Scales ( Hemiptera , Superfamily Coccoidea ) Chapter 9 . 3

Abstract Scale insects are frequent invaders. With 129 established species, they numerically represent one of the major group of insects alien to Europe. Scales are usually small insects with wingless females. Due to this small size and concealment, many species, mainly belonging to the families Diaspididae, Pseudococcidae and Pseudococcidae, have been accidentally introduced to Europe, mostly originating from tropical regions and essentially from Asia. Th e trade of fruit trees and ornamentals appears to be the usual pathway of introduction. At present, alien scales represent an important component of the European entomofauna, accounting for about 30% of the total scale fauna.


Introduction
Coccoidea or scale insects is a large superfamily in the order Hemiptera with a worldwide distribution.Th ey are unusually small insects, highly specialized for plant parasitism, that have evolved diff erent kinds of metamorphosis depending on sex and family.Scale insects are characterized by sexual dimorphism: females are wingless, usually small (from 0.5 -10mm), with an oval or round but fl at to fairly convex body form, sometimes bud shaped, and often protected by waxy secretions or covers.Th e adult females may exhibit reduction or loss of appendages, depending on family and instar, and are often sedentary or sessile.Adult males are usually winged and inconspicuous, do not feed and live a few days.Scale insect identifi cation is mainly based upon the morphology of adult females that persist on the host plant longer than the other stages.
Females usually take three or four developmental stages to reach maturity, males usually fi ve.Parthenogenesis is quite common.Eggs are usually laid under the female body, under the scale cover, or in waxy egg-sacs.Dispersal is carried out by fi rst instars.
Scale insects feed on various parts of the host plant (leaves, fruits, stems, branches and roots) and are frequently introduced and acclimatized in diff erent parts of the world.Th is is due to their small size (fi rst instars are about 0.2-0.3mm;adult females usually are from 0.5 to10mm long) and their concealment using waxy secretions; beside many species live in hidden habitats (under leaf sheaths, in bark crevices or on roots) so that they can easily escape visual quarantine inspections.Once in a new territory, parthenogenesis and high fecundity favour quick colonization starting from a few females: for example, a single female Neopulvinaria innumerabilis may lay up to 8000 eggs (Canard 1968).

Taxonomy of the scale species alien to Europe
According to Ben-Dov et al. (2006) the superfamily Coccoidea comprises 22 families, with more than 7300 described species.In Europe, native representatives of 12 families have so far been recognized.On the basis of the best known western and central European coccoid faunas (France, Italy, Hungary) (Ben-Dov et al. 2006, Foldi 2001, Pellizzari and Russo 2004), the total number of scale insects present in Europe is likely to reach about 400-450 species.Aliens recorded in Europe up until 2007 account for 129 species which include the following eight families: Diaspididae (60 species), Pseudococcidae (37), Coccidae (23), Eriococcidae (3), Margarodidae (2), Asterolecanidae, Ortheziidae, and the alien family Phoenicococcidae, each with one species (Table 9.3.1).Unlike for other taxa, aliens represent an important component of the scale fauna currently present in Europe,i.e. near 30% (Fig. 9.3.1).
Th e remaining fi ve native families (Aclerdidae, Cerococcidae, Kermesidae, Lecanodiaspididae, Micrococcidae) each have one or two species in Europe: none of them is a pest, with the exception of the family Kermesidae (8 species in Europe), in which Kermes vermilio and Nidularia pulvinata exhibit outbreaks in urban environments only.
One species, Dactylopius coccus Costa, representing the alien family Dactylopiidae, has been included among aliens to Europe, even though it is present only in Canary islands, Madeira and Azores, where it was intentionally introduced.Th ese islands belong politically to Europe (Spain, Portugal) but biogeographically they belong to Macaronesia, a biogeographic Atlantic region quite distinct from the European continent and with a unique fl ora and fauna.

Diaspididae
Armoured scale insects are the commonest alien scales incidentally introduced all over the world: this is probably due to their small dimension and camoufl age.Th e 60 alien species account for nearly half (44.6%) of an estimated 130 species in Europe.Many notorious pests of fruit trees such as Pseudaulacaspis pentagona (the white peach scale-see factsheet 14.45)) and Diaspidiotus perniciosus (San José scale -see factsheet 14.44)) belong to this family: these species are still pests of fruit trees in spite of the introduction of specifi c parasitoids from their native area.Th e Asiatic armoured scales of Citrus are largely found in European Citrus groves and presently number 10 species.Th eir "invasion" started around 1850 with Parlatoria ziziphi and Lepidosaphes becki and is still going on with the arrival and establishment of Unaspis yanonensis (1969), Aonidiella citrina (1994), Chrysomphalus aonidum (2000).Several armoured scales commonly occur throughout European greenhouses (e.g.Diaspis echinocacti, Chrysomphalus dictyospermi, Diaspis bromeliae, Abgrallaspis cyanophylli), even if they cannot be considered as established.In some cases, species recorded only in greenhouses in northern and central Europe are established outdoors in southern countries (i.e.Furchadaspis zamiae, Chrysomphalus aonidum).Some armoured scales thought to be of Afrotropical origin or cryptogenic (e.g.Aspidiotus nerii, Hemiberlesia lataniae, H. rapax) are very common in natural habitats of the Mediterranean countries (including small islands).

Pseudococcidae
Mealybugs are covered with mealy or cottony wax, have a distinct segmentation and are mobile.Th e 37 alien mealybugs account for roughly one fourth (25.7%) of the ca.140 European species and most of them are polyphagous.Planococcus citri, Pseu- dococcus longispinus, P. viburni and P. calceolariae arrived and established during the 19th century and are presently the most common species on ornamental plants, both outdoors and indoors.P. citri, fi rst recorded in 1813, is still a pest of Citrus and ornamental plants.Several mealybugs have been recorded in only one or two countries to date (e.g.Palmicultor palmarum, Phenacoccus madeirensis, Rhizoecus americanus, Trochiscococcus speciosus), both outdoors and in greenhouses, on ornamental plants.

Coccidae
About 70 species of soft scales are recorded in Europe.Of these, there are 23 aliens to Europe representing 32.8% of the fauna, and are mainly pests of fruit trees and ornamentals.Among them, the polyphagous Coccus hesperidum and Saissetia oleae, the well-known Mediterranean Black Scale, are probably the most ancient arrivals which established in the countries surrounding the Mediterranean Basin.Most recent arrivals are Pulvinaria hydrangeae, P. regalis (see factsheet 14.41), Ceroplastes japonicus and, in warmer places, Protopulvinaria pyriformis, invasive on trees and ornamental plants in urban environments.Some species, such as Coccus pseudomagnoliarum, after fi rst spreading in Mediterranean Citrus groves, later became more localised and less common.On the other hand, the American Pulvinaria innumerabilis is still considered a pest of vine, more than 40 years after its arrival in European vineyards.Several species (e.g.Saissetia coff eae, S. oleae, C. hesperidum, Eucalymnatus tessellatus, Parasaissetia nigra) are rather common in greenhouses of central and northern Europe, while in southern Europe are outdoors pests.

Eriococcidae
European felt scales number about 50 species.Among them, only three alien felt scales have been so far recorded.Th e Australian Eriococcus araucariae is widespread on Araucaria trees growing in Mediterranean countries, the American E. coccineus is recorded on succulent plants and Ovaticoccus agavium is quite common on Agave sp.growing outdoors.

Margarodidae
European margarodids recorded up until now number 15 species.Two alien margarodids, Icerya purchasi (the cottony cushion scale) and I. formicarum, invaded Europe at very diff erent times.Th e latter species is known from a single record in 2001 in Corsica and its establishment is unknown.On the other hand, the Australian I. purchasi has both established and caused an agricultural and environmental impact.It arrived and established in many Mediterranean countries between the end of 1800 and the fi rst decades of 1900 and was very destructive to Citrus groves.Th e high infestations led to the introduction of the Australian coccinellid Rodolia cardinalis, for biological control.Presently, the cottony cushion scale is mainly a pest of ornamental plants such as Pittosporum, Acacia and Mimosa.It is also a very common species in semi-natural habitats (i.e. the Mediterranean maquis), far away from cultivated areas, where it develops on autochthonous wild plants such as Cistus, Genista, Smilax and Rosmarinus.Two other margarodids, Marchalina hellenica and Matsucoccus feytaudi, are alien in Europe, entirely due to deliberate introduction.

Asterolecanidae
About 10 species of asterolecanids are present in Europe.Of these, the only alien pit scale is the Asiatic Bambusaspis bambusae, a species associated with bamboos.

Ortheziidae
Ortheziids consist of 10 species in Europe.Among these, Insignorthezia insignis, a polyphagous Neotropical species, has been reported in European greenhouses since the end of 19th century.Apparently I. insignis is established outdoors only in Portugal and France.

Phoenicococcidae
Phoenicococcus marlatti, the Red Date Palm Scale, thought to originate in the Middle East or North Africa, is the only species currently placed in the family Phoenicococcidae.It is considered a minor pest of commercial dates, whereas in Spain, France and Italy, it infests ornamental palms (mainly Phoenix canariensis).

Temporal trends of introduction in Europe of alien scale species
Fig. 9.3.2.presents the temporal variation in the mean number of new alien species recorded per year since 1492.Serious studies of the Coccoidea began in mid 19th century.From that time, to the mid-1970s, the introduction of alien species was relatively constant, averaging 0.66 species per year.Since then, there is an apparent increase in alien introductions, up to an average of 1.15 species per year.
In interpreting this chart, account should be taken of "old" alien species, found and described in Europe, (i.e.Aspidiotus nerii, Planococcus citri, Coccus hesperidum, Saissetia oleae) for which the introduction date is based only on the date of their fi rst description.In the case of the most harmful alien scales, the date of fi rst introduc-tion to Europe and the chronology of their invasion is known more precisely (i.e. for Pseudaulacaspis pentagona, Icerya purchasi, Diaspidiotus perniciosus).Moreover, records of alien scales depend on the presence of specialists in a given country.For instance, during the 1970-80s, advances in systematic knowledge and the increasing number of active coccidologists led to the "discovery" of several species which have probably been introduced a long time before.Th e great rise in the global exchanges of plants and quarantine inspections can explain the increases in subsequent years up until the present.
Among the scale insects introduced to Europe from the end of 19 th century to 1960s there are several pests of fruit trees and Citrus (i.e.Diaspidiotus perniciosus, Lepidosaphes gloverii, Pseudaulacaspis pentagona, Ceroplastes sinensis, Icerya purchasi), whereas in the last 40 years the most numerous introduced scales are pest of ornamental plants, both outdoors and indoors (i.e.Pulvinaria regalis, P. hydrangeae, Ceroplastes japonicus, Protopulvinaria pyriformis, Parassaisetia nigra, Trochiscococcus speciosus), the main scale of agricultural importance being Neopulvinaria innumerabilis, a pest of vine.

Origin of the alien species
Th e geographical origin of introduced scale insects shows a large dominance of species from tropical areas, essentially Asia, followed by southern American species (Fig. 9.3.3).Th e precise origin remains unknown for about one fourth of alien scales.Among the most widespread aliens to Europe are Diaspidiotus perniciosus of temperate Asian, Planococcus citri from tropical Asia, Ceroplastes sinensis from Central-America, Parthenolecanium fl etcheri from Northern-America, Saissetia oleae from the Afrotropics, Icerya purchasi from Australasia, and Lepidosaphes beckii as cryptogenic species.

Distribution of the alien species in Europe
It should be borne in mind that, as for the other arthropod groups, the number of records of alien scales in European countries, refl ects, in part, diff erences of study intensity and the number of local taxonomists.Moreover, the geographic position of some countries such as France, Italy and Spain, whose climatic conditions vary from high montane, continental to Mediterranean, allows establishment of species from very diff erent geographical areas.Two countries present a particularly high number of alien species: France with 90 species and Italy with 92 species (Fig. 9.3.4).Lagging far behind are Spain, Great Britain and Portugal with 50, 43 and 41 species, respectively.Th e islands of the Atlantic, not represented in the fi gure, have respectively 51 aliens in the Canaries, 44 in Madeira and 22 in the Azores.Th ere are 12 alien species recorded in at least 20 countries, namely Coccus hesperidum (28 countries), Pulvinaria fl occifera (21), Saissetia coff eae (24), S. oleae (26), Aspidiotus nerii (26), Diaspidiotus perniciosus (26), Pinnaspis aspidistrae (20), Pseudaulacaspis pentagona (21), Planococcus citri (22), Pseudococcus longispinus (22) and P. viburni (26).Th ese are all polyphagous species, with the exception of Unaspis euonymi, monophagous on Euonymus spp., recorded in 22 countries.A total of 20 species (15%) are present only in one country.

Scale species alien in Europe
With regard to scale insects alien in Europe, that is originating from another European area where native and introduced through human activity, only very few certain cases are known.Marchalina hellenica is native to Turkey and Greece and presently invasive in the small island of Ischia (Italy).It was introduced there in 1960 to study endosymbiosis, but unfortunately escaped from laboratory breeding and presently is a pest of pines (Tranfaglia and Tremblay 1984).Matsucoccus

Pathways of introduction in Europe of alien scale species
Scale insects are highly specialized, sedentary, plant-parasitic insects and the only pathway of introduction is the horticultural and ornamental trade: importation and trade  of fruit and Citrus trees, ornamental trees and bushes, bulbs and corms, has led to incidental introduction and subsequent spread of scale insects.More recently, the "fashion" of succulent plant cultivation and the subsequent increase in plant importation and plant exchanges among collectors is responsible for the introduction and spread of several species such as Delottococcus euphorbiae, Hypogeococcus pungens, Trochiscococcus speciosus, Vryburgia rimariae, Spilococcus mamillariae and Eriococcus coccineus.Importation of bonsais from Asia could allow the introduction and spread of Rhizoecus hibisci, a mealybug living on roots and recently intercepted several times by European quarantine services.

Ecosystems and habitats invaded in Europe by alien scale species
Alien, established scale insects colonize strongly anthropogenic habitats such as cultivated agricultural lands, horticultural and domestic habitats, urban environments, gardens and parks, botanic gardens, nurseries and greenhouses, but they have also spread to natural habitats.Mediterranean Citrus groves host a large community of alien scales: 18 diff erent species have been so far recorded.Th ese are: Icerya purchasi Planococcus citri, Pseudococcus calceolariae, P. longispinus, Ceroplastes sinensis, Coccus hesperidum, C. pseudomagnoliarum, Saissetia oleae, Aonidiella aurantii, A. citrina, As-  pidiotus nerii, Chrysomphalus dictyospermi, C. aonidum, Lepidosaphes beckii, L. gloverii, Parlatoria pergandii, P. ziziphi and Unaspis yanonensis.Some polyphagous scales are urban pests, largely distributed in urban parks and gardens, on trees and ornamentals (i.e.Pulvinaria regalis, P. hydrangeae, Ceroplastes japonicus), whereas they are absent or very rare in the countryside.A few monophagous species are only known in Botanical gardens, where they persist outdoors, at a low population levels, on exotic plants Several other monophagous species remain strictly associated to their original, exotic ornamental plants, and have a correspondingly wide distribution in Europe (i.e.Parthenolecanium fl etcheri, Pulvinaria mesembryanthemi, Eriococcus araucariae).On the other hand, some polyphagous species (i.e.Diaspidiotus perniciosus, Pseudaulacaspis pentagona, Pulvinaria fl occifera) have spread from cultivated areas to natural woodland and forest habitats (Balachowsky 1932b, Balachowsky 1936).Others (Antonina graminis,

Impact of alien scale species
Scale insects are plant pests, especially of fruit trees, woody ornamentals, forest trees and greenhouse plants.Th ey cause damage to plants by sap sucking.Moreover, except for Diaspididae and Asterolecaniidae, they excrete honeydew that covers leaves and fruits and allows the development of sooty mould.Th is black sooty mould can reduce photosynthesis by 70%, leading to early senescence, with smaller and premature fruits, and loss of aesthetic value (Mibey 1997).Moreover, Coccidae and Pseudococcidae are vectors of closteroviruses.For example, Planococcus citri and Pulvinaria innumerabilis may transmit the Grapevine Leafroller-associated Virus (GLRaV-1, GLRaV-3) and the Corky Bark disease (GVA, GVB) (Sforza et al. 2003, Zorloni et al. 2006).Diaspididae cause discolouration on leaves, red or black spots on fruits, and twig dieback.Pesticides are commonly applied to control scale insects in fruit orchards and Citrus groves.Infestations of alien scales in orchards have led to the introduction to Europe, from their native area, of many natural enemies for biological control purposes.Polyphagous Balachowsky (1953) Parlatoria ziziphi (Lucas, (1996)

Figure 9
Figure 9.3.1 Taxonomic overview of the scale species alien to Europe compared to the native fauna.Species alien to Europe include cryptogenics.

Figure
Figure 9.3.2Temporal trends in the mean number of new records per year of scale species alien to Europe from 1492 to 2007.Th e number above the bar indicates the absolute number of species in this time period.

Figure
Figure 9.3.3Geographic origin of the scale species alien to Europe.

Figure 9
Figure 9.3.4Numbers of established alien scale species in the European countries and main islands according to Table 9.3.1.Archipelago: 1 Azores 2 Madeira 3 Canary islands.

Table 9 .3.1.
List and main characteristics of the scale species alien to Europe.Status: A: Alien to Europe; C: cryptogenic specie s.Country codes abbreviations refer to ISO 3166 (see appendix I).Habitat abbreviations refer to EUNIS (see appendix II).Only selected references are given.Last update 29/05/200 Family Species Status

Table 9 .
3.2.List and main characteristics of the scale species alien in Europe.Country codes abbreviations refer to ISO 3166 (see appendix I).Habitat abbreviations refer to EUNIS (see appendix II).Only selected references are given.Last update 29/05/2009