The genus Aphidura (Hemiptera, Aphididae) in the collection of the Muséum national d’Histoire naturelle of Paris, with six new species

Abstract Specimens were studied of 65 samples of the genus Aphidura (Aphididae, Aphidinae, Macrosiphini) from the collection of the Muséum national d’Histoire naturelle (Paris). The possible synonymies of three pairs of species are discussed. New aphid host plant relationships are reported for Aphidura bozhkoae, Aphidura delmasi, Aphidura ornata, Aphidura pannonica and Aphidura picta; this last species is recorded for first time from Afghanistan. The record of Aphidura pujoli from Pakistan is refuted. The fundatrices, oviparous females and males of Aphidura delmasi are described. Six new species are established: Aphidura gallica sp. n. and Aphidura amphorosiphon sp. n. from specimens caught on species of Silene (Caryophyllaceae) from France and Iran, respectively, Aphidura pakistanensis sp. n., Aphidura graeca sp. n. and Aphidura urmiensis sp. n. from specimens caught on species of Dianthus, Gypsophila and Spergula (Caryophyllaceae) from Pakistan, Greece and Iran, respectively, and Aphidura iranensis sp. n. from specimens caught on Prunus sp. from Iran. Modifications are made to the keys by Blackman and Eastop to aphids living on Dianthus, Gypsophyla, Silene, Spergula and Prinsepia and Prunus (Rosaceae). An identification key to apterous viviparous females of species of Aphidura is also provided.


introduction
In the early 1980s G. Remaudière and D. Hille Ris Lambers studied some samples of Aphidura (Hemiptera, Aphididae, Aphidinae, Macrosiphini) belonging to the Remaudière collection, which was at that time at the Institut Pasteur in Paris, but later moved to the Muséum national d'Histoire naturelle. They made preliminary works to describe several new species of this genus, but the work was interrupted and a manuscript draft was never prepared due to the illness and death in April 1984 of Hille Ris Lambers. Some of the slides studied by Hille Ris Lambers were sent with the rest of his collection to the British Museum (Natural History), currently the Natural History Museum, in London. Some years later Remaudière did establish one new species in this genus (Remaudière 1989) but this was from specimens that had not been part of his studies with Hille Ris Lambers.
All those samples, together with the rest of the specimens of Aphidura of the above-mentioned collection, have now been studied, and the results are presented in this paper.
The genus Aphidura was morphologically well defined by Hille Ris Lambers (1956), and the type species, A. ornata Hille Ris Lambers, is also well defined, so no doubt exists about the correct taxonomic position of the species included within it. Apterous viviparous aphids can be identified as Aphidura, in addition to the characteristics of the tribe Macrosiphini, by the presence of a pair of mesosternal mammariform processes (in Hille Ris Lambers's words: «Distinct, conspicuously pigmented or pale, rough mammiform processi present on anterior part of mesosternum in apterae and larvae»), together with a triangular or tongue-shaped cauda and reniform spiracular apertures centred in the respective sclerites.
Similar mesosternal processes are also present in several species of Brachycaudus van der Goot, 1913, mainly belonging to subgenus Acaudus van der Goot, 1913, and in the sole species of Zinia, Z. veronicae Shaposhnikov, 1950. These species of Brachycaudus have a helmet-shaped cauda and wide, rounded spiracular apertures, and Z. veronicae has a rounded cauda, reniform spiracular apertures that are placed in the posterior half of the spiracular sclerites and, in addition the dorsal cuticle is densely spinulose (Hille Ris Lambers 1956, Shaposhnikov 1950, Andreev 2004.
The genus exhibits a Mediterranean-Pontian-Turanian distribution with extensions to neighbouring areas and exceptionally -A. mordvilkoi -to the Russian Far East. The current known distribution of each species is shown in the species identification key at the end of this paper, A. picta being the species with the widest distribution (Blackman and Eastop 2006, Holman 2009, Nieto Nafría et al. 2012.

Material and methods
Aphidura specimens of the aphid collection of the Muséum national d'Histoire naturelle of Paris, mounted in microscopic slides, belonging to 65 samples (Table 1) have been studied.

NOTES:
In the "Locality" column, supplementary information and upper administrative unit (such as county, department, province, regional unit, etc.) are respectively given in square brackets and in parentheses. cated otherwise as width or diameter. A Leica DC digital 96 camera with IM 1000 version 1.10 software was used for the photomicrographs, which have been taken and mounted by L. M. Fernández Blanco.
In the modifications to the identification keys by Eastop (1994, 2006) that are included in the discussion of each species, the terms that they use (for example 'hair' instead of 'seta' and 'clavate' instead of 'swollen') have been retained so that they can be easily understood and used by those accustomed to them.

Generic characters
Apterous viviparous aphids can be identified as Aphidura by the presence of a pair of mesosternal mammariform processes, as mentioned above, and also by the following characters: (1) frons w-shaped with rugose or scabrous lateral tubercles not much higher than the broad median tubercle; (2) cephalic dorsum not ornamented or with spinules, which may be more-or-less scattered or in groups; (3) clypeus and mandibular and maxillar lamina more-or-less pigmented like cephalic dorsum and rostrum; (4) antennae not longer than body length; (5) secondary sensoria absent; (6) antennal segment I and II scabrous or rugose, segment III with scattered scales, and IV-VI more-or-less imbricated; (7) rostrum extending backward beyond middle coxae or reaching hind coxae; (8) ultimate rostral segment triangular with straight margins, usually darker than the previous segments; (9) legs with coxae and trochanters pale, femora entirely pale or with a darker distal part; tibiae pale in general with a distal portion smoky, exceptionally entirely pale, and tarsi brown; (10) first segment of tarsi with 2-4 setae; (11) abdominal spiracular apertures reniform, placed in the middle of small spiracular sclerites; (12) intersegmental sclerites well defined and usually pigmented, and embodied in the segmental sclerites if these are present; (13) thorax and abdomen often with a dorsal pattern of sclerotisation that is very variable between species, and can also vary within them (see below terminological usage); (14) siphunculi usually with a distinct preapical incision and flange, but variable in shape (see below for details and terminological usage); (15) cauda triangular to tongue-shaped; (16) spinules present, more-or-less conspicuously and densely, on mesosternal mammariform processes, postsiphuncular sclerites, spiracular sclerites 7, and abdominal terga 7 and 8; (17) antennal and dorsal setae short or very short, with blunt, frayed or (rarely) incrassated apex; (18) dorsal setae not placed on tubercles, except sometimes in A. acanthophylli; (19) ventral setae longer than respective dorsal and pointed; and (20) setae on dorsal faces of femora and on proximal parts of tibiae with blunt or frayed apex, other setae on legs pointed.
The alate viviparous females have no mesosternal mammariform processes, and differ from apterae by having: (a) longer and more pigmented antennae, (b) round, double-rimmed secondary sensoria scattered along the ventral face of antennal segment III, and rarely on segment IV, (c) pigmentation of legs more extensive and darker; (d) dor-sal abdomen often with more sclerotisation than in apterae, but again this varies greatly both between and within species; (e) spinules also present in the marginal sclerites.
Regarding the thoracic and abdominal dorsal sclerotisation, the term "spinopleural patch" is utilized here for a continuous sclerotisation of spinal and marginal areas of two or more segments (Figs 2B,D,4A,6A), and the term "discal plate" is utilized for the continuous and extensive sclerotisation of spinal, pleural and marginal areas of three or more segments (Figs 1A,C,2A,C).
The siphunculi of Aphidura species are variable in shape: (a) cylindrical, subcylindrical (delicately tapering to the apex) or conspicuously tapering from base to apex, straight or curved outward (Figs 1D,2A,4B,6A); (b) slightly swollen -«cylindrical with very tapering apex, below their middle very little attenuated, so that they might be considered as very slightly clavate» (Hille Ris Lambers 1956)-, having the maximal width of the distal half less than 1.2 times the minimal width of the stem (Figs 2D, 3A, 5B, 6A); (c) markedly swollen, with large base, cylindrical stem and a conspicuously swollen distal portion, the width of which is conspicuously greater (at least 1.2 times) than the minimal stem width (Figs 1A,4D,5C,6B).

Synonymies in Aphidura
Possible synonymies of three pairs of Aphidura species are discussed: A. bharatia and A. ornatella, A. mingens and A. picta, and finally A. prinsepiae and A. mordvilkoi. Eastop and Blackman (2005) established that A. bharatia is a synonym of the older name A. ornatella. Both species are considered valid by  because he found differences between aphids identified as bharatia and others identified as ornatella, although he does not refer to Eastop and Blackman's paper. In our opinion these differences could be enough to keep the validity of both species, but they can also be an expression of intraspecific variability, which would present a cline North to South; Kadyrbekov himself shows differences between ornatella populations from Kazakhstan and Tajikistan.
Characters of studied apterous and alate vivipara (Figs 1A, B; Table 2 for six alatae from Pakistan; only one alate of this species was previously known ]), overlap characters mentioned by Kadyrbekov for southern (from India and Pakistan) and northern (from Kazakhstan and Tajikistan) populations. In conclusion, we consider it is preferable to keep the synonymy.
The species pair Aphidura mingens and A. picta provides a similar situation: they are considered synonymous names by Eastop and Blackman (2005) and valid names by , who found differences in the siphunculi shape (slightly swollen in picta specimens and subcylindrical, more or less tapering and curved outwards in mingens specimens) and in several quantitative characters. The original description of A. picta is quite unsatisfactory because it is based on one specimen «untypical of the species as a whole» (Eastop and Blackman, op. cit), which «might be a fundatrix of that species [A. ornata]» (Hille Ris Lambers 1956), and the species is so variable in sclerotisation, pigmentation, siphuncular shape and setal length (Fig. 1C).   In our opinion the synonymy can stand, because V. F. Eastop studied a wide number of specimens from diverse provenances (host plants, localities and dates), including types (R. L. Blackman, pers. com.), and also because of our observations, or at least it should be maintained in the sense that there is only one variable species involved. Nevertheless the valid name for this species could be A. mingens if the holotype of A. picta could be shown to be a fundatrix of A. ornata, in which case A. picta would be a synonym of that species. Blackman and Eastop (2006) showed that Aphidura mordvilkoi and A. prinsepiae could be synonyms.  established the synonymy. We have found differences between specimens identified as prinsepiae by Patshchenko and other ones identified as mordvilkoi by Shaposhnikov (Fig. 1D), similar to those shown by . All of them can be considered to be a consequence of intraspecific variability. In conclusion, the established synonymy can be kept.

New host plant and country records
Collection data for the following first records are shown in Table 1.
Aphidura bozhkoae ( Fig. 2A) is recorded for the first time on Prunus spinosa and on P. prostrata; it was previously recorded from several other species habitually placed in Prunus, although some of them can be classified in Cerasus or in Aflatunia.
Aphidura delmasi (Fig. 2B) is recorded for the first time on Silene viscosa; it has previously been recorded on other species of Silene.
Aphidura ornata (Fig. 2C) is recorded for the first time on Silene inaperta, S. nutans and S. saxifraga; it has been recorded previously on four other species of Silene.
Aphidura pannonica (Fig. 2D) is recorded for the first time on Gypsophila paniculata; this aphid has been previously recorded from several species of Silene.
Aphidura picta (Fig. 1C) is recorded for the first time (i) on Silene glauca and (ii) from Afghanistan. This aphid has been recorded on several species of Silene, and also of Dianthus; and it was known from Iran, Tajikistan and Pakistan, and other Asiatic and European countries.

Aphidura pujoli, amendment of distribution
The identification made by G. Remaudière, of four apterous viviparous females belonging to his sample 014072 from Pakistan, as A. pujoli is not correct; in fact these specimens belong to a new species, A. pakistanensis. In consequence the record of A. pujoli from Pakistan by Naumann-Etienne and Remaudière (1976) is incorrect, and A. pujoli (Fig. 3A) remains restricted to Europe, having been recorded from Portugal, Spain, France (including Corsica), Switzerland, Italy (including Sicily), and Ukraine.
Male. From 4 specimens (Fig. 3D). Apterous. Also very similar to the fundatrigenous aptera, but smaller, with paler legs (only tarsi are smoky) and longer antennae. Aedeagus and parameres brown. Metric and meristic features in Table 2.

New species
Six new species are established: A. gallica and A. amphorosiphon, which live on species of Silene, A. pakistanensis, A. graeca and A. urmiensis, which live on other caryophyllaceous plants (respectively species of Dianthus, Gypsophila and Spergula), and A. iranensis, which lives on Prunus.
Aphidura gallica sp. n. urn:lsid:zoobank.org:act:7C59AAC8-D440-4EAC-B376-047DA69F053A http://species-id.net/wiki/Aphidura_gallica Apterous viviparous female (Figs 4A,B). Colour in life unknown. Head yellowish brown with rugosity near the eyes. Antennal segments I-IV as pale as cephalic dorsum, and V and VI darker. Dorsal pigmentation and sclerotisation very variable. In several specimens, holotype included prothorax with complete but pale band, metathorax with brown spinopleural transverse band and setiferous marginal sclerites, abdominal segments 1-6 with an extensive dark spinopleural patch, partially fragmented in midline and with an irregular lateral margin partly incorporating the marginal sclerites; abdominal segments 7 and 8 with bands paler than patch. In other specimens, dorsum mainly membranous, with pale brown to brown pleural sclerites on abdominal segments 1-6, which are irregular in shape and sometimes joined between segments, and several very small and pale marginal setiferous sclerites. Other specimens have an intermediate degree of sclerotisation and pigmentation. Mesosternal mammariform processes yellowish, thin and tall. Siphunculi cylindrical, dark, and densely covered with denticulate scales. Cauda triangular (sometimes with a slight constriction) with pointed apex, and not darker than legs. Anal and genital plates as pale as cauda. Metric and meristic features in Table 3.
Alate viviparous female (Fig. 4C). Head brown, as dark as thorax. Abdominal segments 1 and 2 with spinal sclerites; segments 4-5 with spinopleural patch, sometimes partially joined with the spinopleural bands on 3 and 6; segments 1-6 with marginal sclerites; segment 7 with a band paler than previously mentioned sclerites; segment 8 with pale setiferous sclerites, sometimes coalesced together. Metric and meristic features in Table 3.  Etymology. The specific name of the new species, gallica, is an adjective that refers to the Galia, France in times of the Roman Empire, in feminine; it is also coincident with the specific name of the host plant of the holotype.
Discussion. See the discussion of the following new species.
Aphidura amphorosiphon sp. n. urn:lsid:zoobank.org:act:812E7A5A-0BE0-4424-8661-38A7D0CC268C http://species-id.net/wiki/Aphidura_amphorosiphon Apterous viviparous female (Fig. 4D). Colour in life unknown. Head yellowish brown to brown. Antennal segments II-III or II-V pigmented like cephalic dorsum, and I and IV-VI or only VI darker than others. Mesosternal mammariform processes rounded, low and pale. Several specimens (holotype included) are pale in general with dark brown intersegmental sclerites, brown postsiphuncular and spiracular sclerites, pale brown setiferous sclerites on abdominal segments 6-8, sometimes coalescing together into transverse bands. The most pigmented specimen has a transverse spinopleural band on prothorax, fragmented bands on mesothorax and abdominal segments 1, 6 and 7, fragmented spinopleural patches on abdominal segments 2-5, and setiferous sclerites on metathorax and abdominal segments 1 and 8. Siphunculi markedly swollen, with stem nearly smooth, and pale or with a smoky apical portion. Cauda triangular, sometimes with a slight constriction near the base, and as pale as the greater part of siphunculi and legs. Genital and anal plates as pale as cauda. Metric and meristic features in Table 3. Alate viviparous female (Fig. 5A). Head brown, as pigmented as pro-and pterothorax and darker than antennae, tarsi and distal portions of femora and tibiae. Abdominal segments 3-5 with a spinopleural patch, and 7-8 with transverse bands. Siphunculi as dark as pigmented parts of femora. Other qualitative features as in apterae. Metric and meristic features in Table 3.
Male. Winged. Qualitatively very similar to alate viviparous females; with dark parameres. Metric and meristic features in Table 3.
Discussion. The distinctive features of A. amphorosiphon sp. n. and A. gallica sp. n. are summarized in the identification key to apterae of Aphidura in the general discussion, and in the following modification to the key to aphids on Silene (Blackman and Eastop 2006) for addition of Aphidura amphorosiphon and A. gallica (Aphidura spp. from Iran and from France respectively in that key), and also A. massagetica and A. nomadica, which have been recently described , with deletion of couplets 28 to 34, although several propositions have been partially or completely reutilised: Etymology. The specific name of the new species is an adjective that refers to Pakistan, in feminine. 10-14 13 9-18 7-10 … Cauda [number] 6-8 7 9-14 6-6 NOTE. Used abbreviations: Ant., Antennal; b. d., basal diameter; n, number of measured specimens; segm., segment.
Discussion. Aphidura pakistanensis sp. n. is the third species of the genus living on Dianthus. Its distinctive features are summarized in the identification key to apterae of Aphidura in the general discussion, and in the following modification to the key to aphids on Dianthus (Blackman and Eastop 2006) for addition of A. pakistanensis:

7
ABD TERG 1 and 7 without MTu. SIPH subcylindrical or slightly swollen). Anterior part of mesosternum with a pair of spinal mammariform processes ...7A -ABD TERG 1 and 7 with MTu. SIPH tapering from base to flange, with no trace of swelling. Etymology. The specific name of the new species is an adjective that means inhabitant of Greece, in feminine.
Discussion. Aphidura graeca sp. n. lives on Gypsophila, as does A. gypsophilae, and also A. pannonica, which has been above recorded on this plant-genus for first time. The distinctive features of Aphidura graeca are summarized in the identification key to apterae of Aphidura in the general discussion and in the following modification to the key to aphids on Gypsophila (Blackman and Eastop 2006), to include A. graeca and A. pannonica, and also A. naimanica and A. togaica, which have recently been described   (Fig. 5D). Colour in life unknown. Head yellowish brown to brown. Clypeus bigger than those of the other species of Aphidura. Antennae yellowish brown, with brown segment VI, distal 1/3 of V, and articulation between IV and V. Mesosternal mammariform processes well separated from one another, pale and round. Intersegmental sclerites small and dark brown; spiracular sclerites on segment 7 wider and darker than other abdominal spiracular sclerites; abdominal segments 3-6 with pleural and sometimes very small setiferous spinal sclerites, or with spinopleural sclerites; abdominal terga 7 and 8 pale. Siphunculi with narrow base, cylindrical (usually with slight outward curve) or slightly swollen, and as pale as tibiae. Cauda tongueshaped, pale like genital and anal plate. Metric and meristic features in Table 4. Types. Holotype: Apterous viviparous female (specimen 5), on Spergula marina, Shahi island, Lake Urmia (East Azerbaijan), Iran, 5-VIII-1955, Remaudière leg. (sample i962). Paratypes: 42 apterous with the same data that the holotype; plus 6 apterous viviparae on S. marina, Charimboulaki, Lake Urmia (West Azerbaijan), Iran, 9-VIII-1955, Remaudière leg. (sample i004a).
Etymology. The specific name, urmiensis is an adjective that refers to lake Urmia, in feminine, from the name of the Catholic Chaldean Archdiocese of Urmia.
Discussion. The distinctive features of A. urmiensis sp. n., which lives on Spergula marina are summarized in the identification key to apterae of Aphidura in the general discussion and in the following modification to key to aphids on Spergula and Spergularia (Blackman and Eastop 2006) (Fig. 6A). Colour in life unknown. Head brown. Vertex with spinules disposed in scattered groups. Prothorax and at least some of abdominal segment 2-4 with small marginal tubercles; abdominal segment 8 with 0-2, most frequently 1, small spinal tubercles. Mesosternal mammariform processes rounded and pale. Dorsal pigmentation and sclerotisation very variable. In several specimens (holotype included) prothorax with a complete band, mesothorax with a band with lateral windows, metathorax with two large spinopleural sclerites; abdominal segments 1-5 with several setiferous marginal sclerites, and a spinopleural patch, which has irregular edges and windows and may be coalesced with the metathoracic sclerites; abdominal segment 6 with small intersiphuncular and two postsiphuncular sclerites; segments 7 and 8 with brownish band; intersegmental sclerites are embodied in the above; spiracular sclerites inconspicuous. In less sclerotized and paler specimens the bands and patch are broken. Siphunculi slightly swollen, ornamented with denticulate scales, and paler than cephalic dorsum and dorsal thoracic-abdominal sclerotized areas. Cauda thin triangular, paler than siphunculi. Genital plate pale; anal plate coloured like cauda. Metric and meristic features in Table 4. Types. Holotype: Apterous viviparous female (specimen 1), on Prunus sp., Khoy [30 km North] (West Azerbaijan), Iran, 1700 m, 7-VIII-1955, G. Remaudière leg. (sample i982). Paratypes: 5 apterous viviparous females, with the same collecting data as holotype.
Etymology. The specific name of the new species, iranensis, is an adjective that refers to Iran, in feminine.
Discussion. Aphidura iranensis sp. n. is the second species of the genus living on species of Prunus. Its distinctive features are summarized in the identification key to apterae of Aphidura in the general discussion, and in the following modification to the key to aphids on Prunus (Blackman and Eastop 1994)  Anterior part of mesosternum with a pair of spinal mammariform processes, ornamented with spinules (Fig. 89B)

General discussion
The features that distinguish the apterous viviparous females of the Aphidura species which share host plants have been described in the modifications to Blackman and Eastop's keys to aphids on different plant genera Eastop 1994, 2006) in the particular discussion of each new species. The previously known and the new species together can be distinguished from each other using the following key to apterous viviparous females of species of Aphidura. In brackets are: (1) morphological characters that do not have correspondence in the other proposition of the disjunctive, but which are useful to confirm identification; (2) host plants, and distribution data; and (3) illustration reference. In the distribution of each species the countries are in geographical order from West to East, so that a quick general assessment of the distribution of each species can be made. The key uses data of species recently described from the respective original descriptions ; other data are from literature and personal observations. A. melandrii is accessible by two routes, because several specimens have slightly swollen siphunculi (maximal swollen width at least 1.2 times minimal stem width) and others have conspicuously swollen siphunculi. A. pujoli (from Blackman and Eastop op. cit.) and A. delmasi (this paper) are monoecious holocyclic, and A. amphorosiphon is very possibly holocyclic (this paper). The life cycle of the other species of the genus is unknown. It is possible that three types of life cycle currently exist in this genus, as in Brachycaudus van der Goot, 1913: (i) monoecious (and probably holocyclic) on a rosaceous species (e.g. A. bozhkoae on Prunus spp. and A. mordvilkoi on Prinsepia sinensis), (ii) monoecious on a caryophyllaceous species (and also probably holocyclic, e.g. A. delmasi and A. pujoli), and (iii) dioecious cycle with rosaceous species as primary host, and caryophyllaceous species as secondary host.

Key to apterous viviparous females of
For us the more probable hypothesis is that all current species of Aphidura are monoecious, but that their common ancestor was dioecious, as in various other genera of Macrosiphini, and later the Aphidura branch diversified into two monoecious lineages, one Rosaceae-feeding and the other Caryophyllaceae-feeding. This is analogous to the South American species of Pentamyzus Hille Ris Lambers, 1966 which are all monoecious holocyclic, with several species living on Acaena (Rosaceae) and others on Alopecurus, Hordeum or Poa (Poaceae) (Nieto Nafría et al. 2002).