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Rhinariaphis – A remarkable new aphid genus from Afghanistan (Hemiptera: Aphididae: Aphidinae)
Zoologischer Anzeiger 277 (2018) 75e84
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Research paper
Rhinariaphis e A remarkable new aphid genus from Afghanistan (Hemiptera: Aphididae: Aphidinae) Mariusz Kanturski a, *, Andrey V. Stekolshchikov b a b
Department of Zoology, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Bankowa 9, 40-004 Katowice, Poland Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, 199034 Russia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 April 2018 Received in revised form 3 September 2018 Accepted 17 September 2018 Available online 12 October 2018
In this paper, we describe a new aphid genus, Rhinariaphis gen. nov., from the tribe Macrosiphini (Aphididae: Aphidinae) with the type species Rhinariaphis tuberculata sp. nov., from specimens that have been collected in Afghanistan, where it is associated with Lophanthus pinetorum (¼Nepeta cabulica) (Lamiaceae). Rhinariaphis is superficially similar to the Hyperomyzus subgenus Neonasonovia due to its characteristically shaped siphunculi, but it is also similar to the genera Eucarazzia and Klimaszewskia because of some of the characters of the ultimate rostral segment. Representatives of this genus can easily be distinguished from other Macrosiphini genera due to the presence of numerous secondary rhinaria on antennal segments III, IV and V as well as by the thick setae on their large tuberculate bases. In addition to the taxonomy of the genus, a scanning electron microscopy (SEM) study was performed and the main morphological characters are presented with detailed descriptions of the antennal and body sensilla. © 2018 Elsevier GmbH. All rights reserved.
Keywords: Aphids Description Macrosphini SEM Sensilla
1. Introduction Macrosiphini Wilson, 1910 of the subfamily Aphidinae (Hemiptera: Aphididae), with 243 described genera (Favret 2018) to date, is the most numerous and diverse aphid tribe (Blackman 2010; Blackman & Eastop 2006; Heie 1994, 1995). Aphids from this tribe are also one of the most controversial tribes within Aphidinae (Choi et al. 2018) most probably due to their unresolved taxonomy and systematics, which could be the result of a large scale speciation in during a rather short time (Heie 1992). Macrosiphini is also a tribe with the largest number of monotypic genera, which have also € recently been described (Zhang et al. 2013; Barjadze & Ozdemir 2014; Stekolshchikov 2014; Kanturski & Wieczorek 2015; Nieto Nafría et al. 2017; Kanturski et al. 2018). The genera of the aphids in this tribe primarily differ in characters such as their head, antennae and features of antennal tubercles features, dorsal surface, sclerotization or chaetotaxy as well as features of the siphunculi, tarsi and cauda (Heie 1992; Blackman 2010). The central, southern and eastern areas of Asia are known as one of the largest and most diverse biodiversity centres in the world
* Corresponding author. E-mail address: [email protected] (M. Kanturski). https://doi.org/10.1016/j.jcz.2018.09.004 0044-5231/© 2018 Elsevier GmbH. All rights reserved.
(Squires 2014; UNEP-WCMC 2016). These parts of the Asian continent are also considered to be a biodiversity centre of aphids, for which many species and genera have been described (Blackman & Eastop 2018). To date, the areas of India, China, Japan and Korea are the best elaborated. The aphid fauna of Central Asia seems to be equally well recognised, but the focus has primarily been in Uzbekistan and Tajikistan. Against this background, the area of Afghanistan, which has about 62 known, described and recorded aphid species, has been insufficiently studied (Narzikulov 1972; Narzikulov & Umarov 1971, 1972a, 1972b). While working in the Aphididae collection in the Natural Hisum national d'Histoire tory Museum in London and in the Muse naturelle in Paris, specimens of an undescribed aphid species that have been collected in Afghanistan were found. The species was listed in the key to aphids on Nepeta as “genus and sp. nr Hyperomyzus (Neonasonovia)” by Blackman & Eastop (2018). Due to its similarities to the Macrosiphini genera Eucarazzia del Guercio and Klimaszewskia Szelegiewicz, a comparison of these three taxa was performed. After a careful examination of these species, we believe € rner, Eucarazzia and that it is not congeneric with Hyperomyzus Bo Klimaszewskia. Moreover, it also does not fit into any known genus in the tribe. Accordingly, we propose a new genus e Rhinariaphis gen. nov. for the new species Rhinariaphis tuberculata sp. nov.
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2. Material and methods 2.1. Specimens examined and abbreviations Specimens used for the comparisons in this study: € rner): POLAND, Hyperomyzus (Neonasonovia) picridis (Bo Bobrowniki Namiarki, 29.06.2006, three apterous viviparous females (3 apt), Picris hieracioides, Ł. Depa leg., DZUS; Wojkowice, 21.06.2007, 3 apt, P. hieracioides, Ł. Depa leg., DZUS. Eucarazzia elegans (Ferrari): FRANCE, Bormes-les-Mimosas, re leg., 25520 25.02.1972, 4 apt, Calamintha acinos, G. Remaudie MNHN; PAKISTAN, Kalam, 16.08.1991, 3 apt (and 3 apt used for the SEM study), Nepeta sp., Nauman leg., 22521 MNHN. Klimaszewskia dracocephali Szelegiewicz: Holotype: MONGOLIA, Narijn Teel, 16.06.1977, 1 apt, Dracocephalum foetidum, S. Klimaszewski leg., APH-4698, PAS; Paratypes: the same data as the holotype, 1 apt, APH-4699, PAS; 1 apt, APH-4700, PAS; 1 apt, APH4701, PAS. Klimaszewskia salviae (Nevsky): IRAN, Lalezar, 26.06.1955, 1 apt, re leg., 22519 MNHN, 1 apt (and 3 apt Salvia lalesarica, G. Remaudie used for the SEM study) 22519 MNHN; TAJIKISTAN: Takov, 23.08.1966, 1 apt, Salvia sp., Umarov leg., 1984-340 BMNH. Data about the examined material of the new genus and species are given in the description section. The specimens were examined using a Nikon Eclipse E600 light microscope with a differential interference contrast (DIC) and photographed with a Nikon DS-Fi camera. Measurements are given in millimetres. The following abbreviations are used: BLdbody length (from the anterior border of the head to the end of the cauda); HWdgreatest head width across the compound eyes; ANTdantennae or their lengths; ANT I, II, III, IV, V, VIdantennal segments I, II, III, IV, V, VI or their lengths (the ratios between the antennal segments are simply given as e.g. ‘VI: III’); LS ANT IIIdlength of the longest setae of ANT III; BD IIIdbasal articular diameter of ANT III; BASEdbasal part of the last antennal segment or its length; PTd the processus terminalis of the last antennal segment or its length; URSdultimate segments of the rostrum (IV þ V) or their length; H FEMdhind femora length; H TIBIdhind tibiae length; HT Idfirst segment of the hind tarsus, HT IIdsecond segment of the hind tarsus or its length, SIPH L e siphunculi length, SIPH W e siphunculi width, GP L e genital plate length, GP Wdgenital plate width; BMNH e Natural History Museum, London (United Kingdom); um national d’Histoire naturelle, Paris (France); MNHN e Muse PAS e Zoological Museum, Polish Academy of Sciences, Warsaw (Poland); DZUS e Hemiptera Collection of the Department of Zoology, University of Silesia in Katowice (Poland); ZIN RAS e Zoological Institute of the Russian Academy of Sciences. The holotype of the new species will be deposited in the BMNH. Paratypes will be deposited in the BMNH, MNHN, DZUS and ZIN RAS. 2.2. Scanning electron microscopy Specimens for the SEM analyses were preserved in 70% ethanol for several days. A method from that by Kanturski et al. (2017) was used to prepare them. The specimens were transferred from the ethanol into a 6% phosphotungstic acid (PTA) solution in 70% ethanol for 24 h. Dehydration was performed by an ethanol series of 80%, 90%, 96% and two changes of absolute ethanol for 30 min each. The dehydrated specimens were dried using a hexamethyldisilazane (HMDS) solution with absolute ethanol in proportions of 1:3, 1:2; 2:3 for 30 min each followed by two changes of
undiluted HMDS. Samples were mounted on aluminium stubs with double-sided adhesive carbon tape and sputter-coated in a Pelco SC-6 sputter coater (Ted Pella Inc., Redding, CA, USA). The specimens were imaged using a Hitachi SU8010 field emission scanning electron microscope (FE-SEM) (Hitachi High-Technologies Corporation, Tokyo, Japan) at 5, 10 and 15 kV accelerating voltages with a secondary electron detector (ESD). 3. Results Rhinariaphis gen. nov. (Figs 1e8; Tables 1 and 2) Type species. Rhinariaphis tuberculata sp. nov., here designated. Diagnosis. The apterous viviparous females that were examined in this study could easily be recognised by their quite evident combination of morphological features such as the presence of numerous secondary rhinaria on ANT III, IV and V, setose URS, large dorsal abdominal wart-like setae bases and clavate siphunculi. It is impossible to find another Macrosiphini genus that could have the same characters to put the new species in. Due to the morphological characteristics and some similarities, Rhinariaphis may be placed near the genera Hyperomyzus (especially the subgenus Neonasonovia Hille Ris Lambers), Eucarazzia and Klimaszewskia representatives. The apterous viviparous females of Rhinariaphis are close to the species of the genera Eucarazzia and Klimaszewskia due to the large number of accessory setae of URS and thick rigid, capitate setae on body and appendages. Although it also shares the type of siphunculi, secondary rhinaria distribution (on ANT III-V) and number of ventral setae on HT I (three) with Eucarrazia and Rhinariaphis, it differs from them due to its less clavate siphunculi (distinctly swollen in the clavate part in Eucarazzia), the dorsal side of abdomen that is covered by large tubercles (dorsum without tubercles in Eucarazzia) and the location of the rhinaria on ANT III, which are distributed on the entire length of the segment (in Eucarazzia, the rhinaria occupy only the distal part of the segment). The new genus differs from Klimaszewskia due to the different number (three) of setae on HT I (five in Klimaszewskia), clavate siphunculi (siphunculi tapering in Klimaszewskia) and secondary rhinaria that distributed on ANT III-V. Moreover, those on ANT III are located on the entire length of the segment (rhinaria only on ANT III, but on the proximal part of the segment in Klimaszewskia) and the dorsal side of the abdomen with large and wide tubercles (tubercles are remarkably small and narrow in Klimaszewskia). The new genus shares the presence of secondary rhinaria (distributed on the entire length of the segment), HT I chaetotaxy and superficially clavate siphunculi with Neonasonovia species. Both genera vary as to the presence of rhinaria on two more antennal segments, despite the fact that in some H. (Neonasonovia) picridis individuals, one accidental rhinarium was found on ANT IV. Moreover, the siphunculi differ in the ratio of the swollen part to the narrow part in both taxa. The new genus differs from Hyperomyzus (Neonasonovia) due to the dorsal side of the abdomen with setae that arise from large and wide wart-like bases, secondary rhinaria on ANT VI and V and better-developed, divergent antennal tubercles (dorsal side of the abdomen smooth, secondary rhinaria only on ANT III, low antennal tubercles). Some small similarities are also visible with two Macrosiphini species Chaetosiphon (Pentatrichopus) tetrarhodum (Walker, 1849) and Capitophorus hippophaes (Walker, 1852) (Heie 1994). The apterous viviparous females of those two species are characterised by secondary rhinaria that are sometimes present on ANT IV and V. In Ch. tetrarhodum, the dorsal tubercles are only present in the spinal position and the SIPH are not swollen. In C. hippophaes, on the other hand, there are only spinal (and double in addition) tubercles and the URS is not strongly hairy.
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Fig. 1. Comparison of the most important characters of Rhinariaphis (a, b, g, j, m, p) with other closely related genera e Eucarazzia (c, d, h, k, n, r) and Klimaszewskia (e, f, i, l, o, s): ventral side of URS (a, c, e); dorsal side of URS (b, d, f); dorsal side of abdomen with large setae bases (g), smooth (h), with small setae bases (i); hind tibiae chaetotaxy (j, k, l); hind tarsi with three ventral setae of HT I and pointed empodial setae (m), hind tarsi with three ventral setae of HT I and pointed empodial setae (n), hind tarsi with five ventral setae of HT I and slightly spatulate empodial setae (o); SIPH clavate (p), wide clavate (r), tubular (s).
The detailed differences between the analysed genera are listed in Table 1. Description (see Table 2). Apterous viviparous females (mounted specimens). Colour. Live: unknown. In mounted specimens: head light brown to brown. ANT brown with paler basal part of ANT III and distal part of ANT VI. Thorax membranous, pale to yellow. Femora of legs pale to yellow with brown patches in the distal part (but the very distal apex lighter), tibiae yellow to light brown with darker distal parts and tarsi. Abdomen membranous pale to yellow. Siphunculi uniformly yellow to light brown or with a paler basal half. Genital plate, cauda and anal plate yellow to light brown (Fig. 3). Structures. Body oval or egg-shaped. Head smooth with well-developed smooth antennal tubercles with divergent inner sides (Fig. 4a). Head chaetotaxy: dorsal side of the head covered by four pairs of long, rigid, thick setae with capitate or fan-shaped apices, 0.030e0.055 mm long. Frons with two setae, ANT tubercles with 2e4 setae. ANT 6 e segmented, longer than the body, with
small, rounded and slightly protuberant secondary rhinaria. ANT III with 15e28 secondary rhinaria (Fig. 4c), ANT IV shorter or longer than ANT V with 9e25 secondary rhinaria (Fig. 4d). ANT V shorter than ANT VI with 4e16 secondary rhinaria (Fig. 4e). Secondary rhinaria distributed on entire length of segments, mostly in one row (Fig. 2a). Primary rhinaria on ANT V and VI with ciliated rings. ANT VI with long PT (Fig. 4f). ANT chaetotaxy: ANT covered by thick and rigid setae with capitate apices. ANT III setae as long as or longer than the width of the segment. ANT I with 7e8, ANT II with 4e5, ANT III with 14e20, ANT IV with 8e12, ANT V with 5e9 setae. ANT VI with 3e4 basal, 3e4 apical and 5e6 setae on the PT. Rostrum reaching mesosternum. URS triangle with numerous accessory setae (Fig. 1a and b). URS with 24e40 fine and pointed accessory setae (Fig. 5a and b). Mesosternal furca fused. H FEM covered by thick, rigid setae with capitate apices or blunt with little expanded apices, 0.020e0.040 mm long. H TIB covered by thick, rigid setae with capitate and pointed (distal part) apices, shorter or longer than the width of tibiae, 0.020e0.060 mm long. Dorsal side
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thick and rigid with capitate apices, 0.025e0.050 mm long on ABD I-VI and 0.030e0.055 mm long on ABD VII-VIII (Fig. 5d and e). ABD VIII with 4e6 setae. SIPH clavate from about half of their length with a well-developed flange with 2e3 rows of polygonal reticulation (Fig. 1p). Cauda tongue-shaped with 6e9 setae (Fig. 4b). Genital plate with two anterior and 10e16 posterior setae (Fig. 5f). Etymology. The name of the new genus Rhinariaphis is female in gender. The name refers to large number of secondary rhinaria on antennal segment III-V, what is very unusual in apterous viviparous females in Macrosiphini. Rhinariaphis tuberculata sp. nov. Apterous viviparous female. (Figs 1-8; Tables 1 and 2) Description. As the description of the genus. 4. Notes on SEM morphology and sensilla 4.1. General morphology
Fig. 2. Comparison of the distribution of secondary rhinaria of ANT III of: (a) entire length of the segment in P. tuberculata, (b) only in the apical part in E. elegans, (c) only on the basal part in K. dracocephali.
Fig. 3. Apterous viviparous female of Rhinariaphis tuberculata gen. nov. et sp. nov. e general view.
of thorax and abdomen with very well-developed wart-like bases of setae in the spinal pleural and marginal positions. Each wart-like base has one rigid seta on the apex (Fig. 1g). Body and appendages covered by capitate setae (Fig. 1j). First segments of tarsi with 3-3-3 ventral setae (Fig. 1m). Abdomen with a pair of spinal wart-like bases on ABD I-VII, pair of pleural wart-like bases on ABD I-IV and a pair of marginal wart-like bases on ABD I-VI. Dorsal setae
The head is separated from the pronotum, which is separated from the rest of thorax. The meso- and metanotum are fused together and fused with ABD I-VII. The pronotum has two (one pair) of small and low spinal projections that lie horizontally and two pairs of larger marginal ones that lie vertically. The same arrangement of projections is visible on the mesonotum, but the spinal bases are larger and similar to the other ones on the body. The metanotum has three pairs of projections e spinal, pleural and marginal ones. The abdomen is characterised by paired spinal wartlike bases of dorsal setae on ABD I-VII, pleural bases on ABD I-IV and marginal ones on ABD V-VI. On ABD V-VII in the pleural area, small, sometimes slightly raised sclerites were observed. The wart-like bases have one or rarely two thick and rigid trichoid sensilla, which are also present in the pleural and marginal areas but without projections. ABD VIII in the form of a solid sclerite is separate from the other abdominal tergites (Fig. 6). On the dorsal side of the head, thick, rigid and clearly capitate trichoid sensilla are visible and can be divided into three groups e frontal, on ANT tubercles and on the vertex. The trichoid sensilla of the posterior part of the head are situated on low but visible sclerites (Fig. 7a). Dorsal thoracic and abdominal projections are cone shaped with one thick and rigid trichoid sensillum on the very apex, but some tubercles may also have an additional sensillum near the basal part of the tubercle. The surface of the dorsal tubercles is smooth, but the cuticle between them are clearly pleated in the form of transverse stripes or a polygonal reticulation (Fig. 7b). The dorsal trichoid sensilla are characterised by raised, cone-shaped sockets, which are smooth and distinctly capitate (Fig. 7c). The SIPH are clavate, distinctly swollen from about half of their length with a smooth surface and a well-developed flange. The cauda is slightly tapered near the base (Figs. 3 and 7d). The anal plate is in the form of a semi-circular sclerite, which the genital plate is quite large with a solid sclerite with only few setae (Fig. 7e and f). 4.2. Antennal sensilla The antennal segments have seven kinds of sensilla. The small multiporous placoid sensilla (secondary rhinaria) on ANT III-V are the most clearly seen as one or two rows on the entire length of each segment (Fig. 8aec). The apical parts of ANT V and BASE of ANT VI also have a clearly visible large multiporous placoid sensillum and a group of placoid and coeloconic sensilla (Fig. 8c and d). The large multiporous the placoid sensillum on ANT V (primary rhinarium) is rounded, situated in a deep cavity inside the segment and is surrounded by a very well-developed sclerotic ring with
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Fig. 4. Rhinariaphis tuberculata characters: (a) head, (b) end of the abdomen, (c) ANT III, (d) ANT IV, (e) ANT V, (f) ANT VI, arrows show the primary rhinaria.
Fig. 5. Rhinariaphis tuberculata characters: (a) ventral side of URS, (b) dorsal side of URS, (c) distal part of the hind tibiae and hind tarsus, (d) surface of the dorsal side of the abdomen, (e) abdominal chaetotaxy, (f) genital plate.
20e25 medium and long, irregular projections with very short ones between them (Fig. 8e). The primary rhinaria on the apical part of the ANT VI base are tightly attached to each other, lie deep in cavities inside the segment and are also surrounded by sclerotic rings with numerous projections of the same shape and length as those on ANT V. The large multiporous sensillum (major rhinarium) is the largest, rounded and flat. Small multiporous placoid sensilla
are situated very close to the large placoid multiporous sensillum and more or less visible. Four sunken coeloconic sensilla represent the external group of sensilla; three of them lie very close to the small multiporous sensilla and the very apical one is neighbours with the large multiporous placoid sensillum (Fig. 8f). Small multiporous placoid sensilla and sunken coeloconic sensilla are the accessory rhinaria. On the ventral side of the pedicel, one
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Fig. 6. SEM of apterous viviparous female of Rhinariaphis tuberculata dorsal side of body.
rhinariolum was observed. The rhinariolum is similar to the sunken coeloconic sensilla on ANT VI in the shape of the projection but differs in the round and very smooth edges of the cavity (Fig. 8g and h). All of the antennal segments also have two kinds of trichoid
sensilla. ANT I-ANT VI BASE are covered by type-I trichoid sensilla. These are thick, rigid and with distinctly capitate apices. The sockets of these sensilla are in the form of a truncate cone or are trapezoidal (Fig. 8i, j, k). ANT VI PT is characterised by the presence of short, rigid and slightly pointed type-III trichoid sensilla. The sockets of these sensilla are also in the form of a truncate cone (Fig. 8l and m). The small placoid sensilla on ANT III-V are rounded, different in size, slightly protuberant and lie in cavities that are surrounded by rings of smooth edges (Fig. 8n and o). Diagnosis. As the generic diagnosis. Etymology. The authors followed the original naming given by D. Hille Ris Lambers on the slides of the new species as the apterous viviparous females are characterised by the dorsal side of thorax and abdomen with many large wart-like setae bases. Distribution and biology. To date, the genus and species are only known from Afghanistan where it is associated with Lophanthus spp. Material examined: Holotype e AFGHANISTAN, Paghman, 06.06.1975, Lophanthus pinetorum (¼Nepeta cabulica), one apterous viviparous female (1 apt), marked as 1 and H, van den Bosh leg., BM1984-340 (1) e present marking, BMNH. Paratypes: the same place and date as the holotype, 1 apt marked as 2, BM1984-340 (1) e present marking, BMNH; 2 apt, BM1984-340 (2), BMNH; 2 apt, BM1984-340 (3), BMNH; 2 apt, BM1984-340 (4), BMNH; 2 apt, BM1984-340 (5), ZIN RAS; 2 apt, BM1984-340 (6), DZUS; 1 apt, 2 larvae, BM1984-340 (7), BMNH; 2
Fig. 7. SEM of general morphological characters of Rhinariaphis tuberculata: (a) head, (b) surface of the dorsal side of the abdomen, (c) fine structure of the abdominal trichoid sensillum, (d) dorsal side of the end of the abdomen, (e) lateral side of the end of the abdomen, (f) genital plate.
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Fig. 8. SEM of antennal sensilla of Rhinariaphis tuberculata: (a) ANT III with secondary rhinaria, (b) ANT IV with secondary rhinaria, (c) ANT V with primary rhinarium on the apical part and secondary rhinaria, (d) ANT VI BASE with primary rhinaria, (e) fine structure of the primary rhinarium on ANT V, (f) fine structure of the primary rhinaria on ANT VI BASE, (g) pedicel with a rhinariolum and type-I trichoid sensillum, (h) fine structure of the rhinariolum, (i) type-I trichoid sensilla and small multiporous placoid sensilla on ANT III, (j, k) fine structure of the type-I trichoid sensilla, (l, m) fine structure of the type-III trichoid sensilla of ANT VI PT, (n, o) fine structure of the small multiporous placoid sensilla on ANT III-V.
apt, BM1984-340 (9), BMNH; Charikar, 21.05.1975, 2 apt, L. pinetorum (¼N. cabulica), van den Bosh leg., BM1984-340 (8) e present e, G. marking, BMNH; Kotal Kheder, 17.05.1959, 1 apt, Labie re leg., 22522, MNHN; 1 apt, 22523, MNHN; 1 apt, 22524, Remaudie MNHN; 1 apt, 22525, MNHN; 1 apt, 22526, MNHN; 2 apt, 22527, MNHN; 1 apt, 22528, MNHN; 1 apt, 22529, MNHN; 1 apt, 22530, MNHN; 1 apt, 22531, MNHN; 1 apt, 22532, MNHN; 1 apt, 22533, MNHN; 1 apt, 22534, MNHN; 1 apt, 22535, MNHN; 2 apt, 22536, MNHN; 1 apt, 22537, MNHN; 2 apt, 22538, MNHN; 2 apt, 22539, MNHN; 4 apt, 22540, MNHN; 2 apt, 22541, MNHN1 (3 apt used for the SEM study).
5. Taxonomical comments Blackman and Eatop's (2018) key to aphids on Nepeta (including Lophanthus). The new species is inserted into couplet 10 in their key:
9. SIPH markedly clavate. Secondary rhinaria usually present on ANT IV (eV) as well as III … 10. - SIPH tapering. Secondary rhinaria absent, or only on ANT III … 11. 10. Cauda not longer than its basal width. Rhinaria mainly on distal part of ANT III and on IV. Dorsal abdominal hairs not arising from projections … Eucarazzia elegans. - Cauda c.2 its basal width. Rhinaria evenly distributed over ANT III, IV and V. Dorsal abdominal hairs arising from large wartlike bases … . Rhinariaphis tuberculata. 11. ANT tubercles well developed, divergent. R IV with 16e24 accessory hairs. Marginal tubercles (MTu) present on ABD TERG 2e5, but not on 1 and 7. ANT III with 3e12 secondary rhinaria … Klimaszewskia altaica. - ANT tubercles weakly developed. R IV usually with 2 accessory hairs. ABD TERG 1 and 7 with MTu. ANT III usually without rhinaria … 12.
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Table 1 Comparison of the apterous viviparous females of the most similar genera: Rhinariaphis, Hyperomyzus (Neonasonvia), Eucarazzia and Klimaszewskia. Character
Rhinariaphis
Hyperomyzus (Neonasonovia)
Eucarazzia
Klimaszewskia
ANT III rhinaria
Present. Mostly in one row on the entire length of the segment Present. Mostly in one row on the entire surface of the segment Present. Mostly in one row on the entire surface of the segment 24e40 Not larger than the abdominal stigmal pores 3-3-3 Hairlike Clavate. The narrower basal part clearly longer than the swollen part and narrower than half of the swollen part. Surface always smooth.
Present. In 1e3 rows on the entire length of the segment Absent or present (a few in one row
Present. In one row on the distal part of the segment Present. In one row on the distal part of the segment.
Present. In 2e3 rows on the proximal part of the segment Absent
Absent
Absent
Absent
10e12 Larger than the abdominal stigmal pores 3-3-3 Hairlike Clavate. The narrower basal part clearly shorter than half of the length of the swollen part and as wide as or wider than half of the swollen part. If without any of these combinations of characters, then the SIPH almost tubular and imbricated Tongue-shaped, more or less constricted in the middle of the length. If not constricted then the SIPH almost tubular. Short and rigid. Apices slightly wider (narrow capitate) with a wrinkled or ragged surface. In some species, setae blunt. Low Smooth, without tubercles
20e22 Not larger than the abdominal stigmal pores 3-3-3 Hairlike Remarkably clavate. The narrower part slightly shorter than the strongly swollen part and evidently narrower than half of the swollen part
16e42 Not larger than the abdominal stigmal pores 5-5-5 Slightly spatulate Tubular, tapering with distinct imbrication
Triangle, shorter that its basal width
Tongue-shaped, not constricted. Longer than its basal width
Long, thick and rigid with narrow capitate apices
Long, thick and rigid with narrow capitate apices
Low Smooth, without tubercles
Well developed, divergent Wrinkled, with low tubercles, narrow at the bases
ANT IV rhinaria
ANT V rhinaria
URS accessory setae Thoracic stigmal pores HT I ventral setae Parempodia Siphunculi
Cauda
Tongue-shaped, not constricted. Longer than its basal width
Appendages setae
Long, thick and rigid with wide capitate apices
ANT tubercles Abdominal dorsum
Well developed, divergent Wrinkled with large tubercles, wide at the bases
Table 2 Measurements and ratios values of apterous viviparous females of Rhinariaphis tuberculata gen. nov. et sp. nov. Character
Apterous viviparous female
BL HW ANT ANT III ANT IV ANT V ANT VI BASE PT URS H FEM H TIB HT I HT II SIPH L SIPH W GP L GP W CAUDA L CAUDA W HW:ANT ANT:BL PT:BASE ANT VI:ANT III ANT V:ANT III ANT IV:ANT III LSIII:BDIII URS:ANT III URS:ANT VI URS:BASE URS:HT II HT II:ANT III HT II:ANT VI HT II:BASE SIPH:CAUDA SIPH:BL CAUDA L:CAUDA W
1.85e2.82 0.44e0.54 2.05e2.98 0.48e0.69 0.37e0.59 0.33e0.56 0.68e0.95 0.13e0.17 0.55e0.78 0.12e0.14 0.67e1.02 1.20e1.95 0.03e0.04 0.08e0.11 0.37e0.49 0.07e0.11 0.14e0.22 0.24e0.31 0.23e0.30 0.10e0.15 0.18e0.21 1.05e1.18 4.14e4.48 1.14e1.41 0.61e0.82 0.64e0.85 1.09e1.28 0.18e0.26 0.13e0.18 0.76e0.96 1.09e1.66 0.12e0.19 0.11e0.14 0.57-0-78 1.51e1.84 0.16e0.20 1.85e2-30
Although the establishment of yet another mono-specific genus of Macrosiphini may be disappointing for some of aphidologists, after a deeper examination of the monotypic genera in other groups of aphids, the number of those in Macrosiphini is not excessively large. According to Blackman & Eastop (2018) and Favret (2018), of the approximately 241 valid genera, 90 are known to be monotypic and 27% of all of them belong to the Macrosiphini genera. On the other hand, in Aphidini monotypic genera, they constitute only 16% of the 82 described genera. The percentage of monotypic genera in Macrosiphini seems to be on a normal level compared to other aphid groups such as, e.g. Panaphidini (29%), Fordini (28%), Pemphigini (40%) or Nipponaphidini (29%). Moreover, when the subfamily level is compared, the share of monotypic genera to all known genera is similar and only varies at a level of 20e30% (Fig. 9). Going a little deeper in the analysis of the origin and occurrence of monotypic Macrosiphines, 50% of the known genera are described from different parts of Asia, which has one of the highest numbers of biodiversity centres (Central Asia, China, India Himalaya and Japan) (Fig. 10). Taking into account the sometimes very diverse, vast or mountainous areas of many Asiatic countries, the level of diversity of the monotypic genera may be still be unrecognised. Some recent aphid studies have shown that there are situations in which new species are described in the monotypic genera such as the Macrosiphini genus Aphthargelia Hottes, where a second species has been described 55 years after the genus was established (Jensen 2013). Moreover, in Kaochiaoja Tao, 1963, a new species from India was described last year (Joshi & Blackman 2017). In the Chaitophorinae monotypic Yamatochaitophorus Higuchi, a second species was described from China (Jiang et al. 2016). Considering that the aphid fauna of Afghanistan is only known to a very basic degree and taking into account the alpine and diverse character of most of the Afghan area, we expect more species of Rhinariaphis to be discovered. In addition, the collection
M. Kanturski, A.V. Stekolshchikov / Zoologischer Anzeiger 277 (2018) 75e84
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Fig. 9. Share of monotypic genera within Aphididae subfamilies.
References
Fig. 10. Analysis of the monotypic Macrosipini genera in those described here and those occurring in different continents.
of fresh live specimens of P. tuberculata will provided the opportunity to perform molecular analyses in order to determine its position and relationships with other Macrosiphini species.
Acknowledgements We are sincerely grateful to Paul A. Brown (Natural History Museum, London, UK), Dr. Daniele Matile-Ferrero, Dr. Adeline Soulier-Perkins, Prof. Thierry Bourgoin and the late Prof. George re (Muse um National d'Histoire Naturelle, Paris, France) Remaudie for their kind help and support during the internships in the collections as well as for the loan of the many slides of Macrosiphini. We would like to thank the Editor and two anonymous Reviewers for all comments and suggestions that improved the first version of the manuscript. Mariusz Kanturski gratefully acknowledges the Scholarship for Outstanding Young Scientists from the Ministry of Science and Higher Education of Poland (1165/E-340/STYP/12/17).
€ Barjadze, S., Ozdemir, I., 2014. A new genus of Macrosiphini Wilson, 1910 (1887) (Hemiptera: Aphididae) from Rhododendron in Turkey. Zootaxa 3835 (1), 121e126. Blackman, R.L., 2010. Aphids e Aphidinae (Macrosiphini). Handb. Identif. Br. Insects 2 (7), 413. þ CD. Blackman, R.L., Eastop, V.F., 2006. Aphids on the World's Herbaceous Plants and Shrubs, vol. 2. Wiley, Chichester, p. 1439. Blackman, R.L., Eastop, V.F., 2018. Aphids on the World's Plants: an Identification and Information Guide [cited 06 Jan 2018]. Available from: http://www. aphidsonworldsplants.info/. Choi, H., Shin, S., Jung, S., Clarke, D.J., Lee, S., 2018. Molecular phylogeny of Macrosiphini (Hemiptera: Aphididae): an evolutionary hypothesis for the Pterocomma-group habitat adaptation. Mol. Phylogenet. Evol. 121, 12e22. Favret, C., 2018. Aphid Species File. Version 5.0/5.0. [02.07.2018]. http://Aphid. SpeciesFile.org. Heie, O.E., 1992. The Aphidoidea of Fennoscandia and Denmark IV. Aphidinae. Part 1 of Macrosiphini, vol. 25. Fauna entomologica scand, p. 188. Heie, O.E., 1994. The Aphidoidea of Fennoscandia and Denmark V. Aphidinae. Part 2 of Macrosiphini, vol. 28. Fauna entomologica scand, p. 242. Heie, O.E., 1995. The Aphidoidea of Fennoscandia and Denmark VI. Aphidinae. Part 3 of Macrosiphini and Lachnidae, vol. 31. Fauna entomologica scand, p. 222. Jensen, A.S., 2013. The aphid genus Aphthargelia Hottes (Hemiptera: Aphididae), with one new species. Zootaxa 3701 (3), 381e392. Jiang, L.-Y., Chen, J., Qiao, G.-X., 2016. Yamatochaitophorus yichunensis, a new species of aphid (Aphididae: Chaitophorinae) from northeast China. ZooKeys 612, 41e49. Joshi, S., Blackman, R.L., 2017. A new bamboo-feeding species of Kaochiaoja Tao (Hemiptera: Aphididae) from India. Zootaxa 4363 (4), 569e575. Kanturski, M., Wieczorek, K., 2015. Blackmania gen. nov. and the related genus Acaudella (Hemiptera: Aphididae: Aphidinae). Entomol. Sci 18, 442e451. Kanturski, M., Akbar, S.A., Favret, C., 2017. Morphology and sensilla of the enigmatic Bhutan pine aphid Pseudessigella brachychaeta Hille Ris Lambers (Hemiptera: Aphididae) e a SEM study. Zool. Anz. 266, 1e13. Kanturski, M., Barjadze, S., Jensen, A., Wieczorek, K., 2018. A comparative morphological revision of the aphid genus Myzaphis van der Goot, 1913 (Insecta: Hemiptera: Aphididae) revealed a new genus and three new species. PloS One 13 (3), e0193775. Narzikulov, M.N., 1972. New species of aphids of the Macrosiphini group from Afghanistan. Dokl. Akad. Nauk. Tadzh. SSR 15, 65e67 (in Russian). Narzikulov, M.N., Umarov, Sh.A., 1971. Contribution to the aphid fauna (Homoptera, Aphidinae) of Afghanistan. Part I. Izvyes. Akad. Nauk Tadzh. SSR 4 (45), 94e99 (in Russian). Narzikulov, M.N., Umarov, Sh.A., 1972a. New species of aphids of the genus Brachyunguis from Afghanistan. Dokl. Akad. Nauk. Tadzh. SSR 15, 62e65 (in Russian). Narzikulov, M.N., Umarov, Sh.A., 1972b. Contribution to the aphid fauna (Homoptera, Aphidinae) of Afghanistan. Part I. Izvyes. Akad. Nauk. Tadzh. SSR 1 (46), 36e40 (in Russian).
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pez Ciruelos, S.I., 2017. Delfinoia, a new Nieto Nafría, J.M., Mier Durante, M.P., Lo South American aphid genus (Hemiptera, Aphididae, Macrosiphini) on cayaponia (cucurbitaceae). ZooKeys 671, 49e60. Squires, D., 2014. Biodiversity conservation in Asia. Asia Pac. Policy Stud. 1 (1), 144e159. Stekolshchikov, A.V., 2014. Miyazakia, a new aphid genus from Japan (Hemiptera: Aphididae: Macrosiphini). Zootaxa 3861 (6), 575e584.
UNEP-WCMC, 2016. The State of Biodiversity in Asia and the Pacific: a Mid-term Review of Progress towards the Aichi Biodiversity Targets. UNEP-WCMC, Cambridge, UK. Zhang, B., Lou, Y.-M., Qiao, G.-X., 2013. A new genus and species of Macrosiphini (Hemiptera, Aphididae) from China, living on Isodon eriocalyx. ZooKeys 359, 1e12.
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Research paper
Rhinariaphis e A remarkable new aphid genus from Afghanistan (Hemiptera: Aphididae: Aphidinae) Mariusz Kanturski a, *, Andrey V. Stekolshchikov b a b
Department of Zoology, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Bankowa 9, 40-004 Katowice, Poland Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, 199034 Russia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 April 2018 Received in revised form 3 September 2018 Accepted 17 September 2018 Available online 12 October 2018
In this paper, we describe a new aphid genus, Rhinariaphis gen. nov., from the tribe Macrosiphini (Aphididae: Aphidinae) with the type species Rhinariaphis tuberculata sp. nov., from specimens that have been collected in Afghanistan, where it is associated with Lophanthus pinetorum (¼Nepeta cabulica) (Lamiaceae). Rhinariaphis is superficially similar to the Hyperomyzus subgenus Neonasonovia due to its characteristically shaped siphunculi, but it is also similar to the genera Eucarazzia and Klimaszewskia because of some of the characters of the ultimate rostral segment. Representatives of this genus can easily be distinguished from other Macrosiphini genera due to the presence of numerous secondary rhinaria on antennal segments III, IV and V as well as by the thick setae on their large tuberculate bases. In addition to the taxonomy of the genus, a scanning electron microscopy (SEM) study was performed and the main morphological characters are presented with detailed descriptions of the antennal and body sensilla. © 2018 Elsevier GmbH. All rights reserved.
Keywords: Aphids Description Macrosphini SEM Sensilla
1. Introduction Macrosiphini Wilson, 1910 of the subfamily Aphidinae (Hemiptera: Aphididae), with 243 described genera (Favret 2018) to date, is the most numerous and diverse aphid tribe (Blackman 2010; Blackman & Eastop 2006; Heie 1994, 1995). Aphids from this tribe are also one of the most controversial tribes within Aphidinae (Choi et al. 2018) most probably due to their unresolved taxonomy and systematics, which could be the result of a large scale speciation in during a rather short time (Heie 1992). Macrosiphini is also a tribe with the largest number of monotypic genera, which have also € recently been described (Zhang et al. 2013; Barjadze & Ozdemir 2014; Stekolshchikov 2014; Kanturski & Wieczorek 2015; Nieto Nafría et al. 2017; Kanturski et al. 2018). The genera of the aphids in this tribe primarily differ in characters such as their head, antennae and features of antennal tubercles features, dorsal surface, sclerotization or chaetotaxy as well as features of the siphunculi, tarsi and cauda (Heie 1992; Blackman 2010). The central, southern and eastern areas of Asia are known as one of the largest and most diverse biodiversity centres in the world
* Corresponding author. E-mail address: [email protected] (M. Kanturski). https://doi.org/10.1016/j.jcz.2018.09.004 0044-5231/© 2018 Elsevier GmbH. All rights reserved.
(Squires 2014; UNEP-WCMC 2016). These parts of the Asian continent are also considered to be a biodiversity centre of aphids, for which many species and genera have been described (Blackman & Eastop 2018). To date, the areas of India, China, Japan and Korea are the best elaborated. The aphid fauna of Central Asia seems to be equally well recognised, but the focus has primarily been in Uzbekistan and Tajikistan. Against this background, the area of Afghanistan, which has about 62 known, described and recorded aphid species, has been insufficiently studied (Narzikulov 1972; Narzikulov & Umarov 1971, 1972a, 1972b). While working in the Aphididae collection in the Natural Hisum national d'Histoire tory Museum in London and in the Muse naturelle in Paris, specimens of an undescribed aphid species that have been collected in Afghanistan were found. The species was listed in the key to aphids on Nepeta as “genus and sp. nr Hyperomyzus (Neonasonovia)” by Blackman & Eastop (2018). Due to its similarities to the Macrosiphini genera Eucarazzia del Guercio and Klimaszewskia Szelegiewicz, a comparison of these three taxa was performed. After a careful examination of these species, we believe € rner, Eucarazzia and that it is not congeneric with Hyperomyzus Bo Klimaszewskia. Moreover, it also does not fit into any known genus in the tribe. Accordingly, we propose a new genus e Rhinariaphis gen. nov. for the new species Rhinariaphis tuberculata sp. nov.
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2. Material and methods 2.1. Specimens examined and abbreviations Specimens used for the comparisons in this study: € rner): POLAND, Hyperomyzus (Neonasonovia) picridis (Bo Bobrowniki Namiarki, 29.06.2006, three apterous viviparous females (3 apt), Picris hieracioides, Ł. Depa leg., DZUS; Wojkowice, 21.06.2007, 3 apt, P. hieracioides, Ł. Depa leg., DZUS. Eucarazzia elegans (Ferrari): FRANCE, Bormes-les-Mimosas, re leg., 25520 25.02.1972, 4 apt, Calamintha acinos, G. Remaudie MNHN; PAKISTAN, Kalam, 16.08.1991, 3 apt (and 3 apt used for the SEM study), Nepeta sp., Nauman leg., 22521 MNHN. Klimaszewskia dracocephali Szelegiewicz: Holotype: MONGOLIA, Narijn Teel, 16.06.1977, 1 apt, Dracocephalum foetidum, S. Klimaszewski leg., APH-4698, PAS; Paratypes: the same data as the holotype, 1 apt, APH-4699, PAS; 1 apt, APH-4700, PAS; 1 apt, APH4701, PAS. Klimaszewskia salviae (Nevsky): IRAN, Lalezar, 26.06.1955, 1 apt, re leg., 22519 MNHN, 1 apt (and 3 apt Salvia lalesarica, G. Remaudie used for the SEM study) 22519 MNHN; TAJIKISTAN: Takov, 23.08.1966, 1 apt, Salvia sp., Umarov leg., 1984-340 BMNH. Data about the examined material of the new genus and species are given in the description section. The specimens were examined using a Nikon Eclipse E600 light microscope with a differential interference contrast (DIC) and photographed with a Nikon DS-Fi camera. Measurements are given in millimetres. The following abbreviations are used: BLdbody length (from the anterior border of the head to the end of the cauda); HWdgreatest head width across the compound eyes; ANTdantennae or their lengths; ANT I, II, III, IV, V, VIdantennal segments I, II, III, IV, V, VI or their lengths (the ratios between the antennal segments are simply given as e.g. ‘VI: III’); LS ANT IIIdlength of the longest setae of ANT III; BD IIIdbasal articular diameter of ANT III; BASEdbasal part of the last antennal segment or its length; PTd the processus terminalis of the last antennal segment or its length; URSdultimate segments of the rostrum (IV þ V) or their length; H FEMdhind femora length; H TIBIdhind tibiae length; HT Idfirst segment of the hind tarsus, HT IIdsecond segment of the hind tarsus or its length, SIPH L e siphunculi length, SIPH W e siphunculi width, GP L e genital plate length, GP Wdgenital plate width; BMNH e Natural History Museum, London (United Kingdom); um national d’Histoire naturelle, Paris (France); MNHN e Muse PAS e Zoological Museum, Polish Academy of Sciences, Warsaw (Poland); DZUS e Hemiptera Collection of the Department of Zoology, University of Silesia in Katowice (Poland); ZIN RAS e Zoological Institute of the Russian Academy of Sciences. The holotype of the new species will be deposited in the BMNH. Paratypes will be deposited in the BMNH, MNHN, DZUS and ZIN RAS. 2.2. Scanning electron microscopy Specimens for the SEM analyses were preserved in 70% ethanol for several days. A method from that by Kanturski et al. (2017) was used to prepare them. The specimens were transferred from the ethanol into a 6% phosphotungstic acid (PTA) solution in 70% ethanol for 24 h. Dehydration was performed by an ethanol series of 80%, 90%, 96% and two changes of absolute ethanol for 30 min each. The dehydrated specimens were dried using a hexamethyldisilazane (HMDS) solution with absolute ethanol in proportions of 1:3, 1:2; 2:3 for 30 min each followed by two changes of
undiluted HMDS. Samples were mounted on aluminium stubs with double-sided adhesive carbon tape and sputter-coated in a Pelco SC-6 sputter coater (Ted Pella Inc., Redding, CA, USA). The specimens were imaged using a Hitachi SU8010 field emission scanning electron microscope (FE-SEM) (Hitachi High-Technologies Corporation, Tokyo, Japan) at 5, 10 and 15 kV accelerating voltages with a secondary electron detector (ESD). 3. Results Rhinariaphis gen. nov. (Figs 1e8; Tables 1 and 2) Type species. Rhinariaphis tuberculata sp. nov., here designated. Diagnosis. The apterous viviparous females that were examined in this study could easily be recognised by their quite evident combination of morphological features such as the presence of numerous secondary rhinaria on ANT III, IV and V, setose URS, large dorsal abdominal wart-like setae bases and clavate siphunculi. It is impossible to find another Macrosiphini genus that could have the same characters to put the new species in. Due to the morphological characteristics and some similarities, Rhinariaphis may be placed near the genera Hyperomyzus (especially the subgenus Neonasonovia Hille Ris Lambers), Eucarazzia and Klimaszewskia representatives. The apterous viviparous females of Rhinariaphis are close to the species of the genera Eucarazzia and Klimaszewskia due to the large number of accessory setae of URS and thick rigid, capitate setae on body and appendages. Although it also shares the type of siphunculi, secondary rhinaria distribution (on ANT III-V) and number of ventral setae on HT I (three) with Eucarrazia and Rhinariaphis, it differs from them due to its less clavate siphunculi (distinctly swollen in the clavate part in Eucarazzia), the dorsal side of abdomen that is covered by large tubercles (dorsum without tubercles in Eucarazzia) and the location of the rhinaria on ANT III, which are distributed on the entire length of the segment (in Eucarazzia, the rhinaria occupy only the distal part of the segment). The new genus differs from Klimaszewskia due to the different number (three) of setae on HT I (five in Klimaszewskia), clavate siphunculi (siphunculi tapering in Klimaszewskia) and secondary rhinaria that distributed on ANT III-V. Moreover, those on ANT III are located on the entire length of the segment (rhinaria only on ANT III, but on the proximal part of the segment in Klimaszewskia) and the dorsal side of the abdomen with large and wide tubercles (tubercles are remarkably small and narrow in Klimaszewskia). The new genus shares the presence of secondary rhinaria (distributed on the entire length of the segment), HT I chaetotaxy and superficially clavate siphunculi with Neonasonovia species. Both genera vary as to the presence of rhinaria on two more antennal segments, despite the fact that in some H. (Neonasonovia) picridis individuals, one accidental rhinarium was found on ANT IV. Moreover, the siphunculi differ in the ratio of the swollen part to the narrow part in both taxa. The new genus differs from Hyperomyzus (Neonasonovia) due to the dorsal side of the abdomen with setae that arise from large and wide wart-like bases, secondary rhinaria on ANT VI and V and better-developed, divergent antennal tubercles (dorsal side of the abdomen smooth, secondary rhinaria only on ANT III, low antennal tubercles). Some small similarities are also visible with two Macrosiphini species Chaetosiphon (Pentatrichopus) tetrarhodum (Walker, 1849) and Capitophorus hippophaes (Walker, 1852) (Heie 1994). The apterous viviparous females of those two species are characterised by secondary rhinaria that are sometimes present on ANT IV and V. In Ch. tetrarhodum, the dorsal tubercles are only present in the spinal position and the SIPH are not swollen. In C. hippophaes, on the other hand, there are only spinal (and double in addition) tubercles and the URS is not strongly hairy.
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Fig. 1. Comparison of the most important characters of Rhinariaphis (a, b, g, j, m, p) with other closely related genera e Eucarazzia (c, d, h, k, n, r) and Klimaszewskia (e, f, i, l, o, s): ventral side of URS (a, c, e); dorsal side of URS (b, d, f); dorsal side of abdomen with large setae bases (g), smooth (h), with small setae bases (i); hind tibiae chaetotaxy (j, k, l); hind tarsi with three ventral setae of HT I and pointed empodial setae (m), hind tarsi with three ventral setae of HT I and pointed empodial setae (n), hind tarsi with five ventral setae of HT I and slightly spatulate empodial setae (o); SIPH clavate (p), wide clavate (r), tubular (s).
The detailed differences between the analysed genera are listed in Table 1. Description (see Table 2). Apterous viviparous females (mounted specimens). Colour. Live: unknown. In mounted specimens: head light brown to brown. ANT brown with paler basal part of ANT III and distal part of ANT VI. Thorax membranous, pale to yellow. Femora of legs pale to yellow with brown patches in the distal part (but the very distal apex lighter), tibiae yellow to light brown with darker distal parts and tarsi. Abdomen membranous pale to yellow. Siphunculi uniformly yellow to light brown or with a paler basal half. Genital plate, cauda and anal plate yellow to light brown (Fig. 3). Structures. Body oval or egg-shaped. Head smooth with well-developed smooth antennal tubercles with divergent inner sides (Fig. 4a). Head chaetotaxy: dorsal side of the head covered by four pairs of long, rigid, thick setae with capitate or fan-shaped apices, 0.030e0.055 mm long. Frons with two setae, ANT tubercles with 2e4 setae. ANT 6 e segmented, longer than the body, with
small, rounded and slightly protuberant secondary rhinaria. ANT III with 15e28 secondary rhinaria (Fig. 4c), ANT IV shorter or longer than ANT V with 9e25 secondary rhinaria (Fig. 4d). ANT V shorter than ANT VI with 4e16 secondary rhinaria (Fig. 4e). Secondary rhinaria distributed on entire length of segments, mostly in one row (Fig. 2a). Primary rhinaria on ANT V and VI with ciliated rings. ANT VI with long PT (Fig. 4f). ANT chaetotaxy: ANT covered by thick and rigid setae with capitate apices. ANT III setae as long as or longer than the width of the segment. ANT I with 7e8, ANT II with 4e5, ANT III with 14e20, ANT IV with 8e12, ANT V with 5e9 setae. ANT VI with 3e4 basal, 3e4 apical and 5e6 setae on the PT. Rostrum reaching mesosternum. URS triangle with numerous accessory setae (Fig. 1a and b). URS with 24e40 fine and pointed accessory setae (Fig. 5a and b). Mesosternal furca fused. H FEM covered by thick, rigid setae with capitate apices or blunt with little expanded apices, 0.020e0.040 mm long. H TIB covered by thick, rigid setae with capitate and pointed (distal part) apices, shorter or longer than the width of tibiae, 0.020e0.060 mm long. Dorsal side
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thick and rigid with capitate apices, 0.025e0.050 mm long on ABD I-VI and 0.030e0.055 mm long on ABD VII-VIII (Fig. 5d and e). ABD VIII with 4e6 setae. SIPH clavate from about half of their length with a well-developed flange with 2e3 rows of polygonal reticulation (Fig. 1p). Cauda tongue-shaped with 6e9 setae (Fig. 4b). Genital plate with two anterior and 10e16 posterior setae (Fig. 5f). Etymology. The name of the new genus Rhinariaphis is female in gender. The name refers to large number of secondary rhinaria on antennal segment III-V, what is very unusual in apterous viviparous females in Macrosiphini. Rhinariaphis tuberculata sp. nov. Apterous viviparous female. (Figs 1-8; Tables 1 and 2) Description. As the description of the genus. 4. Notes on SEM morphology and sensilla 4.1. General morphology
Fig. 2. Comparison of the distribution of secondary rhinaria of ANT III of: (a) entire length of the segment in P. tuberculata, (b) only in the apical part in E. elegans, (c) only on the basal part in K. dracocephali.
Fig. 3. Apterous viviparous female of Rhinariaphis tuberculata gen. nov. et sp. nov. e general view.
of thorax and abdomen with very well-developed wart-like bases of setae in the spinal pleural and marginal positions. Each wart-like base has one rigid seta on the apex (Fig. 1g). Body and appendages covered by capitate setae (Fig. 1j). First segments of tarsi with 3-3-3 ventral setae (Fig. 1m). Abdomen with a pair of spinal wart-like bases on ABD I-VII, pair of pleural wart-like bases on ABD I-IV and a pair of marginal wart-like bases on ABD I-VI. Dorsal setae
The head is separated from the pronotum, which is separated from the rest of thorax. The meso- and metanotum are fused together and fused with ABD I-VII. The pronotum has two (one pair) of small and low spinal projections that lie horizontally and two pairs of larger marginal ones that lie vertically. The same arrangement of projections is visible on the mesonotum, but the spinal bases are larger and similar to the other ones on the body. The metanotum has three pairs of projections e spinal, pleural and marginal ones. The abdomen is characterised by paired spinal wartlike bases of dorsal setae on ABD I-VII, pleural bases on ABD I-IV and marginal ones on ABD V-VI. On ABD V-VII in the pleural area, small, sometimes slightly raised sclerites were observed. The wart-like bases have one or rarely two thick and rigid trichoid sensilla, which are also present in the pleural and marginal areas but without projections. ABD VIII in the form of a solid sclerite is separate from the other abdominal tergites (Fig. 6). On the dorsal side of the head, thick, rigid and clearly capitate trichoid sensilla are visible and can be divided into three groups e frontal, on ANT tubercles and on the vertex. The trichoid sensilla of the posterior part of the head are situated on low but visible sclerites (Fig. 7a). Dorsal thoracic and abdominal projections are cone shaped with one thick and rigid trichoid sensillum on the very apex, but some tubercles may also have an additional sensillum near the basal part of the tubercle. The surface of the dorsal tubercles is smooth, but the cuticle between them are clearly pleated in the form of transverse stripes or a polygonal reticulation (Fig. 7b). The dorsal trichoid sensilla are characterised by raised, cone-shaped sockets, which are smooth and distinctly capitate (Fig. 7c). The SIPH are clavate, distinctly swollen from about half of their length with a smooth surface and a well-developed flange. The cauda is slightly tapered near the base (Figs. 3 and 7d). The anal plate is in the form of a semi-circular sclerite, which the genital plate is quite large with a solid sclerite with only few setae (Fig. 7e and f). 4.2. Antennal sensilla The antennal segments have seven kinds of sensilla. The small multiporous placoid sensilla (secondary rhinaria) on ANT III-V are the most clearly seen as one or two rows on the entire length of each segment (Fig. 8aec). The apical parts of ANT V and BASE of ANT VI also have a clearly visible large multiporous placoid sensillum and a group of placoid and coeloconic sensilla (Fig. 8c and d). The large multiporous the placoid sensillum on ANT V (primary rhinarium) is rounded, situated in a deep cavity inside the segment and is surrounded by a very well-developed sclerotic ring with
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Fig. 4. Rhinariaphis tuberculata characters: (a) head, (b) end of the abdomen, (c) ANT III, (d) ANT IV, (e) ANT V, (f) ANT VI, arrows show the primary rhinaria.
Fig. 5. Rhinariaphis tuberculata characters: (a) ventral side of URS, (b) dorsal side of URS, (c) distal part of the hind tibiae and hind tarsus, (d) surface of the dorsal side of the abdomen, (e) abdominal chaetotaxy, (f) genital plate.
20e25 medium and long, irregular projections with very short ones between them (Fig. 8e). The primary rhinaria on the apical part of the ANT VI base are tightly attached to each other, lie deep in cavities inside the segment and are also surrounded by sclerotic rings with numerous projections of the same shape and length as those on ANT V. The large multiporous sensillum (major rhinarium) is the largest, rounded and flat. Small multiporous placoid sensilla
are situated very close to the large placoid multiporous sensillum and more or less visible. Four sunken coeloconic sensilla represent the external group of sensilla; three of them lie very close to the small multiporous sensilla and the very apical one is neighbours with the large multiporous placoid sensillum (Fig. 8f). Small multiporous placoid sensilla and sunken coeloconic sensilla are the accessory rhinaria. On the ventral side of the pedicel, one
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Fig. 6. SEM of apterous viviparous female of Rhinariaphis tuberculata dorsal side of body.
rhinariolum was observed. The rhinariolum is similar to the sunken coeloconic sensilla on ANT VI in the shape of the projection but differs in the round and very smooth edges of the cavity (Fig. 8g and h). All of the antennal segments also have two kinds of trichoid
sensilla. ANT I-ANT VI BASE are covered by type-I trichoid sensilla. These are thick, rigid and with distinctly capitate apices. The sockets of these sensilla are in the form of a truncate cone or are trapezoidal (Fig. 8i, j, k). ANT VI PT is characterised by the presence of short, rigid and slightly pointed type-III trichoid sensilla. The sockets of these sensilla are also in the form of a truncate cone (Fig. 8l and m). The small placoid sensilla on ANT III-V are rounded, different in size, slightly protuberant and lie in cavities that are surrounded by rings of smooth edges (Fig. 8n and o). Diagnosis. As the generic diagnosis. Etymology. The authors followed the original naming given by D. Hille Ris Lambers on the slides of the new species as the apterous viviparous females are characterised by the dorsal side of thorax and abdomen with many large wart-like setae bases. Distribution and biology. To date, the genus and species are only known from Afghanistan where it is associated with Lophanthus spp. Material examined: Holotype e AFGHANISTAN, Paghman, 06.06.1975, Lophanthus pinetorum (¼Nepeta cabulica), one apterous viviparous female (1 apt), marked as 1 and H, van den Bosh leg., BM1984-340 (1) e present marking, BMNH. Paratypes: the same place and date as the holotype, 1 apt marked as 2, BM1984-340 (1) e present marking, BMNH; 2 apt, BM1984-340 (2), BMNH; 2 apt, BM1984-340 (3), BMNH; 2 apt, BM1984-340 (4), BMNH; 2 apt, BM1984-340 (5), ZIN RAS; 2 apt, BM1984-340 (6), DZUS; 1 apt, 2 larvae, BM1984-340 (7), BMNH; 2
Fig. 7. SEM of general morphological characters of Rhinariaphis tuberculata: (a) head, (b) surface of the dorsal side of the abdomen, (c) fine structure of the abdominal trichoid sensillum, (d) dorsal side of the end of the abdomen, (e) lateral side of the end of the abdomen, (f) genital plate.
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Fig. 8. SEM of antennal sensilla of Rhinariaphis tuberculata: (a) ANT III with secondary rhinaria, (b) ANT IV with secondary rhinaria, (c) ANT V with primary rhinarium on the apical part and secondary rhinaria, (d) ANT VI BASE with primary rhinaria, (e) fine structure of the primary rhinarium on ANT V, (f) fine structure of the primary rhinaria on ANT VI BASE, (g) pedicel with a rhinariolum and type-I trichoid sensillum, (h) fine structure of the rhinariolum, (i) type-I trichoid sensilla and small multiporous placoid sensilla on ANT III, (j, k) fine structure of the type-I trichoid sensilla, (l, m) fine structure of the type-III trichoid sensilla of ANT VI PT, (n, o) fine structure of the small multiporous placoid sensilla on ANT III-V.
apt, BM1984-340 (9), BMNH; Charikar, 21.05.1975, 2 apt, L. pinetorum (¼N. cabulica), van den Bosh leg., BM1984-340 (8) e present e, G. marking, BMNH; Kotal Kheder, 17.05.1959, 1 apt, Labie re leg., 22522, MNHN; 1 apt, 22523, MNHN; 1 apt, 22524, Remaudie MNHN; 1 apt, 22525, MNHN; 1 apt, 22526, MNHN; 2 apt, 22527, MNHN; 1 apt, 22528, MNHN; 1 apt, 22529, MNHN; 1 apt, 22530, MNHN; 1 apt, 22531, MNHN; 1 apt, 22532, MNHN; 1 apt, 22533, MNHN; 1 apt, 22534, MNHN; 1 apt, 22535, MNHN; 2 apt, 22536, MNHN; 1 apt, 22537, MNHN; 2 apt, 22538, MNHN; 2 apt, 22539, MNHN; 4 apt, 22540, MNHN; 2 apt, 22541, MNHN1 (3 apt used for the SEM study).
5. Taxonomical comments Blackman and Eatop's (2018) key to aphids on Nepeta (including Lophanthus). The new species is inserted into couplet 10 in their key:
9. SIPH markedly clavate. Secondary rhinaria usually present on ANT IV (eV) as well as III … 10. - SIPH tapering. Secondary rhinaria absent, or only on ANT III … 11. 10. Cauda not longer than its basal width. Rhinaria mainly on distal part of ANT III and on IV. Dorsal abdominal hairs not arising from projections … Eucarazzia elegans. - Cauda c.2 its basal width. Rhinaria evenly distributed over ANT III, IV and V. Dorsal abdominal hairs arising from large wartlike bases … . Rhinariaphis tuberculata. 11. ANT tubercles well developed, divergent. R IV with 16e24 accessory hairs. Marginal tubercles (MTu) present on ABD TERG 2e5, but not on 1 and 7. ANT III with 3e12 secondary rhinaria … Klimaszewskia altaica. - ANT tubercles weakly developed. R IV usually with 2 accessory hairs. ABD TERG 1 and 7 with MTu. ANT III usually without rhinaria … 12.
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Table 1 Comparison of the apterous viviparous females of the most similar genera: Rhinariaphis, Hyperomyzus (Neonasonvia), Eucarazzia and Klimaszewskia. Character
Rhinariaphis
Hyperomyzus (Neonasonovia)
Eucarazzia
Klimaszewskia
ANT III rhinaria
Present. Mostly in one row on the entire length of the segment Present. Mostly in one row on the entire surface of the segment Present. Mostly in one row on the entire surface of the segment 24e40 Not larger than the abdominal stigmal pores 3-3-3 Hairlike Clavate. The narrower basal part clearly longer than the swollen part and narrower than half of the swollen part. Surface always smooth.
Present. In 1e3 rows on the entire length of the segment Absent or present (a few in one row
Present. In one row on the distal part of the segment Present. In one row on the distal part of the segment.
Present. In 2e3 rows on the proximal part of the segment Absent
Absent
Absent
Absent
10e12 Larger than the abdominal stigmal pores 3-3-3 Hairlike Clavate. The narrower basal part clearly shorter than half of the length of the swollen part and as wide as or wider than half of the swollen part. If without any of these combinations of characters, then the SIPH almost tubular and imbricated Tongue-shaped, more or less constricted in the middle of the length. If not constricted then the SIPH almost tubular. Short and rigid. Apices slightly wider (narrow capitate) with a wrinkled or ragged surface. In some species, setae blunt. Low Smooth, without tubercles
20e22 Not larger than the abdominal stigmal pores 3-3-3 Hairlike Remarkably clavate. The narrower part slightly shorter than the strongly swollen part and evidently narrower than half of the swollen part
16e42 Not larger than the abdominal stigmal pores 5-5-5 Slightly spatulate Tubular, tapering with distinct imbrication
Triangle, shorter that its basal width
Tongue-shaped, not constricted. Longer than its basal width
Long, thick and rigid with narrow capitate apices
Long, thick and rigid with narrow capitate apices
Low Smooth, without tubercles
Well developed, divergent Wrinkled, with low tubercles, narrow at the bases
ANT IV rhinaria
ANT V rhinaria
URS accessory setae Thoracic stigmal pores HT I ventral setae Parempodia Siphunculi
Cauda
Tongue-shaped, not constricted. Longer than its basal width
Appendages setae
Long, thick and rigid with wide capitate apices
ANT tubercles Abdominal dorsum
Well developed, divergent Wrinkled with large tubercles, wide at the bases
Table 2 Measurements and ratios values of apterous viviparous females of Rhinariaphis tuberculata gen. nov. et sp. nov. Character
Apterous viviparous female
BL HW ANT ANT III ANT IV ANT V ANT VI BASE PT URS H FEM H TIB HT I HT II SIPH L SIPH W GP L GP W CAUDA L CAUDA W HW:ANT ANT:BL PT:BASE ANT VI:ANT III ANT V:ANT III ANT IV:ANT III LSIII:BDIII URS:ANT III URS:ANT VI URS:BASE URS:HT II HT II:ANT III HT II:ANT VI HT II:BASE SIPH:CAUDA SIPH:BL CAUDA L:CAUDA W
1.85e2.82 0.44e0.54 2.05e2.98 0.48e0.69 0.37e0.59 0.33e0.56 0.68e0.95 0.13e0.17 0.55e0.78 0.12e0.14 0.67e1.02 1.20e1.95 0.03e0.04 0.08e0.11 0.37e0.49 0.07e0.11 0.14e0.22 0.24e0.31 0.23e0.30 0.10e0.15 0.18e0.21 1.05e1.18 4.14e4.48 1.14e1.41 0.61e0.82 0.64e0.85 1.09e1.28 0.18e0.26 0.13e0.18 0.76e0.96 1.09e1.66 0.12e0.19 0.11e0.14 0.57-0-78 1.51e1.84 0.16e0.20 1.85e2-30
Although the establishment of yet another mono-specific genus of Macrosiphini may be disappointing for some of aphidologists, after a deeper examination of the monotypic genera in other groups of aphids, the number of those in Macrosiphini is not excessively large. According to Blackman & Eastop (2018) and Favret (2018), of the approximately 241 valid genera, 90 are known to be monotypic and 27% of all of them belong to the Macrosiphini genera. On the other hand, in Aphidini monotypic genera, they constitute only 16% of the 82 described genera. The percentage of monotypic genera in Macrosiphini seems to be on a normal level compared to other aphid groups such as, e.g. Panaphidini (29%), Fordini (28%), Pemphigini (40%) or Nipponaphidini (29%). Moreover, when the subfamily level is compared, the share of monotypic genera to all known genera is similar and only varies at a level of 20e30% (Fig. 9). Going a little deeper in the analysis of the origin and occurrence of monotypic Macrosiphines, 50% of the known genera are described from different parts of Asia, which has one of the highest numbers of biodiversity centres (Central Asia, China, India Himalaya and Japan) (Fig. 10). Taking into account the sometimes very diverse, vast or mountainous areas of many Asiatic countries, the level of diversity of the monotypic genera may be still be unrecognised. Some recent aphid studies have shown that there are situations in which new species are described in the monotypic genera such as the Macrosiphini genus Aphthargelia Hottes, where a second species has been described 55 years after the genus was established (Jensen 2013). Moreover, in Kaochiaoja Tao, 1963, a new species from India was described last year (Joshi & Blackman 2017). In the Chaitophorinae monotypic Yamatochaitophorus Higuchi, a second species was described from China (Jiang et al. 2016). Considering that the aphid fauna of Afghanistan is only known to a very basic degree and taking into account the alpine and diverse character of most of the Afghan area, we expect more species of Rhinariaphis to be discovered. In addition, the collection
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Fig. 9. Share of monotypic genera within Aphididae subfamilies.
References
Fig. 10. Analysis of the monotypic Macrosipini genera in those described here and those occurring in different continents.
of fresh live specimens of P. tuberculata will provided the opportunity to perform molecular analyses in order to determine its position and relationships with other Macrosiphini species.
Acknowledgements We are sincerely grateful to Paul A. Brown (Natural History Museum, London, UK), Dr. Daniele Matile-Ferrero, Dr. Adeline Soulier-Perkins, Prof. Thierry Bourgoin and the late Prof. George re (Muse um National d'Histoire Naturelle, Paris, France) Remaudie for their kind help and support during the internships in the collections as well as for the loan of the many slides of Macrosiphini. We would like to thank the Editor and two anonymous Reviewers for all comments and suggestions that improved the first version of the manuscript. Mariusz Kanturski gratefully acknowledges the Scholarship for Outstanding Young Scientists from the Ministry of Science and Higher Education of Poland (1165/E-340/STYP/12/17).
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