Abstract
Plants link interactions between aboveground and belowground organisms. Herbivore-induced changes in plant chemistry are hypothesized to impact entire food webs by changing the strength of trophic cascades. Yet, few studies have explored how belowground herbivores affect the behaviors of generalist predators, nor how such changes may act through diverse changes to the plant metabolome. Using a factorial experiment, we tested whether herbivory by root-knot nematodes (Meloidogyne incognita) affected the aboveground interaction among milkweed plants (Asclepias fascicularis or Asclepias speciosa), oleander aphids (Aphis nerii), and aphid-tending ants (Linepithema humile). We quantified the behaviors of aphid-tending ants, and we measured the effects of herbivore treatments on aphid densities and on phytochemistry. Unexpectedly, ants tended aphids primarily on the leaves of uninfected plants, whereas ants tended aphids primarily at the base of the stem of nematode-infected plants. In nematode-infected plants, aphids excreted more sugar per capita in their ant-attracting honeydew. Additionally, although plant chemistry was species-specific, nematode infection generally decreased the richness of plant secondary metabolites while acting as a protein sink in the roots. Path analysis indicated that the ants’ behavioral change was driven in part by indirect effects of nematodes acting through changes in plant chemistry. We conclude that belowground herbivores can affect the behaviors of aboveground generalist ant predators by multiple paths, including changes in phytochemistry, which may affect the attractiveness of aphid honeydew rewards.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data and corresponding R code will be archived in Dryad https://doi.org/10.5061/dryad.wm37pvmkv
References
Abad P, Favery B, Rosso MN, Castagnone-Sereno P (2003) Root-knot nematode parasitism and host response: molecular basis of a sophisticated interaction. Mol Plant Pathol 4:217–224. https://doi.org/10.1046/J.1364-3703.2003.00170.X
Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134
Agrawal AA, Petschenka G, Bingham RA et al (2012) Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol 194:28–45. https://doi.org/10.1111/j.1469-8137.2011.04049.x
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Baylis M, Pierce NE (1991) The effect of host-plant quality on the survival of larvae and oviposition by adults of an ant-tended lycaenid butterfly, Jalmenus evagoras. Ecol Entomol 16:1–9
Bezemer TM, van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624. https://doi.org/10.1016/j.tree.2005.08.006
Bezemer TM, De Deyn GB, Bossinga TM et al (2005) Soil community composition drives aboveground plant-herbivore-parasitoid interactions. Ecol Lett 8:652–661. https://doi.org/10.1111/j.1461-0248.2005.00762.x
Bristow CM (1991) Are ant-aphid associations a tritrophic interaction? Oleander aphids and argentine ants. Oecologia 87:514–521. https://doi.org/10.1007/BF00320414
Brooks ME, Kristensen K, van Bentham KJ et al (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400
Carolan JC, Caragea D, Reardon KT et al (2011) Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/proteomic approach. J Proteome Res 10:1505–1518. https://doi.org/10.1021/pr100881q
Clark RE, Gutierrez Illan J, Comerford MS, Singer MS (2019) Keystone mutualism influences forest tree growth at a landscape scale. Ecol Lett 22:1599–1607. https://doi.org/10.1111/ele.13352
Collingborn FMB, Gowen SR, Mueller-Harvey I (2000) Investigations into the biochemical basis for nematode resistance in roots of three Musa cultivars in response to Radopholus similis infection. J Agric Food Chem 48:5297–5301. https://doi.org/10.1021/jf000492z
Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol 40:297–331. https://doi.org/10.1146/annurev.en.40.010195.001501
Engler JD, De Vleesschauwer V, Burssens S et al (1999) Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell 11:793–807
Fischer MK, Shingleton AW (2001) Host plant and ants influence the honeydew sugar composition of aphids. Funct Ecol 15:544–550. https://doi.org/10.1046/j.0269-8463.2001.00550.x
Folgarait PJ (1998) Ant biodiversity and its relationship to ecosystem functioning: a review. Biodivers Conserv 7:1221–1244. https://doi.org/10.1023/A:1008891901953
Fox J, Weisberg S (2019) An R companion to applied regression, 3rd edn. Sage, Thousand Oaks, CA
Gheysen G, Mitchum MG (2019) Phytoparasitic nematode control of plant hormone pathways. Plant Physiol 179:1212–1226. https://doi.org/10.1104/pp.18.01067
Haegeman A, Mantelin S, Jones JT, Gheysen G (2012) Functional roles of effectors of plant-parasitic nematodes. Gene 492:19–31. https://doi.org/10.1016/j.gene.2011.10.040
Haribal M, Renwick JAA (1996) Oviposition stimulants for the monarch butterfly: flavonol glycosides from Asclepias curassavica. Phytochemistry 41:139–144
Heil M (2015) Extrafloral nectar at the plant-insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs. Annu Rev Entomol 60:213–232
Helmus MR, Dussourd DE (2005) Glues or poisons: which triggers vein cutting by monarch caterpillars? Chemoecology 15:45–49. https://doi.org/10.1007/s00049-005-0291-y
Hol WHG, De Boer W, Termorshuizen AJ et al (2013) Heterodera schachtii nematodes interfere with aphid-plant relations on Brassica oleracea. J Chem Ecol 39:1193–1203. https://doi.org/10.1007/s10886-013-0338-4
Holbrook CC, Knauft DA, Dickson DW (1983) A technique for screening peanut for resistance to Meloidogyne arenaria. Plant Dis 67:957–958
Hothorn T, Bretz F, Westfall P, et al (2019) Simultaneous inference in general parametric models. Version 1.4–10. R-core team, Available online at: https://multcomp.R-forge.R-project.org. Accessed 4 Mar 2019
Huang W, Siemann E, Carrillo J, Ding J (2015) Belowground herbivory limits induction of extrafloral nectar by above-ground herbivores. Ann Bot 115:841–846
Hunter MD (2016) The phytochemical landscape. Princeton University Press, Princeton, NJ
Johnson SN, Clark KE, Hartley SE et al (2012) Aboveground–belowground herbivore interactions: a meta-analysis. Ecology 93:2208–2215
Johnson SN, Mitchell C, McNicol JW et al (2013) Downstairs drivers-root herbivores shape communities of above-ground herbivores and natural enemies via changes in plant nutrients. J Anim Ecol 82:1021–1030
Kaplan I, Denno RF (2007) Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol Lett 10:977–994. https://doi.org/10.1111/j.1461-0248.2007.01093.x
Kaplan I, Halitschke R, Kessler A et al (2008) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406. https://doi.org/10.1890/07-0471.1
Kaplan I, Sardanelli S, Denno RF (2009) Field evidence for indirect interactions between foliar-feeding insect and root-feeding nematode communities on Nicotiana tabacum. Ecol Entomol 34:262–270. https://doi.org/10.1111/j.1365-2311.2008.01062.x
Kaplan I, Sardanelli S, Rehill BJ, Denno RF (2011) Toward a mechanistic understanding of competition in vascular-feeding herbivores: an empirical test of the sink competition hypothesis. Oecologia 166:627–636. https://doi.org/10.1007/s00442-010-1885-9
Khan MR, Khan MW (1995) Effects of ammonia and root-knot nematode on tomato. Agric Ecosyst Environ 53:71–81. https://doi.org/10.1016/0167-8809(94)00553-Q
Komarnytsky S, Esposito D, Poulev A, Raskin I (2013) Pregnane glycosides interfere with steroidogenic enzymes to down-regulate corticosteroid production in human adrenocortical H295R cells. J Cell Physiol 228:1120–1126. https://doi.org/10.1002/jcp.24262
Kremer JMM, Nooten SS, Cook JM et al (2018) Elevated atmospheric carbon dioxide concentrations promote ant tending of aphids. J Anim Ecol 87:1475–1483. https://doi.org/10.1111/1365-2656.12842
Landhäusser SM, Chow PS, Dickman LT et al (2018) Standardized protocols and procedures can precisely and accurately quantify non-structural carbohydrates. Tree Physiol 38:1764–1778. https://doi.org/10.1093/treephys/tpy118
Lefcheck JS (2016) piecewiseSEM: Piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Eco Evol 7:573–579
Lenth R, Singmann H, Love J et al (2019) Estimated marginal means, aka least-squares means. Version 1.4. R-core team, available online at: https://github.com/rvlenth/emmeans. Accessed 26 June 2019
Martel JW, Malcolm SB (2004) Density-dependent reduction and induction of milkweed cardenolides by a sucking insect herbivore. J Chem Ecol 30:545–561. https://doi.org/10.1023/B:JOEC.0000018628.48604.79
Masters GJ, Brown VK, Gange AC (1993) Plant mediated interactions between above- and belowground insect herbivores. Oikos 66:148–151. https://doi.org/10.2307/3545209
Molyneux RJ, Campbell BC, Dreyer DL (1990) Honeydew analysis for detecting phloem transport of plant natural products. J Chem Ecol 16:1899–1909
Mundim FM, Pringle EG (2018) Whole-plant metabolic allocation under water stress. Front Plant Sci 9:852. https://doi.org/10.3389/fpls.2018.00852
Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75
Panda N, Banerjee S, Mandal NB, Sahu NP (2006) Pregnane glycosides. Nat Prod Commun. https://doi.org/10.1177/1934578X0600100813(1:1934578X0600100813)
Petschenka G, Fei CS, Araya JJ et al (2018) Relative selectivity of plant cardenolides for Na+/K+-ATPases from the monarch butterfly and non-resistant insects. Front Plant Sci 9:1424. https://doi.org/10.3389/fpls.2018.01424
Pringle EG, Dirzo R, Gordon DM (2011) Indirect benefits of symbiotic coccoids for an ant-defended myrmecophytic tree. Ecology 92:37–46
Pringle EG, Novo A, Ableson I et al (2014) Plant-derived differences in the composition of aphid honeydew and their effects on colonies of aphid-tending ants. Ecol Evol 4:4065–4079. https://doi.org/10.1002/ece3.1277
Pringle EG, Ableson I, Kerber J et al (2017) Orthogonal fitness benefits of nitrogen and ants for nitrogen-limited plants in the presence of herbivores. Ecology 98:3003–3010. https://doi.org/10.1002/ecy.2013
Pringle RM, Kartzinel TR, Palmer TM et al (2019) Predator-induced collapse of niche structure and species coexistence. Nature 570:58
R Core Team (2019) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria
Ramirez RA, Spears LR (2014) Stem nematode counteracts plant resistance of aphids in alfalfa, Medicago sativa. J Chem Ecol 40:1099–1109. https://doi.org/10.1007/s10886-014-0504-3
Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483
Richards LA, Dyer LA, Forister ML et al (2015) Phytochemical diversity drives plant–insect community diversity. PNAS 112:10973–10978. https://doi.org/10.1073/pnas.1504977112
Roeske CN, Seiber JN, Brower LP, Moffitt CM (1976) Milkweed cardenolides and their comparative processing by monarch butterflies (Danaus plexxipus L.). In: Wallace JW, Mansell RL (eds) Biochemical interaction between plants and insects. Plenum Press, New York, pp 93–167
Rothschild M, Euw J, Reichstein T (1970) Cardiac glycosides in oleander aphid, Aphis nerii. J Insect Physiol 16:1141–1145. https://doi.org/10.1016/0022-1910(70)90203-9
Sasser JN, Eisenback JD, Carter CC, Triantaphyllou AC (1983) The international Meloidogyne project-its goals and accomplishments. Annu Rev Phytopathol 21:271–288
Shurtleff MC, Averre CW (2005) Diagnosing plant diseases caused by nematodes. The American phytopathological society, St. Paul, Minnesota, USA
Smith RA, Mooney KA, Agrawal AA (2008) Coexistence of three specialist aphids on common milkweed, Asclepias syriaca. Ecology 89:2187–2196
Soler R, Van der Putten WH, Harvey JA et al (2012) Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms. J Chem Ecol 38:755–767. https://doi.org/10.1007/s10886-012-0104-z
Strauss SY, Irwin RE (2004) Ecological and evolutionary consequences of multispecies plant-animal interactions. Annu Rev Ecol Evol Syst 35:435–466. https://doi.org/10.1146/annurev.ecolsys.35.112202.130215
Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc B 274:151–164. https://doi.org/10.1098/rspb.2006.3701
Tao L, Hunter MD, de Roode JC (2017) Microbial root mutualists affect the predators and pathogens of herbivores above ground: mechanisms, magnitudes, and missing links. Front Ecol Evol. https://doi.org/10.3389/fevo.2017.00160
Therneau TM (2015) A package for survival analysis in S. Version 2.38. https://CRAN.R-project.org/package=survival. Accessed 18 Nov 2019
Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4:147. https://doi.org/10.1007/s10311-006-0068-8
Trudgill DL, Blok VC (2001) Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathol 39:53–77. https://doi.org/10.1146/annurev.phyto.39.1.53
van Dam NM, Wondafrash V, Mathur V, Tytgat TOG (2018) Differences in hormonal signaling triggered by two root-feeding nematode species result in contrasting effects on aphid population growth. Front Ecol Evol. https://doi.org/10.3389/fevo.2018.00088
Völkl W, Woodring J, Fischer M et al (1999) Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia 118:483–491
Wäckers FL, Bezemer TM (2003) Root herbivory induces an above-ground indirect defence. Ecol Lett 6:9–12
Wallace JW, Mansell RL (eds) (1976) Biochemical interaction between plants and insects. Plenum Press, New York
Warashina T, Noro T (2000a) Steroidal glycosides from the aerial part of Asclepias incarnata. Phytochemistry 53:485–498. https://doi.org/10.1016/S0031-9422(99)00560-9
Warashina T, Noro T (2000b) Cardenolide and oxypregnane glycosides from the root of Asclepias incarnata L. Chem Pharm Bull 48:516–524
Wardle DA, Bardgett RD, Klironomos JN et al (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633
Wyatt R, Hunt DM (1991) Hybridization in north American Asclepias. II Flavonoid Evidence Syst Bot 16:132–142. https://doi.org/10.2307/2418978
Zehnder CB, Hunter MD (2007) Interspecific variation within the genus Asclepias in response to herbivory by a phloem-feeding insect herbivore. J Chem Ecol 33:2044–2053. https://doi.org/10.1007/s10886-007-9364-4
Züst T, Agrawal AA (2016a) Mechanisms and evolution of plant resistance to aphids. Nat Plants 2:16206. https://doi.org/10.1038/NPLANTS.2015.206
Züst T, Agrawal AA (2016b) Population growth and sequestration of plant toxins along a gradient of specialization in four aphid species on the common milkweed Asclepias syriaca. Funct Ecol 30:547–556. https://doi.org/10.1111/1365-2435.12523
Züst T, Agrawal AA (2017) Plant chemical defense indirectly mediates aphid performance via interactions with tending ants. Ecology 98:601–607. https://doi.org/10.1002/ecy.1707
Acknowledgements
We are deeply indebted to Michael Reichelt (MPICE, Jena, Germany) for helping us to think broadly about milkweed chemistry. We also thank Sybille Lorenz (MPICE, Jena, Germany) for analyzing our samples by UHPLC-ESI-HRMS, and we thank the members of the Pringle Lab, the Plant-Insect Group (“PIG”) at UNR, and three anonymous reviewers for their constructive comments on the manuscript. EGP was funded by an Alexander von Humboldt Fellowship, and both authors were funded by the University of Nevada, Reno.
Author information
Authors and Affiliations
Contributions
FMM and EGP conceived and designed the experiments. FMM performed the experiments. FMM and EGP analyzed and interpreted the data and wrote the manuscript.
Corresponding authors
Additional information
Communicated by Colin Mark Orians.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mundim, F.M., Pringle, E.G. Phytochemistry-mediated disruption of ant–aphid interactions by root-feeding nematodes. Oecologia 194, 441–454 (2020). https://doi.org/10.1007/s00442-020-04777-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04777-8