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The histology and ultrastructure of the salivary glands of Neopanorpa longiprocessa (Mecoptera: Panorpidae)

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Abstract

The salivary glands of Panorpidae usually exhibit distinct sexual dimorphism and are closely related to the nuptial feeding behavior. In this study, the salivary glands of Neopanorpa longiprocessa were investigated using light microscopy and transmission electron microscopy. The salivary glands are tubular labial glands and consist of a scoop-shaped salivary pump, a common salivary duct, and a pair of salivary tubes. The male and female salivary glands are remarkably different in the bifurcation position of the common salivary duct and the length and shape of the secretory tubes. Compared with the simple female salivary glands, the male’s are more developed as their paired elongated salivary tubes can be divided into two parts, the glabrate anterior tube and the posterior tube with many secretory tubules. The ultrastructural study shows that the male salivary tubes have strong secretory function. The existence of different secretion granules indicates that there are some chemical reactions or mixing occurring in the lumen. Based on the ultrastructural characteristics, the functions of the different regions of the salivary tube have been speculated. The relationship between the salivary glands and nuptial feeding behavior of N. longiprocessa has been briefly discussed based on the structure of the salivary glands.

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References

  • Ali DW (1997) The aminergic and peptidergic innervation of insect salivary glands. J Exp Biol 200:1941–1949

    CAS  PubMed  Google Scholar 

  • Azevedo DO, Zanuncio JC, Zanuncio JS Jr, Martins GF, Marques-Silva S, Sossai MF, Serrão JE (2007) Biochemical and morphological aspects of salivary glands of the predator Brontocoris tabidus (Heteroptera: Pentatomidae). Braz Arch Biol Technol 50:469–477

    CAS  Google Scholar 

  • Berhanu A, Abera A, Nega D, Mekasha S, Fentaw S, Assefa A, Gebrewolde G, Wuletaw Y, Assefa A, Dugassa S, Tekie H, Tasew G (2019) Isolation and identification of microflora from the midgut and salivary glands of Anopheles species in malaria endemic areas of Ethiopia. BMC Microbiol 19:85

    PubMed  PubMed Central  Google Scholar 

  • Beutel RG, Friedrich F, Hörnschemeyer T, Pohl H, Hünefeld F, Beckmann F, Meier R, Misof B, Whiting MF, Vilhelmsen L (2011) Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola. Cladistics 27:341–355

    Google Scholar 

  • Billen J, Joye L, Leuthold RH (1989) Fine structure of the labial gland in Macrotermes bellicosus (Isoptera, Termitidae). Acta Zool 70:37–45

    Google Scholar 

  • Bockwinkel G, Sauer KP (1994) Resource dependence of male mating tactics in the scorpionfly, Panorpa vulgaris (Mecoptera, Panorpidae). Anim Behav 47:203–209

    Google Scholar 

  • Byers GW, Thornhill R (1983) Biology of the Mecoptera. Annu Rev Entomol 28:203–228

    Google Scholar 

  • Castellanos N, Martínez LC, Silva EH, Teodoro AV, Serrão JE, Oliveira EE (2017) Ultrastructural analysis of salivary glands in a phytophagous stink bug revealed the presence of unexpected muscles. PLoS One 12:e0179478

    PubMed  PubMed Central  Google Scholar 

  • Chapman RF (1998) The insect: structure and function, 4th edn. Cambridge Univ. Press, Cambridge

    Google Scholar 

  • Cossolin JFS, Martínez LC, Pereira MJB, Vivan LM, Bozdoğan H, Fiaz M, Serrão JE (2019) Anatomy, histology, and ultrastructure of salivary glands of the burrower bug, Scaptocoris castanea (Hemiptera: Cydnidae). Microsc Microanal 25:1–9

    Google Scholar 

  • Dallai R, Mercati D, Mashimo Y, Machida R, Beutel RG (2017) The morphology and ultrastructure of salivary glands of Zoraptera (Insecta). Arthropod Struct Dev 46:508–517

    CAS  PubMed  Google Scholar 

  • Del Bene G, Cavallo V, Lupetti P, Dallai R (1999) Fine structure of the salivary glands of Heliothrips haemorrhoidalis (Bouché) (Thysanoptera: Thripidae). Int J Insect Morphol Embryol 28:301–308

    Google Scholar 

  • Engels S, Sauer KP (2006) Resource-dependent nuptial feeding in Panorpa vulgaris: an honest signal for male quality. Behav Ecol 17:628–632

    Google Scholar 

  • Engels S, Sauer KP (2008) A secondary sex trait under construction: age- and nutrition-related salivary gland development in a scorpionfly (Insecta: Mecoptera). J Zool Syst Evol Res 46:133–136

    Google Scholar 

  • Engqvist L, Sauer KP (2001) Strategic male mating effort and cryptic male choice in a scorpionfly. Proc R Soc Lond B 268:729–735

    CAS  Google Scholar 

  • Friedrich F, Pohl H, Beckmann F, Beutel RG (2013) The head of Merope tuber (Meropeidae) and the phylogeny of Mecoptera (Hexapoda). Arthropod Struct Dev 42:69–88

    PubMed  Google Scholar 

  • Hidayah ASN, Wahida ON, Shafinaz MNN, Idris AG (2013) Morphology of salivary gland and distribution of dopamine and serotonin on red palm weevil (RPW), Rhynchophorus ferrugineus (Coleoptera: Curculionidae). AIP Conf Proc 1571:345–348

    CAS  Google Scholar 

  • Hua BZ, Chou I (1997) The Panorpidae (Mecoptera) of Funiu Mountain in Henan Province. Entomotaxonomia 19:273–278

    Google Scholar 

  • Krenn HW (2007) Evidence from mouthpart structure on interordinal relationships in Endopterygota? Arthropod Syst Phyl 65:7–14

    Google Scholar 

  • Kumar D, Yadav PR, Venugopal KJ, Singh AK (1995) Studies on the salivary glands of an aquatic bug, Lethocerus Indicus (Belostomatidae): morphological, histological and preliminary electron microscopic investigations. Int J Trop Insect Sci 16:51–61

    Google Scholar 

  • Li N, Hu G-L, Hua B-Z (2019) Complete mitochondrial genomes of Bittacus strigosus and Panorpa debilis and genomic comparisons of Mecoptera. Int J Biol Macromol 140:672–681

    CAS  PubMed  Google Scholar 

  • Liu SY, Hua BZ (2010) Histology and ultrastructure of the salivary glands and salivary pumps in the scorpionfly Panorpa obtusa (Mecoptera: Panorpidae). Acta Zool 91:457–465

    Google Scholar 

  • Ma N, Hua BZ (2011) Structural evidence why males of Panorpa liui offer prey rather than salivary mass as their nuptial gift. Acta Zool 92:398–403

    Google Scholar 

  • Ma N, Liu SY, Hua BZ (2011) Morphological diversity of male salivary glands in Panorpidae (Mecoptera). Eur J Entomol 108:493–499

    Google Scholar 

  • Martínez LC, do Carmo Queiroz Fialho M, Zanuncio JC, Serrão JE (2014) Ultrastructure and cytochemistry of salivary glands of the predator Podisus nigrispinus (Hemiptera: Pentatomidae). Protoplasma 251:535–543

    PubMed  Google Scholar 

  • Martínez LC, Zanuncio JC, Morais WCC, Plata-Rueda A, Cedeño-Loja PE, Serrão JE (2015) Ultrastructure of the salivary glands of the stink bug predator Podisus distinctus. Microsc Microanal 21:1514–1522

    PubMed  Google Scholar 

  • Miao Y, Wang J-S, Hua B-Z (2019) Molecular phylogeny of the scorpionflies Panorpidae (Insecta: Mecoptera) and chromosomal evolution. Cladistics 35:385–400

    Google Scholar 

  • Misof B, Liu S, Meusemann K, Peters RS, Xin Z (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–767

    CAS  PubMed  Google Scholar 

  • Morrison MN (1989) Gel electrophoretic studies with reference to functional morphology of the salivary glands of Acanthaspis pedestris Stål. (Insecta: Heteroptera: Reduviidae). Proc Indian Acad Sci (Anim Sci) 98:167–173

    Google Scholar 

  • Nelson DL, Cox MM (2017) Lehninger principles of biochemistry, 7th edn. W. H. Freeman, New York

    Google Scholar 

  • Palmer CM (2010) Diversity of feeding strategies in adult Mecoptera. Terr Arthropod Rev 3:111–128

    Google Scholar 

  • Potter E (1938) The internal anatomy of the order Mecoptera. Trans R Entomol Soc Lond 87:467–501

    Google Scholar 

  • Ramm C, Wayadande A, Baird L, Nandakumar R, Madayiputhiya N, Amundsen K, Donze-Reiner T, Baxendale F, Sarath G, Heng-Moss T (2015) Morphology and proteome characterization of the salivary glands of the western chinch bug (Hemiptera: Blissidae). J Econ Entomol 108:2055–2064

    CAS  PubMed  Google Scholar 

  • Sahayaraj K, Kanna AV, Kumar SM (2009) Gross morphology of feeding canal, salivary apparatus and digestive enzymes of salivary gland of Catamirus brevipennis (Servile) (Hemiptera: Reduviidae). J Entomol Res Soc 12:37–50

    Google Scholar 

  • Sauer KP, Lubjuhn T, Sindern J, Kullmann H, Kurtz J, Epplen C, Epplen JT (1998) Mating system and sexual selection in the scorpionfly Panorpa vulgaris (Mecoptera: Panorpidae). Naturwissenschaften 85:219–228

    CAS  Google Scholar 

  • Schin K, Kroeger H (1980) (Na+ + K+)-ATPase activity in the salivary gland of a dipteran insect, Chironomus thummi. Insect Biochem 10:113–117

    CAS  Google Scholar 

  • Serrão JE, Castrillon MI, dos Santos-Mallet JR, Zanuncio JC, Gonçalves TCM (2008) Ultrastructure of the salivary glands in Cimex hemipterus (Hemiptera: Cimicidae). J Med Entomol 45:991–999

    PubMed  Google Scholar 

  • Thornhill R (1981) Panorpa (Mecoptera: Panorpidae) scorpionflies: systems for understanding resource-defense polygyny and alternative male reproductive efforts. Annu Rev Ecol Syst 12:355–386

    Google Scholar 

  • Uceli L, Pirovani V, Vicente N, Pikart T, Ferreira PS, Serrão J (2011) Morphology of the reproductive and digestive tracts of Adparaproba gabrieli (Heteroptera: Miridae). Int J Trop Insect Sci 31:219–224

    Google Scholar 

  • Walker GP (2009) Chapter 228 – salivary glands. In: Resh VH, Cardé RT (eds) Encyclopedia of insects, 2nd edn. Academic Press, San Diego, pp 897–901

    Google Scholar 

  • Whiting MF (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zool Scr 31:93–104

    Google Scholar 

  • Zhong W, Hua B-Z (2013) Mating behaviour and copulatory mechanism in the scorpionfly Neopanorpa longiprocessa (Mecoptera: Panorpidae). PLoS One 8:e74781

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong W, Qi ZY, Hua BZ (2015) Atypical mating in a scorpionfly without a notal organ. Contrib Zool 84:305–315

    Google Scholar 

  • Zhu YC, Yao J, Luttrell R (2016) Identification of genes potentially responsible for extra-oral digestion and overcoming plant defense from salivary glands of the tarnished plant bug (Hemiptera: Miridae) using cDNA sequencing. J Insect Sci 16:60

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Ji-Shen Wang (Northwest A&F University, Yangling, China) for assistance in species identification. Our manuscript was greatly improved by critical reviews of Prof. Bao-zhen Hua (Northwest A&F University, Yangling, China) and two anonymous reviewers. We also thank Ning Sun, Xiang-Hua Liu, and Cai-Li Zhang (Henan University of Chinese Medicine) for the technical assistance in TEM.

Funding

This research was supported by the National Natural Science Foundation of China (grant nos. 31672346 and 31401989).

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Correspondence to Chao Yue.

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Ma, N., Zhang, YX. & Yue, C. The histology and ultrastructure of the salivary glands of Neopanorpa longiprocessa (Mecoptera: Panorpidae). Protoplasma 258, 59–69 (2021). https://doi.org/10.1007/s00709-020-01549-2

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