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Sensory Receptors Associated with the Labial Tip and Precibarium of Philaenus spumarius L. (Hemiptera: Aphrophoride)

Published online by Cambridge University Press:  14 November 2019

Emanuele Ranieri
Affiliation:
Department of Agricultural, Food and Environmental Sciences, Marche Polytechnic University, Ancona60131, Italy
Sara Ruschioni
Affiliation:
Department of Agricultural, Food and Environmental Sciences, Marche Polytechnic University, Ancona60131, Italy
Paola Riolo*
Affiliation:
Department of Agricultural, Food and Environmental Sciences, Marche Polytechnic University, Ancona60131, Italy
Nunzio Isidoro
Affiliation:
Department of Agricultural, Food and Environmental Sciences, Marche Polytechnic University, Ancona60131, Italy
Roberto Romani
Affiliation:
Department of Agricultural, Food and Environmental Sciences, University of Perugia, Perugia06121, Italy
*
*Author for correspondence: Paola Riolo, E-mail: p.riolo@univpm.it
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Abstract

The meadow spittlebug, Philaenus spumarius (Linnaeus) (Hemiptera: Aphrophoridae), is an important vector for the xylem-limited bacterium Xylella fastidiosa (Wells, Raju, Hung, Weisburg, Mandelco-Paul, and Brenner), which is associated with olive quick decline syndrome in southern Italy. The mouthparts of Hemiptera have important roles in host plant selection, feeding behavior and for vectoring pathogens that cause plant diseases. In this study, the functional morphology of the sensory structures located on the labium tip and precibarium of P. spumarius was investigated using scanning and transmission electron microscopy. The labium tip is composed of two symmetrical sensory complexes, each with five different types of sensilla: aporous sensilla trichodea type 1 and 2; uniporous sensilla chaetica type 1 and 2; and multiporous sensilla basiconica. The precibarium of P. spumarius has two kinds of sensory structures: bulbous sensilla and papillae sensilla. In particular, two groups of sensilla are located on the epipharynx: a distal group that consists of ten papillae sensilla and a proximal group composed of six papillae sensilla and two bulbous sensilla, while the hypopharynx has only two papillae sensilla. The involvement of these sensory structures in the context of feeding behavior and pathogen transmission is discussed.

Type
Micrographia
Copyright
Copyright © Microscopy Society of America 2019

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Footnotes

a

These authors contributed equally to this manuscript.

References

Altner, H & Prillinger, L (1980). Ultrastructure of invertebrate chemo-, thermo-, and hygroreceptors and its functional significance. Int Rev Cytol 67, 69139.CrossRefGoogle Scholar
Altner, H, Sass, H & Altner, I (1977). Relationships between structure and function of antennal chemo-, hygro-, and thermoreceptive sensilla in Periplaneta americana. Cell Tissue Res 176, 389405.CrossRefGoogle Scholar
Backus, EA (1985). Anatomical and sensory mechanisms of leafhopper and planthopper feeding behavior. In The Leafhoppers and Planthoppers, Nault, LR & Rodriguez, JG (Eds.), pp. 163194. New York: Wiley.Google Scholar
Backus, E (1988). Sensory systems and behaviours which mediate hemipteran plant feeding: A taxonomic overview. J Insect Physiol 34(3), 151165.CrossRefGoogle Scholar
Backus, EA & McLean, D (1985). Behavioral evidence that the precibarial sensilla of leafhoppers are chemosensory and function in host discrimination. Entomol Exp Appl 37, 219228.CrossRefGoogle Scholar
Backus, EA & McLean, DL (1982). The sensory systems and feeding behavior of leafhoppers. I. The aster leafhopper, Macrosteles fascifrons Stal (Homoptera, Cicadellidae). J Morphol 172, 361379.CrossRefGoogle Scholar
Backus, EA & McLean, DL (1983). The sensory systems and feeding behavior of leafhoppers. II. A comparison of the sensillar morphologies of several species (Homoptera: Cicadellidae). J Morphol 176, 314.10.1002/jmor.1051760102CrossRefGoogle Scholar
Backus, EA & Morgan, DJW (2011). Spatiotemporal colonization of Xylella fastidiosa in its vector supports the role of egestion in the inoculation mechanism of foregut-borne plant pathogens. Phytopathology 101, 912922.CrossRefGoogle ScholarPubMed
Bernays, EA & Chapman, RF (2007). Host-Plant Selection by Phytophagous Insects, vol. 2. Berlin: Springer Science & Business Media.Google Scholar
Bourgoin, T & Deiss, V (1994). Sensory plate organs of the antenna in the Meenoplidae-Kinnaridae group (Hemiptera: Fulgoromorpha). Int J Insect Morphol Embryol 23, 159168.10.1016/0020-7322(94)90008-6CrossRefGoogle Scholar
Brlansky, RH, Timmer, LW, French, WJ & McCoy, RE (1983). Colonization of the sharpshooter vector, Oncometopia nigricans and Homalodisca coagulata by xylem-limited bacteria. Phytopathology 73(4), 530535.10.1094/Phyto-73-530CrossRefGoogle Scholar
Brozek, J & Bourgoin, T (2013). Morphology and distribution of the external labial sensilla in Fulgoromorpha (Insecta: Hemiptera). Zoomorphology 132, 3365.CrossRefGoogle Scholar
Bruno, D, Grossi, G, Salvia, R, Scala, A, Farina, D, Grimaldi, A, Zhou, JJ, Bufo, SA, Vogel, H, Grosse-Wilde, E, Hansson, BS & Falabella, P (2018). Sensilla morphology and complex expression pattern of odorant binding proteins in the vetch aphid Megoura viciae (Hemiptera: Aphididae). Front Physiol 9, 777.CrossRefGoogle Scholar
Campbell, CAM, Pettersson, J, Pickett, JA, Wadhams, LJ & Woodcock, CM (1993). Spring migration of damson-hop aphid, Phorodon humuli (Homoptera, Aphididae), and summer host plant-derived semiochemicals released on feeding. J Chem Ecol 19, 15691576.CrossRefGoogle Scholar
Cariddi, C, Saponari, M, Boscia, D, De Stradis, A, Loconsole, G, Nigro, F, Porcelli, F, Potere, O & Martelli, GP (2014). Isolation of a Xylella fastidiosa strain infecting olive and oleander in Apulia, Italy. J Plant Pathol 96(2), 425429.Google Scholar
Cornara, D, Cavalieri, V, Dongiovanni, C, Altamura, G, Palmisano, F, Bosco, D, Porcelli, F, Almeida, RPP & Saponari, M (2017). Transmission of Xylella fastidiosa by naturally infected Philaenus spumarius (Hemiptera, Aphrophoridae) to different host plants. J Appl Entomol 141(1–2), 8087.CrossRefGoogle Scholar
Cornara, D, Sicard, A, Zeilinger, AR, Porcelli, F, Purcell, AH & Almeida, RPP (2016). Transmission of Xylella fastidiosa to grapevine by the meadow spittlebug. Phytopathology 106(11), 12851290.CrossRefGoogle ScholarPubMed
Dai, W, Pan, L, Lu, Y, Jin, L & Zhang, C (2014). External morphology of the mouthparts of the whitebacked planthopper Sogatella furcifera (Hemiptera: Delphacidae), with special reference to the sensilla. Micron 56, 816.CrossRefGoogle Scholar
de Jong, Y, Verbeek, M, Michelsen, V, Per de Place, B, Los, B, Steeman, F, Bailly, N, Basire, C, Chylarecki, P, Stloukal, E, Hagedorn, G, Wetzel, FT, Glöckler, F, Kroupa, A, Korb, G, Hoffmann, A, Häuser, C, Kohlbecker, A, Müller, A, Güntsch, A, Stoev, P & Penev, L (2014). Fauna Europaea – All European animal species on the web. Biodivers Data J 2, e4034.CrossRefGoogle Scholar
Dethier, VG (1982). Mechanism of host-plant recognition. Entomol Exp Appl 31(1), 4956.CrossRefGoogle Scholar
Dippel, S, Kollmann, M, Oberhofer, G, Montino, A, Knoll, C, Krala, M, Rexer, KH, Frank, S, Kumpf, R, Schachtner, J & Wimmer, EA (2016). Morphological and transcriptomic analysis of a beetle chemosensory system reveals a gnathal olfactory center. BMC Biol 14, 90.10.1186/s12915-016-0304-zCrossRefGoogle ScholarPubMed
EFSA (2015). Panel on Plant Health (PLH): Scientific opinion on the risks to plant health posed by Xylella fastidiosa in the EU territory, with the identification and evaluation of risk reduction options. EFSA J 13(262), 39894251.10.2903/j.efsa.2015.3989CrossRefGoogle Scholar
Fereres, A & Moreno, A (2009). Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res 141(2), 158168.CrossRefGoogle ScholarPubMed
Forbes, AR (1969). The stylets of the green peach aphid, Myzus persicae (Homoptera: Aphididae). Can Entomol 101, 3141.CrossRefGoogle Scholar
Foster, S, Goodman, LJ & Duckett, JG (1983). Ultrastructure of sensory receptors on the labium of the rice brown planthopper. Cell Tissue Res 230(2), 353366.CrossRefGoogle ScholarPubMed
Garzo, E, Bonani, JP, Lopes, JRS & Fereres, A (2012). Morphological description of the mouthparts of the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae). Arthropod Struct Dev 41, 7986.CrossRefGoogle Scholar
Germinara, GS, Ganassi, S, Pistillo, MO, Di Domenico, C, De Cristofaro, A & Di Palma, AM (2017). Antennal olfactory responses of adult meadow spittlebug, Philaenus spumarius, to volatile organic compounds (VOCs). PLoS One 12(12), e0190454.CrossRefGoogle Scholar
Haverkamp, A, Yon, F, Keesey, IW, Mißbach, C, Koenig, C, Hansson, BS, Baldwin, IT, Knaden, M & Kessler, D (2016). Hawkmoths evaluate scenting flowers with the tip of their proboscis. Elife 5, e15039.CrossRefGoogle ScholarPubMed
Hill, BL & Purcell, PH (1995). Acquisition and retention of Xylella fastidiosa by an efficient vector, Graphocephala atropunctata. Phytopathology 85(2), 209212.10.1094/Phyto-85-209CrossRefGoogle Scholar
Hoy, CW, Zhou, X, Nault, LR, Miller, SA & Styer, J (1999). Host plant, phytoplasma, and reproductive status effects on flight behavior of aster leafhopper (Homoptera: Cicadellidae). Ann Entomol Soc Am 92(4), 523528.CrossRefGoogle Scholar
Jackson, BC, Blua, MJ & Bextine, B (2008). Impact of duration versus frequency of probing by Homalodisca vitripennis (Hemiptera: Cicadellidae) on inoculation of Xylella fastidiosa. J Econ Entomol 101(4), 11221126.CrossRefGoogle ScholarPubMed
Keil, TA (1997). Functional morphology of insect mechanoreceptors. Microsc Res Tech 39, 506531.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Kent, KS & Griffin, LM (1990). Sensory organs of the thoracic legs of the moth Manduca sexta. Cell Tissue Res 259(2), 209223.CrossRefGoogle ScholarPubMed
Krugner, R, Sisterson, MS & Lin, H (2012). Effects of gender, origin, and age on transmission of Xylella fastidiosa to grapevines by Homalodisca vitripennis (Hemiptera: Cicadellidae). Ann Entomol Soc Am 105(2), 280286.CrossRefGoogle Scholar
Landi, L, Riolo, P, Murolo, S, Romanazzi, G, Nardi, S & Isidoro, N (2015). Genetic variability of stolbur phytoplasma in Hyalesthes obsoletus (Hemiptera: Cixiidae) and its main host plants in vineyard agroecosystems. J Econ Entomol 108(4), 15061515.CrossRefGoogle ScholarPubMed
Leopold, RA, Freeman, TP, Buckner, JS & Nelson, DR (2003). Mouthpart morphology and stylet penetration of host plants by the glassy-winged sharpshooter, Homalodisca coagulata (Homoptera: Cicadellidae). Arthropod Struct Dev 32, 189199.CrossRefGoogle Scholar
Le Ru, B, Renard, S, Allo, MR, Le Lannic, J & Rolland, JP (1995). Ultrastructure of sensory receptors on the labium of the cassava mealybug, Phenacoccus manihoti Matile Ferrero. Entomol Exp Appl 77, 3136.Google Scholar
Lewis, CT & Marshall, AT (1970). The ultrastructure of the sensory plaque organs of the antennae the Chinese lantern fly, Pyrops candelaria L. (Homoptera, Fulgoridae). Tissue Cell 2, 375385.CrossRefGoogle Scholar
Liang, X, Zhang, C, Li, Z, Xu, L & Dai, W (2013). Fine structure and sensory apparatus of the mouthparts of the pear psyllid, Cacopsylla chinensis (Yang et Li) (Hemiptera: Psyllidae). Arthropod Struct Dev 42, 495506.CrossRefGoogle Scholar
Malone, M, Watson, R & Pritchard, J (1999). The spittlebug Philaenus spumarius feeds from mature xylem at the full hydraulic tension of the transpiration stream. New Phytol 143(2), 261271.CrossRefGoogle Scholar
Mclean, D & Kinsey, MG (1984). The precibarial valve and its role in the feeding behavior of the pea aphid, Acyrthosiphon pisum. Bull ESA 30(2), 2631.Google Scholar
Minuz, RL, Isidoro, N, Casavecchia, S, Burgio, G & Riolo, P (2013). Sex-dispersal differences of four phloem-feeding vectors and their relationship to wild-plant abundance in vineyard agroecosystems. J Econ Entomol 106(6), 22962309.CrossRefGoogle ScholarPubMed
Mitchell, PL (2004). Heteroptera as vectors of plant pathogens. Neo Trop Entomo 33(5), 519545.CrossRefGoogle Scholar
Nielson, MW (1968). The Leafhopper Vectors of Phytopathogenic Viruses (Homoptera, Cicadellidae): Taxonomy, Biology, and Virus Transmission (No. 1382). Washington: US Department of Agriculture.Google Scholar
Nottingham, SF, Hardie, J, Dawson, GW, Hick, AJ, Pickett, JA, Wadhams, LJ & Woodcock, CM (1991). Behavioral and electrophysiological response of aphids to host and nonhost plant volatiles. J Chem Ecol 17(6), 12311242.CrossRefGoogle Scholar
Park, KC & Hardie, J (2004). Electrophysiological characterisation of olfactory sensilla in the black bean aphid, Aphis fabae. J Insect Physiol 50(7), 647655.CrossRefGoogle ScholarPubMed
Pompon, J, Quiring, D, Goyer, C, Giordanengo, P & Pelletier, Y (2011). A phloem-sap feeder mixes phloem and xylem sap to regulate osmotic potential. J Insect Physiol 57, 13171322.CrossRefGoogle ScholarPubMed
Ranieri, E, Ruschioni, S, Riolo, P, Isidoro, N & Romani, R (2016). Fine structure of antennal sensilla of the spittlebug Philaenus spumarius L. (Insecta: Hemiptera: Aphrophoridae). I. Chemoreceptors and thermo-/hygroreceptors. Arthropod Struct Dev 45, 432439.CrossRefGoogle ScholarPubMed
Redak, RA, Purcell, AH, Lopes, JRS, Blua, MJ, Mizell, RF & Andersen, PC (2004). The biology of xylem fluid-feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annu Rev Entomol 49, 243270.CrossRefGoogle ScholarPubMed
Riolo, P, Minuz, RL, Anfora, G, Stacconi, MVR, Carlin, S, Isidoro, N & Romani, R (2012). Perception of host plant volatiles in Hyalesthes obsoletus: behavior, morphology, and electrophysiology. J Chem Ecol 38, 10171030.CrossRefGoogle ScholarPubMed
Romani, R, Salerno, G, Frati, F, Conti, E, Isidoro, N & Bin, F (2005). Oviposition behaviour in Lygus rugulipennis: A morpho-functional study. Ent Exp Appl 115(1), 1725.CrossRefGoogle Scholar
Romani, R, Stacconi, MVR, Riolo, P & Isidoro, N (2009). The sensory structures of the antennal flagellum in Hyalesthes obsoletus (Hemiptera: Fulgoromorpha: Cixiidae): A functional reduction? Arthropod Struct Dev 38, 473483.CrossRefGoogle ScholarPubMed
Rosell, RC, Lichty, JE & Brown, JK (1995). Ultrastructure of the mouthparts of adult sweet potato whitefly, Bemisia tabaci Gennadius (Homoptera: Aleyrodidae). Int J Insect Morphol Embryol 24, 97306.CrossRefGoogle Scholar
Ruschioni, S, Ranieri, E, Riolo, P, Romani, R, Almeida, RPP & Isidoro, N (2019). Functional anatomy of the precibarial valve in Philaenus spumarius (L.). PLoS One 14(2), e0213318.CrossRefGoogle Scholar
Ruschioni, S, Riolo, P, Verdolini, E, Peri, E, Guarino, S, Colazza, S, Romani, R & Isidoro, N (2015). Fine structure of antennal sensilla of Paysandisia archon and electrophysiological responses to volatile compounds associated with host palms. PLoS One 10(4), e0124607.CrossRefGoogle ScholarPubMed
Ruschioni, S, Romani, R, Riolo, P & Isidoro, N (2012). Morphology and distribution of antennal multiporous gustatory sensilla related to host recognition in some Trichogramma spp. Bull Insectol 65, 171176.Google Scholar
Saponari, M, Loconsole, G, Cornara, D, Yokomi, RK, Stradis, ADE, Boscia, D, Bosco, D, Martelli, GP, Krugner, R & Porcelli, F (2014). Infectivity and transmission of Xylella fastidiosa by Philaenus spumarius (Hemiptera: Aphrophoridae) in Apulia, Italy. J Econ Entomol 107, 14.CrossRefGoogle ScholarPubMed
Schoonhoven, LM, Van Loon, B, van Loon, JJ & Dicke, M (2005). Insect-Plant Biology. Oxford: Oxford University Press on Demand.Google Scholar
Thorsteinson, AJ (1960). Host selection in phytophagous insects. Annu Rev Entomol 5(1), 193218.10.1146/annurev.en.05.010160.001205CrossRefGoogle Scholar
Tjallingii, WF (1995). Regulation of phloem sap feeding by aphids. In Regulatory Mechanisms in Insect Feeding, Chapman, RF & De Boer, G (Eds.), pp. 190209. Boston: Springer.CrossRefGoogle Scholar
Tjallingii, WF & Mayoral, A (1992). Criteria for host-plant acceptance by aphids. Proceedings of the 8th International Symposium on Insect-Plant Relationships, Menken, SBJ, Visser, JH & Harrewijn, P (Eds.), pp. 280282. Dordrecht: Springer.CrossRefGoogle Scholar
Ullman, DE & McLean, DL (1986). Anterior alimentary canal of the pear Psylla, Psylla pyricola Foerster (Homoptera, Psyllidae). J Morphol 189, 8998.CrossRefGoogle Scholar
Walker, GP & Gordh, G (1989). The occurrence of apical labial sensilla in the Aleyrodidae and evidence for a contact chemosensory function. Entomol Exp Appl 51, 215224.CrossRefGoogle Scholar
Wang, T, Pan, L, Zhang, Y & Dai, W (2015). Morphology of the mouthparts of the spittlebug Philagra albinotata Uhler (Hemiptera: Cercopoidea: Aphrophoridae). Arthropod Struct Dev 44, 121130.CrossRefGoogle Scholar
Weintraub, PG & Beanland, L (2006). Insect vectors of phytoplasmas. Annu Rev Entomol 51, 91111.CrossRefGoogle ScholarPubMed
Zacharuk, RY (1980). Ultrastructure and function of insect chemosensilla. Ann Rev Entomol 25, 2747.CrossRefGoogle Scholar
Zhao, L, Dai, W, Zhang, C & Zhang, Y (2010). Morphological characterization of the mouthparts of the vector leafhopper Psammotettix striatus (L.) (Hemiptera: Cicadellidae). Micron 41, 754759.CrossRefGoogle Scholar