Table Of ContentZOOSYSTEMATICA 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 “archeo-
coccids”), 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 sub-
genus of Puto. The monotypic fossil family Pennygullaniidae is considered by us a new subjec-
tive 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
© 2012 Zoological Institute, Russian Academy of Scienсes
98 I.A. GAVRILOV-ZIMIN & E.M. DANZIG. TAXONOMIC POSITION OF THE GENUS PUTO
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-
© 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 99
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)
© 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 101
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 coc-
cidological 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-
lar genera of Phenacoccini mealybugs, such
cidae (see below).
as Heliococcus Šulc, 1912, Coccura Šulc,
1908, Fonscolombia Lichtenstein, 1877, and
Synapomorphic characters of Puto
Phenacoccus are characterized by obligate
with Pseudococcidae
ovoviviparity (Trapeznikova & Gavrilov,
Cerarii. The presence of cerarii is a 2008; Trapeznikova, 2011; Gavrilov & Tra-
unique apomorphic character of all mealy- peznikova, unpublished).
© 2012 Zoological Institute, Russian Academy of Scienсes, Zoosystematica Rossica 21(1): 97–111
106 I.A. GAVRILOV-ZIMIN & E.M. DANZIG. TAXONOMIC POSITION OF THE GENUS PUTO
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
