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Philaenus spumarius: when an old acquaintance becomes a new threat to European agriculture

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Abstract

The unique color pattern polymorphism and the foamy nymphal case of the meadow spittlebug Philaenus spumarius have attracted the attention of scientists for centuries. Nevertheless, since this species has never been considered a major threat to agriculture, biological, ecological and ethological data are missing and rather scattered. To date this knowledge has become of paramount importance, in view of the discovery of P. spumarius main role in the transmission of the bacterium Xylella fastidiosa in Italy, and possibly in other European countries. The aim of this review is to provide a state of the art about this species, with particular focus on those elements that could help developing environmental friendly and sustainable control programs to prevent transmission of X. fastidiosa. Moreover, recent findings on the role of the meadow spittlebug as vector of the fastidious bacterium within the first reported European bacterium outbreak in Apulia (South Italy) will be discussed.

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Fig. 1

Photos by A. Fereres and D. Cornara

Fig. 2

Figure elaborated from Cornara et al. (2016b)

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References

  • Almeida RP, Nunney L (2015) How do plant diseases caused by Xylella fastidiosa emerge? Plant Dis 99:1457–1467

    Article  Google Scholar 

  • Almeida RPP, Purcell AH (2003) Homalodisca coagulata (Hemiptera, Cicadellidae) transmission of Xylella fastidiosa to almond. Plant Dis 87:1255–1259

    Article  Google Scholar 

  • Almeida RP, Purcell AH (2006) Patterns of Xylella fastidiosa colonization on the precibarium of sharpshooter vectors relative to transmission to plants. Ann Entomol Soc Am 99:884–890

    Article  Google Scholar 

  • Almeida RP, Blua MJ, Lopes JR, Purcell AH (2005) Vector transmission of Xylella fastidiosa: applying fundamental knowledge to generate disease management strategies. Ann Entomol Soc Am 98:775–786

    Article  Google Scholar 

  • Andersen PC, Brodbeck BV, Mizell RF (1992) Feeding by the leafhopper, Homalodisca coagulata, in relation to xylem fluid chemistry and tension. J Insect Physiol 38:611–622

    Article  CAS  Google Scholar 

  • Barber GW, Ellis WO (1922) Eggs of Tree Cercopidae. Psyche 29:1–3

    Article  Google Scholar 

  • Ben-Ze’ev I, Kenneth RG (1981) Zoophthora radicans and Zoophthora petchi sp. nov. [Zygomycetes: Entomophthorales], two species of the “Sphaerosperma group” attacking leaf-hoppers and frog-hoppers [Hom.]. Entomophaga 26:131–142

    Article  Google Scholar 

  • Berry AJ, Willmer PG (1986) Temperature and the colour polymorphism of Philaenus spumarius (Homoptera: Aphrophoridae). Ecol Entomol 11:251–259

    Article  Google Scholar 

  • Biedermann R (2002) Leafhoppers (Hemiptera, Auchenorrhyncha) in fragmented habitats. Denisia 176:523–530

    Google Scholar 

  • Bleicher K, Orosz A, Cross J, Markó V (2010) Survey of leafhoppers, planthoppers and froghoppers (Auchenorrhyncha) in apple orchards in South-East England. Acta Phytopathol Hun 45:93–105

    Article  Google Scholar 

  • Blua MJ, Campbell K, Morgan DJW, Redak RA (2005) Impact of a screen barrier on dispersion behavior of Homalodisca coagulata (Hemiptera: Cicadellidae). J Econ Entomol 98:1664–1668

    Article  PubMed  CAS  Google Scholar 

  • Bodino N, Plazio E, Cavalieri V, Dongiovanni E, Ripamonti M, Volani S, Gilioli G, Fumarola G, Di Carolo M, Porcelli F, Bosco D (2017) Host-plant association and host-shifting of nymphs and adults of Philaenus spumarius L. in Italian olive orchards. In: Proceedings 3rd Hemipteran-plant interactions symposium (HPIS), Madrid, Spain, 4–8 June 2017, p 36

  • Braccini P, Pavan F (2000) Auchenorryncha: potential vectors of phytoplasms associated with vine yellows. Informatore Agrario 56:103–107

    Google Scholar 

  • Burrows M (2003) Biomechanics: froghopper insects leap to new heights. Nature 424:509

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Liang AP (2015) Identification of a self-regulatory pheromone system that controls nymph aggregation behavior of rice spittlebug Callitettix versicolor. Front Zool 12:1–12

    Article  Google Scholar 

  • Chen X, Meyer-Rochow VB, Fereres A, Morente A, Liang AP (2017) The role of biofoam in shielding spittlebug nymphs (Insecta, Hemiptera, Cercopidae) against bright light. Ecol Entomol. https://doi.org/10.1111/een.12496

    Article  Google Scholar 

  • Chmiel SM, Wilson MC (1979) Estimation of the lower and upper developmental threshold temperatures and duration of the nymphal stages of the meadow spittlebug, Philaenus spumarius. Environ Entomol 8:682–685

    Article  Google Scholar 

  • Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J, McMahon TA, Ortega CN, Sauer EL, Sehgal T, Young S (2015) Biodiversity inhibits parasites: broad evidence for the dilution effect. Proc Natl Acad Sci 112:8667–8671

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cornara D, Porcelli F (2014) Observations on the biology and ethology of Aphrophroridae: Philaenus spumarius in the Salento peninsula. In: Proceedings “International symposium on the European outbreak of Xylella fastidiosa in olive”, Gallipoli–Locorotondo, Italy, 21–24 Oct 2014

  • Cornara D, Cavalieri V, Dongiovanni C, Altamura G, Palmisano F, Bosco D, Porcelli F, Almeida RP, Saponari M (2016a) Transmission of Xylella fastidiosa by naturally infected Philaenus spumarius (Hemiptera, Aphrophoridae) to different host plants. J Appl Entomol. https://doi.org/10.1111/jen.12365

    Article  Google Scholar 

  • Cornara D, Saponari M, Zeilinger AR, de Stradis A, Boscia D, Loconsole G, Bosco D, Martelli GP, Almeida RPP, Porcelli F (2016b) Spittlebugs as vectors of Xylella fastidiosa in olive orchards in Italy. J Pest Sci. https://doi.org/10.1007/s10340-016-0793-0

    Article  Google Scholar 

  • Cornara D, Sicard A, Zeilinger AR, Porcelli F, Purcell AH, Almeida RPP (2016c) Transmission of Xylella fastidiosa to grapevine by the meadow spittlebug. Phytopathology 106:1285–1290

    Article  PubMed  CAS  Google Scholar 

  • Crews L, McCully M, Canny M, Huang C, Ling L (1998) Xylem feeding by spittlebug nymphs: some observations by optical and cryo-scanning electron microscopy. Am J Bot 85:449–460

    Article  PubMed  CAS  Google Scholar 

  • Daugherty MP, Almeida RPP (2009) Estimating Xylella fastidiosa transmission parameters: decoupling sharpshooter number and feeding period. Entomol Exp Appl 132:84–92

    Article  Google Scholar 

  • de Meyer M, de Bruyn L (1984) On the phenology of some Pipunculidae (Diptera) in Belgium. Bulletin et Annales de La Société Royale Belge D’entomologie 120:123–131

    Google Scholar 

  • Delong DM, Severin HH (1950) Spittle-insect vectors of Pierce’s disease virus. Hilgardia 19:339–376

    Article  Google Scholar 

  • Denance N, Legendre B, Briand M, Olivier V, de Boisseson C, Poliakoff F, Jacques MA (2017) Several subspecies and sequence types are associated with the emergence of Xylella fastidiosa in natural settings in France. Plant Pathol. https://doi.org/10.1111/ppa.12695

    Article  Google Scholar 

  • Dongiovanni C, Cavalieri V, Altamura G, Di Carolo M, Fumarola G, Saponari M, Porcelli F (2016) Preliminary results of comparative efficacy evaluation trials against Philaenus spumarius L., vector of Xylella fastidiosa. Options Méditerranéennes, A No. 121, 2017—Xylella fastidiosa & the Olive Quick Decline Syndrome (OQDS). A serious worldwide challenge for the safeguard of olive trees, pp 79–80

  • Drosopoulos S (2003) New data on the nature and origin of colour polymorphism in the spittlebug genus Philaenus (Hemiptera: Aphorophoridae). Ann Soc Entomol Fr 39:31–42

    Article  Google Scholar 

  • Drosopoulos S, Asche M (1991) Biosystematic studies on the spittlebug genus Philaenus with the description of a new species. Zool J Linn Soc 101:169–177

    Article  Google Scholar 

  • Drosopoulos S, Remane R (2000) Biogeographic studies on the spittlebug Philaenus signatus Melichar, 1896 species group (Hemiptera: Aphrophoridae) with the description of two new allopatric species. Ann Soc Entomol Fr 36:269–277

    Google Scholar 

  • Dugravot S, Backus EA, Reardon BJ, Miller TA (2008) Correlations of cibarial muscle activities of Homalodisca spp. sharpshooters (Hemiptera: Cicadellidae) with EPG ingestion waveform and excretion. J Insect Physiol 54:1467–1478

    Article  PubMed  CAS  Google Scholar 

  • Eden-Green S, Balfas R, Sutarjo T (1992) Characteristics of the transmission of Sumatra disease of cloves by tube-building cercopoids, Hindola spp. Plant Pathol 41:702–712

    Article  Google Scholar 

  • Edwards WD (1935) Strawberry pests including the spittlebug. Ann Rep Oregon State Hortic Soc 27:58–65

    Google Scholar 

  • EFSA (2015) Scientific Opinion on the risk to plant health posed by Xylella fastidiosa in the EU territory, with the identification and evaluation of risk reduction options. EFSA J 13:3989

    Article  Google Scholar 

  • Fauna Europaea (2016) Museum für Naturkunde Leibniz-Institut für Evolutions- und Biodiversitätsforschung Invalidenstr. Berlin, Germany. https://fauna-eu.org/

  • Fereres A (2015) Insect vectors as drivers of plant virus emergence. Curr Opin Virol 10:42–46

    Article  PubMed  Google Scholar 

  • Fisher EH, Allen TC (1946) Alfalfa and clover severely damaged by spittlebugs. What’s new in farm science. Wis Agric Exp Stn Bull 469:15–16

    Google Scholar 

  • Frazier NW (1965) Xylem viruses and their insect vectors. In: Proceedings of the international conference on virus and vectors on perennial hosts, with special reference to Vitis, pp 91–99

  • Frazier NW, Freitag JH (1946) 10 additional leafhopper vectors of the virus causing pierces disease of grapes. Phytopathology 36:634–637

    Google Scholar 

  • Freeman JA (1945) Studies in the distribution of insects by aerial currents. J Anim Ecol 104:128–154

    Article  Google Scholar 

  • Giampetruzzi A, Saponari M, Loconsole G, Boscia D, Savino VN, Almeida RP, Zicca S, Landa BB, Chacón-Diaz C, Saldarelli P (2017) Genome-wide analysis provides evidence on the genetic relatedness of the emergent Xylella fastidiosa genotype in Italy to isolates from Central America. Phytopathology 107:816–827

    Article  PubMed  Google Scholar 

  • Gibson DO (1974) Batesian mimicry without distastefulness? Nature 250:77–79

    Article  PubMed  CAS  Google Scholar 

  • Goidanich A (1954) Enciclopedia Agraria Italiana. Roma, REDA

    Google Scholar 

  • Grant JF, Lambdin PL, Follum RA (1998) Infestation levels and seasonal incidence of the meadow spittlebug (Homoptera: Cercopidae) on musk thistle in Tennessee. J Agric Entomol 15:83–91

    Google Scholar 

  • Guglielmino A, Bückle C, Remane R (2005) Contribution to the knowledge of the Auchenorrhyncha fauna of Central Italy (Hemiptera, Fulgoromorpha et Cicadomorpha). Marburger Entomologische Publikationen 3(3):13–98

    Google Scholar 

  • Gulijeva EM (1961) Pennitsa P. spumarius-vreditel’ Zernovykh lul’tur v Azerbaidzhane. Izvest Akad Navk SSR Ser Biol I Med Nauk 5:73–81

    Google Scholar 

  • Halkka O (1962) Equilibrium populations of Philaenus spumarius L. Nature 193:93–94

    Article  Google Scholar 

  • Halkka O (1964) Geographical, spatial and temporal variability in the balanced polymorphism of Philaenus spumarius. Heredity 19:383–401

    Article  Google Scholar 

  • Halkka O, Heinonen L, Raatikainen M, Vasarainen A (1966) Crossing experiments with Philaenus spumarius (Homoptera). Hereditas 56:306–312

    Article  Google Scholar 

  • Halkka O, Raatikainen M, Vasarainen A, Heinonen L (1967) Ecology and ecological genetics of Philaenus spumarius (L.)(Homoptera). Ann Zool Fenn 4:1–18

    Google Scholar 

  • Halkka O, Raatikainen M, Halkka L, Lokki J (1971) Factors determining the size and composition of island populations of Philaenus spumarius (L.)(Homoptera). Acta Entomol Fenn 28:83–100

    Google Scholar 

  • Halkka O, Kohila T, Komila T (1976) Persistence of visual polymorphism, despite a low rate of predation, in Philaenus spumarius (L.)(Homoptera, Aphrophoridae). Ann Zool Fenn 13:185–188

    Google Scholar 

  • Halkka O, Raatikainen M, Halkka L, Raatikainen T (1977) Coexistence of four species of spittle-producing Homoptera. Ann Zool Fenn 14:228–231

    Google Scholar 

  • Halkka A, Halkka L, Halkka O, Roukka K, Pokki J (2006) Lagged effects of North Atlantic Oscillation on spittlebug Philaenus spumarius (Homoptera) abundance and survival. Glob Change Biol 12:2250–2262

    Article  Google Scholar 

  • Harper G, Whittaker JB (1976) The role of natural enemies in the colour polymorphism of Philaenus spumarius (L.). J Anim Ecol 45:91–104

    Article  Google Scholar 

  • Henderson G, Hoffman GD, Jeanne RL (1990) Predation on cercopids and material use of the spittle in aphid-tent construction by prairie ants. Psyche 97:43–53

    Article  Google Scholar 

  • Hewitt WB, Frazier NW, Houston BR (1942) Transmission of Pierce’s disease of grapevine with a leafhopper. Phytopathology 32:8

    Google Scholar 

  • Hill B, Purcell AH (1995) Acquisition and retention of Xylella fastidiosa by an efficient vector, Graphocephala atropunctata. Phytopathology 85:209–212. https://doi.org/10.1094/Phyto-85-209

    Article  Google Scholar 

  • Hill BL, Purcell AH (1997) Populations of Xylella fastidiosa in plants required for transmission by an efficient vector. Phytopathology 87:1197–1201

    Article  PubMed  CAS  Google Scholar 

  • Hill GT, Sinclair WA (2000) Taxa of leafhoppers carrying phytoplasmas at sites of ash yellows occurrence in New York State. Plant Dis 84:134–138

    Article  Google Scholar 

  • Hoffman G, Mcevoy PB (1985a) Mechanical limitations on feeding by meadow spittlebugs Philaenus spumarius (Homoptera: Cercopidae) on wild and cultivated host plants. Ecol Entomol 10:415–426

    Article  Google Scholar 

  • Hoffman GD, McEvoy PB (1985b) The mechanism of trichome resistance in Anaphalis margaritacea to the meadow spittlebug Philaenus spumarius. Entomol Exp Appl 39:123–129

    Article  Google Scholar 

  • Horsfield D (1977) Relationships between feeding of Philaenus spumarius (L.) and the amino acid concentration in the xylem sap. Ecol Entomol 2:259–266

    Article  Google Scholar 

  • Horsfield D (1978) Evidence for xylem feeding by Philaenus spumarius (L.)(Homoptera: Cercopidae). Entomol Exp Appl 24:95–99

    Article  Google Scholar 

  • Ivanauskas A, Valiūnas D, Jomantienė R, Picciau L, Davis RE (2014) Possible insect vectors of “Candidatus Phytoplasma asteris” and “Ca. Phytoplasma pruni”-related strains in Lithuania. Žemdirbystė (Agriculture) 101:313–320

    Article  Google Scholar 

  • Karban R, Strauss SY (2004) Physiological tolerance, climate change, and a northward range shift in the spittlebug, Philaenus spumarius. Ecol Entomol 29:251–254

    Article  Google Scholar 

  • Keskinen E, Meyer-Rochow VB (2004) Post-embryonic photoreceptor development and dark/light adaptation in the spittle bug Philaenus spumarius (L.)(Homoptera, Cercopidae). Arthropod Struct Dev 33:405–417

    Article  PubMed  Google Scholar 

  • Killiny N, Almeida RP (2009) Xylella fastidiosa afimbrial adhesins mediate cell transmission to plants by leafhopper vectors. Appl Environ Microb 75:521–528

    Article  CAS  Google Scholar 

  • Killiny N, Prado SS, Almeida RP (2010) Chitin utilization by the insect-transmitted bacterium Xylella fastidiosa. Appl Environ Microb 76:6134–6140

    Article  CAS  Google Scholar 

  • Killiny N, Rashed A, Almeida RP (2012) Disrupting the transmission of a vector-borne plant pathogen. Appl Environ Microb 78:638–643

    Article  CAS  Google Scholar 

  • King DR (1952) The ecology of the Meadow Spittlebug Philaenus leucophthalmus (L.) L Family Cercopidae. PhD thesis, The Ohio State University

  • Koga R, Bennett GM, Cryan JR, Moran NA (2013) Evolutionary replacement of obligate symbionts in an ancient and diverse insect lineage. Environ Microbiol 15:2073–2081

    Article  PubMed  Google Scholar 

  • Kogan M (1998) Integrated pest management: historical perspectives and contemporary developments. Ann Rev Entomol 43:243–270

    Article  CAS  Google Scholar 

  • Krell RK, Boyd EA, Nay JE, Park YL, Perring TM (2007) Mechanical and insect transmission of Xylella fastidiosa to Vitis vinifera. Am J Enol Vitic 58:211–216

    CAS  Google Scholar 

  • Krewer G, Dutcher JD, Chang CJ (2002) Imidacloprid insecticide slows development of pierce’s disease in bunch grapes. J Entomol Sci 37:101–112. https://doi.org/10.18474/0749-8004-37.1.101

    Article  CAS  Google Scholar 

  • Labroussaa F, Zeilinger A, Almeida RP (2016) Blocking the transmission of a non-circulative vector-borne plant pathogenic bacterium. Mol Plant Microbe Interacions 29:535–544

    Article  CAS  Google Scholar 

  • Landi F, Prandini A, Paltrinieri S, Mori N, Bertaccini A (2007) Detection of different types of phytoplasmas in stone fruit orchards in northern Italy. Bull Insectol 60:163

    Google Scholar 

  • Lavigne B (1959) Biology of Philaenus leucophthalmus (L.), in Massachusetts. J Econ Entomol 52:904–907

    Article  Google Scholar 

  • Lees DR, Dent CS (1983) Industrial melanism in the spittlebug Philaenus spumarius (L) (Homoptera: Aphrophoridae). Biol J Linn Soc 19:115–129

    Article  Google Scholar 

  • Lewis WJ, Van Lenteren JC, Phatak SC, Tumlinson JH (1997) A total system approach to sustainable pest management. Proc Natl A Sci 94:12243–12248

    Article  CAS  Google Scholar 

  • Lis A, Maryańska-Nadachowska A, Kajtoch L (2015) Relations of Wolbachia infection with Phylogeography of Philaenus spumarius (Hemiptera: Aphrophoridae) populations within and beyond the Carpathian contact zone. Microb Ecol 70(2):509–521

    Article  PubMed  PubMed Central  Google Scholar 

  • Loconsole G, Saponari M, Boscia D, D’Attoma G, Morelli M, Martelli GP, Almeida RPP (2016) Intercepted isolates of Xylella fastidiosa in Europe reveal novel genetic diversity. Eur J Plant Pathol 146:85–94

    Article  CAS  Google Scholar 

  • Lopes JRS, Krugner R (2016) Transmission ecology and epidemiology of the citrus variegated chlorosis strain of Xylella fastidiosa. In: Vector-mediated transmission of plant pathogens. pp 195–208

  • 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 143:261–271

    Article  Google Scholar 

  • Martelli GP, Boscia D, Porcelli F, Saponari M (2016) The olive quick decline syndrome in south-east Italy: a threatening phytosanitary emergency. Eur J Plant Pathol 144:235–243

    Article  Google Scholar 

  • Maryańska-Nadachowska A, Kuznetsova VG, Lachowska D, Drosopoulos S (2012) Mediterranean species of the spittlebug genus Philaenus: modes of chromosome evolution. J Insect Sci 12:1–17

    Article  Google Scholar 

  • Masters GJ, Brown VK, Clarke IP, Whittaker JB, Hollier JA (1998) Direct and indirect effects of climate change on insect herbivores: Auchenorrhyncha (Homoptera). Ecol Entomol 23:45–52

    Article  Google Scholar 

  • Matteoni JA, Sinclair WA (1988) Elm yellows and ash yellows. In: Hiruki C (ed) Tree mycoplasmas and mycoplasma diseases. University of Alberta Press, Edmonton, pp 19–31

    Google Scholar 

  • Medler JT (1955) Method of predicting the hatching date of the meadow spittlebug. J Econ Entomol 48:204–205

    Article  Google Scholar 

  • Mundinger FG (1946) The control of spittle insects in strawberry plantings. J Econ Entomol 39:299–305

    Article  CAS  Google Scholar 

  • Nast J (1972) Palaearctic Auchenorrhyncha (Homoptera) an annotated checklist. Polish Science Publications, Warszawa

    Google Scholar 

  • Nicoli Aldini R, Guardiani MC, Cravedi P (1998) Faunistical notes on the hoppers (Homoptera Auchenorrhyncha) in vineyards in the province of Piacenza. Bollettino di Zoologia Agraria e di Bachicoltura 30:61–68

    Google Scholar 

  • Nieri R, Mazzoni V, Gordon SD, Krugner R (2017) Mating behavior and vibrational mimicry in the glassy-winged sharpshooter, Homalodisca vitripennis. J Pest Sci 90:887–899

    Article  Google Scholar 

  • Novotny V (1992) Vertical-distribution of leafhoppers (Hemiptera, Auchenorrhyncha) within a meadow community. Acta Entomol Bohemos 89:13–20

    Google Scholar 

  • Novotny V, Wilson MR (1997) Why are there no small species among xylem-sucking insects? Evol Ecol 11:419–437

    Article  Google Scholar 

  • Olmo D, Nieto A, Androver F, Urbano A, Beidos O, Juan A et al (2017) First detection of Xylella fastidiosa on cherry (Prunus avium) and Polygala myrtifolia plants, in Mallorca Island, Spain. Plant Dis 101:1820

    Google Scholar 

  • Ossiannilsson F (1981) The Auchenorrhyncha (Homoptera) of Fennoscandia and Denmark. Part 2: the families Cicadidae, Cercopidae, Membracidae, and Cicadellidae (excl. Deltocephalinae). Fauna Entomologica Scandinavica 7:223–593

    Google Scholar 

  • Pagliano G, Alma A (1997) Ricerche etologiche su Gorytini e Alyssonini (Hymenoptera Sphecidae) parassitoidi di Auchenorryncha (Rhynchota Homoptera). Rivista Piemontese di Storia Naturale 18:173–181

    Google Scholar 

  • Paião FG, Meneguim AM, Casagrande EC, Leite RP (2002) Envolvimento de cigarras (Homoptera, Cicadidae) na transmissão de Xylella fastidiosa em cafeeiro. Fitopatol Bras 27:67

    Google Scholar 

  • Pavan F (2000) Occurrence on elm and phenology of Auchenorrhyncha potential vectors of the phytoplasma associated with elm yellows disease. Bollettino di Zoologia Agraria e di Bachicoltura 32:59–68

    Google Scholar 

  • Pavan F (2006) Xylem-feeding auchenorrhyncha potentially involved in Pierce’s disease of grapevines in Europe. Bollettino di Zoologia Agraria e di Bachicoltura 38:103–114

    Google Scholar 

  • Pearson WD (1991) Effect of meadow spittlebug and Australian crop mirid on white clover seed production in small cages. N Z J Agric Res 34:439–444

    Article  Google Scholar 

  • Phillipson J (1960) A contribution to the feeding biology of Mitopus morio (F) (Phalangida). J Anim Ecol 29:35–43

    Article  Google Scholar 

  • Ponder KL, Watson RJ, Malone M, Pritchard J (2002) Mineral content of excreta from the spittlebug Philaenus spumarius closely matches that of xylem sap. New Phytol 153:237–242

    Article  CAS  Google Scholar 

  • Poos FW (1953) The meadow spittlebug, how to control it. U. S. D. A. Leaflet, p 341

  • Purcell AH (1980) Almond leaf scorch: leafhopper and spittlebug vectors. J Econ Entomol 73:834–838

    Article  Google Scholar 

  • Purcell AH (1981) Vector preference and inoculation efficiency as components of resistance to Pierce’s disease in European grape cultivars. Phytopathology 71:429–435

    Article  Google Scholar 

  • Purcell AH (1997) Xylella fastidiosa, a regional problem or global threat? J Plant Pathol 79:99–105

    Google Scholar 

  • Purcell AH, Finlay AH, McLean DL (1979) Pierce’s disease bacterium: mechanism of transmission by leafhopper vectors. Science 206:839–841

    Article  PubMed  CAS  Google Scholar 

  • Purcell AH, Gravena S, Donadio LC (1994) Sharpshooter in citrus crops. In: Citrus-integrated management of insect and mite pests. Bebedouro, Estaçao Experimental de Citricultura, pp 213–229

  • Puterka GJ, Glenn DM, Sekutowski DG, Unruh TR, Jones SK (2003) Particle film, surround WP, effects on glassy-winged sharpshooter behavior and its utility as a barrier to sharpshooter infestation in grapes. Plant Health Prog. https://doi.org/10.1094/PHP-2003-0321-RS

    Article  Google Scholar 

  • Putman WL (1953) Notes on the bionomics of some Ontario Cercopids (Homoptera). Can Entomol 85:244–248

    Article  Google Scholar 

  • Quartau JA, Borges PA (1997) On the colour polymorphism of Philaenus spumarius (L.)(Homoptera, Cercopidae) in Portugal. Miscellania Zoologica 20:19–30

    Google Scholar 

  • 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 45:432–439

    Article  PubMed  Google Scholar 

  • Rashed A, Killiny N, Kwan J, Almeida RP (2011) Background matching behaviour and pathogen acquisition: plant site preference does not predict the bacterial acquisition efficiency of vectors. Arthropod Plant Interactions 5:97–106

    Article  Google Scholar 

  • Robertson A, Gibbs AJ (1937) Spermatogenesis and fertilization in Philaenus spumarius Fallen. J Trop Med Hyg 40:257–262

    Google Scholar 

  • Rodrigues AS, Silva SE, Marabuto E, Silva DN, Wilson MR, Thompson V et al (2014) New mitochondrial and nuclear evidences support recent demographic expansion and an atypical phylogeographic pattern in the spittlebug Philaenus spumarius (Hemiptera, Aphrophoridae). PLoS ONE 9(6):e98375

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Salerno M, Russo V, Sefa V, Lamaj F, Basher N, Verrastro V, Porcelli F (2017) Zelus renardii an assassin bug candidate for Philaenus spumarius biocontrol. In: European conference on Xylella. Finding answer to a global problem. Palma de Mallorca, 13–15 Nov 2017, pp 22–23

  • Sanderlin RS, Melanson RA (2010) Insect transmission of Xylella fastidiosa to pecan. Plant Dis 94:465–470

    Article  Google Scholar 

  • Saponari M, Boscia D, Nigro F, Martelli GP (2013) Identification of DNA sequences related to Xylella fastidiosa in oleander, almond and olive trees exhibiting leaf scorch symptoms in Apulia (southern Italy). J Plant Pathol 95:668

    Google Scholar 

  • Saponari M, Loconsole G, Cornara D, Yokomi RK, De Stradis A, 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 107:1316–1319

    Article  PubMed  Google Scholar 

  • Saponari M, Boscia D, Altamura G, D’Attoma G, Cavalieri V, Loconsole G, Zicca S, Dongiovanni C, Palmisano F, Susca L, Morelli M, Potere O, Saponari A, Fumarola G, Di Carolo M, Tavano D, Savino V, Martelli GP (2016) Pilot project on Xylella fastidiosa to reduce risk assessment uncertainties. EFSA Supporting Publications. EN-1013, pp 60

  • Scholl JM, Medler JT (1947) Spittle bugs in relation to alfalfa seed production in Wisconsin. J Econ Entomol 40:446–448

    Article  PubMed  CAS  Google Scholar 

  • Schulz CA, Meijer J (1978) Migration of leafhoppers (Homoptera: Auchenorrhyncha) into a new polder. Ecography 1:73–78

    Article  Google Scholar 

  • Severin H (1950) Spittle-insect vectors of Pierce’s disease virus. II. Life history and virus transmission. Hilgardia 19:357–376

    Article  Google Scholar 

  • Sinclair WA, Griffiths HM (1994) Ash yellows and its relationship to dieback and decline of ash. Annu Rev Phytopathol 32:49–60

    Article  Google Scholar 

  • Smith RL (ed) (1984) Human sperm competition. In: Sperm competition and the evolution of animal mating systems. Academic Press, San Diego, CA, pp 602–652

  • Stewart AJA, Lees DR (1988) Genetic control of colour/pattern polymorphism in British populations of the spittlebug Philaenus spumarius (L.)(Homoptera: Aphrophoridae). Biol J Linn Soc 34:57–79

    Article  Google Scholar 

  • Stewart AJ, Lees DR (1996) The colour/pattern polymorphism of Philaenus spumarius (L.) (Homoptera: Cercopidae) in England and Wales. Philos Trans R Soc B 351:69–89

    Article  Google Scholar 

  • Strona G, Carstens CJ, Beck PS (2017) Network analysis reveals why Xylella fastidiosa will persist in Europe. Sci Rep 7:71

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Svanberg I (2016) Cuckoo spit in Northern European folk biology. In: SLA. pp 117–121

  • Thompson V (1973) Spittlebug polymorphic for warning coloration. Nature 242:126–128

    Article  Google Scholar 

  • Thompson V (1994) Spittlebug indicators of nitrogen-fixing plants. Ecol Entomol 19:391–398

    Article  Google Scholar 

  • Thompson V (2004) Associative nitrogen fixation, C4 photosynthesis, and the evolution of spittlebugs (Hemiptera: Cercopidae) as major pests of neotropical sugarcane and forage grasses. Bull Entomol Res 94:189–200

    Article  PubMed  CAS  Google Scholar 

  • Tishechkin DYu (2013) Two new species of the genus Philaenus (Homoptera, Aphrophoridae) from Iran. Entomol Rev 1:73–76

    Article  Google Scholar 

  • Tubajika KM, Civerolo EL, Puterka GJ, Hashim JM, Luvisi DA (2007) The effects of kaolin, harpin, and imidacloprid on development of Pierce’s disease in grape. Crop Prot 26:92–99

    Article  CAS  Google Scholar 

  • Van Driesche RG, Prokopy RJ, Coli WM (1987) Potential for increased use of biological control agents in Massachusetts apple orchards. Res Bull Mass Agric Exp Stn 718:6–21

    Google Scholar 

  • Walker GP (2000) A beginner’s guide to electronic monitoring of homopteran probing behavior. In: Walker GP, Backus EA (eds) Principles and applications of electronic monitoring and other techniques in the study of homopteran feeding behavior. Thomas say publications in entomology, Entomological Society of America, Lanham, MD, pp 14–40

  • Waloff N (1973) Dispersal by flight of leafhoppers (Auchenorrhyncha: Homoptera). J Appl Ecol 10:705–730

    Article  Google Scholar 

  • Watson R, Pritchard J, Malone M (2001) Direct measurement of sodium and potassium in the transpiration stream of salt-excluding and non-excluding varieties of wheat. J Exp Bot 52:1873–1881

    Article  PubMed  CAS  Google Scholar 

  • Weaver CR (1951) The seasonal behaviour of meadow spittlebug and its relation to a control method. J Econ Entomol 44:350–353

    Article  CAS  Google Scholar 

  • Weaver CR, King DR (1954) Meadow spittlebug, Philaenus leucophthalmus (L.). Ohio Agric Exp Stat Bull 741:1–99

    Google Scholar 

  • West J, Lees DR (1988) Temperature and egg development in the spittlebug Philaenus spumarius (L.)(Homoptera: Aphrophoridae). The Entomologist 13:46–51

    Google Scholar 

  • Whittaker JB (1969) The biology of Pipunculidae (Diptera) parasitising some British Cercopidae (Homoptera). Physiol Entomol 44:17–24

    Google Scholar 

  • Whittaker JB (1970) Cercopid spittle as a microhabitat. Oikos 21:59–64

    Article  Google Scholar 

  • Whittaker JB (1973) Density regulation in a population of Philaenus spumarius (L.)(Homoptera: Cercopidae). J Anim Ecol 42:163–172

    Article  Google Scholar 

  • Wiegert RG (1964) Population energetics of meadow spittlebugs (Philaenus spumarius L.) as affected by migration and habitat. Ecol Monogr 34:217–241

    Article  Google Scholar 

  • Wilson MC, Shade RE (1967) Relative attractiveness of various luminescent colors to the cereal leaf beetle and the meadow spittle bug. J Econ Entomol 60:578–580

    Article  Google Scholar 

  • Wise MJ, Kieffer DL, Abrahamson WG (2006) Costs and benefits of gregarious feeding in the meadow spittlebug, Philaenus spumarius. Ecol Entomol 31:548–555

    Article  Google Scholar 

  • Witsack W (1973) Experimental and ecological investigations on forms of dormancy in homoptera-cicadina (Auchenorrhyncha). 2. On ovarian parapause and obligatory embryonic diapause in Philaenus spumarius (L.)(Aphrophoridae). Zoologische Jahrbücher: Abteilung für Systematik, Okologie und Geographie der Tiere 100:517–562

  • Yurtsever S (2000) On the polymorphic meadow spittlebug, Philaenus spumarius (L.)(Homoptera: Cercopidae). Turk J Zool 24:447–460

    Google Scholar 

  • Zajac MA, Wilson MC (1984) The effects of nymphal feeding by the meadov spittlebug, Philaenus spumarius (L.) on strawberry yield and quality. Crop Prot 3:167–175

    Article  Google Scholar 

  • Zajac MA, Hall FR, Wilson MC (1989) Heat unit model for the development of meadow spittlebug (Homoptera Cercopidae) on strawberry. Environ Entomol 18:347–350

    Article  Google Scholar 

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Acknowledgements

Authors would like to acknowledge an EFSA procurement action on the information on biology and control of vectors of Xylella fastidiosa, the European Union Horizon 2020 research and innovation program under Grant Agreement No. 635646 POnTE (Pest Organisms Threatening Europe), and Grant Agreement No. 727987 XF-ACTORS.

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  1. Instituto de Ciencias Agrarias, Consejo Superior de Investigaciones Cientificas, ICA-CSIC, Calle Serrano 115 dpdo, 28006, Madrid, Spain

    D. Cornara & A. Fereres

  2. Università di Torino, Dipartimento di Scienze Agrarie, Forestali e Alimentari, Largo Paolo Braccini, 2, 10095, Grugliasco, TO, Italy

    D. Bosco

  3. Istituto per la Protezione Sostenibile delle Piante, Consiglio Nazionale delle Ricerche, Strada delle Cacce, 73, 10135, Torino, Italy

    D. Bosco

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Cornara, D., Bosco, D. & Fereres, A. Philaenus spumarius: when an old acquaintance becomes a new threat to European agriculture. J Pest Sci 91, 957–972 (2018). https://doi.org/10.1007/s10340-018-0966-0

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