Melaphis Walsh, Reference von Dohlen, Kurosu and Aoki1867

Type species. Brysocrypta rhois Fitch, Reference Fitch1866.

Synonym. Truncaphis Theobald, Reference Theobald1918 (type species Truncaphis newsteadii Theobald, Reference Theobald1918).

Life history. The Melaphis species described here have a complex life cycle involving alternation between Rhus species and mosses, with at least five parthenogenetic generations and one sexual generation, exhibiting nine functionally and morphologically distinct body forms: (1) the biparental fundatrix that initiates gall formation on the primary host with two functional forms – a vagile first instar and relatively sessile later instars; (2) the wingless offspring of the fundatrix (fundatrigenia, possibly more than one generation); (3) a winged generation that leaves the gall and migrates to the secondary host (fundatrispuria or emigrant); (4) one or more (at least facultatively) wingless generations on the secondary host (alienicola or exulis) with two different types of first instars: a vagile black form deposited by the fundatrispuria, and a yellow, less active form deposited by the adult alienicolae; (5) a winged generation that migrates from the secondary host to the primary host (sexupara or remigrant); (6) the sexual generation (male and sexual female) that lack wings and mouthparts, the female producing only one offspring. Unlike other host-alternating Eriosomatinae, migration to the primary host occurs in the spring, rather than the autumn; thus the sense of the terms “spring migrant” and “fall migrant” commonly applied to host-alternating aphid life cycles is reversed in this group, and will be avoided.

Migration from moss begins in mid-May in Ontario and west Québec, with sexuparae forming loose aggregations and depositing sexuals on previous year twigs of Rhus at the time that expansion of current year shoot buds begins. Small aggregations tend to occur within a few centimetres below the expanding leaf, but large aggregations may consist of >100 individuals scattered along 0.5 m of stem. There they deposit larvae of the sexual forms and die immediately thereafter. Although sexuals are initially found scattered along the stem, moulting individuals are more densely clustered close to the base of the expanding shoot (but usually still below the lowest of these shoots) suggesting a further active aggregation by first instar sexuals. The sexuals undergo four moults over a period of four or five days.

In most aphids, the sexual female lays an egg, which is the overwintering form. Moran (Reference Moran1989) postulated that eggs laid on Rhus in the spring remained dormant until the following spring in a biennial life cycle. However, the sexual female is in fact ovoviviparous. Complete development of the single embryo within the shell-less egg takes place within the body of the living sexual female, and the larval fundatrix emerges from the membranous egg immediately after deposition, as described by Takada (Reference Takada1991) for Schlechtendalia chinensis (Bell). Thus, the usual practice among aphid workers of using the term ovipara for the sexual female is inappropriate in this group.

Deposition of larval fundatrices begins two to three weeks after copulation, i.e. in early to mid-June. The first instar fundatrix moves to the distal unexpanded leaves of the new shoot, where it may remain for several days, apparently initiating feeding only after the leaflets begin to unfold. Within one or two days of settling, feeding by the fundatrix on the upper (adaxial) surface of a leaflet results in the formation of an obvious pocket on the abaxial surface of the leaflet opening onto the adaxial surface. Subsequent instars of the fundatrix occur within the closed gall. As a consequence of aggregation by the sexuparae, galls tend to occur in clusters, so that a single compound leaf usually bears several galls (Fig. 6) and often many leaves of a single shoot are affected.

Fig. 6

Galls of Melaphis species on Rhus typhina. A. Immature galls in early July, view of adaxial surface of leaf. B. Aggregation of mature galls, Odessa, Ontario, September 1992. C–D. Mature galls of M. asafitchi showing variations in shape, Marlborough Forest, Ottawa, Ontario, September 2014.

At least three generations develop within the gall, namely the fundatrix, at least one generation of apterae, and the alate emigrants. We have found living fundatrices containing embryos as late as mid-August. Adult alatae begin to appear within the gall in mid to late August (in North Carolina, alates collected as early as 7 August (slides in USNM)) and continue to develop throughout September; some alatoid nymphs may still be present in galls as late as early October. The gall opens by formation of longitudinal slits in the neck of the gall after the majority of individuals have become adult. In Ontario, migration to moss occurs over an extended period from the mid-September to early October, as the host leaves begin to senesce and fall; in Virginia, United States of America they “may be found flying at the last of October” according to Baker (Reference Baker1917). During this period, infested leaves are often apparent from a distance because they tend to senesce and redden earlier than other leaves of the same plant. Open galls are subject to heavy predation by Syrphidae (Diptera) larvae. The number of alates produced in a single gall is usually in the hundreds, but we have observed up to 3750 developing within large galls.

Apterae and developing sexuparae on moss develop within a loose cocoon-like wax cell. Summer generations on moss do occur; we have reared both sexuparae and larvae of a further moss-feeding generation from the same moss sample collected in early May, and Moran (Reference Moran1989) reports that she established “long-lived” colonies on moss. Populations in Europe currently assigned to Melaphis rhois appear to persist entirely on mosses (Heie Reference Heie1980) as do populations in Washington State (Pike et al. Reference Pike, Graf, Foottit, Maw, von Dohlen and Harpel2012). However, the required minimum number of generations on moss is unknown. Various stages in the life history of Melaphis species are illustrated in Supplementary Figure S1.

Host plants. Galls of Group 1 and Group 2 have both been found on both Rhus glabra Linnaeus and Rhus typhina Linnaeus; Group 3 galls have so far been collected only on R. glabra. Known moss hosts include Haplocladium microphyllum (Hedwig) Brotherus (Leskeaceae) (Moran Reference Moran1989), Dicranum scoparium Hedwig (Dicranaceae), Rhytidiadelphus loreus (Hedwig) Warnstorf (Hylocomiaceae) (Pike et al. Reference Pike, Graf, Foottit, Maw, von Dohlen and Harpel2012), and Polytrichum juniperinum Hedwig (Polytrichaceae) (our observations). We have observed feeding on the moss rhizoids in contact with the rock substrate, but the label on a slide from North Carolina, United States of America in the USNM states “feeding in leaf axils”.

Generic diagnosis. In North America, alate forms may be separated from other Fordini by the transverse, linear, secondary rhinaria; and from other Eriosomatinae by the combination of: lack of siphunculi, setae associated with the wax-gland plates outside the adjacent plate (Fig. 10G) (within the plate in Pemphigini), wax plates composed of an aggregation of similar facets (at least some wax plates with facets in a ring-like or rosette-like arrangement in many Eriosommatini), and the more-or-less concave inner margin of the pterostigma beyond radial vein (Fig. 12). Apterae on moss are distinguished by tarsal fusion and wax-gland pattern, as in the key by Pike et al. (Reference Pike, Graf, Foottit, Maw, von Dohlen and Harpel2012). Other apterous forms are easily distinguished by the obligatory association with Rhus.

Emigrants from the gall may be separated from Asian Melaphidina by the combination of short pterostigma (elongate and reaching wing apex in Schlechtendalia (Blackman and Eastop Reference Blackman and Eastop1994, Reference Blackman and Eastop2017)) and possession of numerous transverse, narrow rhinaria (versus fewer, broad and band-like or extensive plate-like rhinaria in most Asian species) with simple margins (spinulose margins in Nurudea meitanensis (Tsai and Tang)) (Yang et al. Reference Yang, Chen, Feng and Chen2009).

Generic description. General characteristics. Siphunculi absent. Ultimate rostral segment without accessory setae, but with anterior primary setae displaced basad. When facetted wax-gland plates are present, each with a single associated seta located outside of the plate.

All apterous morphs with compound eye absent (except for triommatidion) and without secondary antennal rhinaria.

All alate forms with apex of pterostigma acute, often with the posterior margin of the pterostigma beyond the origin of the radius slightly concave (Fig. 12); secondary rhinaria transverse-linear; in individuals with all four antennal flagellum fully developed, first flagellomere is the longest, second and third shortest and similar in length, fourth 0.6–0.9 times first.

Fundatrix, first instar (Fig. 7). In life dark with caudal wax filaments. Body sclerotic; dorsal setae relatively long, spine-like, longest as long as antennal pedicel; wax glands not aggregated into facets. Spiracles conspicuous, circular; thoracic spiracles about twice diameter of abdominal spiracles. Antenna with four antennomeres (i.e., with two flagellomeres). Scape broader than long, about 1.5 times diameter of pedicel. First flagellomere about as long as or a bit longer than pedicel; with a single subapical seta; primary rhinarium transversely oval. Ultimate flagellomere with terminal process about half length of basal part, with four terminal setae; basal part with two setae; primary rhinarium circular. Ultimate rostral segment with anterior primary setae displaced to middle of segment. Each tarsus (Fig. 10A) with basitarsus distinct, but broadly joined to distitarsus; apico-ventral basitarsal setae 2, long (reaching or slightly exceeding base of claw); apicodorsal setae of distitarsus about twice length of claw, curved, finely capitate; pretarsal setae (i.e., setiform parempodia on unguitractor plate) curved, reaching apex of claw; claw slender, attenuate, about one-third length of distitarsus.

Fig. 7

Fundatrix of undetermined Melaphis species, first instar. A. Dorsal aspect of CNCHEM007770.1. B. Ventral aspect of CNCHEM007071.1. C. Lateral aspect of CNCHEM007770.1. Scale bar=100 µm.

Fundatrix, adult. In life, yellow, globular. All setae minute, inconspicuous. Wax glands not aggregated into facets, body with an even light wax coat. Antennae with four antennomeres, ultimate antennomere longest. Rhinarium of first flagellomere round, set basad of distal margin of flagellomere; terminal process of ultimate flagellomere about 0.25 length of basal part of flagellomere. Ultimate rostral segment short, 1.0–1.5 times longer than basal width. Trochanter fully fused to femur; tibia shorter than femur of same leg. Tarsi with basitarsus broadly fused to distitarsus, demarcation line distinct to obscure; two inconspicuous basitarsal setae about 0.2 time ventral length of basitarsus; apicodorsal setae of distitarsus about as long as distance from base of seta to base of claw; pretarsal setae obscure, less than thickness of unguitractor plate. Cauda with two setae.

Fundatrigenia (second generation aptera in gall). In life bright yellow, globular; smaller than fundatrix and with appendages relatively longer. Wax glands aggregated into facetted plates. Antenna with four to six antennomeres, usually five. Ultimate antennomere with terminal process <0.15 times base. Trochanter fused with femur without obvious demarcation. Basitarsus and distitarsus broadly joined but demarcation usually distinct; with two or three basitarsal setae. Claw about one-third length of distitarsus, with attenuate apex; pretarsal setae not apparent. Cauda usually with four setae (range 2–4).

Fundatrispuria (alate emigrant from gall). In life, dark, abdomen dark green (overall appearance dark grey due to wax bloom), wings hyaline with green pterostigma. Body length 1.0–1.7 mm. Slide-mounted specimens with head and pterothorax darkly pigmented; legs (including coxa), antenna, cauda, genital, and anal plates pigmented but paler than head and pterothorax; pronotum lightly pigmented or hyaline; abdominal tergite 8 hyaline, or with lightly to distinctly pigmented scleroites at bases of setae; abdomen otherwise hyaline. Antenna (Fig. 8A–I) with six antennomeres (Fig. 8A–B, 8D–E), but often with first and second flagellomeres partially or completely fused to give an apparent antenna with five antennomeres (Fig. 8F–G) (often bilaterally asymmetrical in same individual; in almost all such antenna, at the point of fusion a hyaline area of cuticle is present on the dorsal surface and the rhinaria are distorted); occasionally with second and third (Fig. 8C) or first through third (Fig. 8H) flagellomeres fused; terminal process of distal flagellomere about 0.1 times length of base. Primary rhinarium of penultimate flagellomere fused with distal secondary rhinarium, often forming a broad band-like field; primary rhinarium of ultimate flagellomere sometimes fused with irregular patch-like or band-like distal secondary rhinarium and represented by sections of ciliate margin, or separate but largely enveloped by arms of an irregular patch-like or branched secondary rhinarium; accessory rhinaria of ultimate flagellomere usually remain separate. Secondary rhinaria present on all flagellomeres; transverse, usually narrow and separated by at least their own width, occasionally adjacent rhinaria anastomosing or fused into a broader band; extending up to three quarters of circumference of flagellomere, usually not extending onto mid-dorsal surface but occasionally forming a complete ring encircling the flagellomere. Basal half of basal flagellomere surface generally smooth, with obscure transverse rows of minute spinules distally; distal flagellomeres more distinctly spinulose (occasionally a row of spinules aligned with margin of a secondary rhinarium thus appearing as if the rhinarium has a spiculose margin). Trochantero-femoral suture incomplete, apparent only on anterioventral surface of mesothoracic and metathoracic legs and on posteroventral surface of prothoracic leg. Basitarsus most often with three, less often with two, apico-ventral setae; when three present the middle seta sometimes displaced basad, rarely with a single additional plantar seta. Plantar surface of distitarsus with five to nine pairs of setae. Full complement of facetted wax-gland plates distributed as follows: four pairs on head (but some or all are frequently missing or reduced to single facet, or the area represented by a roughened patch without distinct facets: one rarely expressed pair on anteroventral surface of head anterior to median ocellus, one infrequently expressed pair near anterodorsal margin of head, one pair between lateral ocelli, one pair near posterior margin of head), two pairs on pronotum, one pair near posteromedian margin of mesonotal lobes, one pair on metanotum (often absent), three pairs on each of abdominal terga 1–6, and two pairs on abdominal tergite 7, sometimes merging to form one or two continuous plates, zero to two pairs on abdominal tergite 8 (Fig. 9). Abdominal tergite 8 with four to nine setae (usually six to eight). Forewing with pterostigma not reaching wing apex; media unbranched, atrophied basally, sometimes also missing apically, or rarely not apparent for entire length; cubital veins approximate at base, usually complete to base. Hind wing with two transverse veins arising separately. Cauda with two to six setae, usually four.

Fig. 8

Antenna of alate forms of Melaphis species. A–H. Alatae from gall (fundatrispuriae). A–B. Melaphis rhois CNCHEM085826.6, dorsal and ventral aspect. C. Melaphis rhois CNCHEM085823.5, dorsal aspect showing fusion of second and third flagellomeres. D–E. Melaphis asafitchi CNCHEM085637.1 dorsal and ventral aspect. F–G. Melaphis asafitchi CNCHEM084142.9 dorsal and ventral aspect with fusion of first and second flagellomeres. H. Melaphis asafitchi CNCHEM085796.2, dorsal aspect with fusion of first to third flagellomeres. I–L. Melaphis asafitchi, sexupara: I–J. CNCHEM85936.26, dorsal and ventral aspect. K–L. CNCHEM85937.21, dorsal and ventral aspect, showing fusion of first to third flagellomeres. Scale bar=100 µm.

Fig. 9

Apex of abdomen of fundatrispuriae of Melaphis species showing distribution of wax glands. A. Melaphis asafitchi CNCHEM085786.5, without wax glands on abdominal tergite 8. B. Melaphis rhois CNCHEM084807.4. Scale bar=100 µm.

Alienicola (exulis), first instar (deposited by fundatrispuria) (Fig. 10E–F). Grey-black in life. Antenna with four antennomeres; rhinarium of basal flagellomere small, round, with distinct fringe of cilia; ultimate flagellomere with transverse rows of small spinules; rhinarium of ultimate flagellomere transversely oval, distinctly ciliate. Basitarsus broadly fused to distitarsus (Fig. 10C), but demarcation line distinct; ventral basitarsal setae 2, about as long as ventral length of basitarsus; distitarsus with a few transverse rows of spinules; apicodorsal setae of distitarsus reaching middle of claw; claw with distal part long and slender; pretarsal setae reaching end of claw. Body with full complement of wax plates (three pairs on head, two pairs on pronotum, two pairs on mesonotum and metanotum, three pairs on abdominal segments 1–7, zero to two pairs on abdominal segment 8) (Fig. 10G). Cauda with two setae.

Fig. 10

Melaphis species. A–C. Metatarsus. A. Fundatrix first instar CNCHEM007071.1, species undetermined. B. Melaphis asafitchi, alienicola first instar from fundatrispuria CNCHEM085814.10. C. Sexual female first instar CNCHEM007375.1, species undetermined. D. Adult sexual female CNCHEM007771.1, postpartum, habitus, undetermined species. E–F. First instar alienicolae from fundatrispuriae. E. Melaphis rhois CNCHEM085811.4, habitus, ventral aspect. F–G. Melaphis asafitchi CNCHEM085814.10. F. Habitus, ventral aspect. G. Apex of abdomen, dorsal aspect, showing distribution of wax glands and setae. Scale bar for A–C, G=50 µm. Scale bar for D–F=100 µm.

Alienicola aptera (exulis; aptera on moss). In life, dull yellow to somewhat greyish yellow, surrounded by loose wax filaments; legs (including coxae) and antennae brown to dusky; front of head, cauda, anal, and genital plates dusky. Body with facetted wax plates (three pairs on head, two pairs on pronotum, two pairs on mesonotum and metanotum, three pairs on abdominal segments 1–7, zero to two pairs on abdominal segment 8). Antenna with fout to five antennomeres, ultimate antennomere longest. Metatibia shorter than, to about as long as, metafemur. Basitarsus broadly fused to distitarsus (Fig. 10B), separation sometimes at least partially demarcated by unpigmented line or irregular window along the line of fusion; ventral basitarsal setae 2, shorter than length of ventral surface of basitarsus; apicodorsal setae shorter than distance from base of these setae to basal articulation of claw. Cauda with two setae. Measurements given by Pike et al. (Reference Pike, Graf, Foottit, Maw, von Dohlen and Harpel2012) under M. rhois may be a composite of two species.

Alienicola, first instar (deposited by aptera alienicola on moss). Dull pale yellow in life (in contrast to dark colour of larvae deposited by fundatrispuria).

Sexupara (alate migrant from moss). Colour and wax-gland distribution similar to fundatrispuria. Antenna usually with five antennomeres (first apparent flagellomere resulting from fusion of first and second flagellomeres, usually with an unpigmented window on dorsal surface of composite flagellomere or other distortion at point of fusion); sometimes with a full complement of six antennomeres (Fig. 8I–J), sometimes with first three flagellomeres fused to give a four antennomere appearance (Fig. 8K–L). Antennomeres shorter than corresponding antennomeres of the fundatrispuria, with rhinaria fewer in number and generally extending no more half circumference of antennomere. Primary rhinarium of penultimate antennomere usually clearly differentiated from secondary rhinaria, round to transverse-oval with obscurely to distinctly ciliate margin, but sometimes similar to secondary rhinaria (transverse with smooth margin); primary rhinarium of ultimate antennomere small and round to large and oval, with distinctly ciliate margins. Basitarsus with two apico-ventral setae. Distitarsus shorter than in fundatrispuria; plantar surface with two or three pairs of setae. Cauda with two setae.

Sexual female (Fig. 10D). Colour in life dark olive to black. Body length of first instar about 620 µm, of adult about 550 µm. Apterous. Rostrum absent. Body setae very short, inconspicuous. Wax-gland plates obscure, often with only on to three facets. Legs short, femur about as long as tibia of same leg; femur and tibia both about 2.5 times longer than greatest width. Tarsomeres fully fused; claw short, blunt; apicodorsal seta of distitarsus long and curved (Fig. 10C), about twice as long as claw; ventral setae of basitarsus of adult shorter then ventral length of basitarus (longer in first instar); pretarsal setae of adult inconspicuous, about half as long as claw (but capitate and about 1.3 times longer than claw in first instar). Cauda with two setae.

Male. Similar to sexual female, body length of adult about 300 µm.

Gall. Initiated by feeding by the first instar fundatrix on upper surface of the lamina of a leaflet adjacent to major veins (not “am Mittelnerv”, i.e., “on midvein”, as stated by Mordvilko (Reference Mordvilko1935)). A spherical pocket extending above and below the blade forms around the fundatrix and subsequently expands below the blade, usually also with a conical projection above the blade, the opening becoming closed by trichomes at adaxial opening and by tissue expansion within neck. Immature gall globular (Fig. 6A), pale green, about 2.0–2.5 mm in diameter at the time the fundatrix undergoes its final moult to adult. Veins adjacent to gall become more or less swollen and adaxial surface reddened. Mature gall (Fig. 6B–D) globular to pyriform, unilocular, largely red in colour in exposed locations, but usually with pale yellow to yellow-green areas on the side protected from the sun, pale areas more extensive in shaded locations; up to 50 mm in length and up to 45 mm at greatest diameter. The gall surface is often irregular to weakly lobed. Galls distinctly bilobed to near the base occasionally occur, and very rarely galls have several deep lobes. It is not clear if these are the product of a single fundatrix (with lobes possibly resulting from a leaflet vein interfering with gall expansion) or result from the settling of more than one fundatrix at the same site; we have found recently initiated galls with more than one fundatrix, but only one surviving beyond first instar. Vestiture of the gall surface reflects the general vestiture of the host plant: those on Rhus glabra are largely glabrous while those on R. typina are finely setose.

Comments. Fitch (Reference Fitch1866) described the antenna of the alate form from the gall as having four antennomeres, with “the first joint slightly the shortest, and the second joint rather the longest”. Because Fitch states that the “second joint” is the longest, we presume he overlooked the scape due to retraction into the head in dried specimens, and that his “first joint” is the pedicel and the “second joint” is the apparent first flagellomere of a five-antennomere antenna. Walsh (Reference Walsh1867) established Melaphis as distinct on the basis of possession (chiefly) of four-antennomere antennae, and explicitly stated that “the typical two joints of the scape are soldered together” as are “the typical joints 1 and 2 of the flagellum”; Walsh did recognise, however, that almost a quarter of the 28 specimens he examined had one antenna with “five segments” (i.e., first two flagellomeres not fused). We have seen no specimens with fusion of the scape and pedicel, and believe that Walsh was also mistaken in this regard. We have seen several specimens having one antenna with four apparent antennomeres (the first, second, and third flagellomeres are more or less fused), but in this case either the “third joint” would be the longest if the scape is taken into account, or the antenna would be described as having three antennomeres if the scape is ignored.

Fitch (Reference Fitch1866) described material collected in early September well before galls had fully matured, as evidenced by his indication that each gall contained zero to four winged individuals and that the galls were closed. As noted by Walsh (Reference Walsh1867), the colours given by Fitch for the alate form in the gall are for teneral individuals.

The gender of Melaphis is feminine (Cortés Gabaudan et al. Reference Cortés Gabaudan, Nieto Nafría, Favret, Barbagallo, Sano and Stekolshchikov2011), by analogy with the conventionally established gender of Aphis. Thus, the correct spelling of “M. minutus” is M. minuta.

Melaphis rhois (Fitch, Reference Fitch1866)

Brysocrypta rhois Fitch, Reference Fitch1866 (original combination).

Neotype. Fundatrispuria (alate emigrant from gall), CNCHEM084187.2 (Fig. 11); United States of America: Pennsylvania: State College (Sunset Park); ex Rhus glabra; 22.viii.2013; R.G. Foottit. Deposited in Canadian National Collection of Insects, Arachnids, and Nematodes, Ottawa, Ontario, Canada (CNC). Neotype here designated.

Fig. 11

Melaphis rhois, neotype, CNCHEM084187.2, habitus. Scale bar=100 µm.

Diagnosis. Usually separable from M. asafitchi new species by longer ultimate rostral segment (usually exceeding 65 µm in all morphs sufficiently characterised; for fundatrispuriae, a value of [0.03×[total length of flagellum]−0.14×[ultimate rostral segment]−0.09×[distal metatarsomere]+3.0] is negative; abdominal segment 8 often with wax-gland plates. For isolated individuals with length of last rostral segment near 65 µm or fundatrispuriae with discriminant function value near 0, definitive diagnosis by mitochondrial COI-5P sequence is required.

Description. The following description includes only morphs for which individuals of known COI haplotype are available. See the generic description for general characteristics of the fundatrix, adult alienicola and sexual forms.

Fundatrigenia (second generation aptera in gall). As described for genus, with measurements in Table 7. Body length 0.9–1.2 mm. Antenna with five to six (usually five) antennomeres. Ultimate rostral segment >68 µm long.

Table 7

Summary of length measurements for Melaphis rhois and Melaphis asafitchi fundatrigeniae (apterae in gall on Rhus).

Note: Both antennae of each individual (if present) were measured; thus n for antennae is the total number of antennae measured rather than number of individuals. The prefix “A” signifies antennomere, where A1 is the scape and A3 is the first flagellomere. Apparent antennomere 3 of individuals with five antennomeres is considered homologous with fused antennomeres A3 and A4, thus subsequent antennomere is A5, and terminal antennomere of all antennae is A6. Antennomere lengths of different degrees of fusion (i.e., apparent 4, 5, and 6 antennomeres) are reported separately, as well as length for homologous extents for all antennae. A3/4 and A3/4/5 indicate fused antennomeres, while A3+A4, A3+A4+A5 and flagellum (=A3–A6) represent the total span of the indicated antennomeres whether fused or not. 5 ant and 6 ant indicate specimens with five or six antennomeres, respectively. A6 includes terminal process. Femur length includes trochanter. Measurements in micrometres.

Fundatrispuria (alate emigrant from gall). As described for genus, with measurements as given in Table 8 and rhinarial distribution in Table 9.

Table 8

Summary of length measurements for of Melaphis rhois and Melaphis asafitchi fundatrispuriae migrating from Rhus to moss.

Note: See caption for Table 7 for labelling of antennomeres. Metafemur includes trochanter. Antennal and leg measurements for type specimens are for left/right appendages. All length measurements in micrometres.

Table 9

Rhinarial (primary+secondary) counts for specimens fundatrispuriae of Melaphis rhois and Melaphis asafitchi.

Note: Labelling of antennomeres as in Table 7. Counts for types are for left/right antenna.

Expression of wax glands on abdominal tergite 8 (Fig. 9B) is variable; the basic pattern consists of two pairs of facetted plates as on tergite 7, with expression ranging from absent (in 62% of 190 specimens examined), through a few scattered single facets up to completely confluent fully developed plates covering much of the tergite (neotype with two pairs of distinct plates).

Of 300 specimens, 67% from 18 localities have both antennae with six antennomeres, 28% have one five-antennomere antenna, and five per cent of individuals have both antennae with five antennomeres (i.e., about 19% of all individual antennae have five antennomeres). Two individuals examined have one antenna with the second and third flagellomeres (rather than first and second) partly fused.

Alienicola, first instar (deposited by fundatrispuria) (Fig 10E). As described for genus. Body 330–450 µm long. First flagellomere about 1.6 (range 1.4–1.9) times length of pedicel. Rostrum reaching middle of abdomen, apex of third rostral segment reaches posterior margin of metacoxa; ultimate rostral segment 1.2 times length of ultimate rostral segment and 1.6 times length of metatarsus. Measurements of antennomeres, rostrum, and metathoracic leg parts given in Table 10.

Table 10

Measurements for Melaphis rhois and Melaphis asafitchi first instar offspring of fundatrispuriae.

Note: Femur length includes trochanter. Measurements in micrometres.

Sexupara (alate migrant from moss). As described for genus, with measurements in Table 11. Length of ultimate rostral segment >64 µm, average length of flagellum 311 µm.

Table 11

Measurements for Melaphis rhois and Melaphis asafitchi sexuparae migrating from moss to Rhus.

Note: See Table 7 for terminology regarding antennomeres. Femur length includes trochanter. Measurements in micrometres.

Mitochondrial cytochrome oxidase subunit1, 5' region (DNA barcode). Sequence of specimen from same gall as neotype, Genbank accession KY754324. Additional sequence variants given in BOLD data set DS-MELAPHIS (www.boldsystems.org/index.php/Public_SearchTerms?query=DS-MELAPHIS).

Distribution. Widespread in United States of America and in southeastern Canada. Canada: southern Ontario, southern Québec, Nova Scotia. United States of America: Arkansas, Arizona, Georgia, New Jersey, Pennsylvania, Washington (all confirmed by COI-5P sequence); Kentucky, Maine, Massachusetts, New Hampshire, North Carolina (based on morphology only).

Hosts. Primary hosts: Rhus glabra, Rhus typhina. Confirmed secondary hosts: Haplocladium microphyllum (Moran Reference Moran1989), Dicranum scoparium (Pike et al. Reference Pike, Graf, Foottit, Maw, von Dohlen and Harpel2012).

Material examined. Fundatrispuriae (fp) and fundatrigeniae (fg) measured for morphometric analysis (see Supplementary Tables S1–S3 for additional details) – Canada: Ontario: Actinonolite, Price Conservation Area, 17.ix.2009; Beech Corners, Buckshot Lake, 25.ix.1993 and 25.xi.2008; Chaffeys Locks, 17.ix2009; Griffith, Matawatchan River, 24.ix.2009; Khartoum, 24.ix.2009; Maberley, Highway 7 at McGowan Lake, 16.ix.1993 and 17.ix.2009; Mallorytown, 17.ix.2009; Mount St. Patrick, English Road, 24.ix.2009; Ottawa, Marlborough Forest, 19.vi.1993; Prescott, Pruner Road, 13.vi.1993; Prince Edward County at Deseronto bridge, 17.ix.2009; Robertsville, 16.vi.1993 and 24.ix.2009; South Lake (Taylor/Berryton), 17.ix.2009; Westbrook, Highway 401 service centre, 13.vi.1993; Westport, Perth Road North near Lennon Road, 17.ix.2009. Québec: Parc de la Gatineau, Champlain Lookout, 19.ix.1993 and 17.ix.2009; Parc de la Gatineau, Hickory Trail, 10.ix.2001; United States of America: Pennsylvania: State College, 22.viii.2013.

Additional specimens – Canada: Ontario: Point Anne, Rhus typhina, 18.v.1993, E. Maw, 93EM-016 (5 sexuparae) [CNC]; Québec: Parc de la Gatineau, reared from Polytrichum, 31.v.1994, E. Maw, 94EM-015.1 (1 sexupara) [CNC]; Shawinigan, “sumack”, 23.viii.1939, L. Daviault (7 fg) [CNC]. United States of America: Kentucky: Greenup County, 24.ix.1971, D. Barnett, Ky-106, 72-1834 (1 fp) [USNM]; Maine: Orono, Rhus, 15.x.1935, E.M. Patch 18-35 (76 fp) [CNC]; Massachusetts: Quincey, sumac in galls, viii.1980 (4 fg) [USNM]; New Hampshire: Claremont, sumac, 15.ix.1917, Mosher, Q.13619 (5 fp) [USNM]; North Carolina: Fletcher, sumac, 23.ix.1960, C.F.S[mith], 60-1081 (3 fp) [USNM]; Pennsylvania: Philipsburg, sumac, 24.ix.1959, Pepper (4 fp) [USNM] .

Comments. According to Barnes (Reference Barnes1988), almost all aphid material from Fitch’s collection is currently housed in USNM and in New York State Museum (Albany, New York, United States of America). A few of his aphid specimens are also found in the Museum of Comparative Zoology (Harvard University, Cambridge, Massachusetts, United States of America). There is no existing material of Brysocrypta rhois examined by Fitch in any of these institutions. As it is unknown which species Fitch actually had at hand (possibly both) we have designated a neotype. COI-5P Group 1 is selected to carry the name M. rhois. Current evidence suggests that this is the more widespread species. The neotype was selected from among specimens collected at State College, Pennsylvania, as this is the nearest locality to Fitch’s original collections for which we have sequenced individuals. This specimen belongs to the subgroup (COI-5P Subgroup 1a) to which GenBank accession U36747 belongs. These decisions serve to maintain the usage of this name in previous phylogenetic and endosymbiont studies based on material collected by Moran in Arizona (Moran et al. Reference Moran, Munson, Baumann and Ishikawa1993, Reference Moran, von Dohlen and Baumann1995; Rouhbakhsh et al. Reference Rouhbakhsh, Lai, von Dohlen, Clark, Baumann and Baumann1996; Clark et al. Reference Clark, Moran and Baumann1999; Nováková et al. Reference Nováková, Hypša, Klein, Foottit, von Dohlen and Moran2013). The samples used by Yang et al. (Reference Yang, Chen, Havill, Feng and Chen2010), the sequence used by Li et al. (Reference Li, Jiang and Qiao2014), and the sequences generated by Ren et al. (Reference Ren, Zhong, Kurosu, Aodi, Ma, von Dohlen and Wen2013) belong to subgroup 1b. We interpret the subgroups as variants of a single species.

Melaphis asafitchi Foottit and Maw, new species

Type series. Holotype: fundatrispuria (alate emigrant from gall), CNCHEM085883.2 (Fig. 12); Canada: Ontario: Kemptville, G. Howard Ferguson Forest Station, 45.037°N 75.667°W; ex Rhus typhina; 17.ix.2009; E. Maw. Deposited in CNC. Paratypes: fundatripuriae (fp) and fundatrigeniae (fg) measured for morphometric analysis (see Supplementary Tables S1–S3 for additional details) – Canada: Ontario: Actinolite, Price Conservation Area, 17.ix2009 (12 fp); Beech Corners, Buckshot Lake, 25.ix.2008 (3 fp); Chaffeys Locks, 17.ix.2009 (3fp, 7 fg); Griffith, Matawatchan River, 24.ix.2009 (6 fp); Kemptville, Ferguson Forestry Station, 17.ix.2009 (8 fp); Khartoum, 24.ix.2009 (8 fp, 6 fg); Maberley, Highway 7 at McGowan Lake, 17.ix.2009 (9 fp, 2 fg); Mallorytown, 17.ix.2009 (12 fp); Mount St. Patrick, English Road, 24.ix.2009 (3 fp, 5 fg); Prince Edward County at Deseronto bridge, 17.ix.2009 (2 fg); South Lake (Taylor/Berryton), 17.ix.2009 (3 fp, 1 fg). Québec: Parc de la Gatineau, Champlain Lookout, 17.ix.2009 (8 fp); Parc de la Gatineau, Hickory Trail, 10.ix.2001 (3 fp); United States of America: Pennsylvania: State College, 22.viii.2013 (3 fp). Deposited in Canadian National Collection (CNC), National Museum of Natural History (USNM) (3 fp, 2 fg), and Natural History Museum (London, United Kingdom) (3 fp, 2 fg).

Fig. 12

Melaphis asafitchi, holotype, CNCHEM085883.2, habitus. Scale bar=100 µm.

Diagnosis. Usually separable from M. rhois by the shorter ultimate rostral segment (usually less than 65 µm in all morphs sufficiently characterised; for fundatrispuriae, value of [0.03×[total length of flagellum]−0.14×[ultimate rostral segment]−0.09×[distal metatarsomere]+3.0] is positive; abdominal segment 8 without wax-gland plates. For isolated individuals with length of last rostral segment near 65 µm or fundatrispuriae with discriminant function value near 0, definitive diagnosis by mitochondrial COI-5P sequence.

Description. The following description includes only morphs for which individuals of known COI haplotype are available. See the generic description for general characteristics of the fundatrix, adult alienicola and sexual forms.

Fundatrigenia (second generation aptera in gall). As described for genus, with measurements as in Table 7. Body length 0.9–1.2 mm. Rostrum and legs relatively shorter and antennae relatively longer than in M. rhois. Ultimate rostral segment <68 µm long. Antenna with four to six (usually 5) antennomeres.

Fundatrispuria (alate emigrant from gall). As described for genus, with measurements as given in Table 8 and rhinarial distribution in Table 9. Wax-gland facets lacking on abdominal tergum 8 (all specimens examined). About 57% of 325 specimens from 20 galls have both antennae with six antennomeres, 30% have one five-antennomere antenna, and 14% of individuals have both antennae with five antennomere (i.e., about 28% of all individual antennae have five antennomeres). Two individuals had one antenna with the three basal flagellomeres fused, resulting in an apparent four-antennomere antenna.

Alienicola, first instar (deposited by fundatrispuria) (Fig. 10F–G). As described for genus. Body 320–425 µm long. First flagellomere about 1.1 (range 0.8–1.2) times length of pedicel. Rostrum reaching just beyond posterior margin of metacoxa, apex of third rostral segment not reaching posterior margin of metacoxa; ultimate rostral segment 1.0 times length of ultimate antennomere and 1.4 times length of metatarsus. Measurements of antennomeres, rostrum, and metathoracic leg parts given in Table 10.

Sexupara (alate migrant from moss). As described for genus, with measurements in Table 11. Ultimate rostal segment <66 µm. Mean length of antennal flagellum 276 µm.

Mitochondrial cytochrome oxidase subunit1, 5' region (DNA barcode). Holotype, GenBank KY754388. Additional sequence variants are available in BOLD data set DS-MELAPHIS (www.boldsystems.org/index.php/Public_SearchTerms?query=DS-MELAPHIS).

Distribution. Canada: southern Ontario, southern Québec, Nova Scotia (confirmed by COI-5P sequence); New Brunswick (based on morphology). United States of America: Pennsylvania, Washington (confirmed by COI-5P sequence); Illinois, Maine, Maryland, Minnesota, New York (based on morphology).

Hosts. Primary hosts: Rhus glabra, Rhus typhina. Confirmed secondary hosts: undetermined mosses (specimens included in Pike et al. Reference Pike, Graf, Foottit, Maw, von Dohlen and Harpel2012 as M. rhois).

Etymology. Named in honour of Dr. Asa Fitch (1809–1879), the first American professional entomologist, who first described a species of Melaphis.

Additional material examined. Canada: New Brunswick: Burton, 23.ix.1933, C.E. Atwood, 18788-31 (3 fp) [CNC]; Ontario: Chaffeys Lock, Clear Lake Road, Rhus typhina, 20.v.2014, E. Maw and B. Richardson, 2014EM-0015 (20 sexuparae); Québec: Cté Papineau, Notre Dame de la Salette, Rhus typhina, 12.ix.1981, L. Jobin (64 fp); Parc de la Gatineau, Rhus typhina, 21.v.1994, E. Maw, 94EM-018; 20.v.2014, 28.v.2014, E. Maw and B. Richardson, 2014EM-010 A,-0021 (35 sexuparae) [all in CNC]. United States of America: Illinois: Milan, galls on sumac, 16.viii.1885, accession number 7134 (1 fg, numerous L4 fp) [USNM]; Maine: Orono, Rhus glabra, 26.ix.1956, D. Folsom, 56-21 (6 fp, 1 fg) [CNC]; Maryland: Cabin John, Rhus glabra, 14.viii.1932, M.G. van Meter [USNM]; Glen Elg, sumac, 15.viii.1962, W.T. Johnson, Md 62-47, 62-22591 (4 fp) [USNM]; Geneld [?=Glen Elg], Rhus typhina, 16.viii.1962, W.T. Johnson (5 fp) [USNM]; Minnesota: Detroit Lakes, Rhus glabra, 3.ix.1984, V.H.J. Beregovey, 84-10669 (2 fp) [USNM]; Le Sueur, Rhus glabra, 21.ix.1907, G.G. Ainslie, number 199 (34 fp) [USNM]; New York: Ithaca, Rhus, 6.x.1924, M. Reidy, 514-24 (8 fp); West Point, Rhus glabra, 28.vii.1896, J.A. Williams (2 fg and numerous L4 fp) [USNM]; Pennsylvania: State College, Waddle, 25.viii.1962, Rhus glabra, J.O. Pepper, JOP62-51 (4 fp) [USNM]; Coraopolis, 12.ix.1916, sumac, Q-13214 (6 fp) [USNM].

Melaphis minuta Baker and Truncaphis newsteadii Theobald

The length of the ultimate segment of the rostrum of Baker’s material (83–84 µm) of Melaphis minuta is slightly beyond the upper end of the range of this measurement among other available sexuparae, and would suggest that it is the species with the longer rostrum, M. rhois. However, the length of the antennal flagellum in the single syntype seen and in the measurements given by Baker (Reference Baker1919) are less than the minimum we have observed for the species with the shorter antenna in the sexupara, M. asafitchi (Baker’s measurements seem to have a granularity of about 16 µm, but even inflating each of his measurements by 8 µm, the maximum value is about the same as the shortest length found for M. asafitchi, an unusual specimen with the first three flagellomeres fused). Thus, given this combination of characters, it is currently not possible to assign M. minuta to either of the two species discussed here. It is possible that it corresponds to our COI-5P Group 3, or is yet another species.

Melaphidine apterae on moss in the United Kingdom, originally described as Truncaphis newsteadii, and in Sweden are currently assigned to Melaphis rhois. However, given the sparse knowledge of the moss-inhabiting forms of both the North American and the Asian species, the extent of intraspecific variation is unknown, and the assignment of the European populations to one of the described species would be premature without supporting molecular evidence. Ren et al. (Reference Ren, Zhong, Kurosu, Aodi, Ma, von Dohlen and Wen2013) suggested the possibility that these populations are a relict of an indigenous European melaphidine species.