Abstract
A new myrmecophilous species of root mealybug, Williamsrhizoecus udzungwensis sp. n., is described from individuals found living within a nest of Acropyga silvestrii in the Udzungwa Mountains of Tanzania. Acropyga ants are highly specialized, obligate associates of scale insects, typically members of the scale family Xenococcidae. Acropyga are best known for vertically transmitting trophobiotic partners during their nuptial flights and for housing them within brood chambers. This article presents the first record of trophobiosis between a species of Williamsrhizoecus and Acropyga, and only the second record of an association between Acropyga and rhizoecids in the Old World. This discovery contributes important information about the few species of Rhizoecidae confirmed to engage in these unique symbioses, each putatively the result of a past horizontal transmission event from a xenococcid to a rhizoecid lineage. Included is a discussion on the diagnosis of Williamsrhizoecus and an updated key to the species.
References
Akino, T., Knapp, J.J., Thomas, J.A. & Elmes, G.W. (1999) Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proceedings of the Royal Society B, 266, 1419–1426.
https://doi.org/10.1098/rspb.1999.0796
Blaimer, B.B., LaPolla, J.S., Branstetter, M.G., Lloyd, M.W. & Brady, S.G. (2016) Phylogenomics, biogeography and diversification of obligate mealybug-tending ants in the genus Acropyga. Molecular Phylogenetics and Evolution, 102, 20–29.
https://doi.org/10.1016/j.ympev.2016.05.030
Bünzli, G.H. (1935) Untersuchungen über coccidophile Ameisen aus den Kaffeefeldern von Surinam. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 16, 455–581.
https://doi.org/10.3929/ethz-a-000099183
Caballero, A. & Ramos-Portilla, A.A. (2018) Hypogeal scale insects (Hemiptera: Coccomorpha) of the coffee agro-system in Chiapas state, Mexico, with description of a new species of Williamsrhizoecus Kozár and Konczné Benedicty (Rhizoecidae). The Journal of Basic and Applied Zoology, 79, 1–7.
https://doi.org/10.1186/s41936-018-0054-2
Caballero, A., Ramos-Portilla, A.A., Suárez-González, D., Serna, F., Gil, Z.N. & Benavides, P. (2019) Scale insects (Hemiptera: Coccomorpha) on coffee roots (Coffea arabica L.) in Colombia, with records of associated ants (Hymenoptera: Formicidae). Ciencia y Tecnología Agropecuaria, Mosquera, Colombia, 20, 93–116.
https://doi.org/10.21930/rcta.vol20_num1_art:1250
Danzig, E.M. & Gavrilov-Zimin, I.A. (2014) Fauna of Russia and neighbouring countries. Palaearctic mealybugs (Homoptera, Coccinea, Pseudococcidae). Russian Academy of Sciences, Zoological Institute, New Series, 148, 1–678.
Delabie, J.H. (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotropical Entomology, 30, 501–516.
https://doi.org/10.1590/S1519-566X2001000400001
Delabie, J.H., Mantovani, J.E. & Maurício, C. (1991) Observaões sobre a biologia de duas espécies de Acropyga (Formicidae, Formicinae, Plagiolepidini) associadas rizosfera do cacaueiro. Revista Brasileira de Biologia, 51, 185–192.
Downie, D.A. & Gullan, P.J. (2004) Phylogenetic analysis of mealybugs (Hemiptera: Coccoidea: Pseudococcidae) based on DNA sequences from three nuclear genes, and a review of the higher classification. Systematic Entomology, 29, 238–259.
https://doi.org/10.1111/j.0307-6970.2004.00241.x
Elmes, G.W., Barr, B., Thomas, J.A. & Clarke, R.T. (1999) Extreme host specificity by Microdon mutabilis (Diptera: Syrphidae), a social parasite of ants. Proceedings of the Royal Society B, 266, 447–453.
https://doi.org/10.1098/rspb.1999.0658
García Morales, M., Denno, B.D., Miller, D.R., Miller, G.L., Ben-Dov, Y., & Hardy, N.B. (2016) ScaleNet: a literature-based model of scale insect biology and systematics. Database, 2016, bav118. Available from: http://scalenet.info/ (accessed 13 August 2020)
https://doi.org/10.1093/database/bav118
Gavrilov-Zimin, I.A. (2018) Ontogenesis, morphology and higher classification of archaeococcids (Homoptera: Coccinea: Orthezioidea). Zoosystematica Rossica, 2018, 1–264.
https://doi.org/10.31610/zsr/2018.supl.2.1
Hardy, N.B., Gullan, P.J. & Hodgson, C.J. (2008) A subfamily-level classification of mealybugs (Hemiptera: Pseudococcidae) based on integrated molecular and morphological data. Systematic Entomology, 33, 51–71.
https://doi.org/10.1111/j.1365-3113.2007.00408.x
Hodgson, C. (2012) Comparison of the morphology of the adult males of the rhizoecine, phenacoccine and pseudococcine mealybugs (Hemiptera: Sternorrhyncha: Coccoidea), with the recognition of the family Rhizoecidae Williams. Zootaxa, 3291 (1), 1–79.
https://doi.org/10.11646/zootaxa.3291.1.1
Hodgson, C. (2020) A review of neococcid scale insects (Hemiptera: Sternorrhyncha: Coccomorpha) based on the morphology of the adult males. Zootaxa, 4765 (1), 001–264.
https://doi.org/10.11646/zootaxa.4765.1.1
Johnson, C., Agosti, D., Delabie, J.H., Dumpert, K., Williams, D., Tschirnhaus, M.V. & Maschwitz, U. (2001) Acropyga and Azteca ants (Hymenoptera: Formicidae) with scale insects (Sternorrhyncha: Coccoidea): 20 million years of intimate symbiosis. American Museum Novitates, 3335, 1–18.
https://doi.org/10.1206/0003-0082(2001)335<0001:AAAAHF>2.0.CO;2
Kozár, F. & Konczné Benedicty, Z. (2007) Rhizoecinae of the World. Plant Protection Institute, Hungarian Academy of Sciences Budapest, 617 pp.
LaPolla, J.S. (2004) Acropyga (Hymenoptera: Formicidae) of the world. Contributions of the American Entomological Institute, 33, 1–130.
LaPolla, J.S. (2005) Ancient trophophoresy: a fossil Acropyga (Hymenoptera: Formicidae) from Dominican amber. Transactions of the American Entomological Society, 131, 21–28.
LaPolla, J.S. & Spearman, L.A. (2007) Characterization of an Acropyga arnoldi mating swarm and early stage colony founding behavior. Transactions of the American Entomological Society, 133, 449–452.
https://doi.org/10.3157/0002-8320-133.3.449
LaPolla, J.S., Burwell, C., Brady, S.G. & Miller, D.R. (2008) A new ortheziid (Hemiptera: Coccoidea) from Australia associated with Acropyga myops Forel (Hymenoptera: Formicidae) and a key to Australian Ortheziidae. Zootaxa, 1946 (1), 55–68.
https://doi.org/10.11646/zootaxa.1946.1.3
LaPolla, J.S., Cover, S.P. & Mueller, U.G. (2002) Natural history of the mealybug-tending ant, Acropyga epedana, with descriptions of the male and queen castes. Transactions of the American Entomological Society, 128, 367–376.
Malsch, A.K.F., Kaufmann, E., Heckroth, H.P., Williams, D.J., Maryati, M. & Maschwitz, U. (2001) Continuous transfer of subterranean mealybugs (Hemiptera, Pseudococcidae) by Pseudolasius spp. (Hymenoptera, Formicidae) during colony fission? Insectes Sociaux, 48, 333–341.
https://doi.org/10.1007/PL00001786
Normark, B.B., Okusu, A., Morse, G.E., Peterson, D.A., Itioka, T. & Schneider, S.A. (2019) Phylogeny and classification of armored scale insects (Hemiptera: Coccomorpha: Diaspididae). Zootaxa, 4616 (1), 1–98.
https://doi.org/10.11646/zootaxa.4616.1.1
Prins, A.J. (1982) Review of Anoplolepis with reference to male genitalia, and notes on Acropyga (Hymenoptera, Formicidae). Annals of the South African Museum, 89, 215–247.
Schneider, S.A., Giliomee, J.H., Dooley, J.W. & Normark, B.B. (2013) Mutualism between armoured scale insects and ants: new species and observations on a unique trophobiosis (Hemiptera: Diaspididae; Hymenoptera: Formicidae: Melissotarsus Emery). Systematic Entomology, 38, 805–817.
https://doi.org/10.1111/syen.12033
Schneider, S.A. & LaPolla, J.S. (2011) Systematics of the mealybug tribe Xenococcini (Hemiptera: Coccoidea: Pseudococcidae), with a discussion of trophobiotic associations with Acropyga Roger ants. Systematic Entomology, 36, 57–82.
https://doi.org/10.1111/j.1365-3113.2010.00546.x
Smith, C.R., Oettler, J., Kay, A. & Deans, C. (2007) First recorded mating flight of the hypogeic ant, Acropyga epedana, with its obligate mutualist mealybug, Rhizoecus colombiensis. Journal of Insect Science, 7, 1–5.
https://doi.org/10.1673/031.007.1101
Tanaka, H. (2016) A new genus and species of Rhizoecidae (Hemiptera, Sternorrhyncha, Coccomorpha) associated with Acropyga yaeyamensis (Hymenoptera, Formicidae, Formicinae). ZooKeys, 616, 115–124.
https://doi.org/10.3897/zookeys.616.9442
Williams, D.J. (1970) The mealybugs (Homoptera, Coccoidea, Pseudococcidae) of sugar-cane, rice and sorghum. Bulletin of Entomological Research, 60, 109–188.
https://doi.org/10.1017/S0007485300034209
Williams, D.J. (1998) Mealybugs of the genera Eumyrmococcus Silvestri and Xenococcus Silvestri associated with the ant genus Acropyga Roger and a review of the subfamily Rhizoecinae (Hemiptera, Coccoidea, Pseudococcidae). Bulletin of the British Museum, Natural History, Entomology, 67, 1–64.
Williams, D.J. (2004) A synopsis of the subterranean mealybug genus Neochavesia Williams and Granara de Willink (Hemiptera: Pseudococcidae: Rhizoecinae). Journal of Natural History, 38, 2883–2899.
https://doi.org/10.1080/00222930310001657856