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REDIA, 102, 2019: 113-119
a Instituto de Biología Integrativa de Sistemas (I2SysBio). Universidad de Valencia - CSIC. Centro Mixto Universidad de
Valencia-CSIC (Paterna, Valencia). Spain.
Corresponding Author: Alice Casiraghi; ali.casi@outlook.it
Casiraghi A., Martínez-Torres D., Pérez Hidalgo N. – Confirmation of the presence of Pachypappa warshavensis
(Nasonov, 1894) [Hempitera Aphididae] in the Iberian Peninsula.
The aphid Pachypappa warshavensis (Nasonov) (Aphididae: Eriosomatinae: Pemphigini) on its primary host
Populus alba L. is properly confirmed in the Iberian Peninsula. The species was initially cited as Asiphum varsoviensis
(Mordvilko, 1835) in Spain, but the absence of specimens in the entomological collections, as well as the alleged limited
distribution to the countries of Northern and Eastern Europe, made it removed from the list of the Ibero-Balearic aphids.
P. warshavensis is a Palaearctic species that is widely distributed in Europe (Belarus, Germany, Hungary, Poland,
Romania, Serbia, Spain, Sweden and Ukraine) and Central Asia (Kazakhstan). The identification based on
morphological and molecular characters (COI) has been confirmed and the fundatrix and its winged fundatrigenia are
described. In addition, phylogenetic relationships based on COI sequences of P. warshavensis with other Pachypappa
species available in the databases are presented.
KEY WORDS: Aphids, COI, Populus alba, faunistic studies, Eriosomatinae, Pemphigini.
ALICE CASIRAGHI a - DAVID MARTÍNEZ-TORRES a- NICOLÁS PÉREZ HIDALGO a
CONFIRMATION OF THE PRESENCE OF PACHYPAPPA WARSHAVENSIS
(NASONOV, 1894) [HEMPITERA APHIDIDAE] IN THE IBERIAN PENINSULA
INTRODUCTION
The genus Pachypappa Koch 1856 corresponds to a little
aphid taxon from the Pemphigini tribe (Hemiptera: Aphididae:
Eriosomatinae), that host alternates between species of
Populus L. (the primary host) and different secondary hosts,
not always known, but frequently being different species of
Picea Dietrich (five species) or Salix L. (two species) (PIKE et
al., 2012; BLACKMAN and EASTOP, 2019).
Pachypappa groups 13 species with Holarctic distribution
(FAVRET, 2019). Of these, three are Nearctic (Canada and
United States), and the rest are widely distributed in the
Palaearctic region, from Britain to Japan, or only in a part of
it (BLACKMAN and EASTOP, 2019).
Currently, six species are present in several countries of
Northern and Central Europe: P. marsupialis Koch 1856, P.
myrtilli Börner 1950 (only in Germany), P. populi (Lin -
naeus 1758), P. tremulae (Linnaeus 1761), P. vesicalis Koch
1856 and P. warshavensis (Nasonov 1894) (NIETO NAFRÍA
et al., 2011; BLACKMAN and EASTOP, 2019). The genus is
characterized by large fundatrices without waxy plates and
alatae spring migrants always having wax plates and
forewings generally with a once-branched medial vein
(BLACKMAN and EASTOP, 2019).
Like most species of Pemphigini and other Erioso -
matinae, their full (holocyclic) life cycles are rather
complex and their ability to develop paracycles on sub -
terranean parts of their secondary hosts makes their
taxonomy problematic in some species. However, nowa -
days some of these taxonomic problems can be solved using
molecular studies (PIKE et al., 2012).
In early-June 2018 typical pseudogalls made by
Pachypappa aphid colonies were found on several white
poplars in the city of León (Fig. I). A detailed study of the
fundatrix, and alatae viviparous females revealed that they
belonged to the aphid genus Pachypappa, and more
specifically to Pachypappa warshavensis (Nasonov), a
species that was mentioned for the first time in the Iberian
Peninsula by GÓMEZ-MENOR and NIETO (1977) as Asiphum
varsoviensis (Mordvilko, 1835), currently synonym of P.
warshavensis (Nasonov, 1894). However, the absence of
specimens of this sample in the entomological collections
that could confirm it, the null results after the efforts made
for its location, as well as its limited distribution to the
countries of northern and eastern Europe, made think to
PÉREZ HIDALGO and NIETO NAFRÍA (2003a) that this species
was not present in Spain and that it could be an
identification error.
Our records, therefore confirm definitively the presence
of this species of Pemphigini in the Iberian Peninsula.
MATERIALS AND METHODS
MATERIAL COLLECTED
Aphids were collected on 4-vi-2018 from various plants
of Populus alba L. located between coordinates 42.610522,
-5.590680 and 42.605037, -5.586273, in a green area on the
left bank of the Bernesga river, along a path in the city of
León. Half of the sampled aphids were put in 100% ethanol
for molecular analysis and the other half in 70% ethanol
solution for morphological studies. The aphids (sample
references: 1850 and 1779) and the DNA were deposited in
the aphidological collection of the Institute for Integrative
Systems Biology (Mixt Center of University of Valencia
and CSIC).
MORPHOLOGICAL STUDY
Subsequently, the individuals in 70% ethanol were used
to mount microscope slides following the methodology
– Received 31 May 2019 Accepted 8 October 2019
http://dx.doi.org/10.19263/REDIA-102.19.17
described by NIETO NAFRÍA and MIER DURANTE (1998).
Identification at the species-level was carried out using
quan titative and qualitative characters, following the
identification keys of HEIE (1980) and BLACKMAN and
EASTOP (2019). A camera lucida fitted to the microscope
was used for the drawings and the microphotographs were
taken with a Leica DC digital camera with IM 1000 version
1.10 software.
DNA EXTRACTION AND PCR AMPLIFICATION
The specimens conserved in 100% ethanol were used in
DNA extraction following the HotSHOT method (Hot
Sodium Hydroxide and Tris) (TRUETT et al., 2000). In a
second step, a 710 bp fragment of the 5’ region of the
mitochondrial cytochrome c oxidase subunit 1 (COI) was
amplified using primers LCO1490 and HCO2198 (FOLMER
et al., 1994). 3 µl of the extracted DNA was used for every
amplification. PCR conditions were as follows: 94°C for 1
min; 35 cycles of 94°C for 30 s, 48°C for 1 min and 68°C
for 1 min; a final extension step of 7 min at 68°C was
included after cycling.
SEQUENCING AND ANALYSIS OF DNA SEQUENCES
PCR products were purified by ammonium precipitation
and reconstituted in 10 µL of LTE buffer (10mM Tris,
0,1mM EDTA). Sequencing of the amplified fragments was
done using PCR primers and conducted using the Big Dye
Terminator v3.1 Cycle Sequencing Kit (Applied
Biosystems) following the manufacturer’s instructions.
Samples were loaded onto an ABI 3700 automated
sequencer. Sequences corresponding to each sample were
assembled using Staden package v2.0.0 (STADEN et al.,
1998). Multiple alignments were carried out with Clustal X
v1.81 (THOMPSON et al., 2002) with gap opening and gap
extension penalties of, respectively, 10.0 and 0.2, and then
manually revised. MEGA7 (KUMAR et al., 2016) was used
to align sequences and to do the phylogenetic analysis. The
Neighbor-joining algorithm on Kimura 2-parameters
distances was used to build a phylogenetic tree including
several Pachypappa sequences available at NCBI
(accession numbers MG508635.1, MF830952.1, KR0
29847.1 and GU679671.1) along with the sequence of P.
warshavensis here reported. Node support was obtained
after 500 bootstrap replicates. The sequence of the species
Mordwilkoja vagabunda (Walsh 1863) was used as
outgroup (accession number KR043679.1).
RESULTS
MORPHOLOGICAL DATA
The analysis of qualitative and quantitative (metric and
meristic) characters of the specimens available (one
fundatrix and hundreds of fundatrigeniae viviparous fema -
les) confirmed that they belong to the genus Pachypappa,
because the fundatrix lacks waxy plates and the funda -
trigeniae viviparous females have oval primary rhinaria
surrounded by distinct rings of shorts hairs and small
114 A. CASIRAGHI ET AL. REDIA, Vol. 102, 2019
Fig. I – Several colonies of Pachypappa war -
shavensis (Nasonov) on Populus alba.
CONFIRMATION OF THE PRESENCE OF PACHYPAPPA WARSHAVENSIS (NASONOV, 1894) [HEMPITERA APHIDIDAE] … 115
siphuncular pores, with a diameter shorter than 2.3 times
the articular diameter of antennal segment III (HEIE, 1980).
The association with Populus alba and the presence of
secondary sensoria with thick sclerotic rims on the distal
half of the antennal segment III (Fig. II, 1), among other
characters, identified it as P. warshavensis (Nasonov) (HEIE,
1980; BLACKMAN and EASTOP, 2019).
The only one fundatrix caught is large (4.34 mm) but
with short appendages (antenna of 0.6 mm and 0.14 times
the body length and hind tibia 0.62 mm and 0.14 times the
body length). In life, it is reddish-brown and lacks waxy
plates and siphunculi. The antenna (Figs. II, 2; III, 2) has
five segments without secondary sensoria and the antennal
segment III is 0.64 times the rest of antennal flagellum and
the terminal process is 0.09 times the part basal of the last
antennal segment (D). The rostrum is around 0.77 mm and
the apical rostral segment is 0.19 mm, 1.32 times its basal
width and 0.9 times the segment of the hind tarsus. The
cauda is rounded and short (0.09 mm and 0.38 times its
width). The anal plate has a large number of setae (around
35) and the genital plate have 14 on the anterior part and 25
on posterior marge (Fig. III, 3). The setae on the vertex is
around 0.09 mm and 2.73 times the articular diameter of
antennal segment III. The spinal setae on abdominal
segment III is 0.036 mm and the marginal of the same
segment is 0.042 mm (1.09 and 1.27 times D, respectively)
and the setae on abdominal segment VIII is 0.093 mm and
2.82 times D.
The alate fundatrigenia females (measurements based
on 20 specimens) are large (2.9-3.84 mm), with wings of
3.69 mm and 2.88 times its maximal width and with the
medial vein variable: unbranched (14% of 100 studied
specimens) (Fig. IV, 1) or with a fork, short (7%) (Fig. IV,
2) or quite big (75%) (Fig. IV, 3), even different medial vein
phenotypes can appear in the same individual. Colour in life
Fig. II – Antenna of the fundatrigenia alata (1), with detail of
secondary sensoria on antennal segment III and primary sensoria
of the last antennal segment, and antenna of the fundatrix (2) of
Pachypappa warshavensis (Nasonov).
Fig. III – Fundatrix of Pachypappa warshavensis (Nasonov): habitus (1) and detail of the anterior (2) and posterior (3) part of the body.
116 A. CASIRAGHI ET AL. REDIA, Vol. 102, 2019
Fig. IV – Forewings of several fundatrigeniae alatae of Pachy -
pappa warshavensis (Nasonov) with medial vein variable: un -
branched (1), with a short (2) or big (3) fork (the arrows indicate
the branches of the medial vein).
is reddish-brown (see also http://influentialpoints.com/
Gallery/Pachypappa_aphids.htm) and in slide, they have
brown head, thorax, legs, spiracular sclerites and cauda,
anal and genital plates and spinal sclerotization on
abdominal segments IV to VIII (Fig. V).
The antennae are 1.05-1.17 mm, and 0.30-0.37 times the
body length (Fig. V, 1). The antennal segment III is 0.31-
0.36 mm and have 3 to 7 secondary sensoria located in 68%
of the distal part of the segment (Fig. II, 1), the IV is 0.16-
0.19 mm and have from 1 to 4 secondary sensoria, the V is
0.18-0.23 mm and have until 3 secondary sensoria, and the
VI is 0.22-0.26 mm and without secondary sensoria; the
terminal process is 0.13-0.20 times the basal part of the last
segment and the diameter of the primary sensoria on
antennal segment VI is 0.02-0.05 mm. The antennal
segment III have 5 to 12 setae that are 1.22-2.14 times the
articular diameter of the same article (D). The rostrum is
0.69-0.77 mm and its apical rostral segment is 0.17-0.20
mm, 1.51-2.56 times its basal width and 0.59-0.68 times the
segment of the hind tarsus; and have two accessory hairs.
The siphunculi pores are very small, around 0.04-0.05 mm
and 0.60-0.89 times the diameter in the middle of the hind
tibia. The cauda is rounded and short (1.1-2.10 mm and
0.20-0.41 times its width) and have 16 to 20 setae, some of
which are longer and thicker (Fig. V, 3). The anal plate
shows a variable number of setae, from 28 to 48, while the
genital plate has around 18-27 (with 6 to 11 on anterior
half), with the setae of anterior part slightly longer and
Fig. V – Fundatrigenia alata of Pachy -
pappa warshavensis (Nasonov): habi tus
(1), abdomen (2) and dorsal (3) and
ventral (4) view of the posterior part of
the body.
thicker (Fig. V, 4). The hind legs have femora of 0.32-0.45
mm and tibiae of 0.48-0.57 mm and 0.09-0.14 and 0.14-
0.17 times the body length, respectively; and the setae of
hind tibia are 0.05-0.08 mm and 2.00-2.35 times D.
Formula tarsal 2.2.2. The wax plates are absent on the head
and present on the prothorax and metathorax (a spinal pair
and another marginal), mesothorax (one pair spinal) and on
all abdominal segments (a spinal pair on abdominal
segments I to VIII and a marginal pair on the segments I to
VII, that in the latter can be divided) (Fig. V, 2). The body
setae are pointed and large: on frons are 0.05-0.09 mm
(2.25-3.43 times D), the spinal setae on the abdominal
segment III are 0.11–0.15 mm (3.89-6.71 times D) and the
marginal of the same segment are 0.10–0.13 mm (3.56-6.00
times D), while the ventral ones are more delicate and a
little shorter (0.08-0.15 mm and 3.25-6.25 times D) and the
setae on the abdominal segment VIII (4 to 10) are 0.18–0.21
mm and 6.67-8.71 times D. Nine specimens were dissected
to count the embryos, finding a range between 105-269,
with a mean value of 200 embryos.
MOLECULAR DATA
The phylogenetic tree including other Pachypappa
species built using molecular data corresponding to a partial
sequence of the mtDNA gene encoding the subunit I of the
cytochrome oxidase (COI) confirmed that the specimens
belong to the Pachypappa genus (Fig. VI).
BIOLOGY AND DISTRIBUTION
Pachypappa warshavensis shows mainly P. alba as
primary host, although there are also records on P.
canescens, P. euphratica and P. pruinosa (SHAPOSHNIKOV,
1964; CARTER and DANIELSSON, 1993) and there is a record
on the Nearctic Populus tremuloides Michx. (POLJAKOVIĆ-
PAJNIK, 2006) in Serbia, that must be confirmed. According
to SZELEGIEWICZ (1982), apterae recorded on roots of Salix
caprea L. could be assigned to this species. Also, CARTER
and DANIELSSON (1993) tentatively associate P.
warshavensis to adult apterae and alatoid nymphs found
around roots of Populus canescens in Wales (in October)
and on fine roots in England (in June), but these both
relations need experimental transfers and molecular studies.
Pachypappa warshavensis is a Palaearctic species that is
widely distributed in Europe (Belarus, Germany, Hungary,
Poland, Romania, Serbia, Sweden and Ukraine) and more
recently was recorded in Central Asia (Kazakhstan)
(HOLMAN, 2009; KADYRBEKOV, 2011). Several authors
(GÓMEZ-MENOR and NIETO, 1977) and later HEIE (1980)
mentioned P. warshavensis in Spain but PÉREZ HIDALGO and
NIETO NAFRÍA (2003a,b) not included this species in the
review of the Iberian Eriosomatinae because they did not
find specimens to corroborate this record in any
aphidological collection. Our record confirms the presence
of this species in the Northwest of Spain (province of León)
and allows us to think that it is also present in the province
of Madrid according GÓMEZ-MENOR and NIETO (1977).
DISCUSSION
The species of genus Pachypappa present complex cycles
with up to six very different morphs (fundatrix,
fundatrigenia alata, virginogenia aptera, sexupara, ovipara
and male). As a result, not all morphs have been correctly
described for every species and some of them are not even
known (PIKE et al., 2011; BLACKMAN and EASTOP, 2019). In
the case of P. warshavensis there are descriptions of
fundatrix and fundatrigenia alata (HEIE, 1980) made with
few specimens and characters (SZELEGIEWICZ, 1982), which
sometimes generates problems when identifying the known
forms of the different species.
Our morphological identification was carried out using
the keys for fundatrix of HEIE (1980) and the keys to
identify alatae of HEIE (1980) and BLACKMAN and EASTOP
(2019). In these last keys, they use the medial vein
parameter (once-branched or unbranched vein) to separate
the genus Gootiella Tullgren and to discriminate
Pachypappa at a specific level. In particular, the last
operation results problematic, because the polymorphism of
the medial vein (Fig. V), which can have a big branch, a
small branch or be unbranched and also because every
individual can show different polymorphism at the same
time, one on each forewing (see description of fundatrigenia
alata).
Also in the identification, we even considered the
description of P. warshavensis of HEIE (1980) and we
CONFIRMATION OF THE PRESENCE OF PACHYPAPPA WARSHAVENSIS (NASONOV, 1894) [HEMPITERA APHIDIDAE] … 117
Fig. VI – Neighbour-joining phylogenetic tree (COI) from sequences of species of Pachypappa.
noticed that our fundatrix is slightly bigger (4.34 mm) than
the fundatrix presented by him (4 mm). But, in any case, the
number of the hairs can clearly separate the fundatrix of P.
warshavensis (Fig. II) of the fundatrix of P. tremulae (see
figure A in plate 1 in STROYAN, 1975).
Other problems showed up with the molecular analysis
because sequences of Pachypappa warshavensis are not
present in NCBI and we did not find specific matches using
BLAST.
Although the species of the subfamily Eriosomatinae are
among the first species of aphids mentioned in the Iberian
Peninsula (PÉREZ HIDALGO and NIETO NAFRÍA, 2003b),
some of them are difficult to locate although they live on
very abundant and frequent plants, such as different species
of Populus, or because they form colonies in roots of their
secondary hosts.
Currently, the lack of aphidologists and faunistic studies
means that there are large gaps in the known distribution of
many species. However, the recent fondness for
photography has helped in meeting and citing some species
of aphids, apparently scarce, by naturalists or photography
enthusiasts, as is the case of Plocamaphis flocculosa (Weed)
a boreal species detected recently in the Iberian Peninsula
(PÉREZ HIDALGO et al., 2016).
The known distribution of Pachypappa species and their
chorology suggested aphidologists that their presence in
territories of the Iberian Peninsula was unlikely since they
were assumed to be boreal species (PÉREZ HIDALGO and
NIETO NAFRÍA, 2003a).
Pachypappa warshavensis is widely distributed in Europe
on Populus alba and probably also in the Iberian Peninsula.
For this reason, we consider appropriate and useful the
contribution that citizen science can give (WHEELER and
VALDECASAS, 2010). Allowing naturalists to search and
document the presence of organisms and interacting with
experts to obtain information without excessive effort, may
thus establish a beneficial symbiosis for all players in this
game of knowledge enrichment (HAND, 2010; GURA, 2013).
Pachypappa species are recorded as important pests for
both deciduous (as Populus) or evergreen (as Picea) forest
trees (BARJADZE and JAPOSHVILI 2007). In particular,
spruces can suffer from aphids attacks: for example,
damages to spruce seedlings, some very severe, have been
documented in nurseries in Canada (LAVALLÉE, 1987).
Targeted plants appear severely affected, with gradually
yellowing of needles and sometimes even needles falling.
The genus can even affect the Norway spruce, grown for
Christmas market (ALFORD, 1991). In Europe, Pachypappa
vesicalis is considered as pest (WAT T et al., 1997) and its
presence is well established in spruce plantations in Britain,
on trees of all ages (CARTER and DANIELSSON, 1991). P. war -
sha vensis is recorded as pest of aspen with P. marsupialis in
Georgian urban habitats (BARJADZE and JAPOSHVILI, 2007),
but the commercial interest in Populus spp. is not relevant.
At the moment the genus Pachypappa is under control
and causes very little damage (SUTHERLAND and VAN
EERDEN, 1980; WONG, 1982; EL-SAYE D, 2019) but we lack
information about this aphid group as disease vector for
plants and at the same time we know little about its natural
predators and pathogens that can be used in its biological
control. Experiments were carried out only for another
species of Pemphigini, for example, Pemphigus betae
Doane, and never with Pachypappa (LAVALLÉE, 1987; SWAN
and PAPP, 1972; HARPER, 1961). More investigations are
required to understand the possible risks for the agroforest
business.
ACKNOWLEDGEMENTS
The authors are very grateful to the reviewers of the
manuscript, to Barbara Osiadacz (Poznań University of Life
Sciences, Poznań, Poland) and Andrey Stekolshchikov
(Zoological Institute of Russian Academy of Science, Saint
Petersburg, Russia) for facilitating the publications of N.V.
Nasonov, A. Mordvilko and H. Szelegiewicz about Pachy -
pappa warshavensis and to Francesca Maria Gatti (Civica
Scuola Interpreti e Traduttori Altiero Spinelli, Milan, Italy)
for the translation of articles in Russian. The investigation
was conducted in the context of Project CGL2015-68188-P,
funded by “Ministerio de Economia, Industria y
Competitividad” of Spain (MIMECO).
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