Skip to main content
SpringerLink
Log in

Effects of above- and belowground herbivory of specialists and generalists on the growth and defensive chemicals of introduced and native Chinese tallow seedlings

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Spatially separated aboveground (AG) and belowground (BG) herbivores can affect each other and alter plant growth and defense, although the outcome of AG-BG herbivore interactions may vary with herbivore type (specialists versus generalists). Here, we explored how AG and BG specialists and generalists interacted on different plant genotypes.

Methods

We subjected native and introduced seedlings of T. sebifera to herbivory by a specialist/generalist caterpillar, and BG herbivory by a root-knot nematode. We compared interactions between the herbivores and how they influenced the growth and defensive chemicals in T. sebifera.

Results

A field survey showed that AG insect exclusion greatly increased the root knot number of nematodes. However, a common-garden experiment showed that the AG specialist only facilitated nematodes on native seedlings, while the AG generalist only facilitated nematodes on introduced plants. The larval biomass of the specialist caterpillar was lower but that of the generalist caterpillar was higher on nematode-infested plants than on uninfested plants. Consistently, laboratory bioassays showed that consumption by the generalist caterpillar increased on nematode-infested plants, but consumption by the specialist caterpillar decreased. The above AG-BG herbivore interactions could be partially explained by changes in tannins and flavonoids. The changes in biomass, tannins and flavonoids after bouts of AG or BG herbivory were dependent on the type of AG caterpillars.

Conclusion

Our results demonstrate that herbivore type is important in shaping AG-BG interactions, and highlight the importance of measuring AG and BG linkages to fully understand how plants respond to different groups of herbivores.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AG:

aboveground

BG:

belowground

No:

no nematode

Nema:

nematode inoculation

References

  • Agrawal AA, Kotanen PM, Mitchell CE, Power AG, Godsoe W, Klironomos J (2005) Enemy release? An experiment with congeneric plant pairs and diverse above and belwogound enemies. Ecol 86:2979–2989

    Google Scholar 

  • Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302

    CAS  PubMed  Google Scholar 

  • Alston DG, Bradley JR, Schmitt JDP, Coble HD (1991) Response of Helicoverpa zea (Lepidoptera: Noctuidae) populations to canopy development in soybean as influenced by Heterodera glycines (Nematoda, Heteroderidae) and annual weed population densities. J Econ Entomol 84:267–276

    Google Scholar 

  • Arjen B, Aska G (2016) Plant-mediated systemic interactions between pathogens, parasitic nematodes, and herbivores above- and belowground. Annu Rev Phytopathol 54:499–527

    Google Scholar 

  • Barah P, Bones AM (2015) Multidimensional approaches for studying plant defence against insects: from ecology to omics and synthetic biology. J Exp Bot 66:479–493

    CAS  PubMed  Google Scholar 

  • Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecol 84:2258–2268

    Google Scholar 

  • Barker K (1985) Nematode extraction and bioassays. In: Barker KRCC, Sasser JN (eds) An advanced treatise on Meloidogyne, vol 2. North Carolina State University Graphics, Raleigh

    Google Scholar 

  • Bezemer TM, van Dam NM (2005) Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol Evol 20:617–624

    PubMed  Google Scholar 

  • Bezemer TM, Wagenaar R, Van Dam NM, Wäckers FL (2003) Interactions between above- and belowground insect herbivores as mediated by the plant defense system. Oikos 101:555–562

    Google Scholar 

  • Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889

    Google Scholar 

  • Bruce K, Cameron G, Harcombe P, Jubinsky G (1998) Introduction, impact on native habitats, and management of a woody invader, the Chinese tallow tree, Sapium sebiferum (L.) Roxb. Nat Areas J 17:255–260

    Google Scholar 

  • Carter-Wientjes CH, Russin JS, Boethel DJ, Griffin JL, McGawley EC (2004) Feeding and maturation by soybean looper (Lepidoptera: Noctuidae) larvae on soybean affected by weed, fungus, and nematode pests. J Econ Entomol 97:14–20

    PubMed  Google Scholar 

  • Erb M, Robert CAM, Hibbard BE, Turlings TCJ (2011) Sequence of arrival determines plant-mediated interactions between herbivores. J Ecol 99:7–15

    Google Scholar 

  • Forkner RE, Marquis RJ, Lill JT (2004) Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecol Entomol 29:174–187

    Google Scholar 

  • Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hichri I, Barrieu F, Bogs J, Kappel C, Delrot S, Lauvergeat V (2011) Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J Exp Bot 62:2465–2483

    CAS  PubMed  Google Scholar 

  • Huang W, Carrillo J, Ding J, Siemann E (2012) Invader partitions ecological and evolutionary responses to above- and belowground herbivory. Ecol 93:2343–2352

    Google Scholar 

  • Huang W, Siemann E, Ding J (2018) Eco-evolutionary dynamics of above- and belowground herbivores and invasive plants. In: Ohgushi T, Wurst S, Johnson SN (eds) Aboveground-belowground community ecology. Springer International Publishing, Cham, pp 271–291

    Google Scholar 

  • Huang W, Siemann E, Wheeler GS, Zou J, Carrillo J, Ding J (2010) Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98:1157–1167

    Google Scholar 

  • Huang W, Siemann E, Yang X, Wheeler GS, Ding J (2013) Facilitation and inhibition: changes in plant nitrogen and secondary metabolites mediate interactions between above-ground and below-ground herbivores. Proc Royal Soc B: Biol Sci 280:20131318

    Google Scholar 

  • Hunter MD (2001) Out of sight, out of mind: the impacts of root-feeding insects in natural and managed systems. Agric For Entomol 3:3–9

    Google Scholar 

  • Jia Z, Tang M, Wu J (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    Google Scholar 

  • Johnson SN, Clark KE, Hartley SE, Jones TH, McKenzie SW, Koricheva J (2012) Aboveground-belowground herbivore interactions: a meta-analysis. Ecol 93:2208–2215

    Google Scholar 

  • Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714

    Google Scholar 

  • Kafle D, Hanel A, Lortzing T, Steppuhn A, Wurst S (2017) Sequential above- and belowground herbivory modifies plant responses depending on herbivore identity. BMC Ecol 17:10

    Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S, Denno RF (2008a) Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory. Ecol Lett 11:841–851

    PubMed  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008b) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecol 89:392–406

    Google Scholar 

  • 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

    Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Google Scholar 

  • Lankau RA (2007) Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol 175:176–184

    PubMed  Google Scholar 

  • Li X, Guo W, Siemann E, Wen Y, Huang W, Ding J (2016) Plant genotypes affect aboveground and belowground herbivore interactions by changing chemical defense. Oecol 182:1107–1115

    Google Scholar 

  • Li X, Li B, Meng L (2017) Below-ground nematode herbivory of resistant soybean cultivars impairs the performances of an above-ground caterpillar and its parasitoid. Ecol Entomol 42:712–720

    Google Scholar 

  • Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:417–422

    PubMed  Google Scholar 

  • MacKay J, Kotanen PM (2008) Local escape of an invasive plant, common ragweed (Ambrosia artemisiifolia L.), from above-ground and below-ground enemies in its native area. J Ecol 96:1152–1161

    Google Scholar 

  • Makkar H (2003) Quantification of tannins in tree and shrub foliage: a laboratory manual. Springer, New York

    Google Scholar 

  • Mao R, Lu X, Ding J (2011) Effects of a nematode Meloidogyne incognita and its interaction with above-ground herbivory on an invasive wetland plant, alligator weed (Alternanthera philoxeroides). Plant Species Biol 26:73–83

    Google Scholar 

  • Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373

    Google Scholar 

  • Nishida R (2014) Chemical ecology of insect-plant interactions: ecological significance of plant secondary metabolites. Biosci Biotechnol Biochem 78:1–13

    CAS  PubMed  Google Scholar 

  • Ohgushi T, Wurst S, Johnson SN (2018) Current knowledge and future challenges of aboveground and belowground community ecology. In: Ohgushi T, Wurst S, Johnson SN (eds) Aboveground-belowground community ecology. Springer International Publishing, Cham, pp 345–361

    Google Scholar 

  • Papadopoulou GV, van Dam NM (2017) Mechanisms and ecological implications of plant-mediated interactions between belowground and aboveground insect herbivores. Ecol Res 32:13–26

    CAS  Google Scholar 

  • Thompson T, Bidart MG (2017) Oviposition preferences of Plutella xylostella are influenced by the type of plant induction and glucosinolate hydrolysis profiles. J Insect Behav 30:507–518

    Google Scholar 

  • Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4:147–157

    CAS  Google Scholar 

  • van Dam NM, Harvey JA, Wäckers FL, Bezemer TM, van der Putten WH, Vet LEM (2003) Interactions between aboveground and belowground induced responses against phytophages. Basic Appl Ecol 4:63–77

    Google Scholar 

  • van Dam NM, Heil M (2011) Multitrophic interactions below and above ground: en route to the next level. J Ecol 99:77–88

    Google Scholar 

  • van Dam NM, Raaijmakers CE, van der Putten WH (2005) Root herbivory reduces growth and survival of the shoot feeding specialist Pieris rapae on Brassica nigra. Entomol Exp Appl 115:161–170

    Google Scholar 

  • van der Putten WH (2012) Climate change, aboveground-belowground interactions, and species' range shifts. Annu Rev Ecol Evol S 43:365–383

    Google Scholar 

  • Wang M, Bezemer TM, Der Putten WHV, Brinkman EP, Biere A (2018) Plant responses to variable timing of aboveground clipping and belowground herbivory depend on plant age. J Plant Ecol 11:696–708

    Google Scholar 

  • Wang M, Biere A, Van der Putten WH, Bezemer TM (2014) Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance. Oecol 175:187–198

    Google Scholar 

  • Wang Y, Siemann E, Wheeler GS, Zhu L, Gu X, Ding J (2012a) Genetic variation in anti-herbivore chemical defences in an invasive plant. J Ecol 100:894–904

    Google Scholar 

  • Wang Y, Zhu L, Gu X, Wheeler GS, Purcell M, Ding J (2012b) Pre-release assessment of Gadirtha inexacta, a proposed biological control agent of Chinese tallow (Triadica sebifera) in the United States. Biol Control 63:304–309

    Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Sci 304:1629–1633

    CAS  Google Scholar 

  • Wei H, He M, Lu X, Ding J (2016) Differences in interactions of aboveground and belowground herbivores on the invasive plant Alternanthera philoxeroides and native host A. sessilis. Biol Invasions 18:3437–3447

    Google Scholar 

  • Willett WC (2002) Balancing life-style and genomics research for disease prevention. Sci 296:695–698

    CAS  Google Scholar 

  • Wondafrash M, Van Dam N, Tytgat T (2013) Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects. Front Plant Sci 4:1–15

    Google Scholar 

  • Wouters FC, Blanchette B, Gershenzon J, Vassão DG (2016) Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores. Phytochem Rev 15:1127–1151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wurst S, Der Putten WHV (2007) Root herbivore identity matters in plant-mediated interactions between root and shoot herbivores. Basic Appl Ecol 8:491–499

    Google Scholar 

  • Zheng H, Wu Y, Ding J, Binion D, Fu WRR (2005) Invasive plants established in the United States that are found in Asia and their associated natural enemies. Forest Health Technology Enterprise Team, Morgantown

    Google Scholar 

  • Zou J, Siemann E, Rogers WE, DeWalt SJ (2008) Decreased resistance and increased tolerance to native herbivores of the invasive plant Sapium sebiferum. Ecography 31:663–671

    Google Scholar 

Download references

Acknowledgements

We would like to thank Shunliang Feng, Yazhen liu, Wei Wang, Ruiling Liu for insect collection and experimental assistance. We especially thank the group of Jianqing Ding for providing part of tallow seeds, and two anonymous reviewers for their valuable comments on earlier versions of this paper. We would also like to thank Van Driesche Scientific Editing for editing of the manuscript. This study was funded by the National Natural Science Foundation of China (31800423, 31660087), and the Natural Science Foundation of Guangxi Province (2018GXNSFBA281172).

Author information

Authors and Affiliations

  1. Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, Nanning, 530004, Guangxi, China

    Xiaoqiong Li, Xu Gao & Si Shen

  2. Guangxi Youyiguan Forest Ecosystem Research Station, Pingxiang, 532600, Guangxi, China

    Xiaoqiong Li

  3. Biosciences Department, Rice University, Houston, TX, 77005, USA

    Evan Siemann

  4. Guangxi Crop Genetic Improvement and Biotechnology Lab, Guangxi Academy of Agricultural Sciences, Nanning, 530007, Guangxi, China

    Wenfeng Guo

Authors
  1. Xiaoqiong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xu Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Evan Siemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Si Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenfeng Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wenfeng Guo.

Additional information

Responsible Editor: Hans Lambers.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 25 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, X., Gao, X., Siemann, E. et al. Effects of above- and belowground herbivory of specialists and generalists on the growth and defensive chemicals of introduced and native Chinese tallow seedlings. Plant Soil 455, 65–78 (2020). https://doi.org/10.1007/s11104-020-04666-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-020-04666-2

Keywords

Search

Navigation