Skip to main content
SpringerLink
Log in

Energetic cost of girdling in a notodontid caterpillar, Oedemasia leptinoides

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

In North America, notodontid caterpillars feed predominantly on hardwood trees; some cause significant economic damage with periodic outbreaks. The late instars of several species cut girdles around the petiole, rachis, or stem before feeding on distal leaf blades. Little is known about the benefits or costs of girdling for caterpillars. In this paper, we analyzed the energetic cost of girdling by comparing final instars of a girdling notodontid, Oedemasia leptinoides, with two non-girdling notodontids, Cecrita guttivitta and Lochmaeus manteo. Time allocated to four behaviors (girdling, feeding, walking, and inactive) was measured in the field with 3-h observations each day over three days. We also measured metabolic rates for the four behaviors using flow-through respirometry. The metabolic rate for each behavior was multiplied by the time spent over the 9 h of observation to estimate the total energetic cost of each behavior. In the field, O. leptinoides on black hickory (Carya texana) spent 4.6 ± 0.9% of their time girdling. They cut girdles primarily on the first day and fed on leaves mostly on days 2 and 3. Their metabolic rate during girdling was similar to feeding and walking, but greater than inactivity. Overall, the larvae utilized 6.4 ± 1.2% of their total energy while girdling. Relative to non-girdlers, O. leptinoides larvae spent significantly less time and energy feeding on leaves suggesting a trade-off between girdling and feeding. To our knowledge, this study is the first to quantify the energetic cost of an insect behavior for modifying host plants before feeding.

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

Data availability

Data are included in the manuscript as online resource 4.

References

  • Aidley DJ (1976) Increase in respiratory rate during feeding in larvae of the armyworm, Spodoptera exempta. Physiol Entomol 1:73–75. https://doi.org/10.1111/j.1365-3032.1976.tb00890.x

    Article  Google Scholar 

  • Albanese G, Nelson MW, Vickery PD, Sievert PR (2007) Larval feeding behavior and ant association in frosted elfin, Callophrys irus (Lycaenidae). J Lepid Soc 61:61–66

    Google Scholar 

  • Andersen PC, Brodbeck BV, Herzog DC (2002) Girdling-induced nutrient accumulation in above ground tissue of peanuts and subsequent feeding by Spissistilus festinus, the three-cornered alfalfa hopper. Entomol Exp Appl 103:139–149. https://doi.org/10.1023/A:1020379717372

    Article  CAS  Google Scholar 

  • Appel HM, Martin MM (1992) Significance of metabolic load in the evolution of host specificity of Manduca sexta. Ecology 73:216–228

    Article  Google Scholar 

  • Babst BA, Ferrieri RA, Thorpe MR, Orians CM (2008) Lymantria dispar herbivory induces rapid changes in carbon transport and partitioning in Populus nigra. Entomol Exp Appl 128:117–125

    Article  CAS  Google Scholar 

  • Becker VO (2014) Checklist of New World Notodontidae (Lepidoptera: Noctuoidea). Lepidoptera Novae 7:1–40

    Google Scholar 

  • Bernays EA (1997) Feeding by lepidopteran larvae is dangerous. Ecol Entomol 22:121–123. https://doi.org/10.1046/j.1365-2311.1997.00042.x

    Article  Google Scholar 

  • Borazjani A, Graves CH Jr, Hedin PA (1985) Occurrence of juglone in various tissues of pecan and related species. Phytopathology 75:1419–1421

    Article  CAS  Google Scholar 

  • Casey TM (1993) Effects of temperature on foraging of caterpillars. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 5–28

    Google Scholar 

  • Castañeda LE, Figueroa CC, Fuentes-Contreras E, Niemeyer HM, Nespolo RF (2009) Energetic costs of detoxification systems in herbivores feeding on chemically defended host plants: a correlational study in the grain aphid, Sitobion avenae. J Exp Biol 212:1185–1190. https://doi.org/10.1242/jeb.020990

    Article  CAS  PubMed  Google Scholar 

  • Choong MF (1996) What makes a leaf tough and how this affects the pattern of Castanopsis fissa leaf consumption by caterpillars. Funct Ecol 10:668–674

    Article  Google Scholar 

  • Chown SL, Haupt TM, Sinclair BJ (2016) Similar metabolic rate-temperature relationships after acclimation at constant and fluctuating temperatures in caterpillars of a sub-Antarctic moth. J Insect Physiol. https://doi.org/10.1016/j.jinsphys.2015.11.010

    Article  PubMed  Google Scholar 

  • Cipollini D, Walters D, Voelckel C (2014) Costs of resistance in plants: from theory to evidence. Annu Plant Rev 47:263–307

    Article  CAS  Google Scholar 

  • Clarke AR, Zalucki MP (2000) Foraging and vein-cutting behaviour of Euploea core corinna (W. S. Macleay) (Lepidoptera: Nymphalidae) caterpillars feeding on latex-bearing leaves. Aust J Entomol 39:283–290

    Article  Google Scholar 

  • Dussourd DE (1993) Foraging with finesse: Caterpillar adaptations for circumventing plant defenses. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 92–131

    Google Scholar 

  • Dussourd DE (2017) Behavioral sabotage of plant defenses by insect folivores. Annu Rev Entomol 62:15–34. https://doi.org/10.1146/annurev-ento-031616-035030

    Article  CAS  PubMed  Google Scholar 

  • Dussourd DE, Peiffer M, Felton GW (2016) Chew and spit: tree-feeding notodontid caterpillars anoint girdles with saliva. Arthropod-Plant Interact 10:143–150

    Article  Google Scholar 

  • Dussourd DE, Van Valkenburg M, Rajan K, Wagner DL (2019) A notodontid novelty : Theroa zethus caterpillars use behavior and anti-predator weaponry to disarm host plants. PLoS ONE 14:e0218994. https://doi.org/10.1371/journal.pone.0218994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eichenseer H, Mathews MC, Powell JS, Felton GW (2010) Survey of a salivary effector in caterpillars: Glucose oxidase variation and correlation with host range. J Chem Ecol 36:885–897

    Article  CAS  Google Scholar 

  • Eyles A, Bonello P, Ganley R, Mohammed C (2010) Induced resistance to pests and pathogens in trees. New Phytol 185:893–908

    Article  Google Scholar 

  • Farag MA (2008) Headspace analysis of volatile compounds in leaves from the Juglandaceae (walnut) family. J Essent Oil Res 20:323–327. https://doi.org/10.1080/10412905.2008.9700023

    Article  CAS  Google Scholar 

  • Farmer EE (2014) Leaf defence. Oxford University Press, Oxford

    Book  Google Scholar 

  • Felton GW, Chung SH, Hernandez MGE, Louis J, Peiffer M, Tian D (2014) Herbivore oral secretions are the first line of protection against plant-induced defences. Annu Plant Rev 47:37–76

    Article  CAS  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. https://doi.org/10.1111/j.1365-2311.2004.0590.x

    Article  Google Scholar 

  • Ganong CN, Dussourd DE, Swanson JD (2012) Girdling by notodontid caterpillars: Distribution and occurrence. Arthropod Plant Interact 6:621–633. https://doi.org/10.1007/s11829-012-9214-3

    Article  Google Scholar 

  • Goren R, Huberman M, Goldschmidt EE (2010) Girdling: Physiological and horticultural aspects. Hortic Rev 30:1–36

    Google Scholar 

  • Heinrich B (1983) How avian predators constrain caterpillar foraging. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 224–247

    Google Scholar 

  • Heinrich B, Collins SL (1983) Caterpillar leaf damage, and the game of hide-and-seek with birds. Ecology 64:592–602

    Article  Google Scholar 

  • Karban R, Agrawal AA (2002) Herbivore offense. Annu Rev Ecol Syst 33:641–664

    Article  Google Scholar 

  • Kassambara A (2020) rstatix: Pipe-friendly framework for basic statistical tests. R package version 0.6.0. https://CRAN.R-project.org/package=rstatix

  • Kingsolver JG (2000) Feeding, growth, and the thermal environment of cabbage white caterpillars, Pieris rapae L. Physiol Biochem Zool 73:621–628

    Article  CAS  Google Scholar 

  • Kukal O, Dawson TE (1989) Temperature and food quality influences feeding behavior, assimilation efficiency and growth rate of arctic woolly-bear caterpillars. Oecologia 79:526–532

    Article  Google Scholar 

  • Lighton JR (2008) Measuring metabolic rates: A manual for scientists. Oxford University Press, New York

    Book  Google Scholar 

  • Lindroth RL, Anson BD, Weisbrod AV (1990) Effects of protein and juglone on gypsy moths: Growth performance and detoxification enzyme activity. J Chem Ecol 16:2533–2547. https://doi.org/10.1007/BF01017476

    Article  CAS  PubMed  Google Scholar 

  • Marquis RJ, Passoa SC, Lill JT, Whitfield JB, Le Corff J, Forkner RE, Passoa VA (2019) Illustrated guide to the immature Lepidoptera on oaks in Missouri. FHAAST-2018–05. Morgantown, WV: U.S. Department of Agriculture, Forest Service, Forest Health Assessment and Applied Sciences Team

  • Martinat PJ, Allen DC (1988a) Saddled prominent outbreaks in North America. Northern J Appl Forestry 5:88–91

    Article  Google Scholar 

  • Martinat PJ, Allen DC (1988b) Behavior of saddled prominent Heterocampa guttivitta (Walker)(Lepidoptera: Notodontidae) larvae in a northern hardwood forest. J New York Entomol Soc 96:470–478

    Google Scholar 

  • McEvoy PB (1984) Increase in respiratory rate during feeding in larvae of the armyworm, Spodoptera exempta. Physiol Entomol 9:191–195. https://doi.org/10.1111/j.1365-3032.1976.tb00890.x

    Article  Google Scholar 

  • Mitchell PL, Newsom LD (1984) Histological and behavioral studies of threecornered alfalfa hopper (Homoptera: Membracidae) feeding on soybean. Ann Entomol Soc Am 77:174–181

    Article  Google Scholar 

  • Moctezuma C, Hammerbacher A, Heil M, Gershenzon J, Méndez-Alonzo OK (2014) Specific polyphenols and tannins are associated with defense against insect herbivores in the tropical oak Quercus oleoides. J Chem Ecol 40:458–467. https://doi.org/10.1007/s10886-014-0431-3

    Article  CAS  PubMed  Google Scholar 

  • Montllor CB, Bernays EA (1983) Invertebrate predators and caterpillar foraging. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 170–202

    Google Scholar 

  • Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Caterpillar saliva beats plant defenses. Nature 416:599–600

    Article  CAS  Google Scholar 

  • Neal JJ (1987) Metabolic costs of mixed-function oxidase induction in Heliothis zea. Entomol exp appl 43:175–179

    Article  CAS  Google Scholar 

  • Noel ARA (1970) The girdled tree. Bot Rev 36:162–195

    Article  Google Scholar 

  • Orians CM, Thorn A, Gómez S (2011) Herbivore-induced resource sequestration in plants: why bother? Oecologia 167:1–9

    Article  Google Scholar 

  • Paro CM, Arab A, Vasconcellos-Neto J (2014) Specialization of Atlantic rain forest twig-girdler beetles (Cerambycidae: Lamiinae: Onciderini): variation in host-plant use by microhabitat specialists. Arthropod-Plant Interact 8:557–569

    Google Scholar 

  • Pearse IS, Hipp AL (2012) Global patterns of leaf defenses in oak species. Evolution 66:2272–2286. https://doi.org/10.1111/j.1558-5646.2012.01591.x

    Article  PubMed  Google Scholar 

  • Pearse IS, Gee WS, Beck JJ (2013) Headspace volatiles from 52 oak species advertise induction, species identity, and evolution, but not defense. J Chem Ecol 39:90–100

    Article  CAS  Google Scholar 

  • Pfannenstiel RS, Hunt RE, Yeargan KV (1995) Orientation of a hemipteran predator to vibrations produced by feeding caterpillars. J Insect Behav 8:1–9

    Article  Google Scholar 

  • R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  • Reudler JH, Lindstedt C, Pakkanen H, Lehtinen I, Mappes J (2015) Costs and benefits of plant allelochemicals in herbivore diet in a multi enemy world. Oecologia 179:1147–1158

    Article  CAS  Google Scholar 

  • Rivera-Vega LJ, Acevedo FE, Felton GW (2017) Genomics of Lepidoptera saliva reveals function in herbivory. Curr Opin Insect Sci 19:61–69. https://doi.org/10.1016/j.cois.2017.01.002

    Article  PubMed  Google Scholar 

  • Rodriguez-Saona C, Crafts-Brandner SJ, Williams L, Paré PW (2002) Lygus hesperus feeding and salivary gland extracts induce volatile emissions in plants. J Chem Ecol 28:1733–1747

    Article  CAS  Google Scholar 

  • Schultz JC (1983) Habitat selection and foraging tactics of caterpillars in heterogeneous trees. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic Press, New York, pp 61–90

    Chapter  Google Scholar 

  • Takai H, Ozawa R, Takabayashi J et al (2018) Silkworms suppress the release of green leaf volatiles by mulberry leaves with an enzyme from their spinnerets. Sci Rep 8:11942. https://doi.org/10.1038/s41598-018-30328-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thiboldeaux RL, Lindroth RL, Tracy JW (1994) Differential toxicity of juglone (5-hydroxy-1,4-naphthoquinone) and related naphthoquinones to saturniid moths. J Chem Ecol 20:1631–1641. https://doi.org/10.1007/BF02059885

    Article  CAS  PubMed  Google Scholar 

  • Turlings TCJ, Erb M (2018) Tritrophic interactions mediated by herbivore induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu Rev Entomol 63:433–452

    Article  CAS  Google Scholar 

  • Voelckel C, Jander G (2014) Insect-plant interactions. Annual Plant Reviews, vol 47. Wiley, Oxford

    Book  Google Scholar 

  • Westerterp KR (2017) Doubly labelled water assessment of energy expenditure: principle, practice, and promise. Eur J Appl Physiol 117:1277–1285. https://doi.org/10.1007/s00421-017-3641-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou S, Lou YR, Tzin V, Jander G (2015) Alteration of plant primary metabolism in response to insect herbivory. Plant Physiol 169:1488–1498. https://doi.org/10.1104/pp.15.01405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Many thanks to all who allowed us to place mercury vapor lights on their property to collect notodontid females (Reid and Ginny Adams, Ben Cash, Steve Karafit, Jerry Mimms, Robert Parker, Steve Runge, Scott Henderson Gulf Mountain WMA, Woolly Hollow State Park, Ouachita Mountain Biological Station). Permits were kindly provided by the Arkansas Game and Fish Commission (scientific collection permits #051120181 and 041820193) and the Arkansas Department of Parks and Tourism (permits #043-2018 and 050-2019). Thanks also to an anonymous reviewer for helpful suggestions, to Adrian Barrerra for assistance with data collection in the lab and field, Madison Srebalus for help rearing caterpillars, Deb Moon for noting that O. leptinoides larvae cut girdles even on excised stems, Arkansas State Parks for permission for field trials at Woolly Hollow State Park, and the University of Central Arkansas for financial support.

Funding

The research was supported by funding from the University of Central Arkansas (Graduate School, Department of Biology, College of Natural Sciences and Mathematics, University Research Council).

Author information

Authors and Affiliations

  1. Department of Biology, University of Central Arkansas, 180 Lewis Science Center, Conway, AR, 72035, USA

    Brianna K. Trejo, Matthew E. Gifford & David E. Dussourd

Authors
  1. Brianna K. Trejo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew E. Gifford
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David E. Dussourd
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DED, MEG, BT conceived and designed the experiments. BT performed the experiments. BT, MEG, DED analyzed the data. BT, DED wrote the paper.

Corresponding author

Correspondence to David E. Dussourd.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Scientific collection permits #051120181 and 041820193 issued by the Arkansas Game and Fish Commission for permission to collect moths. Permits #043–2018 and 050–2019 from the Arkansas Department of Parks and Tourism for permission to collect moths and complete field experiments at Woolly Hollow State Park.

Additional information

Handling Editor: Heikki Hokkanen.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Oedemasia leptinoides larva on a pecan leaf repeatedly compressing a girdle with its mandibles before coating the girdle surface with saliva (wmv 20157 KB)

11829_2021_9805_MOESM2_ESM.pdf

Total time that caterpillars spent a) feeding, b) walking, and c) inactive over 9 hours of observation (means ± 1 SE). Three caterpillar species were tested: Ol = O. leptinoides (n = 13), Cg = C. guttivitta (n = 17), Lm = L. manteo (n = 9). For each behavior, the time allocated to the behavior by the three caterpillar species differed significantly (one-way ANOVAs, P < 0.005 in each case). In each graph, bars with different letters differ significantly (P < 0.05 Tukey post hoc tests) (pdf 368 KB)

11829_2021_9805_MOESM3_ESM.pdf

Metabolic rate for a) feeding, b) walking, and c) inactivity (means ± 1 SE, n = 4-9 larvae/behavior/species). Bars with different letters differ significantly (P < 0.05) using Tukey post hoc tests. Abbreviations: Ol = O. leptinoides, Cg = C. guttivitta, Lm = L. manteo (pdf 365 KB)

Excel file with data from each experiment (xlsx 39 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Trejo, B.K., Gifford, M.E. & Dussourd, D.E. Energetic cost of girdling in a notodontid caterpillar, Oedemasia leptinoides. Arthropod-Plant Interactions 15, 161–170 (2021). https://doi.org/10.1007/s11829-021-09805-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-021-09805-9

Keywords

Search

Navigation