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Citation: Orlova-Bienkowskaja,
M.J.; Bie´
nkowski, A.O. Low Heat
Availability Could Limit the Potential
Spread of the Emerald Ash Borer to
Northern Europe (Prognosis Based
on Growing Degree Days per Year).
Insects 2022,13, 52. https://doi.org/
10.3390/insects13010052
Academic Editor: Dimitrios N. Avtzis
Received: 23 October 2021
Accepted: 28 December 2021
Published: 2 January 2022
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Attribution (CC BY) license (https://
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4.0/).
insects
Article
Low Heat Availability Could Limit the Potential Spread of the
Emerald Ash Borer to Northern Europe (Prognosis Based on
Growing Degree Days per Year)
Marina J. Orlova-Bienkowskaja * and Andrzej O. Bie ´nkowski
A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 119071 Moscow, Russia;
bienkowski@yandex.ru
*Correspondence: marinaorlben@yandex.ru
Simple Summary:
Emerald ash borer is a devastating pest of ash trees. This beetle, native to Asia and
established in North America, European Russia and Ukraine is quickly spreading and approaching
the borders of the European Union. We made the first prognosis of the potential range of this pest in
Europe based on heat availability. Our calculations have shown that, in most European countries, the
climate is warm enough for the establishment of the emerald ash borer. However, this pest would
probably not be able to establish itself in some regions of Norway, Sweden, Finland, Ireland and
Great Britain, because there is not enough heat to complete development (the summer is too cold
and too short). Therefore, there is a hope that European ash (Fraxinus excelsior) could escape from the
emerald ash borer in some parts of the British Isles and Scandinavia.
Abstract:
Emerald ash borer Agrilus planipennis (Coleoptera: Buprestidae) is one of 20 priority
quarantine pests of the European Union. It is native to Asia and is established in the USA, Canada,
European Russia, and Ukraine. We made the first prognosis of the potential range of A. planipennis
in Europe based on heat availability. Mean annual growing degree days base 10
◦
C (AGDD
10
) was
calculated for each grid square (0.25
◦×
0.25
◦
latitude x longitude degrees) on the Earth’s surface.
Minimal AGDD
10
recorded in the grid squares currently occupied by A. planipennis was 714
◦
in Asia,
705
◦
in North America, and 711
◦
in European Russia. Agrilus planipennis has never been recorded
in localities with AGDD
10
below 700
◦
. If the phenotypic plasticity would not allow this species to
overcome this threshold, cold regions of Europe would probably not be invaded by A. planipennis.
Thus, Fraxinus excelsior could potentially escape from A. planipennis in some regions of Norway,
Sweden, Finland, Ireland, and Great Britain.
Keywords: emerald ash borer; EAB; Buprestidae; jewel beetles; Coleoptera; Fraxinus; forest pest
1. Introduction
Emerald ash borer Agrilus planipennis (Fairmaire, 1888) (Coleoptera: Buprestidae)
is an alien pest of ash trees (Fraxinus spp.) in the USA, Canada, European Russia and
Ukraine [
1
,
2
]. This beetle, native to East Asia [
3
], was first recorded in North America in
2002, in Michigan [
4
] and in Europe in 2003, in Moscow [
5
]. Since that time, the pest has
been spreading over both continents and killing millions of ash trees. Agrilus planipennis
is a major threat to ash trees in Europe; it is included in the list of 20 priority quarantine
pests of the European Union (EU) [
6
,
7
]. Now, the border of the A. planipennis range is just
120 km from the border of the EU; A. planipennis will inevitably appear in the EU soon [
8
,
9
].
The most commonly infested ash trees in European Russia and Ukraine are the green ash,
Fraxinus pennsylvanica Marsh. This ash species was introduced for landscape plantings
from North America in the 20th century and is known to be highly susceptible to emerald
ash borer [
10
]. All ash species native to Europe (Fraxinus excelsior L., F. ornus L. and F.
angustifolia Vahl.) are susceptible to A. planipennis [
11
]. It is very important to assess the
Insects 2022,13, 52. https://doi.org/10.3390/insects13010052 https://www.mdpi.com/journal/insects
Insects 2022,13, 52 2 of 11
potential range of the species in Europe, since it is an essential part in planning measures to
mitigate economic and ecological losses from the future outbreak.
Climate and distribution of susceptible host plants are critical factors considered in
predicting the potential distributions of alien species including A. planipennis [
12
]. Several
prognoses of the potential range in Europe based on different approaches have been
made [
13
–
15
]. Since the main factor limiting A. planipennis distribution is host availability,
a high-resolution map of A. planipennis invasion risk for southern central Europe (Austria,
Switzerland, Liechtenstein, southern Germany) was based on the distribution of ash trees
F. excelsior [
13
]. Another model based on the maximum entropy modelling (MaxEnt) used
the combination of 19 climatic parameters has shown that the regions of Europe adjacent
to the known range of A. planipennis are suitable for this species; therefore, the climatic
factors would not prevent the spread to adjacent regions [
14
]. The prognosis based on
the minimum winter temperature as a possible limiting factor has shown that low winter
temperatures would not prevent the spread of A. planipennis in all regions of Europe, except
some eastern districts of European Russia [15].
Heat availability is one of the main factors determining the distribution of insect
species [
16
]. The distribution of insects to the cold regions is often limited by the amount
of heat (degree days) necessary to complete the life cycle. For example, the distribution
of the two spotted oak buprestid, Agrilus biguttatus Fabricus, in Europe is limited by
this factor [
17
]. It was hypothesized that low heat availability could limit the spread of
A. planipennis to the north [
18
]. The only prognosis of A. planipennis potential range taking
into account heat availability was recently made for Great Britain [19].
Here, we present the first prognosis of A. planipennis potential spread in the whole of
Europe based on heat availability. Our calculations indicate that this climatic parameter
could limit the potential spread of A. planipennis to Northern Europe.
2. Materials and Methods
2.1. Occurrences of Agrilus planipennis
We compiled a table of occurrences of A. planipennis in Asia, North America and
Europe (Table S1) using the information from current databases and articles [
1
–
3
,
20
,
21
].
The new occurrence in the city of Azov was added to the table (Table S1). We detected
characteristic exit holes and larval galleries and collected one dead adult A. planipennis
from under the bark of Fraxinus pennsylvanica in the city of Azov on 8 September 2021. It is
the first record of A. planipennis in the Rostov Region and the most south-western locality
of the current range.
2.2. Calculation of Annual Growing Degree Days
The data on air temperature for each day from the beginning of 2003 through the end
of 2020 were obtained from the ERA5-Land Global Atmospheric Reanalysis dataset for
each grid square (0.25
◦×
0.25
◦
latitude
×
longitude degrees) on the Earth’s surface [
22
].
We have chosen these last 18 years because A. planipennis was first recorded in Europe in
2003 [
5
]. The year of the first record always differs from the year of the establishment of
the population. We can never know exactly when A. planipennis was established in the
particular locality. Mean AGDD of an 18 year is an integrated parameter which gives us
the general information about average heat availability in the particular locality.
The life cycle of A. planipennis in the colder regions (in particular, in Moscow) is
2 years, i.e., the larvae develop under the bark all year-round [
23
]. Therefore, the annual
growing degree days (AGDD) were chosen as a parameter for the prognosis of the potential
range. The base temperature of 10
◦
C was chosen because it is a standard base temperature
previously used in the studies on A. planipennis phenology [24].
The mean AGDD10 were calculated in each grid square as follows:
1.
The daily mean temperature was calculated for each day as a mean of the temperatures
at 00:00, 02:00, 04:00, 06:00, 08:00, 10:00, 12:00, 14:00, 16:00, 18:00, 20:00 and 22:00 UTC.
Insects 2022,13, 52 3 of 11
2.
Then the growing degree days base 10
◦
C from 1 January to 31 December were
calculated for each year since 2003 to 2020 (AGDD10 in each particular year).
3. Then the mean AGDD10 per year in 2003–2020 was calculated.
A detailed description of the calculation method and the computer code used is
provided in the Supplementary Material (File S1). The results of the calculations are
provided in the Excel table (Table S2).
2.3. Analysis and Visualisation of Results
The analysis of AGDD
10
in each grid square occupied by A. planipennis in Asia, North
America, European Russia and Ukraine allowed us to determine the minimum AGDD
10
recorded in the occupied grid squares. Then we made a map of AGDD
10
distribution
in Europe and revealed the regions of Europe where AGDD
10
is less than this threshold.
The visualization was created using DIVA-GIS 7.5 [
25
]. The source of information for the
F. excelsior range was the chorological maps for the main European woody species [26].
Shape files of countries and administrative units were obtained from DIVA GIS Free
Spatial Data [
27
]. Shape files of the F. excelsior range, countries and administrative units
were published in open-access sources published under a creative commons license [
26
,
27
].
3. Results
3.1. Heat Availability in the Regions Currently Occupied by A. planipennis
AGDD
10
in the grid squares currently occupied by A. planipennis varies from 705 to
3676 (Table 1).
Table 1.
Minimum and maximum mean AGDD
10
in 2003–2020 (
◦
C) in the grid squares currently
occupied by A. planipennis in different continents.
Continent Minimum Maximum
Asia 714 2778
North America 705 3676
Europe (Russia and Ukraine) 711 2046
The distribution of AGDD
10
in the current range of A. planipennis is shown in Figures 1–3.
The minimum values of AGDD
10
recorded in Asia, North America and European Russia
are very close to each other: slightly more than 700
◦
.Agrilus planipennis has never been
recorded in the grid squares with AGDD10 less than 700◦.
The distribution of A. planipennis in its native range is not only limited by distri-
bution of its host plants [
12
]. The host plant of A. planipennis in Asia, Fraxinus mand-
shurica Rupr., [
28
] occurs on the Sakhalin Island, some districts of Primorye Territory and
Khabarovsk Territory, although A. planipennis is absent there [
29
] (Figure 4). The mini-
mum heat availability (AGDD
10
) in grid squares occupied by F. mandshurica is 574
◦
, while
A. planipennis has been never recorded in the grid squares with AGDD
10
below 700
◦
. It
indicates that heat availability could be one of the factors limiting the distribution of
A. planipennis in the north of its range.
3.2. Heat Availability in Europe
3.2.1. General Distribution of Heat Availability
The map of the heat availability over the whole Europe is shown in Figure 5. In the
majority of Europe, AGDD
10
is above 700
◦
. However, in the North (Norway, Sweden,
Finland, Great Britain, Ireland, north of European Russia) and some mountain territories
(the Carpathians, Pyrenees, Alps, Caucasus) there are regions where AGDD
10
is below
this threshold.
Ash trees of different species are often planted outside their native ranges in Europe.
Survival of these artificial plantings is important, but more important is the survival of ash
trees in their native ranges, since ash trees play an important role in the communities of
Insects 2022,13, 52 4 of 11
broad-leaved forests; hundreds of species of animals, plants and fungi ecologically depend
on Fraxinus spp. [
7
]. The native range of F. excelsior occupies almost the whole of Europe,
except the very south and very north (Figure 6). The heat availability is higher than 700
◦
in
the most part of the range, except some northern and mountain regions.
Insects 2022, 13, x FOR PEER REVIEW 4 of 14
Figure 1. Heat availability in the native range of Agrilus. planipennis in Asia. Mean AGDD
10
per year
in 2003–2020 is indicated with colours (see the legend). CN—China, JP—Japan, KP—Democratic
People’s Republic of Korea, KR—Republic of Korea, RU—Russia. The information about occur-
rences of A. planipennis was obtained from the review of its native range [3].
Figure 2. Heat availability in the current invasive range of Agrilus. planipennis in North America.
Mean AGDD
10
per year in 2003–2020 is indicated with colours (see the legend). CA—Canada, US—
Figure 1.
Heat availability in the native range of Agrilus. planipennis in Asia. Mean AGDD
10
per year
in 2003–2020 is indicated with colours (see the legend). CN—China, JP—Japan, KP—Democratic
People’s Republic of Korea, KR—Republic of Korea, RU—Russia. The information about occurrences
of A. planipennis was obtained from the review of its native range [3].
Insects 2022, 13, x FOR PEER REVIEW 4 of 14
Figure 1. Heat availability in the native range of Agrilus. planipennis in Asia. Mean AGDD
10
per year
in 2003–2020 is indicated with colours (see the legend). CN—China, JP—Japan, KP—Democratic
People’s Republic of Korea, KR—Republic of Korea, RU—Russia. The information about occur-
rences of A. planipennis was obtained from the review of its native range [3].
Figure 2. Heat availability in the current invasive range of Agrilus. planipennis in North America.
Mean AGDD
10
per year in 2003–2020 is indicated with colours (see the legend). CA—Canada, US—
Figure 2.
Heat availability in the current invasive range of Agrilus. planipennis in North America.
Mean AGDD10 per year in 2003–2020 is indicated with colours (see the legend). CA—Canada, US—
United States. The information about occurrences of Agrilus planipennis was obtained from Emerald
Ash Borer Info and Global Biodiversity Information Facility [1,21].
Insects 2022,13, 52 5 of 11
Insects 2022, 13, x FOR PEER REVIEW 5 of 14
United States. The information about occurrences of Agrilus planipennis was obtained from Emerald
Ash Borer Info and Global Biodiversity Information Facility [1,21].
Figure 3. Heat availability in the current range of Agrilus planipennis in European Russia and
Ukraine. Mean AGDD
10
per year in 2003–2020 is indicated with colours (see the legend). RU—Rus-
sia, UA—Ukraine. The information about occurrences of A. planipennis was obtained from recent
publications [9,19]. Some occurrences are indicated with letters: A—Azov, M—Moscow, P—Saint
Petersburg, S—Smolensk, Y—Yaroslavl, N—Nikolskoe Village (Astrakhan Region). The new occur-
rence in Azov is published for the first time.
The distribution of A. planipennis in its native range is not only limited by distribution
of its host plants [12]. The host plant of A. planipennis in Asia, Fraxinus mandshurica Rupr.,
[28] occurs on the Sakhalin Island, some districts of Primorye Territory and Khabarovsk
Territory, although A. planipennis is absent there [29] (Figure 4). The minimum heat avail-
ability (AGDD
10
)
in grid squares occupied by F. mandshurica is 574°, while A. planipennis
has been never recorded in the grid squares with AGDD
10
below 700°. It indicates that
heat availability could be one of the factors limiting the distribution of A. planipennis in
the north of its range.
Figure 3.
Heat availability in the current range of Agrilus planipennis in European Russia and
Ukraine. Mean AGDD
10
per year in 2003–2020 is indicated with colours (see the legend). RU—
Russia, UA—Ukraine. The information about occurrences of A. planipennis was obtained from
recent publications [
9
,
19
]. Some occurrences are indicated with letters: A—Azov, M—Moscow,
P—Saint Petersburg, S—Smolensk, Y—Yaroslavl, N—Nikolskoe Village (Astrakhan Region). The
new occurrence in Azov is published for the first time.
Insects 2022, 13, x FOR PEER REVIEW 6 of 14
Figure 4. Distribution of Agrilus planipennis and its host plant Fraxinus mandshurica in the northern
part of A. planipennis native range in Asia. Mean AGDD
10
per year in 2003–2020 is indicated with
colours (see the legend). Sources of the information on occurrences: A. planipennis—recent review
of the native range [3], Fraxinus mandshurica—Global Biodiversity Information Facility [29]. Only
localities of F. mandshurica in the grid squares with AGDD
10
less than 700° are shown.
3.2. Heat Availability in Europe
3.2.1. General Distribution of Heat Availability
The map of the heat availability over the whole Europe is shown in Figure 5. In the
majority of Europe, AGDD
10
is above 700°. However, in the North (Norway, Sweden, Fin-
land, Great Britain, Ireland, north of European Russia) and some mountain territories (the
Carpathians, Pyrenees, Alps, Caucasus) there are regions where AGDD
10
is below this
threshold.
Figure 4.
Distribution of Agrilus planipennis and its host plant Fraxinus mandshurica in the northern
part of A. planipennis native range in Asia. Mean AGDD
10
per year in 2003–2020 is indicated with
colours (see the legend). Sources of the information on occurrences: A. planipennis—recent review
of the native range [
3
], Fraxinus mandshurica—Global Biodiversity Information Facility [
29
]. Only
localities of F. mandshurica in the grid squares with AGDD10 less than 700◦are shown.
Insects 2022,13, 52 6 of 11
Insects 2022, 13, x FOR PEER REVIEW 7 of 14
Figure 5. Heat availability in Europe. Mean AGDD
10
per year in 2003-2020 is indicated with colours
(see the legend). The information about occurrences of Agrilus planipennis was obtained from recent
publications [9,19]. IE—Ireland, GB—Great Britain, NO—Norway, SE—Sweden, FI—Finland, RU—
Russia, A—Alps, C—Carpathians, K—Caucasus, P—Pyrenees.
Ash trees of different species are often planted outside their native ranges in Europe.
Survival of these artificial plantings is important, but more important is the survival of
ash trees in their native ranges, since ash trees play an important role in the communities
of broad-leaved forests; hundreds of species of animals, plants and fungi ecologically de-
pend on Fraxinus spp. [7]. The native range of F. excelsior occupies almost the whole of
Europe, except the very south and very north (Figure 6). The heat availability is higher
than 700° in the most part of the range, except some northern and mountain regions.
Figure 5.
Heat availability in Europe. Mean AGDD
10
per year in 2003-2020 is indicated with colours
(see the legend). The information about occurrences of Agrilus planipennis was obtained from recent
publications [
9
,
19
]. IE—Ireland, GB—Great Britain, NO—Norway, SE—Sweden, FI—Finland, RU—
Russia, A—Alps, C—Carpathians, K—Caucasus, P—Pyrenees.
Insects 2022, 13, x FOR PEER REVIEW 8 of 14
Figure 6. Heat availability in the native range of Fraxinus excelsior in Europe. Mean AGDD
10
per year
in 2003–2020 within the native range of F. excelsior is indicated with colours (see the legend). FI—
Finland, GB—Great Britain, IE—Ireland, NO—Norway, RU—Russia, SE—Sweden.
3.2.2. The Distribution of Heat Availability within the Range of Fraxinus Excelsior in
Scandinavia
The only native ash species in the northern part of Europe is European ash (F. excel-
sior) [26]. Heat availability is below 700° AGDD
10
in the most part of Norway, Sweden,
and Finland (Figure 7). There is a hope that these regions could potentially become the
refuges for F. excelsior, where ash trees could escape from A. planipennis. In Denmark, Es-
tonia, southern regions of Sweden and regions along the southern coasts of Norway and
Finland, AGDD
10
is from 700 to 800 °C, i.e., about the minimum recorded in the territories
occupied by A. planipennis.
Figure 6.
Heat availability in the native range of Fraxinus excelsior in Europe. Mean AGDD
10
per
year in 2003–2020 within the native range of F. excelsior is indicated with colours (see the legend).
FI—Finland, GB—Great Britain, IE—Ireland, NO—Norway, RU—Russia, SE—Sweden.
3.2.2. The Distribution of Heat Availability within the Range of Fraxinus Excelsior
in Scandinavia
The only native ash species in the northern part of Europe is European ash (F. excel-
sior) [
26
]. Heat availability is below 700
◦
AGDD
10
in the most part of Norway, Sweden, and
Finland (Figure 7). There is a hope that these regions could potentially become the refuges
for F. excelsior, where ash trees could escape from A. planipennis. In Denmark, Estonia,
southern regions of Sweden and regions along the southern coasts of Norway and Finland,
AGDD
10
is from 700 to 800
◦
C, i.e., about the minimum recorded in the territories occupied
by A. planipennis.
Insects 2022,13, 52 7 of 11
3.2.3. The Distribution of Heat Availability within the Range of Fraxinus Excelsior in
British Isles
Fraxinus excelsior is common over the whole British Isles [
26
]. Our calculations have
shown that AGDD
10
in Ireland, Scotland, Northern Ireland, the most part of Wales and the
northern half of England is less than 700◦(Figure 8).
Figure 7.
Occurrences of Fraxinus excelsior in the territories with AGDD
10
below 700
◦
in Northern
Europe. Mean AGDD
10
per year in 2003–2020 is indicated with colours (see the legend). DK—
Denmark, EE—Estonia, FI—Finland, LT—Lithuania, LV—Latvia, NO—Norway, RU—Russia, SE—
Sweden. 1—occurrences of Agrilus planipennis in Saint Petersburg. The information about the
occurrences of F. excelsior was obtained from Global Biodiversity Information Facility [30–32].
Insects 2022, 13, x FOR PEER REVIEW 10 of 14
Figure 8. Occurrences of Fraxinus excelsior in the territories with AGDD
10
below 700° in British Isles.
GB—Great Britain, IE—Ireland. 1—Scotland, 2—Northern Ireland, 3—England, 4—Wales. Mean
AGDD
10
per year in 2003–2020 is indicated with colours (see the legend). The information about the
occurrences of F. excelsior was obtained from Global Biodiversity Information Facility [33–36].
4. Discussion
4.1. Heat Availability as a Limiting Factor of A. planipennis Range
Our data indicate that low heat availability could potentially limit the future spread
of A. planipennis in Northern Europe. This conclusion is in accordance the conclusion by
Webb et al. for the British Isles [19]. These authors calculated that northern half of the
British Isles is unlikely to provide a suitable environment for A. planipennis to establish,
because the GDD
10
threshold of the start of the emergence of adults
(230° GDD
10
accumu-
lated from
1 January) and the threshold of the peak of adult emergence (500° GDD
10
) are
not
met within a calendar year or are met in autumn [19].
It seems that the potential distribution of A. planipennis in Europe is similar to the
current distribution of the two-spotted oak buprestid Agrilus biguttatus Fabricus. Agrilus
biguttatus is widespread throughout Europe but reaches its northern-most limit in south-
ern Sweden and in the northern half of the UK [16]. The host plants of A. biguttatus (Quer-
cus spp.) are usual over the whole British Isles and in Scandinavia. However, the distribu-
tion of A. biguttatus is thermally limited with heat availability likely to be restrictive, rather
than lethal summer or winter temperatures [16].
Prognoses that predict environmental suitability based on current location of cases
for a pest that is still expanding into new regions may underestimate the area over which
successful establishment is possible. However, our prognosis is based not only on the oc-
currences in invasive ranges in America and Europe, which are still expanding, but also
Figure 8.
Occurrences of Fraxinus excelsior in the territories with AGDD
10
below 700
◦
in British Isles.
GB—Great Britain, IE—Ireland. 1—Scotland, 2—Northern Ireland, 3—England, 4—Wales. Mean
AGDD
10
per year in 2003–2020 is indicated with colours (see the legend). The information about the
occurrences of F. excelsior was obtained from Global Biodiversity Information Facility [33–36].
Insects 2022,13, 52 8 of 11
4. Discussion
4.1. Heat Availability as a Limiting Factor of A. planipennis Range
Our data indicate that low heat availability could potentially limit the future spread of
A. planipennis in Northern Europe. This conclusion is in accordance the conclusion by Webb
et al. for the British Isles [
19
]. These authors calculated that northern half of the British Isles
is unlikely to provide a suitable environment for A. planipennis to establish, because the
GDD
10
threshold of the start of the emergence of adults (230
◦
GDD
10
accumulated from
1 January) and the threshold of the peak of adult emergence (500
◦
GDD
10
) are not met
within a calendar year or are met in autumn [19].
It seems that the potential distribution of A. planipennis in Europe is similar to the
current distribution of the two-spotted oak buprestid Agrilus biguttatus Fabricus. Agrilus
biguttatus is widespread throughout Europe but reaches its northern-most limit in southern
Sweden and in the northern half of the UK [
16
]. The host plants of A. biguttatus (Quercus
spp.) are usual over the whole British Isles and in Scandinavia. However, the distribution
of A. biguttatus is thermally limited with heat availability likely to be restrictive, rather than
lethal summer or winter temperatures [16].
Prognoses that predict environmental suitability based on current location of cases
for a pest that is still expanding into new regions may underestimate the area over which
successful establishment is possible. However, our prognosis is based not only on the
occurrences in invasive ranges in America and Europe, which are still expanding, but also
on the occurrences in the native range in Asia, which is not expanding. The minimum
AGDD
10
in all three continents is almost the same (about 700
◦
). Therefore, it seems that
this figure is close to the minimum heat availability necessary for A. planipennis establish-
ment. It is known that adult female A. planipennis body size (length and mass) depends
on heat availability. The colder is the region, the smaller are adult females [
37
]. This phe-
notypic plasticity allows A. planipennis to survive in the colder regions. However, smaller
A. planipennis females produce fewer eggs [
37
]. Obviously, the limit of this phenotypic
plasticity exists: if the heat availability is too low, females are not able to survive or produce
enough eggs for the establishment of the population
4.2. Comparison of Low Heat Availability and Minimum Winter Temperature as Limiting Factors
of A. planipennis Potential Distribution
It is interesting that low winter temperature and low heat availability pose different
limitations to the potential range of A. planipennis in Europe (Figure 9).
Insects 2022, 13, x FOR PEER REVIEW 11 of 14
on the occurrences in the native range in Asia, which is not expanding. The minimum
AGDD
10
in all three continents is almost the same (about 700°). Therefore, it seems that
this figure is close to the minimum heat availability necessary for A. planipennis establish-
ment. It is known that adult female A. planipennis body size (length and mass) depends on
heat availability. The colder is the region, the smaller are adult females [37]. This pheno-
typic plasticity allows A. planipennis to survive in the colder regions. However, smaller A.
planipennis females produce fewer eggs [37]. Obviously, the limit of this phenotypic plas-
ticity exists: if the heat availability is too low, females are not able to survive or produce
enough eggs for the establishment of the population
4.2. Comparison of Low Heat Availability and Minimum Winter Temperature as Limiting
Factors of A. planipennis Potential Distribution
It is interesting that low winter temperature and low heat availability pose different
limitations to the potential range of A. planipennis in Europe (Figure 9).
Figure 9. Distribution minimum winter temperature and heat availability in Europe. Mean AGDD
10
per year in 2003–2020 is indicated with colours (see the legend). 1—territories, which are not suitable
for Agrilus planipennis establishment because of the extreme winter cold [15], 2—localities of A.
planipennis. FI—Finland, GB—Great Britain, IE—Ireland, NO—Norway, RU—Russia, SE—Sweden.
Our previous calculations have shown A. planipennis populations survive in the ter-
ritories where the minimum daily temperature is above 34° C, but do not survive in the
territories where the daily temperature is below 34° C [15]. Temperature below 34° C is
not rare in the east of European Russia but is extremely rare in Western Europe. Therefore,
winter cold could limit of A. planipennis spread in the east of European Russia but could
probably not limit its spread in Western Europe. Our current calculations have shown that
fortunately the spread of the pest in the north of Europe could be potentially limited by
low heat availability.
4.3. Perspectives for Future Researches
Variation in frequency and intensity of surveillance for A. planipennis between re-
gions means that, for some areas, we can be less confident that a lack of report means that
the pest is absent. The surveys of ash trees in the northern regions of European Russia and
in the Far East are necessary for obtaining more detailed information about distribution
of A. planipennis in the North.
AGDD
10
in the high-altitude regions of the Alps, Pyrenees, Carpathians and Cauca-
sus is less than 700°. The more detailed calculations of heat availability with higher reso-
lution and the comparison with the high-resolution map of the distribution of ash trees
Figure 9.
Distribution minimum winter temperature and heat availability in Europe. Mean AGDD
10
per year in 2003–2020 is indicated with colours (see the legend). 1—territories, which are not
suitable for Agrilus planipennis establishment because of the extreme winter cold [
15
], 2—localities of
A. planipennis. FI—Finland, GB—Great Britain, IE—Ireland, NO—Norway, RU—Russia, SE—Sweden.
Our previous calculations have shown A. planipennis populations survive in the ter-
ritories where the minimum daily temperature is above 34
◦
C, but do not survive in the
Insects 2022,13, 52 9 of 11
territories where the daily temperature is below 34
◦
C [
15
]. Temperature below 34
◦
C is
not rare in the east of European Russia but is extremely rare in Western Europe. Therefore,
winter cold could limit of A. planipennis spread in the east of European Russia but could
probably not limit its spread in Western Europe. Our current calculations have shown that
fortunately the spread of the pest in the north of Europe could be potentially limited by
low heat availability.
4.3. Perspectives for Future Researches
Variation in frequency and intensity of surveillance for A. planipennis between regions
means that, for some areas, we can be less confident that a lack of report means that the
pest is absent. The surveys of ash trees in the northern regions of European Russia and in
the Far East are necessary for obtaining more detailed information about distribution of
A. planipennis in the North.
AGDD
10
in the high-altitude regions of the Alps, Pyrenees, Carpathians and Cau-
casus is less than 700
◦
. The more detailed calculations of heat availability with higher
resolution and the comparison with the high-resolution map of the distribution of ash trees
(Fraxinus excelsior,F. ornus and F. angustifolia) are necessary to assess whether some high-
altitude regions could become potential refuges of ash trees from A. planipennis.
Warmer temperatures appear to have contributed to recent northward range shifts
of some native wood-boring forest pests in Europe, including jewel beetles (Coleoptera:
Buprestidae): Coraebus florentinus Herbst and Agrilus sulcicollis Lacordaire [
16
]. Therefore,
the future warming could potentially affect the spread of A. planipennis to the North. The
analysis of the possible impact of the future climate change on the potential spread of
A. planipennis is a perspective for future research.
It is known that the duration of the life cycle of A. planipennis depends on the tempera-
ture: in the warmer regions, the life cycle is usually 1 year, while in the colder regions it is
2 years [
23
]. It is important to reveal in what regions of Europe the potential development
could be 1 year, because in such regions the spread of A. planipennis could be faster than in
others. The estimation of the potential duration of the life cycle in different parts of Europe
is also a perspective for future research.
5. Conclusions
1. Minimum AGDD10 recorded in the localities of A. planipennis in the three continents
are almost the same: 714
◦
in Asia, 705
◦
in North America, and in 711
◦
Europe. Agrilus
plenipennis has been never recorded in the regions with AGDD10 below 700◦.
2.
In the majority of Europe, AGDD
10
is more than 700
◦
. Therefore, low heat availability
would probably not limit the spread of A. planipennis in most of European countries.
3.
Heat availability in most regions of Norway, Sweden, Finland, and Ireland and in
the northern half of Great Britain is less than 700
◦
. If the phenotypic plasticity would
not allow the pest to overcome this threshold, A. planipennis would potentially not
establish in these regions. Therefore, Fraxinus excelsior could potentially escape from
A. planipennis in these regions.
Supplementary Materials:
The following are available online at https://www.mdpi.com/article/10
.3390/insects13010052/s1, Table S1: Localities, where A. planipennis has been recorded in Asia, North
America and Europe; File S1: Detailed description of the calculations of the mean AGDD
10
. Table S2:
Results of calculations: the mean AGDD10 per year in 2003–2020 in each grid square.
Author Contributions:
Conceptualization, M.J.O.-B.; validation, A.O.B.; investigation, M.J.O.-B.;
resources, A.O.B.; writing—Original draft preparation, M.J.O.-B.; writing—Review and editing,
A.O.B.; visualization, M.J.O.-B.; funding acquisition, A.O.B. All authors have read and agreed to the
published version of the manuscript.
Funding:
This research was funded by RUSSIAN SCIENCE FOUNDATION, grant number 22-24-00166.
Institutional Review Board Statement: Not applicable.
Insects 2022,13, 52 10 of 11
Data Availability Statement:
All data generated during this study are in the electronic supplements
(Supplementary Materials).
Acknowledgments:
We are grateful to our son A.A. Bie
´
nkowski (The faculty of Computational
Mathematics and Cybernetics of Lomonosov Moscow State University, Russia) for help with the
mathematical treatment.
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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