Uroleucon australe Nieto Nafría & Mier Durante,

Durante, M. Pilar Mier, Ortego, Jaime, Von Dohlen, Carol D. & Nafría, Juan Manuel Nieto, 2020, A further contribution to the knowledge of Uroleucon species (Hemiptera, Aphididae) living on Adesmia (Fabaceae) in southern South America, with description of a new species from Chile, Zootaxa 4748 (3), pp. 548-560: 553-559

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Uroleucon australe Nieto Nafría & Mier Durante

sp. n.

Uroleucon australe Nieto Nafría & Mier Durante  , sp. n.

Types. Holotype: apterous viviparous female, CHILE, Aysén Region, Capitán Prat province, Villa O’Higgins: La Baranda (48º 15’ S, 72º 21’ W, 430 m a.s.l.), on Adesmia boronioides  ; 18-January-2019; Mier Durante, Nieto Nafría and Ortego leg., sample CHI-546, specimen number 2 on a slide with one paratype; collection of the University of León (León, Spain)GoogleMaps  . Paratypes (9 viviparous apterous females, 49 oviparous females and 11 males): CHILE  , same data as that of the holotype, 6 apterous viviparous females and 4 oviparous females; CHILE, Aysén Region  , General Carrera province, General Carrera lake South bank (46º 37’ S, 72º 21’ W, 520 m a.s.l.), 20-January-2019, 2 apterous viviparous females; CHILE, Magallanes RegionGoogleMaps  , Última Esperanza province, Sarmiento de Gamboa lake South bank (51º 02’ S, 72º 47’ W, 160 m a.s.l.), 5-February-2016, 6 oviparous females and 4 males; CHILEGoogleMaps  , Última Esperanza province, Cerro Castillo 5 km South (51º 17’ S, 72º 24’ W, 140 m a.s.l.), 6-February-2016, 1 viviparous apterous female, 39 oviparous females and 7 males; all them on Adesmia boronioides, Mier Durante, Nieto Nafría and Ortego  leg.; collections of the University of León (León, Spain), Jaime Ortego (Mendoza, Argentina) and The Natural History Museum (London, United Kingdom)GoogleMaps  .

Apterous viviparous females. Figures 1View FIGURE 1 D–1I. Based on 10 specimens. Colour when alive matte green due to the presence of whitish waxy powder. Body 3.23–3.70 mm long and pear-shaped with long antennae and legs and noticeable siphunculi and cauda. Mounted specimens more-or-less very light brown with light brown to blackishbrown head, appendages, siphunculi, genital and anal plates and cauda, see details below. Setae on dorsum of body and antennae and several on legs thick and with apex truncate; other setae more-or-less pointed. Marginal tubercles absent. Head, including clypeus and mandibular and maxillary laminae, medium-brown. Frons sinuous, medialfrontal tubercle lower than the frontal-lateral (or antennal) tubercles. Cephalic dorsum with two pale anterior setae and four pale posterior setae. Antennal segment I darker than head, mainly on its inner side, and dorsally striate; antennal segment II pigmented as the head and weakly ornamented on its dorsal side; antennal segment III nearly smooth and progressively darkened from base, pigmented like segment II to a blackish brown extreme distal portion; antennal segment IV with transverse marks, and dark brown with a distal portion blackish brown; segments V and VI imbricated and dark brown. Sensoria round and with thick walls; primary sensoria ciliate; secondary sensoria small, non-protruding, more-or-less aligned from the end of the paler part of the segment. Rostrum reaching past middle coxae; proximal rostral segments (I and II) are pigmented as head and as middle strip of segment III, whose sides are very pigmented, almost black, as much as the ultimate segment (= rostral segments IV+V in Blackman & Eastop 2019), which is narrow. In the legs, the dominant pigmentation is similar to that of the head, except for areas internal-proximal of coxae, dorsal-distal of femora and distal about one eighth of tibiae, and entire tarsi, which can be darker up to blackish brown. Leg segments are smooth, except for tarsi. Thoracic and abdominal dorsum with shriveled appearance and no more pigmented than the cephalic dorsum, with small, brown spiracular and intersegmental-muscular-sclerites only present on thorax. Setiferous sclerites are completely absent in several specimens, in the most “ornamented” specimens they are present on abdominal segments 6 to 8 and on marginal areas of segments 3 and 4, although not associated with all setae; note that thoracic and abdominal setiferous sclerites are frequent, wide and well pigmented in most Uroleucon  , but usually absent in species living on Adesmia  . Siphunculi are progressively pigmented from medium-brown to dark brown, cylindrical and more-or-less as thick as the hind tibiae on most of their length, enlarged at its base, trumpet-shaped at the apex, with very small flange, and with small polygonal cells arranged in 8 to 10 rows and much more clearly defined than those of U. adesmiae  and U. nahuelhuapense  . Subgenital plate bicolored, being paler on the lateral-posterior edge. Anal plate as dark as the darkest part of siphunculi. Cauda lanceolate, more-or-less blunt at the apex, no darker than the palest part of siphunculi, with long and delicate setae. Metric and meristic features are in Table 3.

Alate viviparous females. Unknown.

Oviparous females. Figure 3DView FIGURE 3. Based on 49 specimens (24 measured, taken from all samples). Very similar to viviparous apterous females, with the following differences: (1) bright green when alive; (2) hind tibia somewhat swollen on proximal third with scent plates extending distally beyond the swollen portion; (3) pigmented zones of appendages paler, especially in specimens from Magallanes region, which have no brown areas on coxae and femora; (4) siphunculi paler and not so trumpet-shaped, presenting a slight flange; (5) cauda also paler. Quantitative features are in Table 3.

Males. Figures 3E and 3FView FIGURE 3. Based on 11 specimens. Apterous. Brown when alive. They are also very similar to apterous viviparous females, although slightly smaller, with siphunculi shorter than viviparae and oviparae, less markedly trumped-shaped and with a more-or-less marked flange, and cauda also shorter and more-or-less triangular. Scent plates are present in the hind tibiae, which are very slightly thickened than the tibiae of the other legs; the presence of these pheromonal structures is very surprising because they are typical of oviparous females in Aphidinae  . Mounted specimens show: an intense pigmentation of antennal segments III to VI; abundant dorsal setiferous sclerites on thoracic and abdominal segments as pigmented as the intersegmental and spiracular sclerites, those on segment 8 coalescing in some specimens; a transverse band on segment 7; and sometimes few and very scattered ventral sclerites on other abdominal segments. Quantitative data are in Table 3.

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Etymology. The specific name australe  is an epithet in neutral gender because Uroleucon  is neutral, that means “belonging or relative to the south” and refers to the very southern distribution of the species.

Bionomics. Uroleucon australe  feeds on the small stems of small plants of Adesmia boronioides Hook.  f. ( Fabaceae  ), which is its only known host. It can be conjectured that the alate viviparae in this species are infrequent, because they and their nymphs are unknown, and alatae are also infrequent in the other two Uroleucon  species living on Adesmia  ,. Males and oviparous females have been collected in the middle of summer, which shows that the life cycle of the species is abbreviated. As the males are apterous, it is clear that the species is monoecious, not host-alternating.

The presence of scent plates in several apterous viviparous females is not surprising if they belong to autumnal generations. All studied males bear scent plates, but it is not possible to ensure that this is a universal character of the U. australe  males, because the studied specimens were collected in two locations very close to each other.

Geographical distribution. The new species is currently known in four Chilean localities with low altitude and south to parallel 46º S, in the Aysén and Magallanes regions, north and south of the Patagonian ice fields, which are connected in viable ways for the movement of insects in general by two corridors east and west of those fields. The eastern corridor has characteristics of climate and vegetation that are more similar to those of the collection sites, whilst the western corridor, formed by islands and fjords, is very humid and forested. Thus, it is possible that the species could also be found in Chubut and Santa Cruz ( Argentina) in areas near the mountain range.

Molecular analyses. Comparisons of U. australe  sp. n. COI and tRNAleu-COII sequences with other South American Uroleucon  , as well as northern hemisphere species, confirmed that U. australe  was genetically most similar to U. nahuelhuapense  (results not shown). Genetic distances between U. australe  and U. nahuelhuapense  were 1.7% for COI and 1.1% for tRNAleu-COII. These distances are within the range found previously for closely related aphid species ( Foottit et al. 2008; Nieto Nafría et al. 2019), and corroborate the distinction of U. australe  sp. n. based on morphology.

Taxonomic discussion. The differences between Uroleucon  species are usually based on the qualitative and quantitative characters exhibited by the respective apterous viviparous females; in fact, the keys to Uroleucon  species by Blackman & Eastop (2019), and the successive keys to identify the South American Uroleucon  species ( de Carvalho et al. 1998; Mier Durante and Ortego 2008; Nieto Nafría et al. 2019) refer to characteristics of this morph, which may be the only one known, although features of alate viviparae are complementarily used in several disjunctive couplets. Apterae of several South American Uroleucon  species differ from related species by some characteristics, sometimes very few, which can overlap in part, such as in the differences between U. bereticum (Blanchard)  , U. macolai (Blanchard)  and U. mendocinum Mier Durante and Ortego. The  same occurs in other species-rich aphid genera, for example, between specimens of Aphis fabae Scopoli  , A. rumicis Linnaeus  and A. solanella Theobald  , or even in genera with few species, for example between apterous viviparae of Hyperomyzus lactucae (Linnaeus)  and of H. pallidus Hille Ris Lambers. To  carry out the identifications in these cases, several characters with overlapping ranges, sometimes extensive, must be studied in a large series of specimens. However, sometimes a solitary character can resolve the identification, even if it is qualitative and infrequently used for the identification of aphids of that group.

Apterous viviparous females of U. nahuelhuapense  and U. australe  sp. n. are very similar to each other in quantitative features, and the only appreciable differences between them, although largely overlapping, are listed in Table 4. These differences have to be assessed with caution because the quantity of samples studied is small and their geographical origin is limited or very limited. However, the two species can be separated by two very obvious qualitative characteristics: body colour when alive and shape of siphunculi; apterous viviparous females of U. nahuelhuapense  are bright green whereas those of U. australe  sp. n. are matte green, and siphunculi of U. nahuelhuapense  are subconical ( Figure 1BView FIGURE 1), whereas those of U. australe  sp. n. are distally trumpet-shaped. ( Figure 1GView FIGURE 1).

In certain cases, alate viviparous females assist in distinguishing some South American Uroleucon  species, but the alatae of U. australe  sp. n. are not known. On the contrary, oviparous females and males of U. nahuelhuapense  and U. australe  sp. n. are known and they help with taxonomic separation of the two species. The contribution of oviparous females to identification is small, because like apterous viviparae the oviparae of the two species are very similar. Useful features of oviparae in U. nahuelhuapense  and U. australe  sp. n. are listed in Table 4.

Contrary to what is typical for aphids, the males of U. australe  sp. n. have a greater number of distinguishing characters than are found in the females, particularly the viviparous females. Several differences between males of both species ( Table 4) refer to the siphunculi and the cauda, which greatly influence the general appearance of these specimens and allow us to easily separate them ( Figures 3B and 3EView FIGURE 3).

The key by Nieto Nafría et al. (2019) can be used to identify apterous viviparous females of U. australe  sp. n. after minor adjustments in disjunctive couplets 13, 14 and 15, which are in bold and underlined font, and including the new disjunctive couplet 15’, as follows:

13. Siphunculi usually at least 1.5 times cauda, which is 0.24−0.47 mm and can have 13 or less setae or 17– 41 setae, if more than 17 then ultimate rostral segment 1.1–1.4 times hind tarsi second segment, and antennal segment VI processus terminalis at most 4. 6 times antennal segment VI base and antennal segments I and II paler than most of the antennal flagellum............ 14

- {without changes} Siphunculi usually at most 1.6 times cauda, which is 0.30−0.83 mm and has 9−31 setae............. 18

14 {without changes} First tarsal segments with 3 setae. Siphunculi shorter than 1.8 times caudal length. [Antennal segment III with 2–8 secondary sensoria in apterae (restricted to proximal half) and 6–22 in alatae]. Pale to medium-green in life. On Baccharis  species and Hysterionica jasionoides  . Argentina: Catamarca, La Rioja, Mendoza, San Juan; Chile: Coquimbo .................................................................................................... U. essigi 

- First tarsal segments usually with 4–5 setae, if only 3 setae present on some legs then siphunculi 1.6 –2.3 times cauda.... 15

15 Apterae with 2– 15 secondary sensoria restricted to proximal 53% of the length of segment. On Adesmia boronioides  . [Anten- nal segment VI processus terminalis 3.2– 4.6 times antennal segment VI base; ultimate rostral segment 1.1–1.4 times hind tarsi second segment, which is 0.13– 0-18 mm; siphunculi 1.5 –2.3 times cauda, which is 0.33 –0.47 mm. Setae on antennal segment III 28– 53 μm] .......................................................................................15’

- {without changes} Apterae with 4–16 secondary sensoria extending over most of length of segment. Other above-mentioned characters are not presented together. On species of Asteraceae  ................................................ 16

15’ Distal part of siphunculi cylindrical and with a conspicuous terminal flange. Bright emerald green in life. Cauda with 17–29 setae. Siphunculus usually more 9.1–15.2 (exceptionally down to 8.4) times its width at the beginning of reticulation. Second segment of hind tarsi 0.13–0.17 mm. 10–21 dorsal setae on abdominal segments 2 to 5, being the spinal ones 23–50 μm long. Argentina: Neuquén ..................................................................... U. nahuelhuapense 

- Distal part of siphunculi trumpet-shaped and with a small terminal flange. Matte green with whitish was powder in life. Cauda with 26–41 setae. Siphunculus 8.3–11.3 times its width at the beginning of reticulation. Second segment of hind tarsi 0.16–0.18 mm. 12–15 dorsal setae on abdominal segments 2 to 5, being the spinal ones 25–38 μm long. Chile: Aysén and Magallanes ......................................................................................... U. australe  sp.n.

TABLE 3. Metric and meristic features of U. australe sp. n.: apterous viviparous females (apt.viv.fem.), oviparous fe- males (ov.fem.) and males (males). Numbers in parentheses are exceptional data, or very exceptional if parentheses are duplicates. NOTES: (1), specimen from Cerro Castillo (Magallanes region).

Feature apt.viv.fem. ov.fem. males
  n=10 n=24 n=11
body (cauda included) [mm] 3.23–3.70 2.40–3.30 2.03–2.43
body / siphunculus [times] 4.26–5.07 4.09–5.37 3.85–6.55
setae on head dorsum behind the anterior discal pair [number] 4–5 ((3))4(5) ((3))4
setae on vertex [μm] 43–60(73) 50–60 45–53
setae on vertex [times D] 1.0–1.3 1.2–1.4 1.2–1.5
antenna [mm] 2.72–3.53 2.85–3.50 1.93–2.98
antenna / body [times] 0.8–1.0 0.9–1.2 0.9–1.4
antennal segment III [mm] 0.70-0.93 0.71–0.89 0.64–0.75
setae on antennal segment III [μm] 28–40 30–50 40–48
setae on antennal segment III [times D] 0.6–0.9 0.7–1.1 1.1–1.3
secondary sensoria on antennal segment III [number] (4)7–12(15) 2–9 46–62
antennal segment III with secondary sensoria [%] 25–51 25–57 ~95
antennal segment IV [mm] 0.47–0.95 0.49–0.69 0.48–0.66
secondary sensoria on antennal segment IV [number] // // 10–24
antennal segment V [mm] 0.47–0.66 0.47–0.65 0.40–0.53
secondary sensoria on antennal segment V [number] // // (1)4–11
antennal segment VI base [mm] 0.16–0.20 0.16–0.20 0.13–0.20
antennal segment VI processus terminalis [mm] 0.62–0.78 0.69–0.84 0.59–0.68
antennal segment VI processus terminalis / antennal segment III [times] 0.7–1.0 0.8–1.1 0.8–1.0
antennal segment VI: processus terminalis / base [times] 3.7–4.6 3.8–4.9 (3)4.1–4.9
ultimate rostral segment [mm] 0.18–0.22 0.18–0.20 0.17–0.19
ultimate rostral segment / antennal segment VI base [times] 1.0–1.3 1.0–1.2 0.9–1.3
ultimate rostral segment / second segment hind tarsus [times] 1.1–1.3 1.1–1.3 1.1–1.2
ultimate rostral segment / its basal diameter [times] 2.2–2.9 2.2–3.1 2.3–2.7
setae on ultimate rostral segment, accessory [number] 6–10 7–10 6–8
hind femur [mm] 0.98–1.16 0.85–1.10 0.73–0.90
hind tibia [mm] 1.78–2.13 1.63–1.95 1.40–1.63
scent plates on a hind tibia [number] (1) (10)–(12) 16–95 1–17
scent plates on both hind tibiae [number] (1) (22) 53–189 5–32
scent plates, occupied length of hind tibia [percentage] (1) (25)–(34) 36–59 19–38
setae on first tarsal segments ((3))(4)5 (4)5 ((3))(4)5
second segment hind tarsus [mm] 0.16–0.18 0.15–0.17 0.14–0.16
setae on abdominal segment 2 to 5, dorsal, total [number] 12–15 10–14 12–15
setae on abdominal segment 2 to 5, marginal each side [number] 2–3 2–3 2–3
setae on abdominal segment 2 to 5, spinal & pleural [number] 8–9 6–10 8–10
setae on abdominal segment 2 to 5, spinal [μm] 25–38 28–50 38–48
setae on abdominal segment 2 to 5, spinal [times D] 0.6–0.8 0.6–1.3 1.0–1.4
setae on abdominal segment 2 to 5, ventral [number] 46–76 42–64 36–45
setae on abdominal segment 8 [number] 8–12 7–16 6–8
setae on abdominal segment 8 [μm] 48–68 45–78 45–70
setae on abdominal segment 8 [times D] 1.1–1.4 1.1–1.9 1.2–2.0

males (ov.fem.) and males (males). Numbers in parentheses are exceptional data, or very exceptional if parentheses are duplicates. NOTES: (1), specimen from Cerro Castillo (Magallanes region).