Abstract
A new genus of lady beetle, Moiradiomus gen. nov. (Coleoptera: Coccinellidae Latreille, 1807: Diomini Gordon, 1999 ), and four new species are described from Costa Rica, representing the first known occurrences of obligate phytophagous lady beetle species outside of the tribe Epilachnini Mulsant, 1846 (sens. Ślipiński 2007). The new species are described, illustrated and keyed, and their life histories discussed. Each species of Moiradiomus occurs on a separate species of Piper L., 1753 (Piperaceae Giseke, 1792), where the larva constructs a small silken tent between leaf veins and inside this shelter induces the production of food bodies, which are its exclusive source of food. Background information is provided on lady beetle trophic relations and other insect/Piper symbioses. The taxonomic history of Diomus Mulsant, 1850 and related species in the tribe Diomini is reviewed and existing errors in observation, interpretation, identification, and classification are corrected in order to provide a more meaningful context for understanding the new genus. The tribe Diomini is rediagnosed and recircumscribed to include Diomus, Decadiomus Chapin, 1933, Heterodiomus Brèthes, 1925, Dichaina Weise, 1923, Andrzej Ślipiński, 2007, and Moiradiomus. Magnodiomus Gordon, 1999 and Erratodiomus Gordon, 1999 are removed from Diomini and transferred to Hyperaspidini Costa, 1849, subtribe Selvadiina Gordon, 1985 stat. nov. Mimoscymnus Gordon, 1994 and Planorbata Gordon, 1994, originally described in Coccidulini Mulsant, 1846 are also transfered to Hyperaspidini and placed in Mimoscymnina subtribe nov. (type genus Mimoscymnus). The main morphological characters distinguishing Diomini and Hyperaspidini are described and illustrated. A key to genera of Diomini sensu novo is provided. The identification of the Australian Diomus species illustrated in Gordon’s publication on North American lady beetles is corrected from D. pumilio Weise, 1885 to D. tenebricosus (Boheman, 1859), however specimens recently collected in California do not match these genitalic illustrations and are identified as true D. pumilio. The following species of Diomus are transferred to Decadiomus as new combinations: D. balteatus (LeConte, 1878), D. floridanus (Mulsant, 1850), D. amabilis (LeConte, 1852), D. liebecki (Horn, 1895), D. myrmidon (Mulsant, 1850), D. humilis (Gordon, 1976), D. pseudotaedatus (Gordon, 1976), D. taedatus (Fall, 1901), D. bigemmeus (Horn, 1895), and D. austrinus (Gordon, 1976). Decadiomus seini Segarra, 2014 is placed as a junior synonym of D. austrinus. The following new species of Moiradiomus are described: M. clotho sp. nov., M. lachesis sp. nov., M. atopos sp. nov., M. nanita sp. nov.
References
Akbar, W., Carlton, C. & Reagan, T.E. (2009) Life cycle and larval morphology of Diomus terminatus (Coleoptera: Coccinellidae) and its potential as a biological control agent of Melanaphis sacchari (Hemiptera: Aphididae). Annals of the Entomological Society of America, 102, 96–103.
https://doi.org/10.1603/008.102.0110
Ali, M., Naqvi, A., Perveen, R., Ahmad, K. & Hussain, I. (2014) First record of the tribe Bulaeini (Coleoptera: Coccinellidae) with generic and species descriptions from Pakistan. Pakistan Journal of Zoology, 46 (5), 1475–1478.
Böving, A.G. (1933) Description of the larvae of Decadiomus pictus Chapin (Scymnini, Coccinellidae). Proceedings of the Entomological Society of Washington, 46, 101–04.
Brèthes J. (1925) Sur une collection de Coccinellides (et un Phalacridae) du British Museum. Anales del Museo de Historia Natural de Buenos Aires, 33, 145–175. [in French]
Callejas, R. (2014) Piperaceae. In: Hammel, B.E., Gayum, M.H., Herrera, C. & Zamora, N. (Eds.), Manual de Plantas de Costa Rica, Volumen VII, Dicotiledóneas (Picramniaceae - Rutaceae). Missouri Botanical Garden Press, St. Louis, Missouri, pp. 6–326. [in Spanish]
Canepari, C., Gordon, R.D. & Hanley, G.A. (2016) South American Coccinellidae (Coleoptera), Part XVII: Systematic revision of the genera Cyrea Gordon and Canepari and Tiphysa Mulsant (Hyperaspidinae: Brachiacanthini). Insecta Mundi, 0486, 1–180.
Casey, T.L. (1899) A revision of the American Coccinellidae. Journal of the New York Entomological Society, 7 (2), 71–169.
Chapin, E.A. (1933) A new genus of West Indian Coccinellidae (Coleoptera). Proceedings of the Biological Society of Washington, 46, 95–99.
Chapin, J.B. (1974) The Coccinellidae of Louisiana (Insecta: Coleoptera). Louisiana Agricultural Experiment Station Bulletin, 682, 2–87.
Chapman, R.F. (1998) The Insects. Structure and Function. 4th Edition. Cambridge University Press, Cambridge, 770 pp.
https://doi.org/10.1017/CBO9780511818202
Chazeau, J. (1987) Complement sur les Diomus de Nouvelle-Guinee et des archipels voisins (Coleoptera: Coccinellidae). Revue France d'Entomologie, Nouvelle Serie, 9, 101–113. [in French]
Chazeau, J. (1993) Diomus Neo-Guineens: nouvelles especes de Papouasie et complements sur la repartition des especes connues (Coleoptera: Coccinellidae). Annales de la Societe Entomologique de France, 29, 141–158. [in French]
Dyer, L.A., Letourneau, D.K., Williams, W. & Dodson, C. (1999) A commensalism between Piper marginatum Jacq. (Piperaceae) and a coccinellid beetle at Barro Colorado Island, Panama. Journal of Tropical Ecology, 15, 841–846.
https://doi.org/10.1017/s0266467499001212
Escalona, H.E., Zwick, A., Li, H., Wang, X., Pang, H., Hartley, D., Jermin, L.S., Nedved, O., Misof, B., Niehuis, N., Ślipiński, A. & Tomaszewska, W. (2017) Molecular phylogeny reveals food plasticity in the evolution of true ladybird beetles (Coleoptera: Coccinellidae: Coccinellini). BMC Evolutionary Biology, 17 (151), 1–11.
https://doi.org/10.1186/s12862-017-1002-3
Eizaguirre, S. (1998) Diomus (Coleoptera: Coccinellidae) un género nuevo para la fauna ibérica. Munive, Ciencias Naturales—Natur Zieutziak, 50, 43–66. [in Spanish]
Fischer, R.C., Richter, A., Wanek, W. & Mayer, V. (2002) Plants feed ants: food bodies of myrmecophytic Piper and their significance for the interaction with Pheidole bicornis ants. Oecologia, 133, 186–192.
https://doi.org/10.1007/s00442-002-1000-y
Fürsch, H. (1987) Ubersicht uber die Genera und Subgenera der Scymnini mit besonderer Berucksichtigung der Westpalaearktis (Insecta, Coleoptera, Coccinellidae). Entomologische Abhandlungen, 51 (4), 57–74. [in German]
Gastreich, K.R. & Gentry, G.L. (2004) Faunal studies in model Piper spp. systems, with a focus on spider-induced indirect interactions and novel insect-Piper mutualisms. In: Dyer, L.A. & Palmer, A.P.N. (Eds.), Piper: a Model Genus for Studies of Phytochemistry, Ecology, and Evolution. Kluwer Academic/Pelnum Publishers, New York, USA, pp. 97–116.
https://doi.org/10.1007/978-0-387-30599-8_6
Gentry, A.H. (1990) Floristic similarities and differences between southern Central America and upper Central Amazonia. In: Gentry, A.H. (Ed.), Four Neotropical rainforests. Yale University Press, New Haven, Connecticut, pp. 141–157.
Giorgi, J.A., Vandenberg, N.J., McHugh, J.V., Forrester, J.A., Ślipiński, S.A., Miller, K.B., Shapiro, L.R. & Whiting, M.F. (2009) The evolution of food preferences in Coccinellidae. Biological Control, 51, 215–231.
https://doi.org/10.1016/j.biocontrol.2009.05.019
González, G.F. (2015) Especies nuevas y nuevos registros de coccinélidos (Coleoptera: Coccinellidae) de Ecuador. Boletín de la Sociedad Entomológica Aragonesa (S.E.A.), 57, 143–163. [in Spanish]
González, G.F. (2016) Descripción de 11 especies nuevas del genera Diomus Mulsant (Coleoptera; Coccinellidae: Diomini) de America del Sur y nuevos registros para Brasil, Colombia, Ecuador y Peru. Boletín de la Sociedad Entomológica Aragonesa (S.E.A.), 59, 47–63. [in Spanish]
González, G. & Honour, R. (2011) Especies nuevas del género Diomus Mulsant (Coleoptera, Coccinellidae) de América del Sur. Boletin de la Sociedad Entomologica Aragonesa, 49, 1–14. [in Spanish]
Gordon, R.D. (1976) The Scymnini of the United States and Canada: Key to genera and revision of Scymnus, Nephus and Diomus. Bulletin of the Buffalo Society of Natural Sciences, 28, 1–362.
Gordon, R.D. (1985) The Coccinellidae (Coleoptera) of America north of Mexico. Journal of the New York Entomological Society, 93, 1–912.
Gordon, R.D. (1994) South American Coccinellidae (Coleoptera). Part IV: definition of Exoplectrinae Crotch, Azyinae Mulsant, and Coccidulinae Crotch; a taxonomic revision of Coccidulini. Revista Brasileira de Entomologia, 38, 681–775.
Gordon, R.D. (1999) South American Coccinellidae (Coleoptera), Part VI: A systematic revision of the South American Diomini, new tribe (Scymninae). Annales Zoologici, 49 (1), 1–219.
Gordon, R. D., Canepari, C. & Hanley, G.A. (2014) South American Coccinellidae (Coleoptera), Part XVI: systematic revision of Brachiacantha Dejean (Coccinellidae: Hyperaspidini). Insecta Mundi, 0390, 1–76.
Gordon, R.D. & González, G. (2003) Descriptions of the male of Heterodiomus marchali Brethes and a new species of Chilean Heterodiomus Brethes (Coleoptera: Coccinellidae: Scymninae: Diomini). Insecta Mundi, 17 (3–4), 237–239.
Gordon, R.D. & Hilburn, D.J. (1990) The Coccinellidae (Coleoptera) of Bermuda. Journal of the New York Entomological Society, 98, 265–309. [http://www.jstor.org/25009841]
Hentz, M.G. & Nuessly, G.S. (2002) Morphology and biology of Diomus terminatus (Coleoptera: Coccinellidae), a predator of Sipha flava (Homoptera: Aphidae). Florida Entomologist, 85, 276–278.
https://doi.org/10.1653/0015-4040(2002)085[0276:MABODT]2.0.CO;2
Hodek, I. & Honěk, A. (1996) Ecology of Coccinellidae. Kluwer, Dordrecht, XVI + 464 pp.
https://doi.org/10.1007/978-94-017-1349-8
Hopkinson, J.E., Kramer, S.M. & Zalucki, M.P. (2016) Developmental biology and prey preference of Diomus notescens Blackburn (Coleoptera: Coccinellidae): A predator of Aphis gossypii Glover (Hemiptera: Aphididae). Biological Control, 96, 101–107.
https://doi.org/10.1016/j.biocontrol.2016.02.006
Iablokoff-Khnzorian, S.M. (1976) Die paläarktischen Genera der Marienkäfer-Tribus Scymnini nebst Bemerkungen über Scymnus fuscatus (Coleoptera: Coccinellidae). Entomologica Germanica, 2, 374–380.
Iqbal, Z., Nasir, M.R., Bodlah, I., Qureshi, R. & Aihetasham, A. (2014) Notes on three morphs of Bulaea lichatschovii (Hummel) (Coleoptera: Coccinellidae) from Northern Pakistan. Punjab University Journal of Zoology, 32 (2), 203–208.
Jaramillo, M.A., Callejas, R., Davidson, C., Smith, J.F., Stevens, A. & Tepe, E.J. (2008) A phylogeny of the tropical genus Piper (Piperaceae) using ITS and the chloroplast intron psbJ-petA. Systematic Botany, 33, 647–660.
https://doi.org/10.1600/036364408786500244
Korschefsky, R. (1931) Pars. 118, Coccinellidae. I. In: Junk, W. & Schenkling, S. (Eds.), Coleopterorum Catalogus. W. Junk, Berlin, pp. 1–224.
Kovář, I. (1996) Morphology and anatomy. In: Hodek, I. & Honěk, A. (Eds.), Ecology of Coccinellidae. Kluwer, Dordrecht, pp. 1–18.
https://doi.org/10.1007/978-94-017-1349-8_1
Leng, C.W., Wickham, H.F. & Mutchler, A.J. (1920) Catalogue of the Coleoptera of America, north of Mexico. JD Sherman, Jr., Mount Vernon, New York, 470 pp.
Leschen, R.A.B. & Buckley, T.R. (2007) Multistate characters and diet shifts: evolution of Erotylidae (Coleoptera). Systematic Biology, 56 (1), 97–112.
https://doi.org/10.1080/10635150701211844
Letourneau, D.K. (1983) Passive aggression: an alternative hypothesis for the Piper-Pheidole association. Oecologia, 60, 122–126.
https://doi.org/10.1016/10.1007/bf00379331
Letourneau, D.K. (1990) Code of ant-plant mutualism broken by parasite. Science, 248, 215–217.
https://doi.org/10.1126/science.248.4952.215
Letourneau, D.K. (1991) Parasitism of ant-plant mutualisms and the novel case of Piper. In: Huxley, C.R. & Cutler, D.F. (Eds.) Ant-plant interactions. Oxford University Press, Oxford, pp. 390–396.
Letourneau, D.K. (1998) Ants, stem-borers, and fungal pathogens: Experimental tests of a fitness advantage in Piper ant-plants. Ecology, 79, 593–603.
https://doi.org/10.2307/176956
Mader, L. (1955) Evidenz der paläarktischen Coccinelliden und ihrer Aberrationen in Wort und Bild. 2. Entomologische Arbeiten aus dem Museum G. Frey Tutzing bei Muenchen, 6, 765–1035. [in German]
Magro, A., Lecompte, E., Magne, F., Hemptinne, J. & Crouau-Roy, B. (2010) Phylogeny of ladybirds (Coleoptera: Coccinellidae): are the subfamilies monophyletic? Molecular Phylogenetics and Evolution, 54, 833–848.
https://doi.org/10.1016/j.ympev.2009.10.022
Meyerdirk, D.E. (1983) Biology of Diomus flavifrons (Blackburn) (Coleoptera: Coccinellidae), a citrus mealybug predator. Environmental Entomology, 12, 1275–1277.
https://doi.org/10.1093/ee/12.4.1275
Moser, S.E., Harwood, J.D. & Obrycki, J.J. (2008) Larval feeding on Bt hybrid and non-Bt corn seedlings by Harmonia axyridis (Coleoptera: Coccinellidae) and Coleomegilla maculata (Coleoptera: Coccinellidae). Environmental Entomology, 37 (2), 525–533.
https://doi.org/10.1603/0046-225x(2008)37[525:lfobha]2.0.co;2
Obrycki, J.J. & Kring, T.J. (1998) Predaceous Coccinellidae in biological control. Annual Review of Entomology, 43, 295–321.
https://doi.org/10.1146/annurev.ento.43.1.295
Paiva, E.A.S., Buono, R.A. & Lombardi, J.A. (2009) Food bodies in Cissus verticillata (Vitaceae): ontogenesis, structure and functional aspects. Annals of Botany, 103, 517–524.
https://doi.org/10.1093/aob/mcn237
Pang, H., Shunxiang, R., Zeng, T. & Pang, X. (2004) Species diversity and utilization of Coccinellidae in China. Science and Technology Press of Guangdong, Guangzhou, 168 + xxiv pp. [in Chinese]
Pang, X.F. & Gordon, R.D. (1986) The Scymnini (Coleoptera: Coccinellidae) of China. The Coleopterists Bulletin, 40 (2), 157–199.
Pang, H. & Ślipiński, A. (2009) Revision of the Australian Coccinellidae (Coleoptera). genus Diomus Mulsant. Part 1. Annales Zoologici, 59 (4), 641–698.
https://doi.org/10.3161/000345409x485008
Pang, H. & Ślipiński, A. (2010) Revision of the Australian Coccinellidae (Coleoptera). Genus Diomus Mulsant. Part 2. Annales Zoologici, 60 (4), 645–702.
https://doi.org/10.3161/000345410X550382
Poorani, J. (2002) An annotated checklist of the Coccinellidae (Coleoptera) (excluding Epilachninae) of the Indian subregion. Oriental Insects, 36, 307–383.
https://doi.org/10.1080/00305316.2002.10417335
Peck, S.B. (2016) The beetles of the Lesser Antilles (Insecta, Coleoptera): diversity and distributions. Insecta Mundi, 0460, 1–360.
Peck, S.B. & Thomas, M.C. (1998) A distributional checklist of the beetles (Coleoptera) of Florida. Arthropods of Florida and Neighboring Land Areas, 16, 1–80.
https://doi.org/10.2307/3495846
Quijano-Abril, M.A., Callejas, R. & Miranda-Esquivel, D.R. (2006) Areas of endemism and distribution patterns for Neotropical Piper species (Piperaceae). Journal of Biogeography, 33, 1266–1278.
https://doi.org/10.1111/j.1365-2699.2006.01501.x
Rees, B.E., Anderson, D.M., Bouk, D. & Gordon, R.D. (1994) Larval key to genera and selected species of North American Coccinellidae (Coleoptera). Proceedings of the Entomological Society of Washington, 96, 387–412.
Rickson, F.R. & Risch, S.J. (1984) Anatomical and ultrastructural aspects of the ant-food cell of Piper cenocladium C.DC (Piperaceae). American Journal of Botany, 71 (9), 1268–1274.
https://doi.org/10.2307/2443651
Risch, S.J. (1982) How Pheidole ants help Piper plants. Brenesia, 19 (20), 545–548.
Risch, S.J. & Rickson, F.R. (1981) Mutualism in which ants must be present before plants produce food bodies. Nature, 291, 149–150.
https://doi.org/10.1038/291149a0
Risch, S., McClure, M., Vandermeer, J. & Waltz., S. (1977) Mutualism between three species of tropical Piper (Piperaceae) and their ant inhabitants. American Midland Naturalist, 98, 433–444.
https://doi.org/10.2307/2424991
Robertson, J.A., Ślipiński, A., Moulton, M., Shockley, F.W, Giorgi, A., Lord, N.P., McKenna, D.D., Tomaszewska, W., Forrester, J., Miller, K.B., Whiting, M.F. & McHugh, J.V. (2015) Phylogeny and classification of Cucujoidea and the recognition of a new superfamily Coccinelloidea (Coleoptera: Cucujiformia). Systematic Entomology, 40, 745–778.
https://doi.org/10.1111/syen.12138
Samways, M.J., Osborn, R. & Saunders, T.L. (1997) Mandible form relative to the main food type in ladybirds (Coleoptera: Coccinellidae). Biocontrol Science and Technology, 7, 275–286.
https://doi.org/10.1080/09583159730974
Sasaji, H. (1968) Phylogeny of the family Coccinellidae (Coleoptera). Etizenia, Occasional Publications of the Biological Laboratory, Fukui University, 35, 1–37.
Schupp, E.W. & Feener, D.H. (1991) Phylogeny, lifeform, and habitat dependence of ant-defended plants in a Panamanian forest. In: Huxley, C. & Cutler, D.F. (Eds.) Ant-Plant Interactions. Oxford University Press, Oxford, pp. 175–197.
https://doi.org/10.1017/s0007485300051579
Seago, A.E., Giorgi, J.A., Li, J.& Ślipiński, A. (2011) Phylogeny, classification and evolution of ladybird beetles (Coleoptera: Coccinellidae) based on simultaneous analysis of molecular and morphological data. Molecular Phylogenetics and Evolution, 60 (1), 137–151.
https://doi.org/10.1016/j.ympev.2011.03.015
Segarra-Carmona, A.E. & Otero, M. (2014) Four new ladybug species belonging to Decadiomus Chapin (Coleoptera: Coccinellidae) from Puerto Rico. Neotropical Entomology, 43 (6), 555–563.
https://doi.org/10.1007/s13744-014-0243-8
Ślipiński, S.A. (2007) Australian ladybird beetles (Coleoptera: Coccinellidae). Their biology and classification. ABRS, Canberra, 288 pp.
Sutherland, T.D., Young, J.H., Weisman, S., Hayashi, C.Y. & Merritt, D.J. (2010) Insect silk: one name, many materials. Annual Review of Entomology, 55, 171–188.
https://doi.org/10.1146/annurev-ento-112408-085401
Tepe, E.J., Vincent, M.A. & Watson, L.E. (2007a) Stem diversity, cauline domatia, and the evolution of ant-plant associations in Piper section Macrostachys (Piperaceae). American Journal of Botany, 94, 1–11.
https://doi.org/10.3732/ajb.94.1.1
Tepe, E.J., Vincent, M.A. & Watson, L.E. (2007b) The importance of petiole structure on inhabitability by ants in Piper section Macrostachys (Piperaceae). Botanical Journal of the Linnean Society, 153, 181–191.
https://doi.org/10.1111/j.1095-8339.2006.00601.x
Vandenberg, N.J. (2002) Coccinellidae Latreille 1807. In: Arnett, R.H. Jr., Thomas, M.C., Skelley, P.E. & Frank, J.H. (Eds.), American Beetles. CRC Press, Boca Raton, pp. 371–389.
Vandenberg, N.J. & Perez-Gelabert, D.E. (2007) Redescription of the Hispaniolan ladybird genus Bura Mulsant (Coleoptera: Coccinellidae) and justification for its transfer from Coccidulinae to Sticholotidinae. Zootaxa, 1586 (1), 39–46.
https://doi.org/10.11646/zootaxa.1586.1.4
Vandenberg, N.J., Iverson, A. & Liere, H. (2018) A new species of myrmecophilous lady beetle in the genus Diomus (Coleoptera: Coccinellidae: Diomini) from Chiapas, Mexico that feeds on green coffee scale, Coccus viridis (Green) (Hemiptera: Coccidae). Zootaxa, 4420 (1), 113–122.
https://doi.org/10.11646/zootaxa.4420.1.6
Vantaux, A., Roux, O., Magro, A., Ghomsi, N.T., Gordon, R.D., Dejean, A. & Orivel, J. (2010) Host-Specific Myrmecophily and Myrmecophagy in the Tropical Coccinellid Diomus thoracicus in French Guiana. Biotropica, 42, 622–629.
https://doi.org/10.1111/j.1744-7429.2009.00614.x
Weise, J. (1895) Neue Coccinelliden, sowie Bemerkungen zu bekannten Arten. Annales de la Sociéte Entomologie Belgique, 39,120–146. [in German]
Weise, J. (1923) Results of Dr. E. Mjöberg's Swedish Scientific Expedition to Australia 1910–1913. 31. Chrysomeliden und Coccinelliden aus Queensland. Arkiv för Zoologi, 15 (12), 1–150.
Whitehead, V.B. (1967) The validity of the higher taxonomic categories of the tribe Scymnini (Coleoptera: Coccinellidae). Dissertation, Doctor of Philosophy in Entomology, University of California, Berkeley, 312 pp. [unpublished thesis]
Wingo, C.W. (1952) The Coccinellidae (Coleoptera) of the upper Mississippi Basin. Iowa State Journal of Science, 27, 15–53.