MN (2006) Ontogenetic shift from facilitation to competition in a desert shrub. J Ecol 94:973–979
Montgomery RA, Reich PB, Palik BJ (2010) Untangling positive and negative biotic interactions: views from above and below ground in a forest ecosystem. Ecology 91:3641–3655
Niinemets Ü (2010) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. For Ecol Manag 260:1623–1639
Noumi Z, Chaieb M, Le Bagousse-Pinguet Y, Michalet R (2016) The relative contribution of short-term versus long-term effects in shrub-understory species interactions under arid conditions. Oecologia 180:529–542
Padilla FM, Pugnaire FI (2006) The role of nurse plants in the restoration of degraded environments. Front Ecol Environ 4:196–202
Paterno GB, Siqueira Filho JA, Ganade G (2016) Species-specific facilitation, ontogenetic shifts and consequences for plant community succession. J Veg Sci 27:606–615. https://doi.org/10.1111/jvs.12382
Quero JL, Villar R, Marañón T, Zamora R (2006) Interactions of drought and shade effects on seedlings of four Quercus species: physiological and structural leaf responses. New Phytol 170:819–833. https://doi.org/10.1111/j.1469-8137.2006.01713.x
Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia 73:486–489. https://doi.org/10.1007/BF00379405
Schiffers K, Tielbörger K (2006) Ontogenetic shifts in interactions among annual plants. J Ecol 94:336–341
Schlatterer EF, Hironaka M (1972) Some factors influencing tolerance to moisture stress of three range grasses. J Range Manage 25:364–367
Scott RL, Cable WL, Hultine KR (2008) The ecohydrologic significance of hydraulic redistribution in a semiarid savanna: hydraulic redistribution in a semiarid savanna. Water Resour Res 44:13. https://doi.org/10.1029/2007WR006149
Sheley RL, James JJ (2014) Simultaneous intraspecific facilitation and interspecific competition between native and annual grasses. J Arid Environ 104:80–87. https://doi.org/10.1016/j.jaridenv.2014.01.019
Smith MD (2011) An ecological perspective on extreme climatic events: a synthetic definition and framework to guide future research. J Ecol 99:656–663
Soliveres S, DeSoto L, Maestre FT, Olano JM (2010) Spatio-temporal heterogeneity in abiotic factors modulate multiple ontogenetic shifts between competition and facilitation. Perspect Plant Ecol Evol Syst 12:227–234
Soliveres S, Smit C, Maestre FT (2015) Moving forward on facilitation research: response to changing environments and effects on the diversity, functioning and evolution of plant communities. Biol Rev Camb Philos Soc 90:297–313. https://doi.org/10.1111/brv.12110
Svejcar T, James J, Hardegree S, Sheley R (2014) Incorporating plant mortality and recruitment into rangeland management and assessment. Rangeland Ecol Manag 67(6):603–613
Wright A, Schnitzer SA, Reich PB (2014) Living close to your neighbors: the importance of both competition and facilitation in plant communities. Ecology 95:2213–2223
Wright A, Schnitzer SA, Reich PB (2015) Daily environmental conditions determine the competition-facilitation balance for plant water status. J Ecol 103(3):648–656. https://doi.org/10.1111/1365-2745.12397
Yahdjian L, Sala OE (2002) A rainout shelter design for intercepting different amounts of rainfall. Oecologia 133:95–101. https://doi.org/10.1007/s00442-002-1024-3
Zhang G, Zhao W, Zhou H, Yang Q, Wang X (2018) Extreme drought stress shifts net facilitation to neutral interactions between shrubs and sub-canopy plants in an arid desert. Oikos 127:381–391. https://doi.org/10.1111/oik.04630
Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer-Verlag, New York. https://doi.org/10.1007/978-0-387-87458-6
Acknowledgements
We thank B. Bingham and C. Swanson for assistance with drought canopies, A. Muldoon for statistical support and L. Ziegenhagen for help with plant identification. We also thank E. Denton, L. Pyle and several anonymous reviewers for comments that greatly improved this manuscript. This research was funded through the United States Department of Agriculture, Agricultural Research Service Area-wide project for Ecologically Based Invasive Plant Management of Annual Grasses in the Great Basin Ecosystem. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the United States Government.
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ES, RS, and JJ conceived and designed the study. ES collected and analyzed the data. ES and RS wrote the manuscript. JJ made editorial contributions.
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Swanson, E.K., Sheley, R.L. & James, J.J. Do shrubs improve reproductive chances of neighbors across soil types in drought?. Oecologia 192, 79–90 (2020). https://doi.org/10.1007/s00442-019-04559-x
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DOI: https://doi.org/10.1007/s00442-019-04559-x