Ecological Indica o s 124 (2021) 107434
A ailable online 29 Janua y 2021
1470-160X/© 2021 The Au ho s. Published by Else ie L d. This is an open access a icle unde he CC BY license (h p://c ea i ecommons.o g/licenses/by/4.0/).
Sho No e
The ep esen a ion po en ial o ap o s o globally impo an na u e
conse a ion a eas
A. San angeli
a
,
b
,
c
,
d
,
*
, M. Gi a dello
e
a
Resea ch Cen e o Ecological Change, O ganismal and E olu iona y Biology Resea ch P og amme, Uni e si y o Helsinki, PO Box 65 (Viikinkaa i 1), 00014 Helsinki,
Finland
b
Helsinki Ins i u e o Li e Science, Uni e si y o Helsinki, FI-00014 Helsinki, Finland
c
The Helsinki Lab o O ni hology, Finnish Museum o Na u al His o y, Uni e si y o Helsinki, Finland
d
Fi zPa ick Ins i u e o A ican O ni hology, DST-NRF Cen e o Excellence, Uni e si y o Cape Town, Cape Town, Sou h A ica
e
cE3c - Cen e o Ecology, E olu ion and En i onmen al Changes/Azo ean Biodi e si y G oup and Uni e sidade dos Aço es – Dep o de Ciˆ
encias e Engenha ia do
Ambien e, PT-9700-042, Ang a do He oísmo, Aço es, Po ugal
ARTICLE INFO
Keywo ds:
Su ogacy
Umb ella species
Bi ds o p ey
Flagship species
Global p io i iza ion
Indica o species
ABSTRACT
S emming om a pe asi e lack o knowledge on biodi e si y, impo an a eas o conse a ion a e ypically
iden i ied using a subse o well known species, commonly e med su oga e o indica o g oups. Bi ds ha e been
commonly used as biodi e si y su oga es due o he good le el o knowledge on hei axonomy, ecology and
dis ibu ion. Rap o s in pa icula ha e been o en p oposed as an e ec i e su oga e o o he biodi e si y based
on hei die a y di e si y, being a he op o he ood chain, hei p e e ence o highly p oduc i e a eas, hei
gene ally h ea ened s a us and high public appeal. Howe e , so a he su ogacy e ec i eness o ap o s has
been la gely s udied locally o using a na ow selec ion o su oga e and su oga ed axa.
He e we use a spa ial conse a ion planning ool o quan i y he su ogacy pe o mance o ap o s, o e all and
by di e en ap o g oups (hawks and eagles, alcons, ul u es, owls) o ep esen impo an biodi e si y a eas
(such as IUCN p o ec ed a eas and key biodi e si y a eas), wilde ness a eas and he wo lds eco egions. We
compa ed he abo e su ogacy pe o mance wi h ha o all o he non- ap o a ian species.
We show ha ap o s pe o m ma ginally wo se han all o he a ian species in ep esen ing impo an
biodi e si y a eas and eco egions. Howe e , ap o s ep esen a ion o wilde ness a eas was simila o sligh ly
be e compa ed o ha o using all non- ap o bi ds. We also epo a la ge a ia ion in he ep esen a ion
pe o mance by he ou ap o g oups. Falcons had a pa icula ly high po en ial in ep esen ing p o ec ed a eas
and wilde ness a eas, equaling o la gely su passing he ep esen a ion po en ial p o ided by all ap o s and all
o he non- ap o bi ds.
O e all, he esul s sugges ha ap o s, and pa icula ly alcons, can pe o m ela i ely well in ep esen ing
some impo an a eas o conse a ion, such as p o ec ed a eas and wilde ness a eas, bu a e ela i ely poo
su oga es o key biodi e si y a eas and eco egions. These a he con as ing esul s call o cau ion on he use o
ap o s as global su oga es o wide biodi e si y.
1. In oduc ion
Knowledge abou biodi e si y and i s dis ibu ion, commonly
e e ed o as he Linnean and Wallacean sho alls, is e y limi ed
(Whi ake e al., 2005). Consequen ly, he iden i ica ion o p io i y
a eas o biodi e si y conse a ion o en elies on a na ow selec ion o
species ac ing as su oga es o wide biodi e si y ( he su ogacy
concep ; Ca o, 2010). Howe e , ypically his na ow selec ion o su -
oga e species (i.e. ypically well moni o ed species used o ep esen
o he species, he su oga ed species, in a aining a conse a ion
objec i e; Ca o, 2010) is assumed, implici ly o explici ly, o be an
e ec i e su oga e o biodi e si y (La sen e al., 2012). This assump ion
o en emains un es ed, lea ing us in an unce ain and po en ially
misleading si ua ion o alse belie ha p io i izing conse a ion
* Co esponding au ho a : Resea ch Cen e o Ecological Change, O ganismal and E olu iona y Biology Resea ch P og amme, Uni e si y o Helsinki, PO Box 65
(Viikinkaa i 1), 00014 Helsinki, Finland.
E-mail add ess: [email p o ec ed] (A. San angeli).
Con en s lis s a ailable a ScienceDi ec
Ecological Indica o s
jou nal homepage: www.else ie .com/loca e/ecolind
h ps://doi.o g/10.1016/j.ecolind.2021.107434
Recei ed 20 Oc obe 2020; Recei ed in e ised o m 10 Decembe 2020; Accep ed 17 Janua y 2021
Ecological Indica o s 124 (2021) 107434
2
owa ds a eas impo an o speci ic su oga e axa does ha e an impac
on a much wide ange o species.
Bi ds a e commonly used as su oga es o biodi e si y owing o he
la ge and ypically high quali y ele an in o ma ion on hei axonomy
and dis ibu ion, hei b oad appeal o he public and o en conspicuous
na u e (La sen e al., 2012). Among bi ds, ap o s ha e been pa icula ly
highligh ed as a po en ially e ec i e su oga e g oup o wide biodi-
e si y (Se gio e al., 2006, 2008). Rap o s, as mos la ge p eda o s, a e
gene ally globally h ea ened by inc easing human ac i i ies, wi h
popula ions o se e al species, like many ul u es, apidly declining
(McClu e e al., 2018). Being a he op o ecological ood chains, ap o s
may ac as sen inels o en i onmen al change, gi ing ea ly wa nings o
po en ial an h opogenic impac s on biodi e si y (Bu ield, 2008;
Don´
aza e al., 2016). Rap o s p e e ence o a di e si y o p ey ac oss
he ood chain, and o highly p oduc i e a eas, may acili a e hei ole
as umb ella o o he biodi e si y (Se gio e al., 2008; Bu gas e al.,
2014). Mo eo e , due o hei appeal and cha isma, ap o s a e widely
app ecia ed by he public and well s udied by scien is s (Buechley e al.,
2019), and can ac as lagship species, le e aging unds o help p ese e
biodi e si y as a whole (Don´
aza e al., 2016; McGowan e al., 2020).
While local s udies ha e a emp ed o quan i y he su ogacy e ec-
i eness o ap o s a he local scale and/o wi h a na ow selec ion o
su oga e and su oga ed species, a global analysis o he su ogacy
e ec i eness o ap o s is s ill lacking. Mos impo an ly, he s udies
conduc ed so a ha e exclusi ely ocused on ap o ep esen a ion o
o he species (Se gio e al., 2006, 2008; Bu gas e al., 2014), whe eas
none ha e add essed ap o ep esen a ion po en ial o impo an con-
se a ion a eas, ha is, hose a eas ha ha bo species and ecosys ems o
conse a ion conce n.
As he occu ence o ap o s is ypically associa ed wi h a eas o high
species ichness and in ac ecosys ems (Se gio e al., 2008), he e we aim
o quan i y how well ap o s can ep esen globally impo an e es ial
a eas o biodi e si y conse a ion as well as wild a eas. Using a global
conse a ion p io i iza ion app oach, we i s compa e he e ec i eness
o ap o s wi h ha o all o he non- ap o bi d species in ep esen ing
impo an a eas o biodi e si y conse a ion, such as p o ec ed a eas,
key biodi e si y a eas, wilde ness a eas, e es ial eco egions. Nex ,
wi hin he ap o guild, we also aim o compa e he ep esen a ion o
hose a eas by ou dis inc sub-g oups o ap o species di e ing in hei
ecology, li e-his o y and ex inc ion isk, namely hawks and eagles, al-
cons, owls and ul u es. This g ouping ollows he a ionale and
app oach o Buechley e al. (2019).
2. Ma e ial and me hods
2.1. S udy egion and su oga e g oups
The a ge egion o his s udy includes all e es ial a eas o he
wo ld.
As su oga e axa we conside ed wo main g oups o bi ds, all ap-
o s, o de s Accipi i o mes, Ca ha i o mes, Falconi o mes, S igi-
o mes (n =557 species) and all o he non- ap o bi ds (n =10353).
Wi hin ap o s, we also conside ed ou con as ing g oups wi h
dis inc i e ecology, li e-his o y, and conse a ion s a us: Hawks and
eagles, alcons, owls, ul u es (n =234, 64, 236, 23). The selec ion o
ap o s and hei sub-g oups s ic ly ollows ha used by wo ecen
s udies (McClu e e al., 2018; Buechley e al., 2019). Mo eo e , he se-
lec ion o all species as de ailed abo e was condi ional on he a ail-
abili y o hei digi ized ange maps as p o ided by Bi dLi e
In e na ional and Na u eSe e (2015) and was es ic ed o species
whose ange o e laps, a leas pa ly, e es ial a eas. Fo all su oga e
axa, we only used he b eeding and esiden ange o each species. This
seasonal es ic ion aims o a oid noise s emming om he species being
only pa ly p esen in an a ea, and also because mos o he conse a ion
planning s udies ocus on he b eeding and esiden ange o he species
(e.g. Mon esino Pouzols e al., 2014; San angeli e al., 2019a, 2019b,
2020). The ange o each species was as e ized o a esolu ion o 50 km
×50 km. This esolu ion was deemed coa se enough o minimize he
impac o bo h commission and omission e o s associa ed o he species
anges. Changes in he esolu ion we e howe e ound o ha e only a
ma ginal impac on he esul s o such ypes o analyses (Mon esino
Pouzols e al., 2014).
2.2. Su oga ed g oups
As su oga ed g oups, we ocused on a eas widely ecognized as
p io i y o global biodi e si y conse a ion, wilde ness a eas and he
di e si y o he wo ld’s eco egions. The p o ec ed a eas (he ea e PA) o
he global e es ial ealm a e es ablished unde he In e na ional
Union o Conse a ion o Na u e (IUCN) wi h he aim o e ec i ely
conse e he composi ion, s uc u e, unc ion and e olu iona y po en ial
o biodi e si y (Dudley, 2008). These a eas a e widely ecognized as
s ongholds o biodi e si y conse a ion (Wa son e al., 2014). Fo he
pu pose o his s udy, we conside ed all PAs (i.e. all IUCN PA ca ego ies
oge he ), as well as he s ic ly PAs (IUCN ca ego ies I o IV) only as a
sepa a e laye . While s ic ly PAs a e included wi hin all PAs, he
a ionale o conside ing also he s ic ly p o ec ed a eas is because in
hese si es de elopmen is no allowed and access o en es ic ed,
he eby hey may ep esen e en mo e impo an s ongholds o
biodi e si y conse a ion unde s ong human p essu es (Rehbein e al.,
2020).
Simila ly, wi hin bu also ou side o he cu en PA ne wo k, Key
Biodi e si y A eas (KBA) a e iden i ied as essen ial si es o a e species
ex inc ions, being o en e ugia o a e and endange ed biodi e si y
(Newbold e al., 2015). Wilde ness a eas a e iden i ied as he las
emaining in ac ecosys ems globally, which unc ion na u ally and
suppo a disp opo iona e ange o ecosys em se ices and biodi e si y
(Wa son and Ven e , 2017). Mo eo e , ep esen a i e examples o he
wo lds ecosys ems ha e been mapped h ough he iden i ica ion o he
global eco egions which ha bo excep ional biodi e si y (Olson e al.,
2001). In his s udy, we hus collec ed spa ial da a on he wo ld’s PAs
( om www.p o ec edplane .ne ), KBAs (Bi dLi e In e na ional, 2019),
wilde ness a eas (Las o he Wild Da a Ve sion 2 2005) and he wo lds
e es ial eco egions (Olson e al., 2001). As o he su oga e g oups,
also hese su oga ed laye s we e as e ized o he same esolu ion o 50
km ×50 km. While some o hese su oga ed laye s ine i ably would
o e lap in space, such as KBAs and PAs, hey a e spa ially sepa a ed
enough, and a e selec ed based on di e en c i e ia wi h di e en in-
e p e a ions ha hey would allow meaning ul compa isons.
2.3. Su ogacy analyses
In o de o assess he e ec i eness o ap o s as su oga es o p io i y
a eas o biodi e si y and ecosys em conse a ion, we used he spa ial
conse a ion planning so wa e Zona ion .4 (Moilanen e al., 2014).
Zona ion p oduces balanced anking o conse a ion p io i ies o e a
s udy landscape by i e a i ely emo ing he landscape uni o leas
conse a ion alue while accoun ing o he emaining dis ibu ions o
ea u es (Moilanen e al., 2005). The emo al ule o landscape uni s
chosen he e was he addi i e bene i unc ion, as his has been ecom-
mended as he mos obus unc ion when unning su ogacy analyses
(Di Minin and Moilanen, 2014; Moilanen e al., 2014). Essen ially, by
assigning a weigh >0 o he su oga e ea u es, and a weigh o ze o o
he su oga ed ea u es, he algo i hm iden i ies he key p io i y a eas
o he su oga e ea u es and simul aneously calcula es he dis ibu ion
co e age emaining o each su oga ed ea u e a each s ep o he
i e a ion. In ou case, ac oss all he zona ion uns (see de ails below), we
assigned an equal weigh o one o all su oga e ea u es, and a weigh o
ze o o all su oga ed ea u es. We se up six di e en zona ion uns, in
each he su oga e g oup consis ed in u n in ap o s only, all o he non-
ap o bi d species, as well as ou ap o sub-g oups: Hawks and eagles,
alcons, owls, ul u es. The se o su oga ed ea u es was ins ead he
A. San angeli and M. Gi a dello
Ecological Indica o s 124 (2021) 107434
3
same ac oss he six uns and consis ed on one laye o he KBAs, one o
he wilde ness a eas, one o all PAs (including all six ca ego ies o PAs
as de ined by IUCN) and one o he s ic ly PAs (IUCN ca ego ies I o
IV), and one laye o each o he 816 e es ial eco egions. The zona-
ion ou come consis s o maps o he p io i y anking as well as pe o -
mance cu es ha de ine he co e age o each o he su oga ed ea u es
o each p opo ion o he landscape i ually p o ec ed acco ding o he
p io i y anking ob ained om he su oga e ea u es. Tha is, how much
each su oga ed ea u e is co e ed when p io i y a eas o he su oga e
ea u es a e p o ec ed a a de ined le el, e.g. om p o ec ing only he
op 5% iden i ied p io i ies o su oga es o much mo e. Thus, in o de
o expose he di e ences in he su ogacy po en ial o he six di e en
su oga e g oups, we show he pe o mance cu es o hese in ela ion o
each o he su oga ed ea u es. We also closely highligh di e ences in
su ogacy po en ial when he op anked 5, 17 and 30% o he landscape
is p o ec ed based on p io i ies sough by conside ing in u n each o he
six su oga e g oups.
3. Resul s
The ep esen a ion o PAs (o e all as well as only he s ic PAs) and
KBAs was gene ally simila , o sligh ly lowe (co e age loss by abou 1
o 3%) when p io i ies a e iden i ied using ap o s as compa ed o all
o he non- ap o bi ds (Figs. 1 and 2). Con e sely, ap o s in gene al
pe o med simila ly o sligh ly be e (by 1% inc ease in co e age) han
all o he non- ap o bi ds in ep esen ing wilde ness a eas, bu la gely
wo se (co e age loss by up o 9%) in ep esen ing eco egions (Figs. 1
and 2). Measu able di e ences in su ogacy pe o mance be ween he
ou g oups o ap o s a e e iden , wi h alcons ou pe o ming all o he
ap o and also non- ap o g oups in ep esen ing PAs and especially
wilde ness a eas.
4. Discussion
We show ha he co e age o impo an biodi e si y (i.e. PAs and
KBAs) a eas is ma ginally lowe (loss in co e age o abou 1 o 3%) when
p io i ies a e iden i ied using all ap o s as compa ed o using all o he
a ian non- ap o species. O e all, his loss in ep esen a ion a ied ac-
co ding o he su oga ed g oup, being highes , when conside ing
s ic ly PAs and especially eco egions (up o 9% ep esen a ion loss
when using ap o s). Con e sely, ap o p io i ies allow a simila o
sligh ly highe co e age o wilde ness a eas compa ed o p io i ies
iden i ied using all o he non- ap o bi d species. In e es ingly, he
su ogacy po en ial e ec i eness a ied g ea ly among he di e en
ap o g oups. Falcons had a pa icula ly high po en ial in ep esen ing
PAs and wilde ness a eas, equaling o la gely su passing he ep esen-
a ion po en ial p o ided by all ap o s and all o he bi ds.
The inding ha conse a ion p io i y a eas iden i ied based on all
ap o s aid he co e age o impo an biodi e si y a eas a almos he
same e iciency as when using all o he non- ap o bi d species can ha e
p ac ical implica ions. This sugges s ha i may be possible o use he
limi ed numbe (n =557) o ap o species, which a e well known and
o en wi h dedica ed moni o ing and esea ch p og ams (Bu ield,
2008), o iden i y impo an biodi e si y a eas globally ins ead o using
all o he o e 10 000 a ian species. In a local s udy, Se gio e al., (2006)
ound ha a ne wo k o p o ec ed a eas was mos e icien in achie ing
biodi e si y co e age when based on ap o s as compa ed o species a
lowe ophic le els. Tha s udy was based on six su oga e species, o
Fig. 1. Zona ion pe o mance cu es ep esen ing he inc ease in co e age o each biodi e si y a ea (Y-axis in each o he 5 panels) as he hypo he ical p opo ion o
landscape p o ec ed inc eases (X-axis). Each panel shows he pe o mance in co e ing each o he i e biodi e si y a eas (IUCN PAs, IUCN s ic ly p o ec ed a eas
ca ego ies I o IV, key biodi e si y a eas, wilde ness a eas and he wo lds eco egions) by each o he six su oga e g oups conside ed: Non- ap o bi d species, all
ap o s combined, hawks and eagles, ul u es, alcons and owls.
A. San angeli and M. Gi a dello
Ecological Indica o s 124 (2021) 107434
4
which one is a hawk (Accipi e gen ilis) and he o he s a e owls. Ano he
simila s udy ound he same hawk species o pe o m well in indica ing
a eas o high biodi e si y, also ou pe o ming an owl species (S ix
U alensis; Bu gas e al., 2014). Ou esul s, while bea ing in mind he
di e ences in he app oach, seem o pa ly align o hose om ea lie
s udies, pa icula ly wi h ega ds o he su ogacy pe o mance o hawks
and eagles, and alcons. We show ha alcons in pa icula ou pe o m
all o he ap o s and non ap o bi ds in ep esen ing PAs o e all, and
also he s ic ly PAs when he op 5% p io i ies a e conside ed. Global
alcon ichness and conse a ion p io i y a eas a e s ongly biased o-
wa ds highly p oduc i e egions in he opics (Buechley e al., 2019).
These a eas, being o en unde se e e p essu es om an h opogenic
ac i i ies, also include a la ge numbe o PAs, which may explain hei
inc eased co e age when p io i ies a e se based on alcons as compa ed
o o he g oups.
Falcons in pa icula , bu also o he g oups o diu nal ap o s,
including hawks and eagles, and ul u es, we e ound o ou pe o m all
o he non- ap o bi ds and owls in ep esen ing wilde ness a eas. This
esul may likely s em om he long-his o y o pe secu ion, pa icula ly
on diu nal ap o s (Thiollay, 2006; Ama e al., 2012; Pohja-Myk a e al.,
2012), ha may ha e shaped hei p e e ence owa ds he mos p is ine,
emo e and wild places le on Ea h. A he same ime, in ac ecosys ems
may also o e wide nes ing and o aging esou ces, wi h an o e all
la ge ca ying capaci y o hese en i onmen s compa ed o mo e
deg aded ones (Wa son e al., 2018), he eby suppo ing la ge pop-
ula ions o diu nal ap o s compa ed o o he g oups.
Rap o s in gene al pe o med wo se han all o he non- ap o species
in ep esen ing he wo ld’s eco egions. This inding may s em om he
ac ha eco egions a e homogeneously sca e ed ac oss he globe,
he e o e a la ge se o su oga e species wi h di e en li e-his o ies,
ecology and biogeog aphy, such as he non- ap o ca ego y in his
s udy, makes i mo e likely o ep esen wide egions globally as
compa ed o a na ow selec ion o su oga e species (La sen e al.,
2012), such as ap o s. This asse ion is also suppo ed by ou inding
showing ha owls pe o m bes among all ap o g oups in ep esen ing
eco egions. Owls ichness is among he mos widely dis ibu ed globally
o all he ou ap o g oups (Buechley e al., 2019), which may allow
his g oup o co e mos o he eco egions.
This is he i s a emp o quan i y he su ogacy po en ial o ap o s
a a global scale. Simila analyses ha e been conduc ed a he global
le el using he wo ld’s ca ni o es (Di Minin e al., 2016). The esul s
om such global analyses should hus be in e p e ed wi h cau ion, as
hey can highligh b oad pa e ns ha need o be con i med locally o
egionally using highe - esolu ion da a. Fo example, he e we used a
a he coa se esolu ion o 50 km ×50 km. While his esolu ion may
educe omission e o s (when he species is mis akenly hough o be
absen ) in he dis ibu ion da a, i may s ill su e om commission e -
o s (when he species is mis akenly hough o be p esen ). Beyond he
local s udies which a e al eady a ailable (Se gio e al., 2006, 2008;
Bu gas e al., 2014; Di Minin and Moilanen, 2014), i will be hus
impo an o pe o m su ogacy analyses o he ype p esen ed he e a
he na ional o egional le el and by conside ing a b oade axonomic
di e si y, including non-a ian species. This can be possible by ha -
nessing he unp eceden ed in o ma ion on species ecology, li e-his o y
and biogeog aphy ha is now made a ailable hanks o ci izen science
p og ams and open da a pla o ms such as e-bi d and Global Biodi e si y
In o ma ion Facili y (Fink e al., 2020; GBIF.o g, 2020).
Fig. 2. Rep esen a ion o he i e biodi e si y a eas (IUCN PAs, IUCN s ic ly p o ec ed a ea ca ego ies I o IV, key biodi e si y a eas, wilde ness a eas and he wo lds
eco egions) by each o he six su oga e g oups conside ed (non- ap o bi d species, all ap o s combined, hawks and eagles, ul u es, alcons and owls) when 5, 17
and 30% o a hypo he ical landscape would be p o ec ed. Please no e he change in scale o he y-axis be ween he panels.
A. San angeli and M. Gi a dello
Ecological Indica o s 124 (2021) 107434
5
5. Conclusions
Unde a pe asi e sho age o knowledge on species ecology and
dis ibu ion, and a lack o esou ces o moni o ing and conse a ion,
good su oga es o biodi e si y can help o p io i ise a eas o conse -
a ion and p e en ing species ex inc ion. Rap o s, and pa icula ly al-
cons, pe o m ela i ely well in ep esen ing PAs and especially
wilde ness a eas, bu a e ela i ely poo su oga es o KBAs and eco -
egions. As such, we cau ion on he use o ap o s as global su oga es o
wide biodi e si y, as hei ep esen a ion pe o mance clea ly a ies
based on he g oup o ap o s and he ype o conse a ion a ea
conside ed.
CRediT au ho ship con ibu ion s a emen
A. San angeli: Concep ualiza ion, Me hodology, In es iga ion,
Visualiza ion, W i ing - o iginal d a , W i ing - e iew & edi ing. M.
Gi a dello: Concep ualiza ion, Me hodology, W i ing - e iew &
edi ing.
Decla a ion o Compe ing In e es
The au ho s decla e ha hey ha e no known compe ing inancial
in e es s o pe sonal ela ionships ha could ha e appea ed o in luence
he wo k epo ed in his pape .
Acknowledgemen s
AS was suppo ed by he Academy o Finland (g an n. 307909), he
Jane ja Aa os E kon S¨
a¨
a i¨
o, Finnish Minis y o he En i onmen . We
also hank M. Romano and an anonymous e iewe o hei aluable
commen s ha helped imp o e his wo k.
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A. San angeli and M. Gi a dello