Identification of a quarantine mealybug Pseudococcus viburni (Signoret, 1875) (Hemiptera:

Pseudococcidae) for Colombia using integrative taxonomy.

Alejandro Caballero
Universidad Nacional de Colombia, Facultad de Ciencias Agrarias, Bogotá, Colombia.

Falta Mario Vargas,

Universidad Nacional de Colombia, (DATOS)

Takumasa Kondo
Corporación Colombiana de Investigación Agropecuaria - AGROSAVIA, Centro de Investigación
Palmira, Laboratorio de entomología, Palmira, Colombia.

Andrea Amalia Ramos-Portilla

Instituto Colombiano Agropecuario (ICA), Dirección Técnica de Sanidad Vegetal, Bogotá,
Colombia.

William Duarte Gómez

Universidad de Ciencias Aplicadas, Facultad de Ingeniería Agronómica, Bogotá, Colombia.

Abstract. The obscure mealybug Pseudococcus viburni (Signoret) (Hemiptera: Pseudococcidae),

considered of quarantine importance, is recorded for the first time for Colombia. The specimens
were collected on Opuntia cylindrica and Mammillaria sp. (Cactaceae), Escallonia paniculata
(Escalloniaceae), Ficus carica L. (Moraceae), Coffea arabica L. (Rubiaceae), Citrus sp. (Rutaceae),
Cestrum nocturnum L. and Solanum betaceum (Solanaceae) in Bogotá, Colombia. Specimens were
identified based on the morphology and morphometric analysis of the adult female, molecular
techniques and geographical and host information. An updated list of Pseudococcus Signoret
species recorded in Colombia is provided.

Key words. Coccoidea, Coccomorpha, Neotropical region, Quarantine pest.

Introduction

The Pseudococcidae (Hemiptera: Coccomorpha) is the second largest family of scale insects in
terms of species numbers (García Morales et al. 2016). Members of the Pseudococcidae are small,
plant-sucking insects commonly known as “mealybugs” (Downie & Gullan 2004). The
Pseudococcidae is composed of approximately 2000 described species in more than 270 genera
(García Morales et al. 2016). Damage results from sap removal, the injection of toxins, honeydew
contamination and associated sooty molds that grow on the surfaces where the excreted honeydew
accumulates, and occasionally from the effects of transmitted plant viruses (McKenzie 1967). Some
species are considered as major agricultural pests and can cause serious problems when introduced
into new geographical areas without their natural enemies (Miller et al. 2002, 2005).

Pseudococcus Westwood, 1840, is one of the most species-rich genera in the Pseudococcidae,
composed of 154 species (García Morales et al. 2016). Several species are considered as
agricultural pests, because of their polyphagous habits and wide distribution (Correa et al. 2015;
González 2011; Granara de Willink & Dughetti 2012; Miller et al. 2002). Twenty species of
Pseudococcus are known to occur in Colombia and many of them have been recorded affecting
several crops of economic importance (Figueroa 1946, 1952; Kondo et al. 2008; Posada 1989;
Villegas-García & Benavides-Machado 2011).
The obscure mealybug, Pseudococcus viburni (Signoret, 1875) is native to the Neotropical region
and is considered a quarantine pest in many countries around the world (Charles 2011). In the
Neotropical region, it has been recorded from Argentina, Bolivia, Brazil, Chile, Costa Rica, Cuba,
Ecuador, Guadalupe, Guatemala, Panama, Peru, Uruguay and Venezuela (Ben-Dov 1994; Culik et
al. 2007; Gimpel & Miller 1996; Vera et al. 2012; Williams & Granara de Willink 1992) (Salazar
1972; González 1983; Matile-Ferrero and Étienne 2006;). In Colombia, P. viburni has the status of
Quarantine Absent Pest (Instituto Colombiano Agropecuario ICA 2018).

Due to the vast morphological variation, P. viburni belongs to the “Pseudococcus maritimus”
species–complex, composed of 32 species (Correa et al. 2011; Gimpel & Miller 1996).
Morphological and molecular studies put this species closer to Psedococcus bryberia Gimpel and
Miller, P. eriocerei Williams, P. mandio Williams, P. maritimus (Ehrhorn), and P. meridionalis
Prado (Correa et al. 2011; Downie & Gullan 2004; von Ellenrieder & Watson 2016; Gimpel &
Miller 1996; Hardy et al. 2008; Pacheco da Silva et al. 2017). A variety of taxonomic tools have
been used to resolve this species complex, including molecular techniques, morphological studies of
postembrionary stages, and biological information, i.e. host range, geographic distribution, and
mealybug–parasitoid relationship approaches (Charles 2011; Correa et al. 2015; Gimpel & Miller
1996; Wakgari & Giliomee 2004). Because of the difficulty in identifying specimens belonging to
this complex that includes species of economic and quarantine importance, it is necessary to use
different tools that allow for an accurate identification.

The objective of this study is to report P. viburni for the first time in Colombia using
morphological, morphometric, molecular tools, as well as host and geographical data analysis.
Herein is reported new intraspecific variation and host plant information for P. viburni, briefly
diagnose the species, and list some important features that aid in differentiating it from closely
related species. An updated list of Pseudococcus species recorded from Colombia is also provided.

Materials and methods

Collecting and preparating samples

Mealybugs were collected in situ, from Opuntia cylindrica (Lam.) DC. 1828 (Fig. 1 A–D),
Mammillaria sp. (Cactaceae), Escallonia paniculata (Ruiz & Pav.) Roem. & Schult., 1819
(Escalloniaceae) (Fig. 1 E–H), Ficus carica L., 1753 (Moraceae), Coffea arabica L., 1753
(Rubiaceae), Cestrum nocturnum L., 1753, and Solanum betaceum Cavanilles, 1799 (Solanaceae) in
Bogotá D.C. and Citrus sp. (Rutaceae) in Popayan city, Colombia. Specimens were stored in 75%
ethanol and labelled with their respective collecting data. Slide-mounted specimens were prepared
according to Sirisena et al. (2013) with modifications. Mealybug specimens were collected under a
collecting permit “Permiso marco de recolección de especímenes de especies silvestres de la
diversidad biológica con fines de investigación científica no comercial” [Permit framework for
collecting of specimens of wild species of the biological diversity for non-commercial scientific
research purposes], resolution No. 1466, expedited on December 3, 2014, by the Autoridad
Nacional de Licencias Ambientales (ANLA) [Colombian National Authority Environmental
Permits]. The specimens studied are deposited in the following museums: “Universidad Nacional
Agronomía Bogotá” (UNAB) and the “Colección Taxonómica Nacional de Insectos Luis María
Murillo, Corporación Colombiana de Investigación Agropecuaria (Corpoica), Centro de
Investigación Tibaitatá, Mosquera, Cundinamarca, Colombia” (CTNI).

Morphological identification and morphometric analysis

Adult female specimens were identified using the descriptions by (Williams & Granara de Willink
1992) and Gimpel and Miller (1996) and taxonomic keys of Williams and Granara de Willink
(1992), Gimpel and Miller (1996), (Williams 2004) and (von Ellenrieder & Watson 2016).
Identification of nymphs were carried out with descriptions of (Gimpel & Miller 1996; Wakgari &
Giliomee 2004) and taxonomic keys of Gimpel and Miller (1996) and (Gullan 2000). Terminology
of morphological characters follow that of Gimpel and Miller (1996). A Nikon SMZ-1 stereoscope
was used for macroscopic observation.

A morphometric analysis was carried out to define if the population by host was composed by one
or more morphological groups. A total of 50 adult females were examined and 23 variables were
selected according to characters used in diagnoses and taxonomic keys above mentioned (see
supplementary file). First, a descriptive analysis was done by Principal Components Analysis. A
statistical analysis was carried out to define if the host is a critical factor in the morphological
identification of the specimens. The host component was divided into three groups: Mamillaria sp.
Group (20 specimens), Opuntia cylindrica group (20 specimens) and “other hosts” group (2
specimens from Coffea arabica, 2 from Ficus carica, 2 from Solanum betaceum, and 4 from Croton
smithianus). The VARSEDIG algorithm (Guisande et al. 2016) were applied to prioritizing and
selecting variables with capacity for discrimination. The overlap method selects those variables
with lower overlap of the area under the density curve between two groups and the Monte-Carlo test
is used for testing the statistical hypothesis if all means of X and Y values of polar coordinates of
one group are significantly higher or lower that the values of the other group. The algorithm was
performed with the statistical program R (R Development Core Team 2015) and RWizard open
source application. Candisc package (Friendly 2007; Friendly & Fox 2015), Ida of the MASS
package (Venebles & Ripley 2002; Ripley et al. 2015).

Measurement and analysis of microscopic images was conducted using a phase-contrast Nikon
Eclipse E600 microscope, a Lumenera 1-C5 camera and Image Pro Insight v 8.0 software calibrated
with micrometric lamina Leitz Wetzlar (0.01 mm).

Molecular analysis
(Mario Vargas’ section)

Results and discussion

Material Studied. Pseudococcus viburni (Signoret, 1875). Colombia: Cauca, Popayan.

Downtown, 02°26′21.31″N, 76°36′20.26″W, 1776 m a.s.l., 31.viii.2015, coll. A. Caballero, A.
Ramos, ex stems and leaves of Citrus sp. (Rutaceae), 6 adult ♀♀, UNAB [4383]. Cundinamarca,
Bogotá D.C., Barrio Villas de Granada, 04°43′17.09″N, 74°07′24.40″W, 2547 m a.s.l., 31.i.2016,
coll. A. Ramos, ex. main stem and cladodes of Opuntia cylindrica (Cactaceae), 8 adults ♀♀, 1
third- instar nymph ♀, UNAB [4383], CTNI [225]. Cundinamarca, Bogotá D.C., Modelia, 2555 m
a.s. l., 24.x.2015, coll. A. Ramos, ex. Mammillaria sp. (Cactaceae), 9 adults ♀♀, 6 third-instar
nymphs ♀♀, UNAB [4383], CTNI [225]. Cundinamarca, Bogotá D.C., Teusaquillo,
04°38′20.31″N, 74°04′30.08″W, 2560 m a.s.l., 24.x.2015, coll. A. Caballero, ex. Mammillaria sp.
(Cactaceae), 13 adults ♀♀, UNAB [4383], CTNI [225]. Cundinamarca, Bogotá D.C., Engativá,
Barrio Modelia, 04°40′33.91″N, 74°07′02.38″W, 2552 m a.s.l., 12.vi.2016, coll A. Ramos, A.
Caballero, ex. stem of and Escallonia paniculata (Escalloniaceae), 2 adults ♀♀, 1 third-instar
nymph ♀, UNAB [4383], CTNI [225]. COLOMBIA, Cundinamarca, Bogotá D.C., Barrio Villas de
Granada, 04°43′17.09″N, 74°07′24.40″W, 2547 m a.s.l., 26.vi.2016, coll. A. Ramos, ex fruits,
leaves and stems of Coffea arabica (Rubiaceae)–coffee, 1 adult ♀, UNAB [4383]. Cundinamarca,
Bogotá D.C., Barrio Villas de Granada, 04°43′04.27″N, 74°07′21.09″W, 2555 m a.s.l., 25.iii.2016,
coll. A. Ramos, ex fruits, leaves and stems of Ficus carica (Moraceae)–fig, 7 adults ♀♀, UNAB
[4383], CTNI [225]. Cundinamarca, Bogotá D.C., Ciudadela Colsubsidio, 04°43′21.9″N,
74°07′03.82″W, 2555 m a.s.l., 25.iii.2016, coll. A. Ramos, ex stem and branches of Cestrum
nocturnum (Solanaceae)–night jessamine, 1 adult ♀, UNAB [4383]. Cundinamarca, Bogotá D.C.,
Suba, campus Universidad de Ciencias Aplicadas–U.D.C.A., 04°48′0″N, 74°03′0″W, 2570 m a.s.l.,
2.ii.2018, coll. W. Duarte, ex leaves, stems, and fruits of Solanum betaceum (Solanaceae)–tree
tomato, 15 adults ♀♀, UNAB [4383].

Morphological identification
The collected mealybug samples were preliminarily identified as Pseudococcus viburni (Signoret,
1875) (Hemiptera: Pseudococcidae). High populations of P. viburni were found on the stems and
modified leaves of Mammillaria sp. and Opuntia cylindrica, also on leaves, twigs and fruit of E.
paniculata and S. betaceum forming large colonies associated with sooty mould-causing fungi
(species not determined). These three last host species are new host records for P. viburni.

The damage caused on S. betaceum occurs on leaves, twigs and fruits, where the mealybug
populations develop until the tissues undergo necrosis. It was observed that the fruits affected by the
mealybug have a slower development compared to non-affected fruits. The largest concentration of
the mealybug population occurs in peduncles of leaves and fruits.

Pseudococcus viburni (Signoret, 1876) (Pseudococcidae)

Adult female
Diagnosis: Mealybugs with discoidal pores associated with eyes, not in a sclerotized rim (Fig. 2A);
cerarius XII with 15–23 trilocular pores and less than 7 associated oral collar tubular ducts (Fig.
2B); circulus present, more than 70 μm wide, with an intersegmental line (Fig. 2C); translucent
pores absent from hind coxa and trochanter, present on both hind femur and tibia (Fig. 2D–E);
ventral multilocular pores present on abdominal segment IV and posterior segments; dorsal
multilocular pores absent; dorsal oral rim tubular ducts absent from between C16 and anterior
ostiole; ventral oral collar tubular ducts present on submargin, next to C14; ventral oral collar
tubular ducts present on submargin at the level of mid-coxa, numbering 0–2 (adapted from
Williams and Granara de Willink 1992, and Gimpel and Miller 1996).

Table 1 shows the variations present in the studied specimens (n=50). The character states marked
with an asterisk (*) indicate novel interspecific variation. The length of tarsus 124 ± 7.4 (92–140)
µm according to Gimpel & Miller (1996) data (114–142 µm); thirteen specimens have 1 to 5 ventral
multilocular disc pores on abdominal segment III; 6–20 dorsal oral rim tubular ducts on abdomen;
(data not shown in Table 1). Some specimens have an unusual variation that appear to be due to
deformations more than stable characters variation. Three specimens have one partially developed
cerarius on pair C4, C14 and C17; one specimen has just one dorsal oral collar tubular duct in
submarginal area mesad of C3 and another has one duct in same region in submarginal area mesad
to C2.

3rd–instar female nymph

Table 2 shows the character states of the studied specimens, i.e., P. viburni and P. maritimus.
According to (Gimpel & Miller 1996; Wakgari & Giliomee 2004), the characters of immature
specimens do not show differences in measurement, except for the length of the longest anal lobe
setae, which have tendency to P. maritimus. However, the length of the longest anal lobe setae is
not a important character to separating P. viburni from P. jackbeardsleyi, therefore, the differences
found in the studied specimens should be considered as part of the intraspecific variation of P.
viburni.
Figure 1. Host plants of Pseudococcus viburni: A-D. Opuntia cylindrica (Cactaceae) with close-up
images of in situ and alcohol-preserved specimens; E-H. Escallonia paniculata (Escalloniaceae)
with close-up images of specimens on stems and leaves; I-L. Solanum betaceum (Solanaceae) with
close-up images of specimens on leaves, aggregation of mealybugs on branch and fruit peduncles,
necrotic leaves and damage on fruits caused by P. viburni.
The important characters to separate P. viburni and P. maritimus are the number of dorsal oral rim
tubular ducts associated to C15 and C16, thorax and C2; number of ventral multilocular disc pores
and number of ventral collar tubular ducts in submarginal area of C13, C12, between C10–C11 and
abdomen (Gimpel & Miller 1996). In general, the specimens herein studied fit well the descriptions
of P. viburni, but some individuals show differences that should be considered. Three specimens had
1–2 ventral collar ducts in the abdomen; which according to Gimpel and Miller (1996) this kind of
ducts are “usually absent in P. viburni”, in other words, this can be interpreted as to be rarely present
in P viburni. In the case of ventral multilocular disc pores, one of the 14 specimens had one pore near
the vulvar aperture; however, this specimen is not considered to be P. maritimus when all the
characters were considered.

Morphometric population analysis

A descriptive analysis of Principal Components (PCA) conducted on specimens that were identified
as P. viburni based on morphological characters of the adult female did not show groups between
specimens; moreover, specimens of different hosts were mixed in the analysis (Fig. 3 A). A
statistical analysis to check whether all specimens collected from different hosts belong to a unique
morphological group was carried out. Figure 3 B shows the scatterplot of the polar coordinates that
compares the “Mammillaria sp.” group versus other groups (“Opuntia cylindrica” and “other hosts”
groups). No character was capable to separate specimens between groups, keeping all specimens as
a unique cluster. Figure 3 C shows the “Mammillaria sp.” group specimen with the higher
probability to belong, morphologically, to any other host group and Figure 3 D shows the specimen
of any other host group (“Opuntia cylindrica” or “other hosts”) with the higher probability to
belong, morphologically, to the “Mammillaria sp.” group. In both cases, the p–value in both X and
Y polar coordinates is higher than 0.05, so the null hypothesis is accepted (H0=all specimens belong
to unique group), that means that the specimens collected on Mammillaria sp. are like any specimen
collected from any other host. So, it can be said that all specimens belong to a single morphological
group, no matter what host they were collected on.

Morphological comparison
The morphological differences (gray boxes) between the specimens used in this study and closely
related species from the P. maritimus complex are shown in Table 1. The specimens of P. viburni
identified in this study are morphologically different from all species currently included in the P.
maritimus complex. The mealybugs herein studied fit well the description of P. viburni, however,
some characters show some intraspecific variation (characters indicated with an asterisk *).

Morphologically, Pseudococcus meridionalis is probably the closest species to P. viburni (Correa et

al. 2011), but they clearly differ in the number of ventral oral collar tubular ducts in each side of
head (0–6 in P. viburni; 6–16 in P. meridionalis), ventral oral collar tubular ducts between cerarii
10 and 11 (0–2 in P. viburni; 3–17 in P. meridionalis), but there is an overlap in other characters,
i.e., number of dorsal oral rim tubular ducts on abdomen, length of anal lobe setae and length of
interantennal setae (see Correa et al. 2011, table 1). Based on the character states provided by
Correa et al. (2011), the studied specimens were identified as P. viburni. Regarding the number of
ventral oral collar ducts on each side of the head, specimens from this study overlap with P.
meridionalis, but the mean indicates 3 ducts per head on each side with standard deviation of 2; the
extreme values (>6) were seen in only three specimens.
Figure 2. Microphotographs of Pseudococcus viburni (Signoret) adult female with close-ups of
diagnostic features. A. Discoidal pores associated with eyes not set in a sclerotized rim (indicated
by arrows). B. Cerarius XII with more than seven associated oral collar tubular ducts (indicated by
arrows) and more than 14 trilocular pores. C. Circulus greater than 70 µm. D. Translucent pores on
hind femur. E. Translucent pores on hind tibia.
Figure 3. A) Principal Component Analysis plot of specimens of Pseudococcus viburni (Signoret)
indicating its host. B) Scatteretplot of the polar coordinates for Mammillaria sp. group versus other
groups (Opuntia cylindrica and “other host” groups) using the variables ch_4, ch_8 and ch_11. The
inner and outer ellipses show the significance level 0.05 and 0.95, respectively. C) Bivariate
randomization test with x-axis correspond to X polar coordinates and the y-axis to Y polar
coordinates. The blue line indicates the contours of the distribution of randomized values. The two
marginal histograms indicate the univariate test on each axis with its corresponding p-values. The
red point shows the specimen with highest probability of belonging to the Mammillaria sp. group
among all individuals identified as any other host group. D) same bivariate randomization test of
figure C, but this shows the specimen with highest probability of belonging to any other hosts
groups among all included individuals belonging to the Mammillaria sp. group.
Table 1. Morphological comparison between the collected specimens and closely-related species of the Pseudococcus maritimus complex. In the
first column are listed the morphological characters followed by the character state of the analyzed specimens in this study, Pseudococcus viburni,
P. meridionalis, P. maritimus, P. eriocerei, P. mandio and P. bryberia. In the case of specimens studied, the data include the mean, standard
deviation and range of variation in parenthesis, in their corresponding order. The character states values of Pseudococcus maritimus complex are
taken from Gimpel and Miller (1996), Correa et al. (2011), González (2011) and Williams and Granara de Willink (1992). The values of the
specimens studied with an asterisk (*) indicate new information of intraspecific variation with respect to P. viburni.
Study Pseudococcus
Character specimens
viburni meridionalis maritimus eriocerei mandio bryberia
(n=50)
# pairs of cerarii 16 – 17 16–17 17 16–17 16–17 16–17 17
C2 0 0 0 0 0 0–2 0
C3 0 0 0 0 0 0–1 0
C4 0 0 0 0 0 1–3 0
# dorsal oral-collar present
ducts in submarginal C5 0 0 0 0 0 0–3
(no data)
area mesad of cerarii present
C6 0 0 0 0 0 0–3
(no data)
present
C7 0 0 0 0 0 0–1
(no data)
# oral-rim ducts on dorsal 14 ± 2.8
10–18 2–44 19–35 9–22 0–4 12
abdomen (6–20)*
Ventral oral-collar ducts on
3 ± 2 (0–9)* 0–6 6–16 3–25 1–5 1–5 0–2
each side of head
# ventral oral-collar ducts
0.4 ± 0.7
associated with C10 and C11, 0–2 3–17 6–20 0–5 0–6 0–9
(0–3)*
opposite each mid-coxa
# dorsal oral-rim ducts between
C15 and C16 and anterior 0 0 0 2 0 0 2
ostiole
# ventral oral-collar ducts 13 ± 3.3
8–16 7–27 10–25 1–4 0–7 2–11
associated with C12 (5–21)*
162 ± 8.8
Length of labium (µm) 146–207 117–183 154–207 168–180 183–200 124–143
(148–189)
 Length of longest anal lobe 122 ± 9.7
109–136 78–120 136–168 101–119 111–168 69–118
setae (µm) (94–146)*
312 ± 19.1
Length of hind femur (µm) 263–356 no data 239–395 217–267 247–301 180–242
(267–349)
328 ± 19.4
Length of hind tibia (µm) 268–381 no data 261–473 237–284 279–358 190–267
(256–370)*
Ratio of tibia/ tarsus of hind leg 2.2–3.4* 2.2–3 2–2.9 2.2–3.6 2.4–3.1 2.7–3.5 1.8–2.5
Length of circulus (µm) 95–159* 71–148 158–176 98–220 32–60 no data 71–131

Table 2. Morphological comparison of 3rd–instar female of studied specimens, Pseudococcus viburni and Pseudococcus maritimus. In the case of
specimens studied, the data include the mean, standard deviation and range of variation in parenthesis, in their corresponding order. The character
states values of P. viburni and P. maritimus are taken from Gimpel and Miller (1996) and Wakgari and Giliomee (2004).

Study specimens Pseudococcus

Character
(n=14) viburni maritimus
Length of labium (µm) 355.5 ± 23.3 (301–387) 268–390 285–378
Length of hind femur (µm) 187.4 ±11 (161–208) 110–202 146–183
Length of labium (µm) 117.7 ± 7.5 (104–127) 105–169 116–148
Length of longest anal lobe setae (µm) 92.1 ± 9.4 (64–109) 93–127 77–111
Transversal diameter of anal ring (µm) 66.9 ± 3.7 (60–74) 57–70 No data
# ventral Abdominal segments 0 ± 0.5 (0–2) Usually absent 0–2 in each segment
collar tubular between C10 and C11 0 ± 0.3 (0–1) 0–2 0–2
ducts in
submargimal C12 0 ± 0.2 (0–1) 0–1 0–1
region C13 0 ± 0.3 (0–1) 0–1 0–4
submarginal region
# dorsal oral 0 0 1
between C15 and C16
rim tubular
Thorax 3 ± 1 (1–4) 0 0–3
ducts in
submarginal region C2 0 0 1
# ventral multilocular disc pores 0 ± 0.3 (0–1) 0–5 5–9
Host and geographical distribution
Additional information that supports the identification of P. viburni is the host range and
geographical distribution. Specimens found in this study were found on O. cylindrica and
Mammillaria sp. (Cactaceae), E. paniculata (Escalloniaceae), F. carica (Moraceae), C. arabica
(Rubiaceae), Citrus sp. (Rutaceae), C. nocturnum and S. betaceum (Solanaceae). Here, the closely
related species to P. viburni, except P. mandio and P. bryberia, were analized. Pseudococcus
meridionalis have been recorded on Conyza bonariensis (L.) Cronquist, 1943 (Asteraceae),
Diospyros kaki Thunb., 1780 (Ebenaceae), Punica granatum L., 1753 (Lythraceae), Pyrus sp.
(Rosaceae) and Vitis vinifera L., 1753 (Vitaceae) (Correa et al. 2011; Pacheco da Silva et al. 2017).
Pseudococcus eriocerei has been only recorded on Cleistocactus sp. (Cactaceae) and Zingiber sp.
(Zingiberaceae) (Gimpel & Miller 1996). Pseudococcus maritimus has been recorded in association
with around 83 botanical species but non in the Cactaceae family; the records of Ps. maritimus from
Rubiaceae correspond to Spermacoce sp. and that of Solanaceae correspond to Cestrum sp. and
Solanum melongena L., 1753 (Ben-Dov 1994; Gimpel & Miller 1996; Matile-Ferrero 1978).
Meanwhile, P. viburni has been recorded on more than 250 plant species, including Mammillaria
sp., Opuntia sp., F. carica, Coffea sp., C. nocturnum, and five species of Solanum (Ben-Dov 1994;
Gimpel & Miller 1996; Williams 1985, 2004). On this respect, P. viburni identified in this study,
fits well with the recorded host plants of the species.

The geographical range also provides information to define the identity of the studied specimens.
Pseudococcus meridionalis is restricted to the central region of Chile and southern Brazil and P.
eriocerei is only known from Argentina (Ben-Dov 1994; Correa et al. 2011; Gimpel & Miller 1996;
Pacheco da Silva et al. 2017; Williams & Granara de Willink 1992). Pseudococcus maritimus was
recorded from Colombia by (Figueroa 1952), but (Kondo et al. 2008) indicated that this species had
not been collected in Colombia since the first record and there are no voucher specimens available
to verify this record. Lastly, P. viburni is recorded in all neighboring countries of Colombia (i.e.,
Bolivia, Brazil Ecuador, Panama, Peru and Venezuela). In consequence, the presence of P. viburni
in Colombia was to be expected.

With the addition of P. viburni, the number of species belonging to the genus Pseudococcus in
Colombia is increased to 13 (Table 3). Of the Pseudococcus species present in Colombia, P. viburni
is closest to P. peregrinabundus Borchsenius, but it can be differentiated from that species because
P. viburni lacks dorsal multilocular pores on the dorsum (multilocular pores present on dorsum in
P. peregrinabundus) and are also absent ventrally on head region (present on head region on area
anterior to clypeus in P. peregrinabundus).

Table 3. Mealybug species of the genus Pseudococcus Signoret (Hemiptera: Pseudococcidae)

recorded from Colombia. Species marked with an asterisk (*) are considered as dubious records.

Species References
Pseudococcus calceolariae (Maskell, 1879) (Kondo et al. 2008)
Pseudococcus comstocki (Kuwana, 1902) (Figueroa 1952)
Pseudococcus elisae Borchsenius, 1947 (Borkhsenius 1948; Gimpel & Miller 1996;
Williams & Granara de Willink 1992)
Pseudococcus espeletiae Williams and (Ben-Dov 1994; Williams & Granara de
Granara de Willink, 1992 Willink 1992)
Pseudococcus importatus McKenzie, 1960 (Gimpel & Miller 1996)
Pseudococcus jackbeardsleyi Gimpel and (Gimpel & Miller 1996; Kondo et al. 2008)
Miller, 1996
 Pseudococcus landoi (Balachowsky, 1959)
Pseudococcus longispinus (Targioni Tozzetti,
1867)
Pseudococcus maritimus Ehrhorn, 1900*
Pseudococcus microcirculus McKenzie,
1960
Pseudococcus peregrinabundus Borchsenius,
1947
Pseudococcus sociabilis Hambleton, 1935
Pseudococcus viburni (Signoret, 1875)
Balachowsky (1959); Gimpel and Miller
(1996); Kondo and Muñoz (2006); Williams
and Granara de Willink (1992).
Ben-Dov (1994); Figueroa (1952); Kondo
(2001); Kondo et al. (2008); Williams and
Granara de Willink (1992).
Figueroa (1952)
Ben-Dov (1994); Gimpel and Miller (1996);
Kondo (2001); Williams and Granara de
Willink (1992).
Ben-Dov (1994); Borchsenius (1947, 1948);
Gimpel and Miller (1996); Kondo (2001).
Kondo (2001); Kondo et al. (2008); Williams
and Granara de Willink (1992).
Present study

Conclusions

Hitherto, P. viburni was known from almost all countries of South America, for the exception of
Colombia. Due to the quarantine importance of this species, this record is relevant for plant
protection authorities and farmers. The record of P. viburni in Colombia has a restricted distribution
in urban areas of Bogotá. Up to the time of preparation of this study, P. viburni was not found in
cultivated areas on any host, therefore, sampling on different crops in areas near Bogotá must be
continued.

Acknowledgments

The authors express their gratitude to the Universidad Nacional and Museo Entomológico UNAB
for research funding, also to curator of both collections UNAB and CTNI, Erika Vergara for his
help in the curatorial process and the anonymous reviewers for theirs comments and suggestions.

Literature cited

Ben-Dov, Y. (1994) A systematic catalogue of the mealybugs of the world (Insecta, Homoptera,
Coccoidea, Pseudococcidae and Putoidae): with data on geographical distribution, host plants,
biology, and economic importance. Intercept Limited Andover, UK. Available from:
https://books.google.com.co/books?id=UFN3QgAACAAJ.
Borkhsenius, N.S. (1948) Notes on Pseudococcus comstocki, Kuw., and some allied species
(Homoptera: Coccoidea) with description of three new species. Bulletin of Entomological Research
39, 417–421.
Charles, J.G. (2011) Using parasitoids to infer a native range for the obscure mealybug,
Pseudococcus viburni, in South America. BioControl 56, 155–161.
Correa, M., Aguirre, C., Germain, J.-F., Hinrichsen, P., Zaviezo, T., Malausa, T. & Prado, E. (2011)
A new species of Pseudococcus (Hemiptera: Pseudococcidae) belonging to the “Pseudococcus
maritimus” complex from Chile: molecular and morphological description. Zootaxa 2926, 46–54.
Correa, M., Lombaert, E., Malausa, T., Crochard, D., Alvear, A., Zaviezo, T. & Palero, F. (2015)
Mealybug species from Chilean agricultural landscapes and main factors influencing the genetic
structure of Pseudococcus viburni. Scientific Reports 5.
Culik, M.P., Martins, D.S. dos S., Ventura, J.A., Peronti, A.L.B.G., Gullan, P.J. & Kondo, T. (2007)
Coccidae, Pseudococcidae, Ortheziidae, and Monophlebidae (Hemiptera: Coccoidea) of Espírito
Santo, Brazil. Biota Neotropica 7, 61–65.
Downie, D.A. & Gullan, P.J. (2004) Phylogenetic analysis of mealybugs (Hemiptera: Coccoidea:
Pseudococcidae) based on DNA sequences from three nuclear genes, and a review of the higher
classification. Systematic Entomology 29, 238–259.
von Ellenrieder, N. & Watson, G. (2016) A new mealybug in the genus Pseudococcus Westwood
(Hemiptera: Coccomorpha: Pseudococcidae) from North America, with a key to species of
Pseudococcus from the New World. Zootaxa 4105, 65–87.
Figueroa, A. (1946) Catalogo inicial de las cochinillas del Valle del Cauca (Homoptera-Coccoidea).
Revista Facultad Nacional de Agronomía 6, 196–220.
Figueroa, A. (1952) Catalogo de los artropodos de las clases Arachnida e Insecta encontrados en el
hombre, los animales y las plantas de la Republica de Colombia. Acta Agronómica 2, 199–223.
García Morales, M., Denno, B., Miller, D.R., Miller, G.L., Ben-Dov, Y. & Hardy, N.B. (2016)
ScaleNet: A literature-based model of scale insect biology and systematics. Database 2016.
Gimpel, W.F. & Miller, D.R. (1996) Systematic analysis of the mealybugs in the Pseudococcus
maritimus complex (Homoptera: Pseudococcidae). Contributions on Entomology, International 2,
1–163.
González, R.H. (2011) Pseudocóccidos de importancia frutícola en Chile (Hemiptera:
Pseudococcidae). Universidad de Chile Facultad de Ciencias Agronómicas, Santiago.
Granara de Willink, M.C. & Dughetti, A.C. (2012) Una especie nueva de Pseudococcus
(Hemiptera: Coccoidea: Pseudococcidae) sobre forrajeras y soja en Argentina y países vecinos.
Revista de la Sociedad Entomológica Argentina 71, 29–36.
Gullan, P.J. (2000) Identification of the immature instars of mealybugs (Hemiptera:
Pseudococcidae) found on citrus in Australia. Australian Journal of Entomology 39, 160–166.
Hardy, N.B., Gullan, P.J. & Hodgson, C.J. (2008) A subfamily-level classification of mealybugs
(Hemiptera: Pseudococcidae) based on integrated molecular and morphological data. Systematic
Entomology 33, 51–71.
Instituto Colombiano Agropecuario ICA (2018) Plagas Cuarentenarias Ausentes. Available from:
https://www.ica.gov.co/Areas/Agricola/Servicios/Epidemiologia-Agricola/Plagas-
Reglamentadas/Plagas-Cuarentenarias-Ausentes.aspx (July 23, 2018).
Kondo, T., Ramos, A.A. & Vergara, E. (2008) Updated list of mealybugs and putoids from
Colombia (Hemiptera: Pseudococcidae and Putoidae). Boletín del Museo de Entomología de la
Universidad del Valle 9, 29–53.
Matile-Ferrero, D. (1978) Homoptères Coccoidea de l’Archipel des Comores. In: L. Matile (Ed),
Faune Entomologique de l’Archipel de Comores. Mémoires du Museum National d’Histoire
Naturelle (N.S.), Paris, pp. 39–70.
McKenzie, H.L. (1967) Mealybugs of California with taxonomy, biology and control of North
American species (Homoptera: Coccoidea: Pseudococcidae). University of California Press,
Berkeley and Los Angeles.
Miller, D.R., Miller, G.L., Hodges, G.S. & Davidson, J.A. (2005) Introduced scale insects
(Hemiptera: Coccoidea) of the United States and their impact on U.S. agriculture. Proceedings of
the Entomological Society of Washington 107, 123–158.
Miller, D.R., Miller, G.L. & Watson, G.W. (2002) Invasive species of mealybugs (Hemiptera:
Pseudococcidae) and their threat to U.S. agriculture. Proccedings of the Entomological Society of
Washington 104, 825–836.
Pacheco da Silva, V., Kaydan, M.B., Malausa, T., Germain, J., Palero, F. & Botton, M. (2017)
Integrative taxonomy methods reveal high mealybugs (Hemiptera: Pseudococcidae) diversity in
southern Brazilian fruit crops. Scientific Reports 7, 15741.
Posada, L. (1989) Lista de insectos dañinos y otras plagas en Colombia. Boletín Técnico 43. 4th ed.
Instituto Colombiano Agropecuario ICA, Bogotá D.C.
Vera, D., Garrido, S., Aun, E., Lago, J. & Cichon, L. (2012) Determinación del umbral de detección
de Pseudococcus viburni (Hemiptera: Pseudococcidae) por PCR. Revista de la Sociedad
Entomológica Argentina 71, 151–154.
Villegas-García, C. & Benavides-Machado, P. (2011) Identificación de cochinillas harinosas en las
raíces de café en departamentos cafeteros de Colombia. Revista Cenicafé 62, 48–55.
Wakgari, W.M. & Giliomee, J.H. (2004) Description of adult and immature female instars of
Pseudococcus viburni (Hemiptera: Pseudococcidae) found on apple in South Africa. African
Entomology 12, 29–38.
Williams, D.J. (1985) Australian mealybugs. British Museum (Natural History), London.
Williams, D.J. (2004) Mealybugs of southern Asia. Lumpu, The Natural History Museum Kuala:
Southdene SDN. BHD.
Williams, D.J. & Granara de Willink, M.C. (1992) Mealybugs of Central and South America. 1st
ed. CAB International, London, UK. Available from:
https://books.google.com.co/books?id=m9EQAQAAMAAJ.