SPECIAL FEATURE ON SOYBEAN APHID A Guide to Separating Aphis

SPECIAL FEATURE ON SOYBEAN APHID A Guide to Separating Aphis glycines Matsumura and Morphologically Similar Species That Share Its Hosts DAVID J. VOEGTLIN,1 SUSAN E. HALBERT,2 AND GEXIA QIAO3 Ann. Entomol. Soc. Am. 97(2): 227Ð232 (2004) ABSTRACT Aphis glycines Matsumura shares its hosts with two other aphid species, Aphis nasturtii Kaltenbach and Aphis gossypii Glover. Tables of characters and photographs are provided to assist in the separation of these three species. A photographic plate showing a gynopara, male, ovipara, and late summer apterous vivipara of A. glycines is included. KEY WORDS Aphis glycines, Aphis nasturtii, Aphis gossypii, Rhamnus cathartica, morphology THE ARRIVAL OF THE SOYBEAN aphid, Aphis glycines Matsumura, in North America has necessitated taxonomic work to identify consistent characters useful for distinguishing it from other species that share the same host plants. It is not surprising that the soybean aphid was initially mistaken for the cotton or melon aphid, Aphis gossypii Glover, because this cosmopolitan pest is morphologically and biologically very close to A. glycines, and A. gossypii is also known to colonize soybean, Glycine max (L.) Merr., in North America. Although colonization of soybean is uncommon in the north central United States, it may be more common in southern regions based on samples from Mississippi that contained only A. gossypii or a mixture of both species. A. glycines overwinters on Rhamnus cathartica L., a host it shares with Aphis nasturtii Kaltenbach. Another species, Aphis frangulae Kaltenbach, has been recorded in North America (Smith and Parron 1978) and is listed as having R. cathartica as a host by Blackman and Eastop (1994). However, Stroyan (1984) and Heie (1986) reported that A. frangulae is limited to R. frangula. We have collected no aphids on R. frangula in the spring, so we have not included A. frangulae in this study. Here, we provide information to help in the separation of the soybean aphid from other species with which it shares hosts. Materials and Methods All specimens have been personally collected or received for identiÞcation from entomologists throughout much of the present distribution of A. glycines in the United States. All are slide mounted in balsam and deposited in the collection of the Illinois Natural History Survey (Champaign, IL). Photo1 Center for Economic Entomology, Illinois Natural History Survey, Champaign, IL 61820 Ð 6970 (e-mail: dvoegtli@uiuc.edu). 2 Division of Plant Industry, FDACS, P.O. Box 147100, Gainesville, FL 32614-7100. 3 Institute of Zoology, Chinese Academy of Sciences, Beijing 100080, PeopleÕs Republic of China, 50011-1100. graphs were taken using a SPOTdigital camera attached to a Nikon compound microscope. Results and Discussion The following are characters that have been useful in separating these species. The sclerotization of the coxae and trochanter (Fig. 1D and E), and the scape and pedicel. The presence or absence of sensoria on the antennal segments, which in genus Aphis are circular membranous areas on the antennae that are surrounded by a distinct border (Fig. 1AÐC). The cauda projects from the last abdominal segment, and in this group of aphids has a constriction and bears setae on the part beyond the constriction (Fig. 1F and G). Lateral sclerites are most visible on sides of abdominal segments IIÐIV anterior to the siphunculi (Fig. 2D), and the sclerites on abdominal segments VI and VII are in the middle of the dorsum. The characters in the tables are based on observations of slidemounted specimens; however, it is possible to see some of these characters in live specimens or specimens in alcohol. For example, it is usually possible to determine whether the coxae and trochanter are pale, dark, or concolorous without making slides. Caudal setae and sensoria on the antennal segments can be seen using a good quality dissecting microscope if the specimens are against a dark background. It has been difÞcult to Þnd A. glycines on R. cathartica in the spring, and of the few colonies that have been found some also contained A. nasturtii. Given the limited material at present, we are unable to separate apterous viviparous females of these two species taken from the primary host. It is possible to separate the spring migrants (Fig. 3) from R. cathartica with the set of characters provided in Table 1, although there is considerable variability and overlap in character states. Separation of summer forms of A. gossypii and A. glycines is complicated by the great morphological variation in A. gossypii. It may not be possible to 2004 Entomological Society of America 0013-8746/04/0227Ð0232$04.00/0 228 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 97, no. 2 Fig. 1. Characters for alate viviparous females. Antennal segments III and IV. (A) A. glycines. (B) A. nasturtii. (C) A. gossypii. Metathoracic coxa and trochanter. (D) A. gossypii (E) A. glycines. Cauda showing caudal setae. (F) A. gossypii (G) A. glycines. determine every specimen collected on soybean with complete certainty. The photographs in Fig. 2 show “typical” apterous and alate summer morphs of both species. The characters given in Table 2 seem to be consistent for material examined of both species from North America, but they may not hold for aphids from other continents and may differ with geography and climate. For detailed information on the morphology of the A. gossypii and A. frangulae complex of species, see Stroyan (1984) and Heie (1986). For A. glycines, see Takahashi et al. (1993), and for A. nasturtii, see Patch (1924), Stroyan (1984), and Heie (1986). In late summer and early autumn, it is possible to Þnd small apterous viviparae mixed in with more normal-sized individuals. These specimens have little, if any, sclerotization and only Þve-segmented antennae. Some collections from September in Mississippi contained these small morphs of both A. glycines and A. gossypii. They can be separated by distinct difference in caudal length and shape. A. glycines retains its longer cauda with the part distad of the constriction showing as an elongate oval with six to nine setae (Fig. 4C), whereas A. gossypii has a shorter cauda with the part distad of the constriction often more circular than oval and usually with four setae. A gynopara, male, and ovipara of A. glycines are shown in Fig. 4. The gynoparae are more similar in sclerotization pattern to the spring migrants than they are to the summer alate viviparae. The sclerotic areas are slightly darker; however, the coxae and trochanters are concolorous, usually pale but sometimes dusky. This character will separate them from the gynoparae of other species on R. cathartica. Eggs can be seen in the ovipara shown on Fig. 4D. We could not Þnd data on the number of eggs that might be produced by a single ovipara. This specimen has six visible eggs that seem to completely Þll its body. Acknowledgments We thank Ben Putler, University of Missouri; David Ragsdale and Susan Weller, University of Minnesota; Bob OÕNeil, Purdue University; Chris DiFonzo, Michigan State University; Robert Alpe, Bureau of Plant Industry, Mississippi; Donald Sudbrink, Delta Research and Extension Center, Mississippi; and John Wedberg, University of Wisconsin, for specimens from outside of Illinois and all our colleagues and many cooperators from throughout Illinois that have sent material in for veriÞcation. We also thank Jim Nardi, University of Illinois, for the use of a digital photographic system. March 2004 VOEGTLIN ET AL.: SEPARATING A. glycines AND SIMILAR SPECIES 229 Fig. 2. Apterous viviparous females from secondary hosts (A) A. glycines, (B) A. gossypii. Alate viviparous females (C) A. glycines, (D) A. gossypii. 230 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 97, no. 2 Fig. 3. Spring migrants taken from Rhamnus cathartica. (A) A. glycines. (B) A. nasturtii. Table 1. Comparison of several characters of alate spring migrants of A. glycines and A. nasturtii from R. cathartica A. glycines Pale to dusky Pale to dark Pale to dark over distal 1/2 Only on segment III 6Ð10 Lacking to present and distinct A. nasturtii Dark Dark Dark over distal 2/3 Segments III, IV, and sometimes V 6Ð8 Lacking to pale Character Coxal color Scape and pedicel Femora Secondary sensoria Caudal setae Sclerites on segments VI and VII Table 2. Comparison of several characters of summer apterous and alate viviparous females of A. gossypii and A. glycines Character A. gossypii Dusky Usually dark throughout Medium, present Dusky 3Ð6 Dark Dark, distinct Dusky to dark Dusky 3Ð6 Present and distinct A. glycines Pale Often pale basally darkening distally Absent or pale Pale 6Ð9 Pale Pale Pale Pale 6Ð11 Absent to indistinct Apterous viviparous females Scape and pedicel Siphunculi Lateral sclerites Cauda Caudal setae Alate viviparous females Scape and pedicel Lateral sclerites Coxae Cauda Caudal setae Sclerites on abdomen VII and VIII March 2004 VOEGTLIN ET AL.: SEPARATING A. glycines AND SIMILAR SPECIES 231 Fig. 4. A. glycines. (A) gynopara. (B) Male. (C) Late summer apterous viviparous female. (D) Ovipara. References Cited Blackman, R. L., and V. F. Eastop. 2000. Aphids on the WorldÕs Crops: An IdentiÞcation and Information Guide. Wiley, New York. Heie, O. 1986. The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. III Family Aphididae: subfamily Pterocommatinae and tribe Aphidini of subfamily Aphidinae. Fauna Entomol. Scand. 17: 1Ð314. 232 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 97, no. 2 Patch, E. M. 1924. The buckthorn aphid. Maine Agric. Exp. Stn. Bull. 317: 29 Ð52. Smith, C. F., and C. S. Parron. 1978. An annotated list of Aphididae (Homoptera) of North America. N.C. Agric. Exp. Stn. Tech. Bull. 255: 1Ð 428. Stroyan, H.L.G. 1884. AphidsÑPterocommatinae and Apidinae (Aphidini) Homoptera, Aphididae. Handbk. Ident. Br. Insects II, 6: 1Ð232. Takahashi, S., M. Inaizumi, and K. Kawakami. 1993. Life Cycle of the soybean aphid Aphis glycines Matsumura, in Japan. Jpn. J. Appl. Entomol. Zool. 37: 207Ð212. Received for publication 19 May 2003; accepted 25 September 2003.