Aphis (Aphis) mirabilis Nieto Nafría & Ortego, 2022

Nafría, Juan Manuel Nieto, Moreno-González, Víctor, Ortego, Jaime, Favret, Colin & Durante, M. Pilar Mier, 2022, Aphis mirabilis sp. n. (Hemiptera, Aphididae, Aphidina), a South American species resembling A. craccivora, and further data on A. tropaeoli, Zootaxa 5183 (1), pp. 22-48 : 37-43

4. Aphis (Aphis) mirabilis Nieto Nafría & Ortego sp. n.

Types. Holotype, apterous viviparous female (number 1 of sample ARG- 221 in a slide with the oviparae 1 and 2), Argentina: Mendoza, Malargüe (35.472º S, 69.570º W, 1410 m a.s.l.), 5-May-1997, on Atriplex nummularia, J. Ortego leg., University of León collection ( León , Spain) . Paratypes: 185 apterous viviparous females, 81 alate viviparous females and 49 oviparous females and 4 males in all, University of León , Jaime Ortego (Málaga, Spain) and Natural History Museum, London ( United Kingdom) collections, belonging to the following nine samples, Argentina: (1) same data as holotype: 16 apterous viviparae, 5 alate viviparae and 22 oviparae females; (2) Mendoza, Malargüe , 10-March-1997, on A. nummularia , 8 apterous viviparae and 6 alate viviparae; (3) Mendoza, Malargüe , 5- April-1997, on A. nummularia , 76 apterous viviparae, 51 alate viviparae and 1 oviparous female; (4) Mendoza, San Carlos , 17-November-1994, on A. lampa , 10 apterous viviparae and 12 alate viviparae; (5) Mendoza, Tupungato , Cruz Negra, 21-November-1997, on A. lampa , 6 apterous viviparae and 4 alate viviparae; (6) Mendoza, San Carlos , 17-November-1994, on Bougainvillea spinosa , 36 apterous viviparae and 1 alate viviparous; (7) Mendoza, Malargüe, Cueva del Tigre , 16-November-1996, on B. spinosa , 23 apterous viviparae and 2 alate viviparae; (8) Mendoza, General Alvear , 20-May-1996, on Robinia pseudoacacia , 7 apterous viviparae and 16 oviparae; (9) Neuquén, Chos Malal , El Domuyo, 4-April-1999, on Adesmia volckmannii , 3 apterous viviparae, 10 oviparae and 4 males .

Other studied material. (A) 862 apterous viviparous females of samples in Table 1 rows 18, 20–24, 26– 29, 32, 35–44, 47, 49, 51–53, 55–58, 61–67, 69–82, 84–102, 104–106, 108–109, 113, 115–123, 125–126, 131– 133, 139–145, 147–148 and 150; several alate viviparous females of some of these samples. (B) Four viviparous females with some features of oviparous females: Argentina, Mendoza, General Alvear , 20-May-1996, on Robinia pseudoacacia .

Note. From here, and for brevity reasons, the name of the species is written without specifying its authors —Nieto Nafría and Ortego— and its subgeneric ascription.

Apterous viviparous females ( Fig. 2 : A, B & C). From 186 specimens, 75 of them measured. Body broadly oval as usual in the genus, 1.113 –1.988 mm long. When alive variously coloured: dark green, pink, caramel, brown, black or sometimes bicoloured, with black siphunculi and cauda, and usually covered by a thin layer of whitish powdery wax, which is more conspicuous on the margins of the body. The clypeus is quite evident, bulging downwards and somewhat expanded forwards, although not exceeding the front line (this character is especially visible in the specimens preserved in ethanol). Metric and meristic features of mounted specimens in Table 3 . Setae in general very pale, thin, and pointed. Head very brown to black and smooth. Frons gently sinuous. Clypeus voluminous, its edges approaching the edges of the antennal pits, dark brown, as are the mandibular and maxillar lames and rostrum. Antennae six-segmented; segments I and II as pigmented as head dorsum, and smooth; antennal flagellum pale for the most part, segment V sometimes brownish distally and segment VI all brown or brownish on its proximal half and darkening towards its apex. Segment III dorsally smooth and with scattered groups of small spicules on its ventral face, with 2–8 setae and very exceptionally with secondary sensoria (1–5). Segment IV with transverse striae; segments V and VI imbricated. Rostrum reaches to or slightly beyond middle coxae. Ultimate rostral segment moderately long and relatively broad, with two accessory setae. Prothoracic marginal tubercles as large as the triommatidia, approximately as long as their basal widths and as long as the closest seta. Coxae, trochanters and distal part (half at most) of femora pigmented like head, darker than the proximal part of femora and most part of tibae, but paler than distal part of tibiae and tarsi. Femora and tibiae with few setae: 3 at most on ventral edge of femora and approximately 20 on the dorsal face of tibiae. Tarsal formula 3.3.2 (very exceptionally 3.3.3). Thoracic segments with marginal and spinal patches more-or-less close to each other, but not forming a continuous band, and spinal ones are sometimes absent; brown and weakly striated. Segmental sclerotization of abdominal dorsum very variable. In the most sclerotized and darkest specimens; segments 1 to 5 with a spino-pleural plate, irregularly edged, extending between the intersegmental sclerites to the marginal areas, in which there are small sclerites, and reticulated but sometimes inconspicuously; segment 6 with a wide and also smooth band, and segments 7 and 8 with small, narrow, spinulose individual transverse bands. In the intermediate specimens, segments 1 to 5 present a spino-pleural plate with holes or transversal bands or large paired sclerites, plus marginal sclerites, and segments 6 to 8 have individual transversal bands of varied surface. Less sclerotized specimens (smaller than 1.50 mm) only have small and dispersed sclerites. Intersegmental sclerites, if evident, are darker than segmental sclerites and the small spiracular sclerites. Marginal tubercles of abdominal segments 1 and 7 usually less voluminous and relatively narrower than the prothoracic tubercles. Intermediate abdominal segments without marginal tubercles. Siphunculi relatively short, uniformly tapering to the apex or tapering on proximal half and almost cylindrical on distal half, with a very small flange, intensely and homogeneously dark brown and imbricated by the presence of small groups of spinules. Abdominal segment 8 with 2 setae. Genital and anal plates dark brown, with 2 (or infrequently 3–5) discal setae and 5–18 posterior setae. Cauda elongate but usually shorter than siphunculi, moderately finger-shaped (because the subproximal constriction is not very marked) or triangular, almost as dark as the siphunculi, and with 4–9 setae.

Alate viviparous females ( Fig. 3 B ). From 81 specimens, 34 of them measured. 1.250 –1.850 mm long. When alive, head, thorax, appendages, siphunculi and cauda black or very dark brown, and abdomen coloured and powdered like the body of apterous viviparae. Clypeus not as swollen as in apterous viviparae. When mounted, very similar to apterae but with darker head, antennae, legs (entirely or mostly), siphunculi and cauda. Antennal segment III with 4–10 secondary sensoria, relatively big and aligned over most of the segment. Marginal tubercles smaller than those of apterae. Abdominal segments 2, 3 and 4 with relatively broad marginal sclerites; segment 6 with a spinal and postsiphuncular sclerites; segments 7 and 8 with individual transverse bands (sometimes very thin or even fragmented), always with spinules; sometimes spino-pleural bands or isolated sclerites are present. Other qualitatively and meristic features like those of apterous viviparae. Metric features in Table 3 .

Oviparous females ( Fig. 3 A ). From 49 specimens, 46 of them measured. Colour, wax powder, and shape of clypeus as in viviparae. Body slightly pear-shaped tapering backwards, 0.950 –1.725 mm long. They are similar to apterous viviparae in most qualitative and meristic features, but with: (1) dorso-abdominal segmental sclerotization very reduced or absent; (2) legs more intensely and widely pigmented; (3) hind tibiae moderately widened and with pheromonal plates, 24–154 in each leg, usually 45–110, and 54–255 in both legs, usually 100–190; (4) abdominal segment 8 with 4–8 setae; (5) cauda less pigmented and with 5–11 setae; and (6) genital plate with a medial pale stripe and with 23–48 setae. Metric characters in Table 3 .

Males, apterous ( Fig. 3 C ). From 4 specimens. Colour when alive unknown. 1.200 –1.375 mm long. Colour when alive unknown, black or dark green with black dorsum possibly. Frons almost straight. Antennae dark throughout their length and with secondary sensory extended in the ventral face, round and with a marked rim, 13–22, 9–14, 8– 13 on segments III, IV and V, respectively. Large and complete cross-bands on all abdominal segments, sometimes contacting the immediate ones, with irregular borders, narrowing between the pleural and marginal area; the band on segment 1 do not reach to marginal area. Legs more pigmented than those of females. Siphunculi very dark, shorter and narrower than those of females. Cauda triangular, as dark as siphunculi and anal plate and genital pieces, with 7 setae. Other qualitative characteristics like those of females. Metric and features in Table 3 .

Other specimens, not types. (i) Apterous and alate viviparae belonging to the problem samples group 2 ( Table 1 ) that have been identified as “problem entity” and show some small differences in relation to the type specimens, which are shown in square brackets in Table 3 . (ii) Four viviparous females (containing embryos) collected on R. pseudoacacia together with specimens of the type series, which show some characteristics of oviparous females; one of them has the complete appearance of an apterous vivipara but with 36 setae on the genital plate and 9 scent plates on the hind tibiae; another two have a pterothorax, 33 and 44 or 68 and 94 scent plates, the dorsal abdominal sclerotization of apterous viviparae, and 46–48 setae on the genital plate; the fourth specimen has a median ocellus, a pterothorax with ill-formed wings, 10 and 18 scent plates in each hind tibia, dorsal abdominal sclerotization of an alate vivipara, and 90 setae on the genital plate.

Bionomics. Type specimens of Aphis mirabilis sp. n. were seen forming compact groups on the fine twigs of Atriplex nummularia Lindl. and Atriplex lampa (Moq.) Gillies (Amaranthaceae) , Bougainvillea spinosa (Cav.) Heimerl (Nyctaginaceae) , and Adesmia volckmannii Phil. and Robinia pseudoacacia L. ( Fabaceae ), sometimes spreading to the underside of leaves or flower bunches. Ad. volckmannii , At. lampa and B. spinosa are native plants, while the other two are allochthonous in South America. The new species can colonize herbaceous plants or shrubs of at least another 21 genera belonging to nine families ( Table 1 ): it is clearly a polyphagous species.

The presence of oviparae and males indicates that A. mirabilis sp. n. has a holocycle. Their collection on three plants of different genera reaffirms the remarkable polyphagia of the species. Because of this polyphagy, one might expect the males to be winged, but we have only found them to be apterous; it may be that the species can have males of both types, as happens in other species of the genus. Sexuals were collected at the beginning of April in El Domuyo , at the beginning of May in Malargüe, and at the end of May in Geneneral Alvear; the temporal difference of the collections can be explained by the altitude and latitude of the three places: El Domuyo, 36.67º S and 1750 m, Malargüe 35.47º S and 1410 m, General Alvear, 34.93º S and 700 m.

Distribution. Aphis mirabilis sp. n. is widely distributed in Argentina: studied specimens were collected in 67 localities belonging to 13 provinces: Catamarca, Chubut, Córdoba, Jujuy, La Pampa, La Rioja, Mendoza, Neuquén, Río Negro, Salta, San Juan, San Luis and Tucumán, and also in one locality of the Chilean region of Arica y Parinacota.

Etymology. The specific name mirabilis of the new species is a Latin adjective that means "amazing", "surprising", since it is very surprising that an aphid species can produce oviparous females on plants of several families, and that its viviparous females (and perhaps also its sexual forms) can live on such a diversity of plants; its gender follows that of the feminine genus name.

Taxonomic discussion, diagnosis. The characteristics of the new species undoubtedly correspond to those of the nominotypical subgenus of the genus Aphis . Most of the apterous viviparous females, those with the ultimate rostral segment longer than the second segment of the hind tarsus, have characters in common with 27 species of Aphidina known in South America; those with the ultimate rostral segment no longer than the second segment of the hind tarsus, have characters in common with A. tropaeoli and A. berberidorum Ortego & Mier Durante ( Nieto Nafría et al., 2019a: identification key, group of species 7 and key couple "N”).

The tarsal formula allows rapid separation of A. mirabilis sp. n. from A. tropaeoli and A. berberidorum : it is 3.3. 2 in A. mirabilis and 3.3. 3 in the other two species.

Apterous viviparae of A. craccivora , A. cytisorum , A. intybi Koch , very similar to each other, and of Brachyunguis bahamondesi Remaudière & Halbert , are the ones of the mentioned "group 7" that conspicuously resemble the new species using the characters commonly used in aphid taxonomy. Aphis mirabilis sp. n. can be differentiated from these three species of Aphis , and even from any other species of genus Aphis known in South America, by a moderate swelling of the clypeus, and from B. bahamondesi because in this species the clypeus is even more swollen.

The somewhat thickened clypeus can be seen in apterous viviparae of A. mirabilis sp. n. preserved in ethanol. To appreciate it in mounted specimens, the specimen must be well positioned, and it is not always possible to decide whether it is sufficiently thick ( Fig. 2B ). Other characteristics can help differentiate the new species from A. craccivora , as presented in the following identification couplet:

- Clypeus swollen (i.e., maximal width of the clypeus 0.75–1.15 times minimal ventral distance between antennal alveoli and maximal distance between the outer edges of the mandibular lamina 1.10–1.35 times minimal ventral distance between the antennal alveoli; see Fig. 2B ). Abdominal segments 1 to 5 or 6 diversely sclerotized: with discal plate (entire or fragmented), spino-pleural plate (entire or fragmented) or isolated sclerites, or widely or entirely membranous. Processus terminalis of antennal segment VI rarely longer than 1.9 and frequently shorter than 1.5 times the base of the segment. Longest seta on abdominal segment 8 goes to 48 µm. Ratio “(6.06 × [antennal segment VI processus terminalis / antennal segment VI base]) – (8.94 × [longer abdominal seta on abdominal segment 8 / subarticular width of antennal segment III])” less than 0........................................................................................... Aphis mirabilis sp. n.

- Clypeus not swollen (i.e. maximal width of the clypeus 0.65–0.85 times minimal ventral distance between antennal alveoli and maximal distance between the outer edges of the mandibular lamina 0.90–1.20 times minimal ventral distance between the antennal alveoli). Abdominal segments 1 to 5 or 6 usually with discal plate (it covers spinal, pleural and marginal areas), sometimes a bit fragmented, only exceptionally and in poor environmental conditions reduced. Processus terminalis of antennal segment VI usually longer than 2.0 times and rarely shorter than 1.6 the base of the segment. Longest seta on abdominal segment 8 usually shorter than 30 µm. Value of “(6.06 × [antennal segment VI processus terminalis / antennal segment VI base]) – (8.94 × [longer abdominal seta on abdominal segment 8 / subarticular width of antennal segment III])” greater than 0...................................................................................... Aphis craccivora

Apterous viviparous females of A. cytisorum and A. intybi are very similar to those of A. craccivora (see Blackman & Eastop, 2020, for identification keys to aphids living on Laburnum and on Cichorium ), in such a way that the differences shown between A. mirabilis sp. n. and A. craccivora serve to differentiate the new species from both the other two species. Additionally, A. cytisorum lives exclusively on woody leguminous plants and A. intybi lives exclusively on Cichorium intybus .

Alate viviparous females of most species of Aphis are very difficult to separate from each other. This also applies to the separation of A. mirabilis sp. n. from A. craccivora and the species close to it that have been mentioned. The identification can be done by the ratio between the processus terminalis and the base of the antennal segment VI, and by the length of the seta of the abdominal segment 8, which are like those of the apterous viviparae. But it can also be done in living or in ethanol-preserved specimens at low magnification as follows:

- Antennae entirely brown or dark brown, with no noticeable difference between the pigmentation of the antennal segments I, II and III. Dorsum of abdominal segments 2 to 5 with marginal sclerites, and usually without bands, disperse small spinal or pleural sclerites can be present......................................................... Aphis mirabilis sp. n.

- Antennal segment III and IV are noticeably paler than segments I and II, which are brown or dark brown. Dorsum of abdominal segments 2 to 5 with marginal sclerites, and usually with bands, sometimes broken..... Aphis craccivora and similar species

Oviparous and male aphids are rarely used in species diagnosis and specimen determination, but they can provide important information for taxonomic decisions (e.g., Mier Durante et al. 2020). The differences between the ovipara and males of A. craccivora and A. mirabilis sp. n. are relevant. Just as with viviparae, the ratio between the two parts of the antennal segment VI (processus terminalis, base) is much smaller in oviparous and male of the new species than in it is in A. craccivora .

The general appearance and almost all other characters of the oviparae of both species are similar to each other, although A. mirabilis sp. n. has a greater number of scent plates ( Table 4 ).

The males are very different, due to the presence of wings in A. craccivora and their absence in the new species. There are also differences in the dorso-abdominal sclerotization. The cauda is longer in the new species than in A. craccivora , both in terms of absolute length as well as in relation to the length of the siphunculi ( Table 5 ).

Figures

FIG. 2. Aphis mirabilis Nieto Nafría & Ortego sp. n., apterous viviparous female.A, general view. B, head, double arrows from top to bottom: minimal ventral distance between antennal alveoli, maximal width of the clypeus, maximal distance between the outer edges of the mandibular lamina; C, hind leg.

FIG. 3. Aphis mirabilis Nieto Nafría & Ortego sp. n. (A, B, C) and A. tropaeoli (D). A, alate viviparous female. B, oviparous female. C, D, male.