Energetic cost of girdling in a notodontid caterpillar, Oedemasia leptinoides

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.

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Data availability

Data are included in the manuscript as online resource 4.

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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).

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

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Correspondence to David E. Dussourd.

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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.

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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)

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)

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)

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

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Keywords

  • Girdling behavior
  • Flow-through respirometry
  • Lepidoptera
  • Notodontidae
  • Oedemasia leptinoides