CONTRIBUTION TO THE KNOWLEDGE OF APHROPHORID SPITTLEBUGS (HEMIPTERA: APHROPHORIDAE) FROM MOROCCO
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May 24, 2022
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Abstract
This paper lists the current fauna of Aphrophoridae family in Morocco. Distribution data of their occurrence in the country are provided. Nine species of aphrophorid spittlebugs found in Morocco are listed, five of them identified and described for the first time in the country and four other species reported in the literature. An identification key of aphrophorid genera and species is given. The Mediterranean spittlebug Philaenus tesselatus Melichar, 1899 (Moroccan specimen) is described and differentiated from the European meadow spittlebug Philaenus spumarius Linnaeus, 1758 (Italian specimen). The newly reported Philaenus sp. specimen found in Morocco is described.
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Smaili, M. C., Haddad, N., Afechtal, M., Streito, J.-C., Ougass, Y., & Benkirane, R. (2022). CONTRIBUTION TO THE KNOWLEDGE OF APHROPHORID SPITTLEBUGS (HEMIPTERA: APHROPHORIDAE) FROM MOROCCO. Acta Entomologica Serbica, 27(1), 1-18. https://doi.org/10.5281/zenodo.6576544
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Copyright: © 2019 The ENTOMOLOGICAL SOCIETY OF SERBIA Staff. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
References
Afechtal, M., Vicent, A., Saponari M., & D'Onghia, A. M. (2018a). Pest Risk Analysis on Xylella fastidiosa in Morocco. Journal of Plant Protection Research, 58(3), 215-219.
Afechtal, M., Benyahia, H., Benaouda, H., & Smaili, M. C. (2018b). Survey on the presence of Xylella fastidiosa and its potential insect vectors in Moroccan citrus orchards. In Unidad de Comunicación y Transferencia de Tecnología del INIA (Eds.), “The IV International Symposium on Citrus Biotechnology: Book of Abstracts”, 16-18 Apr. 2018, Montevideo, Uruguay. SIII-P-4. http://riacnet.net/wp-content/uploads/2018/04/INIA-Serie-tecnica-244-Simposio-Citrus-Web.pdf.
Antonatos, S., Papachristos, D. P., Kapantaidaki, D. E., Lytra, I. C., Varikou, K., Evangelou, V., & Milonas, P. (2020). Presence of Cicadomorpha in olive orchards of Greece with special reference to Xylella fastidiosa vectors. Journal applied entomology, 144, 1-11.
Cavalieri, V., Altamura, G., Fumarola, G., Di-Carolo, M., Saponari, M., Cornara, D., Bosco, D., & Dongiovanni, C. (2019). Transmission of Xylella fastidiosa subspecies pauca sequence type 53 by different insect species. Insects, 10(10), 324. https://doi.org/10.3390/insects10100324.
Cornara, D., Bosco, D., & Fereres, A. (2018). Philaenus spumarius: when an old acquaintance becomes a new threat to European agriculture. Journal of Pest Science, 91, 957–972. https://doi.org/10.1007/s10340-018-0966-0.
Cornara, D., Morente, M., Markheiser, A., Bodino, N., Tsai C. W., Fereres, A., Redak, R. A, Perring, T. M., & Lopes, J. R. S. (2019). An overview on the worldwide vectors of Xylella fastidiosa. Entomologia Genralis, 39(3-4), 157-181.
Cryan, J. R., & Svenson, G. J. (2010). Family-level relationships of the spittlebugs and froghoppers (Hemiptera: Cicadomorpha: Cercopoidea). Systematic Entomology, 35, 393-415.
Davis, C. J., & Mitchell, A. L. (1946). Host records of Philaenus spumarius (L.) at Kilauea, Hawaii National Park (Homoptera:Cercopidae). Proceedings of the Hawaiian Entomological Society, 12, 515-516.
Dietrich, C. H. (2005). Keys to the families of Cicadomorpha and subfamilies and tribes of Cicadellidae (Hemiptera: Auchenorrhyncha). Florida Entomologist, 88(4), 502-517.
https://doi.org/10.1653/00154040(2005)88[502:KTTFO C]2.0.CO;2.
Dietrich, C. H. (2009). Chapter 15- Auchenorrhyncha (Cicadas, Spittlebugs, Leafhoppers, Treehoppers and Planthoppers). In Resh, V. R., & Cardé, R. T. (Eds.), Encyclopedia of insects book 2nd Edn, Elsevier Inc, Academic Press, (US). 56-64.
Drosopoulos, S. (2003). New data on the nature and origin of colour polymorphism in the spittlebug genus Philaenus (Hemiptera:Aphorophoridae). Annales de la Société entomologique de France, 39(1), 31-42.
Drosopoulos, S., & Asche, M. (1991). Biosystematic studies on the spittlebug genus Philaenus with the description of a new species. Zoological journal of the Linnean society, 101, 169-177.
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. Annales de la Société Entomologique de France, 36(3), 269-277.
Drosopoulos, S. & Quartau, J. A. (2002). The spittle bug Philaenus tesselatus Melichar, 1899 (Hemiptera: Auchenorrhyncha: Cercopidae) is a distinct species. Zootaxa, 68, 1-8.
Drosopoulos, S., Maryanska-Nadachowska, A., & Kuznetsova, V. G. (2008). Additional new data proving that early publications on the polymorphism of the spittlebug of the genus Philaenus were lacking in systematics. Bulletin of Insectology, 61(1), 99-100.
Drosopoulos, S., Maryanska-Nadachowska, A., & Kuznetsova, V. G. (2010). The Mediterranean: Area of origin of polymorphism and speciation in the spittlebug Philaenus (Hemiptera, Aphrophoridae). Zoosystematics and Evolution, 86(1), 125-128.
EPPO, (2019). PM 7/24 (4) Xylella fastidiosa. EPPO Bulletin, 49(2), 175-227.
EPPO, (2020). PM 7/141 (1) Philaenus spumarius, Philaenus italosignus and Neophilaenus campestris. EPPO Bulletin, 50(1), 32-40.
Haddad, N., Afechtal, M., Streito, J. C, Ouguas, Y., Benkirane, R., Lhomme, P., & Smaili, M. C. (2021). Occurrence in Morocco of potential vectors of Xylella fastidiosa that may contribute to the active spread of the bacteria. Annales de la Société Entomologique de France, 57, 359-371. DOI: 10.1080/00379271. 2021.1965910.
Halkka, O., & Lallukka, R. (1969). The origin of balanced polymorphism in the spittlebugs (Philaenus: Homoptera). Annales Zoologici Fennici, 6, 431-434.
Kapantaidaki, D. E., Antonatos, S., Evangelou, V., Papachristos, D. P. & Milonas, M. (2021) Genetic and endosymbiotic diversity of Greek populations of Philaenus spumarius, Philaenus signatus and Neophilaenus campestris, vectors of Xylella fastidiosa. Scientific Reports, 11, 3752. https://doi;org/10;1038/s41598-021-83109-z.
Liang, A. (2006). Synonymy of Aphrophora willemsi Lallemand 1946 with Aphrophora salicina (Goeze, 1778) (Hemiptera: Cercopoidea: Aphrophoridae). Journal of the New York Entomological Society, 114(3), 140-143.
Lodos, N., & Kalkandelen, A. (1981). Preliminary list of Auchenorrhycha with notes on distribution and importance of species in Turkey. VI. Families Cercopidae and Membracidae. Turkiye Bitki Koruma Dergisi, 5(3), 133-149.
Mozaffarian, F. (2018). An Identification key to the species of Auchenorrhyncha of Iranian fauna recorded as pests in orchards and a review on the pest status of the species. Zootaxa, 4420(4), 475-501.
Mozaffarian, F., & Wilson, M. R. (2015). The aphrophorid spittlebugs of Iran (Hemiptera: Cercopoidea: Aphrophoridae). Zootaxa, 4052(4), 442-456.
ONSSA, (2016). Evaluation du risque phytosanitaire de Xylella fastidiosa au Maroc. Rapport du Groupe de Travail. Avril 2016. ONSSA, Rabat, Maroc, 51 pp.
Remane, R., & Drosopoulos S. (2001). Philaenus tarifa sp. n.: An additional spittlebug species from southern Spain (Homoptera, Auchenorrhyncha Cercopidae). Mitteilungen aus dem Museum fur Naturkunde in Berlin-Deutsche Entomologische Zeitschrift, 48(2), 277-279.
Rodrigues, A. S. B., Silva, S. E., Marabuto, E., Silva, D. N., Wilson, M. R., Thompson, V., Yurtsever, S., Halkka, A., Borges, P. A. V., Quartau, J. A., Paolo, O. S., & Seabra, S. G. (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), 1-12.
Santoiemma, G., Tamburini, G., Sanna, F., Mori, N., & Marini, L. (2019). Landscape composition predicts the distribution of Philaenus spumarius, vector of Xylella fastidiosa, in olive groves. Journal of Pest Science, 92, 1101-1109.
Saponari, M., Boscia, D., Nigro, F., & Martelli, G. P. (2013). Identification of DNA sequences related to Xylella fastidiosa in oleander, almond and olive trees exhibiting leaf scorch symptoms in Apulia (Southern Italy). Journal of Plant Pathology, 95(3), 659-668.
Saponari, M., Giampetruzzi, A., Loconsole, G., Boscia, D., & Saldarelli, P. (2019). Xylella fastidiosa in olive in Apulia: where we stand. Phytopathology, 109(2), 175-186.
Seabra, S. G., Rodrigues, A. S. B., Silva, S. E., Neto, A. C., Pina-Martins, F., Marabuto, E., Thompson, V., Wilson, M. R., Yurtsever, S., Halkka, A., Rebelo, M. T., Borges, P. A. V., Quartau, J. A., Jiggins, C. D., & Paulo, O. S. (2021) Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data. PeerJ 9:e11425 http://doi.org/10.7717/peerj.11425.
Smaili, M. C., & Afechtal M. (2018). Vecteurs potentiels de Xylella fastidiosa au Maroc. In FAO & ONSSA (Eds.), «Atelier sur la prévention contre l’introduction de Xylella fastidiosa au Maroc » International workshop on Xylella fastidiosa, 13-14 Sep. 2018, IAV Hassan II, Rabat, Morocco, 1-19 pp.
Thompson, V. (1984) Colour polymorphism in the introduced spittlebug Philaenus spumarius (Homoptera: Aphrophoridae) in New Zealand. New Zealund Entomologist, 8, 86-88.
Thompson, V., & Halkka O. (1973) Color polymorphism in some North American Philaenus spumarius (Homoptera: Aphrophoridae) populations. American Midland Naturalist, 89 (2), 348-359.
http://www.jstor.org/stable/2424039.
Afechtal, M., Benyahia, H., Benaouda, H., & Smaili, M. C. (2018b). Survey on the presence of Xylella fastidiosa and its potential insect vectors in Moroccan citrus orchards. In Unidad de Comunicación y Transferencia de Tecnología del INIA (Eds.), “The IV International Symposium on Citrus Biotechnology: Book of Abstracts”, 16-18 Apr. 2018, Montevideo, Uruguay. SIII-P-4. http://riacnet.net/wp-content/uploads/2018/04/INIA-Serie-tecnica-244-Simposio-Citrus-Web.pdf.
Antonatos, S., Papachristos, D. P., Kapantaidaki, D. E., Lytra, I. C., Varikou, K., Evangelou, V., & Milonas, P. (2020). Presence of Cicadomorpha in olive orchards of Greece with special reference to Xylella fastidiosa vectors. Journal applied entomology, 144, 1-11.
Cavalieri, V., Altamura, G., Fumarola, G., Di-Carolo, M., Saponari, M., Cornara, D., Bosco, D., & Dongiovanni, C. (2019). Transmission of Xylella fastidiosa subspecies pauca sequence type 53 by different insect species. Insects, 10(10), 324. https://doi.org/10.3390/insects10100324.
Cornara, D., Bosco, D., & Fereres, A. (2018). Philaenus spumarius: when an old acquaintance becomes a new threat to European agriculture. Journal of Pest Science, 91, 957–972. https://doi.org/10.1007/s10340-018-0966-0.
Cornara, D., Morente, M., Markheiser, A., Bodino, N., Tsai C. W., Fereres, A., Redak, R. A, Perring, T. M., & Lopes, J. R. S. (2019). An overview on the worldwide vectors of Xylella fastidiosa. Entomologia Genralis, 39(3-4), 157-181.
Cryan, J. R., & Svenson, G. J. (2010). Family-level relationships of the spittlebugs and froghoppers (Hemiptera: Cicadomorpha: Cercopoidea). Systematic Entomology, 35, 393-415.
Davis, C. J., & Mitchell, A. L. (1946). Host records of Philaenus spumarius (L.) at Kilauea, Hawaii National Park (Homoptera:Cercopidae). Proceedings of the Hawaiian Entomological Society, 12, 515-516.
Dietrich, C. H. (2005). Keys to the families of Cicadomorpha and subfamilies and tribes of Cicadellidae (Hemiptera: Auchenorrhyncha). Florida Entomologist, 88(4), 502-517.
https://doi.org/10.1653/00154040(2005)88[502:KTTFO C]2.0.CO;2.
Dietrich, C. H. (2009). Chapter 15- Auchenorrhyncha (Cicadas, Spittlebugs, Leafhoppers, Treehoppers and Planthoppers). In Resh, V. R., & Cardé, R. T. (Eds.), Encyclopedia of insects book 2nd Edn, Elsevier Inc, Academic Press, (US). 56-64.
Drosopoulos, S. (2003). New data on the nature and origin of colour polymorphism in the spittlebug genus Philaenus (Hemiptera:Aphorophoridae). Annales de la Société entomologique de France, 39(1), 31-42.
Drosopoulos, S., & Asche, M. (1991). Biosystematic studies on the spittlebug genus Philaenus with the description of a new species. Zoological journal of the Linnean society, 101, 169-177.
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. Annales de la Société Entomologique de France, 36(3), 269-277.
Drosopoulos, S. & Quartau, J. A. (2002). The spittle bug Philaenus tesselatus Melichar, 1899 (Hemiptera: Auchenorrhyncha: Cercopidae) is a distinct species. Zootaxa, 68, 1-8.
Drosopoulos, S., Maryanska-Nadachowska, A., & Kuznetsova, V. G. (2008). Additional new data proving that early publications on the polymorphism of the spittlebug of the genus Philaenus were lacking in systematics. Bulletin of Insectology, 61(1), 99-100.
Drosopoulos, S., Maryanska-Nadachowska, A., & Kuznetsova, V. G. (2010). The Mediterranean: Area of origin of polymorphism and speciation in the spittlebug Philaenus (Hemiptera, Aphrophoridae). Zoosystematics and Evolution, 86(1), 125-128.
EPPO, (2019). PM 7/24 (4) Xylella fastidiosa. EPPO Bulletin, 49(2), 175-227.
EPPO, (2020). PM 7/141 (1) Philaenus spumarius, Philaenus italosignus and Neophilaenus campestris. EPPO Bulletin, 50(1), 32-40.
Haddad, N., Afechtal, M., Streito, J. C, Ouguas, Y., Benkirane, R., Lhomme, P., & Smaili, M. C. (2021). Occurrence in Morocco of potential vectors of Xylella fastidiosa that may contribute to the active spread of the bacteria. Annales de la Société Entomologique de France, 57, 359-371. DOI: 10.1080/00379271. 2021.1965910.
Halkka, O., & Lallukka, R. (1969). The origin of balanced polymorphism in the spittlebugs (Philaenus: Homoptera). Annales Zoologici Fennici, 6, 431-434.
Kapantaidaki, D. E., Antonatos, S., Evangelou, V., Papachristos, D. P. & Milonas, M. (2021) Genetic and endosymbiotic diversity of Greek populations of Philaenus spumarius, Philaenus signatus and Neophilaenus campestris, vectors of Xylella fastidiosa. Scientific Reports, 11, 3752. https://doi;org/10;1038/s41598-021-83109-z.
Liang, A. (2006). Synonymy of Aphrophora willemsi Lallemand 1946 with Aphrophora salicina (Goeze, 1778) (Hemiptera: Cercopoidea: Aphrophoridae). Journal of the New York Entomological Society, 114(3), 140-143.
Lodos, N., & Kalkandelen, A. (1981). Preliminary list of Auchenorrhycha with notes on distribution and importance of species in Turkey. VI. Families Cercopidae and Membracidae. Turkiye Bitki Koruma Dergisi, 5(3), 133-149.
Mozaffarian, F. (2018). An Identification key to the species of Auchenorrhyncha of Iranian fauna recorded as pests in orchards and a review on the pest status of the species. Zootaxa, 4420(4), 475-501.
Mozaffarian, F., & Wilson, M. R. (2015). The aphrophorid spittlebugs of Iran (Hemiptera: Cercopoidea: Aphrophoridae). Zootaxa, 4052(4), 442-456.
ONSSA, (2016). Evaluation du risque phytosanitaire de Xylella fastidiosa au Maroc. Rapport du Groupe de Travail. Avril 2016. ONSSA, Rabat, Maroc, 51 pp.
Remane, R., & Drosopoulos S. (2001). Philaenus tarifa sp. n.: An additional spittlebug species from southern Spain (Homoptera, Auchenorrhyncha Cercopidae). Mitteilungen aus dem Museum fur Naturkunde in Berlin-Deutsche Entomologische Zeitschrift, 48(2), 277-279.
Rodrigues, A. S. B., Silva, S. E., Marabuto, E., Silva, D. N., Wilson, M. R., Thompson, V., Yurtsever, S., Halkka, A., Borges, P. A. V., Quartau, J. A., Paolo, O. S., & Seabra, S. G. (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), 1-12.
Santoiemma, G., Tamburini, G., Sanna, F., Mori, N., & Marini, L. (2019). Landscape composition predicts the distribution of Philaenus spumarius, vector of Xylella fastidiosa, in olive groves. Journal of Pest Science, 92, 1101-1109.
Saponari, M., Boscia, D., Nigro, F., & Martelli, G. P. (2013). Identification of DNA sequences related to Xylella fastidiosa in oleander, almond and olive trees exhibiting leaf scorch symptoms in Apulia (Southern Italy). Journal of Plant Pathology, 95(3), 659-668.
Saponari, M., Giampetruzzi, A., Loconsole, G., Boscia, D., & Saldarelli, P. (2019). Xylella fastidiosa in olive in Apulia: where we stand. Phytopathology, 109(2), 175-186.
Seabra, S. G., Rodrigues, A. S. B., Silva, S. E., Neto, A. C., Pina-Martins, F., Marabuto, E., Thompson, V., Wilson, M. R., Yurtsever, S., Halkka, A., Rebelo, M. T., Borges, P. A. V., Quartau, J. A., Jiggins, C. D., & Paulo, O. S. (2021) Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data. PeerJ 9:e11425 http://doi.org/10.7717/peerj.11425.
Smaili, M. C., & Afechtal M. (2018). Vecteurs potentiels de Xylella fastidiosa au Maroc. In FAO & ONSSA (Eds.), «Atelier sur la prévention contre l’introduction de Xylella fastidiosa au Maroc » International workshop on Xylella fastidiosa, 13-14 Sep. 2018, IAV Hassan II, Rabat, Morocco, 1-19 pp.
Thompson, V. (1984) Colour polymorphism in the introduced spittlebug Philaenus spumarius (Homoptera: Aphrophoridae) in New Zealand. New Zealund Entomologist, 8, 86-88.
Thompson, V., & Halkka O. (1973) Color polymorphism in some North American Philaenus spumarius (Homoptera: Aphrophoridae) populations. American Midland Naturalist, 89 (2), 348-359.
http://www.jstor.org/stable/2424039.