Micromorphology of the proboscis sensilla of Maniola jurtina (Linnaeus, 1758) (Nymphalidae: Satyrinae)

Abstract

Lepidoptera is the most suitable insect order to comprehend the connections between nutrition and mouthparts. The proboscis, which is typically tightly coiled between the labial palps, is a flexible organ used by most adult butterflies for extracting flower nectar and other liquids. We examined the proboscis structure and sensilla of Maniola jurtina Linn. by scanning electron microscope (SEM) in order to contribute to the relationship between food selection and proboscis structure in Satyrinae Sensilla chaetica (s. trichodea) of various lengths is the most common species along the proboscis. Sensilla styloconica is of pluricarinate type. It is densely located only in the distal region and is in rows. It has a long quill with 6 ribs (flat protrusions) and a relatively short nail. In the study, sensilla lengths were compared with the sensilla lengths of some other lepidopteran species.

Keywords

• scanning elektron microscopy
• ultrastructure
• sensilla
• proboscis
• Satyrinae

References

1. [1] H. W. Krenn, “Feeding mechanisms of adult Lepidoptera: structure, function, and evolution of the mouthparts,” Annual Review of Entomology, vol. 55, pp. 307–327, 2010, doi: 10.1146/annurev-ento-11240,085338.
2. [2] J. M. Zaspel, S. J. Weller, and M. A. Branham, “A comparative survey of proboscis morphology and associated structures in fruit-piercing, tear-feeding, and blood-feeding moths in Calpinae (Lepidoptera: Erebidae),” Zoomorphology, vol. 23, no. 3, pp. 203–225, 2011, doi: 10.1007/s00435-011-0132-1.
3. [3] M. S. Lehnert, D. Monaenkova, T. Andrukh, C. E. Beard, P. H. Adler, and K. G. Kornev, “Hydrophobic-hydrophilic dichotomy of the butterfly proboscis,” Journal of the Royal Society Interface, vol. 10, pp. 330–336, 2013.
4. [4] M. S. Lehnert, C. E. Beard, P. D. Gerard, K. G. Kornev, and P. H. Adler, “Structure of the lepidopteran proboscis in relation to feeding guild,” Journal of Morphology, vol. 277, pp. 167–182, 2016.
5. [5] D. Monaenkova, M. S. Lehnert, T. A. Alexander, C. E. Beard, B. R. Alexander, W.-K. Lin, P. H. Adler, and K. G. Kornev, “Butterfly proboscis: combining a drinking straw with a nanosponge facilitated diversification of feeding habits,” Journal of the Royal Society Interface, vol. 9, no. 69, pp. 720–726, 2012, doi: 10.1098/rsif.2011.0392.
6. [6] M. J. Norris, “The feeding-habits of the adult Lepidoptera Heteroneura,” Transactions of the Royal Entomological Society of London, vol. 85, pp. 61–90, 1936.
7. [7] W. Büttiker, “Biological and morphological notes on the fruit-piercing and eye-frequenting moths,” Proceedings of the XI International Congress of Entomology, Vienna, pp. 10–12, 1962.
8. [8] H. Bänziger and W. Büttiker, “Records of eye-frequenting Lepidoptera from man,” Journal of Medical Entomology, vol. 6, no. 1, pp. 53–58, 1969, doi: 10.1093/jmedent/6.1.53.

9. [9] H. Bänziger, “The piercing mechanism of the fruit-piercing moth Calpe [Calyptra] thalictri Bkh. (Noctuidae) with reference to the skin-piercing blood-sucking moth C. eustrigata mps,” Acta Tropica, vol. 27, pp. 53–88, 1970.
10. [10] H. Bänziger, “Biologie der lacriphagen Lepidopteren in Thailand und Malaya,” Revue Suisse de Zoologie, vol. 79, pp. 1381–1469, 1973.
11. [11] H. Bänziger, “Fruit-piercing moths (Lep., Noctuidae) in Thailand: a general survey and some new perspectives,” Mitteilungen der Schweizerischen Entomologischen Gesellschaft, vol. 55, pp. 213–240, 1982.
12. [12] J. A. Downes, “Lepidoptera feeding at puddle-margins, dung, and carrion,” Journal of the Lepidopterists' Society, vol. 27, no. 2, pp. 89–99, 1973.
13. [13] P. H. Adler and D. L. Pearson, “Why do male butterflies visit mud puddles?,” Canadian Journal of Zoology, vol. 60, pp. 322–325, 1982.
14. [14] L. E. S. Eastham and Y. E. E. Eassa, “The feeding mechanism of the butterfly Pieris brassicae L.,” Philosophical Transactions of the Royal Society B, vol. 239, pp. 1–43, 1955.
15. [15] H. W. Krenn, “Functional morphology and movements of the proboscis of Lepidoptera (Insecta),” Zoomorphology, vol. 110, pp. 105–114, 1990, doi: 10.1007/BF01632816.
16. [16] H. F. Paulus and H. W. Krenn, “Vergleichende Morphologie des Schmetterlingsrüssels und seiner Sensillen-ein Beitrag zur phylogenetischen Systematik der Papilionoidea (Insecta, Lepidoptera),” Journal of Zoological Systematics and Evolutionary Research, vol. 34, no. 4, pp. 203–216, 1996, doi: 10.1111/j.1439-0469.1996.tb00826.x.
17. [17] H. W. Krenn, J. D. Plant, and N. U. Szucsich, “Mouthparts of flower-visiting insects,” Arthropod Structure and Development, vol. 34, pp. 1–40, 2005, doi: 10.1016/j.asd.2004.10.002.
18. [18] J. M. Zaspel, S. Coy, K. Habanek, and S. J. Weller, “Presence and distribution of sensory structures on the mouthparts of self-medicating moths,” Zoologischer Anzeiger, vol. 253, no. 1, pp. 6–10, 2013, doi: 10.1016/j.jcz.2013.06.001.
19. [19] L. E. Gilbert, “Pollen feeding and reproductive biology of Heliconius butterflies,” Proceedings of the National Academy of Sciences, vol. 69, no. 6, pp. 1403–1407, 1972.
20. [20] J. K. Yuvaraj, M. N. Andersson, O. Anderbrant, and C. Löfstedt, “Diversity of olfactory structures: A comparative study of antennal sensilla in Trichoptera and Lepidoptera,” Micron, vol. 111, pp. 9–18, 2018, doi: 10.1016/j.micron.2018.05.006.
21. [21] W. Büttiker, H. W. Krenn, and J. F. Putterill, “The proboscis of eye-frequenting and piercing Lepidoptera (Insecta),” Zoomorphology, vol. 116, no. 2, pp. 77–83, 1996, doi: 10.1007/BF02526872.
22. [22] H. W. Krenn, “Proboscis assembly in Lepidoptera—a once in a lifetime sequence of events,” European Journal of Entomology, vol. 94, pp. 495–501, 1997.
23. [23] W. Speidel, H. Fanger, and C. M. Naumann, “The surface microstructure of the noctuid proboscis (Lepidoptera: Noctuidae),” Zoologischer Anzeiger, vol. 234, pp. 307–315, 1996.
24. [24] Y. Mengi and S. S. Çalışkan, “A morphological comparative study of proboscis sensilla between Pierinae and Coliadinae (Lepidoptera: Pieridae),” SHILAP Revista de Lepidopterología, vol. 52, no. 206, pp. 261–267, 2024, doi: 10.57065/shilap.
25. [25] M. J. Faucheux, “Sensillum types on the proboscis of the Lepidoptera: a review,” Annales de la Société Entomologique de France, vol. 49, no. 1, pp. 73–90, 2013, doi: 10.1080/00379271.2013.767514.
26. [26] D. Petr and W. K. Stewart, “Comparative morphology of sensilla styloconica on the proboscis of North American Nymphalidae and other selected taxa (Lepidoptera): Systematic and ecological considerations,” Transactions of the American Entomological Society, vol. 130, no. 4, pp. 293–409, 2004.
27. [27] H. Altner and I. Altner, “Sensilla with both, terminal pore and wall pores on the proboscis of the moth, Rhodogastria bubo Walker (Lepidoptera: Arctiidae),” Zoologischer Anzeiger, vol. 216, nos. 3–4, pp. 129–150, 1986.
28. [28] B. D. Walters, P. J. Albert, and R. Y. Zacharuk, “Morphology and ultrastructure of sensilla on the proboscis of the adult spruce budworm, Choristoneura fumiferana (Clem.) (Lepidoptera: Tortricidae),” Canadian Journal of Zoology, vol. 76, pp. 466–479, 1998, doi: 10.1139/z97-218.
29. [29] E. Städler, M. Städler-Steinbruchel, and W. D. Seabrook, “Chemoreceptors on the proboscis of the female eastern spruce budworm: morphological and histological study,” Mitteilungen der Schweizerischen Entomologischen Gesellschaft, vol. 47, pp. 63–68, 1974.
30. [30] C. Borner, “22. Ordn. Lepidoptera, Schmetterlinge. In Brohmer, P. (Ed.), Fauna von Deutschland,” 4th ed., Leipzig, Germany: X + 561 pp., 1932.
31. [31] S. Candan and N. K. Özyurt, “The morphology of the sensilla on the proboscis of Aporia crataegi (Linnaeus, 1758) (Lepidoptera: Pieridae),” Comm. Journal of Biology, vol. 6, no. 2, pp. 184–189, 2022, doi: 10.31594/commagene.1187494.
32. [32] S. S. Çalışkan, S. Candan, and N. K. Özyurt, “Ultrastructure of the sensilla on the proboscis of adult Tretopteryx pertusalis (Lepidoptera: Pyralidae),” Transactions of the American Entomological Society, vol. 149, no. 2, pp. 179–184, 2023.
33. [33] P. J. DeVries, “Patterns of butterfly diversity and promising topics in natural history and ecology,” in La Selva: Ecology and Natural History of a Neotropical Rainforest, L. A. MacDade et al., Eds., Chicago, IL: University of Chicago Press, pp. 187–194, 1994.
34. [34] P. J. DeVries, D. Murray, and R. Lande, “Species diversity in vertical, horizontal, and temporal dimensions of a fruit-feeding butterfly community in an Ecuadorian rainforest,” Biological Journal of the Linnean Society, vol. 62, no. 3, pp. 343–364, 1997.
35. [35] K. S. Brown Jr. and A. V. L. Freitas, “Atlantic Forest butterflies: indicators for landscape conservation,” Biotropica, vol. 32, pp. 934–956, 2000, doi: 10.1111/j.1744-7429.2000.tb00631.x.
36. [36] K. S. Brown Jr. and A. V. L. Freitas, “Butterflies communities of urban forests in Campinas, São Paulo, Brazil: Structure, instability, environmental correlates, and conservation,” Journal of Insect Conservation, vol. 6, pp. 217–231, 2002, doi: 10.1023/A:1024462523826.
37. [37] T. W. Pyrcz and J. Wojtusiak, “The vertical distribution of Pronophiline butterflies (Nymphalidae, Satyrinae) along an elevational transect in Monte Zerpa (Cordillera de Mérida, Venezuela) with remarks on their diversity and parapatric distribution,” Global Ecology and Biogeography, vol. 11, no. 3, pp. 211–221, 2002, doi: 10.1046/j.1466-822x.2002.00285.x.
38. [38] D. Tobar, J. O. Rangel, and M. G. Andrade, “Diversidad de mariposas (Lepidoptera: Rhopalocera) en la parte alta de la cuenca del río el Roble (Quindío-Colombia),” Caldasia, vol. 24, pp. 393–409, 2002.
39. [39] D. B. Ribeiro, P. I. Prado, K. S. Brown Jr., and A. V. L. Freitas, “Additive partitioning of butterfly diversity in a fragmented landscape: Importance of scale and implications for conservation,” Diversity and Distributions, vol. 14, pp. 961–968, 2008, doi: 10.1111/j.1472-4642.2008.00505.x.
40. [40] L. V. Vu, “Diversity and similarity of butterfly communities in five different habitat types at Tam Dao National Park, Vietnam,” Journal of Zoology, vol. 277, pp. 15–22, 2009, doi: 10.1111/j.1469-7998.2008.00498.x.
41. [41] H. Bänziger, “Skin-piercing blood-sucking moths III: Feeding act and piercing mechanism of Calyptra eustrigata (Hmps) (Lep., Noctuidae),” Mitteilungen der Schweizerischen Entomologischen Gesellschaft, vol. 53, pp. 127–142, 1980.
42. [42] M. J. Faucheux, “Morphology and distribution of sensilla on the cephalic appendages, tarsi and ovipositor of the European sunflower moth, Homoeosoma nebulella Den. & Schiff. (Lepidoptera: Pyralidae),” International Journal of Insect Morphology and Embryology, vol. 20, pp. 291–307, 1991, doi: 10.1016/0020-7322(91)90018-5.
43. [43] M. J. Faucheux, “Sensilla on the antennae, mouthparts, tarsi and ovipositor of the sunflower moth, Homoeosoma electellum (Hulster) (Lepidoptera: Pyralidae): A scanning electron microscopic study,” Annales des Sciences Naturelles, Zoologie et Biologie Animale, vol. 16, pp. 121–136, 1995.
44. [44] E. Hallberg, “Fine-structural characteristics of the antennal sensilla of Agrotis segetum (Insecta: Lepidoptera),” Cell and Tissue Research, vol. 218, pp. 209–218, 1981, doi: 10.1007/BF00210105.
45. [45] P. J. DeVries, The Butterflies of Costa Rica and Their Natural History: Papilionidae, Pieridae, and Nymphalidae, Princeton, NJ: Princeton University Press, 327 pp., 1987.
46. [46] C. Kremen, “Biological inventory using target taxa: A case study of the butterflies of Madagascar,” Ecological Applications, vol. 4, pp. 407–422, 1994.
47. [47] A. L. Viloria, Studies on the Systematics and Biogeography of Some Montane Satyrid Butterflies (Lepidoptera), Ph.D. dissertation, University of London, London, UK, 493 p., 1998.
48. [48] D. L. Murray, Systematics of Neotropical Satyrinae Butterflies (Nymphalidae: Satyrinae: Euptychiina) Based on Larval Morphology and DNA Sequence Data and the Evolution of Life History Traits, Ph.D. dissertation, Louisiana State University, New Orleans, LA, 380 p., 2001.
49. [49] M. C. Singer, P. R. Ehrlich, and L. E. Gilbert, “Butterfly feeding on lycopsid,” Science, vol. 172, pp. 1341–1342, 1971.
50. [50] M. C. Singer and J. Mallet, “Moss feeding by satyrine butterfly,” Journal of Research on the Lepidoptera, vol. 24, p. 392, 1986.
51. [51] P. R. Ackery, “Hostplants and classification: A review of nymphalid butterflies,” Biological Journal of the Linnean Society, vol. 33, pp. 95–203, 1988.
52. [52] G. W. Beccaloni, Á. L. Viloria, S. K. Hall, and G. S. Robinson, Catalogue of the Hostplants of the Neotropical Butterflies, Zaragoza, Spain: Sociedad Entomológica Aragonesa, 536 pp., 2008.
53. [53] H. W. Krenn, K. P. Zulka, and T. Gatschnegg, “Proboscis morphology and food preferences in Nymphalidae (Lepidoptera, Papilionoidea),” Journal of Zoology (London), vol. 253, pp. 17–26, 1998.
54. [54] H. W. Krenn and C. M. Penz, “Mouthparts of Heliconius butterflies (Lepidoptera: Nymphalidae): A search for anatomical adaptations to pollen-feeding behavior,” International Journal of Insect Morphology and Embryology, vol. 27, no. 4, pp. 301–309, 1998, doi: 10.1016/S0020-7322(98)00022-1.
55. [55] L. Ma, H. K., P. Li, J. Liu, and X. Yuan, “Ultrastructure of the proboscis sensilla of ten species of butterflies (Insecta: Lepidoptera),” PLOS ONE, vol. 14, no. 3, p. e0214658, 2019, doi: 10.1371/journal.pone.0214658.
56. [56] H. W. Krenn, “Proboscis sensilla in Vanessa cardui (Nymphalidae, Lepidoptera): Functional morphology and significance in flower-probing,” Zoomorphology, vol. 118, pp. 23–30, 1998, doi: 10.1007/s004350050053.
57. [57] F. Molleman, H. W. Krenn, M. E. Van Alphen, P. M. Brakefield, P. J. DeVries, and B. J. Zwaan, “Food intake of fruit-feeding butterflies: Evidence for adaptive variation in proboscis morphology,” Biological Journal of the Linnean Society (London), vol. 86, pp. 333–343, 2005, doi: 10.1111/j.1095-8312.2005.00533.x.