A newly recognised species that has been confused with the global polyphagous pest scale insect, Coccus hesperidum Linnaeus (Hemiptera: Coccomorpha: Coccidae)

YEN-PO LIN; HIROTAKA TANAKA; LYN G. COOK

doi:10.11646/zootaxa.4320.3.10

Issue: Vol. 4320 No. 3: 18 Sept. 2017

Type: Article

Published: 2017-09-18

DOI: 10.11646/zootaxa.4320.3.10

Page range: 571–591

Abstract views: 136

PDF downloaded: 104

**A newly recognised species that has been confused with the global polyphagous pest scale insect, Coccus hesperidum Linnaeus (Hemiptera: Coccomorpha: Coccidae)**

YEN-PO LIN⁺⁻
HIROTAKA TANAKA⁺⁻
LYN G. COOK⁺⁻

Arthropod Ecology and Biological Control Research Group, Ton Duc Thang University, Ho Chi Minh City, Vietnam Faculty of Applied Sciences, Ton Duc Thang University, Ho Chi Minh City, Vietnam

Faculty of Agriculture, Ehime University, Tarumi 3-5-7, Matsuyama, Ehime 790-8566, Japan.

The University of Queensland, School of Biological Sciences, Brisbane, QLD 4072, Australia.

Hemiptera brown soft scale Coccoidea DNA barcode asexual species coalescent species delimitation

PDF (4MB)

Abstract

Coccus hesperidum L. (Hemiptera: Coccomorpha: Coccidae), the type species of the soft scale genus Coccus L., the family Coccidae and the whole of the scale insects (Coccoidea), is a cosmopolitan plant pest. Using DNA sequence data and morphological comparisons, we determine that there is a distinct species that is morphologically very similar to C. hesperidum. Here, we describe the species as Coccus praetermissus Lin & Tanaka sp. n., based on adult female specimens from Australia, Malaysia and Thailand. The adult female of C. praetermissus sp. n. differs from C. hesperidum in having dorsal setae with bluntly rounded tips, whereas they are sharply pointed in C. hesperidum. A detailed description of the newly recognised species is provided, incorporating adult female morphology and DNA sequences from mitochondrial and nuclear loci. Our examination of slides from The Natural History Museum, London, and several Australian institutions indicates that C. praetermissus sp. n. has been confused sometimes with C. hesperidum s. s. These findings have potential relevance to plant biosecurity and quarantine because C. hesperidum is cosmopolitan whereas C. praetermissus sp. n., which is also polyphagous and the two species can share many host plants, currently appears to be more geographically restricted. Additionally, there is deep genetic divergence within C. praetermissus sp. n. that might indicate that it is a cryptic species complex, but wider geographic sampling is required to test this possibility.

References

Avasthi, R.K. & Shafee, S.A. (1991) Revision of the genus Coccus Linn. in India (Insecta, Homoptera, Coccidae). Journal of the Bombay Natural History Society, 88, 329–348.
Ben-Dov, Y. (1976) Lecanium acuminatum Signoret, 1873 (Insecta, Homoptera, Coccidae): request for designation of a neotype under the plenary powers. Z.N. (S.) 2119. Bulletin of Zoological Nomenclature, 32, 256–260.
Ben-Dov, Y. (1993) A Systematic Catalogue of the Soft Scale Insects of the World. Sandhill Crane Press, Gainesville, Florida, 536 pp.
Ben-Dov, Y. & Hodgson, C.J. (1997) 1.4 Techniques. In: Y. Ben-Dov, Y. & Hodgson, C.J. (Eds.), Soft Scale Insects: Their Biology, Natural Enemies and Control, Vol. 7A. World Crop Pests. Elsevier Science B. V., Amsterdam, pp. 389–395.
Blair, C.A., Blackith, R.E. & Boratyński, K. (1964) Variation in Coccus hesperidum L. (Homoptera: Coccidae). Proceedings of the Royal Entomological Society of London. Series A, General Entomology, 39, 129–134.
https://doi.org/10.1111/j.1365-3032.1964.tb00801.x
Brower, A.V.Z. & DeSalle, R. (1998) Patterns of mitochondrial versus nuclear DNA sequence divergence among nymphalid butterflies: the utility of wingless as a source of characters for phylogenetic inference. Insect Molecular Biology, 7, 73–82.
https://doi.org/10.1046/j.1365-2583.1998.71052.x
Causton, C.E., Peck, S.B., Sinclair, B.J., Roque-Albelo, L., Hodgson, C.J. & Landry, B. (2006) Alien insects: threats and implications for conservation of Galápagos Islands. Annals of the Entomological Society of America, 99, 121–143.
https://doi.org/10.1603/0013-8746(2006)099[0121:AITAIF]2.0.CO;2
Cho, S., Mitchell, A., Regier, J.C., Mitter, C., Poole, R.W., Friedlander, T.P. & Zhao, S. (1995) A highly conserved nuclear gene for low-level phylogenetics: Elongation Factor-1α recovers morphology-based tree for heliothine moths. Molecular Biology and Evolution, 12, 650–656.
Cockerell, T.D.A. (1893a) Notes on Lecanium, with a list of the West Indian species. Transactions of the American Entomological Society, 20, 49–56.
Cockerell, T.D.A. (1893b) A list of West Indian Coccidae. Journal of the Institute of Jamaica, 1, 252–256.
Cockerell, T.D.A. (1896) Preliminary diagnoses of new Coccidae. Psyche, 7 (Supplement), 18–21.
https://doi.org/10.1155/1896/92937
Cockerell, T.D.A. (1897) Notes on new Coccidae. 1. A new coccid pest of greenhouses. 2. A Japanese coccid quarantined at San Francisco. Psyche, 8, 52–53.
https://doi.org/10.1155/1897/86590
De Lotto, G. (1959) Further notes on Ethiopian species of the genus Coccus (Homoptera: Coccoidea: Coccidae). Journal of the Entomological Society of Southern Africa, 22, 150–173.
De Queiroz, K. (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard, D.J. & Berlocher, S.H. (Eds.), Endless Forms: Species and Speciation. Oxford University Press, Oxford, pp. 57–75.
Douglas, J.W. (1886) Note on some British Coccidae (No. 4). Entomologist’s Monthly Magazine, 23, 77–82.
https://doi.org/10.5962/bhl.part.18588
Dowton, M. & Austin, A.D. (1998) Phylogenetic relationships among the microgastroid wasps (Hymenoptera: Braconidae): combined analysis of 16S and 28S rDNA genes and morphological data. Molecular Phylogenetics and Evolution, 10, 354–366.
https://doi.org/10.1006/mpev.1998.0533
Drummond, A. & Rambaut, A. (2006) Analysing BEAST Output. Available from: http://beast.bio.ed.ac.uk/analysing-beast-output (accessed 8 May 2016).
Ehrhorn, E.M. (1898) New Coccidae. The Canadian Entomologist, 30, 244–246.
https://doi.org/10.4039/Ent30244-9
Fernald, M.E. (1903) A catalogue of the Coccidae of the world. Bulletin of the Hatch Experiment Station of the Massachusetts Agricultural College, 88, 1–360.
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
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. Available from: http://scalenet.info (accessed 8 August 2016)
Gavrilov-Zimin, I.A. (2013) New scale insects (Homoptera: Coccinea) from Sulawesi and New Guinea, with some other additions to the Indonesian fauna. Tropical Zoology, 26, 64–86.
https://doi.org/10.1080/03946975.2013.807570
Gennadius, P. 1895. Sur deux nouvelles cochenilles du caroubier dans l'Ile de Chypre (Hem.). Annales de la Société Entomologique de France, 64, cclxxvii.
Giliomee, J.H. (1967) Morphology and taxonomy of adult males of the family Coccidae (Homoptera: Coccoidea). Bulletin of the British Museum (Natural History), Entomology Supplement, 7, 1–168.
Gill, R.J. (1988) The Scale Insects of California: Part 1. The Soft Scales (Homoptera: Coccoidea: Coccidae). California Department of Food & Agriculture, Sacramento, California, 132 pp.
Gill, R.J., Nakahara, S. & Williams, M.L. (1977) A review of the genus Coccus Linnaeus in America north of Panama (Homoptera: Coccoidea: Coccidae). Occasional Papers in Entomology, State of California, Department of Food and Agriculture, 24, 1–44.
Golan, K., Rubinowska, K., Kmieć, K., Kot, I., Górska-Drabik, E., Łagowska, B. & Michałek, W. (2015) Impact of scale insect infestation on the content of photosynthetic pigments and chlorophyll fluorescence in two host plant species. Arthropod-Plant Interactions, 9, 55–65.
https://doi.org/10.1007/s11829-014-9339-7
Green, E.E. (1904) The Coccidae of Ceylon. Part III. Dulau & Co., London, 249 pp.
Hamon, A.B. & Williams, M.L. (1984) The Soft Scale Insects of Florida (Homoptera: Coccoidea: Coccidae). Florida Department of Agriculture & Consumer Services, Division of Plant Industry, Gainesville, Florida, 194 pp.
Hardy, N.B., Gullan, P.J., Henderson, R.C. & Cook, L.G. (2008) Relationships among felt scale insects (Hemiptera: Coccoidea: Eriococcidae) of southern beech, Nothofagus (Nothofagaceae), with the first descriptions of Australian species of the Nothofagus-feeding genus Madarococcus Hoy. Invertebrate Systematics, 22, 365–405.
https://doi.org/10.1071/IS07032
Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W. & Hebert, P.D.N. (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America, 103, 968–971.
https://doi.org/10.1073/pnas.0510466103
Hillis, D.M. & Bull, J.J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology, 42, 182–192.
https://doi.org/10.1093/sysbio/42.2.182
Hodgson, C.J. (1967) Notes on Rhodesian Coccidae (Homoptera: Coccoidea): Part I: The genera Coccus, Parasaissetia, Saissetia and a new genus Mashona. Arnoldia (Rhodesia), 3, 1–22.
Hodgson, C.J. (1994) The Scale Insect Family Coccidae: An Identification Manual to Genera. CAB International, Wallingford, Oxfordshire, 639 pp.
Huelsenbeck, J.P. & Rannala, B. (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology, 53, 904–913.
https://doi.org/10.1080/10635150490522629
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
https://doi.org/10.1007/BF01731581
Kondo, T., Gullan, P.J. & Williams, D.J. (2008) Coccidology. The study of scale insects (Hemiptera: Sternorrhyncha: Coccoidea). Corpoica - Ciencia y Tecnología Agropecuaria, 9, 55–61.
https://doi.org/10.21930/rcta.vol9_num2_art:118
Kuwana, S.I. (1902) Coccidae from the Galápagos Islands. Journal of the New York Entomological Society, 10, 28–33.
Łagowska, B. (1999) Morphological variation in adult female Coccus hesperidum L. (Hemiptera: Coccoidea: Coccidae) in Poland. Entomologica, 33, 105–112.
Lin, Y.-P., Kondo, T., Gullan, P.J. & Cook, L.G. (2013) Delimiting genera of scale insects: molecular and morphological evidence for synonymising Taiwansaissetia Tao, Wong and Chang with Coccus Linnaeus (Hemiptera: Coccoidea: Coccidae). Systematic Entomology, 38, 249–264.
https://doi.org/10.1111/j.1365-3113.2012.00664.x
Lin, Y.-P., Cook, D.H., Gullan, P.J. & Cook, L.G. (2015) Does host-plant diversity explain species richness in insects? A test using Coccidae (Hemiptera). Ecological Entomology, 40, 299–306.
https://doi.org/10.1111/een.12191
Lin, Y.-P., Edwards, R.D., Kondo, T., Semple, T.L. & Cook, L.G. (2017a) Species delimitation in asexual insects of economic importance: The case of black scale (Parasaissetia nigra), a cosmopolitan parthenogenetic pest scale insect. PLoS ONE, 12, e0175889.
https://doi.org/10.1371/journal.pone.0175889
Lin, Y.-P., Ding, Z.Y., Gullan, P.J. & Cook, L.G. (2017b) A newly recognised Australian endemic species of Austrolecanium Gullan & Hodgson 1998 (Hemiptera: Coccidae) from Queensland. Zootaxa, 4272 (1), 119–130.
https://doi.org/10.11646/zootaxa.4272.1.6
Linnaeus, C. (1758) Systema Naturae per Regna Tria naturae, Secundum Classes, Ordines, Genera, Species cum Characteribus, Differentiis, Synonymis, Locis. Tomis I. Edirio Decima, Reformata. Cum Privilegio S:ae R:ae M:tis Sveciae. Impensis Direct. Laurentii Salvii, Holmiae, 824 pp.
Mamet, R. (1936) New species of Coccidae (Hemipt. Homopt.) from Mauritius. Proceedings of the Royal Entomological Society of London, Series B, Taxonomy, 5, 90–96.
https://doi.org/10.1111/j.1365-3113.1936.tb00599.x
Maskell, W.M. (1897) Further coccid notes: with descriptions of new species and discussions of points of interest. Transactions and Proceedings of the New Zealand Institute, 29, 293–331.
Mayr, E. (1942) Systematics and the Origin of Species, from the Viewpoint of a Zoologist. Columbia University Press, New York, 334 pp.
Melville, R.V. (1985) Opinion 1303 Coccus Linnaeus, 1758 and Parthenolecanium Šulc, 1908 (Insecta, Hemiptera, Homoptera): type species designated. The Bulletin of Zoological Nomenclature, 42, 139–141.
Morrison, H. (1921) Some nondiaspine Coccidae from the Malay Peninsula, with descriptions of apparently new species. The Philippine Journal of Science, 18, 637–677.
Morrison, H. (1929) Some neotropical scale insects associated with ants (Hemiptera-Coccidae). Annals of the Entomological Society of America, 22, 33–60.
https://doi.org/10.1093/aesa/22.1.33
Newstead, R. (1892) On new or little known Coccidae, chiefly English (No. 2). Entomologist’s Monthly Magazine, 28, 141–147.
https://doi.org/10.5962/bhl.part.7647
Newstead, R. (1903) Monograph of the Coccidae of the British Isles. Vol. II. Ray Society, London, 270 pp.
Newstead, R. (1908) On a collection of Coccidae and other insects affecting some cultivated and wild plants in Java and in Tropical Western Africa. Journal of Economic Biology, London, 3, 33–42.
Park, D.S., Suh, S.J., Oh, H.W. & Hebert, P.D.N. (2010) Recovery of the mitochondrial COI barcode region in diverse Hexapoda through tRNA-based primers. BMC Genomics, 11, 423.
https://doi.org/10.1186/1471-2164-11-423
Rogers, J. & Wall, R. (1980) A mechanism for RNA splicing. Proceedings of the National Academy of Sciences of the United States of America, 77, 1877–1879.
https://doi.org/10.1073/pnas.77.4.1877
Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180
Ryan, P.G., Ortmann, H.E. & Herian, K. (2014) Cascading effects of introduced scale insects on Nesospiza finches at the Tristan da Cunha archipelago. Biological Conservation, 176, 48–53.
https://doi.org/10.1016/j.biocon.2014.05.020
Saakyan-Baranova, A.A. (1964) On the biology of the soft scale Coccus hesperidum L. (Homoptera, Coccoidea). Entomological Review, 43, 135–147.
Sanders, J.G. (1909) The identity and synonymy of some of our soft scale-insects. Journal of Economic Entomology, 2, 428–448.
https://doi.org/10.1093/jee/2.6.428
Signoret, V. (1873). Essai sur les cochenilles ou gallinsectes (Homoptères - Coccides), 11e partie. Annales de la Société Entomologique de France (serie 5), 3, 395–448.
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation conserved polymerase chain reaction primers. Annals of the Entomological Society of America, 87, 651–701.
https://doi.org/10.1093/aesa/87.6.651
Steinweden, J.B. (1930) Characteristics of some of our California soft scale insects (Coccidae). Monthly Bulletin, Department of Agriculture, State of California, 19, 561–571.
Swofford, D.L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland, Massachusetts, U.S.A..
Tang, F.-T. (1991) The Coccidae of China. Shanxi United Universities Press, Taiyuan, Shanxi, 377 pp. [in Chinese]
Tao, C.-C. Wong, C.-Y. & Chang, Y.-C. (1983) Monograph of Coccidae of Taiwan, Republic of China (Homoptera: Coccoidea). Journal of the Taiwan Museum, 36, 57–107.
Tavaré, S. (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences, 17, 57–86.
Thro, W.C. (1903) Distinctive characteristics of the species of the genus Lecanium. Bulletin, Cornell University Agricultural Experiment Station, Ithaca, N.Y., 209, 205–221.
Tyrrell, W.M. (1896) The Lecaniums of California. Annual Report California Agricultural Experiment Station, 1894–1895, 262–270.
von Dohlen, C.D. & Moran, N.A. (1995) Molecular phylogeny of the Homoptera: a paraphyletic taxon. Journal of Molecular Evolution, 41, 211–223.
https://doi.org/10.1007/BF00170675
Whiting, M.F., Carpenter, J.C., Wheeler, Q.D. & Wheeler, W.C. (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology, 46, 1–68.
https://doi.org/10.1093/sysbio/46.1.1
Williams, D.J. (2007) Carl Linnaeus and his scale insects (Hemiptera: Coccoidea). Zootaxa, 1668, 427–490.
Williams, D.J. & Watson, G.W. (1990) The Scale Insects of the Tropical South Pacific Region, Part 3. The Soft Scales (Coccidae) and other Families. CAB International, Wallingford, Oxfordshire, 264 pp.
Yeates, D.K., Seago, A., Nelson, L., Cameron, S.L., Joseph, L. & Trueman, J.W.H. (2011) Integrative taxonomy, or iterative taxonomy? Systematic Entomology, 36, 209–217.
https://doi.org/10.1111/j.1365-3113.2010.00558.x
Zettler, J.A., Zettler, L.W. & Richardson, L.W. (2012) Pestiferous scale insects on native epiphytic orchids in south Florida: a new threat posed by introduced species. Southeastern Naturalist, 11, 127–134.
https://doi.org/10.1656/058.011.0112
Zimmerman, E.C. (1948) Homoptera: Sternorrhyncha. Insects of Hawaii, 5, 1–464.