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Research articles
Bottom-up effects of host-plant species diversity and top-down effects of ants interactively increase plant performance
Published:05 September 2012https://doi.org/10.1098/rspb.2012.0893
Abstract
While plant diversity is well known to increase primary productivity, whether these bottom-up effects are enhanced by reciprocal top-down effects from the third trophic level is unknown. We studied whether pine tree species diversity, aphid-tending ants and their interaction determined plant performance and arthropod community structure. Plant diversity had a positive effect on aphids, but only in the presence of mutualistic ants, leading to a threefold greater number of both groups in the tri-specific cultures than in monocultures. Plant diversity increased ant abundance not only by increasing aphid number, but also by increasing ant recruitment per aphid. The positive effect of diversity on ants in turn cascaded down to increase plant performance; diversity increased plant growth (but not biomass), and this effect was stronger in the presence of ants. Consequently, bottom-up effects of diversity within the same genus and guild of plants, and top-down effects from the third trophic level (predatory ants), interactively increased plant performance.
References
- 1
Tilman D., Lehman C. L.& Thomson K. T. . 1997 Plant diversity and ecosystem productivity: theoretical considerations. Proc. Natl Acad. Sci. USA 94, 1857–1861.doi:10.1073/pnas.94.5.1857 (doi:10.1073/pnas.94.5.1857). Crossref, PubMed, Web of Science, Google Scholar - 2
Cardinale B. J., Wright J. P., Cadotte M. W., Carroll I. T., Hector A., Srivastava D. S., Loreau M.& Weis J. J. . 2007 Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc. Natl Acad. Sci. USA 104, 18 123–18 128.doi:10.1073/pnas.0709069104 (doi:10.1073/pnas.0709069104). Crossref, Web of Science, Google Scholar - 3
Haddad N. M., Crutsinger G. M., Gross K., Haarstad J., Knops J. M. H.& Tilman D. . 2009 Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol. Lett. 12, 1029–1039.doi:10.1111/j.1461-0248.2009.01356.x (doi:10.1111/j.1461-0248.2009.01356.x). Crossref, PubMed, Web of Science, Google Scholar - 4
Haddad N. M., Crutsinger G. M., Gross K., Haarstad J.& Tilman D. . 2011 Plant diversity and the stability of foodwebs. Ecol. Lett. 14, 42–46.doi:10.1111/j.1461-0248.2010.01548.x (doi:10.1111/j.1461-0248.2010.01548.x). Crossref, PubMed, Web of Science, Google Scholar - 5
Hector A., 2010 General stabilizing effects of plant diversity on grassland productivity at multiple sites through population asynchrony and overyielding. Ecology 91, 2213–2220.doi:10.1890/09-1162.1 (doi:10.1890/09-1162.1). Crossref, PubMed, Web of Science, Google Scholar - 6
Dias A. T., van Ruijven J.& Berendse F. . 2010 Plant species richness regulates soil respiration through changes in productivity. Oecologia 163, 805–813.doi:10.1007/s00442-010-1569-5 (doi:10.1007/s00442-010-1569-5). Crossref, PubMed, Web of Science, Google Scholar - 7
Cook-Patton S. C., McArt S. H., Parachnowitsch A. L., Thaler J. S.& Agrawal A. A. . 2011 A direct comparison of the consequences of plant genotypic and species diversity on communities and ecosystem function. Ecology 92, 915–923.doi:10.1890/10-0999.1 (doi:10.1890/10-0999.1). Crossref, PubMed, Web of Science, Google Scholar - 8
Isbell F. I., Polley H. W.& Wilsey B. J. . 2009 Biodiversity, productivity and the temporal stability of productivity: patterns and processes. Ecol. Lett. 12, 443–451.doi:10.1111/j.1461-0248.2009.01299.x (doi:10.1111/j.1461-0248.2009.01299.x). Crossref, PubMed, Web of Science, Google Scholar - 9
Levine J. M. . 2000 Species diversity and biological invasions: relating local process to community pattern. Science 288, 852–854.doi:10.1126/science.288.5467.852 (doi:10.1126/science.288.5467.852). Crossref, PubMed, Web of Science, Google Scholar - 10
Keddy P. A. . 1984 Plant zonation on lakeshores in Nova Scotia: a test of the resource specialization hypothesis. J. Ecol. 72, 797–808.doi:10.2307/2259532 (doi:10.2307/2259532). Crossref, Web of Science, Google Scholar - 11
Hurlbert A. H. . 2004 Species–energy relationships and habitat complexity in bird communities. Ecol. Lett. 7, 714–720.doi:10.1111/j.1461-0248.2004.00630.x (doi:10.1111/j.1461-0248.2004.00630.x). Crossref, Web of Science, Google Scholar - 12
Srivastava D. S.& Lawton J. H. . 1998 Why more productive sites have more species: an experimental test of theory using tree hole communities. Am. Nat. 152, 510–529.doi:10.1086/286187 (doi:10.1086/286187). Crossref, PubMed, Web of Science, Google Scholar - 13
Crutsinger G. M., Collins M. D., Fordyce J. A., Gompert Z., Nice C. C.& Sanders N. J. . 2006 Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313, 966–968.doi:10.1126/science.1128326 (doi:10.1126/science.1128326). Crossref, PubMed, Web of Science, Google Scholar - 14
Genung M. A., Bailey J. K.& Schweitzer J. A. . 2012 Welcome to the neighbourhood: interspecific genotype by genotype interactions in Solidago influence above- and belowground biomass and associated communities. Ecol. Lett. 15, 65–73.doi:10.1111/j.1461-0248.2011.01710.x (doi:10.1111/j.1461-0248.2011.01710.x). Crossref, PubMed, Web of Science, Google Scholar - 15
Ninkovic V., Al Abassi S., Ahmed E., Glinwood R.& Pettersson J. . 2011 Effect of within-species plant genotype mixing on habitat preference of a polyphagous insect predator. Oecologia 166, 391–400.doi:10.1007/s00442-010-1839-2 (doi:10.1007/s00442-010-1839-2). Crossref, PubMed, Web of Science, Google Scholar - 16
Utsumi S., Ando Y., Craig T. P.& Ohgushi T. . 2011 Plant genotypic diversity increases population size of a herbivorous insect. Proc. R. Soc. B 278, 3108–3115.doi:10.1098/rspb.2011.0239 (doi:10.1098/rspb.2011.0239). Link, Web of Science, Google Scholar - 17
Heil M.& Mckey D. . 2003 Protective ant–plant interactions as model systems in ecological and evolutionary research. Ann. Rev. Ecol. Evol. Syst. 34, 425–453.doi:10.1146/annurev.ecolsys.34.011802.132410 (doi:10.1146/annurev.ecolsys.34.011802.132410). Crossref, Web of Science, Google Scholar - 18
Styrsky J. D.& Eubanks M. D. . 2007 Ecological consequences of interactions between ants and honeydew-producing insects. Proc. R. Soc. B 274, 151–164.doi:10.1098/rspb.2006.3701 (doi:10.1098/rspb.2006.3701). Link, Web of Science, Google Scholar - 19
Trager M. D., Bhotika S., Hostetler J. A., Andrade G. V., Rodriguez-Cabal M. A., McKeon C. S., Osenberg C. W.& Bolker B. M. . 2010 Benefits for plants in ant–plant protective mutualisms: a meta-analysis. PLoS ONE 5, e14308.doi:10.1371/journal.pone.0014308 (doi:10.1371/journal.pone.0014308). Crossref, PubMed, Web of Science, Google Scholar - 20
Stadler B.& Dixon A. F. G. . 2005 Ecology and evolution of aphid–ant interactions. Ann. Rev. Ecol. Evol. Syst. 36, 345–372.doi:10.1146/annurev.ecolsys.36.091704.175531 (doi:10.1146/annurev.ecolsys.36.091704.175531). Crossref, Web of Science, Google Scholar - 21
James D. G., Stevens M. M.& Faulder R. J. . 1999 Ant foraging reduces the abundance of beneficial and incidental arthropods in citrus canopies. Biol. Control. 14, 121–126.doi:10.1006/bcon.1998.0678 (doi:10.1006/bcon.1998.0678). Crossref, Web of Science, Google Scholar - 22
Eubanks M. D. . 2001 Estimates of the direct and indirect effects of red imported fire ants on biological control in field crops. Biol. Control. 21, 35–43.doi:10.1006/bcon.2001.0923 (doi:10.1006/bcon.2001.0923). Crossref, Web of Science, Google Scholar - 23
Mooney K. A. . 2006 The disruption of an ant–aphid mutualism increases the effects of birds on pine herbivores. Ecology 87, 1805–1815.doi:10.1890/0012-9658(2006)87[1805:TDOAAM]2.0.CO;2 (doi:10.1890/0012-9658(2006)87[1805:TDOAAM]2.0.CO;2). Crossref, PubMed, Web of Science, Google Scholar - 24
Mooney K. A. . 2007 Tritrophic effects of birds and ants on a canopy food web, tree growth, and phytochemistry. Ecology 88, 2005–2014.doi:10.1890/06-1095.1 (doi:10.1890/06-1095.1). Crossref, PubMed, Web of Science, Google Scholar - 25
Herms D. A.& Mattson W. J. . 1992 The dilemma of plants: to grow or defend. Q. Rev. Biol. 67, 283–335.doi:10.1086/417659 (doi:10.1086/417659). Crossref, Web of Science, Google Scholar - 26
Mooney K. A.& Agrawal A. A. . 2008 Plant genotype shapes ant–aphid interactions: implications for community structure and indirect plant defense. Am. Nat. 171, E195–E205.doi:10.1086/587758 (doi:10.1086/587758). Crossref, PubMed, Web of Science, Google Scholar - 27
Abdala-Roberts L., Agrawal A. A.& Mooney K. A. In press. Ant–aphid interactions on Asclepias syriaca are mediated by plant genotype and caterpillar damage. Oikos.doi:10.1111/j.1600-0706.2012.20600.x (doi:10.1111/j.1600-0706.2012.20600.x). Crossref, Web of Science, Google Scholar - 28
Wimp G. M.& Whitham T. G. . 2001 Biodiversity consequences of predation and host plant hybridization on an aphid–ant mutualism. Ecology 82, 440–452.doi:10.2307/2679871 (doi:10.2307/2679871). Crossref, Web of Science, Google Scholar - 29
Johnson M. T. . 2008 Bottom-up effects of plant genotype on aphids, ants, and predators. Ecology 89, 145–154.doi:10.1890/07-0395.1 (doi:10.1890/07-0395.1). Crossref, PubMed, Web of Science, Google Scholar - 30
Sampedro L., Moreira X.& Zas R. . 2011 Costs of constitutive and herbivore-induced chemical defenses in pine trees emerge only under low resources availability. J. Ecol. 99, 818–827.doi:10.1111/j.1365-2745.2011.01814.x (doi:10.1111/j.1365-2745.2011.01814.x). Crossref, Web of Science, Google Scholar - 31
Moreira X., Zas R.& Sampedro L. . 2012 Differential allocation of constitutive and induced chemical defenses in pine tree juveniles: a test of the optimal defense theory. PLoS ONE 7, e34006.doi:10.1371/journal.pone.0034006 (doi:10.1371/journal.pone.0034006). Crossref, PubMed, Web of Science, Google Scholar - 32
Moreira X., Sampedro L.& Zas R. . 2009 Defensive responses of Pinus pinaster seedlings to exogenous application of methyl-jasmonate: concentration effect and systemic response. Environ. Exp. Bot. 67, 94–100.doi:10.1016/j.envexpbot.2009.05.015 (doi:10.1016/j.envexpbot.2009.05.015). Crossref, Web of Science, Google Scholar - 33
Sampedro L., Moreira X.& Zas R. . 2011 Resistance and response of Pinus pinaster seedlings to Hylobius abietis after induction with methyl jasmonate. Plant Ecol. 212, 397–401.doi:10.1007/s11258-010-9830-x (doi:10.1007/s11258-010-9830-x). Crossref, Web of Science, Google Scholar - 34
Noguera J. C., Lores M., Alonso-Alvarez C.& Velando A. . 2011 Thrifty development: early-life diet restriction reduces oxidative damage during later growth. Funct. Ecol. 25, 1114–1153.doi:10.1111/j.1365-2435.2011.01856.x (doi:10.1111/j.1365-2435.2011.01856.x). Crossref, Web of Science, Google Scholar - 35
Erel O. . 2004 A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin. Biochem. 37, 277–285.doi:10.1016/j.clinbiochem.2003.11.015 (doi:10.1016/j.clinbiochem.2003.11.015). Crossref, PubMed, Web of Science, Google Scholar - 36
Hansen J.& Møller I. . 1975 Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. Anal. Biochem. 68, 87–94.doi:10.1016/0003-2697(75)90682-X (doi:10.1016/0003-2697(75)90682-X). Crossref, PubMed, Web of Science, Google Scholar - 37
Littell R. C., Milliken G. A., Stroup W. W., Wolfinger R.& Schabenberger O. . 2006 SAS system for mixed models, 2nd edn. Cary, NC: SAS Institute. Google Scholar - 38
Johnson M. T., Lajeunesse M. J.& Agrawal A. A. . 2006 Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecol. Lett. 9, 24–34.doi:10.1111/j.1461-0248.2005.00833.x (doi:10.1111/j.1461-0248.2005.00833.x). Crossref, PubMed, Web of Science, Google Scholar - 39
Genung M. A., 2010 Non-additive effects of genotypic diversity increase floral abundance and abundance of floral visitors. PLoS ONE 5, e8711.doi:10.1371/journal.pone.0008711 (doi:10.1371/journal.pone.0008711). Crossref, PubMed, Web of Science, Google Scholar - 40
Zas R., Solla A.& Sampedro L. . 2007 Variography and kriging allow screening Pinus pinaster resistant to Armillaria ostoyae in field conditions. Forestry 80, 201–209.doi:10.1093/forestry/cpl050 (doi:10.1093/forestry/cpl050). Crossref, Web of Science, Google Scholar - 41
Kidd N. A. C. . 1994 Resource deprival as anti-herbivore strategy in plants, with particular reference to aphids. Eur. J. Entomol. 91, 53–56. Web of Science, Google Scholar - 42
Glinwood R., Ahmed E., Qvarfordt E., Ninkovic V.& Pettersson J. . 2009 Airborne interactions between undamaged plants of different cultivars affect insect herbivores and natural enemies. Arthropod Plant Interact. 3, 215–224.doi:10.1007/s11829-009-9072-9 (doi:10.1007/s11829-009-9072-9). Crossref, Web of Science, Google Scholar - 43
Hendrix D. L., Wei Y.& Legget J. E. . 1992 Homopteran honeydew is determined by both the insect and the plant species. Comp. Biochem. Physiol. 101, 23–27.doi:10.1016/0305-0491(92)90153-I (doi:10.1016/0305-0491(92)90153-I). Crossref, Google Scholar - 44
Douglas A. E. . 1993 The nutritional quality of phloem sap utilized by natural aphid populations. Ecol. Entomol. 18, 31–38.doi:10.1111/j.1365-2311.1993.tb01076.x (doi:10.1111/j.1365-2311.1993.tb01076.x). Crossref, Web of Science, Google Scholar - 45
Loreau M.& Hector A. . 2001 Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72–76.doi:10.1038/35083573 (doi:10.1038/35083573). Crossref, PubMed, Web of Science, Google Scholar - 46
Hooper D. U., 2005 Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35.doi:10.1890/04-0922 (doi:10.1890/04-0922). Crossref, Web of Science, Google Scholar - 47
Flombaum P.& Sala O. E. . 2008 Higher effect of plant species diversity on productivity in natural than artificial ecosystems. Proc. Natl Acad. Sci. USA 105, 6087–6090.doi:10.1073/pnas.0704801105 (doi:10.1073/pnas.0704801105). Crossref, PubMed, Web of Science, Google Scholar - 48
Tilman D., Hill J.& Lehman C. . 2006 Carbon-negative biofuels from low-input high-diversity grassland biomass. Science 314, 1598–1600.doi:10.1126/science.1133306 (doi:10.1126/science.1133306). Crossref, PubMed, Web of Science, Google Scholar - 49
Finke D. L.& Snyder W. E. . 2008 Niche partitioning increases resource exploitation by diverse communities. Science 321, 1488–1490.doi:10.1126/science.1160854 (doi:10.1126/science.1160854). Crossref, PubMed, Web of Science, Google Scholar - 50
Powers M. D., Pregitzer K. S.& Palik B. J. . 2008 Physiological performance of three pine species provide evidence for gap partitioning. For. Ecol. Manage. 256, 2127–2135.doi:10.1016/j.foreco.2008.08.003 (doi:10.1016/j.foreco.2008.08.003). Crossref, Web of Science, Google Scholar
