PROC. ENTOMOL. SOC. WASH. 109(3), 2007. pp. 522-529 A TAXONOMIC REEVALUATION OF OVATUS MENTHARIUS (VAN DER GOOT) (HEMIPTERA: APHIDIDAE) Gary L. Miller, Susan E. Halbert, and Robert G. Foottit (GLM) Systematic Entomology Laboratory, PSI, Agricultural Research Service, MD U.S. Department of Agriculture, Bldg. 005, BARC-West, Beltsville, 20705, U.S.A. (e-mail: [email protected]); (SEH) Florida Department of Agricul- ture and Consumer Services, Division of Plant Industry, Gainesville, FL 32614, U.S.A. (e-mail: [email protected]); (FGF) Agriculture and Agri-Food Canada, Canadian National Collection of Insects, Ottawa, ON KIA 0C6, Canada (e-mail: [email protected]) — Abstract. We reevaluate the status of Ovatus mentharius (van der Goot) in North America which was previously misidentified as Ovatus crataegarius (Walker). Detailed keys for separating O. crataegarius and O. mentharius on Labiatiae, descriptions of apterous viviparae and the alatae of O. mentharius, morphometric analysis, distribution records, and illustrations of O. mentharius are presented. Key Words: aphid, mint, adventive species The genus Ovatus was proposed by der Goot) identified by us (GLM and van der Goot in 1913. Some species of SEH) and others (e.g., Floren 2004) at this genus host alternate between Crae- various ports-of-entry and greenhouse taegus or other woody Pomaceae and facilities within the United States have Labiatae while other species are monoe- brought our attention to this Palearctic cious, associated with Labiatae or other species. It also raised concerns that yet herb families (Heie 1994). A systematic another adventive aphid species may evaluation of Ovatus (sensu Remaudiere represent an ecological threat. All hold- and Remaudiere 1997) in North America ings ofO. menthariuswithin the National by Jensen and Stoetzel (1999) resulted in Museum of Natural History Aphidoidea its revision and subsequent placement of Collection (USNM), Beltsville, MD, four endemic North American species were from port interceptions originating into the genus Abstrusomyzus Jensen and from Europe. Further examination of Stoetzel. Their revision left a single holdings of O. crataegarius revealed species of Ovatus in North America, intermittent collections of O. mentharius Ovatus crataegarius (Walker), which is that had been previously misidentified as considered Palearctic in origin but has O. crataegarius from as far back as 1935. a worldwide distribution (Jensen and Some of these collections represented Stoetzel 1999). border interceptions, but the earliest Adventive aphid species represent ap- record of this species (California in proximately 18% ofthe North American 1935) was possibly not an interception. aphid fauna (Foottit et al. 2006). Recent In addition to the recent port intercep- interceptions of Ovatus mentharius (van tions, discovery (and subsequent eradi- VOLUME NUMBER 109, 3 523 cation) of O. mentharius within experi- areusedinthiswork. Abbreviationsherein mental plots containing mint {Mentha for body length, antennal segment(s), spicata L., M. suaveolens Ehrh., and aptera/apterae (=wingless viviparous fe- Mentha sp.) and basil {Ocimum basilicum male(s)), alata/ alatae (=winged vivipa- L.) and on Mentha spp. at an organic rous female(s)), and immature(s) are listed greenhouse operation in Florida raised as: b.l., a.s., ap., al., andimm., respectively. our concern that this species could be If a collection was made at the same pestiferous. Ovatus mentharms in Florida locality, but on a different date as a pre- represents the easternmost distribution viously listed collection, duplicated infor- of the species in the U.S.A. mation is not repeated. Months are Ovatus mentharius is holocyclic and designated as roman numerals. For exam- monoecious on Mentha spp. while O. ple, the documentation provided for apar- crataegarius is holocyclic and heteroe- ticular locality may be recorded as: cious with Mentha spp. serving as second- FLORIDA: Tallahassee, VI-6-1989, on ary hosts (Heie 1994). Mixed infestations Ocimum basiUcum, D. C. Beard coll., (2 of the two species and morphological ap.) USNM; V-10-1990, VI-29-1991, 1-21- similarities sometimes make identification 1992, on mint [Mentha sp.], (5 ap. on 5 si.) difficult. The current study was undertak- USNM. In this hypothetical example, en to reevaluate the status of O. menthar- the second collection was also found at ius in America North of Mexico by Tallahassee, even though "Tallahassee" was not repeated. Collection data that providing descriptions, illustrations, keys for separating O. crataegarius and O. are the same except for collection date mentharius, distribution records of O. are simply listed sequentially. In exam- mentharius, and morphometric analysis ples where microscope slides record of O. crataegarius and O. mentharius for a county, they are listed first within each state then chronologically. Other additional species clarification. collection localities are listed chronolog- Materials and Methods ically. When specimens are mounted on a single slide (si.), it is not written as Synoptic descriptions are taken from such but is assumed. Bracketed ([ ]) text original descriptions and specimens from represents supplemental information by The Florida State Collection of Arthro- the current authors for clarification pods (FSCA), Gainesville, FL, U.S.A. purposes. and the National Museum of Natural Specimens ofthe adult apterous vivip- History Aphidoidea Collection (USNM), arous morph were used for morphomet- Beltsville, MD, U.S.A. Measurements are ric analysis. Bracketed letters (e.g., {A}) in micrometers (|am) as minimum and in the "Specimens examined" section for maximum ranges of representative speci- O. mentharius indicate those specimens mens. Table 1 also includes summary that were used in the analysis. Seventy- statistics (range, mean, and standard three slides of O. crataegarius were deviation) for O. crataegarius and O. examined from the USNM. Single rep- mentharius. Drawings were begun using resentative specimens of O. crataegarius a camera lucida and completed either by that were measured and used in the hand or by computer-aided illustration analysis are as follows. MEXICO: [inter- programs (Adobe Photoshop®). Most cepted at San Ysidro, CA [?] interception specimens had been cleared and mounted # 2536], 11-27-1961, on Mentha sp., J. or remounted in Canada balsam. Spear coll., USNM; [intercepted at Chi- Morphological terms and structures a- cago, IL, interception # 4785], III-28- dapted from Foottit and Richards (1993) 1963, on Mentha sp.. Rood coll., USNM; 524 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON Table L Summary statistics (range, mean and standard deviation) for measurements of Ovatus crataegarius and Ovatus mentharius in |im. and standardized total sample coefficient (loadings) for variables used in canonical discriminant analysis. — VOLUME NUMBER 109, 3 525 We used principal component analysis species. Jensen and Stoetzel (1999) pro- to investigate relationships among speci- vided characters for separating O. cra- mens and variables and we used canon- taegarius in North America from similar ical variates analysis to determine those taxa in the genera Abstrusomyzus Jensen variables which best separated groups of and Stoetzel, Hyalomyzus Richards, My- specimens (Foottit and Mackauer 1990). zus Passerini, and Phorodon Passerini. All statistical analyses were carried out Ovatus species can be either holocyclic using SAS version 9.1 for Windows® and heteroecious or holocyclic and mon- (SAS Institute Inc., Cary, North Car- oecious. For example, O. crataegarius olina). has primary hosts Crataegus and other Rosaceae and secondary hosts Mentha Results spp., while O. mentharius is holocyclic Ovatus van der Goot 1913 and monoecius on Mentha spp. (Heie Ovatus van der Goot 1913:84. Type 1994). species: My"us mespili van der Goot, 11981429:: xx6x4i;x).{=ByApohriisginianlsidtieissignWaatlikoenr., Ovatus menthar(iFiugss.(v1a9n)der Goot 1913) — Phorodon mentharius van der Goot 1913: North American diagnosis. Small to 82. medium aphids (b.l. 1,000-2,500). An- Ovatus menthastri Hille Ris Lambers tennae 6-segmented, longer than body in 1947: 303. apterae and alatae; apterae without Ovatus mentharius (van der Goot): secondary sensoria, alatae with numer- Eastop and Hille Ris Lambers 1976: ous secondary sensoria on a.s. Ill, fewer 329; Remaudiere and Remaudiere on a.s. IV, and frequently on a.s.V. Head 1997: 135. spiculated, lateral frontal tubercles well — developed with prominent convergent Field features. Fundatrices and ap- rounded processes on the inner sides. terae "pale whitish green" (Hille Ris Apical rostral segments longer than hind Lambers 1947). Alatae "green" (Hille tarsus II. Forewing length of alatae Ris Lambers 1947) or more specifically, ca.1.5 times body length. First tarsal head and thorax brownish green, abdo- segment with 3-3-3 hairs. Dorsal body men green, antenna black, siphunculus setae shorter than those on venter; brownish with paler bases, wings with abdomen with irregularly-shaped sculp- brown-borderd veins (Heie 1994); ovi- turing separated by smooth space, with- parae "pale greenish yellow" (Hille Ris out large dorsal patch although smaller Lambers 1947). faint sclerites present. Siphunculi longer Recognition characters. Apterous vi- than Cauda, with imbrications and dis- vipara (Fig. 1): b.l. 1,060-1,790; width tinct flange. Cauda elongate, spiculated through eyes, 300-400 Head (Fig. 2) with 5-7 setae. sclerotized and scabrous; antennal tuber- — Notes. Various authors (e.g., Eastop cles well developed, converging and and Hille Ris Lambers 1976, Remaudiere bearing setae (Figs. 2, 3); tips of dorsal and Remaudiere 1997) have erroneously head setae blunt. Antenna (Fig. 1) longer recorded ''"Ovatus mespili van der Goot than body, a.s. I (Figs. 2, 3) with anterior (1913)" as the original combination of projection, occasionally obscured on the type species. In fact, Ovatus was some specimens due to orientation in described by van der Goot (1913) with mounting medium, a.s. VI and tip of V Myzus mespili van der Goot (1912) (= darker than other segments on mature Ovatus insitus (Walker)) as the type specimens, setae less than half width of PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON 526 Figs. 1-9. Ovatus mentharius. 1, Apterous vivipara dorsal habitus. 2, Right side, apterous vivipara dorsum ofhead and a.s. I; left side, apterous vivipara venterofhead and a.s. I.. 3, Lateral view ofheade and a.s.I of apterous vivipara. 4, Utimate rostral segment. 5, Dorsal abdominal reticulation. 6, Siphunculus ofapterous vivipara. 7, Cauda ofapterous vivipara. 8, Right side, alatadorsum ofhead and a.s. I; left side, alata venter ofhead and a.s. I. 9, Alata a.s. I-VI. segment; a.s. Ill 300-490 long without 400, mid tibia 450-765, mid tarsus II 65- secondary sensoria; a.s. IV 210-390 long 80 long; hind femur 300-515, hind tibia without sensoria; a.s.V 180-350 without 590-0.935, hind tarsus II 60-95 long. secondary sensoria; base ofa.s.VI 85-1 15 Abdomen dorsally with distinct irregular long; terminal process, 425-590 long. reticulations separated by smooth areas Rostrum extending past metacoxae; ulti- (Fig. 5), occasionally with small faint mate segment (Fig. 4) 100-135 long, lateral sclerites, dorsal setae stout with approximately 3 times as long as wide blunt tips, ventral setae longer with at base, with 2 accessory setae. Fore pointed tip, segment VIII with 4-6 setae; femur 235-375, fore tibia 450-715 long, ventrally spiculose; anal plate with 6-8 fore tarsus II 60-80 long; mid femur 240- setae, genital plate with normal configu- — VOLUME NUMBER 109, 3 527 ration ofsetae. Siphunculus (Fig. 6) 265- of the variables would be sufficiently 455 long, scabrous, tapering slightly and influenced by size variation as to be occasionally slightly curved with several ineffective as species-level discriminators. rows of hexagonal cells below apical The analysis indicated that among the flange. Cauda (Fig. 7) 125-190 long, specimens of O. mentharms there is less elongate, tongue-shaped with 2-3 pairs variation in the a.s. VI, base -length and of lateral setae. the ultimate rostral segment-length, than Alata (Fig. 8).- Similar to apterous in O. cratagarius. female except: b.l. 1,175-1,675; width The canonical variates analysis, which through eyes 310-375. A.s. I (Fig. 9) incorporates the overall variation among protuberance not as pronounced as in the specimens, completely separated the apterae, a.s. Ill 350-425 long, with 19-26 two sets ofspecies representatives on the sensoria; a.s. IV 225-390 long, with 4-15 basis of significant contributions from secondary sensoria; a.s. V 205-330 long, a number ofvariables. Ovatus crataegar- with 0-1 secondary sensoria; base of a.s. ius is characterized by a longer cauda VI 90-1 10 long; terminal process 490-600 and a longer antennal segment III long. Ultimate rostral segment 115-125 compared to those of O. mentharius. long. Forewing length 1,650-2,500, 550- Ovatus mentharius is characterized by 860 at widest point; hindwing 900-1,475 longer legs and a longer siphunculus. — long, 250-420 at widest point. Fore Notes. Identification should consist femur 330-455, fore tibia 650-835 long, of a series of specimens when possible. fore tarsus II 60-80 long; mid femur 300- This is especially true when certain 400, mid tibia 600-825 mid tarsus II 60- characters such as antennal projections 80 long; hind femur 375-535, hind tibia can be obscured or altered during the 810-1,100, hind tarsus II 70-90 long. slide-mounting process. In addition, Siphunculus 225-350 long. Cauda 125- there is variability within such characters 140 long. as secondary sensoria. For example, one Morphometric analysis (Table 1). specimen had 21 and 26 secondary Initial principal component analysis in- sensoria on left and right side a.s.Ill, dicated that a large component (75%) of respectively. This upper count ofsecond- the morphological variation within the ary sensoria is even higher than the specimens was the result of size-related upper range (21) Heie (1994) recorded influences. We reduced the number of for O. mentharius . — variables to 16 from 21 by eliminating Specimens examined. MEXICO: Juar- a.s. IV-length, fore tibia length, and the ez [intercepted at El Paso, TX, intercep- three femur-length measures as these tion #'s 66434, 69197, 00865], V-20-1966 variables were highly correlated (over {A}, VIII-19-1967 {B}, IX-14-1970, on 95%) with other variables. Two speci- Mentha sp., [various collectors include] mens of O. crataegarius (Idaho, III-22- D. S. Cambell, J. Kline, C. Oliver colls., 1973 and Maryland, X-6-1975) were (5 ap. on 3 si.) USNM; Torrean, [inter- eliminated from further analysis as they cepted at El Paso, TX, interception # were likely distorted by compression 001508], IX-2-1970 {C}; on Mentha sp., from the slide-mounting process. D. Mayer coll. (4 ap. and 1 imm.) Further principal component analysis USNM; [interception at San Ysidro, showed that there was a broad distribu- interception # 2535], 11-27-1961 {D}, tion of specimens of both species along on Mentha sp., J. Spear coll. (3 ap.) a size-related axis which still accounted USNM; [interception at Chicago, IL, for approximately 70% of the total interception # 4540], X-18-1962, on variation. This trend indicated that many Mentha sp.. Rood coll. (1 ap.) USNM; PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON 528 [interceptions at El Paso, TX, intercep- secondary sensoria Ovatus crataegarius (Walker) tion #'s 61498, 71850, 70484], X-13- 1962, III-12-1968, XII-15-1968 {E}, on Mentha sp., [and] mint, [and ] "misc. Conclusions mosses" [dubious host association],[var- ious collectors include] G. Dunn, J. W. Identification of O. mentharhis in North America has been problematic Green, McClain C. Oliver colls., (10 a[pi.n,ter2cepatl.ion1 atimAmt,.lanotna,5GAsi,.) iUntSerNcMep;- dO.uecrtaotaemgoarrpihuosloagnidcaalpasritmiiallaroitvieerslawpitohf tion # 0502015], VI-20-2004 {F}, on host plants. However, current morpho- metric analysis supports the contention Mentha sp., P. Haney coll. (3 ap. on 3 si.) FSCA, USNM; [interception at San that they are indeed separate species. Francisco, CA, interception # 0505031], This separation is especially critical not only taxonomically but also from an V-30-2005 {G}, on Mentha sp., J. Iniguez USNM. UNITED STATES: economic standpoint. The economic im- coll. (3 ap.) CALIFORNIA, Berkeley, III-30-1935 portance of the mint hosts (e.g., Mentha spicata) could be a major concern in the {H}, on Mentha spicata, E. O. Essig coll., (7 ap., 4 al., 2 imm. on 8 si.) USNM. spearmint growing region of the Pacific FLORIDA, Orange Co., Apopka, III-l- Northwest. In addition, our report of 2(200a6l.{oI}n,2onsi.M)eFnStChAa,sp.U,SLN.MOs;boSrunweanconlel.e, cbaosniclerasn aforhotshterferpersehsehnetrsbainndaudsdtiryt.ionOanl Co., Live Oak, VI-1-2006, on Mentha sp., a positive note, even though O. menthar- L. L. Davis coll., (2 ap. on 2 si.) FSCA, ius had been recorded from California as USNM. NEW MEXICO, Mesilla Park, early as 1935, there have been apparently IV-25-1956 {J}, on mint, J. J. Durkin no major populations collected since that USNM. UNDETERMINED time. This also is borne out through the coll., (2ap.) absence of O. nientharius in extensive [labeled "Ariz to Juarez to El Paso] V-12- 1964 {K}, on Mentha sp., Overmiller collecting of one of us (SJH) in this coll., (1 ap., 1 al., 1 imm.) USNM. region of the continent. Adventive species ofsternorrhynchous Hemiptera in North America have been Key TO North American Ovatus the subjects of concerted efforts recently VIVIPARAE ON MINTS (e.g.. Miller et al. 2002, Miller and Miller 1. Antennal segment tip V and VI dark in 2003, Miller et al. 2005, Foottit et al. mature adults; apterous viviparous a.s. I 2006). The numbers and rates of intro- with forward projecting process on inner ductions of the Coccoidea and Aphidoi- side (Figs. 2, 3) (on slide-mounted speci- dea have nearly mirrored each other mens this is sometimes difficult to see); siphunculus often longer than distance for the past two centuries (Miller et al. between inner bases (Fig. 1); alatae a.s. 2005, Foottit et al. 2006). Foottit et al. Ill with 19-24 secondary sensoria (occa- (2006) determined that 262 species of sionally more), a.s. IV with 4-13 (occasion- aphids should be considered adventive ally more) secondary sensoria Ovatus mentharhis (van der Goot) to America North of Mexico. It is - Antennal segments I-VI predominantly possible that O. nientharius could repre- dark in mature adults; apterous viviparous sent an addition to this tally. However, a.s. Iwithoutforward projectingprocesson with the exception of the recent collec- inner side; siphunculus usually shorter to tion and eradication of O. nientharius in subequal (occasionally longer) than dis- tance between inner bases; alatae a.s. Ill Florida, it seems as though establishment with 27-34secondarysensoria(occasionally is suspect except in a greenhouse situa- less), a.s. IV with 12-17 (occasionally less) tion. VOLUME NUMBER 109, 3 529 Acknowledgments Heie, O. E. 1994. The Aphidoidea (Hemiptera) of We thank Eric Maw (Agriculture and Fennoscandia and Denmark. V. Family Aphi- didae: Part 2 of tribe Macrosiphini of sub- Agri-Food Canada, Ottawa) for assis- family Aphidinae. Fauna Entomologica Scan- tance with the morphometric analyses. dinavica 28: 1-242. Thanks also to D. Miller (SEL, Behs- Hille Ris Lambers, D. 1947. On some mainly ville, MD), S. Lingafelter (SEL, Wash- Western European aphids. Zoologische Mede- ington, DC), W. Dixon (Gainesville, deelingen 28: 291-333. PL), C. Favret (Beltsville, MD) and A. Jensen, A. S. and M. B. Stoetzel. 1999. An examination of the North American aphid S. Jensen (Moses Lake, WA), for their species currently placed in Ovatus van der reviews of the manuscript. This is Ento- Goot (Hemiptera: Aphididae) with the de- mology Contribution No. 1071, Florida scription of a new genus. Proceedings of the Department ofAgriculture and Consum- Entomological Society of Washington 101(1): 39-56. er Services, Division of Plant Industry, Miller, D. R., G. L. Miller, and G. W. Watson. Bureau of Entomology, Nematology, 2002. Invasive species of mealybugs (Hemi- and Plant Pathology. ptera: Pseudococcidae) and their threat to U.S. agriculture. Proceedings of the Entomo- Literature Cited logical Society of Washington 104(4): 825- Eastop, V. F. and D. Hille Ris Lambers. 1976. 836. Survey of the World's Aphids. Dr. W. Junk, Miller, D. R., G. L. Miller, G. S. Hodges, andJ. A. b.v., The Hague. 573 pp. Davidson. 2005. 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