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Article

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

A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071 Moscow, Russia
*
Author to whom correspondence should be addressed.
Academic Editor: Young-Seuk Park
Forests 2021, 12(9), 1176; https://doi.org/10.3390/f12091176
Received: 7 July 2021 / Revised: 14 August 2021 / Accepted: 27 August 2021 / Published: 30 August 2021
(This article belongs to the Special Issue Prediction and Control of Alien Pests)

Abstract

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.
Keywords: Prociphilus fraxinifolii; Fraxinus pennsylvanica; ash trees; aphids; pests; insects; woolly ash aphid; ash leaf curl aphid Prociphilus fraxinifolii; Fraxinus pennsylvanica; ash trees; aphids; pests; insects; woolly ash aphid; ash leaf curl aphid

1. 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).
Prociphilus fraxinifolii (woolly ash aphid, ash leaf curl aphid) is native to North America and develops on ash trees (Fraxinus spp.) [3]. It has been established in South Africa, Chile, China, Iran and Europe [3]. It was first recorded in Europe in 2003, in Budapest (Hungary) [4], and then it was detected in Ukraine in 2005 [5], Serbia in 2006 [6], Bulgaria in 2007 [7], Great Britain and Spain in 2011 [8,9], Poland in 2012 [10], Germany and Slovenia in 2015 [3,11], European Russia and Romania in 2017 [12,13,14] and Armenia in 2019 [15].
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.

2. Materials and Methods

2.1. 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.

2.2. Identification

Mature apterous and alate females, as well as immature apterous females and nymphs of alate females, were found in leaf nests in all localities. Slides of alate and apterous females were prepared in Berlese fluid and examined under the microscope. The species was identified according to Blackman and Eastop [17]. Prociphilus (M.) fraxinifolii can be distinguished from other species of the genus by the following characteristics (Figure 2). Alate females have 1–3 (1–5 after Blackman and Eastop [17]) irregularly shaped broad secondary rhinaria on antennomere 6, differing in shape from the narrow transverse secondary rhinaria on antennomere 3; antennomere 3 as long as 2.6–3.2× antennomere 2; length of antennomere 2 as long as 1.4–1.5× its width, bearing 3 or 4 hairs. Apterous adult females of P. (M.) fraxinifolii differ from morphologically close P. (Pulvius) probosceus in rostrum very short, much shorter than body, with apical segment (segments 4 + 5) with 3 accessory hairs (2 hairs after Blackman and Eastop [17]). Prociphilus probosceus has more than 10 hairs.
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.

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.

4. Discussion

4.1. 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.

4.2. 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.

5. Conclusions

1. We have first detected P. fraxinifolii in Belarus and eight regions of Europe Russia: Astrakhan, Nizhny Novgorod, Samara, Saratov, Smolensk, Tambov, Volgograd and Voronezh.
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.

Author Contributions

Conceptualization, M.J.O.-B.; investigation, M.J.O.-B. and A.O.B.; writing—original draft preparation, M.J.O.-B.; writing—review and editing, A.O.B.; visualization, M.J.O.-B. All authors have read and agreed to the published version of the manuscript.

Funding

The study was funded by the RUSSIAN SCIENCE FOUNDATION, grant number 21-74-20001.

Data Availability Statement

All new data created in this study are included to the text.

Acknowledgments

We are grateful to R.N. Ishin for the survey of ash trees in Tambov City and collecting specimens of P. fraxinifolii there, to E.A. Baker for the information about P. fraxinifolii in Great Britain, and to S. Halbert and the anonymous reviewer for the valuable comments on the manuscript.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. Leaf nests of Prociphilus fraxinifolii in different regions: (a,b) in Brest (Belarus), (c) in Nikolskoe (Astrakhan region) and (d) in Nizhny Novgorod.
Figure 1. Leaf nests of Prociphilus fraxinifolii in different regions: (a,b) in Brest (Belarus), (c) in Nikolskoe (Astrakhan region) and (d) in Nizhny Novgorod.
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Figure 2. Prociphilus fraxinifolii collected from leaf nests. (a) Adult apterous female with embryons collected in Kantemirovka (Voronezh Region) and (b) alate female collected in Sychevka (Smolensk Region).
Figure 2. Prociphilus fraxinifolii collected from leaf nests. (a) Adult apterous female with embryons collected in Kantemirovka (Voronezh Region) and (b) alate female collected in Sychevka (Smolensk Region).
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Figure 3. Localities of detection of Prociphilus fraxinifolii in Europe. Red dots—our findings. Green triangles—localities indicated in published sources [3,4,5,6,7,8,9,10,11,12,13,14,15,18,19,20,21,22]. AM—Armenia, BG—Bulgaria, BY—Belarus, DE—Germany, ES—Spain, GB—Great Britain, HU—Hungary, PL—Poland, RO—Romania, SI—Slovenia, SR—Serbia, UA—Ukraine, RU—Russia: 1—Smolensk Region, 2—Moscow Region, 3—Nizhny Novgorod Region, 4—Tambov Region, 5—Voronezh Region, 6—Saratov Region, 7—Samara Region, 8—Volgograd Region, 9—Astrakhan Region, 10—Republic of Crimea, 11—Rostov Region, 12—Krasnodar Territory, 13—Republic of Kalmykia, 14—Stavropol Territory, 15—Kabardino-Balkar Republic, 16—Republic of North Ossetia. This map was made using DIVA-GIS 7.5 software [23].
Figure 3. Localities of detection of Prociphilus fraxinifolii in Europe. Red dots—our findings. Green triangles—localities indicated in published sources [3,4,5,6,7,8,9,10,11,12,13,14,15,18,19,20,21,22]. AM—Armenia, BG—Bulgaria, BY—Belarus, DE—Germany, ES—Spain, GB—Great Britain, HU—Hungary, PL—Poland, RO—Romania, SI—Slovenia, SR—Serbia, UA—Ukraine, RU—Russia: 1—Smolensk Region, 2—Moscow Region, 3—Nizhny Novgorod Region, 4—Tambov Region, 5—Voronezh Region, 6—Saratov Region, 7—Samara Region, 8—Volgograd Region, 9—Astrakhan Region, 10—Republic of Crimea, 11—Rostov Region, 12—Krasnodar Territory, 13—Republic of Kalmykia, 14—Stavropol Territory, 15—Kabardino-Balkar Republic, 16—Republic of North Ossetia. This map was made using DIVA-GIS 7.5 software [23].
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Table 1. Localities of detection of P. fraxinifolii in 2019–2021.
Table 1. Localities of detection of P. fraxinifolii in 2019–2021.
Country/
Region
LocalityNumber of Examined F. pennsylvanica Trees and Kind of Planting 2Number of Examined F. excelsior Trees and Kind of PlantingNumber of Infested F. pennsylvanica TreesDate of Survey
Belarus
BrestBrest>100 U0319 June 2021
Russia
AstrakhanAstrakhan City>100 U0211 May 2021
AstrakhanNikolskoe>50 R0213 August 2020
AstrakhanAstrakhanskaya Fishka>100 F0115 May 2021
MoscowZelenograd>500 U20 U>20July and August 2020 and July 2021
MoscowAlabushevo> 50 R028 August 2019
MoscowMoscow City>100 U0328 July 2020
Nizhny NovgorodNizhny Novgorod City>100 U>100 F1019 August 2020
SamaraSamara City>100 U0116 August 2020
SaratovSaratov City>100 U0510 August 2020
SaratovUsovka Island>100 F0315 August 2020
SmolenskVyazma107 U67 U33 August 2019
SmolenskSychevka32 U015 August 2019
Tambov 1Tambov City>100 U0117 August 2020
VolgogradVolgograd City>100 U0211 August 2020
VoronezhBorisoglebsk24 U21 U112 August 2019
VoronezhVorona River valley>100 F>500 F212 August 2019
VoronezhPovorino>100 U01213 August 2019
VoronezhRossosh>100 P1P>2013 August 2019
VoronezhKantemirovka>150 U0>5014 August 2019
VoronezhVoronezh City>500 U>500 F, U5July and August 2021
1 The survey of ash trees in Tambov was made by Roman Ishin. The survey in all other regions was made by the authors of the article. 2 Kind of plantings: U—urban, R—roadside, F—forest, P—protective forest belt around the field.
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