APHIS PRIMA SP. N. (HEMIPTERA, APHIDIDAE), FROM ARGENTINA AND CHILE, FIRST APHID SPECIES WORLDWIDE COLLECTED ON SCHOEPFIACEAE (SANTALALES)

Introduction[Up]

Taxonomic studies of aphids are often aimed at studying the diversity related to plant genera or families. This procedure is especially useful to assess the possible novelty of aphid species, especially if they belong to aphid genera with many species, such as Aphis, Uroleucon, Dysaphis or Macrosiphum (Aphidinae), Chaitophorus (Chaitophorinae) or Cinara (Lachninae) (see ‍Blackman & Eastop, 2021). The authors of this paper have applied this procedure in their taxonomic studies of aphids in temperate or cold-temperate Argentine and Chilean regions for over 20 years (see ‍Blackman & Eastop, 2021: “Bibliography”), having described several species of Aphis and also of Uroleucon (Aphidinae) and Neuquenaphis (Spicaphidinae).

In this work, results of the study of seven samples of aphids collected on Quinchamalium chilense and one from an unidentified species of Arjona (Schoepfiaceae), possibly A. patagonica, are presented, which show the characteristics of the genus Aphis Linnaeus, 1758 (Hemiptera, Aphididae, Aphidina). These plants are herbs with perennial rhizomes.

The Schoepfiaceae family was recognized in APG III, and remains in APG IV (‍Angiosperm Phylogeny Group, 2009, ‍2016). It currently includes three genera: Schoepfia, Arjona and Quinchamalium (‍Hassler, 2019). Schoepfia was classified in Olacaceae until 2009. It currently includes 27 species, 23 of which are South American. Arjona and Quinchamalium were previously classified in Santalaceae; they include respectively 5 and 20 South American species (‍Hassler, 2019), although Vidal-Russell (‍2019) and López Laphitz et al. (‍2015) consider that each of these different genera includes a single species.

No aphids have yet been collected from Schoepfiaceae anywhere in the world. Two Aphis species are known from Santalaceae: A. thesii Holman, 1966 and A. neothesii Pashchenko, 1996 (‍Blackman & Eastop, 2021); these are palaearctic.

The viviparous females collected on Quinchamalium and Arjona are markedly different from those of A. thesii and A. neothesii. They are also different from those of the other Aphis species known in South America (see the Taxonomic Discussion section).

These differences have allowed the establishment of Aphis prima sp. n.

Material and methods[Up]

Standard protocols for collection, rearing, ethanol preservation, slide preparation, and morphometric study have been employed (see ‍Nieto Nafría & Mier Durante, 1998). Microphotographs were taken using a smartphone iPhone 11 through an eyepiece adapted to an Olympus CX41 microscope and were subsequently treated with Corel Photo-Paint 2018 and Microsoft Publisher 2010.

In the collection data: (a) Spanish orthography, diacritics included, was retained in the geopolitical names; (b) geographical coordinates and altitudes were validated using Google Earth Pro, v.7.3.2; and (c) authors’ surnames as collectors of paratypes are abbreviated to M.D., N.N. and O. For the vein terminology see Franielczyk-Pietyra & Wegierek (‍2017).

In the description, text and table, the quantities in parentheses show an exceptional limit on the range of variation of the characteristic.

Results and discussion[Up]

Aphis (Aphis) prima sp. n.

urn:lsid:zoobank.org:act:D2F6DE43-90A4-4F69-87C2-28887233A9D5

Figs. 1–3

Alatae viviparous females (Figs. 2, 3). Based on 49 specimens. 1.225–1.750 mm. When alive head and thorax (including antennae and legs) brown to dark brown, and abdomen neutral green, light green or yellow green. Pigmentation when mounted similar to apterae but with dark brown thorax. Frons straight. Antennal segment III with 7–18 secondary sensoria placed on the ventral face of almost the entire length of the segment; total for both antennae 18–35. Antennal segment IV with (0)1–4 secondary sensoria on each antenna, total for both antennae 1–7. Antennal segment V sometimes (22% of specimens) with 1–2 secondary sensoria. Ultimate rostral segment with 2–3(4) accessory setae, three or four are present in 16 specimens (32.7% of specimens). The veins of the forewings are costal, radial 1, radial sector, media with only two branches [M1+2 and M3] and anterior cubitals 1 and 2; the once-branched media is very unusual in the subfamily. Abdominal dorsum widely membranous with marginal sclerites, which are more extensive than those in aptera, peri-siphuncular sclerites, small setiferous sclerites on abdominal segments 7 and infrequently on segment 6, and an arc-shaped band on segment 8, all of them with spinules. Intersegmental sclerites usually conspicuous, although small and less pigmented than the corresponding marginal ones. The qualitative and meristic characteristics like those of the apterae have been omitted. Metric features in Table 1.

Type material. Holotype, apterous viviparous female (ARG-371-ap.5, on a slide with 3 paratypes), ARGENTINA, Río Negro, Bariloche, San Carlos de Bariloche (41º09’ S, 71º12’ W, 860 m), on Quinchamalium chilense, 19-January-2000, Mier Durante, Nieto Nafría and Ortego leg.; Universidad de León collection (León, Spain).

Paratypes, 124 apterous viviparous females and 49 alate viviparous females: (1) same data as the holotype, 34 apterae and 23 alatae; (2) same locality, host plant and collectors as the holotype, 14-December-2009, 15 apterae and 10 alatae; (3) same locality and host plant as the holotype, 18-April-2012, O. leg., 6 apterae and 8 alatae; (4) same locality and host plant as the holotype, 11-January-2019, O. leg., 12 apterae; (5) Neuquén, Minas, Lagunas Epulafquen (36º52’ S, 70º57’ W, 1440 m), on Q. chilense, 25-January-2000, M.D., N.N. and O. leg.; (6) Neuquén, Los Lagos, Puerto Huemul (41º01’ S, 71º20’ W, 860 m), on Q. chilense, 21-January, 2000; M.D., N.N. and O. leg., 1 alate; (7) Santa Cruz, Lago Argentino, El Chaltén (49º20’ S, 72º53’ W, 750 m), on Arjona ?patagonica, 8-February-2010, Cuesta Segura leg., 14 apterae; and (8) CHILE, Maule, Talca, Paso Pehuenche high slopes (35º59’ S, 70º24’ W, 2520 m) on Q. chilense, 31-January, 2000; M.D., N.N. and O. leg., 24 apterae and 6 alatae.

Apterous viviparous females (Fig. 1). Based on 125 specimens. 1.125–2.125 mm long. When alive neutral green to light green or yellow-green with a very fine layer of waxy powder, with brown antennae and legs. When mounted, light brown or beige because thorax and abdomen are widely membranous, with head, antennae, rostrum, legs and siphunculi brown, and darker than genital and anal plates, cauda and spiracular and dorsal sclerites. Marginal tubercles present in prothorax and abdominal segments 1–(6)7, all of them round, big, low and pale, the abdominal ones sometimes sitting in small sclerites; if these sclerites are not present, the tubercles can go unnoticed because they are as poorly pigmented as the surrounding cuticle. Setae very long, fine and pointed. Head with very few scattered rectilinear ridges. Frons slightly wavy. Ocelli or ocellar spots present on specimens of 5 samples: one in 6.4% of type specimens, two in 4.0%, and three in 6.4%, up to maximum per sample of 33.3%, 8.6% and 14.4%. Antennae six-segmented and longer than half body length. Antennal segments I and II smooth. Antennal flagellum imbricated, although the ventral face on segment III is almost smooth. Antennal segment III with 6–14 setae, and usually with secondary sensoria placed on distal three quarters, 1–8(13) on each antenna and 1–15(26) on both antennae. Rostrum long, reaching back beyond hind coxae. Ultimate rostral segment relatively broad and usually with 2 accessory setae, two specimens have 4 setae (1.6% of type specimens), and 18 specimens have 3 setae (14.4% of type specimens). Tibiae as dark as femora, usually homogeneously pigmented, but in poorly pigmented specimens progressively darkening towards the apex. Tarsal formula 3.3.2. Dorsum of thorax and abdomen in general membranous and tenuously reticulated or smooth; metathorax with a light brown and reticulated spino-pleural patch; abdominal segment 7 sometimes with small and light brown setiferous sclerites; abdominal segment 8 with a narrow arc-shaped sclerite carrying scattered spinules. Spiracular sclerites usually inconspicuous. Siphunculi usually subcylindrical, sometimes tapering, with transverse linear roughness and very marked flange. Genital plate with 2–8(12) discal and (3)6–12 posterior setae. Abdominal segment 8 with (3)4–6(8) setae. Cauda triangular, with (3)5–8 setae. Metric features in Table 1.

Bionomics. Specimens of Aphis prima sp. n. live on Quinchamalium chilense and Arjona sp. (possibly A. patagonica), in loose or disturbed soils. It may also live on other species of these plant genera, perhaps with the exception of A. megapotamica, because this is the only species of the genus that lives outside the Andean territories.

Aphids usually form compact groups on the basal part of the stem, basal leaves, and highest part of the roots; the specimens in very large colonies invade the highest parts of the plant, especially the nymphs of alate viviparae. They are visited by ants.

The life cycle of A. prima sp. n. cannot be specified because no sexuals have been collected. It can be speculated that it is holocyclic due to the climatic characteristics of the collection sites, with cold winters and frequent snowfalls, or on the contrary that it is anoholocyclic because some specimens could subsist on the roots of their host plants during the winter, even under snow, as other aphids do, for example Acyrthosiphon matilei Remaudière & Leclant, 2000 (‍Nieto Nafría & Mier Durante, 2013).

Distribution. Aphis prima sp. n. is known in the Argentine provinces of Neuquén, Río Negro and Santa Cruz and in the Chilean region of Maule, but it can be estimated that this aphid is much more widespread in both countries, and even in Bolivia and Peru, because the altitudes of the collection localities are very diverse (750 to 2500 m) and because there are 1500 km between the northernmost and the southernmost collection localities —Paso Pehuenche in Chile and El Chaltén in Argentina, respectively.

Etymology. The specific name of the new species, prima, is an adjective in nominative feminine singular that means first, because it is the first aphid species collected on species of Schoepfiaceae.

Taxonomic discussion. The characteristics of the studied specimens correspond to those of the subgenus Aphis, including the usual presence of only 2 accessory setae on the ultimate rostral segment (‍García Prieto & Nieto Nafría, 2005), although there is a small quantity of specimens with 3 or 4 accessory setae.

The twice-branched media in the forewings is one of the archetypical characteristics of Aphididae, which remains as such in Aphidinae and Aphidini. The media is only once-branched in some genera of this tribe, for example Schizaphis Börner, 1931 (Aphidini Rhopalosiphina) and Casimira Eastop 1966 (Aphidini Aphidina), and also in three species of Aphis, in addition to Aphis (A.) prima sp. n.; namely A. (Toxoptera) aurantii Boyer de Fonscolombe, 1841 —which is polyphagous and worldwide distributed—, A. (A.) cottieri Carver, 2000 —living on species of Muehlenbeckia (Polygonaceae) in New Zealand—, and A. (A.) elena Lagos-Kutz and Voegtlin, 2017 —living on Pycnanthemum virginianum (Lamiaceae) in the northern United States—. Thus, the once-branched media is not unique to either the subtribe or the genus, but it is extremely rare in the genus and it is not present in any of the species of the genus known in South America, with the exception of A. (T.) aurantii. Aphis prima sp. n. can easily be distinguished from A. cottieri and Aphis elena, because these species lack marginal tubercles on intermediate abdominal segments and have a finger-shaped cauda (‍Carver, 2000; ‍Lagos-Kutz et al., 2017).

The apterous viviparae collected on Arjona (one sample) differ from those collected on Quinchamalium (remaining samples) in some morphological characters (see Table 1, legend). These differences are interpreted as intraspecific variations, which could be related to the latitude of the collection localities or with the species of host plant or with both.

As noted in the introduction, there are two species of Aphis hosted in species of Santalaceae —the family in which the Quinchamalium and Arjona were previously classified— somewhere in the world, specifically on species of Thesium in palaearctic territories. Aphis thesii has been recorded from France, Hungary, Poland and Slovakia and A. neothesii from east Siberia (Russian Federation). Apterous viviparae of both species are very different of those of the new species, because they lack secondary sensoria on antennal segment III and marginal tubercles on intermediate abdominal segments, and they have a finger-like and dark cauda, conspicuously extensive dorso-abdominal sclerotization, and short setae on antennae, legs and body dorsum, and they are when alive dark brown (‍Holman, 1966; ‍Pashchenko, 1993; ‍Osiadacz & Hałaj, 2010, ‍2015).

In Argentina and Chile are known: (‍i) eight species of Aphis whose aptera always or occasionally have secondary sensoria on antennal segment III [six species included in “group 4” of the keys for apterous viviparae of Aphidina known in South America by Nieto Nafría et al. (‍2019), plus A. lugentis Williams, 1911 and A. ortegoi Mier Durante, García Gómez & Nieto Nafría, 2021], and (ii) twenty species without secondary sensoria but always or sometimes with marginal tubercles on the intermediate abdominal segments [16 species included in group 5 of the above-mentioned keys, plus A. conspicua Nieto Nafría & Mier Durante, 2019, A. fuentesi Nieto Nafría & Ortego, 2019, A. gutierreziae Ortego, Mier Durante & Nieto Nafría, 2021 and A. ingeborgae Nieto Nafría & Brown, 2019]. The viviparae of A. prima sp. n. have both secondary sensoria on antennal segment III and marginal tubercles on intermediate abdominal segments, and also a triangular cauda and homogeneously brown tibiae. The viviparae of all of these other species have a finger-shaped cauda; most of them have bicolored tibiae (pale with a dark and contrasted distal portion). Only viviparae of A. lugentis —which also have secondary sensoria on antennal segment III— have homogeneously pigmented tibiae, but these are black or very dark brown.

The presence of secondary sensoria on antennal segment III of apterae, the abundant and big marginal tubercles, the long setae on antennae and legs, and the short cauda are features that A. prima sp. n. shares with Pehuenchaphis agilissima Mier Durante, Nieto Nafría & Ortego, 2003, which lives on the roots of Senecio (‍Mier Durante et al. 2003). However, apterous viviparae of A. prima can easily be separated from those of this last species, in which the siphunculi are very short (at most a little longer than their basal widths) and are placed on abdominal segment 6 (not on segment 5 as usual in Aphidini|), and the antennal setae are much more abundant. The specimens of both species colonize the same part of their respective host plants, are attended by ants and move quickly when disturbed (‍Mier Durante et al., 2003).