pa hogens
A icle
Towa ds New Ho izons: Clima e T ends in Eu ope Inc ease he
En i onmen al Sui abili y o Pe manen Popula ions o
Hyalomma ma gina um (Ixodidae)
Na alia Fe nández-Ruiz 1,2,*,† and Agus ín Es ada-Peña 1,2,†


Ci a ion: Fe nández-Ruiz, N.;
Es ada-Peña, A. Towa ds New
Ho izons: Clima e T ends in Eu ope
Inc ease he En i onmen al
Sui abili y o Pe manen Popula ions
o Hyalomma ma gina um (Ixodidae).
Pa hogens 2021,10, 95.
h ps://doi.o g/10.3390/pa hogens
10020095
Recei ed: 21 Decembe 2020
Accep ed: 16 Janua y 2021
Published: 21 Janua y 2021
Publishe ’s No e: MDPI s ays neu al
wi h ega d o ju isdic ional claims in
published maps and ins i u ional a il-
ia ions.
Copy igh : © 2021 by he au ho s.
Licensee MDPI, Basel, Swi ze land.
This a icle is an open access a icle
dis ibu ed unde he e ms and
condi ions o he C ea i e Commons
A ibu ion (CC BY) license (h ps://
c ea i ecommons.o g/licenses/by/
4.0/).
1Facul y o Ve e ina y Medicine, Uni e si y o Za agoza, 50013 Za agoza, Spain; [email p o ec ed]
2
G oup o Resea ch on Eme ging Zoonoses, Ins i u o Ag oalimen a io de A agón (IA2), 50013 Za agoza, Spain
*Co espondence: na alia. e [email p o ec ed]
† All au ho s con ibu ed equally.
Abs ac :
Ticks and ick-bo ne pa hogens a e changing hei cu en dis ibu ion, p esumably due
o he impac o he clima e ends. On a la ge scale, hese ends a e changing he en i onmen al
sui abili y o Hyalomma ma gina um, he main ec o o se e al pa hogens a ec ing human heal h.
We gene a ed annual models o en i onmen al sui abili y o he ick in he pe iod 1970–2018, using
ha monic eg ession-de i ed da a o he daily maximum and minimum empe a u e, soil mois u e
and wa e apo de ici . The esul s demons a e an expansion o he sui able a ea in Medi e anean
coun ies, sou heas cen al Eu ope and sou h o he Balkans. Also, he models allowed us o in e p e
he impac o he ecological a iables on hese changes. We deduced ha (i) maximum empe a u e
was signi ican o all o he biogeog aphical ca ego ies, (ii) soil humidi y has an in luence in he
Medi e anean clima e a eas, and (iii) he minimum empe a u e and de ici wa e apo did no
in luence he en i onmen al sui abili y o he species. The conclusions clea ly show ha clima e
change could c ea e new a eas in Eu ope wi h sui able clima es o H. ma gina um, while keeping i s
“his o ical” dis ibu ion in he Medi e anean. The e o e, i is necessa y o u he explo e possible
isk a eas o H. ma gina um and i s associa ed pa hogens.
Keywo ds: Hyalomma ma gina um; Eu ope; clima e ends; en i onmen al sui abili y
1. In oduc ion
Majo changes in ecosys ems a e being d i en by he as an h opogenic clima e
change obse ed in he ea ly 21s Cen u y [
1
]. Clima e change is de ined as “a s a is ical
phenomenon ha desc ibes he a e age clima ic condi ions o a egion, e e ed o sys-
ema ic and gene ally g adual changes in he end, which is in eg a ed in o he andom
luc ua ions o he clima e” [
2
]. Since empi ical obse a ions o wea he a e sca e ed
o e ime, and memo y o pas e en s may be incomple e, clima e change is no cap u ed
h ough pe sonal expe ience. Clima e change a ec s he dynamics o many ec o -bo ne
pa hogens [
3
], hei ese oi s and human habi s, o a ye unknown scale. This may esul
in he ( e)eme gence o ec o -bo ne diseases. While s udies a e di e se, p obably he
mos easily cap u ed e ec is he al e a ion o he known dis ibu ion o heal h h ea ening
pa hogens ansmi ed by a h opods [4].
Ticks ansmi he la ges numbe o zoono ic agen s in he No he n Hemisphe e [
5
],
and as such, a e o en he ocus o esea ch ega ding he impac o clima e change on
human heal h. Ticks a e hema ophagous pa asi es ha depend on an en i onmen al niche
o empe a u e and humidi y anges o hei popula ion o pe pe ua e; he o e lap o
his niche wi h he one p e e ed by many e eb a e ese oi s esul s in a eas in which
pa hogens can ci cula e. Changes o he geog aphical dis ibu ion o icks ha e been well
documen ed o se e al species in he Nea c ic [
6
–
8
] and Palea c ic egions [
9
,
10
]. In sho ,
Pa hogens 2021,10, 95. h ps://doi.o g/10.3390/pa hogens10020095 h ps://www.mdpi.com/jou nal/pa hogens
Pa hogens 2021,10, 95 2 o 13
mos s udies ha e connec ed he sp ead o icks wi h wa me empe a u es [
11
]. In e -
es ingly, no epo s seem o exis abou he “decoloniza ion” o icks om hei sou he n
habi a as a po en ial consequence o en i onmen al condi ions becoming oo wa m o d y.
O he han con inuous sp ead by adjacency o popula ions a he inge o hei
en i onmen al niches, icks can also be in oduced in o a e i o y by he uncon olled
mo emen s o li es ock o he seasonal beha io o mig a o y bi ds. Since he pionee ing
wo k by Hoogs aal and his eam [
12
], i has been known ha he mig a o y ou es be-
ween A ica and Eu ope se e as ou es o dissemina ion o icks belonging o he genus
Hyalomma. Bi ds ca y imma u es o a leas wo species o he genus (Hyalomma ma gina um
and Hyalomma u ipes) ha eed o se e al days on hos s, hus allowing anspo a ion and
u he sp ead in o no he n e i o ies. Fo pe manen popula ions o Hyalomma o es ab-
lish, i is belie ed ha a c i ical h eshold o empe a u e is necessa y o ick de elopmen ;
his empe a u e p o ides an index o he chance o es ablishmen . In he second decade o
he 20 h cen u y, i was belie ed ha his was a a e e en , because he c i ical empe a u e
h eshold o mol was no eached ou o he Medi e anean ange o he species [
13
].
Howe e , epo s o adul Hyalomma icks in Eu ope [
14
–
18
] a e becoming inc easingly
common, sugges ing ha he accele a ed wa ming a ec ing cen al Eu ope could impac
he de elopmen o mol ing imma u e icks, allowing adul s o su i e in si es whe e
hey we e his o ically absen . A p e ious s udy based on a model o he physiological
p ocesses o he ick [
19
] demons a ed ha he clima e changes which occu ed du ing
20 h cen u y p omo ed changes in he de elopmen al a es o H. ma gina um. This ick
is conside ed a conce n o human heal h, because Hyalomma icks a e known ec o s o
he C imean–Congo hemo hagic e e i us and Ricke sia aeschlimannii. The o me is
an a bo i us belonging o he genus O honai o i us ( amily Bunya i idae) [
20
]. In ec ed
pa ien s de elop a hemo hagic e e ha has a le hali y anging be ween 3%–50%, de-
pending on he s ain [
21
]. The i al agen can p oduce spo adic cases [
22
] o se e e
ou b eaks in a la ge geog aphic a ea, om wes e n China o he Middle Eas and in he
mos sou heas e n egion o Eu ope [
23
] and mos o A ica [
24
]. Addi ionally, Ricke sia
aeschlimannii is an in acellula bac e ium included in he spo ed e e g oup [
25
] ha is o
eme ging impo ance in egions o Eu ope [26]).
This s udy ocuses on changes induced by he clima e since 1970, on he expec ed
en i onmen al sui abili y (ES) o H. ma gina um in Eu ope. The aim is o add ess he join
changes o se e al wea he a iables a ec ing he li e cycle o he ick, hei ends and
hei e ec s on he expec ed ange o i s adequa e en i onmen . We ex ac ed he daily
maximum and minimum empe a u e, soil su ace and ai wa e apo de ici o each
yea in he a ge pe iod using ha monic eg essions o a new gene a ion o e-assessed
clima e da a. We used he la ges exis ing da ase o eco ds o H. ma gina um o de elop
models add essing he end o ES o he ick, and p oduced mul iple eg essions agains
en i onmen al s esso s o de e mine he a iables d i ing he sui abili y o he ick
acco ding o s anda d bio-geog aphical egions o Eu ope.
2. Resul s
Figu e 1shows he calcula ed changes o ES o H. ma gina um in i e ime slices o
10 yea s o he pe iod 1970–2018. These p edic i e maps a e buil wi h a combina ion o
clima e a iables and he ac ual eco ds o he ick in he pe iod 1990–2006 (see Me hods
o a comple e desc ip ion o he modeling p ocess). The igu e illus a es he changes
o ES in ime chunks ha a e adequa e o illus a ing he spa ial pa e ns o a ia ion.
No able changes occu ed in sou h coas al and nea inne pa s o F ance, wi h an inc ease
o sui able a ea in I aly, sou heas e n cen al Eu ope and sou he n Balkans. A de ailed
analysis o hese da a showed he unexpec ed esul ha changes had occu ed no only in
he inge o he dis ibu ion o H. ma gina um, bu also in zones in he cu en ly known
dis ibu ion o he ick. The inc ease o ES was con inuous h oughou he ime pe iod o
la ge egions in Spain, F ance, I aly and he Aegean coas s. The ob ious inc ease o sui able
condi ions in he sou h-wes e n Ibe ian Peninsula obse ed be ween 1970–1979 (Figu e 1a)
Pa hogens 2021,10, 95 3 o 13
and 1980–1989 (Figu e 1b) is pa icula ly s iking. The pe iod 1990–1999 (Figu e 1c) shows
he inc ease o ES in pa s o cen al Eu ope, C imean Peninsula and no heas Tu key.
The comple e pic u e indica es ha , o he pe iod 2010–2018, he mos d as ic changes
occu ed in po ions o he Medi e anean coas , some la ge a eas a ound sou heas e n
cen al Eu ope and he sou h Balkans. Resul s ega ding cen al Eu ope and Balkans
coun ies a e o special in e es in he con ex o he sp ead o H. ma gina um.
Figu e 2displays he changes in he end o ES obse ed in selec ed LANMAP2 bio-
geog aphic egions o Eu ope, co e ing app oxima ely he 80% o he e i o y (a selec ion
o egions was made o imp o e he cla i y o he p esen a ion o his da a). LANMAP2 is
a gene al desc ip ion o he biogeog aphic egions o Eu ope, and he e o e, he epo ing
o he calcula ed changes acco ding o landscape desc ip ions is o in e es . The end o ES
was calcula ed by a lineal eg ession o i s annual alues in he pe iod 1970–2018. The slope
o he ES h oughou his pe iod was posi i e o e e y e i o y. I is no ewo hy ha he
a eas wi h he highes end o ES we e no hose whe e H. ma gina um was al eady es ab-
lished, bu a he , hose ha a e mos likely o see u u e sp ead, because he en i onmen al
niche is quickly becoming sui able. Figu e 2displays he spa ial end o ha slope. Majo
inc eases o ES o he ick esul ed in a eas o Lusi anian ype clima e, associa ed wi h
landscape ca ego ies o pas u es and pe manen c ops. Pannonian-, A lan ic cen al- and
Con inen al- ype clima es expe ienced d as ic inc eases in ES. A la ge inc ease in ES was
p edic ed o Medi e anean moun ains, sugges ing a sp ead o he sui able en i onmen
o he ick in o highe al i udes. Changes in clima e a iables a e pushing H. ma gina um o
ind adequa e habi a s u he no h and a highe al i udes. In e es ingly, hese changes
a e obse ed in di e en egions o Eu ope, meaning ei he an inc ease o ES in a eas whe e
he ick is al eady p esen o a end owa d sui abili y in si es whe e he icks does no ye
p esen pe manen popula ions. I should be s essed ha he p esen ed ES end is no an
e alua ion o he places ha could be colonized by H. ma gina um, bu only a ep esen a ion
o he speed o change o clima e ai s ela i e o i s en i onmen al sui abili y.
Figu e 1. Con .
Pa hogens 2021,10, 95 4 o 13
Figu e 1.
Spa ial changes o en i onmen al sui abili y o Hyalomma ma gina um in i e ime slices
co e ing pe iods o 10 consecu i e yea s. (
a
) 1970–1979, (
b
) 1980–1989, (
c
) 1990–1999, (
d
) 2000–2009,
(e) 2010–2018.
I is impo an o de i e ecological meaning o he a iables d i ing he changes o
ES o H. ma gina um in Eu ope. We ob ained daily alues o se e al explana o y a iables
using he comple e da ase ans o med ia ha monic eg ession (see de ails in he Me hods
sec ion) including a iables ela ed o maximum and minimum empe a u e, soil humidi y
and wa e apo de ici . We calcula ed mul iple eg essions, e.g., he slopes o ES changes
and o he explana o y a iables, aiming o de e mine how bo h g oups o slopes we e
co ela ed in he pe iod 1970–2018. The esul s a e displayed in Figu e 3, sepa a ely o
a iables ela ed o “wa e ” and hose ela ed o “ empe a u e”. Al hough beyond he
scope o he p esen discussion, i may be no ed ha qua ile 90 empe a u e and he
numbe o days abo e a h eshold empe a u e o 10
◦
C a e good indica o s o he inc ease
o ES and a e he main d i ing a iables in he no he n e i o ies o he a ge egion.
Howe e , his is no he ule o e e y e i o y. Minimum empe a u e and soil humidi y
a e highly co ela ed wi h he slope o ES in some Medi e anean habi a s, sugges ing
ha soil humidi y has a ole in he expansion o ES. I should be no ed ha minimum
empe a u es (i.e., qua ile 10) a e no behind majo changes o ES in he no he n e i o ies,
meaning ha wa me minimum empe a u es a e no co ela ed wi h he obse ed changes
Pa hogens 2021,10, 95 5 o 13
in ES o H. ma gina um a he ime scale conside ed. Ins ead, he esul s show ha he daily
accumula ed empe a u e was he a iable which was bes able o explain he calcula ed
esul s. Wa e apo de ici , a a iable measu ed well abo e he g ound su ace, has li le
impo ance in de ining he changes in ES o he a ge species.
Figu e 2.
The slope o he changes o en i onmen al sui abili y o Hyalomma ma gina um in he a ge
e i o y in he pe iod 1970–2018. A posi i e slope is no co ela ed wi h a sui able en i onmen al
o he ick (see Figu e 1 o his da a), bu a he , only he s eng h o changes o he en i onmen al
a iables in he pe iod o e e ence. These changes a e shown in (
b
) wi h explici e e ence o he
biogeog aphic di isions in (a).

Pa hogens 2021,10, 95 6 o 13
Figu e 3.
En i onmen al a iables wi h s a is ical signi icance in he changes o en i onmen al
sui abili y o Hyalomma ma gina um in he pe iod 1970–2018, ob ained om a mul iple eg ession
among he slope o changes o sui abili y (dependen a iable) and se e al en i onmen al a i-
ables (explana o y a iables). The esul s we e calcula ed sepa a ely o each o a ious selec ed
biogeog aphic a eas, which co e mo e han 80% o he e i o y. Two hea maps a e associa ed
wi h he ables in which he “p” alues o each a iable a e included: cells in ed ep esen highly
signi ican a iables. The abb e ia ions o he a iables a e: SoilQ10, SoilQ90, and Soil (pe cen iles
10 and 90 o he soil mois u e and he o al annual soil mois u e, espec i ely); VPDTo al (sum o
he annual alues o daily wa e apo de ici ), VPDQ10 and VPDQ90 (pe cen iles 10 and 90 o he
o he daily wa e apo de ici ) in igu e (
a
); and TMAX_10 (annual sum o he daily maximum
empe a u e alues exceeding o 10
◦
C), TMAX_Q10 and TMAX_Q90 (pe cen iles 10 and 90 o he o
he daily maximum empe a u e alues), TMAX_d10 (numbe o days in a yea in which maximum
empe a u e exceeded 10
◦
C); TMIN_10 (annual sum o he daily minimum empe a u e alues
exceeding o 10
◦
C), TMIN_Q10 and TMIN_Q90 (pe cen iles 10 and 90 o he o he daily minimum
empe a u e alues), TMIN_d10 (numbe o days in a yea in which minimum empe a u e exceeded
10 ◦C) in igu e (b).
Figu e 4displays he changes obse ed be ween he yea s 1970–1979 and 2010–2018,
using only wo a iables, namely, he sum o maximum empe a u es and he sum o
soil wa e humidi y; hese we e shown o be signi ican ly in ol ed in mul iple eg ession
be ween he slope o changes o ES and ha o ends o he en i onmen al a iables. Only
hese wo pe iods we e conside ed in o de o imp o e he isualiza ion o he cha s and
p o ide a summa y o he obse ed changes. The si es included we e he same biogeo-
g aphical ca ego ies displayed in Figu e 3. O he a iables we e no included in he cha s,
and he commen s below should be conside ed a p oo -o -concep o : (a) empe a u e
Pa hogens 2021,10, 95 7 o 13
is no he only a iable ha changes o imp o e he ES o H. ma gina um; and (b) each
biogeog aphical egion expe ienced changes o di e en wea he a iables, con e ging in o
he eme gence o sui able niche o he ick. T ends a e a iable acco ding o he egion, bu
he gene al iew is an inc ease o he empe a u e oge he wi h a dec ease o soil humidi y.
Changes o soil humidi y we e negligible in some egions (i.e., A lan ic cen al egions), in
which he mos p ominen change was he inc ease o empe a u e. Con inen al- ype si es
mos ly obse ed a dec ease o soil humidi y. Changes in Medi e anean- ype habi a s a e
in e media e, and bo h a iables seemed o ac join ly. Pannonian- ype habi a s obse ed a
clea inc ease o empe a u e be ween he wo pe iods o ime.
1
Figu e 4.
Changes in he sum o daily annual maximum empe a u e and o solid mois u e o
selec ed biogeog aphical egions. The X axis ep esen s he sum o maximum empe a u e in deg ees
Celsius; he Y axis indica es he sum o soil ela i e humidi y in kPa.
Pa hogens 2021,10, 95 8 o 13
3. Discussion
We sough o e alua e he en i onmen al sui abili y o H. ma gina um in he pe iod
1970–2018, i s spa ial ends and he a iables ha a ha e a s onge in luence d i ing he
slow bu ob ious changes obse ed in he a ge e i o y. We used se ies o clima e da a
and geo- e e enced ield eco ds o H. ma gina um. Long se ies o wea he da a a e di icul
o ob ain using sa elli e images, wi h he mos ecen beginning only in 2001, i.e., he
MODIS se ies o Ea h-o bi ing sa elli es. Sa elli es ha e di e en calib a ion p o ocols and
a ela i ely sho li e; he e o e, i is p oblema ic o ha monize da a cap u ed by di e en
se ies o sa elli es, as his would no esul in a long se ies o compa able en i onmen al
da a. While we s ongly suppo he use o sa elli e da a o he p edic i e modelling
o spa ial dis ibu ion o o ganisms [
27
], a long se ies o di e en wea he a iables was
necessa y o his s udy. Fo his pu pose, we chose he e-analyzed da a o he Te aClima e
eposi o y, as hey p o ide a long se ies o da a ex ending back o 1950. As is compulso y
o mechanis ic modeling, his s udy is p edica ed on a se o coo dina es eco ding he
known dis ibu ion o he ick, oge he wi h a se o explana o y a iables o gene a e
he models. We p e iously demons a ed [
27
] ha he use o coe icien s esul ing om a
ha monic eg ession o he mon hly a iables p oduced be e p edic ions han he use o
p e- ailo ed wea he a iables. The la e p o ide a good desc ip ion o he clima e ac oss
he plane , bu hey canno cap u e he beha io o e e y o ganism. Thus, hey do no
adequa ely explain he ac o s egula ing he p esence o pe manen popula ions o he
modeled o ganism. Since ou me hods based on ha monic eg essions can p oduce daily
alues o each ai , his esul s in a con enien me hod o de i e he necessa y a iables
desc ibing he spa ial dis ibu ion. In ou s udy, he eco ds o H. ma gina um we e collec ed
app oxima ely in he pe iod 1990–2006; as such, hese da a we e used as he se o aining
a iables a e aged o i he same pe iod.
T ai s egula ing he coloniza ion o H. ma gina um ha e been asc ibed o he e ec
o empe a u e on de elopmen s ages [
12
]. The hypo hesis o a c i ical h eshold o
accumula ed empe a u e necessa y o he sp ead and coloniza ion o H. ma gina um [
12
]
was unequi ocally con i med by ou esul s in mos o Eu ope. While he TMax qua ile 90
and he numbe o days wi h Tmax abo e a h eshold o 10
◦
C a e o impo ance in almos
e e y ecological egion, hei impac is spa ially di e en , alone o oge he wi h o he
ai s. An unexpec ed esul is he impo ance o he soil mois u e in he d ies egions o
he con inen (i.e., he Medi e anean- ype a eas). I is in e es ing o no e ha his is he
a ea in which H. ma gina um has been his o ically eco ded. We in e p e his esul as he
join e ec o se e al a iables, wi h a spa ially di e en ela i e impo ance collec i ely
p omo ing s able niches in he egion ha is commonly colonized by he ick, esul ing in
he imp o emen o i s ES.
Ano he unexpec ed esul is he lack o signi ican esul s in he mul iple eg essions
linking he end o Tmin wi h ES in many o he coldes pa s o he analyzed e i o y:
minimum empe a u e seems no o be a limi ing ac o o he sui abili y o H. magina um
in cen al Eu ope; his is an a ea ha is commonly conside ed o be unsui able o he
ick because o he eezing minimum empe a u es. Ou esul s show ha minimum
empe a u e, as eco ded o Eu ope, should no be conside ed a ac o esponsible o high
ick mo ali y, as has been widely sugges ed [
28
,
29
], a leas in he ime pe iod conside ed.
The end o ES o H. ma gina um is d i en by changes in a iables ha ha e a spa ially
di e en ela i e impo ance, al hough he daily sum o Tmax and he numbe o days
abo e he h eshold o 10
◦
C seem o be he bes explana o y a iables, a leas in he pe iod
o ime selec ed in he a ge e i o y.
As expec ed, he wa e apo de ici in he ai is no a ai impac ing long- e m
changes o he en i onmen al niche o he ick. I is no possible o gene alize his inding
o o he ick species, because o hei di e en ecological equi emen s. Wa e apo de ici ,
a a iable measu ed well abo e he g ound su ace, is o li le impo ance in delinea ing
he changes o ES o H. ma gina um. This unde lines he impo ance o choosing a iables
wi h ecological meaning o e e y ick species, as opposed o adhe ing o simplis ic, “one
Pa hogens 2021,10, 95 9 o 13
size i s all” app oaches. Howe e , his ai , oge he wi h mean o accumula ed ain all,
ha e been la gely used o model he en i onmen al sui abili y o icks. We would like
o ecommend a e ision o p e iously published conclusions ega ding he e ec o ain
o o he a mosphe ic “wa e ” a iables on he modeling o he en i onmen al niches o
icks. While NDVI (No malized De i ed Vege a ion Index) should be applied when using
sa elli e-de i ed da a, a measu e o soil su ace mois u e seems o be impo an when using
adi ional wea he ai s de i ed om e-assessmen s o clima e eco ding s a ions.
In any case, he e is no ques ion ha wea he ends a e gi ing ise o en i onmen ally
sui able condi ions o H. ma gina um in ela i ely la ge a eas in Eu ope, a inding ha is
consis en wi h nume ous epo s on a eas in he con inen in ecen yea s [
14
–
18
] and a
p e ious analysis, a a oughe esolu ion, buil on a physiological model [
19
] explo ing
de elopmen al and mo ali y a es. When and whe e we expec ha ES would inc ease
o e a c i ical h eshold o allow pe manen popula ions o he ick o become es ablished
is di icul o p edic , because ends a e spa ially di e en . In any case, we hypo hesize
ha en i onmen al changes will no expand no hwa d g adually om he inges o he
cu en ly known ick dis ibu ion. We expec ha la ge e i o ies o he a ge egion
will simul aneously su pass he c i ical en i onmen al h eshold, and as domains will
become sui able in a ew yea s. This hypo hesis is based on he indings epo ed in his
s udy, pinpoin ing he combined e ec s o se e al es ic ing a iables ac ing oge he , an
issue which has no been add essed be o e.
Bo h c i ical alues o empe a u e and soil humidi y impac he ES o H. ma gina um,
bu some a iables ha e a s onge e ec acco ding o he biogeog aphical egion, an
unexpec ed esul o his s udy. The join end o hese ai s is al e ing he ES o he a ge
ick in o he op imum a an unp eceden ed a e in la ge a eas o Eu ope. Ne e heless, i is
necessa y o s ess ha wi hou he adequa e densi y o la ge e eb a es necessa y o eed
he adul icks, pe manen popula ions o H. ma gina um a e highly imp obable, e en i
adequa e en i onmen al condi ions exis . This is hus a call o ac i e su eillance o he
ick, a p elimina y s ep o he adap a ion o he impac o his in asi e species.
4. Ma e ial and me hods
4.1. Backg ound
We aimed o e alua e he ends o ES o H. ma gina um in he pe iod 1970–2018 in a
e i o y co e ing Eu ope, be ween 16
◦
W, 28
◦
N and 49
◦
E, 71
◦
N. In his s udy, we adhe ed
o a s ic de ini ion o he en i onmen al niche o H. ma gina um wi hou conside ing
in e ac ions wi h hos s. We aimed o e alua e he end o he clima e and he changes o
he equisi es o ick su i al, no o p edic he p obabili y o pe manen popula ions o
he ick. The en i onmen al niche o an o ganism is de ined as he combina ion o ai s in
an a ea ha d aw i s p obabili y o pe sis ence [
27
]. To calcula e he ES o H. ma gina um,
we used: (i) a se o clima e a iables be ween he yea s 1970–2018; (ii) an e alua ion o he
ES o he ick using a maximum en opy algo i hm, elying on a se o known eco ds o
he ick; and (iii) an explici e alua ion o ends in he pe iod and a ge e i o y, as well
as a solid e alua ion o he mos impo an d i ing a iables.
4.2. Ob aining Clima e Da a
Clima e da a we e ob ained om he Te aClima e websi e (h p://www.clima ologylab.
o g/ e aclima e.h ml, accessed in Janua y 2020). We chose ou e-assessed p oduc s, a
mon hly in e als, namely: (i) maximum empe a u e (TMax) (ii) minimum empe a u e
(TMin) (iii) wa e apo de ici (WVD), and (i ) soil humidi y (SH), o he pe iod 1970–
2018. These da a ha e a spa ial nominal esolu ion o 4 km. Wa e apo de ici is measu ed
a 2 m abo e he g ound. Acco ding o p e ious s udies on he ecology o he ick [
30
],
hese da a should be adequa e o de ining he en i onmen al niche o H. ma gina um.
Mon hly da a we e ans o med by ha monic eg ession. This echnique was de el-
oped by Fou ie [
31
], enabling he decomposi ion o a ime se ies in o a eg ession de ined
by sine and cosine, including he i s h ee coe icien s o he ha monic eg ession o each