Geoica inbari Barjadze, Halbert, Ben–Shlomo, 2022

Barjadze, Shalva, Halbert, Susan E. & Ben-Shlomo, Rachel, 2022, A new gall-producing species of Geoica Hart, 1894 (Hemiptera: Aphididae Eriosomatinae) from Israel, Zootaxa 5183 (1), pp. 343-354 : 345-352

Geoica inbari Barjadze, Halbert, Ben–Shlomo , sp. nov.

Figs 1–4 , tables 1–2

Type material. Holotype: N TA–T–00007, alate viviparous female on slide, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel Ben-Shlomo ; Paratypes: N TA–T–00001–5, 5 alate viviparous females (fall migrants) on five slides, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel BenShlomo ; N TA–T–00006, 8–10, 4 alate viviparous females (fall migrants) on four slides, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel Ben-Shlomo ; N TA–T–00011–12, 2 alate viviparous females (fall migrants) on 2 slides, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel BenShlomo ; N TA–T–00013–16, 4 alate viviparous females (fall migrants) on 4 slides, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel Ben-Shlomo ; N TA–T–00017–21, 5 alate viviparous females (fall migrants) on 5 slides, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel Ben-Shlomo ; N TA– T–00022, 1 alate viviparous female (fall migrant) on 1 slide, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel Ben-Shlomo ; N TA–T–00023–28, 5 alate viviparous females (fall migrants) and 1 first instar exule borne by fall migrant on 6 slides, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel Ben-Shlomo ; N TA–T–00029–34, 6 apterous fundatrigeniae on 6 slides, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel Ben-Shlomo ; N TA–T–00035–38, 3 alate viviparous females (fall migrants) and 1 apterous fundatrigenia on 4 slides, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel Ben-Shlomo ; N TA–T–00039–45, 5 alate viviparous females (fall migrants) and 1 apterous fundatrigenia and 3 embryos removed from body of fall migrants on 7 slides, on Pistacia palaestina, Mount Hermon , 33°17'18.96"N, 35°44'21.12"E, 1335 m a.s.l., ISRAEL, 12.viii.2016, leg. M. Inbar & Rachel Ben-Shlomo.

Depositories. Holotype (TA–T–00007) is deposited at IZISU and paratypes: 8 alate viviparous females (TA–T– 00001, 00010, 00015, 00019, 00024-25, 00035, 00041); 3 apterae fundatrigeniae (TA–T–00034, 00038, 00044); 1 first instar exule borne by fall migrant (TA–T–00028) and 3 embryos removed from body of fall migrants (TA–T– 00045) are deposited at IZISU; 6 alate viviparous females (TA–T–00002, 00009, 00012, 00014, 00018, 00040) and 2 apterae fundatrigeniae (TA–T–00032-33) are deposited at BMBCO; 6 alate viviparous females (TA–T–00020, 00023, 00026, 00036, 00037, 00042) are deposited at FSCA; 6 alate viviparous females (TA–T–00005, 00006, 00016, 00027, 00039, 00043) are deposited at NHMUK; 8 alate viviparous females (TA–T–00003-4, 00008, 00011, 00013, 00017, 00021, 00022) and 3 apterae fundatrigeniae (TA–T–00029-31) are deposited at SMNHTAU.

Description

Apterous fundatrigeniae (fig. 1) (n=8). Coloration in life: unknown. Pigmentation on slide: head, ANT, rostral III–V, stigma, subgenital and anal plates, femora and cauda are all pale brown.

Body small, 1.03–1.20 mm long, oval, with 5–segmented ANT. ANT cuticle with spinulose imbrications. ANT tubercles undeveloped. Primary rhinaria on ANT IV and V small with ciliate rims, accessory rhinaria ciliated. ANT 0.22–0.30 times BL. Number of setae on ANT I: 4–6, ANT II: 4–8,ANT III: 5–9,ANT IV: 3–5,ANT Vb: 4–9 and PT: 0. PT short with 5 apical and subapical setae, 0.34–0.47, 0.50–0.67 and 0.25–0.31 times ANT VIb, ANT IV and ANT III respectively. ANT IV 0.46–0.54, 0.45–0.56 and 0.36–0.58 times ANT V, ANT III and HT II L respectively. ANT V 0.88–1.09 times ANT III. ANT III 0.80–1.02 times HT II L. MSL on ANT III and frons 0.24–0.46 and 0.30–0.69 times ANT III BD respectively. Head convex. Frons with imbricated cuticle. Eyes only with triommatidia. Rostrum short, slightly passing the middle coxae. URS oblong triangular with blunt apex and 2–3 accessory setae, its length 1.79–2.21, 1.44–2.45 and 0.99–1.32 times URS W, ANT VI b and HT II L respectively. HFEM imbricated dorsally, 0.18–0.21 times BL. HTIB 0.21–0.22 and 2.24–2.94 times BL and ANT III respectively. Tarsi 2–segmented. HT II L 2.57–3.36 times HT II W. First tarsal formula: 3:3:3 or 3:3:2. ABD TERG VIII with 10–13 setae. ABD TERG I–VII and ABD TERG VIII 0.37–0.67 and 0.77–1.00 times ANT III BD respectively. Siphunculi absent. Subgenital plate oval, with spinulose imbrications. Anal plate enlarged and surrounded by the U–shaped ABD TERG VIII and forming a trophobiotic organ. Anal plate and gonapophyses with 34–41 and 5–7 setae respectively. Subgenital plate with 20–30 setae. Cauda small, semicircular with 8–15 setae. Dorsal and ventral setae short and pointed. Wax gland plates multifaceted. Wax gland plates on the head and thorax not discernible; one pair of wax gland plates present in spinal, pleural and marginal positions on each of ABD TERG I–VII. Metric characteristics are given in Table 1 .

Fall migrant (fundatrispuriae) (fig. 2) (n=35). Coloration in life: unknown. Pigmentation on slide: ANT, head, thorax, rostrum, stigmal plates, tarsi, anal and subgenital plates, cauda, gonapophyses and trochanters are brown; apical 1/3 or 1/2 of femora brown, while remaining halves are pale; tibiae brown with relatively paler brown or pale middle section; ABD TERG VII with brown scleroites at the bases of the dorsal setae; ABD TERG VIII with transverse brown bar or brown scleroites at the bases of the dorsal setae.

Body small to medium sized, 1.33–2.47 mm long. BW 0.39–0.57 times BL. ANT cuticle imbricated. ANT 6– segmented, 0.22–0.33 and 1.38–1.64 times BL and HW respectively. Primary rhinaria on ANT V and VI large, non– ciliated and occupying more than half of circumference of a segment, 0.25–0.60 of the antennal length. Different sized secondary rhinaria round, oval or irregular-shaped occupying small portion of circumference or at most its half. Number of secondary rhinaria on ANT III: 2–11, ANT IV: 1–4, ANT V: 0–1, ANT VI: 0. Both primary and secondary rhinaria have on their surfaces 0–14 pit–like depressions (0–8 on ANT III; 0–5 on ANT IV; 1–14 ANT V; 0–8 on ANT VI). Accessory rhinaria (coeloconic sensilla) on ANT VI ciliated. Setae on ANT, body, rostrum and legs pointed. Number of setae on ANT I: 4–5, ANT II: 4–12, ANT III: 3–10, ANT IV: 3–8, ANT V: 2–7 ANT VIb: 4–11 and PT: 0. PT short with 4–5 apical and subapical setae, 0.18–0.36, 0.19–0.34, 0.18–0.32, 0.11–0.23 and 0.04–0.09 times ANT VIb, ANT V, ANT IV, ANT III and HW respectively. ANT VI 0.64–0.97 and (0.92) 1.06–1.48 times ANT III and ANT IV respectively. ANT IV 0.67–1.10, 0.92–1.20, 0.53–0.80 and 0.58–0.80 times ANT VI, ANT V, ANT III and HT II L respectively. ANT V 0.53–0.73 times ANT III. ANT III 0.87–1.12 times HT II L. MSL on ANT III and frons 0.17–0.57 and 0.38–1.00 times ANT III BD respectively. Head convex. Head and thorax without wax gland cells and plates. Rostrum very short, not reaching the middle coxae. URS oblong triangular with blunt apex with 2–4 accessory setae, its length 1.87–2.40, 0.88–1.33, 0.24–0.31 and 0.60–0.77 times URS W, ANT VI b, HW and HT II L respectively. Forewing: costal and subcostal veins pigmented; pterostigma not extending around wing tip and edges pigmented; medial vein of forewing simple. Hind wing with two oblique veins. HFEM imbricated dorsally, 0.11–0.18 and 0.65–0.87 times BL and HW respectively. HTIB 0.20–0.32, 2.91–3.61 and 1.16–1.52 times BL, ANT III and HW respectively. HT II L 5–6.2 and 0.37–0.44 times HT II W and HW respectively. First tarsal formula: 4:3:3 or 3:3:3, rarely 3:4:3 or 4:4:4. SIPH absent.ABD TERG VIII with 8–13 setae. ABD TERG I–VII and ABD TERG VIII 0.32–0.95 and 0.95–2.24 times ANT III BD respectively. Anal plate extending dorso–laterally, completely joined with the cauda and form a perianal ring. Anal plate and gonapophyses with 30–46 and 4–9 setae respectively. Subgenital plate with spinulose imbrications and 46–73 setae on posterior half. Cauda with 14–24 setae. Different sized 1–2 wax gland plates always present on ABD TERG I–VII; several different sized oval or round shaped wax gland plates developed on spinal and sometimes pleural positions with 2–17 cells on ABD TERG I–VII. Metric characteristics are given in Table 1 .

Embryo of apterous exule within adult fall migrant (fig. 3) (n=11). ANT 4–segmented. Primary rhinarium on last antennal segments with ciliate rim. ANT, body and legs with pointed setae. Body length 0.774 –0.982 mm. Eye as triomatidium. Stylets present. URS long with 8–10 accessory setae on it. Tarsi 2–segmented. First tarsal chaetotaxy: 2:2:2. ABD TERG I–VII with 8–20 stout, none-attenuated, pointed ( 0.026 –0.035 mm) and 3–5 similarly shaped marginal ones. Ventral setae short and always pointed. ABD TERG VIII with 12–18 setae. Anal plate with 4 longitudinal rows of pointed setae (30–54 ones).

First instar larva borne by fall migrant (fig. 4) (n=1). Coloration in life: unknown. Pigmentation on slide: frontal part of head, tip of URS, anal plate, cauda, and ABD TERG VIII are all pale brown. Other parts of body pale, sclerotized.

Body small, 0.89 mm long, oval, with 4–segmented ANT. ANT, body, rostrum and legs with pointed setae. ANT cuticle with slight imbrications. ANT tubercles undeveloped. Primary rhinaria on ANT IV and V small with ciliate rims, accessory rhinaria ciliated. ANT 0.42 and 1.19 times BL and HW. BW 0.66 times BL. Number of setae on ANT I: 9, ANT II: 17, ANT III: 24, ANT IVb: 14 and PT: 0. PT short with 4 apical and subapical setae, 0.50, 0.20 and 0.10 times ANT IVb, ANT III and HW respectively. ANT IV 0.59 and 0.92 times ANT III and HT II L respectively. ANT III 1.56 times HT II L. MSL on ANT III and frons 0.97 and 0.86 times ANT III BD respectively. Head convex. Frons with granulated cuticle. Eyes only with triommatidia. Rostrum long, passing the hind coxae. URS long, oblong triangular with blunt apex. URS with 9 accessory setae, its length 3.55, 2.90, 0.56 and 1.77 times URS W, ANT VI b, HW and HT II L respectively. HFEM imbricated dorsally, 0.26 and 0.74 times BL and HW. HTIB 0.34, 0.97 and 1.99 times BL, HW and ANT III respectively. HT II L 3.16 and 0.31 times HT II W and HW. First tarsal formula: 2:2:2. ABD TERG VIII with 16 setae. ABD TERG I–VII and ABD TERG VIII 0.74 and 1.06 times ANT III BD respectively. Anal plate enlarged and surrounded by the U–shaped ABD TERG VIII and forming trophobiotic organ. Anal plate with 40 setae arranged as 4 irregular longitudinal rows. Subgenital plate invisible. Cauda short, semicircular with 11 setae. Wax gland plates as single pores, with pale brown edges. 5 pairs are on the head: one pairs on the frons, one pair medio–anteriorly on dorsum, 2 pairs latero–posteriorly on vertex. Pro–, meso– and metathorax and ABD TERG I–VII with 6 wax gland plates. Wax gland plates on ABD TERG VIII absent. Metric characteristics are given in Table 1 .

Etymology. The specific name is a noun in genitive, given in honour of Prof. Moshe Inbar (former surname Burstein), who has worked intensively on the biology and ecology of the Pistacia gall-producing Fordini aphids for several decades.

Diagnosis. All Geoica species induce sealed galls on the midvein of the leaflet ( Inbar et al. 2004). However, the new species differs from all other known Geoica species by the shape of the galls: it makes ‘coral’–shaped galls (fig. 5), while all other congeners produce spherical galls. The galls that are induced by Slavum wertheimae on lateral buds of P. atlantica are somewhat similar in general shape, but much bigger ( Wertheim & Linder 1961). Besides, fall migrants of Slavum have a single secondary rhinarium on ANT III and IV, while 2–11 and 1–4 secondary rhinaria are present on ANT III and IV, respectively, in the new species. The new species resembles Baizongia by the presence of a trophobiotic organ in apterae, but they are distinguished easily by PT length/PT basal width ratio in fall migrants (less than 2 in the new species, while ca. 3 in Baizongia ) ( Blackman & Eastop 2022). The new species is a member of the Geoica utricularia group and morphologically is most similar to Geoica wertheimae Brown & Blackman , which also lives on Pistacia palaestina . Fall migrants of the new species differ from the same morph of G. wertheimae by: 1. Number of secondary rhinaria: 12–33 on ANT III, 4–13 on ANT IV in G. wertheimae ( Brown & Blackman 1994) , while 2–11 on ANT III, 1–4 on ANT IV in G. inbari ; 2. ANT VI/ANT IV ratio: ANT VI shorter than ANT IV in G. wertheimae (in 92% of measured specimens) ( Brown & Blackman 1994), while it is 1.06–1.48 in G. inbari (in 97% of measured specimens: only a single specimen out of the 35 measured has 0.92).

Molecular analysis. Cluster analyses (Maximum Likelihood) of 1223bp of concatenated mitochondrial COI and 12S genes clearly discriminated between the ‘coral’-shaped and the globular Geoica galling aphids (fig. 6). Intraspecific distances between G. inbari samples were as low as 0.005. Genetic distances between G. inbari and other Geoica species were higher by an order of magnitude ( Table 2 ). Interspecific genetic differences between the new species and its morphologically similar G. wertheime were 4.6–4.7% ( Table 2 ).

Biology. The primary host of G. inbari is P. palaestina . This species is known only from gall–living morphs (apterous fundatrigeniae and fall migrants) and a first instar exule larva borne by a fall migrant in a gall on Pistacia palaestina . This species makes ‘coral’–shaped galls on the midvein of the leaflet ( Wool 1995). Gall–making aphids are generally believed to have intimate and long–standing relationships with their primary host plants, so the morphological difference between the gall of G. inbari and those of another closely–related Geoica species on the same host are remarkable, warranting further investigation. Its secondary host plant, life cycle and other morphs are unknown. Probably the new species has a two-year life cycle as in most other Pistacia –feeding Fordini . The galls are formed early in the spring. The fall migrants emerge in August from the tip of each “coral branch”. Mature galls turn red or yellow (fig. 5) and often secrete sticky resin loaded with terpenes (see Rand et al. 2014). As in other Geoica species, the galls caused early senescence (but not abscission) of the galled leaflet ( Inbar et al. 1995).

Distribution. The host tree, P. palaestina has a widespread distribution in the Mediterranean region. Earlier surveys that referred to the new taxon as “ Baizongiini sp. A” observed only three galls in three localities in northern and central Israel: Mt. Hermon, Mt. Meron and Judean Hills ( Koach & Wool 1977; Wool 1995). Recent surveys (R. Ben-Shlomo & M. Inbar, unpublished data) found the galls at several sites on Mt. Dov and Mt. Hermon ridges (Northern Israel), at 1150–1600 m a.s.l. At some sites, e.g. Mt. Kahal, Mt. Sna’im and Mt. Shezif (Hermon Ridge) several galls were found on specific trees every year.

Discussion. Favret (2022) lists 23 species in the genus Geoica , whereas Blackman & Eastop (2022) deal with only ten. The genus is known poorly, because the populations on grasses have not necessarily been associated with the primary host forms on Pistacia . However, it seems unlikely that the new species already has been described from Poaceae-feeding exules, because most of the 13 species without described forms from Pistacia can be eliminated by geography. Ten are known only from Europe, and the other three are known only from China (2) or India (1) ( Table 3 ). Additionally, two of the ten species in Blackman and Eastop (2022) are known only from grasses, but they are from Central Asia and India, not the Middle East ( Table 3 ). Thus, they also can be eliminated. The remaining eight species have their Pistacia generation accounted for and are separated from the new species easily by morphology and gall shape.

Figures

FIGURES 1–4. Geoica inbari sp. nov. 1. Apterous fundatrigenia (bar: 0.100 mm); 2. Alate viviparous female (fall migrant) (bar: 0.200 mm); 3. Embryo of apterous exule within fall migrant body (bar: 0.200 mm); 4. First instar larva of apterous exule borne by fall migrant (bar: 0.200 mm).