Taxonomic Position of the Genus Puto Signoret (Homoptera: Coccinea: Pseudococcidae)

ZOOSYSTEMATICA ROSSICA, 21(1): 97–111 25 JULY 2012

Taxonomic position of the genus Puto Signoret (Homoptera: Coccinea: Pseudococcidae) and separation of higher taxa in Coccinea Таксономическое положение рода Puto Signoret (Homoptera: Coccinea: Pseudococcidae) и разделение высших таксонов Coccinea

I.A. GAVRILOV-ZIMIN & E.M. DANZIG

И.А. ГАВРИЛОВ-ЗИМИН, Е.М. ДАНЦИГ

I.A. Gavrilov-Zimin & E.M. Danzig, Zoological Institute, Russian Academy of Sciences, 1 Universitetskaya Emb., St Petersburg, 199034, Russia. E-mail: [email protected]

Taxonomic characters of the families Pseudococcidae Cockerell, 1898, Putoidae Beadsley, 1969, Pennygullaniidae Koteja et Azar, 2008 and two superfamilies of Coccinea are discussed in view of phylogenetic meaning of these characters. It is shown that Putoidae Beadsley, 1969 is an unavailable name (nomen nudum); moreover, Putoidae sensu Williams et al., 2011 as a separate family considered in the superfamily Orthezioidea (= an informal group of “archeococcids”), is a taxonomic paradox that lies outside of both cladistic and evolutionary concepts in taxonomy and ignores the majority of well-known and carefully proven facts. There is not a single unique apomorphic character in the monotypic family Putoidae; all characters of the genus Puto Signoret, 1875 are plesiomorphies of all scale insects or synapomorphies with other mealybugs or with the closely related Ceroputo Šulc, 1898. Ceroputo is accepted here as a subgenus of Puto. The monotypic fossil family Pennygullaniidae is considered by us a new subjective synonym of Pseudococcidae. The taxonomic and nomenclatural problems connected with the higher taxa of scale insects and other groups of Homoptera are briefly discussed. Таксономические признаки семейств Pseudococcidae Cockerell, 1898, Putoidae Beadsley, 1969, Pennygullaniidae Koteja et Azar, 2008 и двух надсемейств подотряда Coccinea об- суждаются в свете филогенетического значения этих признаков. Показано, что Putoidae Beadsley, 1969 является непригодным названием (nomen nudum). Более того, Putoidae sensu Williams et al., 2011, принимаемое как отдельное семейство внутри надсемейства Orthezioidea (= неформальная группа “археококциды”), представляет собой таксономи- ческий парадокс, лежащий за рамками как кладистической, так и эволюционной кон- цепций в современной систематике и противоречащий большинству хорошо известных и тщательно изученных фактов. Монотипное семейство Putoidae не имеет ни одной уни- кальной апоморфной черты; все изученные признаки рода Puto Signoret, 1875 являются либо общекокцидными плезиоморфиями, либо синапоморфиями с другими мучнисты- ми червецами и близкородственным Ceroputo Šulc, 1898. Таксон Ceroputo принимается здесь как подрод Puto. Монотипное вымершее семейство Pennygullaniidae рассматрива- ется нами как новый субъективный синоним семейства Pseudococcidae. Кратко обсуж- даются также таксономические и номенклатурные проблемы, связанные с названиями высших таксонов кокцид и родственных групп Homoptera. Key words: mealybugs, scale insects, Hemiptera, Homoptera, Coccoidea, Orthezioidea Ключевые слова: мучнистые червецы, кокциды, Hemiptera, Homoptera, Coccoidea, Orthezioidea

INTRODUCTION practice (see works of E. Danzig, J. Koteja, E. Podsiadlo, R. Jashenko, I. Gavrilov and According to the paper of Williams et al. others)]: Aphidinea, Coccinea, Aleyrodin- (2011), recently published in Zootaxa, two ea, Psyllinea, Cicadinea. The International similar nominal genera of mealybugs, Puto Code of Zoological Nomenclature (below: Signoret, 1875 and Ceroputo Šulc, 1898, the Code) does not regulate now the taxo- which have been considered for many years nomic names higher than family-group as subjective synonyms, must not only be names. We follow the principle introduced distinguished as two separate genera but by Rohdendorf (1977) and consider the must be placed in two different families and suborder names as the family-group ones even in two different superfamilies of Coc- with their own coordination. cinea. Unfortunately, we cannot accept the Probably, it will be better to accept stan- opinion of the cited authors; below, we dis- dardized typified names for all animal higher cuss all the known taxonomic characters of taxa as it is done now for botanical names or Puto in comparison with other scale insects was accepted for insects by paleontologists and in view of evolutionary significance of (History of Insects, 2002). In this case all these characters. proboscidian insects will be covered by the Before further discussion, we need to name Cimicidea Laicharting, 1781. Howev- clarify our concept of the taxonomic posi- er, in view of numerous disputes about the tion of scale insects as a whole and related future of the Code we avoid accepting typi- groups, because: 1) it is not possible to con- fied names for taxa higher than suborders. sider the questions of higher classification The name Hemiptera Linnaeus, 1758, within Coccinea without consideration of frequently used (often under pressure from relationships of scale insects with other pro- editors of journals) in coccidological litera- boscidian insects; 2) many different classifi- ture as an order name for all the groups of cations have been proposed for hemipteroid proboscidian insects, is not accepted by us insects, especially in the last years [see, for in this sense, because: 1) this name was used example, the reviews of Brożek et al. (2003), by C. Linnaeus for proboscidians + thrips Forero (2008), Kluge (2010a, b)]; 3) there (Fig. 1); therefore it is an older synonym for are some nomenclatural problems connect- Condylognatha Börner, 1904; 2) for many ed with names of higher taxa of scale insects years until now, this name has been used by and other hemipteroids; 4) two principally numerous authors for true bugs (Heterop- different approaches to higher classification tera) only; 3) there are at least two sepa- of hemipteroid insects (cladistic and evolu- rate orders (Heteroptera and Homoptera) tionary) are present in the literature. within the “order Hemiptera” accepted by It seems that the oldest non-typified different modern authors. A similar taxo- name for all scale insects is Gallinsecta De nomic situation exists with the well-known Geer, 1776 (Kluge, 2000, 2010a, b). But, and widely used name Rhynchota Burmeis- instead of this name (and several other non- ter, 1835, which originally covered not only typified old names), during the entire his- proboscidians but also Siphunculata. More- tory of coccidology different typified names over, this name is preoccupied by Rhyncho- have been preferred by coccidologists: Coc- ta Billberg, 1820 (= Aphaniptera Kirby et cidae, Coccoptera, Coccoidea, Coccomor- Spence, 1815) (Kluge, 2010a). The oldest pha, Coccinea, Coccina, etc. We recognize name which covers all the recently accept- the scale insects and other homopterans ed proboscidian insects (and only them) as suborders of the order Homoptera, and is Arthroidignatha Spinola, 1850 (Kluge, use the special ending “-nea” for all typified 2000, 2010a, b). Although this name has suborder names in Homoptera [following not been used in entomological literature Pesson (1951) and internal coccidological for many years, in the modern difficult taxo-

Fig. 1. Copy of p. 343 from “Systema Naturae” by C. Linnaeus (1758). nomic and nomenclatural situation with the filter chamber of the digestive tract as well names Hemiptera and Rhynchota we prefer as ability to produce honeydew can be con- to use Arthroidignatha for all proboscidian sidered as synapomorphies of Homoptera insects. (Hamilton, 1981; Lambdin, 2001; D’Urso, As for the widely known and frequently 2002; present paper). We do not see any rea- discussed order name Homoptera Latreille, son to ignore these characters and prefer the 1810, we do not see serious reasons to re- probable morphological synapomorphies of ject it. It originally covered all probocidians Hemelytrata (see, for example, Emeljanov, without true bugs but with the addition of 1987) or believe the untestable data of mo- thrips. However, all other authors used this lecular cladograms based on a small number name in its modern composition, i.e. with- of studied taxa (Campbell et al., 1995; von out thrips. The notion about paraphyletic Dohlen & Moran, 1995; others; see also our content of Homoptera auct. [for review, see comments below, in the section “The data of for example, von Dohlen & Moran (1995) or DNA sequencing”). A detailed historical re- Gullan (1999)] is merely a hypothesis that vision of different phylogenetic reconstruc- considers some facts and ignores others. Ac- tions of proboscidian insects was given by cording to the cladistic point of view, the Brożek et al. (2003) and by Forero (2008) problem boils down to considering synapo- and will not be repeated here. In any case, morphies of the Hemelytrata Fallen, 1829 whether further investigations support the (Cicadinea+Coleorrhyncha+Heteroptera) hypothesis about the paraphyly of the Ho- in contrast to synapomorphies of Homop- moptera or not, it cannot be a reason to reject tera. Some authors (for example, Gullan, the taxon Homoptera. 1999) even affirm that Homoptera is char- The cladistic dogma about rejecting acterized by plesiomorphic characters only. paraphyletic taxa is not based on any sci- Of course, it is not so easy to find reliable entific arguments; it is only based on vol- synapomorphies for all, very diverse groups untary decision. There is not a single sci- of Homoptera. However, such characters as entific reason to suppose that species in large loral sutures defining the mandibular paraphyletic taxa should be less related to plate, the development of wing-coupling each other than the species in holophyletic apparatus, the presence of wax glands and taxa. This main conceptual contradiction

© 2012 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 21(1): 97–111 100 I.A. GAVRILOV-ZIMIN & E.M. DANZIG. TAXONOMIC POSITION OF THE GENUS PUTO between cladistic taxonomy (in its origi- apomorphies of this group. For example, ac- nal W. Hennig’s sence) and evolutionary cording to the scheme of D.E. Shcherbakov taxonomy was discussed in many special and Yu.A. Popov (History of Insects, 2002), papers and books [see, for example, Simp- Sternorhynchi seems to be polyphyletic. son (1961), Mayr (1974), Mayr & Ashlock Moreover, we believe this taxon to be su- (1991), Gorochov (2001), Kerzhner & perfluous in practical classification, because Danzig (2001), Hołyński (2005), Rasnit- it needs to add and use one more rank be- syn (2010), and others] and well phrased tween order and suborder for this group. In by R.B. Hołyński (2005): “…paraphyletic addition, Sternorhynchi Amyot et Serville, taxa do not exist; why not? – because what 1843 is a junior synonym of Plantisuga Du- is paraphyletic is not a taxon; why? – of meril, 1805 (Kluge, 2010a). course because no taxon can be ancestor of As for names of superfamilies within the another taxon… Maybe it is good philoso- Coccinea, they are regulated by the Code phy, but good biology it is certainly not…”. and are well known. However, in the mod- Moreover, paraphyly of any taxon is closely ern coccidological literature, some authors connected with our subjective view of the [including those of the discussed paper of borders of the taxon. For example, if we in- Williams et al. (2011)] use informal and clude the fossil ancestor groups of Arthroi- non-typified names “archaeococcids” and dignatha (in particular, Archescytinoidea) “neococcids” for the same family-groups in Homoptera, the latter will evidently be that were placed in the superfamilies Orth- paraphyletic; on the other hand, if we in- ezioidea and Coccoidea many years ago. clude Archescytinoidea in Hemelytrata, the This strange preference of informal names latter will be paraphyletic. The factual pa- is probably the result of the consistent use leontological data on the appearance of dif- of cladistic dogmata, because Coccoidea ferent Arthroidignatha groups are provided evidently originated from the Orthezioidea in the recent scheme of D.E. Shcherbakov and the latter taxon is paraphyletic [see, for and Yu.A. Popov (History of Insects, 2002). example, the phylogenetic reconstruction As for the frequently used name of Danzig (1980) or the phylogeny of Kote- Sterno(r)rhynch(i)(a) (= Coccinea +Aphi- ja (1989) based on paleontological data]. dinea + Aley ro dinea + Psillinea), we are As a result, we use the following classifi- not sure of the commonly discussed syn- cation in the present paper: Phylogenetic line Paraneoptera Martynov, 1923 (including Zoraptera, Copeognatha, Parasita, Thysanoptera, Homoptera, Coleorrhyncha, Heteroptera) Cohors Hemiptera Linnaeus, 1758 (= Condylognatha Börner, 1904, non Hemiptera auct.) Superordo Thysanoptera Haliday, 1836 Superordo Arthroidignatha Spinola, 1850 (= Hemiptera auct. non Linnaeus, 1758; = Rhynchota auct. non Burmeister, 1835) Ordo Coleorrhyncha Meyers et China, 1929 Ordo Heteroptera Latreille, 1810 (= Hemiptera auct. non Linnaeus, 1758) Ordo Homoptera auct. non Latreille, 1810 Subordo Cicadinea Batsch, 1789 Subordo Psillinea Latreille, 1807 Subordo Aleyrodinea Newman, 1834 Subordo Aphidinea Latreille, 1802 Subordo Coccinea Fallén, 1814 (= Coccoidea auct., Gallinsecta De Geer, 1776) Superfamilia Orthezioidea Amyot et Serville, 1843 (= Paleococcoidea Borchsenius, 1950; = Archeococcidea Bodenheimer, 1952) Superfamilia Coccoidea Fallén, 1814 = Neococcoidea Borchsenius, 1950; = Neococcidea Bodenheimer, 1952)

MATERIAL superfamily Orthezioidea, and try to clearly interpret the characters as plesiomorphic, The paper is based on the scale insect apomorphic, and synapomorphic for higher collection of Zoological Institute, Russian taxa of scale insects. In general, we will ei- Academy of Sciences, St Petersburg (ZIN), ther use well known morphological charac- including species from all the scale insect ters studied in detail, which were already in- groups noted or discussed in this paper; in volved many times in phylogenetic studies particular, sixteen species of Puto and four [for example, in the monograph of Danzig of Ceroputo. (1986) or in the special paper of Miller & Miller (1993)], or provide the consideration RESULTS AND DISCUSSION of some less studied characters, such as, for example, eyes in males, sensory pores, etc. There is no need to provide here the general morphological description of Puto Symplesiomorphic characters of Puto or Pseudococcidae, or Coccinea. This and all scale insects (Coccinea) has been done many times in special coccidological literature as well as in the dis- Genetic system. The genetic system XX- cussed paper of Williams et al. (2011). In X0 is an ancient character of Paraneoptera the same paper the history of taxonomic (Blackman, 1995), present in all suborders conceptions of Puto was also provided. It is of Homoptera. However, it can evolve from interesting that Williams et al. (2011), as its original condition to more complicated well as some other authors (for example, genetic systems. So, in the studied Orth- Hodgson & Foldi, 2006), consider Puto in ezioidea this system evolves also to XX- a separate family “Putoidae” with the au- X0 with multiple sex chromosomes, diplo- thorship of Beardsley, 1969. However, any diploid (2n–2n) and hermaphroditism description or diagnosis of “Putoidae” are (Hughes-Schrader, 1948; Nur, 1980; Nor- absent in the paper of Beardsley, 1969. The mark, 2003; Gavrilov, 2007). In the studied cited author simply mentioned “Putoidae” Coccoidea, the XX-X0 system is demon- once in the paper during consideration of strated by Puto only; the other groups show phylogenetic relationships of Puto and oth- systems with paternal genome elimination er genera of scale insects. So, according to (Lecanoid, Comstockioid, and Diaspidoid) Article 13 of the Code, the name “Putoidae or diplo-diploidy (in Stictococcidae and in Beardsley, 1969” must be considered an un- Lachnodius Maskell, 1898 from Eriococci- available name (nomen nudum). It seems dae) (Hughes-Schrader, 1948; Nur, 1980; that Tang (1992) was the first to provide di- Normark, 2003; Gavrilov, 2007). agnosis of a family group taxon with a name Hitherto, only five American and one Pa- based on the genus Puto; he considered this laearctic species of the genus Puto have been taxon as a tribe Putoini within Pseudococ- studied cytogenetically (Hughes-Schrader, cidae and in addition to Puto, Tang also 1944; Brown & Clevelend, 1968; Gavrilov- included in the tribe the following genera: Zimin, 2011) and no species have been stud- Ceroputo; Artemicoccus Balachowsky, 1953; ied in Ceroputo. In general only about 6% of Coccidohystrix Lindinger, 1943; Rastrococ- Coccoidea species have been studied cyto- cus Ferris, 1954; Berendracoccus Ali, 1975 genetically till now (for review see Gavrilov, synonymised with Phenacoccus Cockerell, 2007) and so, unfortunately, we cannot say 1893 by Williams (2004). if the ancient system XX-X0 remains in Below, we will discuss the characters Puto only or it will be found in the future in used by Williams et al. (2011) for substan- other mealybugs or in other still unstudied tiation of the placement of Puto in a separate groups from numerous families of Coccoi- family outside of Pseudococcidae and in the dea. So, the XX-X0 system as a taxonomic

© 2012 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 21(1): 97–111 102 I.A. GAVRILOV-ZIMIN & E.M. DANZIG. TAXONOMIC POSITION OF THE GENUS PUTO character cannot be used for the separation of Putoidae, not only because it is a plesio- morphy of all Paraneoptera, but also because the distribution of this character is not clear within the superfamily Coccoidea. A similar situation takes place now with Thysanop- tera. As it was shown recently (Brito et al., 2010), these insects preserve plesiomorphic monocentric chromosomes in contrast to all the other Paraneoptera groups which have holocentric chromosomes. However, as we know, nobody excludes Thysanoptera from Paraneoptera, but all specialists consider them as a sister group to Arthroidignatha (= Hemiptera s. str.). Eyes of males. Some morphological terms related to the eyes of scale insects probably need to be clarified. In the modern coc- Fig. 2. Structure of stemma in the male of Plano- cidological literature two terms are usually coccus citri, microtomal dissection [reproduced used: compound eyes (consisting of numer- from Krecker (1909)]. ous ommatidia located close to each other) and ocelli (simple eyes). It is well known nated by a special term “stemmata” (Weber, that the compound eyes and ocelli are in- 1933; Torre-Bueno, 1989). The structure nervated from different (lateral and medial, of the eye of the male of Planococcus citri correspondingly) parts of the cerebrum and (Risso, 1813) illustrated by Krecker (1909) that the number of ocelli is not greater than (Fig. 2) is rather similar to, for example, lar- three in all insects. In scale insects the ocelli val stemma of Cicindela Linnaeus, 1758 (Co- are fully absent (Emeljanov, 1987). Howev- leoptera) (Weber, 1933: fig. 304): a group of er single unicorneal eyes [accessory and pri- retinal cells covered by a single cornea. In mary (larval) eyes, in the terminology of old the collection of ZIN we have found a series authors], being elements of compound eyes, of microtome slides prepared many years are also often referred to as “ocelli” by coc- ago by T.N. Bustshik from the males of Lich- cidologists; it leads to the mixing of terms tensia viburni Signoret, 1873. The internal and misunderstanding. Unfortunately, we structure of the eyes of this species appears do not know any comparative anatomical similar to that of P. citri. Moreover, Krecker studies of eyes in scale insect males in addi- (1909) revealed that nerves from all eyes tion to the old work of Krecker (1909), but of P. citri are connected with “lateral lobes it seems that the compound eyes of scale in- of the supraoesophageal ganglion”, which sects differ from the usual compound eyes of unambiguously supports the presumption other insects, because single unicorneal ele- of absence of ocelli in scale insects. This ments of scale insect compound eyes lay not character can be considered as an apomor- close to each other but with clear gaps and phy of the Coccinea. The reduction of the have a tendency to be reduced in number number of unicorneal eyes in imago and (down to only one unicorneal eye on each larvae seems to be the general character of side of the head of imago). Coccinea+Aphidinea+Aleyrodinea. The same reduction is also known in For many years it has been tradition- Myriapoda, Entognatha and in larvae of dif- ally accepted that two superfamilies of scale ferent groups of Ectognatha (Kluge, 2000), insects, Orthezioidea and Coccoidea, differ and such reduced inicorneal eyes are desig- correspondingly in the presence or absence

© 2012 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 21(1): 97–111 I.A. GAVRILOV-ZIMIN & E.M. DANZIG. TAXONOMIC POSITION OF THE GENUS PUTO 103 of compound eyes. However, at present, Other morphological characters of males. when significant additional data on scale Unfortunately, only two male organs (eyes insects male morphology have been pub- and aedeagus) of different Puto species were lished (Hodgson & Foldi, 2006), it is dif- comparatively analyzed in the paper of Wil- ficult to distinguish true compound eyes liams et al. (2011). The shape of aedeagus from stemmata, because the number of uni- was noted as having two different condi- corneal eyes varies very significantly (from tions (bifid and simple) and varying within 0 to 150 for Coccinea as a whole) between Puto s. str. as shown in Williams et al. (2011: the genera of Orthezioidea as well as within table 1). As for other papers, detailed mor- Coccoidea, but Orthezioidea usually have phological descriptions have been provided a greater number of the eyes. On the other till now for only one species of Puto (P. yuc- hand, males of such genera as Stigmacoccus cae Coquillett, 1890) and one species of Hempel, 1900, Phenacoleachia Cocckerell, Ceroputo (C. pilosellae Šulc, 1898) (Afifi, 1899, Steingelia Nassonov, 1908, Pitycoccus 1968; Hodgson & Foldi, 2006). Moreover, McKenzie, 1942, and Stomacoccus Ferris, it should be noted that nobody described 1917 [all these genera are traditionally in- any males of Ceroputo before or after Afifi cluded in the Orthezioidea; see, for exam- (1968) and we cannot exclude that the ma- ple, Morrison (1928) and Danzig (1986)] terial used by Afifi (Yugoslavia: Belgrade, retain only 36, 16, 14, 10, and 2 stemmata, on Fragaria vesca, 30 Sept. 1961, coll. N. respectively (Hodgson & Foldi, 2006). Mitic-Muzina) was in reality males of Phe- In Coccoidea we also see variation of nacoccus sp. inhabiting the same place as the unicorneal eye number in males, from females of Ceroputo pilosellae. Meanwhile, two to ten stemmata (Giliomee, 1967; Afifi, Ch. Hodgson [personal communication and 1968), but very few species (may be several paper of Hodgson & Foldi (2006)] supposes percent of the total number) of Coccoidea that the following characters of P. yuccae are studied in terms of male morphology can be used to separate it from Ceroputo and till now. According to the paper of Wil- even from other mealybugs. liams et al. (2011), different species of Puto 1) Special collared and satellite setae are have from 5 to 8 pairs of stemmata. So, even present; mesothoracic furca is very similar within Puto s. str. we see significant varia- to that in monophlebids; anterior position tion of the discussed character. Also, from of anus is on peneal sheath; usually four the paper of Williams et al. (2011) it seems hamuli on each hamulohaltere; four or five that there is a clear hiatus in the stemmata campaniform sensilla on trochanter are number between Puto s. str. (5–8 pairs) and present. [These characters are clearly ple- Ceroputo + other mealybugs (1–3 pairs). siomorphic because they are present also in However, Goux (1931) noted that males of different Margarodidae s. l.; the last 2 char- Heliococcus radicicola Goux, 1931 (Pseu- acters vary significantly between genera of dococcidae) had 4 pairs of unicorneal eyes. Margarodidae s. l. in addition (I.G.-Z. and So, any hiatus in this character in Pseudo- E.D.)]. coccidae s.l. is absent, and we see a whole 2) Claw denticle is exceptionally large row of variability from one to eight pairs of [the size of claw denticle varies significantly stemmata in the family. In general, based within Pseudococcidae s. str. (I.G.-Z. and on all the above-mentioned facts, we can be E.D.)]. sure that reduction of the compound eyes 3) Antennal segments show some sign of and the number of unicorneal eyes evolved nodulations on more apical segments [the separately many times in different groups of character does not have a taxonomic signifi- scale insects and that this character cannot cance to our mind; it varies within Marga- be used as an apomorphy of Coccoidea and rodidae s. l. and within Pseudococcidae; see all the more, of Puto. for example, figure 13 showing the anten-

© 2012 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 21(1): 97–111 104 I.A. GAVRILOV-ZIMIN & E.M. DANZIG. TAXONOMIC POSITION OF THE GENUS PUTO nae of Heliococcus radicicola in the paper of insect superfamilies and even within the ge- Goux (1931) (I.G.-Z. and E.D.]. nus Puto s. str., and sometimes even within a 4) Genae are absent (as in Margarodidae population [types of Puto (Ceroputo) grami- s. l.) [the character is plesiomorphic and con- nis Danzig, 1972]. nected directly with the degree of reduction The number of antennal segments in first- of ocular sclerite; in majority of Orthezioidea instar larva. This number is seven for most the ocular sclerite and compound eyes cover studied species of Puto (Williams et al., most part of the male head; when reduction 2011). However, not all species of the genus of compound eyes takes place, the head sur- were studied till now because of the absence face not occupied with eyes looks as genae of first-instar larvae in the available collec- (I.G.-Z. and E.D.)]. tions. It was also noted by Williams et al. Thus, all these additional and very poor- (2011) that “in all mealybugs (Pseudococ- ly studied male characters demonstrate (as cidae), the number of antennal segments in do the characters of adult females) either first-instar nymphs is six at most (Miller, plesiomorphic condition or intergeneric 1991)”. This statement seems to be rather variation which obviously will increase strange, because many (maybe most) mor- in the course of more intensive studies of phological descriptions of mealybug species mealybug males. (and Coccinea in general) do not include Trochanter campaniform sensilla of adult information about immature stages. So, females. These sensilla are present in nu- we cannot say about mealybugs in general. merous scale insects from different families, Moreover, the number of antennal segments but in view of the absence of special his- in scale insects is one of the most variable tological studies it is not clear if these or- morphological characters; it often varies gans have the same origin as campaniform even individually within the same popu- sensilla of other insects (Koteja, 1974; De lation. For example, Williams et al., 2011 Lotto, 1979). The number of trochanter noted that first-instar larva of Ceroputo sensilla varies in scale insects significantly pilosellae Šulc, 1898 (type species of Cero- between higher taxa as well as between puto) had 6-segmented antennae, but Rey- species of the same genus (Morrison, 1928; ne (1954: p. 319) wrote about 7-segmented De Lotto, 1979; Williams et al., 2011). The antennae in the same species. So, this char- highest variation is known for Margarodi- acter cannot be used for any taxonomic de- dae s. l., from two to sixteen sensilla on each cisions in higher taxa. side of the trochanter (Morrison, 1928). For Ortheziidae, 3–4 pores on each side Synapomorphic characters of Puto of trochanter are known (Kozár, 2004). In with all Coccoidea (= Neococcoidea) the Pseudococcidae s. l., the variation from one to four pores on each side of trochan- Abdominal spiracles. They are not de- ter is known (De Lotto, 1979; Williams et tected in Puto as in all Coccoidea (Danzig, al., 2011). The same range of variation was 1986; Hodgson & Foldi, 2006). Among shown by Williams et al. (2011) for 49 spe- Orthezioidea, only Phenacoleachia spp. cies of Puto s. str. As for other mealybugs, have lost abdominal spiracles in the females, it seems that they usually demonstrate two but these spiracles are present in the males sensilla on each side of trochanter, exclud- with perfectly visible tracheae branched ing Lenania De Lotto, 1979 with three sen- to the abdominal margins (Theron, 1962; silla (Williams et al., 2011). So, the higher Hodgson & Foldi, 2006). number of the discussed sensilla in some Parasitism of Hymenoptera wasps. There (but not in all) species of Puto s. str. is a are numerous genera and species of parasit- plesiomorphic character that has an evolu- ic Hymenoptera more or less strongly asso- tionary tendency of decreasing in both scale ciated with respective host species of Coc-

© 2012 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 21(1): 97–111 I.A. GAVRILOV-ZIMIN & E.M. DANZIG. TAXONOMIC POSITION OF THE GENUS PUTO 105 coidea. On the other hand, parasitic wasps bugs (Pseudococcidae s. l.). All species of are almost not known for Orthezioidea Puto have a number (at least 18 pairs) of (Rosen & DeBach, 1977; Trjapitzin, 1989). very well developed cerarii. Rosen & DeBach (1977) wrote: “although Simple tubular ducts. These ducts, pres- large gap in our knowledge exists, it ap- ent in mealybugs including Puto, differ pears as though the association of parasitic significantly in their structure from other Hymenoptera and scale insects has evolved types of ducts that are present in some only after the Neococcoidea was completely Orthezioidea and in different families of separated from the Archeococcoidea”. At Coccoidea. present, two species of Encyrtidae from two Unpaired ventral mycetome. The pres- different genera are known as parasites of P. ence of this structure is a unique synapo- yuccae (see in Scalenet, 2012) that was con- morphy discovered by P. Buchner (1965). sidered by Williams et al. (2011) as a real The reasoning of some authors (Downie & Puto. These two species are Aenasius maplei Gullan, 2004; Hardy et al., 2008) concern- Compere, 1937 and Anagyrus yuccae (Co- ing the presence of different symbiotic bac- quillett, 1890). All the species of the large teria in Puto and in other mealybugs is not genera Aenasius Walker, 1846 (42 species) actual for the present discussion, because and Anagyrus Howard, 1896 (270 species) new, more comprehensive studies (Gruwell are parasites of different mealybugs includ- et al., 2010) have appeared. It is clear now ing Puto and do not live in other scale in- that all morphologically different groups sects, with very rare exceptions of Eriococ- of mealybugs have different symbiotic bac- cidae and Stictococcidae species, and never teria. Moreover, the same bacteria can be in Orthezioidea (Universal Chalcidoidea found in very phylogenetically distant or- Database, 2012). Thus, parasitic wasps of ganisms, as for example, Spiroplasma spp. in these genera do not “see” any difference be- Puto and in Drosophila Fallén, 1823 (Dip- tween Puto and other mealybugs but “see” tera). the difference between Pseudococcidae s. l. and other scale insects. Synapomorphic characters of Puto with Ceroputo Synapomorphic characters of Puto with Pseudococcidae (Coccoidea) and Morphological characters. Dorsal and Phenacoleachiidae (Orthezioidea) ventral trilocular pores are different in size. Eye height is as great as length of the first Trilocular pores and ostioles. Presence of antennal segment. All cerarii are with nu- these well-studied structures only in these merous conical setae. families probably testify to the origin of Ovoviviparity. Ovoviviparity is widely Pseudococcidae directly from Phenacole- distributed within Coccoidea and very achidae or the origin of both families from rarely, in several species only (Phenacole- a common Orthezioidea ancestor (Danzig, achia zealandica, in particular), present in 1986; Cox, 1983). Moreover, Phenacole- Orthezioidea (Gavrilov & Trapeznikova, achia zealandica (Maskell, 1891) demon- unpublished). All species of Puto and Cero- strates ovoviviparity as do Puto, Ceroputo puto, as well as all or most species of simi- and numerous other genera of Pseudococ- cidae (see below). lar genera of Phenacoccini mealybugs, such as Heliococcus Šulc, 1912, Coccura Šulc, Synapomorphic characters of Puto 1908, Fonscolombia Lichtenstein, 1877, and with Pseudococcidae Phenacoccus are characterized by obligate ovoviviparity (Trapeznikova & Gavrilov, Cerarii. The presence of cerarii is a 2008; Trapeznikova, 2011; Gavrilov & Tra- unique apomorphic character of all mealy- peznikova, unpublished).

Character of unclear groups, and by Gullan et al. (2010) for the phylogenetic significance genus Ferrisia Fullaway, 1923. Unfortunately, the use of DNA sequenc- Claw basal spurs. These spurs are pres- ing to reveal relationships between higher ent in most (but not in all) species of Puto taxa now seems to be rather far from the and in Ceroputo mimicus (McKenzie, 1967) reconstruction of real phylogenies [see, for and C. nulliporus (McKenzie, 1960) (Wil- insects in general, the paper of Rasnitsyn liams et al., 2011). If we consider the genus (2010), for example]. For us personally, the Puto in the traditional sense, we can see that main practical problems of this method of this character has geographic variation: all phylogenetic reconstructions of higher taxa the New World species have the spurs, but are the following. in the Palaearctic species the spurs can be 1) The molecular cladograms are not present or absent. There is no special study easily testable in practice; we can only be- of this character in other Coccinea, but a lieve or not believe their data (in contrast to somewhat similar structure is present, for cladograms based on concrete phenotypic example, in Macropulvinaria Hodgson, characters). 1968 [C.H. Hodgson, pers. comm., cit. after 2) When higher taxa are considered, Williams et al. (2011)]. the molecular cladograms, in fact, extrapo- late the data of one or several species from The data of DNA sequencing a particular genus to this genus as a whole. This is probably an acceptable admission for The data of DNA sequencing for analy- small, morphologically homogeneous gen- sis of relationships between organisms are era but, to our mind, this is not acceptable widely used now in different fields of biol- for large, taxonomically difficult genera like ogy and medicine. It is not possible to dis- Puto, Phenacoccus or Trionymus Berg, 1899. cuss here all the particular advantages and 3) DNA sequencing does not operate disadvantages of this approach; they are with huge numbers of species or genera of considered in numerous special papers [see, higher taxa, because it requires fresh and for example, Lukhtanov (2010)]. In general, adequately fixed material for sequencing, the construction of molecular cladograms meanwhile the majority of described spe- is mainly based on the so-called “molecu- cies of Coccinea were collected during the lar clock” hypothesis, which assumes that last 100 and more years and preserved in nucleotide sequences of analyzed genes in numerous museums as specially prepared different organisms evolve with the same Canada-balsam slides. speed due to random mutations. This These problems, in combination with “clock” works more or less correctly when the methodological problems of computer recently diverged groups are compared, for statistical analysis itself [see discussion in example, groups of individuals, populations Lukhtanov (2010)], often lead to the ap- or related species within the same genus. pearance of absolutely bizarre clades which In these cases all or most members of the contradict to all other scientific data on analyzed group can be representatively in- studied taxa. A good example of such bizarre volved in the same study and, in combina- cladograms we can see, for example, on page tion with analysis of other taxonomic char- 49 of the paper of Cook et al. (2002). The acters, the DNA sequencing seems to pro- cladogram presented includes only 19 spe- vide good results, as shown for many genera cies of scale insects from different families of plants and animals. In scale insects, such and suggests that Eriococcus aceris Signoret, a combined taxonomic approach was used 1875 (Eriococcidae) is more “related” to recently by Unruh & Gullan (2007) for the Aonidiella aurantii (Maskell, 1879) (Dias- genus Icerya Signoret, 1876 and related pididae) than to Eriococcus buxi (Fonscol-

© 2012 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 21(1): 97–111 I.A. GAVRILOV-ZIMIN & E.M. DANZIG. TAXONOMIC POSITION OF THE GENUS PUTO 107 ombe, 1834); that Othezia urticae (Linnae- Conclusion on the genus Puto us, 1758) (Ortheziidae) and Puto yuccae are and “family Putoidae” in the same clade, and that Phenacoleachia zealandica is not placed within Coccinea The summarizing of all the above facts, but occupies the “outgroup” position, like including the synapomorphies of Puto with Ceroputo and the evident absence of clear Phylloxera notabilis Pergande, 1904 (Aphi- diagnostic characters for separation of dinea). In any traditional phylogenetic adult females of these taxa, leads us to ac- study this cladogram would be considered a cept Ceroputo as not higher than a subgenus mere artefact, but in the discussed paper it of Puto in the tribe Putoini Tang, 1992. In was provided as one of the scientific results. this case the identification key may be the The second cladogram presented in the following. same paper (fig. 1 on p. 48), includes 39 species of scale insects and seems to be slightly 1(2) More than five pairs of unicorneal eyes more realistic, but as for Puto, the authors present in adult males. First instar larvae with 7-segmented antennae. Sensilla on each have deduced (on p. 50): “The phylogenet- side of female trochanter are usually 3–4 in ic placement of Puto remains unresolved”. number, rarely 2 (as an intraspecific varia- However, in a subsequent paper on molecu- tion only) ...... subgenus Puto lar sequencing of scale insects, Downie & 2(1) Three pairs of unicorneal eyes present in Gullan (2004) state, with reference to Cook adult males. First instar larvae with 6-seg- et al. (2002) and Hodgson (2002), that mented antennae (7-segmented as an intra- “Puto is clearly a separate family” (p. 251), specific variation only). Sensilla on each side of female trochanter are 2 in number, rarely 1 even though the position of Puto on the new or 3 [in P. (C). graminis] ...... cladogram in the paper of Downie & Gullan ...... subgenus Ceroputo (2004) is the same as in the older cladogram of Cook et al. (2002), i.e., unresolved. The So, to our mind, Putoidae as a separate genus is not placed there in the same clade family placed in the superfamily Orthezioi- with other studied species of mealybugs, nor dea (= an informal group of “archeococcids”) is a taxonomic paradox that lies outside of in the clade with any other scale insect fam- both cladistic and evolutionary concepts in ily. The data of Hodgson (2002) on the mor- taxonomy and ignores the majority of well phological characters were discussed above. known and carefully proven facts. There is The recent cladorgam of Hardy et al. not a single apomorphic character in Put- (2008) analyses 33 species using DNA se- oidae; all characters of the genus Puto are quencing [in addition to the species studied plesiomorphies with all scale insects or sy- by Downie & Gullan (2004)] in combina- napomorphies with other mealybugs or with tion with morphological cladistic comput- the closely related Ceroputo. Putoidae as a er analysis of “adult females of 35 species, separate family is evidently a paraphyletic first-instar nymphs of 28 species, and adult taxon that does not include all descendants males of 20 species”. Only 35 species were of Puto, i.e., Ceroputo and other mealybugs. studied morphologically, whereas adult This paraphyly is not a problem for us, but females of all 2000 species of mealybugs it seems that it is not a problem for some and 6000 species of other scale insects pre- cladistic authors either. Now, this is the best served in museums, are available for mor- time to remember the splendid words of one phological analysis. The combined clador- of the co-authors of the paper by Williams gam of Hardy et al. (2008) seems to us to be et al. (2011), P.J. Gullan: “Ideally, all higher more realistic than those in the two previ- taxa should be monophyletic because natu- ously discussed papers, but the position of ral groups provide an unambiguous repre- Puto remains here absolutely the same, i.e., sentation of relationships…” and “Homop- unresolved. tera might not be monophyletic because all

© 2012 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 21(1): 97–111 108 I.A. GAVRILOV-ZIMIN & E.M. DANZIG. TAXONOMIC POSITION OF THE GENUS PUTO diagnostic features used to separate it from str., which really has a number of plesiomor- the Heteroptera are all plesiomorphies…” phic characters, Pennygullania bears only (Gullan, 1999: “Why taxon Homoptera does apomorphic characters of Coccoidea and not exist”). Due to these recommendations, Pseudococcidae: two pairs of stemmata, two we believe that in the present paper we pro- pairs of tail setae, remains of wax secretions vide the answer to the question: why the of trilocular and multilocular pores in larva. taxon Putoidae does not exist. So, we consider Pennygullania as one of the Finally, we present our conception of ancient genera within Pseudococcidae. the taxonomic position of Puto (subordo Coccinea: superfamilia Coccoidea: familia ACKNOWLEDGEMENTS Pseudococcidae: subfamilia Phenacoccinae: tribe Putoini: genus Puto: subgenus Puto, The authors thank all colleagues who partici- subgenus Ceroputo). pated in the discussion on the present paper, especially Dr Ferenc Kozár, Dr Giuseppina Pelliz- zari, Dr Christopher Hodgson, Dr Boda Kaydan, Fossil family Pennygullaniidae Dr Douglas Williams, Dr Penny Gullan, Dr Dmi- Koteja et Azar, 2008, syn. nov. try Gapon, Dr Alexander Emeljanov, Dr Dmi- try Scherbakov, Dr Denian Kondo, Dr Dmitry The fossil species Pennygullania electrina Dmitriev, Dr Valentina Kuznetsova and oth- Koteja et Azar, 2008, described on the basis ers. The work of I. G.-Z. was partly supported of remains of one adult male and a probably by the Russian Foundation for Basic Research congeneric larva in Lower Cretaceous am- (grant no. 11-04-00734-а) and by special grants ber, was placed in the original paper in the of St Petersburg government. The collection of new monotypic genus and monotypic family Zoological Institute of Russian Academy of Sci- ences was financially supported by the Ministry Pennygullaniidae, which in the judgment of of Education and Science of the Russian Federa- Koteja & Azar (2008) “seems to represent a tion (project no. 16.518.11.7070). special branch of neococcids”. However, any special description or differential diagnosis REFERENCES of the family were not provided by Koteja & Azar (2008). The differential diagnosis Afifi S. 1968. Morphology and taxonomy of the of the genus Pennygullania Koteja et Azar, adult males of the families Pseudococcidae 2008 was presented as follows: “slim neococ- and Eriococcidae (Homoptera: Coccoidea). cid with two pairs of simple eyes, slender Bulletin of the British Museum (Natural His- appendages bearing very long setae, solid tory). Entomology. Supplement, 13: 3–210. scutum, thochanter and femur fused, two Beardsley J.W. 1969. A new fossil scale insect (Homoptera: Coccoidea) from Canadian am- pairs of strong tail setae (with two setae in ber. Psyche, 7: 270–279. each group), penial sheath of coccid s. str. Blackman R.L. 1995. Sex determination in in- type” (Koteja & Azar, 2008). Plate 17b in sects. In: Leather S.R. & Hardie J. (Eds) In- the discussed paper, in contrast to the text sect Reproduction. Boca Raton: CRC Press. description, clearly demonstrates that the 255 p. thochanter and femur of the male are not Bodenheimer F.S. 1952. The Coccoidea of Tur- fused. Moreover, these two parts of legs in key. I. Revue de la Faculté des Sciences de scale insects often lie close to one another, so l’Université d’Istanbul (Ser. B), 17: 315–351. that the border between them can be poorly Borchsenius N.S. 1950. Koktsidy SSSR [Scale visible in fossil individuals. Other characters Insects of the USSR]. Moscow–Leningrad: Akademiya Nauk SSSR, Zoological Insti- noted in the diagnosis and in the descrip- tute. 250 p. (In Russian). tion of a probably congeneric larva do not Börner C. 1904. Zur Systematic der Hexapoden. demonstrate, to our mind, anything differ- Zoologischer Anzeiger, 27: 511–533. ent from the morphological characteristics Brito R.O., Affonso P.R.A.M. & Silva Jr. J.C. of Pseudococcidae. In contrast to Puto s. 2010. Chromosomal diversity and phyloge-

netic inferences concerning thrips (Insecta, Forero D. 2008. The systematics of the Hemip- Thysanoptera) in a semi-arid region of Bra- tera. Revista Colombiana de Entomologia, sil. Genetics and Molecular Research, 9(4): 34(1): 1–21. 2230–2238. Gavrilov I.A. 2007. A catalogue of chromosome Brożek J., Szwedo J., Gaj D. & Pilarczyk S. numbers and genetic systems of scale insects 2003. Former and current views on the clas- (Homoptera: Coccinea) of the world. Israel sification of the bugs (Insecta, Hemiptera). Journal of Entomology, 37: 1–45. Genus. Supplement: 85–100. Gavrilov-Zimin I.A. 2011. New cytogenetic Brown S.W. & Cleveland C. 1968. Meiosis in the data for some Palaearctic species of scale male of Puto albicans (Coccoidea–Homop- insects (Homoptera: Coccinea) with karyo- tera). Chromosoma (Berlin), 24: 210–232. systematic notes. Comparative Cytogenetics, Buchner P. 1965. Endosymbiosis of animals with 5(5): 375–390. plant-like microorganisms. New-York: John Giliomee J.H. 1967. Morphology and taxonomy Wiley & Sons. 909 p. of adult males of the family Coccidae (Ho- Campbell B.C., Steffen-Campbell J.D, So- moptera: Coccoidea). Bulletin of the British rensen J.T, Gill R.J. 1995. Paraphyly of Ho- Museum (Natural History). Entomology. Sup- moptera and Auchenorrhyncha inferred from plement, 7: 1–168. 18 S rDNA nucleotide sequences. Systematic Gorochov A.V. 2001. On some theoretical as- Entomology, 20: 175–194. pects of taxonomy (remarks by the practical Cook L.G., Gullan P.J. & Trueman H.E. 2002. taxonomist). Acta Geologica Leopoldensia, A preliminary phylogeny of the scale insects 24(52/53): 57–71. (Hemiptera: Sternorrhyncha: Coccoidea) Goux L. 1931. Notes sur les coccides [Hem.] de based on nuclear small-subunit ribosomal la France (3e note). Description d’une espèce DNA. Molecular Phylogenetics and Evolution, nouvelle. Bulletin de la Société Entomologique 25(1): 43–52. de France, 8: 113–118. Cox J.M. 1984. Relationships of the Phenacole- Gruwell M.E., Hardy N.B., Gullan P.J., Dit- achiidae (Homoptera: Coccoidea). Proceed- tmar K. 2010. Evolutionary relationships ings of the 10th International Symposium of among primary endosymbionts of the mealy- Central European Entomofaunistics, Buda- bug subfamily Phenacoccinae (Hemiptera: pest, 15–20 August 1983: 339–341. Bupadest. Coccoidea, Pseudococcidae). Applied and En- Danzig E.M. 1986. Coccids of the Far-Eastern vironmental Microbiology, 76(22): 7521–7525. USSR (Homoptera: Coccinea). Phylogenetic Gullan P.J. 1999. Why the taxon Homoptera analysis of coccids in the world fauna. New does not exist. Entomologica (Bari), 33: 101– Delhi: Amerind Publishing Co. 450 p. 104. D’Urso V. 2002. The wing-coupling apparatus Gullan P.J., Kaydan M.B. & Hardy N.B. 2010. of Hemiptera Auchenorrhyncha: structure, Molecular phylogeny and species recogni- function, and systematic value. Denisia, 4: tion in the mealybug genus Ferrisia Fullaway 401–410. (Hemiptera: Pseudococcidae). Systematic De Lotto G. 1979. On two podal features in Entomology, 35: 329–339. mealybugs (Homoptera: Coccinea). Journal Hardy N.B., Gullan P.J. & Hodgson C.J. 2008. of the Entomological Society of Southern Af- A subfamily-level classification of mealybugs rica, 42(1): 11–15. (Hemiptera: Pseudococcidae) based on in- Downie D.A. & Gullan P.J. 2004. Phylogenetic tegrated molecular and morphological data. analysis of mealybugs (Hemiptera: Coc- Systematic Entomology, 33: 51–71. coidea: Pseudococcidae) based on DNA se- Hamilton K.G.A. 1981. Morphology and evo- quences from three nuclear genes, and a re- lution of the rhynchotan head (Insecta: He- view of the higher classification. Systematic miptera, Homoptera). The Canadian Ento- Entomology, 29(2): 238–259. mologist, 113(11): 953–974. Emeljanov A.F. 1987. Phylogeny of cicadas (Ho- History of Insects. 2002. A.P. Rasnitsyn & moptera, Cicadina) based on comparative D.L.J. Quicke (Eds). New York, Boston, morphological studies. Trudy Vsesoyuznogo Dordrecht, London, Moscow: Kluwer Aca- Entomologicheskogo Obschestva [Proceed- demic Publishers. 517 p. ings of the Entomological Society of USSR], Hodgson C.J. 2002. Preliminary phylogeny of 69: 19–109. (In Russian). some non-margarodid Coccoidea (Hemip-

tera) based on adult male characters. Bol- Latreille P.A. 1810. Considérations générales lettino di Zoologia Agraria e di Bachicoltura sur l’orde naturel des animaux composant les (Milano), 33(3), 2001: 129–137. classes des Crustacés, des Arachnides, et des Hodgson C.J. & Foldi I. 2006. A review of the Insectes. Avec un tableau méthodique de leurs Margarodidae sensu Morrison (Hemiptera: genres, disposés en familles. Paris: F. Schoell. Coccoidea) and some related taxa based on 444 p. the morphology of adult males. Zootaxa, Linnaeus C. 1758. Systema Naturae, per regna 1263: 1–250. tria naturae, secundum classes, ordines, gen- Hołyński R.B. 2005. Philosophy of science from era, species cum characteribus, differentiis, taxonomist’s perspective. Genus, 16(4): 469– synonymis, locis. Holmiae: Laurentii Salvii. 502. 824 p. Hughes-Schrader S. 1944. A primitive coccid Lukhtanov V.A. 2010. From Haeckel’s phyloge- chromosome cycle in Puto sp. Biological Bul- netics and Hennig’s cladistics to the method letin, 87: 167–176. of maximum likelihood: Advantages and lim- Hughes-Schrader S. 1948. Cytology of coccids itations of modern and traditional approach- (Coccoidea–Homoptera). Advances in Ge- es to phylogeny reconstruction. Entomologi- netics, 2: 127–203. cal Review, 90(3): 299–310. Kerzhner I. & Danzig E. 2001. Hemiptera, Ho- Mayr E., Ashlock P.D. 1991. Principles of sys- moptera, Sternorrhyncha. Bolletino Di Zoolo- tematic zoology. New York: McGrow Hill gia Agraria E Di Bachicoltura (Ser. II), 33(3): Book Co. 475 p. 217–218. Mayr E. 1974. Cladistic analysis or cladistic Kluge N.J. 2000. Sovremennaya systematika classification? Zeitschrift für Zoologische nasekomykh [Modern systematics of insects]. Systematik und Evolutionsforschung, 12(2): St. Petersburg: Lan’. 332 p. (In Russian). 94–128. Kluge N.J. 2010a. Circumscriptional names Meyers J.G. & China W.E. 1929. The systematic of higher taxa in Hexapoda. Bionomina, 1: position of Peloridiidae as elucidated by a fur- 15–55. ther study of the external anatomy of Hemio- Kluge N.J. 2010b. Paradoxical molting process doecus leai China. The Annals and Magazine in Orthezia urticae and other coccids (Ar- of Natural History, 105(3): 282–294. throidignatha: Gallinsecta) with notes on Miller D.R. & Miller G.L. 1993. A new species systematic position of scale insects. Zoosys- of Puto and a preliminary analysis of the phy- tematica Rossica, 19(2): 78–103. logenetic position of the Puto group within Koteja J. 1974. The occurrence of a campani- the Coccoidea (Homoptera: Pseudococci- form sensillum on the tarsus in the Coccinea dae). Jeffersoniana, 4: 1–35. (Homoptera). Bulletin Entomologique de Po- Morrison H. 1928. A classification of the higher logne, 44: 243–252. groups and genera of the coccid family Mar- Koteja J. 1990. Paleontology, 149–163 pp. In: garodidae. United States Department of Agri- Rosen D. (Ed.) Armored Scale Insects, their Bi- culture Technical Bulletin, 52: 1–239. ology, Natural Enemies and Control. Ser. World Normark B.B. 2003. The evolution of alterna- Crop Pests, 4A. Amsterdam: Elsevier. 384 p. tive genetic systems in insects. Annual Re- Koteja J., Azar D. 2008. Scale insects from view of Entomology, 48: 397–423. Lower Cretaceous amber of Lebanon (He- Nur U. 1980. Evolution of unusual chromosome miptera: Sternorrhyncha: Coccinea). Alave- systems in scale insects (Coccoidea: Homop- sia, 2: 133–167. tera). In: Blackman R.L., Hewitt G.M. & Kozár F. 2004. Ortheziidae of the World. Buda- Ashburner M. (Eds.) Insect Cytogenetics: pest: Plant Protection Institute of Hungar- 97–117. London: Royal Entomological So- ian Academy of Sciences. 525 p. ciety. Krecker F.H. 1909. The eyes of Dactylopius. Pesson P. 1951. Ordre des Homoptères. In: Zeitschrift für Wissenschaftliche Zoologie, 93: Grassé P.-P. (Ed.) Traite de Zoologie. X. In- 73–89. sectes supérieurs et Hémiptéroides: 976–1948. Lambdin P.L. 2001. Discourse on the classifica- Paris: Masson et Cie Éditeur. tion of the scale insects. Bolletino Di Zoologia Rasnitsyn A.P. 2010. Molecular phylogenetics, Agraria E Di Bachicoltura (Ser. II), 33(3): morphological cladistics and fossils. Entomo- 209–213. logical Review, 89(1): 85–132.

Reyne A. 1954. A redescription of Puto anten- Sci. (Biol.), Zoological Institute, Russian natus Sign. (Homoptera, Coccidea). With Academy of Sciences. St Petersburg. 232 p. notes on Ceroputo pilosellae Sulc and Macro- (In Russian). cerococcus superbus Leon. Zoologische Med- Trapeznikova I.V. & Gavrilov I.A. 2008. edelingen Uitgegeven door het Rizksmuseum About ovoviviparity in mealybugs (Ho- van Natuurlijke Historie te Leiden, 32: 291– moptera: Coccinea: Pseudococcidae). Trudy 324. Zoologicheskogo Instituta Rossiskoy Aka- Rohdendorf B.B. 1977. The rationalization of demiya Nauk [Proceedings of the Zoologi- names of higher taxa in zoology. Paleontologi- cal Institute, Russian Academy of Sciences], cal Journal, 11: 149–155. 312(1/2): 43–53. (In Russian with English Rosen D. & DeBach P. 1977. Use of scale-insect summary). parasites in Coccoidea systematics. Bulletin Trjapitzin V.A. 1989. Parasiticheskie Hymenop- of the Virginia Polytechnic Institute and State tera semeistva Encyrtidae Palearktiki [Para- University Research Division, 127: 5–21. sitic Hymenoptera of the fam. Encyrtidae of Scalenet. 2012. Visited 1 March 2012. Available the Palaearctic]. Leningrad: Nauka. 488 p. from: Universal Chalcidoidea Database. 2012. Vis- Signoret V. 1875. Essai sur les cochenilles ou ited 1 March 2012. Available from: Simpson G. G. 1961. Principles of animal taxon- Unruh C.M. & Gullan P.J. 2008. Molecular data omy. New York: Columbia Univ. Press. 247 p. reveal convergent reproductive strategies Šulc K. 1898. Studie o coccidech. II. Sitzungsbe- in iceryine scale insects (Hemiptera: Coc- richte der K. Bohmisch Gesellschaft der Wis- coidea: Monophlebidae), allowing the re- senschaften (1897), 66: 1–19. interpretation of morphology and a revised Tang F.T. 1992. The Pseudococcidae of China. generic classification. Systematic Entomol- Shanxi. 768 p. (In Chinese with English ogy, 33: 8–50. summary). Weber H. 1933. Lehrbuch der Entomologie. Theron J.G. 1962. Structure and relationships Stuttgart: Gustav Fischer Verlag. iv + 726 p. of the male of Phenacoleachia zealandica Williams D.J. 2004. Mealybugs of southern (Maskell) (Hemiptera: Coccoidea). Pro- Asia. Kuala Lumpur. 896 p. ceedings of the Royal Entomological Society Williams D.J., Gullan P.J., Miller D.R., Matile- of London, Ser. A (General Entomology), 37: Ferrero D. & Han S.I. 2011. A study of the 145–153. scale insect genera Puto Signoret (Hemip- Torre-Bueno J.R. de la. 1989. The Torre-Bueno tera: Sternorrhyncha: Coccoidea: Putoidae) glossary of Entomology. New York: New York and Ceroputo Šulc (Pseudococcidae) with a Entomological Society. 840 p. comparison to Phenacoccus Cockerell (Pseu- Trapeznikova I.V. 2011. Reproduktivnye oso- dococcidae). Zootaxa, 2802: 1–22. bennosti i kariosistematika muchnistykh cher- Von Dohlen C.D. & Moran N.A. 1995. Molecu- vetsov (Homoptera: Coccinea) [Reproductive lar phylogeny of the Homoptera: a paraphy- features and karyosystematics of mealybugs letic taxon. Journal of Molecular Evolution, (Homoptera: Coccinea)]. Dissertation Cand. 41: 211–223. Received February 1, 2012 / Accepted June 1, 2012