A New Species of the Rhus Gall Aphids ( Aphididae : Eriosomatinae : Fordini ) from Eastern China

Zhu-Mei Ren1,*, Xu Su2, Carol D von Dohlen3 and Jun Wen4,1,* 1School of Life Science, Shanxi University, Taiyuan 030006, Shanxi, China 2Key Laboratory of Medicinal Animal and Plant Resources of the Qinghai-Tibetan Plateau in Qinghai Province, School of Life Science, Qinghai Normal University, Xining 810008, Qinghai, China 3Department of Biology, Utah State University, Utah 84322, U.S.A 4Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington DC 20013, U.S.A Article Information Received 19 December 2017 Revised 18 February 2018 Accepted 28 March 2018 Available online 31 August 2018


INTRODUCTION
T he Rhus gall aphids refer to a lineage of host- alternating aphids that live on species of Rhus (sumacs) as their primary host, on which they induce galls known as Woo-pei-tsze or Chinese gall (Bell, 1851;Tang and Tsai, 1957).The first species described in this group was recorded from China as Aphis chinensis (Bell, 1851); subsequently, a similar species was described from North America.Although initially considered the same species, they were later recognized as members of different genera by various taxonomists (Fitch, 1866;Lichtenstein, 1883;Baker, 1917;Arshad et al., 2017).Eastop and Lambers (1976) designated the species from China and North America as Schlechtendalia chinensis (Lichtenstein, 1883) and Melaphis rhois (Fitch, 1866), respectively.Additional genera and species of this group from eastern Asia were described and analyzed (Matsumura, 1917;Tsai and Tang, 1964;Xiang, 1980;Tang, 1986).So far, six genera and 12 species (the genus Kaburagia including three subspecies) have been recognized in this group (Eastop and Lambers, 1976;Zhang et al., 1999;Yang et al., 2010;Ren et al., 2013Ren et al., , 2017)), and they have been placed in the subtribe Melaphidina of tribe Fordini (Hemiptera, Aphididae, Eriosomatinae) (Eastop and Lambers, 1976;Blackman and Eastop, 1994;Favret, 2013).Matsumura (1917) erected the genus Nurudea based on Nurudea ibofushi from Japan, and distinguished this species from Schlechtendalia chinensis by the regularly ringed secondary sensoria on the 3 rd antennal joint.Tsai and Tang (1964) described N. sinica as closely allied to N. ibofushi, noting that they differ in the structure of sensoria on the apical two joints of the antennae.Eastop and Lambers (1976) synonymized the two species as N. ibofushi.Meanwhile, Matsumura (1917) described two species N. shiraii and N. yanoniella under the new genus Nurudeopsis, which was subsequently merged into Nurudea by later taxonomists (Eastop and Lambers, 1976;Zhang et al., 1999).Therefore, the genus Nurudea currently includes three species: N. ibofushi, N. shiraii and N. yanoniella from China and Japan, and all of them form galls on their primary host plant Rhus chinensis.
In 2009, we collected several galls formed by an aphid species feeding on Rhus hypoleuca Champion ex Bentham in China.After the morphological examinations, we concluded that the collections are similar to the two species, N. shiraii and N. yanoniella, and should be A B S T R A C T recognized as a new species of Nurudea.Here, we formally described this new species.

Materials
Samples of galls were collected from leaf rachises of Rhus hypoleuca on the Mountain Qixing in Shangrao County, Jiangxi Province, China in 2009.Slide-mounted specimens of 15 alate viviparous females from the same gall were used for morphological observations.The remaining samples were observed as references.The holotype and paratypes of the new species (alate viviparous female) and host-plant vouchers (Ren and Li A402 and Ren and Li P402, respectively) were deposited at School of Life Science, Shanxi University, Taiyuan, China.

Methods
Freshly collected aphid samples were immersed in 70% ethanol, then macerated 2-3 min in 15% KOH solution before making permanent slides.Adult alate viviparous specimens were cleared and mounted individually in Canada balsam on microscope slides according to the techniques described by Maw and Foottit (1998).Morphological analyses were performed using a stereomicroscope and an electron microscope, and measurements were taken using a Leica DM2500B microscope.
Aphid morphology was characterized by measuring several morphological features and ratios, and descriptive qualitative features.A total of 50 morphological characters including 20 quantitative characteristics, nine ratios from two measured characters, and the qualitative features from head, thorax and abdomen of the 15 alate adults were evaluated.Aphid terminology in this paper follows Quednau (2003) and Qiao et al. (2005).The unit of measurements is millimeters (mm).

Diagnosis
The body of alate viviparous females oval, surface smooth.Head, thorax and abdomen without wax plates, middle frons curved.Antennae 5-segmented, smooth, processus terminalis one-fourth as long as base of the segment V. Rostrum short and small.First tarsal chaetotaxy: 3, 3, 3. Siphunculi absent.Fore wings with four oblique veins, media veins unbranched.Cauda halfmoon shaped, smooth.Anal plate oblong.

Description
Alate viviparous females oval (Fig. 2).Head and thorax dark brown, abdomen tinge without stripes.Antennae, rostrum and each segment of legs brown, cauda and anal plate light brown.Body surface smooth, front margins of dorsum of head with one pair of small round wax plates and each with 4-6 waxy cells.Thorax and abdomen without wax plates, spiracle round to oval, open or closed.One pair of hairs on the head top and 4-6 pairs of dorsal setae on head.One pair of hairs on the spinal of abdominal tergite I, 4-8 hairs on abdominal tergite III, and length of abdominal tergite I and abdominal tergite III about 0.25-0.50and 1.33-4.00times as long as the widest diameter of antennal segment III, respectively.Middle frons curved, antennae 5-segmented, smooth, entire length 0.32-0.35and 0.45-0.55times as long as body; antennal segment III 0.07-0.09,5-9 times as long as the diameter of the base of the segment, length in proportion to segments I-V: 28-41: 44-60: 100: 88-106: 75-120+19-50, respectively.Processus terminalis one-fourth as long as base of the segment V, antennal segment III with three circular secondary sensoria, and antennal segments IV and V with one small and one large oval secondary sensoria, respectively.Antennal setae short and pointed, segments II and III each with 2 or 3 setae, respectively, and apex of processus terminalis with three short pointed setae.Rostrum short and small, not reaching the base of the middle coxae, rostral segment IV+V sphenoid, 0.06-0.08 in length, and 1.00-1.60times as long as the second hind tarsal segment, with two pairs of primary and one pair of accessory setae.Hind femur 0.23-0.28,and 2.63-3.06times as long as antennal segment III, hind tibia 0.35-0.47,and 0.49-0.69times as long as body.Length of setae on hind tibia 0.01, 0.25-0.40times as long as middle width of the tibia.First tarsal chaetotaxy: 3, 3, 3. Siphunculi absent.Fore wings with four oblique veins, media veins unbranched, and two cubitus veins converging at the base.Cauda half-moon shaped, smooth, and 0.50-0.75times as long as its basal width, with 2 or 3 short setae.Anal plate oblong, with 5-9 short setae, and genital plate transversely oval with 14-20 short setae.

Biology
The galls of this aphid species are formed on the leaves of the apical part of the stem of Rhus hypoleuca.They are rosy red and flower-like with branches irregularly from the base.The shapes of galls were similar to those formed by Nurudea shiraii, measuring approximately 120 by 100 mm.The alate viviparae appear in late September.The mature galls formed by three Nurudea species on their Rhus primary hosts are shown in Figure 3.

Comments
Nurudea zhengii Ren, sp.nov. is closely related to the two other species of Nurudea, N. shiraii and N. yanoniella, and it is readily distinguished from the two congeneric species by the length of antennal segments, the secondary sensoria on the antennal segments, the shape of the gall formed on Rhus host plants, and the species of the primary host plant.Compared to N. shiraii and N. yanoniella, N. zhengii differs in the following points: antennal segment III and IV have nearly the same length as the base of antennal segment V, antennal segment III with three circular secondary sensoria, and antennal segments IV and V with one small and one large oval sensorium, respectively, and its primary host plant is R. hypoleuca.Therefore, the morphological data support the recognition of N. zhengii as a new species in Nurudea.

Fig. 3 .
Fig. 3. Galls formed by three Nurudea aphid species.A, N. shiraii; B, N. yanoniella; C, N. zhengii.The diameter of the gall formed by N. shiraii in real life is approximately 2-3 times larger than that of N. yanoniella and N. zhengii.