﻿Cavariella Del Guercio (Hemiptera, Aphidinae, Macrosiphini) in China, with a new species, new synonymies, and first country records

﻿Abstract The genus Cavariella is distinguished from other Macrosiphini genera (Aphididae, Aphidinae) because it has a supra-caudal process on abdominal tergite VIII which possesses two setae distally. It is Holarctic in distribution, and half of its species are Asian. The Chinese fauna of this genus, 17 species, have been restudied, morphologically and through DNA barcodes. As a result: Cavariellahidaensis Takahashi is transferred to Elatobium; Cavariellasculptura Qiao & Xu, sp. nov. is described from specimens collected on Torilis and Cryptotaenia (Apiaceae); Cavariellacessana Zhang, Chen, Zhong & Li, syn. nov. and Cavariellalargispiracula Zhang, Chen, Zhong & Li, syn. nov. are respectively junior synonyms of Cavariellaaquatica (Gillette & Bragg) and Cavariellasapporoensis Takahashi; Cavariellagilgiana Zhang, Chen, Zhong & Li and Cavariellalhasana Zhang are confirmed as valid species and complete descriptions are provided; Cavariellabhutanensis Chakrabarti & Das, Cavariellanigra Basu, Cavariellapastinacae (Linnaeus), and Cavariellapustula Essig are recorded for the first time from China. Additionally, keys for species of Cavariella known in China are provided and modifications to the key by Blackman and Eastop of aphid species on Angelica (Aphids on World’s Plants) are presented.

The diversity of the genus seems to be very high in China, but still lacks taxonomic research. Based on examination of specimens of Cavariella in China, the genus is systematically revised in this work; the genus includes 42 species in the world, of which 17 species can be found in China.

Materials and methods
Aphid terminology in this paper generally follows Chakrabarti andDas (2009), Favret (2022), and Blackman and Eastop (2022). The order to record each specimen is as follows: the number of specimens, locality, collection date, collection number, host plant, collector.
In this paper, the following abbreviations are used: DNA barcodes of COI were obtained from the Chinese species. COI DNA barcodes were obtained from specimens belonging to samples listed in Table 1. The methods of extracting DNA and PCR thermal regime followed those of Chen et al. (2015). Sequences were assembled by SeqMan II (DNAStar, Inc., Madison, nae shorter than body length, without secondary rhinaria in apterae; in alatae, Ant. III with circular secondary rhinaria distributed over the whole segment, sometimes the secondary rhinaria protruded, Ant. IV and V usually with circular secondary rhinaria. ABD TERG VIII with a spinal supra-caudal process varying from a very long conical process to an indistinct swelling and possessing two setae distally; in alatae, the supra-caudal process is reduced and wart-like. Siphunculus clavate, swollen distally, sometimes elongated cylinder and not swollen, with imbrications. Cauda elongate conical, conical, or tongue-shaped. Taxonomy. The genus Cavariella has been divided into three subgenera, Cavaraiellia Heinze, Cavariellinepicauda Ivanovskaja, and the nominate subgenus Cavariella Del Guercio. Biology. Most species of the genus characteristically alternate hosts, Salix species being the primary host, and plant species of diverse families, frequently Apiaceae the secondary host. Aphids colonize the aerial parts of plants, mainly tender ones.  (Zhang et al 1999).
Biology. The species feeds on tender tips of Apiaceae (Angelica, Heracleum, Pastinaca, Sium) (Miyazaki 1971;Blackman and Eastop 2022). In China, the species feeds on Salix (Fig. 32E), Heracleum, and Angelica. Hence, the species may be heteroecious holocyclic; Salix is the primary host plant and Apiaceae is the secondary host plant.
Biology. The species was found feeding on Salix (Fig. 32G) and Apiaceae in China, and it also been described feeding on Salix in Bhutan (Chakrabarti and Das 2009). So, the species may migrate between the two plants.
Mounted specimens. Body pale, unsclerotized; Ant. V, distal part of rostrum, HT II brown, other parts pale in color. Body dorsum covered with densely papillate tubercles (Fig. 11A). See Table 2 for general measurements.
Abdomen. Abdominal tergites with circular and semicircular sculptures on spino-pleural areas, marginal areas with papillate tubercles (Figs 10F, 11F, H). ABD TERG VIII produced caudad into triangular spinal supra-caudal process and covered with papillate tubercles, constricted and blunt at distal part, exceeding to the end of cauda (Figs 10H, 11J). Dorsal setae of abdomen long, thick, and capitate (Figs 10E, 11J); abdominal tergites I-V each with two or three pairs of spino-pleural setae and one or two pairs of marginal setae, tergite VI with one pair of spinal and one pair of marginal setae, tergite VII with one pair of spinal, pleural and marginal setae, respectively; tergite VIII with two setae at apex and 2-4 marginal setae of supra-caudal process. Spiracles reniform and open. SIPH long clavate, basal 1/2 cylindrical and then gradually swollen towards apical part but constricted at apex (Figs 10G, 11I); basal part smooth, distal part with imbrications, with flange. Cauda pentagonal (Figs 10I, 11K), constricted at base and distal part, with spinulose imbrications and 2-5 setae. Anal plate semicircular, spinulose, with 8-12 setae. Genital plate transversely oval, with sparse spinules in transverse rows, with two anterior setae and six or seven setae along the posterior margin.
Comment. The species was first described by Zhang et al. (1999), but the description was brief and incomplete. So, a detailed description, character illustration, ecological photographs, and DNA barcoding are supplied in this work.
Biology. Primary host plant: Salix, and the aphids feed on young stems (Fig. 33A). Secondary host plant: Apiaceae, and the aphids feed on upper sides of leaves and with ant-attendance ( Fig. 33B, C).

Cavariella konoi
Comment. Cavariella konoi was first described in China by Zhang et al. (1999), but by checking the specimens, it was established that they were misidentified and should be Cavariella nigra Basu, 1964. Biology. The species was found feeding on the undersides of leaves of Salix ( Fig. 33D) in China, and it migrate between Salix and Apiaceae (Blackman and Eastop 2022). Distribution. China (Jilin), Canada, Denmark, Finland, Germany, Japan, Mongolia, Norway, Poland, Russia, Sweden, UK, USA.
Re-description. Apterous viviparous females: body oval, green in life.
Mounted specimens. Body pale, unsclerotized; Ant. V and VI, distal part of rostrum, HT II, SIPH, cauda and anal plate pale brown, other parts pale in color (Fig. 16A). See Table 2 for general measurements.
Thorax. Thoracic nota with oval and semicircular sculptures, distinctly at marginal areas. Dorsal setae of thorax short and blunt; pronotum with two pairs of spinal setae, arranged anteriorly and posteriorly, one pair of pleural and one pair of marginal setae. Legs short. Distal part of femora and tibiae slightly imbricated. Setae on legs short and blunt. First tarsal chaetotaxy: 3, 3, 3. Second tarsal segments with imbrications.
Thorax. As in apterous viviparous females except as follows: dorsum of thorax smooth. Legs normal. Setae on legs long and pointed. Fore wing radius bent, media twice-branched, two cubitus; hind wings with one long longitudinal vein and two obliques. Abdomen. Abdominal tergites I-VII each with one pair of brown marginal sclerites; tergite I with a band at spino-pleural areas, tergites II-V with a brown quadrate sclerite at spino-pleural areas, tergites VI-VIII each with a brown band. Dorsum of abdominal tergites with spinulose imbrications at sclerites, others smooth. Abdominal tergites I-IV each with one pair of small marginal tubercles; ABD TERG VIII with a short warty supra-caudal process (Figs 15K, 17F), with two pointed setae at apex. Dorsal setae of abdomen long and pointed. SIPH clavate, basal 1/2 cylindrical and then distinctly swollen towards apical part but constricted at apex (Fig. 17E); basal 2/3 with wrinkles, distal 1/3 imbricated, with flange. Cauda conical (Fig. 17G), with spinulose imbrications and five setae. Anal plate semicircular, spinulose, with 12-15 setae. Genital plate broadly round, with sparse spinules in transverse rows, with two anterior setae and seven setae along the posterior margin. Others as in apterous viviparous females.
Comment. The species was described by Zhang and Zhong (1981) in China and was considered as synonym of Cavariella aegopodii in Blackman and Eastop (2022). By checking the six syntypes of the species, it is sure that the species resembles Cavariella aegopodii in dorsum sculptures, conical supra-caudal process, the shape of URS, but the species differs from C. aegopodii as follows: URS 0.94-1.07× HT II (C. aegopodii: URS distinctly shorter than HT II, 0.73-0.83× HT II); PT 1.08-1.59× Ant. VIb (C. aegopodii: PT mostly shorter than Ant. VIb); SIPH thick clavate, distal part distinctly swollen, the swollen wide 1.82-1.91× distal wide (C. aegopodii: SIPH clavate, the swollen wide 1.37-1.72× distal wide). Due to these differences in major characters, we remove C. lhasana from synonymy with C. aegopodii and reinstate it as a valid species.
The species resembles Cavariella aspidaphoides in ABD TERG VIII hooded supra-caudal process; dorsum of body with circular sculptures; but differs from C. aspidaphoides as follows: supra-caudal process only with two setae distally (C. aspidaphoides: supra-caudal process with two setae distally and 3-5 short setae marginally); URS with one pair of accessory setae (C. aspidaphoides: URS without accessory setae); PT shorter than Ant. VIb (C. aspidaphoides: PT longer than Ant. VIb).
Description. Apterous viviparous females: body oval, dorsum of body sclerotized, black and ridged, turtle-shaped, venter of abdomen flat and pink, appendages black distally, other parts pale in life (Fig. 36). Nymphs: body pick or orange in color, appendages black distally, thoracic nota and abdominal tergites each with one pair of black spinal and marginal patches, other parts pale in life (Fig. 36B).
Mounted specimens. Body dorsum sclerotized and inconsistently black, spinal area dark brown and pleuro-marginal area pale brown in color (Fig. 25A). Ant. I, II, V, and VI brown, other parts pale brown in color. Legs and SIPH pale brown; cauda and anal plate dark brown in color. Body dorsum covered with densely circular or semicircular sculptures which more developed on spino-pleural areas. See Table 2 for general measurements.
Thorax. Thoracic nota with semicircular and irregular circular sculptures on spino-pleural areas, marginal areas with semicircular sculptures which sparser than spino-pleural areas. Pronotum mostly with one pair of small marginal tubercles. Dorsal setae of thorax short and pointed; pronotum with two pairs of spinal setae, arranged anteriorly and posteriorly, one pair of pleural and one pair of marginal setae; mesonotum with 6-11 spino-pleural setae and two pairs of marginal setae; metanotum with 4-6 spino-pleural setae and two pairs of marginal setae. Legs normal. Distal part of femora with oval and imbricated sculptures; distal part of tibiae imbricated. Setae on legs short and pointed. First tarsal chaetotaxy: 3, 3, 3. Second tarsal segments with imbrications.
Abdomen. Abdominal tergites I-VI with densely circular sculptures on spino-pleural areas (Figs 24E, 25F) and sclerotized dark brown, marginal areas with sparsely semicircular sculptures; abdominal tergite VII with circular sculptures on spino-pleural areas, marginal and posterior with papillate tubercles; ABD TERG VIII with densely papillate tubercles (Fig. 25I). Abdominal tergites I-IV mostly each with one pair of small marginal tubercles; ABD TERG VIII with short cylindrical supra-caudal process covered with semicircular sculptures (Fig. 25H), 0.06-0.07 mm, 1.11-1.43× basal width. Dorsal setae of abdomen short and pointed; abdominal tergites I-V each with two pairs of spinal setae, one pair of pleural and one pair of marginal setae, tergite VI with one pair of spinal, pleural, and marginal setae respectively, tergite VII with one pair of spinal setae; tergite VIII with two spinal setae at apex of supra-caudal process.
Alate viviparous females: body long oval; head and thorax black, abdomen pink, abdominal tergites with a quadrate patch in life (Fig. 36C).
Mounted specimens. Head and thorax black-brown, antennae, legs, distal part of rostrum, SIPH, cauda and anal plate brown, other parts pale in color (Fig. 26A). See Table 2 for general measurements.
Head. As in apterous viviparous females except as follows: dorsum of head smooth. Frons convex, antennal tubercles slightly prominent, not higher than frontal tubercle. Antennae lost (in this specimen). Rostrum reaching mid-coxae.
Thorax. As in apterous viviparous females except as follows: dorsum of thorax smooth. Legs normal. Fore wings radius bent, media twice branched, two cubitus; hind wings with single long longitudinal vein and two obliques.
Abdomen. Abdominal tergites I-V each with one pair of marginal sclerites; tergite I with scattered small sclerites at spino-pleural area, tergite II with a brown band at spino-pleural area, tergites III-VI with a brown quadrate sclerite at spino-pleural areas, tergites VII and VIII each with a across brown band (Fig. 26A). Abdominal tergites with spinulose imbrications at sclerites, others smooth. Abdominal tergites I-IV each with one pair of small marginal tubercles; ABD TERG VIII with a short warty supra-caudal process and with two long and pointed setae at apex (Fig. 26B). Cauda conical (Fig. 26C), with spinulose imbrications and five setae. Anal plate semicircular, spinulose, with 16 setae. Genital plate broadly round, with sparse spinules in transverse rows, with two anterior setae and ten setae along the posterior margin. Others as in apterous viviparous females.
Etymology. The new species is named for its sculptures on the dorsum of body. Comment. The species resembles Cavariella nigra in body dorsum sclerotized; URS long wedge-shaped; short supra-caudal process, but differ from it as follows: dorsum of body ridged, turtle-shaped, venter of abdomen flat and pink in color, appendages black distally, other parts pale in life; in nymphs: body pink or orange in color, appendages black distally, other parts pale (C. nigra: dorsum of body flat, venter of abdomen yellowish white in color; appendages black wholly in life; in nymphs: body yellowish white in color, appendages black wholly in life); body dorsum sclerotized and inconsistently black in specimens, spinal area of dorsum dark brown and pleuro-marginal ones of dorsum pale brown in color; the SIPH pale brown and same as pleuro-marginal area of dorsum in color (C. nigra: body dorsum sclerotized and uniformly black in specimens, the SIPH black brown and same as dorsum of body); marginal area of body with semicircular sculptures (C. nigra: marginal area of body with papillate tubercles).
Diagnosis. The species of the subgenus mostly feed on Apiaceae and are covered with wax in life (Fig. 37). In collected specimens, abdominal tergites I-IV often have circular marginal tubercles; ABD TERG VIII with indistinct supra-caudal process, shorter than Ant. II; rostrum long, sometimes reaching abdominal tergite IV, URS elongated wedge-shaped; cauda tongue-shaped, with > 8 setae; SPHI long cylindrical, with distinct flange, not swollen. Comments. The subgenus contains five species, with only two species distributed in China. Cavariella largispiracula Zhang, Chen, Zhong & Li, 1999 is considered as a junior synonym of Cavariella sapporoensis Takahashi, 1961. Cavariella hidaensis Takahashi, 1961 should be removed to Elatobium Mordvilko, 1914 based morphological and molecular data. Diagnosis. Body white, covered with wax in life (Fig. 37A); thoracic nota and abdominal tergites I-IV each with one pair of circular marginal tubercles (Fig. 27E, G, H); thoracic nota and abdominal tergites I-IV each with one or two pairs of pale brown marginal sclerites, tergites V and VI often with small brown spino-pleural sclerites, tergites VII and VIII each with a brown sclerotic band (Fig. 27I); dorsal setae short and blunt; rostrum reaching abdominal tergite III, URS elongate wedge-shaped, with five or six secondary setae (Fig. 27D); cauda tongue-shaped (Fig. 27K), with 8-13 setae (Qiao et al. 2005).
Comment. The species resembles Cavariella sapporoensis, but the main differences between the two species are as follows: abdominal tergites I-IV sclerotized, tergites VII and VIII each with a brown sclerotic band (C. sapporoensis: only abdominal tergites VII and VIII sometimes with a brown sclerotic band); dorsal setae short and blunt (C. sapporoensis: dorsal setae very long and pointed, curved distally). Biology. The species feeds on undersides of leaves near the roots of Apiaceae (Cicuta virosa) and is with ant attendance (Fig. 37A) (Qiao et al. 2005 Diagnosis. Pronotum and abdominal tergites I-IV each with large and circular marginal tubercles, larger than spiracles (Fig. 29D, F); setae of legs very long, pointed, dense, and curved apexes (Fig. 29G, H), the setae on femora 0.57-0.78× of widest width, the setae on tibiae 0.97-1.39× of mid-width; cauda tongue-shaped, with 9-16 long and pointed setae (Fig. 29M) (Takahashi 1961).
Comment. After researching the holotype of Cavariella largispiracula Zhang, Chen, Zhong & Li, 1999, we found the species is in fact without large circular spiracles, which are in fact marginal tubercles and with normal reniform spiracles (Fig. 31A, C). In C. largispiracula, thoracic nota and abdominal tergites I-IV each with one pair of large marginal tubercles (Fig. 31C); abdominal tergites VIII with a slightly swollen supra-caudal process (Fig. 31D); cauda tongue-shaped (Fig. 31F); setae of legs very long and pointed (Zhang et al. 1999). Therefore, Cavariella largispiracula Zhang, Chen, Zhong & Li, 1999 is considered as a junior synonym of Cavariella sapporoensis Takahashi, 1961. The species resembles Cavariella heraclei Takahashi, 1961, but differs from it as follows: setae of legs long, pointed, dense, and curved apexes (C. heraclei: setae of legs short, blunt, sparse); cephalic setae long and pointed, 1.31-2.74× Ant. IIIBD (C. heraclei: cephalic setae short and blunt, 0.50× Ant. IIIBD); setae of Ant. III long and pointed, 0.86-1.24× Ant. IIIBD (C. heraclei: setae of Ant. III short, 0.50× Ant. IIIBD) (Takahashi 1961).   Biology. The species is usually collected from Apiaceae and feeds on the undersides of leaves with ant attendance (Fig. 37B-D). In China, the apterous oviparous female of the species was found feeding on the leaves of Salix in October. So, the species may alternate host between Salix and Apiaceae.
Distribution. China (Beijing, Gansu, Jilin), Japan.   Figure 34. The ecological habitat photographs of Cavariella nigra Basu in field A two apterae feeding on underside leaves of Salix in spring B the apterae and nymphs feeding on tender stem of Salix in summer C the species feeding on Salix with ant-attendance D the nymphs feeding on tender stem of Salix in summer E, F the species feeding on Apiaceae. Figure 35. The ecological habitat photographs of Cavariella in field. A the apterae and nymphs of Cavariella nipponica Takahashi feeding on the underside leaves of Salix B one aptera of Cavariella pastinacae (Linnaeus) feeding on tender stem of Apiaceae C the apterae and nymphs of Cavariella pustula Essig feeding on tender stem of Salix D the apterae and nymphs of Cavariella salicicola (Matsumura) feeding on tender stem of Salix. Figure 36. The ecological habitat photographs of Cavariella sculptura Qiao & Xu, sp. nov. in field A, B the apterae and nymphs feeding on tender stems of Apiaceae (Torilis scabra) with ant-attendance C one alate, apterae and nymphs feeding on tender stem of Apiaceae (Torilis scabra) D the apterae and nymphs feeding on tender stem of Apiaceae. Figure 37. The ecological photos of Cavariella (Cavariellinepicauda) in field A one alate, apterae and nymphs of Cavariella cicutisucta Qiao feeding on tender stem of Apiaceae B the apterae and nymphs of Cavariella sapporoensis Takahashi feeding on tender stem of Apiaceae C the apterae and nymphs of Cavariella sapporoensis feeding on tender stem of Apiaceae with ant-attendance D one alate of Cavariella sapporoensis feeding on tender stem of Apiaceae.

Keys to the species of Cavariella in China
Key to apterae

DNA barcoding
The DNA barcodes of nineteen species of Cavariella were used, including the new species and others from China. The final alignments of COI sequences consisted of 658 nucleotides, including 162 parsimony-informative sites. Pairwise sequence divergences of COI among the Cavariella species are presented in Table 3. The interspecific genetic distances of the genus averaged 7.78% (range 2.34%-9.46%) and the divergence of the new species to others averaged 7.24% (4.84%-9.42%). The validity of each species was well-supported on NJ tree (Fig. 38). Cavariella hidaensis formed a clade with the genus Elatobium, so the NJ tree verified that the species should be removed to Elatobium, also, confirming morphological examination. Combination of the morphological characters and DNA barcodes supported the species of the genus Cavariella.

Discussion
After checking many specimens of Cavariella, the genus can be distinguished by a convex frons with undeveloped antennal tubercles, the dorsum of the body is covered with irregular sculptures, abdominal tergites VIII with a supra-caudal process and two distal setae, and the siphunculus is mostly clavate. The main characters used to distinguish the species within the genus mainly focus on the ratios of PT/Ant. Vb or Ant. VIb, URS/HT II, the ratio of the supra-caudal process/cauda, and the ratio of SIPH/cauda as well as the shapes of dorsal sculptures, the supra-caudal process, and the shape of SIPH. Because most species in the genus are green or yellow-green in life and feed on the tender tips of host plants, it is difficult to distinguish them using their ecology and habits. The DNA barcodes have successfully divided them, so it can assist to identify the species in the genus easily.

The taxonomic status of Cavariella (Cavariellinepicauda) hidaensis Takahashi
The species was first described by Takahashi in 1961 based on the body dorsum having wavy and semicircular wrinkles; the SIPH was long, cylindrical, and not swollen, and feeding on Salix. However, the species has no supra-caudal process on ABD TERG VIII and with four setae on it, so there are no typical characters to place it into Cavariella Del Guercio. Miyazaki (1971) considered this species as belonging to Elatobium Mordvilko based on the head bearing prominent antennal tubercles which were higher than the median tubercle; SIPH long and cylindrical, curved outward distally; cauda long, conical, and constricted at the median; ABD TERG VIII flat with four setae and without a supra-caudal process. However, the classification status change of the species was not accepted by Blackman and Eastop (2022) or Favret (2022), and Cavariella hidaensis still remains in Cavariella.
We have combined morphological characters and DNA barcoding to confirm that the species should be placed in Elatobium (Fig. 38). Therefore, Cavariella hidaensis Takahashi, 1961 is transferred to Elatobium hidaensis (Takahashi, 1961).