UNCORRECTED PROOF
O iginal a icle
Time-consis en ea angemen o ca abid bee le
assemblages by an u banisa ion g adien in Hunga y
Tibo Magu a
a,
*,Ga
´bo L. Lo
¨ ei
b
,Be
´la To
´ hme
´ e
´sz
c
a
Ho oba
´gy Na ional Pa k Di ec o a e, P.O. Box 216, H-4002 Deb ecen, Hunga y
b
Uni e si y o Aa hus, Depa men o In eg a ed Pes Managemen , Facul y o Ag icul u al Sciences,
Flakkebje g Resea ch Cen e, DK-4200 Slagelse, Denma k
c
Depa men o Ecology, Uni e si y o Deb ecen, P.O. Box 71, H-4010 Deb ecen, Hunga y
a icle in o
A icle his o y:
Recei ed 6 Feb ua y 2008
Recei ed in e ised o m 21 Ap il
2008
Accep ed 21 May 2008
Published online -
Keywo ds:
GLOBENET
Habi a al e a ion hypo hesis
Inc eased dis u bance hypo hesis
In e media e dis u bance
hypo hesis
Species ichness
U banisa ion
abs ac
To examine he impac o u banisa ion on a h opod biodi e si y, ca abid (Coleop e a: Ca -
abidae) assemblages we e s udied o e 2yea s along a u al–u ban g adien ep esen ing
inc easing le els o human dis u bance. Ca abids we e collec ed by pi all apping du ing
hei whole ac i i y pe iod in lowland oak o es pa ches in and nea he ci y o Deb ecen,
Eas e n Hunga y, o e wo seasons (2001–2002). Ca abid ac i i y densi y was signi ican ly
highe in he u al han in he wo o he a eas, bu he e was no signi ican di e ence in
species ichness (measu ed as mean numbe o species caugh / ap). The p opo ion o
o es specialis s signi ican ly dec eased om he u al owa ds he u ban a ea, and he
p opo ion o o es specialis species was signi ican ly highe in he u al and subu ban
a eas han in he u ban one. In con as , he ela i e ac i i y densi y o gene alis species
signi ican ly inc eased along he u al–u ban g adien . Bo h he ela i e numbe o open-
habi a species and hei ac i i y densi y we e signi ican ly highe in he u ban o es
agmen s han in he subu ban and u al ones. The pa e ns ound we e consis en
be ween he 2yea s. Mul idimensional scaling indica ed p onounced changes in species
composi ion along he g adien ; he assemblages in u ban o es agmen s we e mo e
a iable han in he o he a eas. A la ge p opo ion o he a ia ion in o e all ac i i y
densi y, species ichness and he p opo ion o ca abids wi h di e en habi a a ini ies
could be explained by s uc u al habi a a iables (pe cen age co e by canopy, lea li e ,
he bs and decaying wood), and p ey a ailabili y.
ª2008 Published by Else ie Masson SAS.
1. In oduc ion
An inc ease o human popula ion causes inc eased esou ce
use by humans, la ge impac on non-u ban habi a s, and
he con e sion o o iginal, u al habi a s o u ban ones.
U banisa ion is inc easing wo ldwide, and hal o mo e o
he global human popula ion li es in ci ies (Uni ed Na ions,
2004). The ob ious impac o u banisa ion on he o iginal
habi a s is he agmen a ion and loss o he o iginal habi a .
The e a e also changes in empe a u e, soil acidi y, pollu ion,
decomposi ion, ca bon and ni ogen cycling (Niemela
¨, 1999;
Rebele, 1994). U banisa ion causes changes in communi y
* Co esponding au ho .
E-mail add esses: magu [email protected] (T. Magu a), [email p o ec ed] (G.L. Lo
¨ ei), [email p o ec ed] (B. To
´ hme
´ e
´sz).
a ailable a www.sciencedi ec .com
jou nal homepage: www.else ie .com/loca e/ac oec
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1146-609X/$ – see on ma e ª2008 Published by Else ie Masson SAS.
doi:10.1016/j.ac ao.2008.05.010
ac a oecologica xxx (2008) 1–11
ACTOEC2442_p oo 28 June 2008 1/11
Please ci e his a icle in p ess as: Magu a, T. e al., Time-consis en ea angemen o ca abid bee le assemblages by an u ban-
isa ion g adien in Hunga y, Ac a Oecolo. (2008), doi:10.1016/j.ac ao.2008.05.010
UNCORRECTED PROOF
s uc u e and species ichness ia he al e a ion o habi a
s uc u e (Gibb and Hochuli, 2002), habi a agmen a ion
and loss (Gibbs and S an on, 2001), c ea ing oppo uni ies o
in asion o alien species (Honnay e al., 2003), clima e wa m-
ing (Hegelbach, 2001) and inc eased pollu ion (S eine , 1995).
The phases o u banisa ion seem o be simila all o e he
globe, bu i is unknown whe he hese will cause simila
changes in biodi e si y (McDonnell and Picke , 1990).
Compa a i e ecological s udies, done in di e en loca ions
bu using he same ea men s a e impo an o ecological
unde s anding, bu a e e y ew and so ely needed (Law on,
2000). E ec s o u banisa ion on a h opods a e also unde -
s udied, e en i u banisa ion is one o he p ima y causes o
declines in a h opod popula ions (McIn y e, 2000). The Globe-
ne p ojec (Niemela
¨e al., 2000; Niemela
¨and Ko ze, 2000)
aims o examine how u banisa ion a ec s a h opod biodi e -
si y in an o iginally o es ed a ea unde going u banisa ion,
using a g adien app oach (McDonnell and Picke , 1990).
Ca abids (Coleop e a: Ca abidae) we e selec ed o s udy
because hey a e di e se, abundan , hei ela i ely sho gen-
e a ion imes allow hem o espond quickly o an h opogenic
e ec s, and a e easy o sample (Lo
¨ ei and Sunde land, 1996).
S udies published so a analyse ends in he o al numbe
o ca abid indi iduals and species, and he numbe o indi id-
uals and species wi h di e en habi a a ini ies ( o es
specialis species, gene alis and open-habi a species; see
Ala uikka e al., 2002; Niemela
¨e al., 2002; Ishi ani e al.,
2003; Venn e al., 2003; Magu a e al., 2004; Elek and Lo
¨ ei,
2005, 2007; Gaublomme e al., 2005; Sadle e al., 2006).
The published pape s, howe e , ha e se e al sho com-
ings. Mos o hem ely on a single yea o s udy and assume
ha he ends ound in he yea o s udy p o ide a ‘‘ eal’’
pic u e. This can be ques ioned. Fu he , he g adien is no
well cha ac e ised – he subu ban s age is assumed o be
‘‘in-be ween’’ he o he wo phases, he o iginal o es habi a
and he u ban o es agmen (Niemela
¨e al., 2000). Se e al
s udies analysed he o al, o he mean numbe o species
cap u ed, which could be dis o ed by impac s o geog aphy,
clima e and e olu iona y his o y on he ac ual auna (Hus on,
1994).
In ou ea lie wo k (Magu a e al., 2004), we es ed se e al
hypo heses using a single yea o da a. F om hese, he in e -
media e dis u bance hypo hesis (Connell, 1978) has a ely go
suppo , and i is also di icul o quan i y wha cons i u es an
‘‘in e media e’’ le el o dis u bance. The e o e, his hypo he-
sis was no es ed u he . We es ed se e al o mal hypo he-
ses ha could explain he ends o biodi e si y a ec ed by
u banisa ion. These hypo heses would p oduce di e en pa -
e ns bu would no be necessa ily mu ually exclusi e. A
hypo hesis p oposed by G ay (1989) s a es ha inc easing
dis u bance would mono onously dec ease bo h componen s
o di e si y (species ichness and e enness). Mo e equen
and mo e se e e dis up ions would elimina e sensi i e
species, causing a dec ease in species ichness. Species ha
a e able o cope wi h dis u bance would inc ease hei domi-
nance, esul ing in dec easing e enness o he assemblages.
We also es ed a u he de eloped e sion o he ‘‘habi a
al e a ion hypo hesis’’ (Magu a e al., 2004) which assumes
ha inc easing le els o u banisa ion will al e he s uc u e
o he o iginal, u al habi a , causing a dec eased p esence/
dominance o he o es specialis species. Howe e , as he
o iginal habi a pa ches become smalle , species om he
su ounding ma ix will ha e he oppo uni y o pene a e
he emaining habi a islands (Lo
¨ ei e al., 2006) and his could
cause an inc ease in di e si y. The e o e, habi a al e a ion can
cause an o e all dec ease o inc ease o ca abid di e si y. In
a egion wi h ew a ailable gene alis and open-habi a
species, he o e all di e si y change can be de e mined by
he eac ion o o es -associa ed species o u banisa ion. In
a eas wi h many gene alis and open-habi a species, he e
can be an inc ease in o al species ichness.
In his pape , we used da a om 2consecu i e yea s ha
ease he p oblem o ying o gene alise on he basis o a single
yea s udy. We p ecisely posi ioned he subu ban s age
be ween he wo ex emes ( u al and u ban), on he basis o
pe cen age buil -in a ea, using ae ial pho og aphs. Ins ead o
he o al numbe o species and indi iduals, as done by mos
published s udies, we conside ed he p opo ions o species in
di e en classes (specialis s, gene alis s, e c.) in he assem-
blage. Mo e p ecisely, he ollowing hypo heses we e es ed:
(i) di e si y should dec ease om a high alue in he u al
a ea o a low one in he u ban a ea (inc easing dis u bance
hypo hesis, G ay, 1989); and (ii) u banisa ion dec eases he
dominance o o es specialis species and inc eases gene al-
is and open-habi a species om he u al a ea o he u ban
one (habi a al e a ion hypo hesis; Magu a e al., 2004). Ou
analysis indica ed ha u banisa ion causes a decline o
o es -dwelling ca abids bu no an o e all species ichness
dec ease in Hunga y. The ends we ound we e consis en
be ween he 2yea s.
2. Ma e ialsand me hods
2.1. S udy a ea and sampling design
The s udy a eas we e in and a ound he ci y o Deb ecen (Eas -
e n Hunga y, 47320N; 21380E), he second la ges ci y o he
coun y. Th ee o es ed a eas we e selec ed along a u al–
u ban g adien wi hin he bounda ies o he ci y, and in he
su ounding o es (Nagye d}
o Fo es Rese e), as equi ed by
he Globene p o ocol (Niemela
¨e al., 2000). All a eas belong
o a once-con inuous old o es s and (>100 yea s) domina ed
by English oak (Que cus obu ). All agmen s we e 6 ha. We
cha ac e ised he le el o u banisa ion by he ela i e buil -
up a ea, measu ed by he A cView GIS p og am using an ae ial
pho og aph. In he u al a ea, he e we e no buildings (buil -
up a ea 0%) and he o es was con inuous. In he subu ban
a ea, app oxima ely 30% o he su ace was buil -in o pa ed,
while in he u ban a ea, su ace occupied by pa ches o he
o iginal habi a was educed o 40% (60% o he a ea was
buil -up o d as ically di e en om he o iginal o es
habi a ). The dis ance be ween he sampling a eas ( u al, sub-
u ban, u ban) was 1–3 km. Acco ding o Digweed e al. (1995),
his a angemen ul ils he condi ions o pa ch indepen-
dence. Addi ional (no quan i ied) ypes o dis u bance we e
he p esence o people and he in ensi y o o es y/habi a
main enance ope a ions. In he u al o es he e was no
egula o es y in e en ion. In he subu ban a ea, he
allen ees and b anches we e egula ly emo ed, bu he
ac a oecologica xxx (2008) 1–112
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ACTOEC2442_p oo 28 June 2008 2/11
Please ci e his a icle in p ess as: Magu a, T. e al., Time-consis en ea angemen o ca abid bee le assemblages by an u ban-
isa ion g adien in Hunga y, Ac a Oecolo. (2008), doi:10.1016/j.ac ao.2008.05.010
UNCORRECTED PROOF
unde s o y was no hinned. Mos pa hs we e no co e ed
wi h a mac. In he u ban a ea, in addi ion o he ou ine
o es y ope a ions as in he subu ban a ea, he sh ub laye
was s ongly hinned. G ass be ween he o es pa ches was
egula ly mo ed, and he mowed g ass was aken away. The e
we e se e al asphal -co e ed pa hs, inc easing he isola ion
be ween he o es ed pa ches.
The sampling egime ollowed he Globene p o ocol
(Niemela
¨e al., 2002). A ou si es pe u banisa ion s age, a
leas 50 m om each o he , 10 pi all aps (65 mm diame e ,
75% e hylene glycol as p ese a i e, wi h co e s) we e
deployed andomly. T apped bee les we e collec ed
o nigh ly om he end o Ma ch o he end o No embe in
2001 and 2002. T aps we e placed a he same loca ions
in bo h yea s. Ca abids we e iden i ied o species using keys
in Hu˚ ka (1996). Vouche specimens a e held in he Depa -
men o Zoology, Deb ecen Uni e si y.
Six en i onmen al ac o s we e measu ed ha we e
assumed o a ec he dis ibu ion o ca abids. Wi hin a ci cle
o 2 m diame e a ound e e y ap, we es ima ed he pe cen -
age co e by lea li e , decaying wood, he bs, sh ubs and ee
canopy. We also coun ed he numbe o o he in e eb a es
(o he Coleop e a, Chilopoda, Diplopoda, Gas opoda, and
Isopoda) cap u ed in he aps,which is a measu e o he
amoun o po en ial p ey (Se gee a, 1994).
2.2. Da a analyses
Nes ed analyses o a iance wi h epea ed measu es we e
pe o med o es di e ences in he o e all ca abid ac i i y
densi y, species ichness, he p opo ions o o es specialis ,
gene alis and open-habi a species in he assemblages
among he h ee sampling a eas ( u al, subu ban, u ban),
he 12 si es, and be ween he 2yea s (2001 and 2002). Da a
om he indi idual aps (si es nes ed wi hin he sampling
a eas) we e used. G ound bee les we e ca ego ised in o o es
specialis , gene alis and open-habi a species acco ding o
in o ma ion in Hu˚ ka (1996). Da a we e es ed o no mali y
(Kolmogo o –Smi no es , Sokal and Rohl , 1995) and all o
hem p o ed o be no mally dis ibu ed ( esul s no shown).
Tukey es o mul iple compa isons among means was pe -
o med when ANOVA esul s e ealed signi ican di e ences
among means.
The composi ion o ca abid assemblages along he u al–
u ban g adien was compa ed a si e le el by non-me ic
mul idimensional scaling (MDS), using he Hellinge dis ance
(Legend e and Legend e, 1998). The ela ionships be ween he
measu ed habi a a iables and he o e all ca abid ac i i y
densi y, species ichness and he p opo ion o ca abids wi h
di e en habi a a ini ies we e examined by mul iple linea
eg ession analyses (Ku ne e al., 1996).
3. Resul s
3.1. Ca abid di e si y along he u al–u ban g adien
Al oge he , we cap u ed 4421 indi iduals ep esen ing 59
species (2140 indi iduals o 50 species in 2001, and 2281
indi iduals o 46 species in 2002; Table 1). In he u al a ea,
35 species and 2451 indi iduals we e caugh (1206 indi iduals,
25 species in 2001, 1245 indi iduals, 28 species in 2002); 34
species and 1026 indi iduals we e cap u ed in he subu ban
a ea (457 indi iduals, 26 species in 2001, 569 indi iduals, 27
species in 2002), and 944 indi iduals belonging o 51 species
we e cap u ed in he u ban a ea (477 indi iduals, 43 species
in 2001, 467 indi iduals, 38 species in 2002). The mos nume -
ous species was P e os ichus oblongopunc a us in all habi a s
and bo h yea s (excep in he u ban a ea in 2002), and in o al,
made up 47% o he o al ca ch. In he u al o es , Ca abus
iolaceus (in bo h yea s), Synuchus i alis (in 2002 only) and
Ca abus con exus (bo h yea s) we e also nume ous. In he
subu ban a ea, Ha palus a dus,C. con exus and C. iolaceus,
while in he u ban habi a s, Ama a con exio ,Pla yde us u us,
and H. a dus we e common (Table 1).
The o e all ca abid ac i i y densi y was signi ican ly
highe in he u al han in he u ban and subu ban a eas.
Howe e , he e we e no s a is ically signi ican di e ences
in he o e all species ichness (Table 2 and Fig. 1).
3.2. Pa e ns o species ca ego ised by habi a a ini y
The p opo ion o indi iduals belonging o o es specialis
species dec eased signi ican ly om he u al a ea owa ds
he u ban one; he p opo ion o he o es specialis species
was signi ican ly highe in he subu ban and u al a eas
han in he u ban one (Table 2 and Fig. 2).
An opposi e endency was obse ed o gene alis s, whose
ela i e ac i i y densi y inc eased signi ican ly along he
u al–u ban g adien (Table 2 and Fig. 2). The e we e no s a is-
ically signi ican di e ences in he p opo ion o gene alis
species among he s udied a eas, al hough his was highes
in he u ban a ea (Table 2 and Fig. 2).
Bo h he ela i e ac i i y densi y o open-habi a species
and hei p opo ion in he o al species ichness we e signi -
ican ly highe in he u ban a ea compa ed o he subu ban o
u al ones (Table 2 and Fig. 2).
3.3. Compa ison o he ca abid assemblages
The ca abid assemblages o he u al, subu ban and u ban
a eas could be sepa a ed om each o he by he o dina ion
(Fig. 3). The ca abid assemblages in he u ban o es agmen s
we e sepa a ed om he o he s along he i s axis. The
composi ion o he ca abid assemblages o subu ban and u al
a eas was mo e simila o each o he han o he ca abid
assemblages o he u ban o es agmen s. The he e ogenei y
o he ca abid composi ion among he si es o he gi en a ea,
exp essed by he size o he con ex hull on he o dina ion
g aph, inc eased om he u al a ea owa ds he u ban one
(Fig. 3).
3.4. The in luence o habi a ac o s on
ac i i y densi y and species occu ence
The u ban si es had highe g ound and ai empe a u es han
he o he wo habi a ypes. The subu ban si es had a highe
ela i e humidi y and lea li e and sh ub co e , while he
u al si es had he highes pe cen age co e o decaying
wood, he bs and p ey a ailabili y. The o e all ac i i y densi y
ac a oecologica xxx (2008) 1–11 3
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ACTOEC2442_p oo 28 June 2008 3/11
Please ci e his a icle in p ess as: Magu a, T. e al., Time-consis en ea angemen o ca abid bee le assemblages by an u ban-
isa ion g adien in Hunga y, Ac a Oecolo. (2008), doi:10.1016/j.ac ao.2008.05.010
UNCORRECTED PROOF
Table 1 – The numbe s and habi a a ini y o ca abid species cap u ed in pi all aps in and a ound he ci y o Deb ecen,
Hunga y, 2001–2002. Species sequence is acco ding o he biannual o al (mos common i s ). F [ o es specialis species,
G[habi a gene alis species, O [open-habi a species
Species Habi a a ini y 2001 2002 To al
Ru al Subu ban U ban Ru al Subu ban U ban
P e os ichus oblongopunc a us F 795 197 60 710 263 57 2076
Ca abus iolaceus G 124 30 51 113 48 24 390
Ha palus a dus O 3553 343434 70259
Ca abus con exus F 46 41 0 78 66 1 232
Pla yde us u us G 4018 453923 31196
Ama a con exio G 12 6 52 35 20 61 186
Synuchus i alis O 13 3 1 133 3 6 159
P e os ichus s enuus G 7 25 10 4 27 17 90
Ama a saphy ea F 268 4138 665
P e os ichus melana ius G 0133122562
P e os ichus nige G 17 4 9 6 11 13 60
No iophilus u ipes G 3 11 28 4 3 10 59
Pseudoophonus u ipes O 12 4 6 7 22 4 55
Anisodac ylus nemo i agus O 0026002652
Ophonus ni idulus G 321 1101 045
S omis pumica us G1914181043
Bembidion lamp os O302900941
Ha palus la us G 906151839
Ha palus xan hopus winkle i G0003102134
Cala hus uscipes O 0011301529
Ha palus lu eico nis G 1 20 5 0 0 0 26
Ama a amilia is G 4 3 4 0 2 12 25
Badis e lace osus G19206321
Ca abus g anula us G11250413
Licinus dep essus O00615113
No iophilus palus is G21541013
Badis e bulla us G00401712
Panagaeus bipus ula us G00405312
Ama a an hobia G00500510
Ama a o a a G00300710
Badis e me idionalis G02700110
Calosoma inquisi o F 000100010
Ama a communis O0050049
P e os ichus an h acinus G0000358
Ama a simila a O1121106
P e os ichus melas G0013015
Ama a consula is O0102003
Cala hus e a us G0011013
Cli ina osso G0030003
Poecilus cup eus O0010023
Pseudoophonus g iseus O0001023
Agonum lugens G0010012
Anisodac ylus signa us O0000112
Asaphidion la ipes O0020002
No iophilus bigu a us G0020002
Oxypselaphus obscu us G1100002
T echus quad is ia us G0101002
Ama a lucida G0000011
Anchomenus do salis O0010001
Cala hus melanocephalus G0010001
Ca abus ull ichi G0010001
Diach omus ge manus O0010001
Ha palus dis inguendus O0100001
Leis us e ugineus G1000001
Ophonus schaube ge ianus O1000001
Poecilus e sicolo O0000011
P e os ichus mace O0010001
P e os ichus mino G0000101
P e os ichus o oideus G0000011
Numbe o indi iduals 1206 457 477 1245 569 467 4421
Numbe o species 25 26 43 28 27 38 59
ac a oecologica xxx (2008) 1–114
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ACTOEC2442_p oo 28 June 2008 4/11
Please ci e his a icle in p ess as: Magu a, T. e al., Time-consis en ea angemen o ca abid bee le assemblages by an u ban-
isa ion g adien in Hunga y, Ac a Oecolo. (2008), doi:10.1016/j.ac ao.2008.05.010
UNCORRECTED PROOF
Table 2 – Nes ed ANOVA wi h epea ed measu es showing di e ences in o e all ca abid ac i i y densi y, species ichness
and in he p opo ion o o es specialis species, gene alis and open-habi a species along he u al–u ban g adien and
among he 12 si es. Yea [ he e ec o s udy yea (2001 and 2002). Resul s o he Tukey es indica e which a ea(s) di e s
signi ican ly ( p<0.05) om he o he s; o example ‘‘U ban >Subu ban [Ru al’’ indica es ha he a iable was
signi ican ly highe in he u ban a ea han in he subu ban and u al a eas ( hese wo a eas a e no di e en om ha poin
o iew)
Va iable Sou ce d MS Fp Tukey es
O e all ca abid ac i i y densi y Be ween-Subjec s E ec s
G adien 2 9015.2040 6.0905 <0.05 U ban ¼Subu ban <Ru al
Si es 9 1480.1970 7.7209 <0.001
E o 108 191.7130
Wi hin-Subjec s E ec s
Yea 1 91.2670 1.0968 ns
Yea G adien 2 53.0040 0.6370 ns
Yea Si es 9 160.1690 1.9248 ns
E o 108 83.2148
O e all ca abid species ichness Be ween-Subjec s E ec s
G adien 2 51.9875 2.2853 ns
Si es 9 22.7486 4.4642 <0.001
E o 108 5.0958
Wi hin-Subjec s E ec s
Yea 1 8.4375 1.7553 ns
Yea G adien 2 0.1625 0.0338 ns
Yea Si es 9 11.9541 2.4868 <0.02
E o 108 4.8069
P opo ion o o es specialis indi iduals Be ween-Subjec s E ec s
G adien 2 6.2697 29.6362 <0.001 U ban <Subu ban <Ru al
Si es 9 0.2116 5.3790 <0.001
E o 108 0.0393
Wi hin-Subjec s E ec s
Yea 1 0.0216 0.6503 ns
Yea G adien 2 0.0819 2.4616 ns
Yea Si es 9 0.0719 2.1594 <0.05
E o 108
P opo ion o o es specialis species Be ween-Subjec s E ec s
G adien 2 1.5360 17.0754 <0.001 U ban <Subu ban ¼Ru al
Si es 9 0.0900 3.7112 <0.001
E o 108 0.0242
Wi hin-Subjec s E ec s
Yea 1 0.0021 0.0903 ns
Yea G adien 2 0.0132 0.5813 ns
Yea Si es 9 0.0424 1.8652 ns
E o 108 0.0227
P opo ion o gene alis indi iduals Be ween-Subjec s E ec s
G adien 2 2.8950 19.5546 <0.001 U ban >Subu ban >Ru al
Si es 9 0.1480 4.2750 <0.001
E o 108 0.0346
Wi hin-Subjec s E ec s
Yea 1 0.0064 0.1601 ns
Yea G adien 2 0.0104 0.2618 ns
Yea Si es 9 0.0445 1.1183 ns
E o 108 0.0398
P opo ion o gene alis species Be ween-Subjec s E ec s
G adien 2 0.4979 3.7210 ns
Si es 9 0.1338 3.6711 <0.001
E o 108 0.0365
Wi hin-Subjec s E ec s
Yea 1 0.0005 0.0128 ns
Yea G adien 2 0.0119 0.3114 ns
Yea Si es 9 0.0436 1.1428 ns
E o 108 0.0381
(con inued on nex page)
ac a oecologica xxx (2008) 1–11 5
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ACTOEC2442_p oo 28 June 2008 5/11
Please ci e his a icle in p ess as: Magu a, T. e al., Time-consis en ea angemen o ca abid bee le assemblages by an u ban-
isa ion g adien in Hunga y, Ac a Oecolo. (2008), doi:10.1016/j.ac ao.2008.05.010
UNCORRECTED PROOF
was only in luenced by he b co e (posi i ely, in bo h yea s)
and canopy co e (nega i ely, in 1yea ). The o e all species
ichness was only a ec ed (posi i ely) in 1yea by he numbe
o po en ial p ey i ems. The p opo ion o indi iduals belong-
ing o o es specialis species was posi i ely in luenced (in
bo h yea s) by he co e o lea li e , decaying wood and
he bs, and in 1yea , he numbe o po en ial p ey i ems. The
p opo ion o o es specialis species was simila ly in luenced
by he same ac o s, bu only in 1yea –excep lea li e co e ,
which had a posi i e in luence on his pa ame e in bo h yea s
o s udy (Table 3).
The p opo ion o indi iduals belonging o gene alis
species was nega i ely in luenced by decaying wood (bo h
yea s), lea li e , and he b co e (in 1yea only). None o he
measu ed habi a a iables had a signi ican in luence on
he numbe o gene alis species (Table 3).
The ela i e ac i i y densi y o open-habi a species was
nega i ely in luenced by se e al habi a cha ac e is ics: he ex-
en o he b co e (bo h yea s), lea li e and he p esence o
decaying wood (one -bu no he same- yea ). The p opo ion
o open-habi a species had a nega i e ela ionship wi h lea li -
e , canopy co e and he p esence o decaying wood (Table 3).
4. Discussion
4.1. Di e si y changes along he g adien
We ound ha he o e all ca abid ac i i y densi y was signi -
ican ly highe in he u al han in he u ban and subu ban
a eas, bu he o e all di e ences in species ichness we e
s a is ically no signi ican . Simila di e si y pa e ns we e
de ec ed in Belgium (Gaublomme e al., 2005), and Bulga ia
(Niemela
¨e al., 2002). In Denma k, he u ban a ea had he
highes species ichness (Elek and Lo
¨ ei, 2007).
Gi en ha mos o he p o ound changes in habi a quali y
du ing u banisa ion is in ui i ely in e p e ed as making he
habi a less a ou able o a h opods, i is su p ising ha
ou esul s did no suppo he ’’inc easing dis u bance’’ hy-
po hesis (G ay, 1989). The o e all species ichness o ca abids
was almos as high in he hea ily dis u bed u ban o es ag-
men s as in he less dis u bed u al a ea. This is in con as
wi h indings in Canada (Niemela
¨e al., 2002), England (Sadle
e al., 2006), Finland (Niemela
¨e al., 2002; Venn e al., 2003) and
Fig. 1 – Mean alues (±SE) o he o e all ca abid ac i i y
densi y ( op) and species ichness (bo om) along he u al–
u ban g adien a Deb ecen, Hunga y, in 2001–2002.
Table 2 (con inued)
Va iable Sou ce d MS Fp Tukey es
P opo ion o open-habi a indi iduals Be ween-Subjec s E ec s
G adien 2 0.6739 6.1562 <0.05 U ban >Subu ban ¼Ru al
Si es 9 0.1095 3.4740 <0.001
E o 108 0.0315
Wi hin-Subjec s E ec s
Yea 1 0.0849 2.5231 ns
Yea G adien 2 0.0614 1.8233 ns
Yea Si es 9 0.0267 0.7930 ns
E o 108 0.0337
P opo ion o open-habi a species Be ween-Subjec s E ec s
G adien 2 0.3171 9.3649 <0.01 U ban >Subu ban ¼Ru al
Si es 9 0.0339 1.3403 ns
E o 108 0.0253
Wi hin-Subjec s E ec s
Yea 1 0.0017 0.0545 ns
Yea G adien 2 0.0376 1.1967 ns
Yea Si es 9 0.0299 0.9520 ns
E o 108 0.0314
ac a oecologica xxx (2008) 1–116
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ACTOEC2442_p oo 28 June 2008 6/11
Please ci e his a icle in p ess as: Magu a, T. e al., Time-consis en ea angemen o ca abid bee le assemblages by an u ban-
isa ion g adien in Hunga y, Ac a Oecolo. (2008), doi:10.1016/j.ac ao.2008.05.010
UNCORRECTED PROOF
Japan (Ishi ani e al., 2003). A possible eason is he di e ences
in he size o he a ailable species pool o he di e en habi a
a ini y ca ego ies. In Hunga y, open-habi a species could
ha e a la ge species pool, and hus could con ibu e mo e
species han coun ies wi h ex ensi e o es s, such as Finland.
As a consequence, open-habi a - a ou ing species can
inc ease he species ichness in u ban o es agmen s in
Hunga y mo e han in Finland.
4.2. Dominance changes along he g adien
U banisa ion causes se e al o ms o dis u bance, all o which
con ibu e o he al e a ion o he o iginal habi a s (Gilbe ,
1989; Niemela
¨, 1999). The habi a al e a ion hypo hesis was
suppo ed, because he p opo ion o he indi iduals and
species in o es specialis s was signi ican ly highe , while
he p opo ion o indi iduals o gene alis and open-habi a
species as well as hei numbe o species we e signi ican ly
lowe in he less dis u bed u al a ea han in he mo e
dis u bed u ban one. The p opo ion o gene alis species
also inc eased along he u al–u ban g adien . Simila esul
we e ob ained in Belgium (Gaublomme e al., 2005), England
(Sadle e al., 2006), Finland (Ala uikka e al., 2002), and Japan
(Ishi ani e al., 2003), as o es specialis indi iduals we e mo e
likely caugh in subu ban and u al a eas han in he u ban
one.
The esponse by gene alis ca abids is mo e complica ed,
as he e was no di e ence in he numbe o gene alis indi id-
uals along he u al–u ban g adien in Belgium (Gaublomme
e al., 2005) o Japan (Ishi ani e al., 2003) bu hey we e mo e
dominan in he u ban a ea han in he subu ban and u al
ones in Canada, Finland (Niemela
¨e al., 2002), as well as
Denma k (Elek and Lo
¨ ei, 2007). An idiosync a ic esponse
was ound in ano he s udy in Finland whe e mo e gene alis
indi iduals we e collec ed om u al a eas han ei he u ban
o subu ban ones (Ala uikka e al., 2002).
U banisa ion caused he s onges e ec on he o es
specialis ca abid species. These species equi e si es wi h
a special mic oclima e, he p esence o dead and decaying
ees, signi ican co e o lea li e , sh ubs and he bs, oge he
o ming he undis u bed o es loo habi a (Desende e al.,
1999). Habi a al e a ion caused by u banisa ion appea s o
elimina e a ou able mic osi es and con ibu es o he decline
o o es specialis s in he assemblage. Along he s udied
g adien , he dis u bance was he lowes in he o iginal o es
( u al a ea), mode a e in he subu ban a ea ( allen ees
egula ly emo ed, medium numbe o human isi o s), and
highes in he u ban o es agmen s ( hinned sh ub laye ,
0.8
Fig. 2 – Mean alues (±SE) o he ela i e ac i i y densi y ( op ow) and species ichness (bo om ow) o o es specialis ,
gene alis and open-habi a g ound bee le species along he u al–u ban g adien a Deb ecen, Hunga y, in 2001–2002.
ac a oecologica xxx (2008) 1–11 7
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ACTOEC2442_p oo 28 June 2008 7/11
Please ci e his a icle in p ess as: Magu a, T. e al., Time-consis en ea angemen o ca abid bee le assemblages by an u ban-
isa ion g adien in Hunga y, Ac a Oecolo. (2008), doi:10.1016/j.ac ao.2008.05.010
UNCORRECTED PROOF
highes numbe o isi o s). This inc easing dis u bance was
e lec ed by he dec easing p opo ion o o es specialis ca a-
bids. Fu he , habi a al e a ion accompanying u banisa ion
inc eased he p opo ion o bo h gene alis and open-habi a
ca abids. This is in ag eemen wi h G ay’s Inc easing Dis u -
bance Hypo hesis (G ay, 1989), acco ding o which he gene -
alis (oppo unis ic) species should gain dominance wi hin
he assemblage as dis u bance inc eases. Gene alis species
can in ade dis u bed o es habi a s as hey ole a e he
al e ed condi ions (Koi ula, 2002; Koi ula and Niemela
¨, 2003;
Magu a e al., 2000, 2003). The signi ican al e a ion o he o ig-
inal habi a s in he u ban a ea was also e lec ed by he
dominance o open-habi a species in he assemblage. The
u ban pa k con ains se e al mic ohabi a s ha open-habi a
species can colonise. P e ious s udies (Koi ula, 2002; Koi ula
and Niemela
¨, 2003; Magu a e al., 2000, 2001) also emphasised
ha he numbe o open-habi a species inc eased as he
closu e o he o es s and dec eased. Recen wo k (Ha ley
e al., 2007) indica ed ha open-habi a species could success-
ully colonise g assland pa ches in u ban a eas. Such ‘‘ma ix
species’’ can pene a e o es agmen s in an ag icul u al
landscape (Lo
¨ ei e al., 2006), and p obably also he gene ally
small u ban o es agmen s.
4.3. Composi ional changes along he g adien
The o dina ion analysis sepa a ed he u ban si es om he
subu ban and u al ones, indica ing ha u banisa ion caused
a conside able change in he composi ion o ca abid assem-
blages along he u al–u ban g adien . The composi ion o
ca abid assemblages was simila a he subu ban and u al
si es. Fo es specialis species p e e ed he mode a ely
dis u bed o ligh ly dis u bed a eas (subu ban and u al),
while gene alis and open-habi a species p e e ed he u ban
a ea. The highes composi ional he e ogenei y was a he
Fig. 3 – O dina ion (non-me ic mul idimensional scaling
using he Hellinge dis ance) o he ca abid assemblages
along he s udied u al–u ban g adien a Deb ecen,
Hunga y, in 2001–2002. Analysis was made a si e le el;
he s ess o he wo-dimensional con igu a ion was
0.1033. Open symbols: da a om 2001, closed symbols:
da a om 2002.
Table 3 – Rela ionship be ween he selec ed en i onmen al a iables and he o e all ca abid ac i i y densi y, species ichness and he p opo ion o o es specialis
species, gene alis and open-habi a species as de e mined by mul iple linea eg ession analysis (d [6, 113 in all cases). Posi i e and nega i e ela ionships a e
indica ed. ns: no signi ican , *: p<0.05, **: p<0.01, ***: p<0.001
O e all ac i i y
densi y
O e all species
ichness
P opo ion o o es
specialis indi iduals
P opo ion o o es
specialis species
P opo ion o gene alis
indi iduals
P opo ion o
gene alis species
P opo ion o open-
habi a indi iduals
P opo ion o open-
habi a species
2001 2002 2001 2002 2001 2002 2001 2002 2001 2002 2001 2002 2001 2002 2001 2002
F9.5839 5.6831 5.7969 3.6355 4.4663 7.5187 2.4285 3.1693 2.6044 3.5664 1.1471 1.5259 2.7737 2.3581 2.8575 0.4967
Signi icance 0.0001 0.0001 0.0001 0.005 0.0005 0.0001 0.05 0.01 0.05 0.005 0.40 0.20 0.05 0.05 0.05 0.85
R0.5807 0.4815 0.4851 0.4022 0.4378 0.5342 0.3380 0.3795 0.3485 0.3990 0.2396 0.2738 0.3583 0.3336 0.3630 0.1603
Lea li e co e þ
ns
þ
ns
ns
ns
þ** þ** þ** þ***
ns
ns
ns
ns
**
ns
Decaying wood þ
ns
þ
ns
þ
ns
ns
þ*** þ** þ*þ
ns
*** þ
ns
ns
**
ns
*þ
ns
He b co e þ*** þ** þ
ns
þ
ns
þ*** þ*** þ*þ
ns
*
ns
ns
ns
** *
ns
ns
Sh ub co e
ns
ns
þ
ns
ns
þ
ns
ns
þ
ns
ns
ns
ns
þ
ns
þ
ns
ns
þ
ns
ns
ns
Canopy co e *
ns
ns
þ
ns
þ
ns
ns
þ
ns
ns
þ
ns
ns
þ
ns
ns
ns
þ
ns
*þ
ns
P ey ac i i y
densi y
þ
ns
þ
ns
þ** þ
ns
ns
þ**
ns
þ*þ
ns
ns
þ
ns
ns
ns
ns
ns
ns
ac a oecologica xxx (2008) 1–118
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ACTOEC2442_p oo 28 June 2008 8/11
Please ci e his a icle in p ess as: Magu a, T. e al., Time-consis en ea angemen o ca abid bee le assemblages by an u ban-
isa ion g adien in Hunga y, Ac a Oecolo. (2008), doi:10.1016/j.ac ao.2008.05.010
UNCORRECTED PROOF
u ban si es (exp essed by he size o he con ex hull on he
o dina ion g aph). In he u ban a ea, he o es pa ches had
o es specialis , as well as gene alis and open-habi a spe-
cies. Because o he high le el o agmen a ion, dis u bance,
and isola ion, o es specialis s did no appea consis en ly
in all u ban o es agmen s. Mo eo e , he colonisa ion
success o gene alis and open-habi a species a he u ban
si es seems o be a iable, and hus he composi ion o in ad-
ing species a ied. Con a y o his, in he less dis u bed o es
a ea, o es specialis species and he dominan and subdom-
inan gene alis species we e p esen a mos si es leading o
lowe composi ional he e ogenei y. The mode a ely dis u bed
subu ban a ea lies be ween he o he wo. Niemela
¨(1999) also
no iced ha composi ional he e ogenei y among si es (b-
di e si y) is high in u ban a eas.
4.4. The impac o habi a cha ac e is ics on ca abids
Reg ession analyses showed ha a signi ican p opo ion o
he a ia ion in o e all ac i i y densi y, species ichness and
in he p opo ion o ca abids wi h di e en habi a a ini y
was associa ed wi h selec ed habi a ac o s. The o e all
ca abid ac i i y densi y (numbe o bee les/ ap) inc eased
wi h inc easing he b co e and dec easing canopy co e .
The dec eased canopy co e may p o ide a a ou able habi a
o he in ading open-habi a and gene alis species,which
may inc ease he o e all ac i i y densi y.
The p opo ion o bo h indi iduals and species belonging
o o es specialis species inc eased as he co e by lea li e
co e , decaying wood, and he bs as well as p ey a ailabili y
inc eased. Lea li e g ea ly in luences he spa ial occu ence
pa e n o ca abids (Koi ula e al., 1999; Magu a e al., 2000,
2004, 2005; Taboada e al., 2004). A high co e o lea li e
and decaying wood ma e ial indica e an undis u bed o es
habi a which is p e e ed by o es specialis s and p o ides
shel e agains p eda o s, sui able si es o aes i a ion, hibe -
na ion, egg and la al de elopmen . The inc easing he b co e
may also in luence mic oclima e (e.g. empe a u e and ai
mois u e),which is an impo an ac o con olling g ound
bee le dis ibu ion (Niemela
¨e al., 1992; Magu a e al., 2000).
Mo eo e , he e may be a posi i e co ela ion be ween he
co e o he bs and he amoun o he bi o ous in e eb a es.
He bi o ous in e eb a es could be p ey o p eda o y ca a-
bids and can p o ide a mo e uni o m esou ce dis ibu ion
in ime (Niemela
¨and Spence, 1994; Niemela
¨e al., 1996) esul -
ing in agg ega ion o ca abids a mic osi es wi h abundan
p ey (B yan and W a en, 1984; Guillemain e al., 1997;
Fou nie and Lo eau, 1999).
The p opo ion o indi iduals belonging o gene alis
species and ha o bo h indi iduals and species o open-
habi a -associa ed ones dec eased as he lea li e and decay-
ing wood co e inc eased. Guillemain e al. (1997) showed ha
he abundance o habi a gene alis species dec eases wi h
inc easing lea li e hickness. The nega i e ela ionship
be ween he b co e and he p opo ion o indi iduals o
bo h gene alis and open-habi a species could indica e
habi a ‘‘ esis ance’’ hampe ing g ound bee le mo emen .
The p opo ion o open-habi a species inc eased as he
canopy co e dec eased –such species may be a ac ed o
ligh and a oid shaded a eas.
4.5. Implica ions o he managemen
o u ban o es agmen s
U ban g een a eas ha e ec ea ional impo ance and inc ease
he quali y o u ban li e (Niemela
¨, 1999). Cu en u ban habi a
managemen , howe e , is one o he leading causes o al e -
a ion in indigenous a h opod assemblages (Da is, 1978).
The e o e, he e is a g owing need o managemen s a egies,
which simul aneously conside ec ea ional, economic and
conse a ion c i e ia (Gilbe , 1989).
The a ailable in o ma ion om he Globene p ojec
(Ala uikka e al., 2002; Niemela
¨e al., 2002; Ishi ani e al.,
2003; Venn e al., 2003; Magu a e al., 2004; Elek and Lo
¨ ei,
2005, 2007; Gaublomme e al., 2005; Sadle e al., 2006), as
well as o he esea ch (G andchamp e al., 2000; Welle and
Ganzho n, 2004) indica es ha u ban o es agmen s can s ill
be ela i ely species- ich, bu he assemblages a e domina ed
by gene alis and open-habi a species. The dominance o
o es specialis species in he assemblages signi ican ly
dec eased along he dis u bance g adien . We no e ha he
impo ance o selec ed habi a ac o s was mos ly consis en
in ime, bu he same ac o s we e no always signi ican .
This unde lines ha single yea s udies, including he majo -
i y o published Globene s udies, does no necessa ily
indica e he impo an ac o s de e mining he s uc u e o
a h opod assemblages. Ou 2-yea s udy is an imp o emen
o e he usual single yea Globene s udies (e.g. Niemela
¨
e al., 2002; Ishi ani e al., 2003; Elek and Lo
¨ ei, 2007; Sadle
e al., 2006) bu longe - e m s udies a e necessa y o gain alid
insigh s in o he impac o u banisa ion on g ound bee les and
on a h opod biodi e si y in gene al.
Un a ou able impac s o pa k managemen on biodi e si y
can be lessened by habi a managemen which minimises he
modi ica ion o habi a s uc u e, he eby allowing he main-
enance o na u al p ocesses o decomposi ion and nu ien
cycling. Recen esea ch indica es ha u ban dwelle s no ice
and app ecia e di e si y in u ban pa ks (Fulle e al., 2007).
Consequen ly, adop ing managemen egimes ha y o
maximise di e si y could also inc ease he alue o u ban
pa ks o people.
Acknowledgmen s
TM was suppo ed by he Hunga ian Scien i ic Resea ch Fund
(g an no. F61651) and by a Bolyai Resea ch Fellowship o he
Hunga ian Academy o Sciences. GL was suppo ed by
a Domus Hunga ica ellowship. We hank Ti ada Molna
´
o ield and labo a o y assis ance and wo anonymous e-
iewe s o commen s on he manusc ip .
e e ences
Ala uikka, D.M., Ko ze, D.J., Ma einen, K., Niemela
¨, J., 2002.
Ca abid and spide assemblages along an u ban o u al
g adien in Sou he n Finland. J. Insec Conse . 6, 195–206.
B yan, K.M., W a en, S.D., 1984. The esponses o polyphagous
p eda o s o spa ial he e ogenei y: agg ega ion by ca abid and
ac a oecologica xxx (2008) 1–11 9
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ACTOEC2442_p oo 28 June 2008 9/11
Please ci e his a icle in p ess as: Magu a, T. e al., Time-consis en ea angemen o ca abid bee le assemblages by an u ban-
isa ion g adien in Hunga y, Ac a Oecolo. (2008), doi:10.1016/j.ac ao.2008.05.010
