Adelges (Annandina) lepsimon Havill & Brunet, 2025

Havill, Nathan P., Brunet, Bryan, Zembrzuski, Zephyr & Tshering, Kaka, 2025, Four new adelgid (Hemiptera: Adelgidae) species from Bhutan, including the first legless species of Aphidomorpha, Zootaxa 5583 (3), pp. 437-461 : 456-458

Adelges (Annandina) lepsimon Havill & Brunet , sp. nov.

( Fig. 8A–D )

Etymology. Invariant combination of the Dzongkha noun, lep, meaning “brain” and Psimon the supervillain from the DC Comics Universe, whose brain is visible through a clear dome on his head. Both are in reference to the large wax glands on the head, that superficially resemble the lobes of a vertebrate brain.

Type material. HOLOTYPE: 1adult exulis, BHUTAN, Mongar, Sengor ,lat. 27.3394,long. 91.0295, 8-IV-2022, on Tsuga dumosa, Kaka Tshering ( USNM) . PARATYPES: 1 first instar exulis exuvium, same data ( CNC#5338329- 10 ) . 1 adult exulis, same data ( CNC#5338329-7 ) . 1 late instar nymph exulis, 1 adult exulis, same data ( NBC) . 1 first instar exulis, 2 first instar nymph exulis exuviae, 1 late instar exulis, same data ( USNM) . 1 late instar exulis, same data ( YPM # ENT594636 ) . 1 adult exulis, same data ( YPM # ENT594641 ) . 1 first instar exulis exuvium, BHUTAN, Mongar, Sengor , lat. 27.3711, long. 91.0234, 7-IV-2022, on Tsuga dumosa, Kaka Tshering (NBC) . 1 late instar nymph sexupara, same data ( USNM) . 2 first instar exulis exuviae, same data ( YPM # ENT594634 ) . 1 first instar exulis, BHUTAN, Wangdue Phodrang, Dungdungnyesa , lat. 27.5377, long. 90.1851, 12-XI-2021, on Tsuga dumosa, Kaka Tshering ( CNC#5338322-9 ) . 1 adult exulis, same data ( CNC#5338322-4 ) . 3 first instar exules, 1 first instar exulis exuvium, same data ( USNM) .

Additional material examined. BHUTAN: Mongar: Sengor: 2 late instar nymph exules ( USNM), 1 first instar exulis, 6 first instar exulis exuviae, 10 late instar nymph exulis exuviae, 12 late instar nymph exules, 3 late instar nymph sexuparae ( YPM), lat. 27.3711, long. 91.0234, 7-IV-2022, on Tsuga dumosa, Kaka Tshering. 2 first instar exules exuviae, 1 late instar nymph sexupara, 6 adult exules ( CNC), 1 first instar exulis, 9 first instar exulis exuviae, 2 late instar nymph exulis exuviae, 9 late instar nymph exules ( USNM), 1 first instar exulis, 16 first instar exulis exuviae, 12 late instar nymph exulis exuviae, 11 late instar nymph exules, 1 late instar nymph sexupara, 12 adult exules ( YPM), lat. 27.3394, long. 91.0295, 8-IV-2022, on Tsuga dumosa, Kaka Tshering . Wangdue Phodrang: Dungdungnyesa: 1 egg, 3 first instar exules, 3 adult exules ( CNC), 2 first instar exules, 1 adult exulis ( NBC), 3 first instar exules, 2 first instar exulis exuviae, 1 late instar nymph exulis exuvium, 1 adult exulis ( USNM), 4 first instar exules, 2 first instar exulis exuviae, 3 late instar nymph exulis exuviae, 6 adult exules ( YPM), lat. 27.5377, long. 90.1851, 12-XI-2021, on Tsuga dumosa, Kaka Tshering .

Diagnosis. Adelges (An.) lepsimon is placed in Annandina by phylogenetic relatedness ( Fig. 1 ), and by the combination of characters outlined in Favret et al. (2015a): feeding on Tsuga , having the first instar exulis with head and pronotum almost completely covered by plates, with margins lined with wax gland facets, four plates on the mesothorax, and six on the metathorax and first five abdominal segments, the adult with a completely fused cephaloprothoracic shield containing many small facets, and by having capitate setae on the ultimate abdominal segments ( Annand 1924; Havill et al. 2022). In A. (An.) lepsimon , the spinal and pleural mesothoracic plates are not always fused, so the diagnosis for Annandina should be amended to specify four or six plates on this segment. The first instar exulis of A. (An.) lepsimon differs from A. (An.) tsugae by having round to oval wax glands proximal to the lateral rows of facets on the head and each thoracic segment, and abdominal segments I–VI with dorso-spinal plates each with a wax gland in the center with 1–4 facets. The adult exulis of A. (An.) lepsimon resembles A. (An.) tsugae , which includes a diversity of genetic lineages in different regions of Asia and North America ( Havill et al. 2016). A future paper will address morphological differences among these lineages compared to A. (An.) lepsimon .

Description. First instar exulis ( Fig. 8A–B ). Body length: n = 10, 0.314 –0.423 (0.355) mm. Pronotum width: n = 11, 0.171 –0.211 (0.193) mm. Body width: n = 11, 0.189 –0.271 (0.220) mm. Dorsal wax glands generally on strongly to moderately sclerotized plates, with facets either arranged as anterior, lateral, or spinal longitudinal lines of individual pores, or as clusters of two to approximately 13 tightly packed, often overlapping pores.

Head and pronotum almost completely covered by moderately to strongly sclerotized plates, separated from each other and along mid-line by a narrow fissure. Each cephalic plate lined with a row of single wax gland facets along the lateral, anterior, and spinal margins. Facets along the spinal margin indistinct, often more visible in exuviae ( Fig. 8B ) than intact nymphs ( Fig. 8A ). Each cephalic plate with a prominent round to oval wax gland with approximately 6–13 tightly packed facets, proximal to anterior row of facets. Ventral wax glands at base of antennae with approximately 3–4 facets.Antenna 3-segmented, segment III distinctly imbricated, length [n = 12, 0.055 –0.062 (0.059) mm], approximately 3.8x its width at midpoint [n = 12, 0.013 –0.018 (0.015) mm], and approximately 1.6x longer than segments I [n = 12, 0.017 –0.022 (0.020) mm] and II [n = 12, 0.015 –0.020 (0.018) mm] combined. Two primary rhinaria on segment III, one subapical and one approximately 1/2 the segment length from the apex, each with a small thumb-like projection. Several accessory rhinaria adjacent to subapical primary rhinarium. Processus terminalis with 5 setae, the apical seta length [n = 11, 0.028 –0.040 (0.036) mm] approximately 3x the rest. Rostrum reaching past hind coxae with ultimate segment 0.8x as long [n = 9, 0.028 –0.039 (0.034) mm] as width of segment III at midpoint [n = 9, 0.037 –0.044 (0.041) mm]. Stylet length [n = 4, 0.630 –0.773 (0.704) mm] approximately 2.0x body length.

Coxae smooth. Femorotrochanters smooth to weakly imbricated, tibiae and second tarsal segments weakly imbricated. Pair of dorso-subapical setae on foreleg, one capitate seta approximately 2x longer than the other acuminate one. Pairs of subequal dorso-subapical capitate setae on mid- and hindlegs. Wax glands antero-lateral to mid- and hindcoxae with approximately 1–6 round to oval facets. Hind femorotrochanter length: n = 12, 0.046 – 0.054 (0.050) mm.

Each thoracic segment lined with a row of single wax gland facets along the lateral, margin, and a round to oval anterior cluster of approximately 2–13 wax gland facets, just proximal to lateral row. Meso- and metanotum with spinal and pleural plates, each plate with a single seta and a single row of 1–5 indistinct spinal and 0–5 lateral wax gland facets. Spinal and pleural plates of the mesothorax often fused. Metathoracic spinal plate sometimes with a central cluster of 1–5 wax gland facets. Abdominal segments I–V with separate lateral, pleural, and spinal wax plates, segment VI–VII with lateral and spinal plates, segment VIII with lateral plates, segment IX lacking plates. Abdominal segments I–VI dorso-spinal plates each with wax gland in the center consisting of a cluster of 1–4 facets. Abdominal segments I–III with pleural plates usually lacking wax gland facets. Abdominal segments IV–V with pleural plates with 1–3 wax facets. Abdominal segments I–VI with lateral plates each with 1–3 lateral facets and a small proximal wax gland with 1–5 facets. Abdominal spiracles minute, hardly visible. Pairs of small, ventro-spinal acuminate setae on abdominal segments I–VIII. Pair of dorso-lateral setae on abdominal segment VIII. Abdominal segment IX with two short acuminate dorsal setae anterior to anus, two longer acuminate ventral setae, and two long capitate setae at apex.

Adult exulis ( Fig. 8D ). Body length: n = 13, 0.764 –1.251 (0.980) mm. Pronotum width: n = 14, 0.402 –0.626 (0.523) mm. Body width: n = 13, 0.502 –0.883 (0.726) mm. Dorsal wax glands generally on moderately to strongly sclerotized plates with numerous, up to more than 200, contiguous to nearly contiguous small round granular facets.

Head and pronotum with sclerotized plates completely fused into cephaloprothoracic shield with largely smooth surface that extends ventrally to surround the base of antennae. Head with very large anterior wax glands with a lateral area mesad to ocelli curling towards, and sometimes touching posterior cephalic wax glands. Pair of cephalic postero-lateral, oval or irregularly shaped wax glands with approximately 25–50 facets. Largest diameter of facets on head subequal to the diameter of the ocellus. Large ventral wax glands on head with approximately 60–110 small round facets on surface at base of antennae. Antenna 3-segmented, segment III [n = 13, 0.029 –0.056 (0.041) mm] approximately 2.0x its width at midpoint [n = 13, 0.016 –0.022 (0.020) mm], approximately 0.9x the length of segments I [n = 13, 0.016 –0.033 (0.025) mm] and II [n = 13, 0.014 –0.029 (0.020) mm] combined. Segment III with subapical primary rhinarium with a few adjacent accessory rhinaria. Processus terminalis with five or six stout setae. Rostrum reaching to anterior margin of hind coxae, with ultimate segment [n = 13, 0.041 –0.091 (0.064) mm] 0.7x the width of segment III at midpoint [n = 13, 0.050 –0.076 (0.063) mm].

Coxae, femorotrochanters, and tibiae smooth, with second tarsal segment weakly imbricated. Large wax glands antero-lateral to coxae with approximately 50–100 loosely packed facets. Hind femorotrochanter length: n = 13, 0.064 –0.144 (0.104) mm.

Pronotum with very large lateral wax glands consisting of bands of up to 200 or more facets, and with posteropleural and postero-spinal irregularly shaped wax glands with 20–70 facets. Meso- and metathoracic segments and abdominal segments I–V with spinal, pleural, and lateral wax glands, circular or elliptical with numerous tightly packed facets. Plates on meso- and metanotum sometimes fused or touching. Abdominal segments VI–VII with lateral and spinal wax glands, segment VIII with lateral wax glands. Abdominal segment IX with large post-anal wax gland. Abdominal segments II–VI with distinct ventral spiracles. Abdominal segments VIII and IX with numerous capitate setae. Ovipositor with gonapophyses [n = 11, 0.075 –0.115 (0.094) mm] approximately 1.4x longer than width across apodemes [n = 11, 0.057 –0.083 (0.067) mm].

Hosts and Distribution. Tsuga dumosa in Bhutan (Mongar, Wangdue Phodrang) ( Fig. 9 ).

Remarks. Adelges (An.) lepsimon feeds between the needles on Tsuga dumosa twigs, in a similar fashion to A. (An.) tsugae , which feeds on T. dumosa and other Tsuga species ( Havill et al. 2016). The two species were collected together at two sites on different trees, so distinguishing them in the field may be difficult. Adelges (An.) lepsimon was collected more rarely than A. (An.) tsugae , which was also collected in Bumthang, Paro, and Thimphu Districts. In addition to exules of A. (An.) lepsimon , we also collected sexupara nymphs with wing pads ( Fig. 8C ), so it is likely that this species migrates to Picea where it completes a holocycle.

Figures

FIGURE 1. Phylogeny of Adelgidae reconstructed using mitochondrial COI and cytb, and nuclear EF1α DNA sequence data. The topology shown is from maximum likelihood analysis with IQ-TREE. Specimen data is shown in Table 1. The new species are highlighted in red. For species with multiple specimens, the country of origin and sometimes the host plant are shown in square brackets to indicate different sources. SH-aLRT and ultrafast bootstrap support from the maximum likelihood analysis, followed by posterior probability from the Bayesian analysis are shown for each clade.

FIGURE 8. Adelges (Annandina) lepsimon. A—D. Exules: first instar (paratype, USNM) (A), first instar exuvium (paratype, USNM) (B), sexupara nymph (paratype, USNM) (C), adult (holotype, USNM) (D).

FIGURE 9. Map of Bhutan showing collection locations for Adelges (Annandina) lepsimon.