A icle
Niche Cha ac e iza ion o Sh ub Func ional G oups along an
A lan ic-Medi e anean G adien
Ad iana E. Ol ho 1, Ca olina Ma ínez-Ruiz 1,2,* and Josu G. Alday 3,4,*


Ci a ion: Ol ho , A.E.;
Ma ínez-Ruiz, C.; Alday, J.G. Niche
Cha ac e iza ion o Sh ub Func ional
G oups along an
A lan ic-Medi e anean G adien .
Fo es s 2021,12, 982. h ps://
doi.o g/10.3390/ 12080982
Academic Edi o :
Panayo is Dimopoulos
Recei ed: 16 May 2021
Accep ed: 22 July 2021
Published: 24 July 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/).
1Á ea de Ecología, Depa amen o Ciencias Ag o o es ales, E.T.S. de Ingenie ías Ag a ias,
Uni e sidad de Valladolid, A da. de Mad id 50, 34071 Palencia, Spain; aol ho [email p o ec ed]
2Sus ainable Fo es Managemen Resea ch Ins i u e, Uni e si y o Valladolid-INIA, E.T.S.II.AA.,
A da. Mad id 50, 34071 Palencia, Spain
3Join Resea ch Uni CTFC–AGROTECNIO–CERCA, 25198 Lleida, Spain
4Depa men o C op and Fo es Sciences, Uni e si a de Lleida, A da Alcalde Ro i a Rou e 191,
25198 Lleida, Spain
*Co espondence: [email p o ec ed] (C.M.-R.); [email p o ec ed] (J.G.A.)
Abs ac :
The iden i ica ion o he ac o s con olling he unde s o y species dis ibu ion and abun-
dance is essen ial o unde s and he ecology and dynamics o na u al o es s and hei managemen
esponse. We assess he ela ionships be ween en i onmen al g adien s and sh ub unc ional g oups
dis ibu ion pa e ns and niche cha ac e is ics in a ansi ional a ea be ween he Eu osibe ian and
Medi e anean biogeog aphic egions in No he n Spain. He e, 772 plo s om he 3 d Spanish
Na ional Fo es In en o y we e used. Sh ub unc ional g oups espond o he same complex en i-
onmen al g adien s as ees, i.e., he no h-sou h clima ic g adien and a slope g adien . Unimodal
esponse cu es o sh ub unc ional g oups and amilies domina e along bo h g adien s, p o iding
e idence o success ul unc ional u no e . Simila o ee species, he niche loca ion o unc ionally
ela ed sh ubs is close. Func ional g oups occupying en i onmen s wi h sha p con as o ansi ional
en i onmen s ha e he b oades niches, whe eas hose specialized unc ional g oups occupying local-
ized habi a s showed he na owes niches. The knowledge o sh ub species dis ibu ions and niche
cha ac e is ics along complex en i onmen al g adien s will imp o e ou abili y o discuss po en ial
conse a ion managemen goals o h ea s due o land-use changes and u u e clima e change.
Keywo ds:
coenoclines; o es in en o y da a; Huisman-Ol -F esco (HOF) modeling; niche wid h;
No he n Spain; sh ub unc ional g oup dis ibu ion
1. In oduc ion
Sh ub species li ing in he o es unde s o y a e impo an elemen s o ecosys em
s uc u e and unc ion, p o iding habi a and o age o wildli e [
1
–
4
] and con ibu ing
signi ican ly o plan di e si y [
5
–
7
]. Being pa icula ly impo an in a eas whe e sh ub
unde s o y is signi ican ly mo e di e se han o es o e s o y, such as he Palencia p o ince
(No he n Spain) [
8
,
9
]. I is widely ecognized ha sh ubs acili a e he g ow h o p o ec ed
species unde hei canopy [
10
], besides he ec ui men o ee seedlings mos ly om Que -
cus L. (oaks) [
11
–
14
] and Pinus L. (pines) species [
15
–
17
] in Medi e anean en i onmen s.
These acili a i e e ec s a e undamen al o egene a e o es ecosys ems in Medi e anean
egions [
18
,
19
]. Addi ionally, sh ubs play a undamen al ole as ecosys em enginee s
o inc ease he e ogenei y in mic o-en i onmen al condi ions a o ing la e-successional
species es ablishmen [
12
,
20
–
22
]. Con e sely, i has been shown ha ce ain sh ubs a o
exo ic species in asion (e.g., in he No he n Cali o nian coas al dunes E icame ia e icoides
(Less.) Jeps. enhances he coloniza ion o he in asi e B omus diand us Ro h [
19
]), and
e en some sh ub species become in asi e in he lack o app op ia e managemen p ac ices
(e.g., Cy isus scopa ius (L.) Link in F ance and Aus alia [
23
,
24
]). Thus, he desc ip ion
o en i onmen al ac o s shaping he dis ibu ion and abundance o unde s o y sh ub
Fo es s 2021,12, 982. h ps://doi.o g/10.3390/ 12080982 h ps://www.mdpi.com/jou nal/ o es s
Fo es s 2021,12, 982 2 o 16
species has undamen al implica ions o o es di e si y conse a ion [
25
,
26
] and o es
managemen [27,28], pa icula ly in he cu en scena io o clima e change [29–31].
Despi e he ac ha sh ubs a e key componen s o o es ecosys ems [
32
,
33
], he e
ha e been ew e o s o model sh ubs abundance o dis ibu ion [
5
,
34
], and e y ew
models o simula ion o o es dynamics inco po a e he esponse o unde s o y ege a-
ion laye s [
26
]. Mos likely, he unde s o y esponses a e mo e complex han o e s o y
esponses. Fo ins ance, mic oclima ic ex emes a e amelio a ed by mode a e o e s o y
co e , which would o he wise be s ess ul o g ound-laye plan s, in con as , high o e -
s o y co e supp esses unde s o y species i espec i e o en i onmen al cons ain s [
5
].
Thus, i migh be assumed ha unde s o y ege a ion has a unimodal esponse o o es
bio ic a iables, such as o e s o y co e [
5
], along wi h en i onmen al g adien s [
35
,
36
].
Ne e heless, as epo ed o opical o es s [
37
,
38
], unde s o y sh ub species migh no
espond o he same complex en i onmen al g adien s as ee species. A he same ime,
sh ub communi y esponses a e o en highly complex [
39
]. The e o e, o educe complexi y,
sh ub species a e usually g ouped acco ding o he ai s hey sha ed in o di e en unc-
ional g oups o plan unc ional ypes [
40
], such as Raunkiæ ’s li e- o ms (chame ophy e,
phane ophy e), dispe sal mode (anemocho y, zoocho y
. . .
) o egene a ion me hod (ge -
mina o , esp ou e ). In any case, a deepe unde s anding o sh ub unc ional esponses o
complex en i onmen al g adien s is needed.
In his sense, we assessed he ela ionships be ween sh ub unc ional g oup dis ibu-
ion pa e ns and niche cha ac e is ics and wo main en i onmen al g adien s (coenoclines)
p e iously iden i ied [
41
] in a ansi ional a ea be ween he Eu osibe ian and Medi e -
anean biogeog aphic egions in No he n Spain. We cha ac e ized he ealized niche o
sh ub unc ional g oups along bo h coenoclines, conside ing ha he species ealized niche
is concei ed as a mul idimensional esponse su ace and is composed by he undamen al
equi emen s o he species and i s unc ion, i.e., in e ac ions wi h o he species h ough
compe i i e exclusion and acili a ion [
42
]. He e, conside ing ha unc ional g oups a e
impo an componen s o ecosys em unc ion [
43
], we used a sh ub- unc ional-g oups
app oach. Ou speci ic objec i es we e: (1) o assess whe he unde s o y sh ub unc ional
g oups esponded o he same egional complex en i onmen al g adien s as ee species
(i.e., al i ude and empe a u e, and s eepness); (2) o de e mine whe he sh ub unc ional
g oups exhibi ed a unimodal esponse o hose en i onmen al g adien s; (3) o quan i y
he op ima and niche wid hs o sh ub unc ional g oups ac oss he main g adien s. The
desc ip ion o sh ub unc ional g oups dis ibu ion and niche ea u es along complex en i-
onmen al g adien s will help o imp o e ou knowledge o discuss po en ial conse a ion
managemen h ea s and goals because o land uses and clima e changes [15].
2. Ma e ials and Me hods
2.1. S udy A ea and Da a Sou ce
The en i onmen al g adien unde s udy uns om he no h o he sou h o he
Palencia p o ince (No he n Spain; 43
◦
04
0
N and 41
◦
46
0
N la i ude, and 3
◦
53
0
W and
5
◦
02
0
W longi ude; Figu e 1A). The g adien is 140 km in leng h and comp ises a high
a ie y o en i onmen al condi ions and landscapes [
9
,
44
], as a esul o he con luence o
he A lan ic and Medi e anean biogeog aphic egions and wo geomo phological uni s ( he
Can ab ian Range and he Cas ilian pla eau), which ha bo g ea ege a ion di e si y [
8
].
The clima e changes om Alpine o he Medi e anean om no h o sou h [
45
], which is
ela ed o opog aphy (Figu e 1B), mainly de e mined by he p esence o he Can ab ian
Range in he no h (al i ude up o 2540 m), and he Cas ilian pla eau (mean al i ude
ca. 800 m) in he Cen e and sou he n pa s o he g adien . The empe a u e inc eases
ma kedly om no h o sou h ollowed by a no o ious inc ease in p ecipi a ion (highe
xe ici y) ha leads o a ise in he con inen al na u e o he clima ic condi ions [
46
]. Thus,
he clima ic and en i onmen al g adien h oughou he Palencia p o ince is o pa icula
in e es when desc ibing and cha ac e izing he o es ege a ion composi ional changes
om spa ial pe spec i es along b oad he e ogeneous en i onmen al g adien s.
Fo es s 2021,12, 982 3 o 16
Fo es s 2021, 12, x FOR PEER REVIEW 3 o 16
800 m) in he Cen e and sou he n pa s o he g adien . The empe a u e inc eases ma k-
edly om no h o sou h ollowed by a no o ious inc ease in p ecipi a ion (highe xe ici y)
ha leads o a ise in he con inen al na u e o he clima ic condi ions [46]. Thus, he cli-
ma ic and en i onmen al g adien h oughou he Palencia p o ince is o pa icula in e -
es when desc ibing and cha ac e izing he o es ege a ion composi ional changes om
spa ial pe spec i es along b oad he e ogeneous en i onmen al g adien s.
Figu e 1. (A) Loca ion o 772 ield plo s om 3SNFI conside ed o s udy in he Palencia p o ince (Spain). Plo s a e ep e-
sen ed o e he Digi al Ele a ion Model (DEM 200 m) using QGIS 3.16.6. (B) Topog aphic g adien o he Palencia p o ince
om he no h (moun ains) o he sou h (limes one moo s), ob ained om DEM 25 m. Bo h DEM om MDT2000 © Ins i-
u o Geog á ico Nacional de España).
Sh ub species da a om 772 pe manen ield plo s (Figu e 1A) om he 3 d Spanish
Na ional Fo es In en o y (3SNFI; 1997–2007) we e used. The SNFI measu e ci cula plo s
o a iable adius (5, 10, 15, and 25 m) sys ema ically dis ibu ed and loca ed on he in e -
sec ion nodes o a 1 × 1 km
2
Uni e sal T ans e se Me ca o g id; only plo s loca ed inside
o es a eas a e measu ed (see [41,46] o u he de ails on plo s selec ion, cha ac e is ics,
and dis ibu ion). T ees wi h a diame e a b eas heigh o 75, 125, 225, and 425 mm a e
measu ed, espec i ely, in each one o he concen ic ci cum e ences. The co e (%) o all
Figu e 1.
(
A
) Loca ion o 772 ield plo s om 3SNFI conside ed o s udy in he Palencia p o ince (Spain). Plo s a e
ep esen ed o e he Digi al Ele a ion Model (DEM 200 m) using QGIS 3.16.6. (
B
) Topog aphic g adien o he Palencia
p o ince om he no h (moun ains) o he sou h (limes one moo s), ob ained om DEM 25 m. Bo h DEM om MDT2000
©
Ins i u o Geog á ico Nacional de España).
Sh ub species da a om 772 pe manen ield plo s (Figu e 1A) om he 3 d Spanish
Na ional Fo es In en o y (3SNFI; 1997–2007) we e used. The SNFI measu e ci cula plo s
o a iable adius (5, 10, 15, and 25 m) sys ema ically dis ibu ed and loca ed on he in e -
sec ion nodes o a 1
×
1 km
2
Uni e sal T ans e se Me ca o g id; only plo s loca ed inside
o es a eas a e measu ed (see [
41
,
46
] o u he de ails on plo s selec ion, cha ac e is ics,
and dis ibu ion). T ees wi h a diame e a b eas heigh o 75, 125, 225, and 425 mm a e
measu ed, espec i ely, in each one o he concen ic ci cum e ences. The co e (%) o all
sh ub species p esen in a ixed plo adius o 10 m [
46
] was in en o ied. A o al o 86 sh ub
species we e egis e ed in he 772 selec ed plo s. Howe e , only 47 o hem we e used
in subsequen analyses o ha ing su icien co e and equency in he plo s, a co ec
axonomical iden i ica ion in he ield [
41
], and a ailable in o ma ion o hei unc ional
ai s in da abases o Sou he n Eu opean Flo a. These 47 sh ub species we e classi ied
in habi a - ela ed unc ional g oups (see Table A1) such as amily, geog aphical dis ibu-
Fo es s 2021,12, 982 4 o 16
ion (A lan ic, Medi e anean, A lan ic-Medi e anean, endemic o he Ibe ian Peninsula),
bio ype (pe ennial, deciduous), Raunkiæ
´
s li e- o m (chame ophy es, phane ophy es),
dispe sal mode (anemocho y, zoocho y, au hoco y, ba oco y, o he ), and egene a ion
me hod (ge mina o , esp ou e ).
2.2. Coenoclines Cha ac e iza ion
In p e ious s udies, an indi ec o dina ion echnique (de ended co espondence
analysis, DCA) was applied on he co e (%) ma ix o all woody species ( ees and
sh ubs) p esen in each o he 772 selec ed plo s [
41
,
46
]. DCA showed ha changes in
he o es ege a ion composi ional changes along he Palencia p o ince we e mainly
de e mined by he no h-sou h clima ic di e ences (DCA1, p ima y coenocline), al hough a
seconda y coenocline also showed a u no e o species ela ed o he slope g adien (DCA2,
s eepness). In pa icula , Fagus syl a ica L. and Que cus pe aea (Ma .) Liebl. domina ed
deciduous moun ain o es s ha a e eplaced by Que cus py enaica Willd. o es s and hose,
in u n, by Que cus aginea Lam. and Que cus ilex subsp. ballo a (Des .) Samp. Fo es s, as
a idi y inc eases owa ds he sou h. Pinus syl es is L. and Pinus nig a J.F. A nold domina ed
coni e ous woodlands in moun ain a eas and de i al moo s (middle pa o he p o ince;
Figu e 1B), whe eas he sou he n limes one moo s (Figu e 1B) a e domina ed by plan a ions
o Pinus halepensis Mill., Pinus pinea L. and Cup esus sempe i ens L. In e es ingly, along
he slope g adien he e is also a u no e o ee species, pa ing na u al Junipe us spp.,
Que cus pe aea,Que cus py enaica, and Fagus syl a ica o es s loca ed on s eeply sloping
si es, and pine plan a ions (Pinus nig a,Pinus pinas e Ai on) ha domina e in la a eas.
The e o e, he sea ch o pa e ns ha ela e ee species ends wi h unde s o y sh ub
unc ional g oup ends along hese wo main coenoclines will gi e us aluable in o ma ion
o managemen and conse a ion.
2.3. Da a Analyses
Fi s , he main wo coenoclines we e p e iously iden i ied (DCA1, DCA2) [
41
,
46
].
The e o e, he e we modeled he abundance (co e pe cen age) o sh ub unc ional g oups
along hese coenoclines using HOF models (HOF = Huisman-Ol -F esco [
47
]) h ough he
‘eHOF’ package ( e sion 1.7 [
48
]) in he R-language en i onmen ( e sion 4.0.3; R De elop-
men Co e Team, Vienna, Aus ia, h p://www. -p ojec .o g, accessed on 1 Feb ua y 2020).
HOF models allow desc ibing he species esponses, which may esul om bo h en i on-
men al condi ions and in a- and in e speci ic in e ac ions [
49
]. HOFs a e a hie a chical
se o esponse models, anked by hei inc easing complexi y (Model I, no species end;
Model II, inc easing o dec easing end; Model III, inc easing o dec easing end below
maximum a ainable esponse; Model IV, symme ical esponse cu e; Model V, skewed
esponse cu e). The selec ion o he mos app op ia e model o each o he unc ional
g oups analyzed was done using he Akaike In o ma ion C i e ium (AIC) [
50
]; smalle
AIC alues indica e mo e pa simonious models. Finally, o hose unc ional g oups wi h
unimodal esponses, he loca ion o niche op ima (
µ
) and niche wid hs (2 ) we e de i ed
om he HOF models [49].
3. Resul s
The mos equen unde s o y sh ub species we e E icaceae:Calluna ulga is (L.) Hull
(in 13.6% o plo s), E ica spp. (12.8%) and E ica aus alis L. (10.1%). O he sh ub species such
as Rosa spp., Cy isus scopa ius (L.) Link, Thymus spp., A c os aphylos u a-u si (L.) Sp eng.,
E ica cine ea L.,and E ica a bo ea L. we e p esen in ca. 3–7% o plo s. Fabaceae,Rosaceae,
and E icaceae accoun ed o 49% o sh ub gene a and 44% o sh ub species.
3.1. Dis ibu ion Pa e ns o Main Sh ub Families along Coenoclines
Fabaceae and Cap i oliaceae we e he unique amilies wi h inde e mina e esponse
cu es (HOF model I) since bo h had low and cons an co e (<1%) along inc easing a idi y
DCA1 coenocline. Thymelaeaceae and Oleaceae (HOF model II wi h a dec easing end) had
Fo es s 2021,12, 982 5 o 16
he g ea es co e in he no he n moun ains wi h a subsequen educ ion owa ds he
sou h (DCA1 le -end; Figu e 2A). Only As e aceae (HOF model II wi h an inc easing end)
showed an inc easing end as a idi y inc eases owa ds he sou h (DCA1 igh -end). The
emainde axonomic g oups showed unimodal esponse cu es (HOF models IV o V;
Figu e 2A and Table 1) wi h op ima a di e en poin s along he g adien , o example,
Aqui oliaceae and Be ulaceae wi h op ima in he no he n moun ains (
DCA1 < 2
) had he
na owes niche wid h (
2 = 0.5
), E icaceae had in e media e niche wid h (
2 = 2.3
) wi h
i s op imum in he ansi ional a ea be ween he A lan ic and Medi e anean condi ions
(
DCA1 ≈2
), Rosaceae and Cis aceae had he b oades niche wid hs (2 = 6.1 and 4.1, espec-
i ely) wi h op ima in he g adien middle (DCA1
≈
4), and Labia ae had in e media e
niche wid h (2 = 2.6) wi h i s op imum a he igh end o DCA1, i.e., owa ds he sou h.
Fo es s 2021, 12, x FOR PEER REVIEW 5 o 16
Sp eng., E ica cine ea L., and E ica a bo ea L. we e p esen in ca. 3–7% o plo s. Fabaceae,
Rosaceae, and E icaceae accoun ed o 49% o sh ub gene a and 44% o sh ub species.
3.1. Dis ibu ion Pa e ns o Main Sh ub Families along Coenoclines
Fabaceae and Cap i oliaceae we e he unique amilies wi h inde e mina e esponse
cu es (HOF model I) since bo h had low and cons an co e (<1%) along inc easing a id-
i y DCA1 coenocline. Thymelaeaceae and Oleaceae (HOF model II wi h a dec easing end)
had he g ea es co e in he no he n moun ains wi h a subsequen educ ion owa ds
he sou h (DCA1 le -end; Figu e 2A). Only As e aceae (HOF model II wi h an inc easing
end) showed an inc easing end as a idi y inc eases owa ds he sou h (DCA1 igh -
end). The emainde axonomic g oups showed unimodal esponse cu es (HOF models
IV o V; Figu e 2A and Table 1) wi h op ima a di e en poin s along he g adien , o
example, Aqui oliaceae and Be ulaceae wi h op ima in he no he n moun ains (DCA1 < 2)
had he na owes niche wid h (2 = 0.5), E icaceae had in e media e niche wid h (2 = 2.3)
wi h i s op imum in he ansi ional a ea be ween he A lan ic and Medi e anean condi-
ions (DCA1 ≈ 2), Rosaceae and Cis aceae had he b oades niche wid hs (2 = 6.1 and 4.1,
espec i ely) wi h op ima in he g adien middle (DCA1 ≈ 4), and Labia ae had in e medi-
a e niche wid h (2 = 2.6) wi h i s op imum a he igh end o DCA1, i.e., owa ds he
sou h.
Figu e 2. HOF-de i ed esponse cu es o main axonomic g oups among sh ubs in Palencia (No he n Spain), ela i e
o he i s (A) and second (B) main coenoclines (DCA1 and DCA2, espec i ely). Fabaceae (Faba) and Cap i oliaceae (Cap i )
wi h HOF model I a e no shown in Figu e 2A. Codes a e p esen ed in Table 1, wi h he addi ional: Thymelaeaceae = Thymel;
Oleaceae = Olea.
Table 1. Loca ion, along DCA1 and DCA2, o op imum (μ), op alue (p edic ed maximum p oba-
bili y), and niche wid hs based on 2 ole ances o axonomic g oups wi h unimodal esponses
(HOF model IV; only HOF model V o Be ulaceae along bo h coenoclines and Aqui oliaceae along
DCA1).
Taxonomic G oup Code μ Top Value 2 -niche
DCA 1
Rosaceae Rosa 3.923 0.006 6.08
Cis aceae Cis a 3.786 0.010 4.10
Labia ae Labia 6.387 0.070 2.55
E icaceae E ica 2.224 0.079 2.25
Be ulaceae Be ul 0.882 0.040 0.49
Aqui oliaceae Aqui o 0.358 0.051 0.48
DCA2
Aqui o
Be ul
Cis a
As e a
E ica
Labia
Olea Rosa
Thymel
0
1
2
3
4
5
012345678
Family co e (%)
DCA1
(A)
Aqui o
Be ul
Cap i
Cis a
As e a
E ica
Labia Faba
Olea
Rosa
Thymel
0
1
2
3
4
5
012345
Family co e (%)
DCA 2
(B)
Figu e 2.
HOF-de i ed esponse cu es o main axonomic g oups among sh ubs in Palencia (No he n Spain), ela i e o
he i s (
A
) and second (
B
) main coenoclines (DCA1 and DCA2, espec i ely). Fabaceae (Faba) and Cap i oliaceae (Cap i )
wi h HOF model I a e no shown in Figu e 2A. Codes a e p esen ed in Table 1, wi h he addi ional: Thymelaeaceae = Thymel;
Oleaceae = Olea.
Table 1.
Loca ion, along DCA1 and DCA2, o op imum (
µ
), op alue (p edic ed maximum p obabil-
i y), and niche wid hs based on 2 ole ances o axonomic g oups wi h unimodal esponses (HOF
model IV; only HOF model V o Be ulaceae along bo h coenoclines and Aqui oliaceae along DCA1).
Taxonomic G oup Code µTop Value 2 -Niche
DCA1
Rosaceae Rosa 3.923 0.006 6.08
Cis aceae Cis a 3.786 0.010 4.10
Labia ae Labia 6.387 0.070 2.55
E icaceae E ica 2.224 0.079 2.25
Be ulaceae Be ul 0.882 0.040 0.49
Aqui oliaceae Aqui o 0.358 0.051 0.48
DCA2
Rosaceae Rosa 4.517 0.014 3.42
E icaceae E ica 1.454 0.056 2.71
Labia ae Labia 1.734 0.023 1.23
As e aceae As e a 1.742 0.006 0.95
Aqui oliaceae Aqui o 3.469 0.030 0.94
Be ulaceae Be ul 3.574 0.087 0.13
Along DCA2 coenocline o inc easing s eepness, any axonomic g oup showed HOF
model I, only Cis aceae (HOF model II wi h a dec easing end) dec eased i s co e owa ds
he s eepes si es (DCA2 igh -end), whe eas Fabaceae,Oleaceae,Thymelaeaceae, and Cap i oli-

Fo es s 2021,12, 982 6 o 16
aceae (HOF model II wi h an inc easing end) inc eased hei co e owa ds he s eepes
si es (DCA2 le -end). The o he axonomic g oups showed unimodal esponse cu es
(HOF models IV o V; Figu e 2B and Table 1) wi h op ima a di e en poin s along he
g adien : Be ulaceae,Aqui oliaceae, and Rosaceae owa ds he s eepes si es (DCA2 > 3.5),
whe eas E icaceae,As e aceae, and Labia ae owa ds he less sloping si es (DCA2 < 2); while
Rosaceae and E icacea had he b oades niche wid hs (2 = 3.4 and 2.7, espec i ely).
3.2. Sh ub Func ional G oup Responses along Coenoclines
Conside ing he geog aphical dis ibu ion, only Medi e anean sh ubs species did
no shows a unimodal esponse cu e along DCA1 coenocline o inc easing a idi y. They
showed an inc easing end below maximum a ainable esponse (HOF model III;
Figu e 3A
)
owa ds he sou h (DCA1 igh -end). The sh ubs classi ied as A lan ic, A lan ic- Medi e -
anean, and endemic o Ibe ian Peninsula showed skewed unimodal esponse cu es
along DCA1 coenocline (model V; Figu e 3A; Table 2). A lan ic sh ubs wi h op imum in
he no he n moun ains (DCA1 < 2) had he b oades niche (2 = 4.4), whe eas A lan ic-
Medi e anean, and endemic o Ibe ian Peninsula sh ubs wi h na owe niches (2 = 1.7
and 2 = 1.1, espec i ely) had he op ima in he ansi ional a ea be ween he A lan ic and
Medi e anean condi ions (DCA1 ≈2).
When bio ype o Raunkiæ
´
s li e- o m was conside ed, bo h deciduous and pe ennial
o phane ophy es and chame ophy es sh ubs showed skewed unimodal esponse cu es
along DCA1 coenocline (model V; Figu e 3B,C; Table 2). Phane ophy es and deciduous
sh ubs showed close niche wid hs (2 = 3.0 and 2.6, espec i ely) wi h he op ima in he
no he n moun ains (DCA1 < 2), whe eas pe ennial and chamaephy es wi h he same
b oades niche wid h (2 = 4.0) had op ima in he ansi ional a ea be ween he A lan ic
and Medi e anean condi ions (DCA1 ≈2).
In he case o sh ub dispe sal modes, only au ocho y and ba ocho y did no display
unimodal esponse cu es along DCA1 coenocline (Figu e 3D): au ocho y showed a HOF
model II wi h a dec easing end owa ds he sou h (DCA1 igh -end), while ba ocho y
showed HOF model III wi h an inc easing end below maximum a ainable esponse
owa ds he sou h (DCA1 igh -end). Anemocho y and zoocho y had he op ima in he
ansi ional a ea be ween he A lan ic and Medi e anean condi ions (DCA1
≈
2), whe eas
‘o he ’ had he op imum in he igh end o DCA1 coenocline, i.e., owa ds he sou h; he
h ee dispe sal modes had simila and in e media e niche wid hs (2 = 2.0–3.3; Table 2).
Bo h ca ego ies o egene a ion me hod displayed skewed unimodal esponse cu es
along DCA1 coenocline (model V; Figu e 3E; Table 2): esp ou e s wi h he op imum in he
no he n moun ains (DCA1 < 2) and ge mina o s wi h he op imum in he middle pa o
he g adien (DCA1 ≈4); bo h wi h na ow niche wid hs (2 < 1.5).
Along DCA2 coenocline o inc easing s eepness, and conside ing sh ub geog aphical
dis ibu ion, only A lan ic sh ubs did no show unimodal esponse cu es bu a HOF
model III wi h an inc easing end (Figu e 3F) owa ds he s eepes si es (DCA2 igh -end).
Sh ubs classi ied as he Medi e anean, A lan ic-Medi e anean, and endemic o he Ibe ian
Peninsula showed skewed unimodal esponse cu es (model V; Table 2) wi h op ima in
he s eepes si es (DCA2 < 2); he A lan ic-Medi e anean sh ubs had he b oades niche
wid h (2 = 3.9).
When bio ype o Raunkiæ
´
s li e- o m we e conside ed (Figu e 3G,H), bo h deciduous
and pe ennial, as well as chame ophy es showed skewed unimodal esponse cu es along
DCA2 coenocline (model V; Table 2) wi h close niche wid hs (2 = 1.5–1.8). Chame ophy es
and pe ennial sh ubs had he op ima in he s eepes si es (DCA2 < 2), whe eas deciduous
sh ubs had he op imum in he middle pa o he slope g adien (DCA2 = 4.6). Phane o-
phy es showed a HOF model II wi h an inc easing end owa ds he s eepes si es (DCA2
igh -end).
Fo es s 2021,12, 982 7 o 16
Fo es s 2021, 12, x FOR PEER REVIEW 7 o 16
Figu e 3. HOF-de i ed esponse cu es o sh ub unc ional g oups in Palencia (No he n Spain),
ela i e o he i s (A–E) and second (F–J) coenoclines (DCA1 and DCA2, espec i ely); (A,F): geo-
g aphical dis ibu ion, (B,G): bio ype, (C,H): Raunkiæ ´s li e- o m, (D,I): dispe sal mode, and (E,J):
egene a ion me hod.
0
5
10
15
20
25
30
012345678
Co e (%)
(A)
A l-Med
A lan ic
Medi e anean
Endemic o IP
0
5
10
15
20
25
30
35
40
45
012345678
Co e (%)
(B)
Pe ennial
Deciduous
0
5
10
15
20
25
30
35
40
012345678
Co e (%)
(C)
Chamephy es
Phane ophy es
O he
0
5
10
15
20
25
30
35
012345678
Co e (%)
(D)
Au hoco y
Ba ocho y
Zoocho y
Anemocho y
0
5
10
15
20
25
30
35
40
012345678
Co e (%)
DCA1
(E)
Resp ou e s
Ge mina o s
0
5
10
15
20
25
30
35
40
45
50
012345
Co e (%)
(F)
ATL-MED
Medi e anean
A lan ic
Endemic IP
0
5
10
15
20
25
30
35
40
45
50
55
012345
Co e (%)
(G)
Pe ennial
Deciduous
0
5
10
15
20
25
30
35
40
45
50
55
012345
Co e (%)
(H)
Chamephy es
Phane ophy es
0
5
10
15
20
25
30
35
40
45
50
012345
Co e (%)
(I)
Anemoco y
Au hoco y
Zoocho y
Ba ocho y
O he
0
5
10
15
20
012345
Co e (%)
(J)
Resp ou e s
Ge mina o s
DCA 2
Figu e 3.
HOF-de i ed esponse cu es o sh ub unc ional g oups in Palencia (No he n Spain),
ela i e o he i s (
A
–
E
) and second (
F
–
J
) coenoclines (DCA1 and DCA2, espec i ely); (
A
,
F
):
geog aphical dis ibu ion, (
B
,
G
): bio ype, (
C
,
H
): Raunkiæ
´
s li e- o m, (
D
,
I
): dispe sal mode, and
(E,J): egene a ion me hod.
Fo es s 2021,12, 982 8 o 16
Table 2.
Loca ion o op imum (
µ
), op alue (p edic ed maximum p obabili y), and niche wid hs
based on 2 ole ances o sh ub unc ional g oups wi h unimodal esponses (HOF model V; only
HOF model IV o ‘au hoco y’ along DCA1 and ‘A lan ic-Medi e anean’ along DCA2). Da a o
A lan ic sh ubs along DCA2 a e no a ailable since hei op ima all ou side he sampled pa o
he g adien .
Fuc ional G oup µTop Value 2 -Niche
DCA1
Geog aphical dis ibu ion
A lan ic 1.69 0.18 4.39
A lan ic-Medi e anean 2.68 0.11 1.69
Endemic o Ibe ian Peninsula 2.08 0.04 1.12
Bio ype
Pe ennial 1.95 0.28 4.01
Deciduous 1.07 0.14 3.05
Raunkiæ ’s li e- o m
Chamaephy es 2.49 0.23 4.02
Phane ophy es 1.26 0.21 2.62
Dispe sal mode
Anemocho y 1.95 0.13 2.06
Zoocho y 2.64 0.20 3.30
O he 6.75 0.08 2.02
Regene a ion me hod
Ge mina o s 0.85 0.08 1.04
Resp ou e s 1.63 0.22 1.15
DCA2
Geog aphical dis ibu ion
Medi e anean 1.05 0.14 1.39
A lan ic-Medi e anean 1.90 0.07 3.9
Endemic o Ibe ian Peninsula 1.27 0.03 1.29
Bio ype
Pe ennial 1.07 0.30 1.78
Deciduous 4.64 0.33 1.52
Raunkiæ ’s li e- o m
Chamaephy es 1.25 0.25 1.72
Dispe sal mode
Zoocho y 4.57 0.28 2.53
Au hoco y 0.97 0.14 0.99
Ba ocho y 1.82 0.01 0.74
O he 1.88 0.04 0.40
Regene a ion me hod
Ge mina o s 3.62 0.10 1.18
Resp ou e s 1.06 0.13 1.39
In he case o sh ub dispe sal modes (Figu e 3I), anemocho y showed a HOF model
III wi h an inc easing end owa ds he s eepes si es (DCA2 igh -end). The emainde
g oups showed unimodal esponse cu es (model V; Table 2) along DCA2 coenocline.
Au hocho y, ba ocho y, and ‘o he ’ wi h e y na ow niche wid hs (2 < 1) had op ima
in he s eepes si es (DCA2 le -end), whe eas zoocho y wi h he b oades niche wid h
(2 = 4.6) had he op imum owa ds he less slopping si es (DCA2 igh -end).
Bo h ca ego ies o egene a ion me hod showed skewed unimodal esponse cu es
along DCA2 coenocline (model V; Figu e 3J; Table 2). Resp ou e s wi h he op imum in
he s eepes si es (DCA2 le -end), and ge mina o s wi h he op imum owa ds he less
slopping si es (DCA2 igh -end); bo h wi h na ow niche wid hs (2 < 1.5).
Fo es s 2021,12, 982 9 o 16
The heigh o he esponse (h), i.e., p obabili y o occu ence, was e y low along
bo h coenoclines, pa icula ly o axonomic g oups (Table 1). Only Labia ae and E icaceae
along DCA1, and Be ulaceae along DCA2 showed p obabili ies o occu ence abo e 7%.
P obabili ies below 20% we e p edic ed o mos o he o he sh ub unc ional g oups along
bo h coenoclines (Table 2).
4. Discussion
O e all, ou indings sugges ha unde s o y sh ub main amilies and unc ional
g oups espond o he same egional complex en i onmen al g adien s as ee species
(i.e., al i ude empe a u e, and s eepness) since mos g oups showed unimodal ends o
bo h g adien s (coenoclines). Howe e , he e we e some amilies (Figu e 2) and unc ional
g oups (Figu e 3) ha showed inc easing and dec easing ends along he coenoclines,
sugges ing ha he op imal niches o hese g oups a e ou o he leng h o hose g adien s.
In any case, he desc ip ion o niche wid h along g adien s o mos impo an sh ub
amilies and unc ional g oups is undamen al o wo ace s: i) o educe he complexi y o
he successional p ocess enabling us o unde s and i be e and being able o use science-
based managemen o biodi e si y and ecosys em se ices conse a ion, and ii) o de elop
sus ainable o es p ac ices. Iden i ying such pa e ns in he ield is c ucial o ad ance
ecological o es knowledge aking in o conside a ion no only he ee componen bu also
sh ub di e si y and unc ion [51].
4.1. Dis ibu ion Pa e ns o Main Sh ub Families along Coenoclines
The dis ibu ion pa e n o he main sh ub amilies along he inc easing a idi y coen-
ocline (DCA1) e lec ed he ecognized en i onmen al g adien om A lan ic empe a e
a eas o he Medi e anean con inen al clima e o he Cas ilian pla eau [
44
]. The sh ub
amilies dominance changes h ough he i s conenocline om he unde s o y sh ubby eg-
e a ion belonging o Aqui oliaceae,Thymelaceae, and Be ulaceae amilies in he mo e A lan ic,
cold and mois o es s o he no he n moun ains and alleys (DCA1 le -end;
Figu e 2A
)
o E icaceae,Rosaceae, and Cis aceae amilies in he less mois o es s o p e-moun ainous
ange (DCA1 cen e), and he mo e heliophilous sh ubby unde s o y wi h Labia ae and
As e aceae amilies cha ac e is ic o he mo e xe ic Medi e anean o es s on limes one and
gypsum soils in he sou h (DCA1 igh -end). Howe e , he e we e wo amilies, Fabaceae
and Cap i oliaceae, ha showed cons an co e alues along he main a idi y coenocline.
I is well known ha Fabaceae g ow in e y di e en a idi y equi emen s, which a o s
hei abili y o inhabi di e en ecosys ems [
8
]. Simila ly, Cap i oliaceae is a amily wi h gen-
e a like Sambucus,Vibu num, and Lonice a widely dis ibu ed in he no he n hemisphe e
adap ed o wide niche equi emen s [8].
The deciduous b oadlea o es s o A lan ic no he n a eas domina ed by Fagus syl-
a ica and Que cus pe aea a e associa ed wi h an unde s o y o Aqui oliaceae,E icaceae,
and Thymelaceae species such as Daphne lau eola L., E ica a bo ea L., Vaccinium my illus L.
Howe e , in moun ain a eas he o es s o he mois es alleys a e composed o Rosaceae
and Be ulaceae species mixed wi h So bus aucupa ia L. and Ilex aqui olium L. unde Be ula
pubescens Eh h. As he a idi y g adien inc eased (i.e., mo ing sou hwa ds), mo e scle o-
phyllous ee species appea ed like Que cus py enaica, which has an unde s o y domina ed
by E icaceae (e.g., Calluna ulga is (L.) Hull, Daboecia can ab ica (Huds.) K.Koch, E ica cine ea
L., E ica scopa ia L.) ha cons i u e he subs i u ion sh ubby unde s o y o mo e ansi ional-
humid woodlands. In u n, coni e woodlands (Pinus syl es is,Pinus uncina a Mill. ex
Mi b.) in he cold and ainy moun ains o he no h, sh ub-unde s o y is domina ed by
E icaceae amily wi h E ica a bo ea a bo ea as he main species. Finally, mo e xe ophy ic and
he mophilic sh ub amilies eplaced his unde s o y when mo ing sou hwa ds, such as
Labia ae and As e aceae (e.g., La andula spp. and Helich ysum s oechas (L.) Moench) domina -
ing unde Que cus ilex subsp. ballo a,Que cus aginea, and Junipe us hu i e a o es s, whe eas
in he limes one moo s o he sou h, unde Pinus halepensis,Pinus pinea, and Cup essuss
sempe i ens plan a ions, heliophyllous and summe d ough sh ub amilies domina e,
Fo es s 2021,12, 982 16 o 16
63.
Ga cía-Du o, J.; Muñoz, A.; Ál a ez, R.; Pesquei a, X.M.; Ri as, M.; Reyes, O.; Casal, M. Papel de los g adien es ambien ales en
la egene ación ege al as incendio en ecosis emas de ma o al de Galicia. In Ac as del 5
◦
Cong eso Fo es al Español. Mon es y
Sociedad: Sabe quéhace ; Sociedad Española de Ciencias Fo es ales: Pon e ed a, Spain, 2009.
64.
Cal o, L.; Tá ega, R.; Luis, E. Regene a ion pa e ns in a Calluna ulga is hea hland in he Can ab ian moun ains (NW Spain):
E ec s o bu ning, cu ing and ploughing. Ac a Oecol. 2002,23, 81–90. [C ossRe ]
65.
Ga cía, D.; Ma ínez, D. Species ichness ma e s o he quali y o ecosys em se ices: A es using seed dispe sal by ugi o ous
bi ds. P oc. Royal Soc. B. 2012,279, 3106–3113. [C ossRe ]