In asi e ho ne s on he oad:
mo o way-d i en dispe sal mus be
conside ed in managemen plans o Vespa elu ina
Ma ia João Ve dasca1, Hugo Rebelo2,3, Luísa G. Ca alhei o1,4, Rui Rebelo1
1Cen e o Ecology, E olu ion and En i onmen al Changes (cE3c), Faculdade de Ciências da Uni e sidade
de Lisboa, C2, Campo G ande, 1749-016 Lisboa, Po ugal 2CIBIO/InBIO, Uni e sidade do Po o, Campus
Ag á io Vai ão, Pad e A mando Quin as, 4485-661 Vai ão, Po ugal 3 CEABN/InBIO, Uni e sidade de
Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Po ugal 4Depa amen o de Ecologia, Uni e sidade Fede al de
Goiás, Goiânia, B asil
Co esponding au ho : Ma ia João Ve dasca (mjoao[email p o ec ed])
Academic edi o : Rami o Bus aman e|Recei ed 9 July 2021|Accep ed 28 Sep embe 2021|Published 15 No embe 2021
Ci a ion: Ve dasca MJ, Rebelo H, Ca alhei o LG, Rebelo R (2021) In asi e ho ne s on he oad: mo o way-d i en
dispe sal mus be conside ed in managemen plans o Vespa elu ina. NeoBio a 69: 177–198. h ps://doi.o g/10.3897/
neobio a.69.71352
Abs ac
Unde s anding he mechanisms ha po en ia e he dispe sion o an in asi e species is essen ial o an icipa e i s
a i al in o new egions and o de elop adequa e managemen ac ions o minimize damage o biodi e si y and
socie y. One o he mos success ul in ade s in Eu ope, he yellow-legged ho ne (Vespa elu ina), is dispe sing
h ough sel -di usion and jump dispe sal. Using in o ma ion on species occu ence in Po ugal om 2013 o
2018, his s udy aimed o unde s and he ange expansion ajec o y o V. elu ina and o iden i y he ole o
clima e, landscape and an h opogenic a iables on he wo mechanisms o sp ead. We ound ha in Po ugal
he in asion is p oceeding as e sou hwa ds (45 km/yea ) along he A lan ic coas han eas wa ds (20 km/
yea ) whe e he clima ic sui abili y g adien is mo e comp essed, wi h jump dispe sal playing an impo an
ole in his di e ence and in he accele a ion o he in asion p ocess. Dispe sal by di usion was bes explained
by he annual ange o empe a u e and p ecipi a ion o he we es mon h, wi h dis ance o sh ub land also
ha ing an impo an ole. Addi ionally, jump dispe sal appea ed o be acili a ed by mo o ways, hin ing a he
ole o human-media ed dispe sal. Indeed, he numbe o nes s ha esul ed om his dispe si e mechanism
we e signi ican ly close o mo o ways han expec ed by chance. To p e en he dispe sal o V. elu ina in o
Medi e anean egions, and in addi ion o a special a en ion o he ad ancing on , ea ly moni o ing p o-
g ams should also a ge a bu e zone on bo h sides o mo o ways, and a eigh shipping hubs.
Keywo ds
Clima ic g adien , di usion dispe sal, human-media ed dispe sal, jump dispe sal, mo o ways, Vespa elu ina
NeoBio a 69: 177–198 (2021)
doi: 10.3897/neobio a.69.71352
h ps://neobio a.penso .ne
Copy igh Ma ia João Ve dasca e al. This is an open access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License
(CC BY 4.0), which pe mi s un es ic ed use, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal au ho and sou ce a e c edi ed.
RESEARCH ARTICLE
Ad ancing esea ch on alien species and biological in asions
A pee - e iewed open-access jou nal
NeoBio a
Ma ia João Ve dasca e al. / NeoBio a 69: 177–198 (2021)
178
In oduc ion
In asi e species can ha e impo an en i onmen al and socioeconomic impac s. Know-
ing he dispe sal ou es o such species is c ucial o an icipa e hei a i al and de ine
adequa e managemen p ac ices in a imely ashion. In asi eness (a dynamic p ope y
o he species) and in asibili y (a p ope y o a loca ion ha can change wi h an h o-
pogenic dis u bance, seasons, clima e change), wo key componen s o biological in a-
sions, a e hough o be p ima ily de e mined by species’ dispe sal abili y and habi a
sui abili y, espec i ely (B ooks 2007). In asi eness is hus media ed by li e s a egies
(Pysek and Richa dson 2007), whe eas in asibili y is ela ed o local condi ions a he
si e, habi a o landscape le els (Vicen e e al. 2010). Fo a isk assessmen o he ul-
ne abili y o a si e o an in asi e species i is he e o e impo an o ha e de ailed in o -
ma ion on bo h he species’ ecological niche (i.e., s a ic in o ma ion, such as clima ic
ole ance) and mo emen abili y, which will egula e i and when sui able a eas away
om he si e whe e he in asion s a ed will be eached (i.e., dynamic in o ma ion).
Including such in o ma ion on dis ibu ion models o in asi e species can help o dis-
inguish sui able habi a ha is, o can be po en ially occupied, om sui able habi a
ha is inaccessible (Mille and Holloway 2015).
As di e en en i onmen al condi ions and landscape he e ogenei y may accele a e
o hampe he in asi e p ocess (Has ings e al. 2005), i is also impo an o iden i y
he pa e ns o ange expansion. Th ee di e en ajec o ies o ange expansion e sus
ime can be conside ed: linea (Andow e al. 1990), biphasic (wi h an ini ial shallow
slope ollowed by a s eep linea slope), and accele a ing wi h ime, quickly eaching he
sa u a ion phase (Shigesada e al. 1995). The h ee expansion pa e ns occu h ough
ei he sel -media ed dispe sal om an ini ial loca ion (di usion; Lockwood e al. 2007)
o jump dispe sal in o egions ela i ely a om he co e dis ibu ion a ea wi hou col-
onizing he egions in be ween, leading o he es ablishmen o nascen colonies (Su-
a ez e al. 2001), “ou pos s” he ea e . I ou pos s es ablish in en i onmen ally sui able
a eas he species can con inue he expansion p ocess om he e, accele a ing i . When
a species sp eads h ough bo h p ocesses (na u al di usion and jump dispe sal), s a i-
ied di usion occu s (Henge eld 1989; Sua ez e al. 2001). In such a p ocess, he ini ial
ange expansion occu s mainly by di usion, bu as he a ea o he ounde popula ion
expands, new nes s c ea ed by long-dis ance e en s accele a e ange expansion in la e
phases (Shigesada e al. 1995; see also some insec examples in Andow e al. (1990)).
Insec s a e he dominan g oup among non-na i e e es ial in e eb a es in Eu-
ope (Roques e al. 2009). Social insec s, in pa icula social Hymenop e a, a e likely o
become success ul in ade s due o hei excellen dispe sal abili ies, high ep oduc i e
a es in an annual li e cycle, b oad die s and habi a anges, colony ini ia ion by a sin-
gle insemina ed queen, and o hei close associa ion wi h human anspo a ion wi h
ela i ely low p obabili y o de ec ion (Molle 1996; Beggs e al. 2011). These cha ac-
e is ics a o he in asi eness o eusocial insec s, gi ing hem a plas ici y o esponses
ha allow hei su i al and es ablishmen in new en i onmen s. Impac s o in asi e
social insec s include changes o ecosys em unc ions, compe i i e displacemen o
Mo o ways speed na u al in asion dynamics o Vespa elu ina 179
na i e species, hyb idiza ion wi h na i e species, h ea s o human o animal heal h
h ough s ings o he ansmission o pa hogens (Schneide e al. 2004; Les e and
Beggs 2019). One example o an in asi e eusocial insec ha is cu en ly sp eading
in Eu ope is he yellow-legged ho ne , (Vespa elu ina Lepele ie , 1836), an agg essi e
p eda o o honeybees and wild pollina o s, ha is pu ing honey and ag icul u al p o-
duc ion a isk (Monceau e al. 2014; Ve dasca e al. 2021). The high dispe sal abili y
o his in asi e combined wi h he lack o ue compe i o s and wi h he a ailabili y o
ood esou ces in Eu ope, has been a o ing i s expansion in his con inen . A e he
acciden al in oduc ion o V. elu ina in F ance in 2004, p obably by a single emale
o igina ing om empe a e sou h-eas e n China (A ca e al. 2015), he in asion sp ead
o o he Eu opean coun ies – Spain, Po ugal, Belgium, I aly, Ge many, Uni ed King-
dom, Ne he lands and Luxembou g, being he ho ne now conside ed an in asi e al-
ien species o conce n in he Eu opean Union (Eu opean Commission 2016). In 2011,
a new in asion was de ec ed in he no h o Po ugal (G osso-Sil a and Maia 2012)
ha hen expanded sou hwa d in o he cen e o Po ugal (Ca alho e al. 2020) ac oss
a clima e g adien be ween Tempe a e and Medi e anean bioclima es (Ri as-Ma ínez
e al. 2017; Say e e al. 2020) and no hwa d in o Galicia (Spain) (Rod íguez-Flo es
e al. 2019). The cu en Eu opean dis ibu ion o his species, mos ly concen a ed
along he A lan ic coas , aligns wi h he clima ic p e e ences p edic ed by Villeman e
al. (2011). As a cen al place o age , wo ke s o V. elu ina op imally explo e o aging
a eas 500 m o 800 m om hei nes s, al hough he maximum homing abili y ( he
maximal dis ance an indi idual is able o a el on i s way home) o he ho ne is much
g ea e (5000 m; Poida z e al. 2018).
The sp ead o V. elu ina in Eu ope has been conside ed a s a i ied di usion p o-
cess, including a mix u e o na u al di usion and jump dispe sal e en s (Be olino
e al. 2016; Robine e al. 2017; Lioy e al. 2019). Jump dispe sal may occu by wo
di e en p ocesses: sel -dispe sal o gynes (queens o he nex gene a ion), which a e
able o ly long dis ances on hei own (18 km/day in ligh mill expe imen s – pe s.
comm., D . D. Sau a d, INRA, F ance o he au ho s o Robine e al. 2017), o
h ough human-media ed dispe sal (Robine e al. 2019). Due o he di icul y in dis-
en angling hese p ocesses, only occu ence poin s ound mo e han 78 km (yea ly
sp ead a e in F ance) om hei nea es neighbo s we e conside ed o esul om long
dis ance dispe sal e en s by Robine e al. (2017). Howe e , Be olino e al. (2016),
wo king in No hwes I aly, conside ed a much sho e dis ance as he limi o e which
human-media ed dispe sal was conside ed he mos likely explana ion o jump dis-
pe sal e en s (yea ly sp ead a e in I aly = 18.3 ± 3.3 km). Besides he di e en me h-
odological app oaches (including he scale o analysis), he di e ences be ween he wo
s udies a e a ibu ed by Be olino e al. (2016) o he I alian moun ainous e i o y,
when compa ed wi h he la gely la no h wes e n and cen al F ance, while Robine
e . al. (2017) jus i y he high sp ead a e in F ance by he abili y o ounde emales o
lying long dis ances in ligh mill expe imen s.
P ecipi a ion and empe a u e a e hough o be he s onges p edic o s o he
in asi e ange o V. elu ina (Villeman e al. 2011), wi h land-use also playing an
Ma ia João Ve dasca e al. / NeoBio a 69: 177–198 (2021)
180
impo an ole a a egional scale (Bessa e al. 2016). This ho ne is now colonizing he
Medi e anean peninsulas, and he e o e being exposed o he i s ime o a Medi e -
anean clima e. As he species sp eads along he ansi ional empe a e-Medi e anean
clima e egions, i is impo an o assess he ex en o sui able a ea a a ine esolu ion,
as well as o unde s and how he in asion p ocess is un olding and he ole o human-
media ed dispe sal. A ecen s udy highligh ed he need o iden i y he coloniza ion
pa hways and plan managemen app oaches o hal he sp ead o V. elu ina in Po ugal
(Ca alho e al. 2020). A a egional scale, he iden i ica ion o a limi ed numbe o key
a iables explaining he dispe sal and es ablishmen success o V. elu ina can acili a e
he c ea ion o e ec i e p e en i e and con ol measu es. In his s udy, we inco po a ed
land co e and an h opogenic d i e s o p edic he isk o in asion by V. elu ina wi h-
in he ansi ional empe a e-Medi e anean zones and in e coloniza ion pa hways.
Mo e speci ically, we (i) assessed he oles o di usion and jump dispe sal on V. elu ina
expansion in o Medi e anean- ype clima es and (ii) iden i ied which en i onmen al
a ibu es a e mos in luen ial on he di ec ion and speed o i s dispe sal.
Ma e ial and me hods
Nes occu ence da a in Po ugal
Fo his s udy, we ocused on he seconda y in oduc ion e en o he ho ne in Po u-
gal and used all o he a ailable Po uguese p esence da a o V. elu ina (8610 eco ds
o nes s, om 2013 o 2018). Da a was ob ained om Bombei os Volun á ios de Vi-
ana do Cas elo and om he online pla o m ‘STOP espa’ (h p://s op espa.icn .p /),
which is managed by he Ins i u o da Conse ação da Na u eza e das Flo es as (ICNF)
and agg ega es all alida ed Po uguese eco ds o V. elu ina nes s ha we e p e iously
egis e ed in he pla o m by ci izens. To a oid spa ial au oco ela ion, we educed
he numbe o occu ence da a poin s h ough he spa ially a e y occu ence da a
ool (pixel size esolu ion: 300 m) in SDM oolbox (B own 2014) in A cGIS 10.4.1
(ESRI 2016); his esul ed in a o al o 7847 poin s (Suppl. ma e ial 2: Appendix A).
To calcula e he con inuous dis ibu ion a ea o V. elu ina (2013 o 2018) we d ew
a 5km bu e a ound each nes . The wo ke s o V. elu ina p obably o age less han
1000m om hei nes , and his bu e o 5 km co esponds o he es ima ed maxi-
mum homing abili y o he species, since ew wo ke s ha e he abili y o pe o m long
ips (Poida z e al. 2018). Mo eo e , and acco ding o (Lioy e al. 2019), mos new
nes s (>90%) in NW I aly we e loca ed wi hin his adius o hei nea es sou ce o he
p e ious yea . All he con iguous bu e s we e agg ega ed o es ablish each yea ’s con-
inuous dis ibu ion; all eco ds ou side he con inuous a ea o he p e ious yea we e
conside ed expansion nes s. F om hese expansion nes s, hose loca ed wi hin he new
con inuous a ea we e conside ed o esul om di usion dispe sal and hose ound
ou side his new limi we e conside ed ou pos s (i.e., an e idence o jump dispe sal,
h ough ei he sel -media ed o human-media ed).
Mo o ways speed na u al in asion dynamics o Vespa elu ina 181
Range expansion
To iden i y he ange expansion ajec o y, we calcula ed he annual inc emen in he
con inuous a ea. The numbe o new ou pos s pe yea was coun ed and hei con-
ibu ion o he o e all expansion was es ima ed by iden i ying hose ou pos s ha
could ha e unc ioned as a sou ce o o he nes s. To asce ain a possible o igin o
each expansion colony and ou pos , we compa ed i s dis ance o he nea es edge o
he con inuous a ea and o he nea es ou pos o he p e ious yea ; all he eco ds o
which he di e ence be ween bo h dis ances was lowe han 5 km (co esponding o
1419 eco ds) we e disca ded, being conside ed o non-a ibu able o igin.
The yea ly expansion esul ing om di usion dispe sal along he N-S and W-E axes
was es ima ed by measu ing he dis ance o he sou h and eas be ween consecu i e limi s
o he con inuous dis ibu ion a ea. The numbe o new nes s es ablished exclusi ely o
he sou h and eas om he p e ious con inuous limi was coun ed and we iden i ied how
many o hese we e ou pos s. Yea ly, o each ou pos , i s dis ance o he nea es sou ce
o he p e ious yea was measu ed. To es o an accele a ion o bo h ypes o expansion,
he slopes o he ela ionships be ween hese dis ances and yea was compa ed wi h ze o.
En i onmen al d i e s
Assuming ha he same a iables in luencing dis ibu ion ha e he po en ial o p o-
mo e i s dispe sal, we conside ed h ee clima ic and eigh land co e and an h opogen-
ic a iables (see Suppl. ma e ial 1: Table S1). Va iables in his s udy we e adap ed om
Bessa e al. (2016), wi h he ollowing changes: i) we excluded NDVI and iso he mal-
i y, ii) we used he dis ance o each speci ic land co e class ins ead o i s pe cen age
because using dis ances assu es be e pe o mance o landscape ea u es (Rainho and
Palmei im 2011), iii) we inco po a ed he classes “dis ance o o es ” and “index o
human in luence” and i ) we included p edic o s ela ed o he dis ance o linea s uc-
u es (mo o ways and ailways). To a oid collinea i y, we inspec ed i he e we e highly
co ela ed a iables ( ≥0.70; Do mann e al. 2013) (see Suppl. ma e ial 1: Table S2).
Fo his analysis we used h ee da ase s: i) bound eco ds ( he se ies o poin s de ining a
minimum con ex polygon ha ep esen s he leading edge o he con inuous in aded
a ea o each pa icula yea , p esumably esul ing om dispe sal by di usion), ii) all
ou pos s ( esul ing om jump dispe sal) and iii) > 18 km ou pos s, ep esen ing he
subse o ou pos s loca ed mo e han 18 km (dis ance a elled in ligh mill expe i-
men s – pe s. comm., D . D. Sau a d, INRA, F ance o he au ho s o Robine e al.
2017) om he con inuous a ea o he espec i e yea , o which he e is p obably a
highe con ibu ion o human-media ed dispe sal.
Da a analyses
To assess which a iables in luence he dispe sal o V. elu ina o each o he h ee da a-
se s we used gene alized linea mixed models (GLMM) wi h he package ‘lme4’ (Ba es e

Ma ia João Ve dasca e al. / NeoBio a 69: 177–198 (2021)
182
al. 2015) in R (Co e Team 2019). We began by unning ull models wi h clima ic, land
co e and an h opogenic d i e s simul aneously. As clima ic a iables a e acknowledged
o be he main ac o s in luencing he species dis ibu ion ac oss a ying spa ial scales
(Pea son and Dawson 2003), we decided o un addi ional models wi h land co e and
an h opogenic a iables only, in an a emp o ind o he possible p edic o s a a egional
scale. Fo each da ase , we se he dependen a iable as he minimum dis ance o he
eco ds o he con inuous a ea o he p e ious yea (we disca ded h ee eco ds ha we e
loca ed less han 5 km om an ou pos es ablished in he p e ious yea , as ha could
be an o shoo o ha ou pos ). To de ec collinea i y be ween explana o y a iables we
used he Vi s ep unc ion in he usdm R package (Naimi e al. 2014) o calcula e he
a iance in la ion ac o (VIF) and excluded he a iables in models wi h a VIF alue
g ea e han he h eshold ( h=3). A a iable “yea ” was included as a andom e ec o
accoun o yea ly clima ic a ia ions ha may a ec he dispe sal o he ho ne . We hen
selec ed he bes model (using he Akaike In o ma ion C i e ion – AIC) wi h he d edge
R unc ion, and gene a ed a e age es ima es o he e ec o each a iable using he mod-
el.a g R unc ion (models wi h del a AIC alues < 2) om he MuMIn package (Ba ón
2009). The esul s we e plo ed using he package is eg (B eheny and Bu che 2017).
As we e i ied ha one an h opogenic p edic o (dis ance o mo o ways; see Re-
sul s) was in luen ial on ho ne jump dispe sal we decided o u he explo e he da a.
Fi s , we inspec ed i he ou pos s’ dis ance o mo o ways was andom, i.e., we es ed
whe he mo o ways may be ac ing as d i e s o jump dispe sal. To accomplish his, we
gene a ed a win andom poin o each ou pos , loca ed a he same Euclidean dis ance
o he con inuous dis ibu ion a ea as he ou pos , and compa ed hei dis ance o mo-
o ways wi h a pai ed samples Wilcoxon es . Second, o bo h da a se s o ou pos s we
an ano he GLMM model, bu his ime wi h he dis ance o he en i e oad ne wo k
o inspec he ela i e impo ance o each oad ca ego y in ho ne jump dispe sal.
To gene a e a isk map o V. elu ina dispe sal and iden i y egions mos a isk o im-
minen in asion, we combined in o ma ion om sui able a eas ( egions wi h ainy win e s
and pleasan summe s, mainly loca ed along he A lan ic coas : Ve dasca e al., unpublished
da a) wi h he geog aphical in o ma ion o he signi ican dispe sal p edic o s o a model
wi h clima e, land co e and an h opogenic a iables (see Suppl. ma e ial 1: TableS4).
These p edic o s we e combined acco ding o hei es ima es o p oduce a dispe sal map.
To de ine he isk a eas a ound mo o ways, we analyzed he pa e n o he numbe o
ou pos s as a unc ion o dis ance o mo o ways. As he numbe o new nes s es ablished
alongside he mo o ways dec eased linea ly wi h dis ance up o 17 km om he highway
(a e ha he e was no appa en ela ion wi h dis ance – see Resul s), we calcula ed his
ela ion o es ima e he wid h o he a eas ha con ained 50% and 75% o he ou pos s.
A ailabili y o da a and ma e ial
Due o p i acy easons, public da a is a ailable in Suppl. ma e ial 2: Appendix A o
Suppo ing In o ma ion in a esolu ion o 5 × 5 km. The p ecise geo-localiza ions ha
suppo he indings o his wo k (which we e used unde license o he cu en s udy)
Mo o ways speed na u al in asion dynamics o Vespa elu ina 183
a e a ailable om he au ho s upon easonable eques and a e pe mission o he
en i ies holding he da a. Da a eques s can be add essed o he co esponding au ho ,
who will make hem a ailable join ly wi h he di e en en i ies ha hold he da a. Any
u he in o ma ion can be ob ained by eques o he au ho s.
Resul s
F om 2013 o 2018, he a ea occupied by V. elu ina in Po ugal expe ienced a 25- old
inc ease ( om 845 km2 o 20,561.26 km2) in a linea manne wi hou accele a ion o
decele a ion (Fig. 1). Expansion was much as e along he no h-sou h axis (45 km/yea )
han along he wes -eas axis ( oughly 20 km/yea ), ega dless o aking place in empe -
a e (in 2014 and 2015) o Medi e anean clima e egions (since 2016) (Fig. 1 and Fig. 2).
0
5000
10000
15000
20000
25000
2013 2014 2015 2016 2017 2018
0
50
100
150
200
250
mk( ae a deipucco e i alumuC 2)
yea
Cumula e dis ance (km)
Cumula e occupied a ea (km2)
Cumula e dis ance o he sou he n limi (km)
Cumula e dis ance o he eas e n limi (km)
Figu e 1. Annual expansion o V. elu ina. The pic u e depic s he wo cumula i e linea dis ances ( igh
axis) be ween he in asion o igin and he successi e limi s o he in asion on o he sou h (black line)
and eas (da k g ey line). The sou he n and eas e n limi s o each yea we e measu ed by simply d awing a
angen o he sou he nmos poin and he eas e nmos poin , espec i ely. The le axis e e s o he yea ly
cumula i e in aded a ea (in km2) esul ing om di usion dispe sal and depic ed as a g ay a ea.
Ma ia João Ve dasca e al. / NeoBio a 69: 177–198 (2021)
184
Figu e 2. In asion pa e n o V. elu ina in Po ugal be ween 2013 and 2018 along he clima ic g adien
(TMP – Tempe a e clima e, SP – Sup amedi e anean clima e, MM – Mesomedi e anean clima e and
TM – The momedi e anean. The igu e depic s he con inuous dis ibu ion a ea o V. elu ina in each
yea and he loca ion o he ou pos s (poin s wi h he highes dispe sal dis ances; see me hods) by yea . The
sui able a ea o he species was e ie ed om an unpublished wo k o he au ho s. The cu en in aded
a ea (by May 2021) is also shown.
Mo o ways speed na u al in asion dynamics o Vespa elu ina 185
Range expansion
The numbe o ou pos s a ied ac oss he di e en yea s om a minimum o 4 in 2016
o a maximum o 46 in 2015. Such ou pos s had a e y high impo ance o he expan-
sion o he ho ne . Indeed, he numbe o new expansion nes s ha we e loca ed nea
he ou pos s es ablished in he p e ious yea was highe han he numbe o new nes s
ound nea he p e ious con inuous limi in all yea s excep 2017 (Table 1).
In he i s h ee yea s (2014–2016), he mean dis ance o new nes s o he nea -
es ou pos was lowe han he dis ance o he con inuous a ea (Suppl. ma e ial 1: Fig.
S1). The e e se scena io occu ed in 2017 and 2018, when almos all ou pos s we e
es ablished in Medi e anean-clima e egions. As he co e dis ibu ion a ea expanded
o he sou h and eas , some ou pos s ha ga e ise o new nes s nea by we e engul ed
in o he con inuous dis ibu ion a ea (i.e., coalescen colony model; Fig. 2).
Ou pos s es ablished sou hwa ds we e o e 3 imes mo e equen han hose es-
ablished eas wa ds (Table 2). The e was a dec ease in he numbe o success ully es ab-
lished nes s since 2016, especially sou hwa ds (Table 2). The slope o he ela ionship
be ween ime and dispe sal dis ance o he sou h and eas was no signi ican ly di e -
en om ze o, o bo h ypes o dispe sal (di usion o jump dispe sal) (Suppl. ma e ial
1: Table S3). Mos ou pos s (90%) we e loca ed mo e han 18 km om he con inuous
a ea o he p e ious yea .
En i onmen al d i e s
Models wi h bo h clima ic and land co e a iables explained mo e a iabili y o he
dispe sal pa e ns o V elu ina han models solely wi h clima ic o land co e a iables
(Suppl. ma e ial 1: Tables S6–S8). A clima ic a iable – p ecipi a ion o he we es
Table 1. The numbe o new nes s and ou pos s o V. elu ina (ou side he con inuous dis ibu ion a ea
o he p e ious yea ), be ween 2014 and 2018.
Yea Numbe o new nes s loca ed nea e he
con inuous a ea o he p e ious yea
Numbe o new nes s loca ed nea e an
ou pos o he p e ious yea
To al numbe
o ou pos s
Numbe o “>
18km ou pos s”
2014 55 83 10 7
2015 418 491 46 46
2016 69 103 4 3
2017 230 163 10 8
2018 165 174 33 29
To al 937 1014 103 93
Table 2. Annual numbe o new occu ences egis e ed exclusi ely sou hwa ds and eas wa ds.
Yea Numbe o new eco ds exclusi ely sou hwa ds Numbe o new eco ds exclusi ely eas wa ds
2014 128 (+ 1 ou pos ) 1 (+ 1 ou pos )
2015 120 (+ 23 ou pos s) 330 (+ 6 ou pos s)
2016 225 (+ 1 ou pos ) 1 ou pos
2017 123 (+ 8 ou pos s) 19 (+ 2 ou pos s)
2018 24 (+ 20 ou pos s) 8 (+ 3 ou pos s)
To al 620 (+ 53 ou pos s) 359 (+ 13 ou pos s)
Ma ia João Ve dasca e al. / NeoBio a 69: 177–198 (2021)
192
whe e a high numbe o he obse a ions and cap u es o V. elu ina in bai - aps
we e eco ded nea highways, emphasizing ha eigh a ic can con ibu e o he
anspo o his species a om he in asion on . The ac ha Bessa and collabo a-
o s (2016) did no ind any ela ion wi h he oad ne wo k could be due o he e y
es ic ed egion ha was used in hei s udy ( oughly 10% o he a ea ha we used
he e). In F ance, Robine e al. (2017) used human popula ion densi y as a p oxy o
ade o es jump dispe sal, no aking in o accoun he oad ne wo k, and concluded
ha he apid sp ead o he ho ne may no be necessa ily media ed by humans. So,
i is possible ha long-dis ance dispe sal e en s ha occu ed in F ance may also ha e
con ibu ed o unin en ional in oduc ions ia mo o ways.
Despi e i being ex emely di icul o p o ide e idence o ea ly in oduc ions,
o he social insec s ha e also p obably been anspo ed acciden ally by humans o e
long dis ances since he es ablishmen o long-dis ance ade ou es (Be elsmeie
2021). Fo example, New Zealand had no social wasp species p io o human colo-
niza ion, bu o e he las cen u y has been in aded by se e al species o social wasps
(Les e and Beggs 2019). Indeed, Vespula ge manica and Vespula ulga is, bo h na i e
om Eu asia, ha e become widesp ead h oughou he New Zealand causing majo
impac s o na i e biodi e si y (Les e e al. 2014). In A gen ina, whe e V. ge manica is
also in asi e, he obse ed s a i ied geog aphical expansion pa e n (which equen ly
exceeds 30 km pe yea , al hough as e o sou h) does no ma ch he obse ed queen
dispe sal abili ies (only a ew hund ed me e s na u ally o ind nes si es), sugges ing
ha human-aided anspo o hibe na ing queens is he cen al d i e o he cu en
dis ibu ion o hese wasps in he coun y (Masciocchi and Co ley 2012). A mo e
local scales, he an h opogenic in luence on he sp ead o in asi e insec s was also
demons a ed. Fo example, he dis ance o ail oad acks in luenced he sp ead o he
in asi e e mi e species Re iculi e mes la ipes (Pe de eau e al. 2019).
Implica ions o he managemen o Vespa elu ina in asion p ocess
Iden i ying pa hways ha acili a e he dispe sal o in asi e species is essen ial o in-
o ming e o s o con ain in asions (Sua ez e . al. 2001). To be success ul, e e y in asi e
species con ol p og am mus conside he p obabili y o de ec ing he species and he
cos o he p ocess. In his wo k, we showed ha 50% o he p esumed new nes s esul -
ing om human-media ed long-dis ance dispe sal es ablished wi hin a 6km wide bu e
along mo o ways. To aise his p opo ion o 75%, he bu e mus be inc eased o 12
km, which ep esen s an almos 70% inc ease in he a ea o be su eyed. Based on esul s
he e, e ec i e measu es o con ain V. elu ina in asions should include ea ly moni o ing
p og ams in a bu e o 5 km ( he maximum homing abili y ha ew ho ne wo ke s can
each: Poida z e al. 2018) a ound he con inuous dis ibu ion a ea o he p e ious yea ,
and 6 km (ideally 12 km) a ound mo o ways. I he clima ic condi ions a e me , he
icini y o he main oads is suscep ible o be colonized as e h ough human-media ed
anspo . E en in highly agmen ed habi a s, he main oads can connec isola ed sui -
able a eas. Fo ins ance, in he egions a isk in sou he n Po ugal, he a ea o be su eyed
can be limi ed only o clima ically a o able egions ha a e eachable by highway. This is

Mo o ways speed na u al in asion dynamics o Vespa elu ina 193
pa icula ly ele an in sou he n Po ugal whe e he isola ed agmen s o sui able land-
scape a e economically e y impo an o beekeeping ac i i ies. The ea ly de ec ion and
con ol o nascen popula ions in hese a eas may be a good way o manage i s sp ead,
a he han ocusing e o s on es ablished in asion on s. Local ou each ac i i ies, es-
pecially hose a ge ed o anspo a ion companies, should also be p io i ized o p e en
he Eu opean mo o way ne wo k om becoming an in asion ou e o he ho ne o new
coun ies. Howe e , di e en ypes o ca go do no ca y he same isk o being in es ed
(as di e en species may di e in hei commodi y associa ions). The e o e, ocused bi-
osecu i y policies o V. elu ina, a e needed, pa icula ly a ge ed o he in e cep ion o
wooden p oduc s’ anspo a ion and man-made goods associa ed wi h ga den ade, due
o he po en ial o hese commodi ies o shel e hibe na ing queens. I is also impo an
o p omo e con ol ac ions on po s o species en y, namely ha bo s along he coas .
Acknowledgemen s
We hank Ins i u o da Conse ação da Na u eza e das Flo es as (ICNF) and Bombei-
os Volun á ios de Viana do Cas elo, o ha ing p o ided he eco ds o V. elu ina
occu ences in Po ugal. We hank José Ped o G anadei o and Ped o Segu ado o
hei insigh s on da a analysis. Fundação pa a a Ciência e a Tecnologia (FCT Po ugal)
p o ided inancial suppo h ough he p ojec UIDB/00329/2020 g an ed o cE3c.
MJV (PD/BD/128351/2017), HR (DL57/2016/EEC2018/07) and LGC (LISBOA-
01-0145-FEDER-028360/EUCLIPO) we e unded by FCT Po ugal. LGC was also
unded by he B azilian Na ional Council o Scien i ic and Technological De elop-
men (CNPq. Uni e sal 421668/2018-0; PQ 305157/2018-3).
Re e ences
Andow DA, Ka ei a PM, Le in SA, Okubo A (1990) Sp ead o in ading o ganisms. Landscape
Ecology 4: 177–188. h ps://doi.o g/10.1007/BF00132860
A ca M, Mougel F, Guillemaud T, Dupas S, Rome Q, Pe a d A, Mulle F, Fossoud A, Cap-
de ielle-Dulac C, To es-Leguizamon M, Chen X, Tan J, Jung C, Villeman C, A nold G,
Sil ain J (2015) Recons uc ing he in asion and he demog aphic his o y o he yellow-
legged ho ne , Vespa elu ina, in Eu ope. Biological In asions 17: 2357–2371. h ps://doi.
o g/10.1007/s10530-015-0880-9
Ba ón K (2009) Mu-MIn: Mul i-model in e ence. h p:// - o ge. -p ojec .o g/p ojec s/mumin/
Ba es D, Mächle M, Bolke BM, Walke SC (2015) Fi ing linea mixed-e ec s models using
lme4. Jou nal o S a is ical So wa e 67(1): 1–48. h ps://doi.o g/10.18637/jss. 067.i01
Beggs J, B ocke ho E, Co ley J, Kenis M, Masciocchi M, Mulle F, Rome Q, Villeman C
(2011) Ecological e ec s and managemen o in asi e alien Vespidae. BioCon ol 56: 505–
526. h ps://doi.o g/10.1007/s10526-011-9389-z
Be elsmeie C (2021) Globaliza ion and he an h opogenic sp ead o in asi e social insec s.
Cu en Opinion in Insec Science 46: 16–23. h ps://doi.o g/10.1016/j.cois.2021.01.006
Ma ia João Ve dasca e al. / NeoBio a 69: 177–198 (2021)
194
Be olino S, Lioy S, Lau ino D, Manino A, Po po a o M (2016) Sp ead o he in asi e yellow-
legged ho ne Vespa elu ina (Hymenop e a: Vespidae) in I aly. Applied En omology and
Zoology 51: 589–597. h ps://doi.o g/10.1007/s13355-016-0435-2
Bessa A, Ca alho J, Gomes A, San a ém F (2016) Clima e and land-use d i e s o in asion:
p edic ing he expansion o Vespa elu ina nig i ho ax in o he Ibe ian Peninsula. Insec
Conse a ion and Di e si y 9: 27–37. h ps://doi.o g/10.1111/icad.12140
B eheny P, Bu che W (2017) Package ‘ is eg’: Visualiza ion o Reg ession Models. The R
Jou nal 9: 56–71. h ps://doi.o g/10.32614/RJ-2017-046
B ooks M (2007) E ec s o land managemen p ac ices on plan in asions in wildland a eas.
In: Nen wig W (Ed.) Biological In asions. Sp inge , Sp inge -Ve lag, Be lin Heidelbe g,
147–162. h ps://doi.o g/10.1007/978-3-540-36920-2_9
B own JL (2014) SDM oolbox: A py hon-based GIS oolki o landscape gene ic, biogeo-
g aphic and species dis ibu ion model analyses. Me hods in Ecology and E olu ion 5:
694–700. h ps://doi.o g/10.1111/2041-210X.12200
Ca alho J, Hipóli o D, San a ém F, Ma ins R, Gomes A, Ca mo P, Rod igues R, G osso‐Sil a
J, Fonseca C (2020) Pa e ns o Vespa elu ina in asion in Po ugal using c owdsou ced da a.
Insec Conse a ion and Di e si y 13(5): 501–507. h ps://doi.o g/10.1111/icad.12418
Chaplin-K ame R, Tuxen-Be man K, K emen C (2011) Value o wildland habi a o sup-
plying pollina ion se ices o cali o nian ag icul u e. Rangelands 33: 33–41. h ps://doi.
o g/10.2111/1551-501X-33.3.33
Choi MB, Ma in S, Lee JW (2012) Dis ibu ion, sp ead, and impac o he in asi e ho ne
Vespa elu ina in Sou h Ko ea. Jou nal o Asia-Paci ic En omology 15: 473–477. h ps://
doi.o g/10.1016/j.aspen.2011.11.004
Do mann CF, Eli h J, Bache S, Buchmann C, Ca l G, Ca é G, Ma quéz JRG, G ube B,
La ou cade B, Lei ão PJ, Münkemülle T, Mcclean C, Osbo ne PE, Reineking B, Sch öde
B, Skidmo e AK, Zu ell D, Lau enbach S (2013) Collinea i y: A e iew o me hods o
deal wi h i and a simula ion s udy e alua ing hei pe o mance. Ecog aphy 36: 027–046.
h ps://doi.o g/10.1111/j.1600-0587.2012.07348.x
Eu opean Commission (2016) Commission Implemen ing Regula ion(EU) 2016/1141 o 13
July 2016 adop ing a lis o in asi e alien species o Union conce n pu suan o Regula ion
(EU) No 1143/2014 o he Eu opean Pa liamen and o he Council. O icial Jou nal o
he Eu opean Union 2016: 4–8.
G osso-Sil a JM, Maia M (2012) Vespa elu ina Lepele ie , 1836 (hymenop e a, Vespidae),
New Species o Po ugal. A qui os En omolóxicos 6: 53–54.
Has ings A, Cudding on K, Da ies K, Dugaw CJ, Elmendo S, F ees one A, Ha ison S,
Holland M, Lamb inos J, Mal adka U, Melbou ne B, Moo e K, Taylo C, Thomson D
(2005) The spa ial sp ead o in asions: new de elopmen s in heo y and e idence. Ecology
Le e s 8: 91–101. h ps://doi.o g/10.1111/j.1461-0248.2004.00687.x
Henge eld B (1989) Dynamics o biological in asions. Chapman & Hall, London.
Hu baue RA, Facon B, Ra igné V, Tu geon J, Foucaud J, Lee CE, Rey O, Es oup A (2011) An-
h opogenically induced adap a ion o in ade (AIAI): con empo a y adap a ion o human-
al e ed habi a s wi hin he na i e ange can p omo e in asions. E olu iona y Applica ions
5(1): 89–101. h ps://doi.o g/10.1111/j.1752-4571.2011.00211.x
Mo o ways speed na u al in asion dynamics o Vespa elu ina 195
ICNF (2019) S op espa. Ins i u o da Conse ação da Na u eza e das Flo es as. h ps://sig.
icn .p /po al/apps/webapp iewe /index.h ml?id=382b1a0c296c430b8b095461e465d8 3
[Decembe 30, 2020]
Les e PJ, Beggs JR (2019) In asion success and managemen s a egies o social Vespula
Wasps. Annual Re iew o En omology 64(2019): 51–71. h ps://doi.o g/10.1146/an-
nu e -en o-011118-111812
Les e PJ, B own SDJ, Edwa ds ED, Holwell GI, Pawson SM, Wa d DF, Wa s CH (2014)
C i ical issues acing New Zealand en omology. New Zealand En omologis 37: 1–13.
h ps://doi.o g/10.1080/00779962.2014.861789
Lioy S, Manino A, Po po a o M, Lau ino D, Romano A, Capello M, Be olino S (2019)
Es ablishing su eillance a eas o ackling he in asion o Vespa elu ina in ou b eaks and
o e he bo de o i s expanding ange. NeoBio a 46: 51–69. h ps://doi.o g/10.3897/
neobio a.46.33099
Lockwood JJL, Hoopes MFM, Ma che i MPM (2007) In asion ecology. Blackwell Publishing,
Malden, 313 pp.
Ma is G, B own M, Cu hbe son A (2011) GB Non-na i e O ganism Risk Assessmen Scheme
o Vespa elu ina nig i ho ax. Sand Hu on, UK [GB Non-Na i e Species sec e a ia ], 61 pp.
Masciocchi M, Co ley J (2012) Dis ibu ion, dispe sal and sp ead o he in asi e social
wasp (Vespula ge manica) in A gen ina. Aus al Ecology 38(2): 162–168. h ps://doi.
o g/10.1111/j.1442-9993.2012.02388.x
Mille JA, Holloway P (2015) Inco po a ing mo emen in species dis ibu ion models. P og ess
in Physical Geog aphy 39: 837–849. h ps://doi.o g/10.1177/0309133315580890
Molle H (1996) Lessons o in asion heo y om social insec s. Biological Conse a ion 78:
125–142. h ps://doi.o g/10.1016/0006-3207(96)00022-5
Monceau K, Bonna d O, Thié y D (2014) Vespa elu ina: A new in asi e p eda o o honeybees
in Eu ope. Jou nal o Pes Science 87: 1–16. h ps://doi.o g/10.1007/s10340-013-0537-3
Naimi B, Hamm NAS, G oen TA, Skidmo e AK, Toxopeus AG (2014) Whe e is posi ional
unce ain y a p oblem o species dis ibu ion modelling? Ecog aphy 37: 191–203. h ps://
doi.o g/10.1111/j.1600-0587.2013.00205.x
Pea son RG, Dawson TP (2003) P edic ing he impac s o clima e change on he dis ibu ion
o species: a e bioclima e en elope models use ul? Global Ecology & Biogeog aphy 12:
361–371. h ps://doi.o g/10.1046/j.1466-822X.2003.00042.x
Pe de eau E, Baudouin G, Bankhead-D onne S, Che alie Z, Zimme mann M, Dupon S,
Dedeine F, Bagnè es A (2019) In asion dynamics o a e mi e, Re iculi e mes la ipes, a di -
e en spacial scales in F ance. Insec s 10(1): e30. h ps://doi.o g/10.3390/insec s10010030
Poida z J, Monceau K, Bonna d O, Thié y D (2018) Ac i i y hy hm and ac ion ange o wo ke s
o he in asi e ho ne p eda o o honeybees Vespa elu ina, measu ed by adio equency iden-
i ica ion ags. Ecology and E olu ion 8(15): 7588–7598. h ps://doi.o g/10.1002/ece3.4182
Po po a o M, Manino A, Lau ino D, Demichelis S (2014) Vespa elu ina Lepele ie (Hymenop-
e a Vespidae): A i s assessmen wo yea s a e i s a i al in I aly. REDIA XCVII: 189–194.
Pyšek P, Richa dson D (2007) T ai s Associa ed wi h In asi eness in Alien Plan s: Whe e Do
we S and? In: Nen wig W (Ed.) Biological In asions. Sp inge -Ve lag, Be lin Heidelbe g,
97–125. h ps://doi.o g/10.1007/978-3-540-36920-2
Ma ia João Ve dasca e al. / NeoBio a 69: 177–198 (2021)
196
Rainho A, Palmei im JM (2011) The impo ance o dis ance o esou ces in he spa ial mod-
elling o ba o aging habi a . PLoS ONE 6: e19227. h ps://doi.o g/10.1371/jou nal.
pone.0019227
Ri as-Ma ínez S, Penas Á, del Río S, Díaz González T, Ri as-Saénz S (2017) Bioclima ology
o he Ibe ian Peninsula and he Balea ic Islands. In: Loidi J (Ed.) The Vege a ion o he
Ibe ian Peninsula. Plan and Vege a ion, ol. 12. Sp inge , Cham., 29–80. h ps://doi.
o g/10.1007/978-3-319-54784-8_2
Robine C, Suppo C, Da ouze E (2017) Rapid sp ead o he in asi e yellow-legged ho ne in
F ance: he ole o human-media ed dispe sal and he e ec s o con ol measu es. Jou nal
o Applied Ecology 54: 205–215. h ps://doi.o g/10.1111/1365-2664.12724
Robine C, Da ouze E, Suppo C (2019) Sp ead modelling: a sui able ool o explo e he ole
o human-media ed dispe sal in he ange expansion o he yellow-legged ho ne in Eu-
ope. In e na ional Jou nal o Pes Managemen 65: 258–267. h ps://doi.o g/10.1080/0
9670874.2018.1484529
Rod íguez-Flo es M, Seijo-Rod íguez A, Olga E, Seijo-Coello M (2019) Sp eading o Vespa
elu ina in no hwes e n Spain: in luence o ele a ion and me eo ological ac o s and e ec
o bai apping on a ge and non – a ge li ing o ganisms. Jou nal o Pes Science 92:
557–565. h ps://doi.o g/10.1007/s10340-018-1042-5
Roques A, Rabi sch W, Rasplus J, Lopez- aamonde C, Nen wig W, Kenis M (2009) Alien
Te es ial In e eb a es o Eu ope. In: Handbook o Alien Species in Eu ope. In ading
Na u e – Sp inge Se ies in In asion Ecology, ol. 3. Sp inge , Do d ech , 63–79. h ps://
doi.o g/10.1007/978-1-4020-8280-1_5
Say e R, Ka agulle D, F ye C, Bouche T, Wol NH, B eye S, W igh D, Ma in M, Bu le K,
Van G aa eiland K, Tou al J, So omayo L, McGowan J, Game ET, Possingham H (2020)
An assessmen o he ep esen a ion o ecosys ems in global p o ec ed a eas using new maps
o Wo ld Clima e Regions and Wo ld Ecosys ems. Global Ecology and Conse a ion 21:
e00860. h ps://doi.o g/10.1016/j.gecco.2019.e00860
Schneide SS, Deg andi-Ho man G, Smi h DR (2004) The a ican honeybee: Fac o s Con-
ibu ing o a success ul biological in asion. Annual Re iew o En omology 49: 351–376.
h ps://doi.o g/10.1146/annu e .en o.49.061802.123359
Shigesada N, Kawasaki K, Takeda Y (1995) Modeling S a i ied Di usion in Biological In a-
sions. The Ame ican Na u alis 146: 229–251. h ps://doi.o g/10.1086/285796
Sua ez A V, Holway DA, Case TJ (2001) Pa e ns o sp ead in biological in asions domina ed
by long-dis ance jump dispe sal: Insigh s om A gen ine an s. P oceedings o he Na ional
Academy o Sciences o he USA 98: 1095–1100. h ps://doi.o g/10.1073/pnas.98.3.1095
Team RC (2019) R: A language and en i onmen o s a is ical compu ing. R Founda ion o
S a is ical Compu ing, Vienna. h ps://www.R-p ojec .o g/
Ve dasca MJ, Godinho R, Rocha R, Po oca e o M, Ca alhei o L, Rebelo R, Rebelo H (2021)
A me aba coding ool o de ec p eda ion o he honeybee Apis mellie a and o he wild
insec s by he in asi e Vespa elu ina. Jou nal o Pes Science. h ps://doi.o g/10.1007/
s10340-021-01401-3
Vicen e J, Al es P, Randin C, Guisan A (2010) Wha d i es in asibili y? A mul i-model in e -
ence es and spa ial modelling o alien plan species ichness pa e ns in no he n Po ugal.
Ecog aphy 33: 1081–1092. h ps://doi.o g/10.1111/j.1600-0587.2010.6380.x
Mo o ways speed na u al in asion dynamics o Vespa elu ina 197
Villeman C, Ba be -Massin M, Pe a d A, Mulle F, Ga gominy O, Jigue F, Rome Q (2011)
P edic ing he in asion isk by he alien bee-hawking Yellow-legged ho ne Vespa elu ina
nig i ho ax ac oss Eu ope and o he con inen s wi h niche models. Biological Conse a ion
144: 2142–2150. h ps://doi.o g/10.1016/j.biocon.2011.04.009
Supplemen a y ma e ial 1
Suppo ing in o ma ion
Au ho s: Ma ia João Ve dasca, Hugo Rebelo, Luísa G. Ca alhei o, Rui Rebelo
Da a ype: ables and igu es (pd . ile)
Explana ion no e: Table S1. Clima e, land co e and an h opogenic a iables wi h
po en ial o a ec he beha iou and es ablishmen o Vespa elu ina. Tables S2.
Co ela ion ma ix o he clima ic, land co e and an h opogenic d i e s ha ha e
he po en ial o a ec he beha iou and es ablishmen o Vespa elu ina in Eu ope:
a) bound eco ds; b) ou pos s; c) ou pos s >18 km. Table S3. Rela ion be ween
dispe sion dis ance ( o sou h and eas ) s ime ei he o sel media ed o jump
dispe sal by es ing h ough - es he signi icance o he slope o he eg ession
when compa ed o ze o (H0: he slope o he eg ession line is 0). Table S4. E ec s
o clima ic, land co e and an h opogenic a iables on he dispe sal o V. elu ina.
Table S5. E ec s o he di e en land co e and an h opogenic p edic o s on he
dispe sion o V. elu ina, conside ing he p edic o dis ance o he en i e oad ne -
wo k, ins ead o dis ance o mo o ways in bound eco ds and bo h se s o ou pos s.
Table S6. Se o bes models wi h clima ic and land a iables acco ding o he di -
e en da ase s (1. bound eco ds; 2. all ou pos and 3. ou pos 18 km). Table7.
Se o bes models wi h clima ic a iables acco ding o he di e en da ase s (1.
bound eco ds; 2. all ou pos and 3. ou pos 18 km). Table S8. Se o bes models
wi h land a iables acco ding o he di e en da ase s (1. bound eco ds; 2. all
ou pos and 3. ou pos 18 km). Figu e S1. Va ia ion o he mean dis ance o he
new eco ds wi hin a gi en yea o he nea es po en ial sou ce: con inuous a ea o
ou pos . E o ba s depic s anda d e o s. Figu e S2. Rela ion be ween he dispe -
sion o Vespa elu ina and signi ican clima ic and land co e a iables acco ding
o he di e en da ase s: bound eco ds, all ou pos s and ou pos 18 km (see Table
3 o he main manusc ip ).
Copy igh no ice: This da ase is made a ailable unde he Open Da abase License
(h p://openda acommons.o g/licenses/odbl/1.0/). The Open Da abase License
(ODbL) is a license ag eemen in ended o allow use s o eely sha e, modi y, and
use his Da ase while main aining his same eedom o o he s, p o ided ha he
o iginal sou ce and au ho (s) a e c edi ed.
Link: h ps://doi.o g/10.3897/neobio a.69.71352.suppl1

Ma ia João Ve dasca e al. / NeoBio a 69: 177–198 (2021)
198
Supplemen a y ma e ial 2
Appendix A
Au ho s: Ma ia João Ve dasca, Hugo Rebelo, Luísa G. Ca alhei o, Rui Rebelo
Da a ype: occu ences (pd . ile)
Explana ion no e: Vespa elu ina occu ences – 5 km esolu ion.
Copy igh no ice: This da ase is made a ailable unde he Open Da abase License
(h p://openda acommons.o g/licenses/odbl/1.0/). The Open Da abase License
(ODbL) is a license ag eemen in ended o allow use s o eely sha e, modi y, and
use his Da ase while main aining his same eedom o o he s, p o ided ha he
o iginal sou ce and au ho (s) a e c edi ed.
Link: h ps://doi.o g/10.3897/neobio a.69.71352.suppl2