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An integrated analysis of hyperspectral and morphological data of cicada ovipositors revealed unexplored links to specific oviposition hosts

  • Zehai Hou
  • Haiying Zhong
  • Christian Nansen
  • Cong WeiEmail author
Original Paper
  • 21 Downloads

Abstract

Oviposition host selection by females greatly influences the survival of insect offspring. Based on data collected from 11 cicada species, we propose a new analytical approach to examine associations between oviposition host selection (live or dead wood) and three types of quantitative data (reflectance data acquired from ovipositors, morphometric data, and types and distribution of various sensilla). The study hypothesis was that a combination of these quantitative data would provide accurate characterization of species with known oviposition hosts and also enable prediction of a species with unknown oviposition hosts. Using cluster analysis based on morphometric and types and distribution of various sensilla as explanatory variables, the 11 cicada species were clearly categorized into two groups, i.e., one group ovipositing in live twigs, and the other group ovipositing in dead twigs. Although host selection of two species with unknown ovipositional preference awaits to be confirmed by future field investigation, we used the proposed integrated functional morphology approach to predict that these two species oviposit in dead twigs. Animal ecologists and evolutionary biologists frequently face the challenge of having incomplete information about function and behavior of animals, and therefore, seek to perform functional morphological studies. The combination of cluster analysis of morphometric and reflectance data as explanatory variables described in this study may be considered of considerable relevance to this broad audience.

Keywords

Cicadidae Oviposition host selection Adaptive trait Hyperspectral imaging Morphometrics Ultrastructure 

Notes

Acknowledgements

We would like to express our deep gratitude to Yunxiang Liu (Northwest A&F University, Yangling, China) for his help with specimen collection. We thank Prof. Masami Hayashi (Tokyo University of Agriculture, Atsugi, Japan) and Chong He (Sun Yat-Sen University, Guangzhou, China) for providing valuable information of oviposition behavior of cicadas. This work was supported by the National Natural Science Foundation of China (Grant no. 31772505, 31572302) to C.W.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

We neither used endangered species nor were the investigated animals collected in protected areas. All applicable international, national, and institutional guidelines for the care and use of animals were followed.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Blaustein L, Kiflawi M, Eitam A, Mangel M, Cohen JE (2004) Oviposition habitat selection in response to risk of predation in temporary pools: mode of detection and consistency across experimental venue. Oecologia 138:300–305.  https://doi.org/10.1007/s00442-003-1398-x CrossRefGoogle Scholar
  2. Blinn DW, Runck C (1989) Substratum requirements for oviposition, seasonal egg densities, and conditions for egg eclosion in Ranatra montezuma (Heteroptera: Nepidae). Ann Entomol Soc Am 82:707–711.  https://doi.org/10.1093/aesa/82.6.707 CrossRefGoogle Scholar
  3. Browning TO (1968) Water and the eggs of insects. In: Beament JWL, Treherne JE (eds) Insects and physiology. American Elsevier Publ Co, New York, pp 315–328Google Scholar
  4. Buxton PA (1932) Terrestrial insects and the humidity of the environment. Biol Rev 7:275–320CrossRefGoogle Scholar
  5. Chadha GK, Roome RE (1980) Oviposition behaviour and the sensilla of the ovipositor of Chilo partellus and Spodoptera littoralis (Lepidoptera: Noctuidae). J Zool 192:169–178.  https://doi.org/10.1111/j.1469-7998.1980.tb04228.x CrossRefGoogle Scholar
  6. Chou I, Lei ZR, Li L, Lu XL, Yao W (1997) The Cicadidae of China (Homoptera: Cicadoidea). Tianze Eldoneio, Hong KongGoogle Scholar
  7. Crump ML (1991) Choice of oviposition site and egg load assessment by a treefrog. Herpetologica 47:308–315Google Scholar
  8. Cyranoski D (2007) Flying insects threaten to deafen Japan. Nature 448:977.  https://doi.org/10.1038/448977a CrossRefGoogle Scholar
  9. Decaro Júnior ST, Martinelli NM, Maccagnan DHB, Ribeiro ES (2012) Oviposition of Quesada gigas (Hemiptera: Cicadidae) in coffee plants. Rev Colomb Entomol 38:1–5Google Scholar
  10. Edney EB (1977) Water balance in land arthropods. Springer, BerlinCrossRefGoogle Scholar
  11. Fisher RA (1936) The use of multiple measurements in taxonomic problems. Ann Eugen 7:179–188.  https://doi.org/10.1111/j.1469-1809.1936.tb02137.x CrossRefGoogle Scholar
  12. Fonseca JP (1945) As cigarras do cafeeiro e seu combate. Boletim Agrícola 8:297–304Google Scholar
  13. Hallberg E, Ahman I (1987) Sensillar types of the ovipositor of Dasineura brassicae: structure and relation to oviposition behaviour. Physiol Entomol 12:51–58.  https://doi.org/10.1111/j.1365-3032.1987.tb00723.x CrossRefGoogle Scholar
  14. Hayashi M, Saisho Y (2015) The Cicadidae of Japan. Seibundo Shinkosha, TokyoGoogle Scholar
  15. Hou Z, Li Q, Yang M, Liu Y, Wei C (2015) Ecology of cicada Meimuna mongolica nymphs: instars, morphological variation, vertical distribution and population density, host-plant selection, and emergence phenology. J Insect Sci 15:42.  https://doi.org/10.1093/jisesa/iev031 CrossRefGoogle Scholar
  16. Hou Z, Luo C, Roberts JD, Wei C (2017) Sexual pair-formation in a cicada mediated by acoustic behaviour of females and positive phonotaxis of males. Sci Rep 7:6453.  https://doi.org/10.1038/s41598-017-06825-5 CrossRefGoogle Scholar
  17. Huk T, Kuhne B (1999) Substrate selection by Carabus clatratus (Coleoptera, Carabidae) and its consequences for offspring development. Oecologia 121:348–354.  https://doi.org/10.1007/s004420050938 CrossRefGoogle Scholar
  18. Hummel NA, Zalom FG, Peng CY (2006) Structure of female genitalia of glassy-winged sharpshooter, Homalodisca coagulata (Say) (Hemiptera: Cicadellidae). Arthropod Struct Dev 35:111–125.  https://doi.org/10.1016/j.asd.2006.05.001 CrossRefGoogle Scholar
  19. Justus KA, Mitchell BK (1996) Oviposition site selection by the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). J Insect Behav 9:887–898.  https://doi.org/10.1007/BF02208976 CrossRefGoogle Scholar
  20. Kundanati L, Gundiah N (2014) Biomechanics of substrate boring by fig wasps. J Exp Biol 217:1946–1954.  https://doi.org/10.1242/jeb.098228 CrossRefGoogle Scholar
  21. Leertouwer HL, Wilts BD, Stavenga DG (2011) Refractive index and dispersion of butterfly chitin and bird keratin measured by polarizing interference microscopy. Opt Express 19:24061–24066.  https://doi.org/10.1364/OE.19.024061 CrossRefGoogle Scholar
  22. Li X, Xu H, Feng L, Fu X, Zhang Y, Nansen C (2017) Using proximal remote sensing in non-invasive phenotyping of invertebrates. PLoS One 12:e0176392.  https://doi.org/10.1371/journal.pone.0176392 CrossRefGoogle Scholar
  23. Luo C, Wei C, Nansen C (2015) How do “mute” cicadas produce their calling songs? PLoS One 10:e0118554.  https://doi.org/10.1371/journal.pone.0118554 CrossRefGoogle Scholar
  24. Mattingly WB, Flory SL (2011) Plant architecture affects periodical cicada oviposition behavior on native and non-native hosts. Oikos 120:1083–1091.  https://doi.org/10.1111/j.1600-0706.2010.18994.x CrossRefGoogle Scholar
  25. Matushkina N, Gorb S (2007) Mechanical properties of the endophytic ovipositor in damselflies (Zygoptera, Odonata) and their oviposition substrates. Zoology 110:167–175.  https://doi.org/10.1016/j.zool.2006.11.003 CrossRefGoogle Scholar
  26. Matushkina N, Lambret P, Gorb S (2016) Keeping the golden mean: plant stiffness and anatomy as proximal factors driving endophytic oviposition site selection in a dragonfly. Zoology 119:474–480.  https://doi.org/10.1016/j.zool.2016.03.003 CrossRefGoogle Scholar
  27. Matzrafi M, Herrmann I, Nansen C, Kliper T, Zait Y, Ignat T, Siso D, Rubin B, Karnieli A, Eizenberg H (2017) Hyperspectral technologies for assessing seed germination and trifloxysulfuron-methyl response in Amaranthus palmeri (Palmer Amaranth). Front Plant Sci 8:474.  https://doi.org/10.3389/fpls.2017.00474 Google Scholar
  28. Moriyama M, Numata H (2006) Induction of egg hatching by high humidity in the cicada Cryptotympana facialis. J Insect Physiol 52:1219–1225.  https://doi.org/10.1016/j.jinsphys.2006.09.005 CrossRefGoogle Scholar
  29. Moriyama M, Numata H (2008) Diapause and prolonged development in the embryo and their ecological significance in two cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata. J Insect Physiol 54:1487–1494.  https://doi.org/10.1016/j.jinsphys.2008.08.008 CrossRefGoogle Scholar
  30. Moriyama M, Numata H (2011) A cicada that ensures its fitness during climate warming by synchronizing its hatching time with the rainy season. Zool Sci 28:875–881.  https://doi.org/10.2108/zsj.28.875 CrossRefGoogle Scholar
  31. Moriyama M, Matsuno T, Numata H (2016) Dead-twig discrimination for oviposition in a cicada, Cryptotympana facialis (Hemiptera: Cicadidae). Appl Entomol Zool 51:1–7.  https://doi.org/10.1007/s13355-016-0438-z CrossRefGoogle Scholar
  32. Morris DW (2003) Toward an ecological synthesis: a case for habitat selection. Oecologia 136:1–13.  https://doi.org/10.1007/s00442-003-1241-4 CrossRefGoogle Scholar
  33. Nansen C (2016) The potential and prospects of proximal remote sensing of arthropod pests. Pest Manag Sci 72:653–659.  https://doi.org/10.1002/ps.4209 CrossRefGoogle Scholar
  34. Nansen C, Elliot N (2016) Remote sensing and reflectance profiling in entomology. Annu Rev Entomol 61:139–158.  https://doi.org/10.1146/annurev-ento-010715-023834 CrossRefGoogle Scholar
  35. Nansen C, Singh K, Mian A, Allison BJ, Simmons CW (2016) Using hyperspectral imaging to characterize consistency of coffee brands and their respective roasting classes. J Food Eng 190:34–39.  https://doi.org/10.1016/j.jfoodeng.2016.06.010 CrossRefGoogle Scholar
  36. R Development Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 17 May 2016
  37. Refsnider JM, Janzen FJ (2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition site choice. Annu Rev Ecol Evol Syst 41:39–57.  https://doi.org/10.1146/annurev-ecolsys-102209-144712 CrossRefGoogle Scholar
  38. Reich P, Downes BJ (2003) Experimental evidence for physical cues involved in oviposition site selection of lotic hydrobiosid caddis flies. Oecologia 136:465–475.  https://doi.org/10.1007/s00442-003-1284-6 CrossRefGoogle Scholar
  39. Resetarits WJ, Wilbur HM (1989) Choice of oviposition site by Hyla chrysoscelis: role of predators and competitors. Ecology 70:220–228.  https://doi.org/10.2307/1938428 CrossRefGoogle Scholar
  40. Rudolf VH, Rödel MO (2005) Oviposition site selection in a complex and variable environment: the role of habitat quality and conspecific cues. Oecologia 142:316–325.  https://doi.org/10.1007/s00442-004-1668-2 CrossRefGoogle Scholar
  41. Spänhoff B, Alecke C (2004) Ecological aspects of the external morphology and functionality of the psychomyiid female ovipositor (Insecta, Trichoptera). Zoomorphology 123:213–220.  https://doi.org/10.1007/s00435-004-0104-9 CrossRefGoogle Scholar
  42. Spänhoff B, Alecke C, Kaschek N, Lange J, Meyer EI (2003) Morphological characteristics of sensilla on the female ovipositor of Lype phaeopa (Psychomyiidae; Trichoptera). J Insect Sci 3:12.  https://doi.org/10.1093/jis/3.1.12 CrossRefGoogle Scholar
  43. Stavenga DG, Leertouwer HL, Hariyama T, De Raedt HA, Wilts BD (2012) Sexual dichromatism of the damselfly Calopteryx japonica caused by a melanin-chitin multilayer in the male wing veins. PLoS One 7:e49743.  https://doi.org/10.1371/journal.pone.0049743 CrossRefGoogle Scholar
  44. Stoffolano JG Jr, Yin LRS (1987) Structure and function of the ovipositor and associated sensilla of the apple maggot, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae). Int J Insect Morphol 16:41–69.  https://doi.org/10.1016/0020-7322(87)90055-9 CrossRefGoogle Scholar
  45. Vilhelmsen L, Isidoro N, Romani R, Basibuyuk HH, Quicke DLJ (2001) Host location and oviposition in a basal group of parasitic wasps: the subgenual organ, ovipositor apparatus and associated structures in the Orussidae (Hymenoptera, Insecta). Zoomorphology 121:63–84.  https://doi.org/10.1007/s004350100046 CrossRefGoogle Scholar
  46. Voss SC, Magni P, Dadour I, Nansen C (2016) Reflectance-based determination of age and species of blowfly puparia. Int J Legal Med 131:263–274.  https://doi.org/10.1007/s00414-016-1458-5 CrossRefGoogle Scholar
  47. Wang Y, Nansen C, Zhang Y (2016) Integrative insect taxonomy based on morphology, mitochondrial DNA and hyperspectral reflectance profiling. Zool J Linn Soc 177:378–394.  https://doi.org/10.1111/zoj.12367 CrossRefGoogle Scholar
  48. White J (1981) Flagging: host defenses versus oviposition strategies in periodical cicadas (Magicicada spp., Cicadidae, Homoptera). Can Entomol 113:727–738.  https://doi.org/10.4039/Ent113727-8 CrossRefGoogle Scholar
  49. White J, Lloyd M (1981) On the stainability and mortality of periodical cicada eggs. Am Midl Nat 106:219–228.  https://doi.org/10.2307/2425158 CrossRefGoogle Scholar
  50. White J, Lloyd M, Karban R (1982) Why don’t periodical cicadas normally live in coniferous forests? Environ Entomol 11:475–482.  https://doi.org/10.1093/ee/11.2.475 CrossRefGoogle Scholar
  51. Wigglesworth VB (1964) The eggs of insects. In: Wigglesworth VB (ed) The life of insects. Weidenfeld and Nicholson, London, pp 76–85Google Scholar
  52. Wigglesworth VB (1972) Development in the egg. In: Wigglesworth VB (ed) The principles of insect physiology. Springer, Dordrecht, pp 1–26CrossRefGoogle Scholar
  53. Yang LH (2006) Periodical cicadas use light for oviposition site selection. Proc R Soc B 273:2993–3000.  https://doi.org/10.1098/rspb.2006.3676 CrossRefGoogle Scholar
  54. Zhong H, Zhang Y, Wei C (2017) Comparative morphology of ovipositor in cicadas (Hemiptera: Cicadidae), with considerations on their taxonomic significances. Zoomorphology 136:461–481.  https://doi.org/10.1007/s00435-017-0363-x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant ProtectionNorthwest A&F UniversityYanglingChina
  2. 2.Zhejiang Academy of Agricultural SciencesHangzhouChina
  3. 3.Department of Entomology and NematologyUniversity of CaliforniaDavisUSA

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