Integrative taxonomy of Acrapex stem borers (Lepidoptera : Noctuidae : Apameini): combining morphology and Poisson Tree Process analyses
Bruno P. Le Ru A B N , Claire Capdevielle-Dulac B , Emmanuel F. A. Toussaint C , Desmond Conlong D E , Johnnie Van den Berg F , Beatrice Pallangyo G , George Ong’amo H , Gilson Chipabika I , Richard Molo J , William A. Overholt K , James P. Cuda L and Gael J. Kergoat M
+ Author Affiliations
- Author Affiliations
A Unité de Recherche IRD 072, icipe-African Insect Science for Food and Health, PO Box 30772, Nairobi, Kenya.
B Unité de Recherche IRD 072, Laboratoire Evolution, Génomes et Spéciation, UPR 9034, 22 CNRS, 91198 – Gif/Yvette, France and Université Paris-Sud 11, 91405 – Orsay, France.
C Zoological State Collection, Münchhausenstraße 21, 81247 – Munich, Germany.
D South African Sugarcane Research Institute, Private Bag X02, Mount Edgecombe, 4300, South Africa.
E School of Biological and Conservation Sciences, University of Kwazulu–Natal, Private Bag X01, Scottsville, Pietermaritzburg, South Africa.
F School of Environmental Sciences and Development, North West University (Potchefstroom Campus), Private Bag X6001, Potchefstroom, 2520, South Africa.
G Biocontrol Programme, PO Box 30031, Kibaha, Tanzania.
H School of Biological Science, College of Physical and Biological Sciences (Chiromo Campus), University of Nairobi, P. O. Box 30197, Nairobi, Kenya.
I Zambia Agriculture Research Institute, Mount Maluku Central Research Station, PO Box 8, Chilanga, Zambia.
J Namulonge Agricultural and Animal Production Research Institute (NAARI), PO Box 7084, Kampala, Uganda.
K Indian River Research and Education Center, University of Florida, Fort Pierce, FL 34945, USA.
L Department of Entomology and Nematology, University of Florida, Gainesville, FL 32611, USA.
M INRA, UMR 1062 CBGP (INRA, IRD, CIRAD, Montpellier SupAgro, Campus de Baillarguet, 34988 Montferrier/Lez, France.
N Corresponding author. Email: bleru@icipe.org
Invertebrate Systematics 28(5) 451-475 https://doi.org/10.1071/IS13062
Submitted: 17 December 2013 Accepted: 16 May 2014 Published: 13 November 2014
Journal Compilation © CSIRO Publishing 2014 Open Access CC BY-NC-ND
Abstract
Ten morphologically similar species of Acrapex from eastern and south-eastern Africa belonging to the A. stygiata and A. albivena groups are reviewed. Six species are described as new: A. brunneella, A. mitiwa, A. mpika, A. salmona, A. sporobola and A. yakoba. The Poaceae host plants of eight species are recorded; four species, A. mitiwa. A. subalbissima, A. syscia and A. yakoba, were found developing exclusively on Imperata cylindrica (L.) Beauv., (Andropogoneae); two species, A. sporobola and A. salmona, on I. cylindrica and Sporobolus macranthelus Chiov. (Zoysieae); and A. albivena on I. cylindrica, Miscanthus capensis (Nees) Andersson (Andropogoneae) and Cymbopogon sp. (Andropogoneae). Acrapex stygiata larvae developed on M. capensis and Cymbopogon sp. The host plants of A. brunneella and A. mpika remain unknown. We also conducted molecular phylogenetics and molecular species delimitation analyses on a comprehensive sample of 49 specimens belonging to nine of the studied species. Molecular phylogenetics and molecular species delimitation analyses provided additional evidence of the validity of the six newly described species but also suggested a level of hidden biodiversity for one of them.
Additional keywords: Acrapex, Imperata cylindrica, molecular phylogenetics, molecular species delimitation, Noctuidae, phylogenetics, Poaceae.
References
Berio, E. (1973). Nuove species e generi di noctuidae africane e asiatiche e note sinonimiche. Parte II. Annali del museo civico di storia naturale, Giacomo doria 79, 126–171.Berio, E. (1976). Nuovi generi e specie di noctuidae dell‘Africa equatoriale. Annali del Museo civico di storia naturale, Giacomo doria 81, 96–123.
Bernays, E. A. (1985). Arthropods for weed control in IPM systems. In ‘Biological Control in Agricultural Integrated Pest Management Systems’ . (Eds M. A. Hoy, D. C. Herzog.) pp. 373–391. (Academic Press: Burlington, MA.)
Dayrat, B. (2005). Toward integrative taxonomy. Biological Journal of the Linnean Society. Linnean Society of London 85, 407–415.
| Toward integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |
Diaz, R., Overholt, W., Cuda, J., Pratt, P., and Fox, A. (2009). Host specificity of Ischnodemus variegatus, an herbivore of West Indian marsh grass (Hymenachne amplexicaulis). BioControl 54, 307–321.
| Host specificity of Ischnodemus variegatus, an herbivore of West Indian marsh grass (Hymenachne amplexicaulis).Crossref | GoogleScholarGoogle Scholar |
Diaz, R., Overholt, W. A., Heard, T. A., Van Klinken, R., and Samayoa, A. (2010). Life history parameters of Ischnodemus variegatus (Signoret) (Hemiptera: Blissidae) reared on two closely related grasses. Biological Control 55, 219–224.
| Life history parameters of Ischnodemus variegatus (Signoret) (Hemiptera: Blissidae) reared on two closely related grasses.Crossref | GoogleScholarGoogle Scholar |
Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
| Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=beec25ccf0d2a98903aa512fd45babe5CAS | 22367748PubMed |
Edgar, R. C. (2004). MUSCLE : a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 1–19.
Erixon, P., Svennblad, B., Britton, T., and Oxelman, B. (2003). Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics. Systematic Biology 52, 665–673.
| Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenetics.Crossref | GoogleScholarGoogle Scholar | 14530133PubMed |
Felix, A.-E., Calatayud, P.-A., Le Ru, B., Capdevielle-Dulac, C., Ong’amo, G., Silvain, J.-F., and Frerot, B. (2013). To be or not to be a species: use of reproductive isolation experiments and genetic analysis to clarify the taxonomic status of two Busseola (Lepidoptera: Noctuidae) species in Kenya. Annales de la Société Entomologique de France 49, 345–354.
Fletcher, D. S. (1961). ‘Noctuidae. Ruwenzori Expedition 1952.’ Vol. 1, pp. 177–323. British Museum (Natural History), London.
Gaede, M. (1935). Noctuidae. In ‘Die Gross-Schmetterlinge der Erde. Macrolepidoptera of the world. a systematic description of the hitherto known Macrolepidoptera. A systematic description of the hitherto known Macrolepidoptera’. (Ed. A. Seitz.) Die Afrikanischen Spinner und Schwärmer. xv. p. 95, pl. 10.
Goolsby, J. A., and Moran, P. (2009). Host range of Tetramesa romana (Hymenoptera: Eurytomidae), a potential biological control agent of giant reed, Arundo donax L. in North America. Biological Control 49, 160–168.
| Host range of Tetramesa romana (Hymenoptera: Eurytomidae), a potential biological control agent of giant reed, Arundo donax L. in North America.Crossref | GoogleScholarGoogle Scholar |
Goolsby, J. A., Moran, P. J., Adamczyk, J. J., Kirk, A. A., Jones, W. A., Marcos, M. A., and Cortés, E. (2009). Host range of the European, rhizome-stem feeding scale Rhizaspidiotus donacis (Hemiptera: Diaspididae), a candidate biological control agent for giant reed, Arundo donax (Poales: Poaceae) in North America. Biocontrol Science and Technology 19, 899–918.
| Host range of the European, rhizome-stem feeding scale Rhizaspidiotus donacis (Hemiptera: Diaspididae), a candidate biological control agent for giant reed, Arundo donax (Poales: Poaceae) in North America.Crossref | GoogleScholarGoogle Scholar |
Grevstad, F. S., Strong, D. R., Garcia-Rossi, D., Switzer, R. W., and Wecker, M. S. (2003). Biological control of Spartina alterniflora in Willapa Bay, Washington using the planthopper Prokelisia marginata: agent specificity and early results. Biological Control 27, 32–42.
| Biological control of Spartina alterniflora in Willapa Bay, Washington using the planthopper Prokelisia marginata: agent specificity and early results.Crossref | GoogleScholarGoogle Scholar |
Hampson, G. F. (1910). ‘Catalogue of the Noctuidae in the Collection of the British Museum.’ (Taylor and Francis: London.)
Hillis, D. M., and Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182–192.
| An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |
Holm, L. G., Donald, P., Pancho, J. V., and Herberger, J. P. (1977). ‘The World’s Worst Weeds: Distribution and Biology.’ (The University Press of Hawaii: Honolulu, Hawaii.)
Holzmueller, E. G., and Jose, S. (2011). Invasion success of cogongrass, an alien C4 perennial grass, in the Southeastern United States: Exploration of the ecological basis. Biological Invasions 13, 435–442.
| Invasion success of cogongrass, an alien C4 perennial grass, in the Southeastern United States: Exploration of the ecological basis.Crossref | GoogleScholarGoogle Scholar |
Janse, A. J. T. (1939). The Moths of South Africa. Cymatophoridae, Callidulidae and Noctuidae (partim). Vol. 3, pp. 307–435. (E.P. and Commercial Printing Co. Ltd: Durban.)
Jose, S., Cox, J., Miller, D. L., Shilling, D. G., and Merit, S. (2002). Alien plant invasions: the story of cogongrass in Southeastern forests. Journal of Forestry 100, 41–44.
Kergoat, G. J., Prowell, D. P., Le Ru, B. P., Mitchell, A., Dumas, P., Clamens, A.-L., Condamine, F. L., and Silvain, J.-F. (2012). Disentangling dispersal and vicariance patterns in armyworms: evolution and historical biogeography of the pest genus Spodoptera (Lepidoptera: Noctuidae). Molecular Phylogenetics and Evolution 65, 855–870.
| Disentangling dispersal and vicariance patterns in armyworms: evolution and historical biogeography of the pest genus Spodoptera (Lepidoptera: Noctuidae).Crossref | GoogleScholarGoogle Scholar | 22939903PubMed |
Kfir, R., Overholt, W. A., Khan, Z. R., and Polaszek, A. (2002). Biology and management of economically important lepidopteran cereal stem borers in Africa. Annual Review of Entomology 47, 701–731.
| Biology and management of economically important lepidopteran cereal stem borers in Africa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVKqtQ%3D%3D&md5=c20f0d066a1470f8778bae94e1ea2144CAS | 11729089PubMed |
Laporte, B. (1975). Diagnoses de 17 nouvelles espèces de Noctuidae d’Ethiopie et du Kenya (Lepidoptères). Bulletin de la Société Linnéenne de Lyon 8, 277–287.
Laporte, B. (1984). Noctuidae in Rougeot, P.-C. (Ed.) Missions Entomologiques en Ethiopie 1976–1982. Mémoires du Museum National d’Histoire Naturelle (Nouvelle Série) 128, 12–51.
Le Ru, B. P., Ong’amo, G. O., Moyal, P., Muchungu, E., Ngala, L., Musyoka, L., Abdullah, B., Kauma, Z., Matama, T., Lada, V. Y., Pallangyo, K., Sidumo, A., Omwega, C., Schulthess, F., Calatayud, P.-A., and Silvain, J.-F. (2006a). Major ecological characteristics of East African noctuid stem borers. Annales de la Société Entomologique de France 42, 353–362.
Le Ru, B., Ong’amo, G. O., Moyal, P., Ngala, L., Musyoka, B., Abdullah, Z., Cugala, D., Defabachew, B., Haile, T. A., Kauma Matama, T., Lada, V. Y., Negassi, B., Pallangyo, K., Ravololonandrianina, J., Sidumo, A., Omwega, C., Schulthess, F., Calatayud, P.-A., and Silvain, J.-F. (2006b). Diversity of lepidopteran stem borers on monocotyledonous plants in eastern Africa and the islands of Madagascar and Zanzibar revisited. Bulletin of Entomological Research 96, 555–563.
| Diversity of lepidopteran stem borers on monocotyledonous plants in eastern Africa and the islands of Madagascar and Zanzibar revisited.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s%2Fgs1arsQ%3D%3D&md5=a4a1da8f9e35847ce9349c0cfacf35afCAS | 17201973PubMed |
Lim, G. S., Balke, M., and Meier, R. (2012). Determining species boundaries in a world full of rarity: singletons, species delimitation methods. Systematic Biology 61, 165–169.
| Determining species boundaries in a world full of rarity: singletons, species delimitation methods.Crossref | GoogleScholarGoogle Scholar | 21482553PubMed |
Lohse, K. (2009). Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006). Systematic Biology 58, 439–442.
| Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006).Crossref | GoogleScholarGoogle Scholar | 20525596PubMed |
Mangoendihardjo, S. (1980). Some notes on the natural enemies of Alang-alang (Imperata cylindrica (L.) Beauv.) in Java. In ‘Proceedings of BTROP Workshop on Alang-alang, Bogor, Indonesia, 27–29 July 1976’. (Ed. B. Soewardi.) pp. 47–55. (BIOTROP SEAMO Regional Center for Tropical Biology: Bogor, Indonesia.)
Massey, F. P., Ennos, A. R., and Hartley, S. E. (2006). Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder. Journal of Animal Ecology 75, 595–603.
| Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder.Crossref | GoogleScholarGoogle Scholar | 16638012PubMed |
Moyal, P. (2006). History of the systematics of the Sesamia sensu lato group of African Noctuid stem borers of monocotyledonous plants (Lepidoptera). Annales de la Société Entomologique de France 42, 285–291.
| History of the systematics of the Sesamia sensu lato group of African Noctuid stem borers of monocotyledonous plants (Lepidoptera).Crossref | GoogleScholarGoogle Scholar |
Moyal, P., Le Ru, B., Conlong, D., Cugala, D., Defabachew, B., Matama-Kauma, T. B., Pallangyo, B., and ‘, J. (2010). Systematics and molecular phylogeny of two African stem borer genera, Sciomesa Tams and Bowden and Carelis Bowden (Lepidoptera: Noctuidae). Bulletin of Entomological Research 100, 641–659.
| Systematics and molecular phylogeny of two African stem borer genera, Sciomesa Tams and Bowden and Carelis Bowden (Lepidoptera: Noctuidae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbkslKqtA%3D%3D&md5=cc9f1e8fbb7d6e99b4a44b3583bf9ef1CAS | 20576171PubMed |
Moyal, P., Tokro, P., Bayram, A., Savopoulou-Soultani, M., Conti, E., Eizaguirre, M., Le Ru, B., Avand-Faghih, A., and Andreadis, S. (2011). Origin and taxonomic status of the Palearctic population of the stem borer Sesamia nonagrioides (Lefèbvre) (Lepidoptera: Noctuidae). Biological Journal of the Linnean Society. Linnean Society of London 103, 904–922.
| Origin and taxonomic status of the Palearctic population of the stem borer Sesamia nonagrioides (Lefèbvre) (Lepidoptera: Noctuidae).Crossref | GoogleScholarGoogle Scholar |
Nylander, J. A. A., Ronquist, F., Huelsenbeck, J. P., and Nieves-Aldrey, J. L. (2004). Bayesian phylogenetic analysis of combined data. Systematic Biology 53, 47–67.
| Bayesian phylogenetic analysis of combined data.Crossref | GoogleScholarGoogle Scholar |
Onyango, F. O., and Ochieng’Odero, J. P. R. (1994). Continuous rearing of the maize stem borer Busseola fusca on an artificial diet. Entomologia Experimentalis et Applicata 73, 139–144.
| Continuous rearing of the maize stem borer Busseola fusca on an artificial diet.Crossref | GoogleScholarGoogle Scholar |
Padial, J. M., Miralles, A., De la Riva, I., and Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology 7, 16.
| The integrative future of taxonomy.Crossref | GoogleScholarGoogle Scholar | 20500846PubMed |
Papadopoulou, A., Bergsten, J., Fujisawa, T., Monaghan, M. T., Barraclough, T. G., and Vogler, A. P. (2008). Speciation and DNA barcodes: testing the effects of dispersal on the formation of discrete sequence clusters. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 2987–2996.
| Speciation and DNA barcodes: testing the effects of dispersal on the formation of discrete sequence clusters.Crossref | GoogleScholarGoogle Scholar | 18522916PubMed |
Pemberton, R. W. (2002). Selection of appropriate future target weeds for biological control. In ‘Biological Control of Invasive Plants in the Eastern United States’. (Eds R. Van Driesche, S. Lyon, B. Blossey, M. Hoddle and R. Reardon.) pp. 375–86. USDA Forest Service Publication FHTET-2002–04.
Pierce, F. N. (1942). The genitalia of the group Noctuidae of the Lepidoptera of the British Islands. (Female). (Classey, Farringdon).
Poole, R. W. (1989). Noctuidae; Lepidopterorum catalogus (Lepidopterorum Catalogus New Series, Fasc. 118), Part 1 and 2).
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=a227fa0ae4120a3a8c06cab96986f12aCAS | 18397919PubMed |
Posada, D., and Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793–808.
| Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests.Crossref | GoogleScholarGoogle Scholar | 15545256PubMed |
Riedel, A., Sagata, K., Suhardjono, Y. R., Tänzler, R., and Balke, M. (2013). Integrative taxonomy on the fast track – towards more sustainability in biodiversity research. Frontiers in Zoology 10, 15.
| Integrative taxonomy on the fast track – towards more sustainability in biodiversity research.Crossref | GoogleScholarGoogle Scholar | 23537182PubMed |
Schlick-Steiner, B. C., Steiner, F. M., Seifert, B., Stauffer, C., Christian, E., and Crozier, R. H. (2010). Integrative taxonomy: a multisource approach to exploring Biodiversity. Annual Review of Entomology 55, 421–438.
| Integrative taxonomy: a multisource approach to exploring Biodiversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVShtQ%3D%3D&md5=225cd409618e3867a1f7bfe80eed831aCAS | 19737081PubMed |
Stamatakis, A. (2006). RaxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RaxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=b0df768ad6679df0c2d42f77d14048ddCAS | 16928733PubMed |
Strand, E. (1916). Neue Nebenformen exotischer Heterocera. Archiv für Naturgeschichte 82, 147–157.
Swezey, O. H. (1927). Insect fauna of Panicum torridum, a native grass in Hawaii. Proceeding of the of the Hawaii Entomological Society 7, 179–182.
Takasu, K., Yoshiyasu, Y., Burrell, A. M., Klein, P. E., Racelis, A., Goosby, J. A., and Overholt, W. A. (2014). Acrapex azumai Sugi (Lepidoptera: Noctuidae) as a possible biological control agent of the invasive weed Imperata cylindrica (L.) Beauv. (Poaceae) in the United States. Lepidoptera Science 65, .
Tams, W. H. T., and Bowden, J. (1953). A revision of the African species of Sesamia Guenée and related genera (Agrotidae-Lepidoptera). Bulletin of Entomological Research 43, 645–679.
Tewksbury, L., Casagrande, R., Blossey, B., Häfliger, P., and Schwarzländer, M. (2002). Potential for biological control of Phragmites australis in North America. Biological Control 23, 191–212.
| Potential for biological control of Phragmites australis in North America.Crossref | GoogleScholarGoogle Scholar |
Toussaint, E. F. A., Condamine, F. L., Kergoat, G. J., Silvain, J.-F., Capdevielle-Dulac, C., Barbut, J., and Le Ru, B. P. (2012). Palaeoenvironmental shifts drove the adaptive radiation of a noctuid stemborer tribe (Lepidoptera, Noctuidae, Apameini) in the Miocene. PLoS ONE 7, e41377.
| Palaeoenvironmental shifts drove the adaptive radiation of a noctuid stemborer tribe (Lepidoptera, Noctuidae, Apameini) in the Miocene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFGgtr7N&md5=ddd26eb09f81a29b30f37e931c467ecbCAS |
Tscharntke, T., and Greiler, H. J. (1995). Insect communities, grasses, and grasslands. Annual Review of Entomology 40, 535–558.
| Insect communities, grasses, and grasslands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtVWlt7k%3D&md5=60bf9a11eb71bc1abaf5d5da9b983f23CAS |
Wapshere, A. J. (1990). Biological control of grass weeds in Australia: an appraisal. Plant Protection Quarterly 5, 62–75.
White, F. (1983). The vegetation of Africa, a descriptive memoir to accompany the UNESCO/AETFAT/UNSO vegetation map of Africa. UNESCO. Natural Resources Research 20, 1–356.
| 1:STN:280:DC%2BD283pvVGquw%3D%3D&md5=c721a66331721ee5787e5afd2577d7a2CAS |
Will, W. W., Mishler, B. D., and Wheeler, Q. D. (2005). The perils of DNA Barcoding and the need for integrative taxonomy. Systematic Biology 54, 844–851.
| The perils of DNA Barcoding and the need for integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |
Zhang, J., Kapli, P., Pavlidis, P., and Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics , .
| A general species delimitation method with applications to phylogenetic placements.Crossref | GoogleScholarGoogle Scholar | 24344194PubMed |
