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A New Pest Species of the Mealybug Genus Ferrisia Fullaway (Hemiptera: Pseudococcidae) from the United States

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A New Pest Species of the Mealybug Genus Ferrisia Fullaway (Hemiptera: Pseudococcidae) from the United States SYSTEMATICS A New Pest Species of the Mealybug Genus Ferrisia Fullaway (Hemiptera: Pseudococcidae) from the United States 1 1, 2 3 P. J. GULLAN, D. A. DOWNIE, AND S. A. STEFFAN Ann. Entomol. Soc. Am. 96(6): 723Ð737 (2003) ABSTRACT A new pest species of Ferrisia (Hemiptera: Pseudococcidae), Ferrisia gilli Gullan, is described and illustrated based on the adult female, third-instar female, and Þrst- and second-instar nymphs. Observation of pharate third-instar males and females failed to reveal sexual dimorphism of the second instar. Diagnosis of this new species was facilitated by the collection of nucleotide sequence data from fragments of a mitochondrial gene (COI) and two nuclear genes (EF-1␣ and 28S). The Þrst phylogenetic study of Ferrisia is presented; combined and separate analyses of the three gene regions support monophyly of F. gilli and suggest that Ferrisia virgata (Cockerell) is a species complex. The known distribution of F. gilli from California and the southeastern United States is reported. It may be native to the southeastern states. This mealybug seems to be polyphagous because it feeds on a variety of species of woody plants, both evergreen and deciduous, as well as on monocots. It has at least three generations annually in central California, where it is newly recognized as a pest in pistachio and almond orchards, but has been present in northern California since at least 1968. The main problems caused by this mealybug in pistachio orchards are contamination of foliage and fruit with honeydew and the concomitant promotion of two major fungal pathogens. KEY WORDS Pseudococcidae, mealybugs, Ferrisia, phylogeny, taxonomy MEALYBUGS OF THE GENUS Ferrisia Fullaway, and espe- many years. The latter was known as the uniparental cially the polyphagous F. virgata (Cockerell) and F. strain of F. virgata (Williams 1985) and then as F. malvastra (McDaniel), are well known as plant pests consobrina (Williams and Watson 1988) until Wil- (McKenzie 1967, Williams and Watson 1988, Miller et liamsÕ (1996) revision. Nur (1977) used electro- al. 2002). They damage plants primarily by sap removal phoretic methods to recognize two sexual and one and by contamination with copious honeydew that parthenogenetic species from specimens that were frequently serves as a substrate for sooty molds and identiÞed as F. virgata, but these electrophoretic taxa sometimes they transmit plant viruses (reviewed by were never associated with any morphological forms Williams 1996). The most recent taxonomic synopsis of F. virgata. Williams and Granara de Willink (1992) of Ferrisia (Williams 1996) recognized 10 species and reported morphological variation in the number and provided a key to distinguish 8 of these species. The position of minute tubular ducts present on the lateral other two species, F. neovirgata Khalid and Shafee and margins of the abdomen of adult female specimens F. quaintancii (Tinsley), seem to have been described assigned to F. virgata. These ducts range from few in based on immature females and thus were not in- number on some specimens to occurring in distinct cluded in WilliamsÕ key. Ferrisia seems to be of New clusters of up to 17 on each margin of abdominal World origin (Williams and Granara de Willink 1992, segments VI and VII. This morphological variation and Williams 1996), although F. malvastra and F. virgata NurÕs results for F. virgata as well as the occurrence of are more widespread, probably as the result of human unusual specimens that cannot be assigned deÞni- activities. tively to any named species suggest the existence of There is a history of problems in distinguishing further species of Ferrisia. For example, specimens of Ferrisia species, especially the biparental F. virgata, Ferrisia infesting pistachio trees in central California which has many synonyms (Williams 1996) and was probably would be identiÞed as F. malvastra in Wil- confused with the parthenogenetic F. malvastra for liamsÕ (1996) key, but the adult females exhibit several morphological differences from F. malvastra. 1 Department of Entomology, University of California, 1 Shields Complexes of morphologically similar species are Avenue, Davis, CA 95616. known in other mealybug genera, and detailed study 2 Current address: Department of Zoology and Entomology, of morphological and/or biological differences often Rhodes University, Grahamstown 6140, South Africa. reveals new species. For example, Beardsley (2001) 3 Division of Agriculture and Natural Resources, University of Cal- ifornia, Kearney Agricultural Center, Parlier, CA 93648. (Current provided evidence for two new sibling species of the address: Department of Biology, 5305 Old Main Hill, Utah State coconut mealybug Nipaecoccus nipae (Maskell), and University, Logan, UT 84322.) previously, Beardsley (1959, 1965) resolved the tax- 0013-8746/03/0723Ð0737$04.00/0 ᭧ 2003 Entomological Society of America 724 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 96, no. 6 onomy of the pineapple mealybug complex involving DNA gene (28S) (Michot et al. 1984). Primers for both the pest Dysmicoccus brevipes (Cockerell) and closely ampliÞcation and sequencing were 5Ј-CAACATT- related species. In contrast, there are examples of TATTTTGATTTTTTGG-3Ј (C1-J-2183 aka Jerry) (Si- environmentally induced variation in morphology in mon et al. 1994) and 5Ј-GCWACWACRTAATAKG- mealybugs (Cox 1983), and such variation can lead to TATCATG-3Ј (C1-N-2568 aka BEN3R, designed by the erroneous recognition of more than one species of T. R. Schultz, Smithsonian Institution) (Brady et al. mealybug. The best example is the recent synonymy 2000) for COI; 5Ј-CARGACGTATACAAAATCGG-3Ј of Pseudococcus calceolariae (Maskell) and P. similans and 5Ј-GCAATGTGRGCIGTGTGGCA-3Ј for EF-1␣ (Lidgett), based on detailed morphological study of (similar to M51.9 and rcM53Ð2 of Cho et al. 1995 mealybugs reared under controlled conditions enclosing a fragment from bases 2832Ð3149 in the (Charles et al. 2000) and supported by molecular data Drosophila melanogaster sequence); and 5Ј- (Beuning et al. 1999). Thus, new mealybug species AGAGAGAGTTCAAGAGTACGTG-3Ј and 5Ј-TTG- should only be described after careful study, prefer- GTCCGTGTTTCAAGACGGG-3Ј for 28S (Belshaw ably using multiple data sources. and Quicke 1997). PCR reaction components and Þnal The main purpose of the present work is to clarify concentrations were 1.5Ð2.5 mM MgCl2, 0.2 mM the taxonomic status of the pest Ferrisia specimens dNTPs, and 1 U Taq polymerase in a proprietary buffer that occur on pistachio trees in California. We used a (PCR Master Mix, Promega Biotech, Madison, WI), combination of morphological and molecular data to 0.2 ␮M each primer, and 5 ␮l DNA template in a Þnal achieve this goal, and we formally describe and name volume of 25 ␮l. The PCR cycling protocol for COI was a new species of Ferrisia, F. gilli Gullan, from a range 95ЊC for 7 min, followed by 40 cycles of 95ЊC for 1 min, of host plants in Alabama, California, Georgia, and 45ЊC for 1 min, and 72ЊC for 1.5 min, with a Þnal Louisiana. This new species may be native to the extension at 72ЊC for 5 min. Protocols for EF-1␣ and southeastern United States. We provide taxonomic 28S were 94ЊC for 4 min followed by 35Ð45 cycles of descriptions and illustrations of the adult and third- 94ЊC for 1 min, 49Ð52ЊC for 1 min, and 72ЊC for 1.5 min, instar females and the Þrst- and second-instar nymphs with a Þnal extension at 72ЊC for 4 min. and describe the biology of this new species in the San PCR products were puriÞed by exonuclease I and Joaquin Valley, CA. This paper also provides the Þrst shrimp acid phosphatase digestion of single-stranded systematic investigation of Ferrisia species based on DNA (primers) and dNTPs (ExoSAP-IT; USB, Cleve- molecular data. We present an estimate of the phy- land, OH). Products were sequenced on both strands logenetic relationships among the common Ferrisia using the ABI Big Dye terminator sequencing reaction species found in the United States based on nucleotide kit (Perkin-Elmer/ABI, Weiterstadt, Germany) on an sequence data from a mitochondrial gene and two ABI Prism 3100 automatic sequencer (Perkin-Elmer) nuclear genes. on 5% acryl/bisacryl Long Ranger gels. Sequences from both strands were assembled using Sequencher ver. 4.0.5 (Gene Codes, Ann Arbor, MI), Materials and Methods and multiple alignments were done with Clustal X ver. 1.81 (Thompson et al. 1997) and edited in MacClade Molecular Methods version 4.0 (Maddison and Maddison 1992). Maximum Freshly collected specimens of four Ferrisia species, parsimony (MP), as well as maximum-likelihood F. malvastra, F. terani Williams and Granara de Willink, (ML) and neighbor-joining (NJ), was used to estimate F. virgata, and the putative new species F. gilli, were trees. For parsimony, a heuristic search was run with obtained preserved in 95Ð100% ethanol, and one ad- 100 replications of random sequence addition. For ditional new species from an old collection made in distance-based analyses, the model of sequence evo- Puerto Rico was obtained in 75% ethanol (Table 1). lution that best Þt the data was found by testing 56 Four other mealybug species were used as outgroups: models using an iterative likelihood procedure imple- Anisococcus adenostomae (Ferris), Maconellicoccus mented in Modeltest ver. 3.06 (Posada and Crandall australiensis (Green and Lidgett), Planococcus citri 1998). Support for clades was estimated by bootstrap- (Risso), and Pseudococcus longispinus (Targioni Toz- ping (1,000 replications for MP and NJ, 100 replica- zetti). These four outgroups were chosen because tions for ML). An incongruence length difference they represented four separate groups in a larger mo- (ILD) test (Farris et al. 1994) was used to determine lecular data set (DAD and PJG, unpublished data). whether to combine data from the three gene frag- Before DNA extraction, all specimens were examined ments. All phylogenetic analyses were executed in under the microscope for the presence of parasitoids.
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