Negative plant–soil feedbacks can serve as a mechanism for plant species coexistence. Despite predicted changes in precipitation patterns due to climate change, little is known as to how the strength and direction of feedbacks change under differing soil moisture regimes. We performed a fully reciprocal greenhouse experiment where seedlings of two co-occurring Asclepias spp. (milkweed) were grown either with their own or the other species’ microbial communities under high or low watering treatments. We found that seedlings of each species were smaller when exposed to conspecific relative to heterospecific soil biota, perhaps due to a build-up of specific soil pathogens. Importantly, this negative feedback diminished under reduced water-availability, and also in the absence of live soil organisms. Our findings suggest that the ability for plants to coexist may be fundamentally altered in areas that face increased drought.
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Afkhami ME, Rudgers JA, Stachowicz JJ (2014) Multiple mutualist effects: conflict and synergy in multispecies mutualisms. Ecology 95:833–844
Agrawal AA, Salminen J, Fishbein M (2009) Metabolism trends in phenolic metabolism of milkweeds (Asclepias): evidence for escalation. Evolution (N Y) 63:663–673. https://doi.org/10.1111/j.1558-5646.2008.00573.x
Al-Karaki G, Al-Raddad A (1997) Effects of arbuscular mycorrhizal fungi and drought stress on growth and nutrient uptake of two wheat genotypes differing in drought resistance. Mycorrhiza 7:83–88
Bauer CR, Kellogg CH, Bridgham SD, Lamberti GA (2003) Mycorrhizal colonization across hydrologic gradients in restored and reference freshwater wetlands. Wetlands 23:961–968. https://doi.org/10.1672/0277-5212(2003)023%5b0961:MCAHGI%5d2.0.CO;2
Bauer JT, Kleczewski NM, Bever JD, Clay K, Reynolds HL (2012) Nitrogen-fixing bacteria, arbuscular mycorrhizal fungi, and the productivity and structure of prairie grassland communities. Oecologia 170:1089–1098. https://doi.org/10.1007/s00442-012-2363-3
Bauer JT, Mack KML, Bever JD (2015) Plant–soil feedbacks as drivers of succession: evidence from remnant and restored tallgrass prairies. Ecosphere 6(9):158. https://doi.org/10.1890/ES14-00480.1
Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: The utility of the feedback approach. J Ecol 85:561–573
Bever JD, Westover KM, Antonovics J (2006) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561. https://doi.org/10.2307/2960528
Bever JD, Mangan S, Alexander HM (2015) Maintenance of plant species diversity by pathogens. Annu Rev Ecol Evol Syst. https://doi.org/10.1146/annurev-ecolsys-112414-054306
Blankinship JC, Niklaus PA, Hungate BA (2011) A meta-analysis of responses of soil biota to global change. Oecologia 165:553–565. https://doi.org/10.1007/s00442-011-1909-0
Brandt AJ, De Kroon H, Reynolds HL, Burns JH (2013) Soil heterogeneity generated by plant–soil feedbacks has implications for species recruitment and coexistence. J Ecol 101:277–286. https://doi.org/10.1111/1365-2745.12042
Brotherson JD (1983) Species composition, distribution, and phytosociology of Iowa Prairie, a mesic tall-grass prairie in Iowa. Gt Basin Nat 43:137–167
Burns JH, Anacker BL, Strauss SY, Burke DJ (2015) Soil microbial community variation correlates most strongly with plant species identity, followed by soil chemistry, spatial location and plant genus. AoB Plants 7:plv030. https://doi.org/10.1093/aobpla/plv030
Connell J (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in forest trees. In: den Boer PJ, Gradwell GR (eds) Dynamics of population. PUDOC, Wageningen, Netherlands, pp 298–312
Fierer NG, Gabet EJ (2002) Carbon and nitrogen losses by surface runoff following changes in vegetation. J Environ Qual 31:1207–1213
Flockhart DTT, Martin TG, Norris DR (2012) Experimental examination of intraspecific density-dependent competition during the breeding period in monarch butterflies (Danaus plexippus). PLoS One 7:1–8. https://doi.org/10.1371/journal.pone.0045080
Fry EL, Johnson GN, Hall AL et al (2018) Drought neutralises plant–soil feedback of two mesic grassland forbs. Oecologia 186:1113–1125. https://doi.org/10.1007/s00442-018-4082-x
Huber L, Gillespie TJ (1992) Modeling leaf wetness in relation to plant disease epidemiology. Annu Rev Phytopathol 30:553–577
IPCC (2014) Climate Change 2014: Synthesis Report. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. Geneva, Switzerland
Janzen D (1970) Herbivores and number of tree species in tropical forests. Am Nat 104:501–528
Jones SE, Lennon JT (2010) Dormancy contributes to the maintenance of microbial diversity. Proc Natl Acad Sci 107:5881–5886. https://doi.org/10.1073/pnas.0912765107
Kaisermann A, de Vries FT, Griffiths RI, Bardgett RD (2017) Legacy effects of drought on plant–soil feedbacks and plant–plant interactions. New Phytol 215:1413–1424. https://doi.org/10.1111/nph.14661
Kartesz JT (2015) The Biota of North America Program (BONAP), maps gener. Chapel Hill, North Carolina
Klips RA, Culley TM (2004) Natural hybridization between prairie milkweeds, Asclepias sullivantii and Asclepias syriaca: morphological, isozyme, and hand-pollination evidence. Int J Plant Sci 165:1027–1037
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70. https://doi.org/10.1038/417067a
Klironomos JN, Zobel M, Tibbett M et al (2011) Forces that structure plant communities: quantifying the importance of the mycorrhizal symbiosis. New Phytol 189:366–370. https://doi.org/10.1111/j.1469-8137.2010.03550.x
Koziol L, Bever JD (2015) Mycorrhizal response trades off with plant growth rate and increases with plant successional status. Ecology 96:1768–1774. https://doi.org/10.1890/14-2208.1
Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant–soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992. https://doi.org/10.1111/j.1461-0248.2008.01209.x
Leung LR, Gustafson WI (2005) Potential regional climate change and implications to U.S. air quality. Geophys Res Lett 32:1–4. https://doi.org/10.1029/2005GL022911
Mangan SA, Schnitzer SA, Herre EA et al (2010) Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755. https://doi.org/10.1038/nature09273
Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology. https://doi.org/10.1890/11-0026.1
Meijer SS, Holmgren M, Van Der Putten WH (2011) Effects of plant–soil feedback on tree seedling growth under arid conditions. J Plant Ecol 4:193–200. https://doi.org/10.1093/jpe/rtr011
Munzbergova Z, Surinova M (2015) The importance of species phylogenetic relationships and species traits for the intensity of plant–soil feedback. Ecosphere. https://doi.org/10.1890/es15-00206.1
Nearing MA, Pruski FF, O’Neal MR (2004) Expected climate change impacts on soil erosion rates: a review. J Soil Water Conserv 59:43–50
Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281. https://doi.org/10.1038/35005072
Pocius VM, Debinski DM, Pleasants JM et al (2017) Milkweed matters: monarch butterfly (Lepidoptera: Nymphalidae) survival and development on nine midwestern milkweed species. Environ Entomol 46:1098–1105. https://doi.org/10.1093/ee/nvx137
Reinhart KO, Rinella MJ (2016) A common soil handling technique can generate incorrect estimates of soil biota effects on plants. New Phytol 210:786–789. https://doi.org/10.1111/nph.13822
Rinella MJ, Reinhart KO (2017) Mixing soil samples across experimental units ignores uncertainty and generates incorrect estimates of soil biota effects on plants. New Phytol 216:15–17. https://doi.org/10.1111/nph.14432
Rinella MJ, Reinhart KO (2018) Toward more robust plant–soil feedback research. Ecology 99:550–556. https://doi.org/10.1002/ecy.2146
Rudgers JA, Bell-Dereske L, Crawford KM, Emery SM (2015) Fungal symbiont effects on dune plant diversity depend on precipitation. J Ecol 103:219–230. https://doi.org/10.1111/1365-2745.12338
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. https://doi.org/10.1890/06-0219
Smith LM, Reynolds HL (2015) Euonymus fortunei dominance over native species may be facilitated by plant–soil feedback. Plant Ecol. https://doi.org/10.1007/s11258-015-0518-0
van der Putten WH, Bardgett RD, Bever JD et al (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. https://doi.org/10.1111/1365-2745.12054
van der Putten WH, Bradford MA, Pernilla Brinkman E et al (2016) Where, when and how plant–soil feedback matters in a changing world. Funct Ecol 30:1109–1121. https://doi.org/10.1111/1365-2435.12657
Vannette RL, Hunter MD (2011) Plant defence theory re-examined: nonlinear expectations based on the costs and benefits of resource mutualisms. J Ecol 99:66–76. https://doi.org/10.1111/j.1365-2745.2010.01755.x
Vannette RL, Hunter MD, Rasmann S (2013) Arbuscular mycorrhizal fungi alter above- and below-ground chemical defense expression differentially among Asclepias species. Front Plant Sci 4:361. https://doi.org/10.3389/fpls.2013.00361
Waring BG, Hawkes CV (2014) Short-term precipitation exclusion alters microbial responses to soil moisture in a wet tropical forest. Microb Ecol. https://doi.org/10.1007/s00248-014-0436-z
Wilson GW, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am J Bot 85:1732–1738. https://doi.org/10.2307/2446507
Woodson RE (1954) The North American species of Asclpias L. Missouri Bot Gard 41:1–211
We are grateful to Dr. Scott Mangan, Mike Dyer and the greenhouse staff at Washington University for their guidance and assistance with this project. We would like to thank Amy Patterson for assisting in the harvesting of these plants. This project was supported by undergraduate research awards provided to A. Snyder from Washington University in St. Louis.
This study was funded by Washington University in St. Louis.
Conflict of interest
The authors declare they have no conflict of interest.
Communicated by Sarah M. Emery.
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Snyder, A.E., Harmon-Threatt, A.N. Reduced water-availability lowers the strength of negative plant–soil feedbacks of two Asclepias species. Oecologia 190, 425–432 (2019). https://doi.org/10.1007/s00442-019-04419-8
- Belowground interactions
- Plant–microbial interactions
- Plant–soil feedback