Adelges (Cholodkovskya) changaphuensis Havill & Brunet, 2025

Adelges (Cholodkovskya) changaphuensis Havill & Brunet , sp. nov.

( Fig. 4A–E View FIGURE 4 )

Etymology. From Changaphu, the locality in Bhutan where spruce trees were found to be heavily infested by this species.

Type material. HOLOTYPE: 1 adult fundatrix, BHUTAN, Thimphu, Changaphu Forest Nursery , lat. 27.4997, long. 89.7176, 2-IV-2020, on Picea spinulosa, Kaka Tshering (USNM) . PARATYPES: 1 first instar fundatrix, 1 adult fundatrix, same data ( NBC) . 1 first instar fundatrix, 1 nymph fundatrix, same data ( USNM) . 1 first instar fundatrix, same data ( YPM # ENT594814 About YPM ) . 1 nymph fundatrix, same data ( YPM # ENT594815 About YPM ) . 1 adult fundatrix, same data ( YPM # ENT594816 About YPM ) . 2 adult gallicolae, BHUTAN, Thimphu, Changaphu , lat. 27.5022, long. 89.7156, 29-VII-2021, on Picea spinulosa, Kaka Tshering ( CNC#5338320-6 View Materials , CNC#5338321-9 View Materials ) . 1 adult gallicola, same data ( NBC) . 1 adult gallicola, same data ( USNM) . 1 adult gallicola, same data ( YPM # ENT594826 About YPM ) .

Additional material examined. BHUTAN: Bumthang: Khandopang : 2 adult fundatrices, 3 fundatrix exuviae ( YPM), 27.4262, 90.9063, 8-IV-2022, on Picea spinulosa, Kaka Tshering GoogleMaps . Thimphu: Changaphu Forest Nursery : 11 late instar nymph fundatrices ( CNC), 1 first instar fundatrix exuvium, 4 late instar nymph fundatrices, 2 adult fundatrices ( USNM), 1 first instar fundatrix exuvium, 5 late instar nymph fundatrices, 3 adult fundatrices ( YPM), lat. 27.4997, long. 89.7176, 2-IV-2020, on Picea spinulosa, Kaka Tshering. 9 fourth instar nymph gallicolae, 17 adult gallicolae ( CNC), 1 adult gallicola ( NBC), 2 late instar nymph gallicolae, 5 adult gallicolae ( USNM), 1 nymph gallicola, 15 adult gallicolae ( YPM), lat. 27.4997, long. 89.7176, 29-VII-2021, on Picea spinulosa, Kaka Tshering. 16 first instar gallicolae ( CNC), 15 galls ( YPM), lat. 27.4997, long. 89.7176, 22-V-2022 on Picea spinulosa, Kaka Tshering .

Diagnosis. The neofundatrix of A. (Ch.) changaphuensis ( Fig. 4A View FIGURE 4 ) is similar to the neosistens of A. (Ch.) viridanus ( Börner 1909; Inouye 1945) in having a wide spinal fissure bisecting the cephalic and prothoracic plates, spinal, pleural, and lateral wax glands on the meso- and metathoracic and first six abdominal segments, and wax glands with facets surrounding a central seta. The A. (Ch.) changaphuensis neofundatrix differs from the A. (Ch.) viridanus neosistens in having separate longitudinal lateral prothoracic plates and differs from all other members of Cholodkovskya in having larger lateral abdominal wax glands arranged around two setae instead of around one seta. The neofundatrix of A. (Ch.) viridanus has not been described to allow direct comparison with the same morph in A. (Ch.) changaphuensis . The general appearance of the wax glands is also similar to neosistentes and neofundatrices in species of Sacchiphantes . The adult fundatrix of A. (Ch.) changaphuensis ( Fig. 4C View FIGURE 4 ) is similar to that of A. (Ch.) viridanus ( Havill et al. 2023) but A. (Ch.) changaphuensis lacks wax glands antero-lateral to forecoxae. Late instar nymphs ( Fig. 4B View FIGURE 4 ) are similar in morphology to the adult but lack an ovipositor. The adult gallicola of A. (Ch.) changaphuensis ( Fig. 4D View FIGURE 4 ) differs from A. (Ch.) viridanus because it does not have anterior and posterior wax glands on each side of the head united. Unlike the gallicolae of other Adelges , the medial vein on the hindwings of A. (Ch.) changaphuensis are either faint or lacking entirely. Also note, that the sexuparae of Adelges (Gilletteella) cooleyi ( Gillette, 1907) and Adelges (Dreyfusia) nordmannianae ( Eckstein, 1890) lack the medial vein on the hindwing, so A. (Ch.) changaphuensis is not the only alate Adelges with this character.

Description. Neofundatrix ( Fig. 4A View FIGURE 4 ). Body length: n = 4, 0.604 –0.722 (0.665) mm. Body width: n = 4, 0.374 – 0.437 (0.404) mm. Dorsal wax glands generally on strongly sclerotized plates, and with 3–6 round to ovoid facets with a granular appearance, loosely packed and arranged around a central stout seta, sometimes merged with neighboring glands to include up to approximately 20 facets arranged around two or three setae.

Head and pronotum with strongly sclerotized spinal and lateral plates, separated from each other and along mid-line by wide fissures. Ocelli borne on small lateral plates. Each spinal cephalic plate with five large wax glands, three apical and two postero-lateral, a sixth slightly raised postero-spinal area with a central seta, usually lacking facets, occasionally with one or several facets. The largest dorsal wax gland facets on the head are slightly smaller than ocellus. Large ventral wax glands on moderately sclerotized sternites posterior to base of antennae with approximately 30 small, round, tightly packed facets. Antennae 3-segmented, segment III distinctly imbricated, very long and slender [n = 6, 0.125 –0.132 (0.129) mm], 7.3x its width at midpoint [n = 6, 0.017 –0.019 (0.018) mm], approximately 2.3x longer than segments I [n = 4, 0.019 –0.034 (0.025) mm] and II [n = 4, 0.020 –0.033 (0.027) mm] combined. Two primary rhinaria on segment III, one subapical and one approximately 1/3 the segment length from the apex, each with a small thumb-like projection. A few accessory rhinaria adjacent to the subapical primary rhinarium. Processus terminalis with five setae, the apical seta length [n = 4, 0.035 –0.041 (0.038) mm] approximately 2x the rest. Rostrum reaching past hind coxae, with ultimate segment as long [n = 5, 0.053 –0.061 (0.057) mm] as width of segment III at midpoint [n = 4, 0.051 –0.056 (0.054) mm]. Stylets very long [n = 2, 3.353 – 3.467 (3.410) mm], approximately 5.1x body length.

Coxae and femorotrochanters smooth, with tibiae weakly imbricated, and second tarsal segments distinctly imbricated. Pair of dorso-subapical capitate setae of fore- and midlegs with one of the pair approximately 2x as long as the other, subequal on hindleg. Mid- and hind-coxae with basal wax glands with approximately 8–12 moderately packed round to ovoid facets. Hind femorotrochanter length: n = 5, 0.096 –0.105 (0.101) mm.

Pronotum with wax glands on the four corners of each spinal plate, each gland with 1–4 facets. Lateral plates of pronotum extended longitudinally with two wax glands, each with approximately 5–12 facets. Meso- and metanotum with dorsal spinal, pleural, and lateral plates, each with a single wax gland. Spinal and pleural wax glands round and arranged around one seta, lateral wax glands oval-shaped along longitudinal axis usually arranged around two setae. Abdominal segments I–VI with dorsal spinal, pleural, and lateral plates, segment VII with spinal and lateral plates, and segment VIII with lateral plates. Abdominal segment IX with a transversely extended plate in central position. Each abdominal plate with a single wax gland. Lateral wax glands of abdominal segments I–VIII transverse oval-shaped with 7–20 facets usually arranged around two setae. Pleural and spinal wax glands of abdominal segments I–VI and spinal glands of segment VII round to oval with 3–7 facets arranged around a single seta. Ventral spiracles on abdominal segments II–VI. All abdominal segments with a ventro-spinal pair of fine acuminate setae, those on segment IX especially long and slender.

Adult fundatrix ( Fig. 4C View FIGURE 4 ). Body length: n = 6, 1.343 –1.903 (1.644) mm. Body width: n = 6, 1.042 –1.226 (1.111) mm. Color in life light green. Dorsal wax glands generally on very lightly sclerotized plates, and with small round, tightly packed facets with borders only slightly darker than the surrounding cuticle.

Sclerotized plates on head and pronotum lacking. Head with 8–10 small anterior wax glands between ocelli, each gland with approximately 3–20 loosely packed facets, the largest of which are approximately half the diameter of the ocellus. Ventral wax glands at base of antennae with approximately 30–40 very small tightly packed facets. Antennae 3-segmented, segment III [n = 6, 0.074 –0.097 (0.083) mm], approximately 3.6x its width at midpoint [n = 6, 0.019 –0.026 (0.023) mm], longer than segments I [n = 6, 0.024 –0.037 (0.031) mm], and II [n = 6, 0.027 –0.033 (0.032) mm] combined. Rostrum reaching to hind coxae, with ultimate segment length [(n = 4, 0.068 –0.091 (0.079) mm] approximately 0.9x width of segment III at midpoint [n = 4, 0.076 –0.099 (0.084) mm].

Coxae, femorotrochanters, and tibiae smooth, second tarsal segments weakly imbricated. Mid- and hind-coxae with transversely oval wax glands bearing 10–25 facets. Hind femorotrochanter length: n = 6, 0.125 –0.224 (0.171) mm.

All thoracic segments and abdominal segments I–VI with spinal, pleural, and lateral wax glands, abdominal segment VII with lateral and spinal wax glands, segment VIII with lateral wax glands. Spiracles on abdominal segments II–VI strongly sclerotized and conspicuous. Numerous acuminate setae on abdominal segments VIII and IX. Ovipositor with length of gonapophyses [n = 4, 0.117 –0.157 (0.130) mm] approximately 1.2x the width across apodemes.

Adult gallicola ( Fig. 4D View FIGURE 4 ). Body length: n = 16, 1.772 –2.610 (2.058) mm. Pronotum width: n = 15, 0.587 –0.812 (0.676) mm. Abdomen width: n = 16, 0.839 –1.221 (0.960) mm. Color in life light green when newly emerged. Dorsal wax glands generally with round, tightly packed facets interspersed with minute setae.

Head with a pair of anterior and a pair of posterior irregular-shaped wax glands with approximately 10–30 facets. Posterior glands may be subdivided into small groups of facets around setae. Antenna distinctly five segmented, n = 12, 0.336 –0.434 (0.381) mm long, segments II–V imbricated. Length of antennal segment III: n = 12, 0.075 –0.088 (0.080) mm, IV: n = 12, 0.080 –0.109 (0.093) mm, n = 12, V: 0.101 –0.137 (0.115) mm. Ratio of length of antennal segments III:IV:V 1.00:1.16:1.43. Antennal segment III tapering sharply towards the base, segments IV and V with a gradual taper below rhinarium. Rhinaria on antennal segments III–V oval, subapical, often with sinuate margins, sometimes appearing triangular in profile. Rhinarium occupying approximately 1/3 of each segment: III: n = 10, 0.25–0.41 (0.34), IV: n = 10, 0.25–0.40 (0.33), V: n = 10, 0.30–0.40 (0.34). Processus terminalis with four or five acuminate setae, with apical seta length [n = 10, 0.015 –0.022 (0.017) mm] approximately 1.9x as long as the rest. Ultimate segment of rostrum length [(n = 14, 0.055 –0.080 (0.064) mm] 0.9x the width of segment III at midpoint [n = 14, 0.058 –0.083 (0.072) mm].

Coxae and femorotrochanters smooth, tibiae very weakly imbricated, and second tarsal segments distinctly imbricated. Hind femur with approximately 15–20 long fine acuminate setae along ventral surface. Length of longest setae on hind femur: n = 15, 0.028 –0.039 (0.034) mm. Hind femorotrochanter length: n = 15, 0.314 –0.408 (0.350) mm.

Each side of pronotum with several small, antero-lateral oval-shaped glands with 2–50 facets, a very large postero-lateral band of approximately 120–150 facets, and a narrow irregular row, 2–5 facets thick, along the posterior edge.Mesonotum with a pair of spinal oval-shaped wax glands bearing approximately 50–60 facets between mesothoracic lobes. Metanotum with a pair of wax glands with approximately 30–60 facets towards the posterior half of the spinal lobes. Forewing length: n = 16, 2.286 –3.023 (2.661) mm. Hindwing length: n = 16, 1.377 –1.892 (1.588) mm. Forewing with medial, cubital, and anal veins straight or only slightly curved back towards the body, leaving the radial sector at acute angles. Hindwing with medial vein faint or lacking.

Abdomen with spinal, pleural, and lateral wax glands on segments I–VI, lateral and pleural wax glands on segment VII, only lateral wax glands on VIII, and a post-anal gland on IX. Lateral glands on abdominal segments I–VII transverse, often crescent-shaped. Spinal glands decrease in size posteriorly. Distinct sclerotized spiracles on abdominal segments II–VI. Abdominal segments VII–VIII with numerous ventral fine acuminate setae, some long and slender. Ovipositor with gonapophyses [n = 11, 0.106 –0.126 (0.114) mm] approximately 1.3x longer than width across apodemes [n = 11, 0.072 –0.101 (0.086) mm].

Gall ( Fig. 4E View FIGURE 4 ). Light green in color, strobile-shaped. Usually occurring singly per node on terminal and lateral buds of new shoots. Consists of swollen needle bases, fused at the axis of the shoot. Chambers internally unconnected. Gall length [n = 9, 21–34 (24.6) mm] approximately 1.9x the width (n = 9, 10–16 (12.7) mm]. Usually without a distal shoot, but occasionally with a distal tuft of shortened needles or short shoot. Distal ends of the needles on gall narrow and sharp, extending approximately 2–5 mm from the surface.

Hosts and distribution. Picea spinulosa in Bhutan (Bumthang, Thimphu) ( Fig. 5 View FIGURE 5 ).

Remarks. The morphological similarities to A. (Ch.) viridanus ( Börner, 1909) , and the sister relationship with A. (Ch.) viridanus in the phylogeny ( Fig. 1 View FIGURE 1 ) supports the placement of A. (Ch.) changaphuensis in subgenus Cholodkovskya . The life cycle of A. (Ch.) changaphuensis cannot be determined from our collections. There is no evidence of host alternation because our survey did not yield specimens with matching DNA barcodes from potential secondary hosts. Galls collected on May 22, 2022 were mature and close to opening. This species could be anholocyclic on Picea , or since in the molecular phylogeny ( Fig. 1 View FIGURE 1 ) it is nested well within a clade of species that use Larix species as secondary hosts, it may alternate between Picea and Larix . The other members of Cholodkovskya , A. (Ch.) viridanus , Adelges (Cholodkovskya) viridulus ( Cholodkovsky, 1911) , and A. (Ch.) oregonensis , all feed on species of Larix . Adelges (Ch.) viridanus has an anholocyclic life cycle in Europe and China with a generation of wingless sistentes that settle on the bark, followed by a series of generations of alates that settle on the needles ( Cholodkovsky 1911; Li & Tsai 1973). In Japan, the fundatrix adult and gallicola nymph of A. (Ch.) v iridanus were recently described, indicating that in that region the species can either be holocyclic, alternating between Larix and Picea , or includes recently diverged anholocyclic populations on Picea ( Havill et al. 2023) . The life cycle of A. (Ch.) v iridulus is anholocyclic on Larix but has only one annual generation of sistens on the bark and no known alate forms. The life cycle of A. (Ch.) oregonensis is unknown, as the species is only known from wingless forms that feed on the needles and the base of needles of Larix in western North America ( Annand 1928). Note that A. (Ch.) oregonensis is not sister to A. (Ch.) viridanus or A. (Ch.) changaphuensis in the molecular phylogeny ( Fig. 1 View FIGURE 1 ), so it may not belong in this subgenus. A more detailed morphological analysis of the adelgid species feeding on Larix , and a more robust phylogeny of the family could help to resolve a more informative delimitation of Cholodkovskya .