Eur. J. Entomol. 98 (3): 257-264, 2001 | DOI: 10.14411/eje.2001.042

A possible role for the dorsolateral protocerebral neurosecretory neurons in the trophic adaptations of Lymantria dispar (Lepidoptera: Lymantriidae)

Vesna PERIĘ-MATARUGA1, Jelica LAZAREVIĘ, Vera NENADOVIĘ
Institute for Biological Research "Sini¹a Stankovię", 29 Novembra 142, 11060 Belgrade, Yugoslavia; e-mail: vesper@ibbi.ibiss.bg.ac.yu

The activity and number of protocerebral neurosecretory neurons of the dorsolateral group (L1, L2 and L2'), as well as the size of the corpora allata were investigated in 5th instar larvae of the gypsy moth (Lymantria dispar) from two populations (oak and locust-tree forests) fed one of two host-plants (oak is a suitable and locust-tree an unsuitable host-plant).
The monitoring of activity related cytological parameters and the number of protocerebral dorsolateral neurosecretory neurons revealed that differently adapted populations respond to nutritive stress differently. The activity of the L1 neurosecretory neurons in the protocerebra of the caterpillars is low in those from the locust-tree forest regardless of host-plant quality. The L2 neurosecretory neurons in the oak population become active when they were fed the unsuitable host-plant whereas their activity was high in locust-tree caterpillars regardless of the host-plant. A decrease in the number of neurosecretory neurons in a response to a novel food was noticed in both populations. The activity of the L2' neurosecretory neurons was similar in all caterpillars, but their number was increased in those from the locust-tree forest. The corpora allata of the locust-tree caterpillars were large whereas those of the oak forest caterpillars only increased in size when they were fed locust-tree leaves.
It is obvious that nutritive stress results in neurosecretory reorganization and changes in the titre of hormones that modulate the morphogenetic programme.

Keywords: Nutritive stress, protocerebral dorsolateral neurosecretory neurons, corpora allata, Lymantria dispar, oak, locust-tree

Received: February 5, 2001; Revised: May 22, 2001; Accepted: June 19, 2001; Published: October 31, 2001  Show citation

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PERIĘ-MATARUGA, V., LAZAREVIĘ, J., & NENADOVIĘ, V. (2001). A possible role for the dorsolateral protocerebral neurosecretory neurons in the trophic adaptations of Lymantria dispar (Lepidoptera: Lymantriidae). EJE98(3), 257-264. doi: 10.14411/eje.2001.042
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References

  1. Agui N., Granger N.A., Bollenbacher W.E. & Gilbert L.I. 1979: Cellular localization of the insect prothoracicotropic hormone: In vitro assay of a single neurosecretory cell. Proc. Natl. Acad. Sci. USA 76: 5694-5698 Go to original source...
  2. Barbosa P. 1978: Host plant exploatation by the gypsy moth, Lymantria dispar. Entomol. Exp. Appl. 24: 28-37 Go to original source...
  3. Bogus M.I. & Scheller K. 1994: Identification of allatotropin-secreting cells in the brain of an insect larva. Naturwissenschaften 81: 87-89 Go to original source...
  4. Borkovec A.B. & Gelman D.B. (eds) 1986: Insect Neurochemistry and Neurophysiology. Humana Press, Clifton, NJ, 523 pp Go to original source...
  5. Chernysh S.I. 1991: Neuroendocrine system in insect stress. In Ivanovic J. & Jankovic-Hladni M. (eds): Hormones and Metabolism in Insect Stress. CRC Press, Boca Raton, pp. 69-97
  6. Dai J.D., Mizoguchi A., Satake L., Ishizaki H. & Gilbert L.I. 1994: Developmental changes in the PTTH content of the Bombyx mori brain-retrocerebral complex and hemolymph: Analysis by immunogold electron microscopy qualitative image analysis and tissue resolved fluoroimmunoassay. Dev. Biol. 171: 212-223 Go to original source...
  7. Downer R.G.H. & Laufer H. 1984: Endocrinology of Insects. Alan R. Liss, Inc., New York, 707 pp
  8. Elkinton J.S. & Liebhold A.M. 1990: Population dynamics of gypsy moth in North America. Annu. Rev. Entomol. 35: 571-596 Go to original source...
  9. Ewen A.B. 1962: An improved aldehyde fuchsin staining technique for neurosecretory products in insects. Trans. Am. Micr. Soc. 81: 94-96 Go to original source...
  10. Felton G.W. 1996: Nutritive quality of plant protein; Source of variation and insect herbivore responses. Arch. Insect Biochem. Physiol. 32: 107-130 Go to original source...
  11. Fescemyer H.W., Masler E.P., Kelly T.J. & Lusby W.R. 1995: Influence of development and prothoracicotropic hormone on the ecdysteroids produced in vitro by prothoracic glands of female gypsy moth (Lymantria dispar) pupae and pharate adults. J. Insect Physiol. 41: 489-500 Go to original source...
  12. Gilbert L. I., Rybcynski R. & Tobe S.S. 1996: Endocrine cascade in insect metamorphosis. In Gilbert L.I., Tata J.R. & Atkinson B.G. (eds.): Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells. Academic Press, New York, pp. 60-98
  13. Gray R.S., Muehleisen D.P. & Bollenbacher W.E. 1994: Multiple peptide expression by the L-NSC in the tobacco hornworm, Manduca sexta. In Borkovec A.B. & Loeb M.J. (eds): Insect Neurochemistry and Neurophysiology 1993. CRC, Boca Raton, FL pp. 251-254
  14. Gruntenko N.E., Khlebodarova T.M., Vasenkova I.A., Sukhanova M.Jh., Wilson T.G. & Rauschenbach I.Yu. 2000: Stress-reactivity of a Drosophila melanogaster strain with impaired juvenile hormone action. J. Insect Physiol. 46: 451-456 Go to original source...
  15. Highnam K.C. 1967: Insect endocrinology. J. Endocrinology 37: 6-8
  16. Hirashima A., Takeya R., Taniguchi E. & Eto M. 1995: Metamorphosis, activity of juvenile-hormone esterase and alteration of ecdysteroid titres: Effects of larval density and various stress on the red flour beetle, Tribolium freemani Hinton (Coleoptera: Tenebrionidae). J. Insect Physiol. 41: 383-388 Go to original source...
  17. Hiruma K. & Agui N. 1977: Relationship between histological changes and functions of the neurosecretory cells in the brain of the cobbage armyworm, Mamestra brassicae L. Appl. Entomol. Zool. 12: 42-49 Go to original source...
  18. Illyinskaya N.B. 1968: The dynamics of seasonal change resistance of insects in relation to diapause and neurosecretion. Acta Soc. Zool. Bohemoslov. 32: 217-222
  19. Ivanovic J., Jankovic-Hladni M., Stanic V., Nenadovic V. & Frusic M. 1989: The role of neurosecretion and metabolism in development of an oligophagous feeding habit in Morimus funereus larvae (Col.: Cerambycidae). Comp. Biochem. Physiol. 94A: 167-171 Go to original source...
  20. Ivanovic J. & Jankovic-Hladni M. 1991: Hormones and Metabolism in Insect Stress. CRC Press, Boca Raton, pp.178
  21. Ivanovic J.P., Stanic V., Raushenbach I. Yu., Jankovic-Hladni M., Nenadovic V. & Budker V.G. 1991: Influence of nutrition substrate on neuroendocrine system in the ontogenesis of a cerambycid Morimus funereus (Insecta). Zh. Obshch. Biol. 52: 205-213
  22. Kawakami A., Kataoka H., Oka T., Mizoguchy A., Kimura-Kawakami M., Adachi T., Iwami M., Nagasawa H., Suzuki A. & Ishizaki H. 1990: Molecular cloning of the Bombyx mori prothoracicotropic hormone. Science 247: 1333-1335 Go to original source...
  23. Kelly T.J., Masler E.P., Thyagaraja B.S., Bell R.A. & Borkovec A.B.1986: Prothoracicotropic hormone stimulation of ecdysone synthesis by the prothoracic glands of the gypsy moth, Lymantria dispar. In Borkovec A.B. & Gelman D.B. (eds): Insect Neurochemistry and Neurophysiology. Humana Press, Clifton, NJ, pp. 327-330 Go to original source...
  24. Kind T.V. 1968: Functional morphology of the neurosecretory system during certain types of larval diapause. Proc. 13th Int. Congr. Entomol., Moscow, pp. 396-397
  25. Lazarevic J. 2000: Physiological and Genetic Mechanisms of Adaptation to Unsuitable Nutrition in Lymantria dispar L. PhD thesis, Fac. Nat. Math. Sci., University of Belgrade, Belgrade, 356 pp
  26. Liebhold A.M., Gottschalk K.W., Muzika R.M., Montgomery M.E., Young R., O'Day K. & Kelley B. 1995: Suitability of North American tree species to the gypsy moth: A summary of field and laboratory tests. USDA For. Serv. Gen. Techn. Rep. NE-211 Go to original source...
  27. Loeb M.J. & Hayes D.K. 1980: Neurosecretion during diapause development in brains of mature embryos of the gypsy moth, Lymantria dispar. Ann. Entomol. Soc. Am. 73: 432-436 Go to original source...
  28. Meng-Ping T., Rong K., Zong-Shun W., John G.S.J. & Chih-Ming Y. 2001: Immunolocalization and possible effect of a moth allatotropin-like substance in a fly, Phormia regina (Diptera: Calliphoridae). J. Insect Physiol. 47: 233-244 Go to original source...
  29. Mitsuhashi J. 1963: Histological studies on the neurosecretory cells of the brain and on the corpus allatum during diapause in some lepidopterous insects. Tokyo Bull. Nat. Inst. Agric. Sci. Ser. C. 16: 67-118
  30. Nijhout H.F. 1999: Control mechanisms of polyphenic development in insects. Bio Sci. 49: 181-192 Go to original source...
  31. Okuda T. & Tanaka S. 1997: An allatostatic factor and juvenile hormone synthesis by corpora allata in Locusta migratoria. J. Insect Physiol. 43: 635-641 Go to original source...
  32. Peric V. 1990: The effect of feeding substrates on the development and activity of the protocerebral neurosecretory neurons Lymantria dispar caterpillars from different populations. M.Sci Thesis, University of Belgrade, Biological faculty, 98 pp
  33. Peric V., Jankovic-Hladni M. & Ivanovic J. 1988: The effect of different feeding substrates on the development of Lymantria dispar L. Plant Prot. 39: 133-138
  34. Peric-Mataruga V. 1997: The Activities of the Antioxidative System Enzymes and of Protocerebrum Neurosecretory Cells under Nutritional Stress Conditions in Lymantria Dispar L. Caterpillars of Different Population Origin. PhD Thesis, Fac. Nat. Math. Sci., University of Belgrade, Belgrade, 219 pp
  35. Peric-Mataruga V., Blagojevic D., Spasic M.B., Ivanovic J. & Jankovic-Hladni M. 1997: Effect of the host plant on the antioxidative defence in the midgut of Lymantria dispar L. caterpillars of different population origins. J. Insect Physiol. 43: 101-106 Go to original source...
  36. Peric-Mataruga V., Lazarevic J. & Nenadovic V. 1998: The effects of a short-term unsuitable diet on protocerebrum neurosecretory neurons of Lymantria dispar L. caterpillars originating from two populations. In Adamovic Z. (ed.): The Gypsy Moth Outbreaks in Serbia, BIG, Beograd, pp. 95-129
  37. Peric-Mataruga V., Lazarevic J. & Nenadovic V. 1999: Short term effects of host plant shift on lateral protocerebrum neurosecretory neurons in Lymantria dispar L. caterpillars. Pesticides 14: 281-298
  38. Pszczolkowski M.A. & Chiang A.S. 2000: Effects of chilling stress on allatal growth and juvenile hormone synthesis in the cockroach, Diploptera punctata. J. Insect Physiol. 46: 923-931 Go to original source...
  39. Raabe M. 1982: Insect Neurohormones. Plenum Press, New York and London, 352 pp Go to original source...
  40. Rossiter M.C. 1991: Maternal effects generate variation in life history: consequences of egg weight plasticity in the gypsy moth. Funct. Ecol. 5: 386-393 Go to original source...
  41. Scharrer B. & Weitzman M. 1970: Current problems in invertebrate neurosecretion. In Bargmann W. & Scharrer B. (eds): Aspects of Neuroendocrinology. Springer-Verlag, Berlin, Heidelberg, New York, pp.1-23 Go to original source...
  42. Sidor C. & Jodal I. 1983: The gypsy moth Porthetria dispar L. health investigation results in the locust tree forest "Bagremara" near Backa Palanka. Plant Prot. 34: 445-455
  43. Sokal R.R. & Rohlf F.J. 1981: Biometry. Freeman, San Francisco, 859 pp
  44. Stockhoff B.A. 1991: Starvation resistance of gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae): Trade-offs among growth, body size, and survival. Oecologia 88: 422-429 Go to original source...
  45. Terriere L.C. & Yu S.J. 1973: Insect juvenile hormones: induction of detoxifying enzymes in the housefly and detoxication by housefly enzymes. Pestic. Biochem. Physiol. 3: 73-83 Go to original source...
  46. Thomsen M. 1965: The neurosecretory system of the adult Calliphora erythrocephala. II. Histology of the neurosecretory cells of the brain and some related structures. Z. Zellforsch. 67: 693-717 Go to original source...
  47. Veelaert D., Tobe S.S., Yu G.G., Schoofs L. & Loof A.D. 1995: Allatostatic and allatotropic factors in the brain of the desert locust Schistocerca gregaria. Belg. J. Zool. 125: 243-249
  48. Yu S.J. 1995: Allelochemical stimulation of ecdysone 20-monooxygenase in fall armyworm larvae. Arch. Insect Biochem. Physiol. 28: 365-375 Go to original source...

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