The fern-feeder aphids (Hemiptera: Aphididae) from China: a generic account, descriptions of one new genus, one new species, one new subspecies, and keys

Abstract Fern-feeder aphids (Hemiptera: Aphididae) in China are represented by 13 species in 10 genera, including a new genus, Vietaphisgen. nov. , a new species, Vietaphis aliquantussp. nov. , from Guizhou and Tibet on Plagiogyria japonicum , and a new subspecies, Amphorophora scabripes galbassp. nov. , from Guizhou on Pentarhizidium intermedium . Two genera, Amphorophora Buckton and Idiopterus Davis, and four species or subspecies, Amphorophora ampullate ben-galensis Hille Ris Lambers and Basu, Idiopterus nephrelepidis Davis, Micromyzodium polypodii Takahashi, and Myzus filicis Basu, are reported for the first time in China. Apterae and alatae of Myzus filicis are redescribed herein, and with host plant notes. The fern-feeder aphid genus Ne-omacromyzus Lee is considered a junior synonym of Idiopterus . Furthermore, Neomacromyzus cyrtomicola Lee is transferred to the genus Idiopterus , as Idiopterus cyrtomicola (Lee), comb. nov. , which is herein considered a junior synonym of Idiopterus nephrelepidis Davis. Keys to Chinese fern-feeder species are provided. Morphological figures and biometrical data of Vietaphis aliquantussp. nov. , Amphorophora scabripes galbassp. nov. , and Myzus filicis are presented.


Introduction
Aphids feeding on ferns are few compared to ones on other host plants, such as gymnosperms, herbaceous monocotyledons, or various angiosperm families. Robinson (1966) reviewed 11 species of fern-feeding aphids (Hemiptera: Aphididae) in North America. Subsequently, Miyazaki (1968) reported 10 fern-feeding aphid species distributed in Japan. Jensen and Holman (2000) provided an accurate list of fern-feeding aphids, including 44 species belonging to 14 genera in the world. Thereafter, studies on fern aphids have been limited and only confined to descriptions of a few new species or new genera (Lee 2006;Su and Qiao 2010).
Among aphid samples collected from South and Southwest China, as part of an ongoing survey of Aphididae in Guizhou and Tibet, fern-feeding aphid samples were obtained. Based on these samples, the fern-feeding aphids from China are herein reviewed. Currently, the fern-feeding aphid fauna of China is represented by 13 species or subspecies belonging to 10 genera.
The original description of the apterae of Myzus filicis Basu was very simple (Basu 1969). Here, based on material collected in China, the apterous viviparous female and the hitherto unknown alatae of M. filicis are described in detail. While checking specimens and the literature, we found that Neomacromyzus Lee is a junior synonym of the genus Idiopterus Davis. As a result, Neomacromyzus cyrtomicola Lee is transferred to Idiopterus, as Idiopterus cyrtomicola (Lee), comb. nov., which is herein considered a junior synonym of Idiopterus nephrelepidis Davis.

Materials and Methods
The host plants of all samples of the new species were determined by the staff of Prof. L. Q. Li and Prof. X. C. Zhang, Institute of Botany, Chinese Academy of Sciences, Beijing, China.
Aphid terminology in this paper generally follows Heie (1994) and Qiao et al. (2006). The measurements are in millimeters.
Specimen depositories: the specimens examined in this study, including types, are deposited in the National Zoological Museum of China, Institute of Zoology, Chinese Academy of Sciences, Beijing, China, except the specimens of Micromyzus judenkoi Carver in the Natural History Museum, London, U.K. (BMNH). Tables: Ant. I, II, III
Biology: This aphid colonizes on ferns ( Figure  17A). The oviparous female still can be observed in November in South China. Etymology: The species name consists in "galbus" (= yellow in Latin). The species is named after its yellow body color when it is alive.

Biology:
The species infests scatteringly on the undersides of the distal parts of fronds of fern, and without causing distinct injury (Figure 17B). The species was not attended by ants.
Distribution: China (Chongqing); perhaps Neotropical in origin (Holman 1974), now almost cosmopolitan, but confined to glasshouses and caves in northern temperate regions (Blackman and Eastop 2006).

Biology:
The species feeds on the undersides of fronds of ferns ( Figure 17C), and anholocyclic (Heie 1994). The species was not seen attended by ants.

Macromyzella Ghosh, Basu & Raychaudhuri
Macromyzella Ghosh, Basu & Raychaudhuri, 1977: 582. Type species: Myzus polypodicola Takahashi, 1921. Comment: The genus is found infesting fern species and is mainly distributed in East Asia. The genus is related to Macromyzus, but differs from it in: members of the genus with shorter setae, which are without sclerites at base, and antennal segment III always without secondary rhinaria.

Biology:
The species infests on the undersides of fronds of ferns ( Figure 17D).

Distribution: China (Hunan).
Biology: The species infests the undersides of fronds of fern, without causing any deformations to the hosts, and was not attended by ants.

Biology:
The species colonized on undersides or upsides of fronds and new growth of ferns ( Figure 17G) in many genera. Anholocyclic on ferns in most places, but in Japan, it is apparently also partially heteroecious holocyclic. Adult fundatrices occurred in late April or early May. They infest young leaves and tender shoots of Hydrangea spp., without causing any deformations to the hosts (Miyazaki 1972).

Comment:
The genus was originally described as subgenus of Micromyzus van der Goot, but with 2-3 setae on first tarsal segments, wing veins normal, and alatae with a dorsal spinal patch. The genus is composed of 12 mostly fern-feeding aphids, and only one species distributes in China.

Biology:
The species infests the undersides of fronds of ferns.

Comment:
The genus is related to Micromyzus and Micromyzella, but members of Micromyzodium have long dorsal body setae and are mainly distributed in Asia. Two species colonized ferns worldwide, along with one species distributed in China. Takahashi  Comment: Ten species infesting fern distribute in Eastern Asia. The genus is closed to Micromyzella, but first tarsal segments with 4 setae, and alatae having dark-bordered wing veins and a strongly curved radial sector. Only one species is reported in China.
Head: slightly brown; with sparse wrinkles near eyes dorsally and spinulose ventrally (Figures 12a, 13b). Middle frontal tubercle indistinct, antennal tubercles very developed, with spinulose imbrications, converging at inner sides, with 3 pairs of antennal tubercles setae and a pair of median frontal setae. Dorsal setae of head short and slightly blunt apices, with 2 pairs of setae between antennae, arranged longitudinally and the anterior setae a little longer than the posterior ones; 2 pairs of setae between compound eyes, arranged transversely. Cephalic setae 0.012-0.022 mm long, the anterior dorsal setae about as long as cephalic ones, the posterior ones 0.0025 mm long, 0.70-1.00 and 0.10-0.11 times as long as basal diameter of antennal segment III, respectively. Ventral setae slightly longer than dorsal ones. Eyes with distinct ocular tubercles. Antennae 6-segmented, distal part of antennal segment III and antennal segments IV-VI dark brown, segments I and II smooth except for inner margin of segment I with sparse imbrications, segments III-VI imbricated, ones on segment III weak (Figures 12b,  12c). Antennae 0.63-0.79 times as long as body, length in proportion of segments I-VI: 25-27，16-21，100，53-55，44-46，33-38+85-94; processus terminalis 2.26-2.97 times as long as basal part of the segment. Antennal setae short and blunt, segments I-VI each with 3 or 4, 3 or 4, 5 or 6, 2, 2, 2+3 setae, respectively, apex of processus terminalis with 3 setae; setae on segment III 0.11-0.22 times as long as basal diameter of the segment. Primary rhinaria ciliated, secondary rhinaria absent. Rostrum reaching between middle and hind coxae; ultimate rostral segment wedge-shaped, apex dark brown (Figures 12d, 13c), 1.83-2.05 times as long as its basal width, 1.30-1.31 times as long as second hind tarsal segment, with 6 primary setae and 4 accessory setae.
Thorax: thoracic nota with C-shaped wrinkles. Venter with spinulous transverse rows. Legs short, tarsi brown, coxae with spinules ventrally, distal parts of femora with sparse spinulous imbrications, and distal parts of hind tibiae very weakly spinulous to smooth, others smooth. Hind femur 1.34-1.44 times as long as antennal segment III. Hind tibiae 0.49-0.53 times as long as body; setae on hind tibiae short with acuminate apices, 0.67-0.80 times as long as middle diameter of the segment. First tarsal chaetotaxy: 3, 3, 2. Hind tibiae of nymph with spinules.
Head: brown, and smooth dorsally and ventrally. Middle frontal tubercle indistinct, antennal tubercles low, parallel at inner sides, with 3 pairs of antennal tubercles setae and a pair of median frontal setae. Dorsal setae of head short and slightly blunt apices, with 2 pairs of setae between antennae, arranged longitudinally; 2 pairs of setae between eyes, arranged transversely. Cephalic setae 0.01 mm long, dorsal setae 0.005 mm long, 0.44 times and 0.22 times as long as basal diameter of antennal segment III, respectively. Antennae 6-segmented, dark brown, segments I and II smooth dorsally except for inner margin of segment I sparse imbricated, segments III-VI with imbrications, ones on segment III weak. Antennae 0.71 times as long as body, length in proportion of segments I-VI: 14，11，100 ，48，42，27+88, processus terminalis 3.21 times as long as the base of the segment. Primary rhinaria ciliated, segments III-V with 18-22, 6-8 and 2 or 3 secondary rhinaria, respectively (Figures 14g, 14h). Antennal setae very short and acute, setae on segment III 0.44 times as long as basal diameter of the segment. Rostrum with 6 primary setae and 4 accessory setae.
Thorax: legs long, distal parts of femora with sparse imbrications, and distal parts of hind tibiae very weakly spinulous, others smooth. Hind femora 1.18 times as long as antennal segment III. Hind tibiae 0.51 times as long as body; setae on hind tibiae 0.85 times as long as middle diameter of the segment.
Abdomen: abdominal tergites I-VI smooth, spinal and lateral patches fused with a large brown patch on abdominal tergites IV-V, tergite VI with a brown stripe and lateral areas connected with the dorsal patch, tergites II-VII each with a pair of marginal patches, marginal patches on tergite VI slightly bigger than others, tergite VII with a faint brown band, and tergite VIII with a brown spinal band. Posterior areas of siphunculi, tergites VII and VIII with spinulous stripes. tergite VIII with 4 setae. Siphunculi cylindrical, brown, distinct imbricated, 0.15 times as long as body, 3.86 times as long as its basal width, 2.47 times as long as cauda. Cauda brown, coniform, distal part slightly acute, with 5 setae. Anal plate transverse oval, with 10 setae. Genital plate broad round with 10 posterior setae and 4 anterior setae. Wing veins normal. Others are similar to apterae. Biology: Infesting loosely on the undersides of fronds of fern and without causing distinct injury ( Figure 17I). The species have not been seen visited by ants.

Comment:
The genus is quite distinctive among the Macrosiphini in having reduced tarsi, with first tarsal chaetotaxy 1, 0, 0 and no claws. The genus is represented by a single species feeding on ferns.

Biology:
In spring, the species live on the young growth of Viburnum spp. and alter to secondary hosts of ferns in Japan (Sorin 1962). In Australia, it probably is anholocyclic on ferns (Blackman and Eastop 2006).

Gender: Feminine.
Diagnosis: Body small. Head smooth dorsally and sparse spinulose ventrally. Antennal tubercles developed, parallel or slightly diverging at the inner margins. Eyes with small and distinct ocular tubercles. Antennae 6-segmented, shorter than body length; antennal segment III in apterae without secondary rhinaria, but segments III-V in alatae present. Wing veins normal. First tarsal chaetotaxy: 3, 3, 3. Hind tibiae of nymphs without spinules. Dorsum of head near eyes with C-shaped wrinkles, dorsum of abdomen with C or Oshaped wrinkles in apterae; alatae with dark dorsal patch on abdomen. Marginal tubercles on abdomen absent. Siphunculi cylindrical with dense imbrications, no constricted under developed flange. Cauda coniform, distal half slightly constricted with 5 setae.

Comments:
The new genus belongs to Macroshiphini (Aphidinae) in having spiracle on abdominal tergites I and II placed close together, lateral frontal tubercles pronounced, abdominal segments II-V or I and VII without marginal tubercles. Among these genera feeding on ferns in the world, the new genus is distinguished from its allied genera like Idiopterus Davis, Macromyzella Ghosh, Basu & Raychaudhuri, Macromyzus Takahashi, Micromyzella Eastop, Micromyzodium David and Micromyzus van der Goot, by the following characters, such as C-or O-shaped wrinkles on abdominal tergites, antennal segment III of apterae without secondary rhinaria, apex of siphunculi without reticulations, dorsal setae of body short and blunt, and alatae with normal wing veins. The new genus differs from other genera in morphology shown in the key.
Relatively, the new genus is more closely related to Macromyzella Ghosh, Basu & Raychaudhuri by the shape of the body and siphunculi compared to other fern-feeding aphids, but differs from Macromyzella as follow: (1) dorsum of head with C-shaped wrinkles only near eyes, other areas smooth, abdominal tergites with C-or O-shaped wrinkles (Macromyzella: dorsum of head spinulose, abdominal tergites with reticulations), (2) antennae shorter than body, 0.50-0.80 times as long as body; processus terminalis short, 1.60-3.00 times as long as basal part of the segment (Macromyzella: antennae as long as or longer than body, 1.00-1.30 times as long as body; processus terminalis long, 4.60-5.80 times as long as basal part of the segment), (3) siphunculi without any reticulations under the flange, with imbrications (Macromyzella: siphunculi with 2-3 lines reticulations under flange, other parts with spinule short transverse stripes).
Biology: Usually, the species of the new genus loosely infest on the distal part of the undersides of fronds, and without causing distinct injury.
Head: faint brown. Dorsum of head smooth except for C-shaped wrinkles near eyes dorsally, and sparse spinules and densely wrinkles ventrally (Figures 15a, 16b). Middle frontal tubercle indistinct, antennal tubercles moderate developed with imbrications, slightly diverging at inner sides, 2 pairs of antennal tubercles setae and a pair of median frontal setae. Dorsal setae of head extremely short and slightly blunt apices, 2 pairs of setae between antennae, arranged longitudinally; and 2 pairs of setae between eyes, arranged transversely. Cephalic setae about as long as dorsal setae, 0.0025 mm long, 0.11-0.15 times as long as basal diameter of antennal segment III. Ventral setae of head slightly longer than dorsal ones. Eyes big with small ocular tubercles. Antennae 6-segmented, inner margin of segment I, and segments II-VI dark brown and imbricated (Figures 15b, 16c). Antennae 0.51-0.63 times as long as body length, length in proportion of segments I-VI: 27-29，23-24 ， 100 ， 47-50 ， 44-52 ， 41-45+77-82, segment IV almost as long as segment V, processus terminalis 1.61-2.27 times as long as base of the segment. Antennal setae similar to head dorsal setae, extremely short and blunt, segments I-VI each with 2-4, 3 or 4, 5or 6, 2-4, 2 or 3, 2+3 setae, respectively, apex of processus terminalis with 3 setae, length of setae on segment III 0.003-0.005 mm, 0.11-0.22 times as long as basal diameter of the segment. Primary rhinaria ciliated, secondary rhinaria absent. Apex of rostrum reaching beyond middle coxae. Ultimate rostral segment wedge-shaped, apex dark brown (Figures 15c,  16d), 1.40-1.82 times as long as its basal width, 1.04-1.19 times as long as second hind tarsal segment, with 6 primary setae and 4 accessory setae.
Thorax: thoracic nota with C-shaped wrinkles. Venter with spinulous transverse rows. Legs short, distal parts of tibiae and tarsi brown, coxae with spinules ventrally, distal parts of femora with sparse and distinct imbrications, and distal parts of hind tibiae with weakly spinules, others smooth. Hind femora 1.13-1.32 times as long as antennal segment III. Hind tibiae 0.31-0.38 times as long as body length, setae on hind tibiae short with acuminate to incrassate apices, 0.01-0.03 mm long, 0.50-0.83 times as long as middle diameter of the segment. First tarsal chaetotaxy: 3, 3, 3. Hind tibiae of nymph with spinules.
Abdomen: tergites smooth. Abdominal tergites I and II with spinal and lateral sclerites fused into a broad brown stripe, tergites III-VI with a big brown patch, tergites II-VII each with a pair of marginal sclerites, marginal sclerites on tergites VI slightly bigger than others, marginal sclerites on tergites II-VII, and basal areas of each a pair of spinal setae on tergites III, IV and VI ornamented by spinules. Posterior areas of siphunculi, tergites VII and VIII with spinulose stripes. Dorsal setae slightly longer than ones of apterae. Marginal setae on tergite Ι 0.010 mm long, and tergite VIII with 4 long setae, spinal setae 0.03-0.04 mm long, 0.50-0.57 times and 1.25-2.43 times as long as basal diameter of antennal segment III, respectively. Siphunculi cylindrical, brown, widest at base, distinct imbricated and with a row of striate under developed flange ( Figure  15i), 0.21-0.23 times as long as body, 4.00-4.96 times as long as its basal width, 3.44-3.68 times as long as cauda. Cauda pale brown, coniform, distal half slightly constricted, 1.20-1.48 times its basal width, with 5 setae. Anal plate transverse oval, brown, with 8 or 9 setae. Genital plate broad round and brown, with 12 short posterior setae and 2 anterior setae. Wing veins normal. Others are similar to apterae. Distribution: China (Guizhou, Tibet). Biology: The species infests Plagiogyria japonica, and usually colonizes loosely the distal part of the undersides of fronds ( Figure  17H), and doesn't cause any deformations to the hosts. The species have not been seen attended by ants.