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Antennal Sensilla in Vespidae: A Comparison Between a Diurnal and a Nocturnal Polistinae Wasp

Part of: Micrographia Collection

Published online by Cambridge University Press:  22 April 2022

Cleber Ribeiro Júnior  and
José Eduardo Serrão Open the ORCID record for José Eduardo Serrão [Opens in a new window]
Cleber Ribeiro Júnior
Affiliation:
Department of General Biology, Federal University of Viçosa, Viçosa, MG, Brazil
José Eduardo Serrão*
Affiliation:
Department of General Biology, Federal University of Viçosa, Viçosa, MG, Brazil
*
*Corresponding author: José Eduardo Serrão, E-mail: [email protected]
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Abstract

Social wasps have a widespread Neotropical distribution and are important pollinators and biological control agents for pest insects. The foraging activity of wasps is influenced by biotic and abiotic factors that are detected by the antennal sensilla that vary according to species, sex, caste, and environmental conditions. This study compares the types and quantities of antennal sensilla with a scanning electron microscope between the nocturnal Apoica flavissima and the diurnal Polistes simillimus wasps. Six types of sensilla were found in the antennae of both species: placoid, coeloconic, basiconic-type 1, basiconic-type 2, trichoid-type 1, and trichoid-type 2. Sensilla chaetica were found only in the scape and pedicel of A. flavissima. In the nocturnal wasp, there are 19,132.27 ± 1,247.72 sensilla in the left and 17,746.46 ± 1,477.46 in the right antennae, whereas in the diurnal wasp 14,936.72 ± 1,271.69 in the left and 16,090.82 ± 1,345.3 in the right antennae. A. flavissima has a longer antennal length and number of sensilla than P. simillimus. The higher number of antennal sensilla in the nocturnal wasp is not linked with the antennal size. The association of antennal sensilla functions with ecological and behavioral factors of A. flavissima and P. simillimus are discussed.

Keywords

Apoica flavissimabehaviorinsectsPolistes simillimusscanning electron microscopysensory organs
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 28 , Issue 3 , June 2022 , pp. 880 - 893
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

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References

Altner, H & Prillinger, L (1980). Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Int Rev Cytol 67, 69–139.CrossRefGoogle Scholar
Andrade, FR & Prezoto, F (2001). Horários de atividade forrageadora e material coletado por Polistes ferreri Saussure, 1853 (Hymenoptera, Vespidae), nas diferentes fases de seu ciclo biológico. Rev Bras Zoocienc 3, 117–128.Google Scholar
Anfora, G, Frasnelli, E, Maccagnani, B, Rogers, LJ & Vallortigara, G (2010). Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a non-social (Osmia cornuta) species of bee. Behav Brain Res 206, 236–239.CrossRefGoogle Scholar
Anfora, G, Rigosi, E, Frasnelli, E, Ruga, V, Trona, F & Vallortigara, G (2011). Lateralization in the invertebrate brain: Left-right asymmetry of olfaction in bumble bee, Bombus terrestris. PLoS One 6, e18903.CrossRefGoogle ScholarPubMed
Basibuyuk, HH & Quicke, DLJ (1999). Gross morphology of multiporous plate sensilla in the Hymenoptera (Insecta). Zool Scr 28, 51–67.CrossRefGoogle Scholar
Bell, E & Sumner, S (2013). Ecology and Social Organisation of Wasps, eLS (Ed.). New Jersey : Wiley.CrossRefGoogle Scholar
Bleeker, MAK, Smid, HM, Van Aelst, AC, Van Loon, JJ & Vet, LEM (2004). Antennal sensilla of two parasitoid wasps: A comparative scanning electron microscopy study. Microsc Res Tech 63, 266–273.CrossRefGoogle ScholarPubMed
Carpenter, JM (2004). Synonymy of the genus Marimbonda Richards, 1978, with Leipomeles Moebius, 1856 (Hymenoptera: Vespidae: Polistinae), and a new key to the genera of paper wasps of the new world. Am Mus Novit 3456, 1–16.Google Scholar
Carpenter, JM & Marques, OM (2001). Contribuição ao Estudo dos Vespídeos do Brasil (Insecta, Hymenoptera, Vespoidea, Vespidae). Brazil: Universidade Federal da Bahia.Google Scholar
Couto, A, Mitra, A, Thiéry, D, Marion-Poll, F & Sandoz, JC (2017). Hornets have it: A conserved olfactory subsystem for social recognition in Hymenoptera? Front Neuroanat 11, 48.CrossRefGoogle ScholarPubMed
Di Palma, A, Pistillo, M, Griffo, R, Garonna, A & Germinara, GS (2019). Scanning electron microscopy of the antennal sensilla and their secretion analysis in adults of Aromia bungii (Faldermann, 1835) (Coleoptera: Cerambycidae). Insects 10, 88.CrossRefGoogle Scholar
Dweck, HKM (2009). Antennal sensory receptors of Pteromalus puparum female (Hymenoptera: Pteromalidae), a gregarious pupal endoparasitoid of Pieris rapae. Micron 40, 769–774.CrossRefGoogle Scholar
Dweck, HKM & Gadallah, NS (2008). Description of the antennal sensilla of Habrobracon hebetor. BioControl 53, 841–856.CrossRefGoogle Scholar
Elisei, T, Guimarães, DL, Ribeiro-Junior, C, Melo, AC, Grazinoli, DJ, Lopes, JFS & Prezoto, F (2008). Influence of environmental factors on the foraging activity of the paper wasp Polistes simillimus (Hymenoptera, Vespidae). Sociobiology 51, 219–130.Google Scholar
Euzébio, DE, Martins, GF & Fernandes-Salomão, TM (2013). Morphological and morphometric studies of the antennal sensilla from two populations of Atta robusta (Borgmeier 1939) (Hymenoptera: Formicidae). Braz J Biol 73, 663–668.CrossRefGoogle Scholar
Evans, HE & West-Eberhard, MJ (1970). The Wasps. Ann Arbor, USA: The University of Michigan Press.Google Scholar
Fialho, MCQ, Guss-Matiello, C, Zanuncio, JC, Campos, LAO & Serrão, JE (2014). A comparative study of the antennal sensilla in corbiculate bees. J Apicult Res 53, 392–403.CrossRefGoogle Scholar
Frasnelli, E, Anfora, G, Trona, F, Tessarolo, F & Vallortigara, G (2010a). Morpho-functional asymmetry of the olfactory receptors of the honeybee (Apis mellifera). Behav Brain Res 209, 221–225.CrossRefGoogle Scholar
Frasnelli, E & Vallortigara, G (2017). Distribution of antennal olfactory and non-olfactory sensilla in different species of bees. Symmetry 9, 139.CrossRefGoogle Scholar
Frasnelli, E, Vallortigara, G & Rogers, LJ (2010b). Response competition associated with right-left antennal asymmetries of new and old olfactory memory traces in honeybees. Behav Brain Res 209, 36–41.CrossRefGoogle Scholar
Frasnelli, E, Vallortigara, G & Rogers, LJ (2012). Left–right asymmetries of behaviour and nervous system in invertebrates. Neurosci Biobehav Rev 36, 1273–1291.CrossRefGoogle ScholarPubMed
Freelance, CB, Majoe, M, Tierney, SM & Elgar, MA (2019). Antennal asymmetry is not associated with social behaviour in Australian Hymenoptera. Austral Ent 58, 589–594.CrossRefGoogle Scholar
Fu, BX, Bellis, GA, Hong, J, Wang, JR, Wu, Q, Tang, QY, Cheng, JA & Zhu, ZR (2012). Morphology, distribution, and abundance of antennal sensilla of male and female macropterous and brachypterous small brown planthopper, Laodelphax striatellus (Fallén) (Hemiptera: Delphacidae). Microsc Res Tech 75, 1492–1512.CrossRefGoogle Scholar
Gao, Y, Luo, LZ & Hammond, A (2007). Antennal morphology, structure and sensilla distribution in Microplitis pallidipes (Hymenoptera: Braconidae). Micron 38, 684–693.CrossRefGoogle Scholar
Gaul, AT (1952). The awakening and diurnal flight activities of vespine wasps. Proc R Entomol Soc Lond Ser A 27, 33–38.Google Scholar
Giannakakis, A & Fletcher, BS (1985). Morphology and distribution of antennal sensilla of Dacus tryoni (Froggatt) (Diptera, Tephritidae). J Austral Entomol Soc 24, 31–35.CrossRefGoogle Scholar
Giannotti, E, Prezoto, F & Machado, LL (1995). Foraging activity of Polistes lanio lanio (Fabr.) (Hymenoptera, Vespidae). An Soc Ent Brasil 24, 455–463.CrossRefGoogle Scholar
Gillott, C (2005). Entomology, 3rd ed. Heidelberg, Netherlands: Springer.Google Scholar
Hallberg, E & Hansson, BS (1999). Arthropod sensilla: Morphology and phylogenetic consideration. Microsc Res Tech 47, 428–439.3.0.CO;2-P>CrossRefGoogle Scholar
Hashimoto, Y (1990). Unique features of sensilla on the antennae of Formicidae (Hymenoptera). Appl Ent Zool 25, 491–501.CrossRefGoogle Scholar
Herzner, G, Schmitt, T, Linsenmair, KE & Strohm, E (2003). Flagellar sensilla in male and female European beewolves, Philanthus triangulum F. (Hymenoptera: Sphecidae). Ent Fenn 14, 237–247.Google Scholar
Huang, ZY, Liu, JY, Zhang, YJ, Guo, CH, Yang, ZD, Lu, W & Zheng, XL (2017). Scanning electron microscopy of antennal sensilla of Megastigmus sichuanensis Doganlar et Zheng (Hymenoptera: Torymidae). Zool Anz 271, 25–32.CrossRefGoogle Scholar
Hunger, T & Steinbrecht, RA (1998). Functional morphology of a doublewalled multiporous olfactory sensillum: The sensillum coeloconicum of Bombyx mori (Insecta, Lepidoptera). Tiss Cell 30, 14–29.CrossRefGoogle Scholar
Hunt, JH, Jeanne, RL & Keeping, MB (1995). Observations on Apoica pallens, a nocturnal Neotropical social wasp (Hymenoptera: Vespidae, Polistinae, Epiponini). Ins Soc 42, 223–236.CrossRefGoogle Scholar
Isidoro, N, Bin, F, Colazza, S & Vinson, SB (1996). Morphology of antennal gustatory sensilla and glands in some parasitoid hymenoptera with hypothesis on their role in sex and host recognition. J Hymenopt Res 5, 206–239.Google Scholar
Jacques, GC, Oliveira, DC, Souza, MM & Silveira, LC (2019). The use of Polistes versicolor (Olivier, 1971) in the control of Ascia monuste orseis (Godart, 1819) in kale cultivation. Agrogeoambiental 11, 96–106.Google Scholar
Jorge, A, Polidori, C & Nieves-Aldrey, JL (2019). Antennal sensilla in male gall-wasps (Hymenoptera: Cynipidae) and insights on the evolution of sexual dimorphism in cynipoid sensory equipment. Zool Anz 283, 213–230.CrossRefGoogle Scholar
Keil, TA (1999). Morphology and development of the peripheral olfactory organs. In Insect Olfaction, Hansson, B (Ed.), pp. 6–44. Berlin: Springer.Google Scholar
Keil, TA & Steinbrecht, RA (1984). Mechanosensitive and olfactory sensilla of insects. In Insect Ultrastructure II, King, RC & Akai, H (Eds.), pp. 477–516. New York: Plenum Press.CrossRefGoogle Scholar
Khodairy, MM & Awad, AA (2013). A study on the sensory structure, in relation to some behavioral ecology of the oriental hornet (Vespa orientalis L.) (Hymenoptera: Vespidae). Life Sci J 10, 1207–1216.Google Scholar
Kleineidam, C, Romani, R, Tautz, J & Isidoro, N (2000). Ultrastructure and physiology of the CO2 sensillum ampullaceumin the leaf-cutting ant atta sexdens. Arthrop Struct Dev 29, 43–55.CrossRefGoogle ScholarPubMed
Kleineidam, C & Tautz, J (1996). Perception of carbon dioxide and other “air-condition” parameters in the leaf cutting ant atta cephalotes. Naturwissenschaften 83, 566–568.Google Scholar
Letzkus, P, Ribi, WA, Wood, JT, Zhu, H, Zhang, SW & Srinivasan, MV (2006). Lateralization of olfaction in the honeybee Apis mellifera. Curr Biol 16, 1471–1476.CrossRefGoogle ScholarPubMed
Liang, QF, Khan, MAZ, Cui, J & Liu, TX (2016). Antennal sensilla ultrastructure in Aphidius gifuensis (Hymenoptera: Braconidae), A parasitoid of Myzus persicae (Hemiptera: Aphididae). Egypt J Bioll Pest Cont 26, 509–514.Google Scholar
Lima, MA & Prezoto, F (2003). Foraging activity rhythm in the Neotropical swarm-founding wasp Polybia platycephala sylvestris Richards, 1978 (Hymenoptera: Vespidae) in different seasons of the year. Sociobiology 42, 745–752.Google Scholar
Liu, Z, Hu, T, Guo, HW, Liang, XF & Cheng, YQ (2021). Ultrastructure of the olfactory sensilla across the antennae and maxillary palps of Bactrocera dorsalis (Diptera: Tephritidae). Insects 12, 289.CrossRefGoogle Scholar
Marques-Silva, S, Matiello-Guss, C, Delabie, JHC, Mariano, CSF, Zanuncio, JC & Serrão, JE (2006). Sensilla and secretory glands in the antennae of a primitive ant: Dinoponera lucida (Formicidae: Ponerinae). Microsc Res Tech 69, 885–890.CrossRefGoogle Scholar
Mciver, SB (1975). Structure of cuticular mechanoreceptors of arthropods. Annu Rev Ent 20, 381–397.CrossRefGoogle ScholarPubMed
Month-Juris, E, Ravaiano, S, Lopes, DM, Fernandes Salomao, TM & Martins, GF (2020). Morphological assessment of the sensilla of the antennal flagellum in different castes of the stingless bee Tetragonisca fiebrigi. J Zool 310, 110–125.CrossRefGoogle Scholar
Nakanishi, A, Nishino, H, Watanabe, H, Yokohari, F & Nishikawa, M (2009). Sex-specific antennal sensory system in the ant camponotus japonicus: Structure and distribution of sensilla on the flagellum. Cell Tiss Res 338, 79–97.CrossRefGoogle ScholarPubMed
Nascimento, FS & Tannure-Nascimento, IC (2005). Foraging patterns in a nocturnal swarmfounding wasp, Apoica flavissima van der Vecht (Hymenoptera: Vespidae). Neotrop Ent 34, 177–181.Google Scholar
Nascimento, MA, Fernandes-Salomão, TM & Martins, GF (2013). Estudo comparativo das sensilas antenais de operárias de Melipona scutellaris Latreille (Hymenoptera: Apidae) de diferentes altitudes. EntomoBrasilis 6, 64–67.CrossRefGoogle Scholar
Nowińska, A & Brożek, J (2017). Morphological study of the antennal sensilla in gerromorpha (Insecta: Hemiptera: Heteroptera). Zoomorphology 136, 327–347.CrossRefGoogle Scholar
Ochieng, SA, Park, KC, Zhu, JW & Baker, TC (2000). Functional morphology of antennal chemoreceptors of the parasitoid Microplitis croceipes (Hymenoptera: Braconidae). Arthrop Struc Dev 29, 231–240.CrossRefGoogle Scholar
Onagloba, EO & Fadamiro, HY (2008). Scanning electron microscopy studies of anennal sensilla of pteromalus cerealellae (Hymenoptera: Pteromalidae). Micron 39, 526–535.Google Scholar
Paula, LC, Andrade, FR & Prezoto, F (2003). Foraging behavior in the Neotropical swarm-founding wasp Parachartergus fraternus (Hymenoptera: Vespidae: Polistinae: Epiponini) during different phases of the biological cycle. Sociobiology 42, 735–744.Google Scholar
Pickett, KM & Wenzel, JW (2007). Revision and cladistic analysis of the nocturnal social wasp genus, Apoica Lepeletier (Hymenoptera: Vespidae: Polistinae: Epiponini). Am Mus Novit 3562, 1–30.CrossRefGoogle Scholar
Polidori, C, Jorge, A & Ornosa, C (2020). Antennal morphology and sensillar equipment vary with pollen diet specialization in andrena bees. Arthrop Struct Dev 57, 100950.CrossRefGoogle ScholarPubMed
Prezoto, F, Giannotti, E & Machado, LL (1994). Atividade forrageadora e material coletado pela vespa social Polistes simillimus Zikán, 1951 (Hymenoptera: Vespidae). Insecta 3, 11–19.Google Scholar
Prezoto, F, Maciel, TT, Detoni, M, Mayorquin, AZ & Barbosa, BC (2019). Pest control potential of social wasps in small farms and urban gardens. Insects 10, 192.CrossRefGoogle ScholarPubMed
Ravaiano, S, Ferreira, R, Campos, LAO & Martins, GF (2014). The antennal sensilla of Melipona quadrifasciata (Hymenoptera: Apidae: Meliponini): a study of different sexes and castes. Naturwissenschaften 101, 603–611.CrossRefGoogle ScholarPubMed
Reeve, HK (1991). Polistes. In The Social Biology of Wasps, Ross, KG & Matthews, RW (Eds.), pp. 99–148. New York: Cornell University Press.Google Scholar
Renthal, R, Velasquez, D, Olmos, D, Hampton, J & Wergin, W (2003). Structure and distribution of antennal sensilla of the red imported fire ant. Micron 34, 405–413.CrossRefGoogle ScholarPubMed
Resende, JJ, Santos, GMM, Bichara-Filho, CC & Gimenes, M (2001). Atividade diária de busca de recursos pela vespa social Polybia occidentalis occidentalis (Olivier, 1791) (Hymenoptera, Vespidae). Rev Bras Zoocienc 3, 105–115.Google Scholar
Ribeiro-Junior, C, Guimarães, DL, Elisei, T & Prezoto, F (2006). Foraging activity rhythm of the neotropical swarm-founding wasp Protopolybia exigua (Hymenoptera, Vespidae, Epiponini) in different seasons of the year. Sociobiology 47, 115–123.Google Scholar
Richards, OW (1978). The Social Wasps of the Americas Excluding the Vespinae. London: British Museum Press.Google Scholar
Richter, MR (2000). Social wasp (Hymenoptera: Vespidae) foraging behavior. Ann Rev Ent 45, 121–150.CrossRefGoogle ScholarPubMed
Rigosi, E, Frasnelli, E, Vinegoni, C, Antolini, R, Anfora, G, Vallortigara, G & Haase, A (2011). Searching for anatomical correlates of olfactory lateralization in the honeybee antennal lobes: A morphological and behavioural study. Behav Brain Res 221, 290–294.CrossRefGoogle ScholarPubMed
Robertson, DJ & Gandhi, KJK (2018). Morphology of male and female antennal sensilla of Ibalia leucospoides ensiger (Hymenoptera: Ibaliidae). Ann Ent Soc Am 111, 13–20.CrossRefGoogle Scholar
Rogers, LJ & Vallortigara, G (2008). From antenna to antenna: Lateral shift of olfactory memory in honeybees. PLoS One 3, e2340.CrossRefGoogle ScholarPubMed
Sawsan, MA & Sawires, SG (2015). Comparative studies on the antennal sense organs of queen and worker honey bees, Apis mellifera L. Egypt Acad J Biol Sci 8, 65–75.Google Scholar
Sevarika, M, Rossi Stacconi, M & Romani, R (2021). Fine morphology of antennal and ovipositor sensory structures of the gall chestnut wasp, Dryocosmus kuriphilus. Insects 12, 231.CrossRefGoogle ScholarPubMed
Shields, DC (2010). High resolution ultrastructural investigation of insect sensory organs using field emission scanning electron microscopy. In Microscopy: Science, Technology, Applications and Education, Méndez-Vilas, A & Díaz, J (Eds.), pp. 321–328. Badajoz, Spain: Formatex.Google Scholar
Silva, IM, Pereira, KD, Spranghers, T, Zanuncio, JC & Serrão, JE (2016). Antennal sensilla and sexual dimorphism of the parasitoid Trichospilus pupivorus (Hymenoptera: Eulophidae). Microsc Microanal 22, 913–921.CrossRefGoogle Scholar
Silveira, OT, Andena, SR, Somavilla, A & Carpenter, JM (2021). Phylogeny and classification of the neotropical social wasps. In Neotropical Social Wasps, Prezoto, F, Nascimento, FS, Barbosa, BC & Somavilla, A (Eds.), pp. 267–291. Cham, Switzerland: Springer.CrossRefGoogle Scholar
Spaethe, J, Brockmann, A, Halbig, C & Tautz, J (2007). Size determines antennal sensitivity and behavioral threshold to odors in bumblebee workers. Naturwissenschaften 94, 733–739.CrossRefGoogle ScholarPubMed
Stefanini, M, De Martino, C & Zamboni, L (1967). Fixation of ejaculated spermatozoa for electron microscopy. Nature 216, 173–174.CrossRefGoogle ScholarPubMed
Suwannapong, G, Niophrom, J & Benbow, ME (2012). Ultramorphology of antennal sensilla in Thai single open nest honeybees (Hymenoptera: Apidae). J Trop Asian Ent 1, 1–12.Google Scholar
West-Eberhard, MJ (1982). The nature evolution of swarming in tropical social wasps. In Social Insects in the Tropics, Vol. 1, Jaisson, P (Ed.), pp. 97–128. Paris, France: Université Paris-Nord.Google Scholar
Wilson, EO (1971). The Insect Societies. Cambridge, USA: The Belknap Press Harvard University.Google Scholar
Xi, YQ, Yin, XM, Zhu, CD, Guerrieri, E & Zhang, YZ (2011). Scanning electron microscopy studies of antennal sensilla of Ooencyrtus phongi (Hymenoptera: Encyrtidae). Microsc Res Tech 74, 936–945.CrossRefGoogle Scholar
Yang, P, Li, ZB, Yang, DR, Peng, YQ & Kjellberg, F (2018). Comparison of the antennal sensilla of females of four fig-wasps associated with Ficus auriculata. Acta Oecol 90, 99–108.CrossRefGoogle Scholar
Yang, SZ, Yang, MH, Xu, Y & Zhang, JT (2021). Antennal sensilla of Chrysis shanghalensis (Hymenoptera: Chrysididae), a larval ectoparasite of Monema flavescens (Lepidoptera: Limacodidae). J Entomol Sci 56, 1–11.CrossRefGoogle Scholar
Zhou, CX, Sun, X, Mi, F, Chen, JY & Wang, MQ (2015). Antennal sensilla in the parasitoid Sclerodermus sp (Hymenoptera: Bethylidae). J Ins Sci 15, 36.CrossRefGoogle Scholar
Zhou, H, Wu, WJ, Zhang, F & Fu, YG (2013). Scanning electron microscopy studies of the antennal sensilla of Metaphycus paasaissetiae Zhang & Huang (Hymenoptera: Encyrtidae). Neotrop Ent 42, 278–287.CrossRefGoogle Scholar
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