Alien scale insects (Hemiptera Coccoidea)

in European and Mediterranean countries:

the fate of new and old introductions
Giuseppina Pellizzari & Francesco
Porcelli

Phytoparasitica
ISSN 0334-2123
Phytoparasitica
DOI 10.1007/s12600-014-0414-5

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Author's personal copy

Phytoparasitica
DOI 10.1007/s12600-014-0414-5

Alien scale insects (Hemiptera Coccoidea) in European

and Mediterranean countries: the fate of new and old
introductions
Giuseppina Pellizzari & Francesco Porcelli

Received: 16 March 2014 / Accepted: 15 May 2014

# Springer Science+Business Media Dordrecht 2014

Abstract This contribution focuses on recent interceptions and introductions of alien scale insects and their
current distribution in European and Mediterranean
countries. Data and collections were gathered in markets, nurseries, and botanical gardens, mostly in Italy,
either indoors or outdoors. New or recent records of the
following alien species are presented: Exallomochlus
hispidus (Morrison); Ferrisia virgata (Cockerell)
(Pseudococcidae); Coccus viridis (Green);
Milviscutulus mangiferae (Green) (Coccidae);
Aonidiella orientalis (Newstead); Aspidiotus destructor
Signoret; Aulacaspis tubercularis Newstead; Fiorinia
fioriniae Targioni Tozzetti; Lepidosaphes pinnaeformis
(Bouch); Pseudaulacaspis brimblecombei Williams
(Diaspididae). New data and pest status of
Phoenicococcus marlatti Cockerell
(Phoenicococcidae) and Trabutina mannipara
(Hemprich & Ehrenberg) (Pseudococcidae) are also reported. The possible repeated introductions of the latter
from North Africa to south Italy by trans-Mediterranean
winds, is hypothesized.

G. Pellizzari
Universit di Padova, Dipartimento di Agronomia, Animali,
Alimenti, Risorse Naturali e Ambiente DAFNAE,
35020 Legnaro, Italy
e-mail: giuseppina.pellizzari@unipd.it
F. Porcelli (*)
Universit di Bari Aldo Moro, Dipartimento di Scienze del
Suolo, della Pianta e degli Alimenti DiSSPA sez. Entomologia
e Zoologia,
70126 Bari, Italy
e-mail: francesco.porcelli@uniba.it

Keywords Global trade . Global warming . Invasive

species . Ornamentals . Urban entomology

Introduction
The trade of exotic trees, ornamentals and fruits is
responsible for many accidental introductions of insects
to countries far away from their native area (Mazzeo
et al. 2014; Pellizzari & Dalla Mont 1997). The arrival
of infested plants in greenhouses allows pest survival,
their reproduction and spread inside and among countries, with the possibility to become indoor pests or, in
the warmer Mediterranean countries, to spread
outdoors.
Scale insects (Coccoidea) are among the most common insects arriving with plants and fruit trade because
of their small size and the ability to hide in protected
parts of the plants, thus escaping visual inspection by
quarantine officers (Pellizzari & Germain 2010). The
introduction of alien scale insects on their host plants
has a long history and started very early in the past,
possibly with the plant trade (Maniero 2000). In recent
years, some alien scales arrived and spread rapidly in
European and Mediterranean countries. For example,
since 1999 the Nearctic mealybug Phenacoccus
peruvianus Granara de Willink (Pseudococcidae) has
spread through Corsica, mainland France, Portugal,
mainland Spain, Majorca, Sicily and United Kingdom
(in glasshouses), mostly on potted Bougainvillea
(Nyctaginaceae) plants, and presently is common outdoors in the Mediterranean (Beltr et al. 2010).

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Phytoparasitica

Aulacaspis yasumatsui Takagi (Diaspididae) spread

quickly as an indoor pest of cycads throughout Europe
(Bulgaria, Croatia, France, Germany, Great Britain, the
Netherlands, Slovenia) (Germain 2002; Malumphy &
Marquart 2012; Masten Milek et al. 2008; Trencheva
et al. 2010). Other alien species have a restricted known
distribution or are possibly overlooked. For example,
Fiorinia phoenicis Balachowsky (Diaspididae) is
known only from a single record outdoors on a palm
in Valencia (Spain) (Seljak & Matile-Ferrero 2012); or
Hypogeococcus pungens Granara de Willink
(Pseudococcidae), a pest of Cactaceae, so far recorded
only in France, Greece, Italy (mainland and Sicily) and
Spain (Beltr & Soto 2011; Ben-Dov et al. 2002;
Mazzeo et al. 2008), but is surely more widely distributed due to the large trade of succulent plants and
exchange by hobbyists.
Occasional inspections of imported trees, ornamentals and fruits in markets, nurseries, botanical gardens,
parks and gardens carried out mostly in Italy from 2010
to 2013 led to the detection of several scale insects that
could become indoor or outdoor pests. Moreover, we
refer to current findings and outbreaks of
Phoenicococcus marlatti Cockerell (Phoenicoccidae)
and Trabutina mannipara (Hemprich & Ehrenberg)
(Pseudococcidae). Both species were once rare in Italy.

Materials and methods

Specimen depositories The Scientific Museums of the
University of Padova (Italy), Department of Agronomy,
Food, Natural Resources, Animals and Environment
Entomology: DAFNAE; the Scale Insect Collection,
Universit degli Studi di Bari Aldo Moro, Dipartimento
di Scienze del Suolo, della Pianta e degli Alimenti
DiSSPA sez. Entomologia e Zoologia, Bari, Italy.
Material examined
Phoenicococcus marlatti slides: 1420/1-6, dry material:
130a & 326a DiSSPA; Trabutina mannipara slides:
1241/1-2, dry material: 624a & 633a DiSSPA;
Exallomochlus hispidus slides: 1693/1-12 DAFNAE;
Ferrisia virgata slides: 1169/1-3 DAFNAE; Coccus
viridis slides: 1774/1-2 DAFNAE; Milviscutulus
mangiferae: 1779/1-7 DAFNAE; Aonidiella orientalis
slides: 1635/a/1-7 DAFNAE; Aspidiotus destructor

slides: 1778/1-3 DAFNAE; Aulacaspis tubercularis

slides: 1773/1 DAFNAE; Fiorinia fioriniae slides:
1729/1-4 DAFNAE; Fiorinia pinicola slides: 1129/1-6
DAFNAE; Lepidosaphes pinnaeformis slides: 32, dry
material: 130 & 326 DiSSPA; Pseudaulacaspis
brimblecombei slides: 1753/1-3 DAFNAE.

Results
Fam. Phoenicococcidae
Phoenicococcus marlatti Cockerell (Fig. 1a,b)
This small species is native to the Middle East and
North Africa, where it is regarded as a pest of date palm,
Phoenix dactylifera (Arecaceae). It was reported by
Silvestri (1934) as introduced to southern Europe,
without any other information; Balachowsky & Mesnil
(1935) recorded it in France (Antibes and Orleans). In
1993 it was first recorded in Spain (Elche palm groves),
where it became a pest (Gomez et al. 1996). The first
reliable Italian records are by Marotta & Tranfaglia
(1990), on Phoenix canariensis in greenhouses and
nurseries, and by Porcelli (1990), on P. canariensis
growing outdoors; a few years later P. marlatti was
recorded on Phoenix roebelenii in Sicily, both in nurseries and in gardens (Sinacori 1995).
In recent years this scale was found infesting ornamental plants of P. dactylifera, P. canariensis and
P. roebelenii growing outdoors in Apulia region ( Bari
and Lecce districts, Italy).
P. roebelenii-infested palms have been monitored
from 2007 to date. P. marlatti proved to develop two
three generations per year. Infestation appears as a white
fluffy wax felt on exposed part of plants that is minutely
dotted with red-brown bodies of adult females. In
concealed parts of the host plants, i.e., between unfolded
leaflets, the adult females appear as pink-dotted white
layers. Infested palms exhibit some weakness and
yellowing of the leaves. During early summer high
predation by Chilocorus bipustulatus L. and Rhyzobius
lophantae Blaisdell (Coccinellidae) has been observed
on infested palms.
Fam. Pseudococcidae
Trabutina mannipara (Hemprich & Ehrenberg, 1829)
(Fig. 1c)

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Fig. 1 (a, b) Phoenicococcus
marlatti collected outdoors on
Phoenix roebelenii near
Melendugno (Apulia region,
Italy). The plants are heavily
infested each spring and recover
partially during autumn and
winter; (c) crawlers swarming
from a group of Trabutina
mannipara females infesting
Tamarix africana in Bari (Apulia
region, Italy); (d) Ferrisia virgata
intercepted on Codiaeum
variegatum imported from Costa
Rica; (e) Coccus viridis ex
Casimiroa edulis imported from
Florida to the Botanical Garden of
Padova (Italy)

a b
c

The manna scale story is described in Danzig &

Miller (1996). T. mannipara is monophagous on
Tamarix spp. (Tamaricaceae) and is distributed in
warmer Mediterranean areas and in central Asia.
Zocchi (1971) records the status of the manna scale
in south Italy as scarce, adds some collection data and
refers to a remote outbreak that occurred in 1933.
Accurate sampling of salt cedar plantations carried
out in the town of Bari (Apulia region, Italy) from 1990
to 1997, provided the opportunity to observe a new
T. mannipara invasion, possibly due to crawlers (first
instars) being carried by winds blowing from North
Africa to southern Italian coasts. An unexpected first

outbreak was observed during the autumn of 1994 on

Tamarix africana trees planted along a promenade.
Massive infestations were found during 1995, on the
same trees and on many others in seafronts and esplanades north and south of Bari (Porcelli et al. 2004).
Despite T. mannipara being regarded as an occasional pest of Tamarix in Italy (Monaco 1977), the scale is
usually not harmful to urban trees in south Italy. On the
other hand, the unpredictable outbreaks that occurred in
recent years, possibly due to re-infestation by windborne crawlers, caused honeydew dropping and sooty
mould development, so that severe pruning of infested
trees was carried out in recreational urban areas.

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Exallomochlus hispidus (Morrison)

This species is a mealybug native to southeastern
Asia, where it is polyphagous, feeding on host plants
belonging to 28 families; it is common on cacao, although it is not recorded as a pest. Information on this
species is scarce. It occurs on stems and fruits and is
attended by the ant Dolichoderus thoracicus (Smith)
(Hymenoptera Formicidae) (Ben-Dov et al. 2013).
Specimens of this species were collected on fruits of
mangosteen (Garcinia mangostana, Clusiaceae) in November 2011 in a market in Milan (Italy) by the authors.
The scales were concealed under the bracts of the fruits,
together with a few live pupae of an ant species; the ants
swarmed in a few days and are so far unidentified.
E. hispidus was intercepted several times in Great Britain on mangosteen and rambutan (Nephelium
lappaceum, Sapindaceae) fruits imported from Indonesia and Malaysia (Williams & Malumphy 2012). According to the same authors, this species should be
considered as transient and with very little possibility
of becoming established, even under artificial
conditions.
Ferrisia virgata (Cockerell) (Fig. 1: d)
The genus Ferrisia contains several Nearctic species
and has been revised recently by Kaydan & Gullan
(2012). F. virgata is a pantropical and subtropical species and one of the most highly polyphagous mealybugs, infesting plant species belonging to 68 families. It
is a pest of many tropical and subtropical plants of
economic importance and a vector of phytopathogenic
viruses. In Europe it is frequently intercepted on
imported fruits and ornamentals (Williams &
Malumphy 2012). With regard to the Mediterranean
countries it has been known for a long time in Egypt
as a pest (Ezzat & Nada 1986), whereas in France it was
recorded outdoors only once, on Punica granatum
(Lythraceae) (Foldi 2000). In Italy specimens of
F. virgata were intercepted on Codiaeum variegatum
plants imported from Costa Rica to a nursery in Tuscany
and sent to the authors for identification. The only other
Ferrisia species present in Mediterranean countries is
F. malvastra (McDaniel), known in Israel (Ben-Dov
2005) and more recently recorded in Spain on Mirabilis
jalapa (Nyctaginaceae) (Beltr & Soto 2011).

Fam. Coccidae
Coccus viridis (Green) (Fig. 1e)

This is a neotropical species widely distributed in the

tropical and subtropical regions; it is highly polyphagous and often a pest of many tropical crops and ornamentals. Live specimens are pale green and semitransparent, with an irregular U-shaped gut with black
spots on the dorsum. Specimens have been collected on
Casimiroa edulis (Rutaceae) imported from Florida,
USA, and which arrived in September 2013 at the
Botanical Garden in Padova, Italy. C. edulis is a new
host plant of C. viridis that has been previously reported
on several other Rutaceae. In Europe an infestation of
C. viridis was reported in a tropical greenhouse in England (Malumphy & Treseder 2012). Control measures
were taken to avoid the spread of the scale in the
Botanical Garden greenhouses.
Milviscutulus mangiferae (Green) (Fig. 2a)
This species was known as Protopulvinaria
mangiferae (Green) until Williams & Watson (1990)
erected the new genus Milviscutulus to insert this species. Live specimens of M. mangiferae are very similar
to Protopulvinaria pyriformis (Cockerell) and can be
confused with the latter with the naked eye. The morphological differences between the two genera and species are highlighted by studying mounted specimens
under high-power magnification.
M. mangiferae is largely distributed in the tropical
and subtropical areas of the world and develops on
many ornamental and fruit trees, mostly on mango
(Mangifera indica, Anacardiaceae). In the Mediterranean basin it is recorded in Israel only, where it is listed
among the pests of mango and develops three annual
generations (Ben-Dov 2012; Wysoki et al. 1993). According to C. Malumphy (personal communication,
2014) it is one of the most frequently intercepted species
of coccid in the UK.
Mango trees, imported from Florida, arrived at the
Botanical Garden in Padova, Italy, in September 2013.
Subsequent inspections revealed the presence of live
M. mangiferae adult females, eggs and crawlers on the
underside of leaves; several leaves were covered with
sooty mould. Control measures were taken to avoid the
spread of the scale in the greenhouses; nevertheless, live
specimens were found in April 2014.
The similar species P. pyriformis (Cockerell)
(Fig. 2b) is presently acclimatized in several Mediterranean countries, where it is a pest of ornamentals and
occasionally of lemon trees (Suma & Cocuzza 2010). It
is present and widespread in France, mainland Italy,
Sicily, Israel, Greece, Portugal, Spain (Ben-Dov et al.

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Fig. 2 (a) Milviscutulus
mangiferae ex Mangifera indica
imported from Florida to the
Botanical Garden of Padova
(Italy); (b) Protopulvinaria
pyriformis, an invasive pest
species recorded in Sardinia; (c)
live Aonidiella orientalis
introduced from Florida (USA);
(d) Aspidiotus destructor
infesting leaves of Caryota mitis,
Padova (Italy); (e) Fiorinia
fioriniae ex Ocotea foetens
growing outdoors in Lisbon
(Portugal); (f) Fiorinia pinicola
collected in Genova (Italy) on
Pittosporum tobira; (g)
Lepidosaphes pinnaeformis
collected off Cymbidium cv. in
Liguria and Apulia (Italy),
prosomal spur in inset (h)

f g

2013) and on the islands of Crete (Jansen et al. 2010)

and Malta (Mifsud & Porcelli 2012). It was recently
detected by the authors also in Sardinia (Pula, Cagliari
district, April 2012), on Schefflera actinophylla and
S. arboricola Variegata (Araliaceae).
Fam. Diaspididae
Aonidiella orientalis (Newstead) (Fig. 2 c)
The female scale is round, flat and yellowish-white,
with sub-central exuviae. It is a highly polyphagous
scale insect, a pest of several agricultural crops and is
widely distributed in tropical and subtropical regions of

the world. It has been present in Israel since 1990 (BenDov & Wysoki 1990) and in Egypt since 1988
(Mohammad et al. 2001); in Egypt it was also recorded
by the authors on ornamental Ficus (Moraceae) and
Rosa (Rosaceae) (Tebe, Luxor, October 2010). It has
been intercepted several times in Great Britain since
1996, mostly on imported mango and guava fruits and
recorded also in a greenhouse on Dictyosperma and
Cocos (C. Malumphy, 2014, personal communication).
Live specimens have been collected on leaves of
Cocos nucifera (Arecaeae) imported from Florida
(USA) to the Botanical Garden of Padova (Italy) in
September 2013.

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Aspidiotus destructor Signoret (Fig. 2d)

The female cover is circular, flat, whitish and semitransparent, with central exuviae; the male cover is oval.
This species is widely distributed in the tropical countries, is highly polyphagous and its main hosts include
coconut and other palms, a number of tropical agricultural plants (e.g. avocado, mango, papaya, breadfruit,
banana) and a wide range of ornamentals. It is a wellknown pest of coconut and severe infestations cause
extensive damage, premature drop of infested leaves
and reduction in fruit production; it is occasionally
found in greenhouses on foliage plants (Miller & Davidson 2006).
With regard to the Mediterranean countries, it was
listed by Ezzat (1958) among the Diaspididae of Egypt,
but deleted in the subsequent list (Ezzat & Nada 1986).
In Europe, it was listed in France and Great Britain
among the scales of greenhouses (Germain & MatileFerrero 2005; Malumphy 2009), mostly on Raphis sp.
(Arecaceae) and palms, and recorded in Slovenia by
Seljak (2010) on ornamental Dracaena marginata
(Dracaenaceae).
An infestation by A. destructor was noticed (in September 2013) on the leaves of Caryota mitis (Arecaceae)
imported from Florida to the Botanical Garden in Padova, Italy. The scales settled on the lower and upper
surface of the leaves. This species could become a pest
in greenhouses and households.
Aulacaspis tubercularis Newstead
The female cover is circular, flat and white, with dark
exuviae near the margin; the male covers are white,
el ong ate d a nd tr i c ar i n at e , o f t e n i n gro up s .
A. tubercularis is widely distributed in tropical areas,
is a polyphagous species and a well recognized pest of
mango in many countries. It was intercepted several
times in Great Britain on imported plants and fruits (C.
Malumphy 2014, personal communication). The species was present in Egypt and Israel in the past
(Balachowsky 1954), but was not recorded there in
subsequent checklists (Ben-Dov 2012; Ezzat & Nada
1986); Porcelli (1990) collected A. tubercularis specimens on mango trees growing outdoors in a nursery in
Sicily. No other records are known so far in the Mediterranean area. Dead and live A. tubercularis males and
females were detected on the leaves of mango plants
(Mangifera indica, Anacardiaceae) imported from Florida (USA) to the Botanical Garden in Padova (Italy) in
September 2013, together with M. mangiferae.
Fiorinia fioriniae Targioni Tozzetti (Fig. 2e)

This is a polyphagous and cosmopolitan species; it is

acclimatized in North African countries and Israel,
where it is regarded as a pest of avocado and palms
(Ben-Dov et al. 2013). In the Mediterranean areas of
Turkey it occurs outdoors on palms and ornamentals
(Kaydan et al. 2007), whereas in European countries it
was recorded so far in greenhouses only (Germain &
Matile-Ferrero 2005).
Specimens of F. fioriniae were collected in 2012 on
leaves and fruits of Ocotea foetens (Lauraceae) growing
outdoors in Lisbon (Portugal). This record points out its
possibility to survive outdoors in the warmer European
countries. Until now it was known outdoors only in the
Portuguese archipelagos of Azores and Madeira and on
the Canary Islands (Spain) (Ben-Dov et al. 2013; Franco
et al. 2011).
Fiorinia pinicola Maskell (Fig. 2f)
The oriental diaspidid F. pinicola was known in
Europe for a long time in Portugal only (Sintra), on
Podocarpus neriifolia (Franco et al. 2011). It was first
recorded in Italy in 2004 on hedges of Pittosporum
tobira (Pittosporaceae) in a park in Genova (Liguria
Region, Italy) (Pellizzari 2005). The leaves displayed
yellow spots on the upper surface, whereas the scales
settled on the lower surface. In 2012, 8 years later, the
same place was checked again and the scale was still
present at a high population density, so it appears to be
fully acclimatized.
Lepidosaphes pinnaeformis (Bouch) (Fig. 2g, h)
This species was recorded in greenhouses in several
north European countries, mostly on Cymbidium
(Orchidaceae), and is a common indoor scale in Great
Britain (Ben-Dov et al. 2013; Malumphy et al. 2012).
Many specimens of this mussel-like species were recorded on Cymbidium cv. at two nurseries: one located
in north Italy (Bastia DAlbenga Savona district, Liguria
region) the other in south Italy (Castellana Grotte, Bari
district, Apulia region). In Apulia region the plants were
cultivated outdoors, in the shade, for sale as flowering
plants, so that they were re-potted depending on the
need. Many plants grow there for 4 years before being
sold and the scales were acclimatized in the rather cold
winter climate of the area, like the Cymbidium plants,
that are considerably more cold-tolerant than other
popular orchids. The observed infestation varied from
mild to moderate, but the orchids flowered abundantly
over the years. No evidence of natural enemies was
observed. L. pinnaeformis has little importance in Italy
and we agree with Miller & Davidson (2005), who

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considered it an occasional pest, even if in the past it had

been a major concern for orchid growers.
Pseudaulacaspis brimblecombei Williams
This is an Australian species, developing mostly on
Proteaceae (Embothrium coccineum, Lomatia
myricoides, Macadamia, Protea nerifolia, Telopea
oreades, T. speciosissima, Telopea sp.) but occurring
also on Cordyline (Agavaceae), Libertia ((Iridaceae)
and Melicopa (Rutaceae) (Henderson 2011). It was introduced into New Zealand, where it became a pest of
the cultivated Telopea plants (Ben-Dov et al. 2013).
Some Telopea plants arrived from New Zealand to a
nursery in Tuscany, Italy, in March 2012 and some
leaves infested by a scale were sent for identification
to the authors in December 2012. Only after that were
the plants exported from Italy to Great Britain and found
to be infested by the diaspid, which developed in greenhouses during the summer (Malumphy & Halstead
2012).
The cultivation of ornamental Proteaceae is increasing in some Mediterranean countries and is based mostly on plants imported from South Africa, Australia and
New Zealand and then resold in other European countries, thereby increasing the risk of incidental introductions of pests.

Comments
Apart from F. pinicola, that proved to be already acclimatized in the mild climate of Liguria Region (north
Italy) and L. pinnaeformis, surviving outdoors in south
Italy, most of the above mentioned scale species are
unlikely to survive outdoors even in southern European
countries, whereas they have the potential to become
pests in greenhouses and households. Nevertheless, the
climate change could play a role in the possible spread
and establishment outdoors, mostly in urban environments, of species previously known as indoor pests
only. For instance Chrysomphalus aonidum (L.) was
known in Europe as a pest of ornamentals (mainly
Dracaena and Kentia plants) in greenhouses. This species was observed in 1999 infesting orange trees and
ornamentals growing outdoors in Valencia (Spain) and
in a few years it spread in Citrus groves and the urban
environment (Garcia Mari et al. 2000). In 2006
C. aonidum was recorded for the first time outdoors,
on ornamental Citrus trees, in southern Italy (Pellizzari
& Vacante 2007) and in the same year on Citrus and

ornamentals in southern Greece, where this species was

considered unlikely to become acclimatized (Stathas &
Kozr 2008). Finally, C. aonidum was first recorded in
2009 outdoors in mainland Portugal (Franco et al. 2011)
and presently it is established in European Citrus groves
(Pellizzari & Germain 2010; Soto et al. 2008; Suma
et al. 2013).
Global warming could play a role in the recent outbreaks of species like Phoenicococcus marlatti and
Trabutina mannipara, otherwise scarcely recorded in
the past. Changes in climate and mild winters promote
not only the northward expansion of some species (i.e.,
Pseudaulacaspis pentagona Targioni Tozzetti in central
Europe) (Kozr 1997), but also increase the chances of
survival of species introduced from warmer parts of the
world.

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