Desperate times call for desperate measures: short-term use of the common ash tree by gypsy moth larvae (Lepidoptera: Erebidae) under density and starvation stress

Authors

  • Slobodan D. Milanović 1. Faculty of Forestry, University of Belgrade, Kneza Višeslava 1, Belgrade 11030, Serbia; 2. Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemědělská 3, 61300 Brno, Czech Republic
  • Marija M. Popović Faculty of Forestry, University of Belgrade, Kneza Višeslava 1, Belgrade 11030
  • Jovan N. Dobrosavljević Faculty of Forestry, University of Belgrade, Kneza Višeslava 1, Belgrade 11030
  • Igor M. Kostić Institute for Multidisciplinary Research, University of Belgrade, Kneza Višeslava 1, Belgrade 11030
  • Jelica M. Lazarević Department of Insect Physiology and Biochemistry, Institute for Biological Research “Siniša Stanković” – National Institute of the Republic of Serbia, University of Belgrade, Bulevar Despota Stefana 142, Belgrade 11000 http://orcid.org/0000-0002-7026-9385

Keywords:

Lymantria dispar, Fraxinus excelsior, non-host use, recovery, Quercus cerris

Abstract

Paper description:

  • Ecological preference of gypsy moth larvae (GML) for non-host ash species increases during insect outbreak. We performed laboratory-feeding trials to assess the conditions that promote short-term use of common ash and the ability of GML to recover from ash ingestion.
  • Growth and consumption were compared between ash fed GML after encountering various density/starvation stresses, and between oak fed and ash-oak switched GML.
  • This is the first report showing that under moderate density/starvation stress GML can temporarily grow on ash leaves and recover after switching to optimal oak leaves.
  • Short-term ash use might give advantage during outbreaks when resources are depleted.


Abstract: Gypsy moth, Lymantria dispar L. (Lepidoptera: Erebidae) feeds on a large number of tree species, while ash, Fraxinus spp. (Lamiales: Oleaceae) species are considered resistant and are only sporadically eaten. To assess the conditions under which late instar gypsy moth larvae (GML) can temporarily use non-host common ash (CA) (F. excelsior L.), and to evaluate their ability to recover from ingestion of this toxic food, we determined the relative growth rate, the relative consumption rate and the amount of produced feces in different laboratory feeding trials. Our report is the first to show that under specific circumstances, the resources acquired after short-term consumption of CA leaves can be utilized for larval growth. We varied the intensity of density and starvation stress prior to feeding on CA leaves. We observed that after moderate stress a group of GML was temporarily capable of coping with CA leaves. Although observed growth and consumption were much lower on CA than on the optimal host oak, Quercus cerris L. (Fagales: Fagaceae), CA-oak-switched larvae showed the ability to recover from short-term use of a toxic non-host foliage. This suggests that feeding on CA might enable GML to survive under conditions of food shortage.

https://doi.org/10.2298/ABS191106067M

Received: November 6, 2019; Revised: November 27, 2019; Accepted: December 16, 2019; Published online: December 30, 2019

How to cite this article: Milanović SD, Popović MM, Dobrosavljević JN, Kostić IM, Lazarević JM. Desperate times call for desperate measures: short-term use of the common ash tree by gypsy moth larvae (Lepidoptera: Erebidae) under density and starvation stress. Arch Biol Sci. 2020;72(1):63-9.

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References

Lance DR. Host-seeking behavior of the gypsy moth: the influence of polyphagy and highly apparent host plants. In: Ahmad S, editor. Herbivorous Insects: Host-seeking Behavior and Mechanisms. New York: Academic Press; 1983. p. 201-24.

Liebhold AM, Gottschalk KW, Muzika RM, Montgomery ME, Young R, O’Day K, Kelly B. Suitability of North American tree species to gypsy moth: a summary of field and laboratory tests. General Technical Report NE-211. Radnor, PA, U. S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station. Radnor, USA: USDA Forest Service; 1995. 34 p.

Lechowicz MJ. Leaf quality and the host preferences of gypsy moth in the northern deciduous forest. In: Talerico RL, Montgomery M, technical coordinators. Proceedings, forest defoliator-host interactions: A comparison between gypsy moth and spruce budworms: Gen. Tech. Rep. NE-85; New Haven, CT; 1986 Apr 5-7. ; 1983 April 5-7, Broomall, PA: U.S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station; 1983. p. 67-82.

Lechowicz MJ, Mauffette Y. Host preferences of the gypsy moth in eastern North American versus European forests. Rev Entomol Que. 1986;31(1):43-51.

Mason CJ, McManus ML. Larval dispersal of the gypsy moth. In: Doane CC, McManus ML, editors. The gypsy moth: research toward integrated pest management. Washington, DC: US Department of Agriculture; 1981. p. 161-201.

Campbell RW, Hubbard DL, Sloan RJ. Patterns of gypsy moth occurrence within a sparse and numerically stable population. Environ Entomol. 1975;4(4):535-42.

Stojanović I. O gubaru (Liparis dispar). Šumar list. 1889;9-10:424-8.

Wittman JT, Aukema BH. Foliage type and deprivation alters the movement behavior of late instar European gypsy moth Lymantria dispar (Lepidoptera: Erebidae). J Insect Behav. 2019;32(1):24-37.

Valentine HT, Wallner WE, Wargo PM. Nutritional changes in host foliage during and after defoliation, and their relation to the weight of gypsy moth pupae. Oecologia. 1983;57(3):298-302.

Rossiter M, Schultz JC, Baldwin IT. Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology. 1988;69(1):267-77.

Mason CJ, Cannizzo Z, Raffa KF. Influence of diet and density on laboratory cannibalism behaviors in gypsy moth larvae (Lymantria dispar L.). J Insect Behav. 2014;27(6):693-700.

Mosher FH. Food plants of the gipsy moth in America. Washington, DC: US Department of Agriculture ; 1915. 39p.

Lechowicz MJ, Jobin L. Estimating the susceptibility of tree species to attack by the gypsy moth, Lymantria dispar. Ecol Entomol. 1983;8(2):171-83.

Žikić V, Stanković SS, Kavallieratos NG, Athanassiou C, Georgiou P, Tschorsnig HP, van Achterberg C. Parasitoids associated with Lymantria dispar (Lepidoptera: Erebidae) and Malacosoma neustria (Lepidoptera: Lasiocampidae) in Greece and comparative analysis of their parasitoid spectrums in Europe. Zool Anz. 2017;270:166-75.

Markovic I, Norris DM, Phillips JK, Webster FX. Volatiles involved in the nonhost rejection of Fraxinus pennsylvanica by Lymantria dispar larvae. J Agr Food Chem. 1996b;44(3):929-35.

Markovic I, Norris DM, Cekic M. Some chemical bases for gypsy moth, Lymantria dispar, larval rejection of green ash, Fraxinus pennsylvanica, foliage as food. J Chem Ecol. 1996a;22(12):2283-98.

Milanović S, Mihajlović L, Karadžić D, Jankovsky L, Aleksić P, Janković-Tomanić M, Lazarević J. Effects of pedunculate oak tree vitality on gypsy moth preference and performance. Arch Biol Sci. 2014;66(4):1659-72.

Thorpe KW, Tatman KM, Sellers P, Webb RE, Ridgway RL. Management of gypsy moths using sticky trunk barriers and larval removal. J Arboric. 1995;21:69-76.

Siliņš I, Šmits A. Ozolu mūķenes Lymantria dispar (Linnaeus, 1758) populācijas reproduktivitātes rādītāju novērtējums masu savairošanās reģionā. Mežzinātne. 2010;22(55):47-69.

Pavlushin SV, Belousova IA, Chertkova EA, Kryukova NA, Glupov VV, Martemyanov VV. The effect of population density of Lymantria dispar (Lepidoptera: Erebidae) on its fitness, physiology and activation of the covert nucleopolyhedrovirus. Eur J Entomol. 2019;116:85-91.

Durkin PR, Follansbee MH. Control/eradication agents for the gypsy moth-human health and ecological risk assessment for DDVP (Dichlorvos) final report. New York: Syracuse Research Corporation; 2004.

Waldbauer GP. The consumption and utilization of food by insects. In: Beament JWL, Treherne JE, Wigglesworth VB, editors. Advances in insect physiology. Vol. 5. London, New York: Academic Press; 1968. p. 229-88.

Farrar RR Jr, Barbour JD, Kennedy GC. Quantifying food consumption and growth in insects. Ann Entomol Soc Am. 1989;82(5):593-8.

McDonald JH. Handbook of Biological Statistics. 3rd ed. Baltimore, Maryland: Sparky House Publishing; 2014. 299 p.

Stoyenoff JL, Witter JA, Montgomery ME. Nutritional indices in the gypsy moth (Lymantria dispar (L.)) under field conditions and host switching situations. Oecologia. 1994;97(2):158-70.

Williams RS, Lincoln DE, Norby RJ. Leaf age effects of elevated CO2-grown white oak leaves on spring-feeding lepidopterans. Glob Change Biol. 1998;4(3):235-46.

Couture JJ, Meehan TD, Lindroth RL. Atmospheric change alters foliar quality of host trees and performance of two outbreak insect species. Oecologia. 2012;168(3):863-76.

Milanović S, Lazarević J, Popović Z, Miletić Z, Kostić M, Radulović Z, Karadzić D, Vuleta A. Preference and performance of the larvae of Lymantria dispar (Lepidoptera: Lymantriidae) on three species of European oaks. Eur J Entomol. 2014a;111(3):371-8.

Kurir A. Die Fraßpflanzen des Schwammspinners (Lymantria dispar L.) Beitrag zur Ernährungsbiologie des Schwammspinners. J Appl Entomol. 1953;34(4):543-86.

Southwood TRE. The number of species of insect associated with various trees. J Anim Ecol. 1961;30(1):1-8.

Markovic I, Norris DM, Nordheim EV. Gypsy moth (Lymantria dispar) larval development and survival to pupation on diet plus extractables from green ash foliage. Entomol Exp Appl. 1997;84(3):247-54.

Pokorska O, Dewulf J, Amelynck C, Schoon N, Joó É, Šimpraga M, Bloemen J, Steppe K, Van Langenhove H. Emissions of biogenic volatile organic compounds from Fraxinus excelsior and Quercus robur under ambient conditions in Flanders (Belgium). Int J Environ An Ch. 2012;92(15):1729-41.

Kostova I, Iossifova T. Chemical components of Fraxinus species. Fitoterapia. 2007;78(2):85-106.

Chen Y, Whitehill JG, Bonello P, Poland TM. Differential response in foliar chemistry of three ash species to emerald ash borer adult feeding. J Chem Ecol. 2011;37(1):29-39.

Cleary MR, Andersson PF, Broberg A, Elfstrand M, Daniel G, Stenlid J. Genotypes of Fraxinus excelsior with different susceptibility to the ash dieback pathogen Hymenoscyphus pseudoalbidus and their response to the phytotoxin viridiol – a metabolomic and microscopic study. Phytochemistry. 2014;102:115-25.

Qazi S, Lombardo D, Abou-Zaid M. A metabolomic and HPLC-MS/MS analysis of the foliar phenolics, flavonoids and coumarins of the Fraxinus species resistant and susceptible to emerald ash borer. Molecules. 2018;23(11):2734.

Bowers MD, Puttick GM. Iridoid glycosides and insect feeding preferences: gypsy moths (Lymantria dispar, Lymantriidae) and buckeyes (Junonia coenia, Nymphalidae). Ecol Entomol. 1989;14(3):247-56.

Konno K, Hirayama C, Yasui H, Nakamura M. Enzymatic activation of oleuropein: a protein crosslinker used as a chemical defense in the privet tree. Proc Natl Acad Sci USA. 1999;96(16):9159-64.

Ahmad S, Pardini RS. Mechanisms for regulating oxygen toxicity in phytophagous insects. Free Radical Bio Med. 1990;8(4):401-13.

Jedinák A, Maliar T, Grančai D, Nagy M. Inhibition activities of natural products on serine proteases. Phytother Res. 2006;20(3):214-7.

Konno K, Hirayama C, Shinbo H. Glycine in digestive juice: a strategy of herbivorous insects against chemical defense of host plants. J Insect Physiol. 1997;43(3):217-24.

Zhu-Salzman K, Zeng R. Insect response to plant defensive protease inhibitors. Annu Rev Entomol. 2015;60:233-52.

Pentzold S, Zagrobelny M, Rook F, Bak S. How insects overcome two-component plant chemical defence: plant β-glucosidases as the main target for herbivore adaptation. Biol Rev. 2014;89(3):531-51.

Corcket E, Giffard B, Sforza RFH. Food webs and multiple biotic interactions in plant–herbivore models. In: Sauvion N, Thiéry D, Calatayud P-A, editors. Advances in Botanical Research. Vol. 81, Insect-Plant Interactions in a Crop Protection Perspective. Academic Press; 2017. p. 111-137.

Ilijin L, Perić-Mataruga V, Radojičić R, Vlahović M, Mrdaković M, Mirčić D, Lazarević J. The influence of increased rearing density on medial protocerebral neurosecretory neurons of Lymantria dispar L. caterpillars. Arch Biol Sci. 2010;62(1):27-37.

Gibbs AG, Reynolds LA. Drosophila as a Model for Starvation: Evolution, Physiology, and Genetics. In: McCue MD, editor. Comparative Physiology of Fasting, Starvation, and Food Limitation. Berlin, Heidelberg: Springer; 2012. p. 37-51.

Price DP, Schilkey FD, Ulanov A, Hansen IA. Small mosquitoes, large implications: crowding and starvation affects gene expression and nutrient accumulation in Aedes aegypti. Parasit Vector. 2015;8(1):252.

Stockhoff BA. Starvation resistance of gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae): trade offs among growth, body size, and survival. Oecologia. 1991;88(3):422-9.

Gui Y, Grant A. Joint effects of density dependence and toxicant exposure on Drosophila melanogaster populations. Ecotox Environ Safe. 2008;70(2):236-43.

Rossiter MC. Genetic and phenotypic variation in diet breadth in a generalist herbivore. Evol Ecol. 1987;1(3):272-82.

Lindroth RL, Weisbrod AV. Genetic variation in response of the gypsy moth to aspen phenolic glycosides. Biochem Syst Ecol. 1991;19(2):97-103.

Lazarević J, Perić-Mataruga V, Prolić Z, Tucić N. Behavioral response to an unsuitable host plant in the gypsy moth (Lymantria dispar L.). Folia Biol-Krakow. 2003;51(1-2):129-31.

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Published

2020-03-24

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Milanović SD, Popović MM, Dobrosavljević JN, Kostić IM, Lazarević JM. Desperate times call for desperate measures: short-term use of the common ash tree by gypsy moth larvae (Lepidoptera: Erebidae) under density and starvation stress. Arch Biol Sci [Internet]. 2020Mar.24 [cited 2024Mar.29];72(1):63-9. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/4780

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