Alien Pests Can Spread Quickly: Wooly Ash Aphid Prociphilus fraxinifolii (Hemiptera: Eriosomatidae) Has Occupied Europe in 18 Years

: Prociphilus fraxinifolii (woolly ash aphid) is a pest of ash trees ( Fraxinus spp.). This species, which is native to North America, was ﬁrst recorded in Europe in 2003, in Budapest, and then began to spread quickly. In 2019–2021, we ﬁrst detected P. fraxinifolii in Belarus (Brest) and eight regions of European Russia, namely Astrakhan, Nizhny Novgorod, Samara, Saratov, Smolensk, Tambov, Volgograd and Voronezh regions. By 2021, P. fraxinifolii has spread over a vast territory in Europe: from Spain in the west to the Volga River in the east. The distance between the westernmost and easternmost localities is 4180 km. The known range is disjunctive: Armenia, Belarus, Bulgaria, Germany, Great Britain, Hungary, Poland, Romania, Spain and 16 regions of European Russia. This case indicates that some alien pests are able to occupy the whole of Europe in less than two decades after the ﬁrst record in the continent. It is known that P. fraxinifolii can infest native ash species F. excelsior , but all our ﬁndings, as well as most ﬁndings indicated in the literature, were on F. pennsylvanica introduced from North America. We never found P. fraxinifolii on F. excelsior even near infested F. pennsylvanica trees.


Introduction
New alien insects from other continents appear and establish in Europe every year [1]. Once established, most alien species do not spread throughout Europe, with about 40% of the species only present in one or two countries [2]. However, some species, including pests, occupy the whole continent quickly [2]. The current article is about one such quickly spreading alien pests-Prociphilus (Meliarhizophagus) fraxinifolii (Riley, 1879) (Hemiptera: Eriosomatidae).
In 2019-2021, we surveyed ash trees in different regions of European Russia and Belarus, because we were involved in the project on the emerald ash borer Agrilus planipennis Fairmaire, 1888 [16]. During these surveys, we noticed P. fraxinifolii in many localities and found out that its current range is much wider than was supposed before. Here we present the information about our findings and summarize all available information about the current distribution of P. fraxinifolii in Europe.

Collection
In 2019-2021, we examined about 2500 F. pennsylvanica and more than 1000 F. excelsior trees in nine regions of European Russia and one region of Belarus (Table 1). In 2019-2021, we monitored the distribution of P. fraxinifolii in Zelenograd City (Moscow Region), where the pest was discovered first in 2017 [12]. When we detected the characteristic leaf nests (Figure 1), we collected aphids, placed them in alcohol and then examined them in the laboratory. The specimens were deposited in the collection of the second author.
(a) (b) Mature and immature apterous viviparous females of P. (M.) fraxinifolii are pale green or pale yellow. Nymphs pale green with thorax pale yellow. Alate viviparous females have grey head and thorax and pale green abdomen. Ocelli and compound eyes (in alate females and nymphs) are black. All morphs are covered by white wax; mature and immature apterous females bear thick curved white wax threads.

Results
We have detected P. fraxinifolii in 28 localities of nine regions of European Russia and in one locality in Belarus (Table 1 and Figure 3).

Results
We have detected P. fraxinifolii in 28 localities of nine regions of European Russia and in one locality in Belarus (Table 1 and Figure 3).
Prociphilus fraxinifolii was detected both in artificial plantings of F. pennsylvanica (urban, roadside and field protection plantings) and in self-seeding trees in riparian forests. The rate of infestation varied from 1 to 30% of F. pennsylvanica trees examined in each locality. The leaf nests usually are seen on seedlings or epicormic shoots, but sometimes also on the branches of large trees. Usually the pest infests from one to five trees standing nearby, while other trees of F. pennsylvanica in the same street or park have no signs or symptoms of infestation. Groups of infested trees are scattered throughout the city.
Prociphilus fraxinifolii was never found to infest F. excelsior in European Russia. Examination of more than 1000 European ash trees (F. excelsior) in seven localities has not revealed any cases of infestation, even in the presence of infested F. pennsylvanica in these localities ( Table 1).
Monitoring of P. fraxinifolii in Zelenograd (Moscow Region) has shown that almost all trees, that were found to be infested in 2017 were still infested by the pest in 2021. Moreover, new infestations in other streets of the city were detected. It indicates that P. fraxinifolii has been established in the city, and its population is likely to increase rather than decrease. In spite of this, the economic effect of the pest in the city seems insignificant (at least for now). Some trees have lost their ornamental value because of the leaf nests, but no cases of trees killed by the pest have been recorded. The same situation was observed in other regions examined. Prociphilus fraxinifolii has become common, especially in the southern regions, but it seems that it does not kill the trees. Prociphilus fraxinifolii was detected both in artificial plantings of F. pennsylvanica (urban, roadside and field protection plantings) and in self-seeding trees in riparian forests. The rate of infestation varied from 1 to 30% of F. pennsylvanica trees examined in each locality. The leaf nests usually are seen on seedlings or epicormic shoots, but sometimes also on the branches of large trees. Usually the pest infests from one to five trees standing nearby, while other trees of F. pennsylvanica in the same street or park have no signs or symptoms of infestation. Groups of infested trees are scattered throughout the city.
Prociphilus fraxinifolii was never found to infest F. excelsior in European Russia. Examination of more than 1000 European ash trees (F. excelsior) in seven localities has not revealed any cases of infestation, even in the presence of infested F. pennsylvanica in these localities ( Table 1).
Monitoring of P. fraxinifolii in Zelenograd (Moscow Region) has shown that almost all trees, that were found to be infested in 2017 were still infested by the pest in 2021. Moreover, new infestations in other streets of the city were detected. It indicates that P. fraxinifolii has been established in the city, and its population is likely to increase rather than decrease. In spite of this, the economic effect of the pest in the city seems insignificant (at least for now). Some trees have lost their ornamental value because of the leaf nests, but no cases of trees killed by the pest have been recorded. The same situation was observed in other regions examined. Prociphilus fraxinifolii has become common, especially in the southern regions, but it seems that it does not kill the trees.

General Distribution in Europe
Prociphilus fraxinifolii has not been recorded in Belarus before. This species is absent in the review of the Aphids of the family Eriosomatidae of Belarus [24]. We have detected P. fraxinifolii in Belarus and eight regions of Europe Russia: Astrakhan, Nizhny Novgorod, Samara, Saratov, Smolensk, Tambov, Volgograd and Voronezh. These findings, as well as recent findings in seven other regions of European Russia (Moscow Region, Rostov Region, Crimea, Krasnodar Territory, Republic of Kalmykia, Stavropol Territory, Kabardino-Balkaria and North Ossetia) [12,20] and in Armenia [15], indicate that P. fraxinifolii has become widespread and common in Eastern Europe.
There is no reliable information about pathways of spread of P. fraxinifolii in European Russia and Belarus. It was hypothesized that P. fraxinifolii could arrive from one region of Europe to another on air currents or on nursery stock [3].
Localities of P. fraxinifolii detection in Europe form several clusters surrounded by territories, where the pest has not been found (Figure 3). This could indicate that the range is disjunctive because the pest was unintentionally introduced to some regions, while it was not introduced to others. Such disjunctive formation of range is typical for alien pests, in particular, for alien pests associated with ash trees [25]. On the other hand, the absence of findings in some territories could simply reflect the absence of surveys. Surprisingly, the information about distribution of P. fraxinifolii in Europe is scarce. There is no map or distributional information in EPPO Global Database [26]. No records of this species in Europe are included to Global Biodiversity Information Facility [27] and only one record is included to European Alien Species Information Network [28]. The surveys are necessary to reveal if P. fraxinifolii occurs in territories surrounded by the known range. There are no data for France, Switzerland, Italy and several other countries.

Host Plants and Ecological Impact
Prociphilus fraxinifolii in Europe infests mainly F. pennsylvanica introduced from North America. We have not found leaf nests of P. fraxinifolii on F. excelsior even near infested F. pennsylvanica trees. Few cases of infestation of F. excelsior native to Europe are known [3]. Thus the potential impact of the pest in different countries would be different depending on the frequency of occurrence of F. pennsylvanica. In particular, F. pennsylvanica is rather rare in Great Britain. Prociphilus fraxinifolii was recorded there only once (2011) [8] and was not found in the subsequent years (Edward A. Baker, personal communication). Fraxinus pennsylvanica is one of the most common trees in urban and roadside plantings and in field protective belts in European Russia [29]. It also is an invasive plant that has established and become abundant in river valleys. Therefore, it is not surprising that P. fraxinifolii also has become common and widespread in European Russia.
At first glance it seems that the economic and ecological impact of P. fraxinifolii is not significant even in the regions, where this pest is abundant. However, it should be taken into account that F. pennsylvanica trees in European Russia are now affected by the most serious alien pest, the emerald ash borer Agrilus planipennis. Agrilus planipennis inevitably will spread to neighboring countries soon [30]. The trees affected by A. planipennis often produce epicormic shoots to survive [31], but according to our observations epicormic shoots are very vulnerable to P. fraxinifolii. Development of P. fraxinifolii on roots and epicormic shoots potentially could worsen the condition of ash trees damaged by A. planipennis.
2. By 2021, i.e., in just 18 years after the first record in Europe, P. fraxinifolii has spread over the vast territory: from Spain in the west to the Volga River in the east. The distance between the westernmost and easternmost localities is 4180 km.
3. The known range is disjunctive and includes Armenia, Belarus, Bulgaria, Germany, Great Britain, Hungary, Poland, Romania, Spain and 16 regions of European Russia. Absence in the intervening regions could be due to lack of observations, scarcity of the host tree, F. pennsylvanica, or variable movement of infested nursery stock.