Ca abid bee les as use ul model o ganisms, indica o s, o bo h? 287
Use ul model o ganisms, indica o s, o bo h?
G ound bee les (Coleop e a, Ca abidae)
e lec ing en i onmen al condi ions
Ma i J. Koi ula
Finnish Fo es Resea ch Ins i u e, Van aa Resea ch Uni , P.O. Box 18, FI-01301 Van aa, Finland
Co esponding au ho : Ma i J. Koi ula ([email p o ec ed])
Academic edi o : D.J. Ko ze |Recei ed 27 No enbe 2009|Accep ed 7 July 2010|Published 20 May2011
Ci a ion: Koi ula MJ (2011) Use ul model o ganisms, indica o s, o bo h? G ound bee les (Coleop e a, Ca abidae)
e lec ing en i onmen al condi ions. In: Ko ze DJ, Assmann T, Noo dijk J, Tu in H, Ve meulen R (Eds) Ca abid
Bee les as Bioindica o s: Biogeog aphical, Ecological and En i onmen al S udies. ZooKeys 100: 287–317. doi: 10.3897/
zookeys.100.1533
Abs ac
Classic s udies ha e success ully linked single-species abundances, li e-his o y ai s, assemblage s uc u es
and biomass o ca abid bee les o pas and p esen , human-caused en i onmen al impac s and a ia ion
in ‘na u al’ condi ions. This e idence has led many o sugges ca abids o unc ion as ‘indica o s’ − a e m
ha bea s mul iple meanings. He e, a conse a ion-o ien ed de ini ion o an indica o is used, ca abid
indica o po en ial om se en iews is e alua ed, and ways o p oceed in indica o esea ch a e discussed.
(1) Ca abid species ichness poo ly indica es he ichness and abundance o o he axa, which unde lines
he impo ance o using mul iple axa in en i onmen al assessmen s. The abili y o assemblage indices and
specialis o unc ional-g oup abundances o e lec a e species and habi a s should be examined in de ail.
(2) Expe imen al e idence sugges s ha ca abids may po en ially se e as keys one indica o s. (3) Ca abids
a e sensi i e o human-al e ed abio ic condi ions, such as pes icide use in ag o-ecosys ems and hea y
me al con amina ion o soils. Ca abids migh hus e lec ecological sus ainabili y and ‘ecosys em heal h’.
(4) Ca abid assemblages hos abundan species cha ac e is ic o pa icula habi a ypes o successional
s ages, which makes hem p omising dominance indica o s. (5) Ca abids e lec a ia ion in ‘na u al’
condi ions, bu ege a ion and s uc u al ea u es a e mo e commonly adop ed as condi ion indica o s.
Ca abids ne e heless p o ide ye ano he , equally accu a e, iew on he s uc u e o he en i onmen . (6)
Ca abids may unc ion as ea ly-wa ning signale s, as sugges ed by ecen s udies linking clima e and ca -
abid dis ibu ions. (7) Ca abids e lec na u al and human-caused dis u bances and managemen , bu he
use ulness o hese esponses o conse a ion pu poses equi es u he esea ch. In summa y, Eu opean
ca abids appea use ul model o ganisms and possibly indica o s because hey a e di e se, axonomically
and ecologically well-known, e icien ly e lec bio ic and abio ic condi ions, a e ele an a mul iple spa-
ial scales, and a e easy o collec in su icien ly la ge numbe s o allow s a is ical analyses. The assump ion
ZooKeys 100: 287–317 (2011)
doi: 10.3897/zookeys.100.1533
www.zookeys.o g
Copy igh M.J. Koi ula. This is an open access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion License, which pe mi s
un es ic ed use, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal au ho and sou ce a e c edi ed.
ReseARCh AR iCle
Launched o accele a e biodi e si y esea ch
A pee - e iewed open-access jou nal
Ma i J. Koi ula / ZooKeys 100: 287–317 (2011)
288
ha ca abid esponses would e lec a e en i onmen al condi ions o he esponses o a e and h ea ened
species ‒ c ucial in o ma ion o conse a ionis s and manage s ‒ has no ye been c i ically e alua ed.
E en i i holds, he use ulness will be con ex dependen : species and hei popula ions a y, condi ions
a y, ques ions pu o wa d a y, and assessmen goals a y.
Keywo ds
abio ic, assessmen , bioindica o , bio ic, change, conse a ion, dis u bance, dominance, ea ly wa ning,
human impac , keys one, managemen , ichness
in oduc ion
Indica o s, in he mos gene al sense, can e e o any hing ha ha e been shown o e-
lec some hing apa om hei indi idualis ic esponse. Fo example, di e en species
e lec habi a ypes h ough hei associa ions wi h pa icula bio ic and abio ic condi-
ions, and a common assump ion is ha he magni ude and di ec ion o his e lec ion
a e no unique o he s udied species. Fo conse a ionis s and en i onmen al manag-
e s, i.e., he po en ial end use s o indica o s, such gene al pa e ns will no su ice. Fo
hem, an indica o should pe mi conclusions ega ding pa icula condi ions o bio-
di e si y, which could no o he wise be concluded ei he wi hou using he indica o
o h ough using easie , cheape and/o quicke assessmen ools. Indeed, Land es e
al. (1988) desc ibed an indica o as being a axon o a s uc u e ”…whose cha ac e is ics
(e.g., p esence o absence, popula ion densi y, dispe sion, ep oduc i e success) a e used as an
index o a ibu es oo di icul , incon enien , o expensi e o measu e o o he species o
en i onmen al condi ions o in e es “. He e I use he e m ‘indica o ’ ollowing his s ic
de ini ion unless s a ed o he wise.
In ecological impac s udies ca abid bee les a e equen ly ci ed as indica o s in he
ague sense desc ibed abo e, bu acco ding o he s ic sense hey should mo e o en
be ci ed as model o s udy o ganisms. A model o ganism is a (g oup o ) species ha is
used o examine a pa icula s udy ques ion (a hypo hesis) unde a esea ch p og amme
(sensu Unde wood 1997; see also den Boe 2002). Fo example, he esea che ’s gen-
e al ques ion migh be ”Does ungicide sp aying a ec soil-dwelling animals?” which
is hen s udied using ca abids o model a biological esponse. I you ype he wo ds
’ca ab*‘ and ’indica o *‘ in o Scopus you ge 172 esul s, and simila ly ISI Web o Sci-
ence p oduces 186 esul s (26 May 2010). Many i no mos o hese s udies ha e li le
o do wi h ca abids indica ing any hing else bu hemsel es, i.e., hei indi idualis ic
esponse o ea men s o in e es , excep pe haps i ial issues such as he sampled
habi a ype. Such ‘wa e ing down’ o e ms may lead o misunde s andings among
scien is s, p ac i ione s and ama eu s, including he media, and o an impo e ishmen
o he scien i ic language.
He e I e alua e he indica o po en ial o ca abid bee les o se en common appli-
ca ions o indica o s (Lindenmaye e al. 2000): (1) indica ing ichness and abundance
o axa o he han ca abids; (2) unc ioning as keys one o ganisms; (3) indica ing hu-
Ca abid bee les as use ul model o ganisms, indica o s, o bo h? 289
man-al e ed abio ic condi ions, he e pollu ion; (4) indica ing pa icula en i onmen al
condi ions h ough nume ical o biomass dominance; (5) e lec ing a ia ion in ‘na u-
al’ condi ions; (6) ac ing as ea ly-wa ning signale s; and (7) indica ing dis u bances
and managemen . Gene ally speaking, he basic equi emen s o he use o indica o s
a e ul illed by mos Eu opean ca abids: good knowledge exis s on (i) condi ions o
which hese species a e adap ed o; (ii) dis ibu ions o he species in a gi en se o
pa ches; (iii) he species’ esponses o en i onmen al a ia ion/al e a ion; and (i ) a i-
a ion in he species’ popula ion dynamics (Ande sen 1999; Lindenmaye e al. 2000;
see "Ca abids as model o ganisms" below).
In his e iew I ask h ee ques ions wi h a combined Eu opean and No h Ame i-
can ocus.
Which ea u es cha ac e ize ca abids as po en ial indica o s? In "Ca abids as mod-
el o ganisms" I b ie ly e iew he cu en s a e o ecological knowledge, in o ma ion
gaps, and me hods used in ca abid esea ch.
Wha kinds o indica o s migh be ound among ca abids, conside ing he se en
indica o ca ego ies abo e? In o he wo ds, wha is he e idence o and agains using
ca abids as indica o s? In "E alua ion o ca abids as indica o s" my aim is o sum-
ma ize key e idence o ca abid indica o po en ial. This Sec ion is in en ionally c i i-
cal, as he use o indica o s in conse a ion should be on an excep ionally solid basis:
h ea ened species o habi a s a e a s ake.
Whe e, and how, should ca abidologis s p oceed in hei sea ch o indica o s?
In "Iden i ying and using ca abid indica o s" I discuss (a) ways o inco po a e
ca abids in o ou ine en i onmen al assessmen s, (b) issues abou ca ying ou
esea ch sea ching o indica o s, and (c) whe e o ind new a eas in he ongoing
indica o hun .
Ca abids as model o ganisms
P e equisi es o being good model o ganisms and also po en ial indica o s include
as knowledge on ca abid axonomy and ecology, as well as ease o collec ing, bu
hese hold mos ly only o no h- empe a e egions (e.g., New 1998). Ca abids a e
axonomically well known, wi h ela i ely s able sys ema ics, and hei ecology has
been widely s udied (Lö ei and Sunde land 1996). Va ia ion in ca abid mo phology,
li e-his o y s a egies and abio ic and bio ic equi emen s a e also ex ensi ely docu-
men ed. We know, o example, many species ha a e specialized o ce ain mois-
u e, empe a u e and shadiness condi ions (Rainio and Niemelä 2003; Niemelä e
al. 2007). Ca abids a e also widely dis ibu ed, om he a c ic and alpine und a o
seasho es, dese s and opical ain o es s, and hey can be common in hese en i on-
men s (Lö ei and Sunde land 1996). Howe e , knowledge abou basic li e-his o y
pa ame e s appea s limi ed o a ew well-s udied species. These pa ame e s include
bi h and dea h a es, popula ion age s uc u e and g ow h a e, esou ce alloca ion
be ween ep oduc ion and g ow h, and he causes and magni ude o a ia ion in
Ma i J. Koi ula / ZooKeys 100: 287–317 (2011)
290
hese. Such pa ame e s a e no only in e es ing bu may appea c ucial o indica o
use (see "Iden i ying and using ca abid indica o s").
The easons o pa icula dis ibu ions, local abundances o beha io al esponses
o ca abids a e gene ally well unde s ood. Ca abids a e in luenced by empe a u e,
mois u e and shade (Thiele 1977), ood quali y and abundance (Lenski 1984; Van
Dijk 1994; Bilde and To 1998; Bilde e al. 2000; Bohan e al. 2001), habi a s uc u e
as e lec ed by he ege a ion (Rykken e al. 1997; Siemann e al. 1998; B ose 2003;
Koi ula e al. 1999; 2003; Taboada e al. 2008), and subs a e sal s, suga s and acidi y
(Me i ee e al. 2001, 2004, 2006; Milius e al. 2006). Mo eo e , seasonal and li e-his-
o y luc ua ions s ongly a ec obse ed abundances and dis ibu ions (Thiele 1977;
Lind o h 1985, 1986; Lö ei and Sunde land 1996). O la gely unknown − hough
o en sugges ed − impo ance a e in a- and in e speci ic in e ac ions, o which compe-
i ion has usually had mino e ec s (Lo eau 1990; Niemelä and Spence 1991; Niemelä
1993a; Cu ie e al. 1996; Ze o B andmay e al. 2004).
In ecological esea ch, bo h landscape and smalle scales appea ele an o ca a-
bids, al hough he o me usually equi es ex ensi e sampling. Ca abids a e no always
conside ed ele an a spa ial scales la ge han a ew hec a es (e.g., Pea ce and Venie
2006). This iew elies on he idea o local popula ions o ‘home anges’ o ca abids
(e.g., den Boe 1990a; Gas on and Blackbu n 1996; Cha ie e al. 1997). Howe e ,
ca abids p edic ably espond o landscape- (he e, a eas la ge han 50 ha) and e en
con inen -le el phenomena (e.g., Henge eld 1987; Ko ze and O’Ha a 2003; Ko ze
e al. 2003). Fo example, ca abids e lec ed isola ion in sou he n Finnish a mlands
(Kinnunen e al. 1996), and esponded o pa ch size and ma ix ype in an u ban land-
scape in Belgium (Gaublomme e al. 2008). The s uc u al he e ogenei y o landscapes
had a iable impac s on di e en ophic g oups o ca abids in Ge many (Pu au e
al. 2005). Mo eo e , ca abid assemblages g adually changed ac oss a o es / a mland
g adien in Sco land (Vanbe gen e al. 2005), and in Canadian pos - i e o es s, log-
ging a iably a ec ed ca abids a he s and le el bu s ongly and p edic ably a he
landscape scale (Koi ula and Spence 2006).
Mos ield s udies on ca abids ha e used pi all aps, which is an easy and cheap
me hod o collec su icien ly la ge samples o allow s a is ical analysis, by acknowledg-
ing ha he ca ch indica es species-speci ic ‘ac i i y densi y’ a he han ue ela i e
abundance (G eenslade 1964). The dominance o one me hod o e o he s in oduces
a knowledge bias. New insigh s would be achie ed by mo e o en applying o he col-
lec ing me hods, such as cap u e-ma k- ecap u e echniques, apping and measu ing
li e bee les, window apping, ee-canopy pes icide sp aying, hand collec ing, and soil
sampling o collec la ae (Su he land 1996).
The ca abid bee le li e a u e e lec s a wide spec um o app oaches o s udy eco-
logical ques ions. Pape s on single species, o al abundance and species ichness a e
common. I he numbe s o collec ed indi iduals a e small, o i gene aliza ions a e e-
qui ed, ca abids a e o en di ided in o unc ional g oups o es he hypo heses pu o -
wa d. These g oups include seasonal abundance peak, ep oduc ion pe iod, diu nal ac-
i i y, body size, wing mo phology (e.g., b achyp e ous/wing-dimo phic/long-winged/
Ca abid bee les as use ul model o ganisms, indica o s, o bo h? 291
lying), ood p e e ences (e.g., p eda o /omni o e/plan -ea e /specialis ), associa ions
wi h habi a openness (e.g., closed ee canopy o ex ensi e ege a ion co e /gene alis /
open phase) and mois u e p e e ences (e.g., d y/mois /we ). Clea ly, species di isions
in o hese g oups in ol e subjec i i y, because many ca ego ies we e o iginally con-
inuous a iables, and may be poo ly known e en in egions wi h a long esea ch adi-
ion. Fligh capabili y in ca abids in No he n and Cen al Eu ope is a good example
o such knowledge gaps (Niemelä e al. 2007). Mo phospecies o highe - han-species
le el app oaches a e a ely applied by ca abidologis s, because di e en species wi hin
a genus a e ecologically di e en and may consequen ly espond di e en ly o he en-
i onmen (Koi ula e al. 2006; Lango and Spence 2006).
Va ious di e si y indices ha e been used on he ca abid ca ch. These include, o
example, a e ac ion (Sande s 1968) and he Shannon-Wiene and Simpson indices
(Magu an 2003; Tó hmé ész and Magu a 2005a). Howe e , di e si y indices may
pe o m inconsis en ly (O’Ha a 2005) and he e o e should no be used as a sole jus i-
ica ion o indica o unc ioning. Ano he obs acle is ha di e si y measu es based on
pi all- ap da a a e p oblema ic because he samples a e biased owa d ac i ely mo -
ing, la ge-sized species (e.g., Mo ill e al. 1990; Lang 2000). As such, hese samples
may ha e li le o do wi h ue assemblage composi ion and s uc u e. The ela ionship
be ween ap samples and ue assemblages is poo ly unde s ood due o he di icul y
in eliably de e mining he la e .
Recen app oaches o desc ibe ca abid assemblage s uc u e include Mean Indi id-
ual Biomass (Szyszko e al. 2000; see "Dominance indica o s"), a ini y indices (Alle-
g o and Sciaky 2003; Tó hmé ész and Magu a 2005b) and indica o alue calcula ions
(IndVal; Du êne and Legend e 1997). A ini y indices aim a emo ing he e ec o
di e ences in species abundances among compa ed habi a ypes while simul aneously
accoun ing o he species’ habi a speci ici y (Magu a e al. 2006a). The IndVal ap-
p oach uses da a collec ed om habi a ypes o in e es , and iden i ies species cha ac-
e is ic o pa icula habi a ypes based on hei abundances and p esences/absences
among all samples (Du êne and Legend e 1997).
e alua ion o ca abids as indica o s
Taxon indica o s
The p esence o a axon indica o e lec s he p esence o a se o o he species, and
i s absence indica es he absence o he en i e se o species (Slobodkin e al. 1980;
Lindenmaye e al. 2000). The unde lying assump ion hus is ha he p esence o
a limi ed subse o all species would indica e he p esence o he comple e se . As
e e y hing canno be measu ed his app oach may sound appealing, bu e idence o
ca abids as axon indica o s is poo . Weak ichness co ela ions wi h ca abids ha e
been demons a ed o spide s (Rush on e al. 1989; Niemelä e al. 1996) and some
o he in e eb a e axa (Duelli and Ob is 1998; Niemelä and Bau 1998). Ba ba o e

Ma i J. Koi ula / ZooKeys 100: 287–317 (2011)
292
al. (2005) ound ha he same s uc u al ea u es o o es s p edic ed bi d, spide and
ca abid ichness in F ance. The u ili y o ichness indica o s becomes e en mo e chal-
lenging a la ge spa ial scales, whe e ichness co ela ions appea o be a biogeog aphic
ule. Species ichness o di e en axa o en co ela e because o he gene al endency
o ichness o inc ease owa d he equa o (Begon e al. 1996); o a na ional-scale in-
e eb a e example, see Väisänen and Heliö aa a (1994).
The axon indica o po en ial o ca abid bee les has no ye been subjec o a se e e
es (sensu Mayo 1997), bu such es s do exis o o he axa. Jonsson and Jonsell
(1999) showed ha s and s uc u e and he ichness o axa bea ing high conse a ion
ele ance (lichens, plan s, wood- o ing ungi and b yophy es) appea ed o be poo a
p io i indica o s o each o he in Swedish bo eal o es s. Likewise, Similä e al. (2006)
ound ha s uc u al cha ac e is ics and plan ichness somewha e lec ed he ichness
o some in e eb a e g oups, bu bee les e y poo ly e lec ed he ichness o o he axa
in Finnish bo eal o es s. Mo eo e , Sæ e sdal e al. (2005) showed ha he deg ee o
o e lap in ichness among six ecological g oups, consis ing o polypo es, b yophy es
and lichens, a ied conside ably om si e o si e in No wegian coni e ous o es s. While
discou aging, hese esul s highligh he impo ance o using mul iple axa in en i on-
men al assessmen s (c . Taylo and Do an 2001; Duelli and Ob is 2003; Paille e al.
2009) and he absu di y o he idea o he exis ence o a single ‘biodi e si y indica o ’.
Conse a ionis s and manage s gene ally ag ee in ha p o ec ing species di e si y
is a p io i y a global and na ional scales. A smalle spa ial scales, howe e , ichness
may appea a misleading conse a ion measu e wi hou conside ing species iden i ies.
Fo example, Koi ula and Spence (2006) showed ha , in ecen ly bu ned Canadian
o es s, logging inc eased he o al ichness o ca abids due o he coloniza ion o gen-
e alis open-a ea associa ed species. Bu simul aneously mos closed- o es species de-
c eased in abundance, he mos d as ic case being he o e en old dec ease o Calosoma
igidum, a ee-canopy ca e pilla hun e (La ochelle and La i iè e 2003). So, a he
ope a ional scale o indi idual o es s ands, should he o es manage adop he mes-
sage ob ained om o al ichness o ha om species equi ing closed o es s?
Keys one indica o s
A keys one indica o is a species, a g oup o species, o a s uc u e ha a ec s i s
en i onmen and he e o e o he species disp opo iona ely s ongly ela i e o i s
abundance (Mills e al. 1993). The lack o a keys one indica o would hus lead o
majo changes in some o he species’ occu ence, abundance and/o dis ibu ion. A
classic example om o es ed en i onmen s is he woodpecke auna (Vi kkala 2006).
These bi ds p oduce nes ing si es o seconda y ca i y-nes e s, a e impo an ec o s
o wood- o ing ungi, and may e en egula e ba k bee le in es a ions, hus bea ing
economic impo ance (Fay e al. 2004). Ca abids ha e in insic biodi e si y alue and
unknown u u e po en ial, and hey can also be conside ed in aluable on an e hical
basis, bu can hey se e as keys one indica o s?
Ca abid bee les as use ul model o ganisms, indica o s, o bo h? 293
E idence on he impo ance o ca abids comes om ag o-ecosys ems, g eenhouses
and labo a o ies. Unde labo a o y condi ions ca abids o age e icien ly on slugs and
eggs, pupae, la ae and adul s o pes insec s (K omp 1999). In he ield, ca abids
indeed p ey on pes in e eb a es, such as slugs, aphids and mi es (e.g., Allen 1979;
Edwa ds e al. 1979; Henge eld 1980a, 1980b; Lu 1987; Sopp e al. 1992; Bohan e
al. 2001). Menalled e al. (1999) manipula ed onion ly (Delia an iqua) pupae using
exclosu es in co n ields and ound a posi i e ela ionship be ween ca abid abundance
and pupal dea h a es. Bu can he a es o o aging in he ield be ecologically and/o
economically impo an ?
Hance (1987) used 1 m2 enclosu es wi h suga bee and na u al densi ies o aphids
eeding on hese plan s, and eleased 0–30 indi iduals o Anchomenus do sale and
Asaphidion la ipes in o hese enclosu es. Such densi ies (up o 30 ind.m-2) a e com-
mon in he ield (Lö ei and Sunde land 1996). In enclosu es wi hou ca abids, he
densi y o aphids inc eased exponen ially. A in e media e ca abid densi ies, he aphid
inc ease was delayed, and a high ca abid densi ies he aphids o en did no inc ease a
all. I is easy o a gue ha his is ecologically and economically impo an , con a y o
some ‘s a is ically signi ican ’ 20–30% abundance changes. While his expe imen can
be c i icized o using un ealis ic, closed minia u e sys ems, i shows ha ca abids ha e
he po en ial o being economically impo an .
Ca abids hus ha e he po en ial, bu lack ield-based e idence, o uly unc-
ioning as keys one indica o s. A e ca abids necessa y o ecosys em unc ioning, and
e en i hey a e, could o he axa eplace hem i hey a e emo ed om an ecosys em?
Cu en ly he e a e no answe s o hese ques ions, bu in many ecosys ems ca abids
a e accompanied by o he abundan gene alis in e eb a es, such as an s, s aphylinid
bee les and spide s (Tu nbull 1973; Bohac 1999). Ca abids a e, on a e age, la ge han
hese h ee, which sugges s a highe ophic le el and pe capi a e ec on, o example,
c op-pes in e eb a es. On he o he hand, ca abids a e o en as ly ou numbe ed o
e en excluded by Fo mica wood an s in Fennoscandian bo eal o es s (e.g., Koi ula e
al. 1999).
Pollu ion indica o s
Pollu ion indica o s e lec human-al e ed abio ic condi ions in he soil, wa e and he
ai (Spelle be g 1994). U ban ecological s udies migh be conside ed in his ca ego y,
wi h he combined ole o e.g. pollu an s, soil compac ion and he ‘hea island’ e ec
(Fo man 2008; Ma zlu e al. 2008). Pollu ion a ec s humans di ec ly, and as such
has been s udied widely o se e al decades using se e al axa, o which lichens may
be he mos amous (Lindenmaye e al. 2000). O he pollu ion indica o s, oo, ha e
been p oposed bu no wi hou p oblems. Fo example, he mollusc Velesunio ambiguus
was long conside ed an excellen indica o o hea y me als in aqua ic sys ems un il
i appea ed ha his species’ up ake o me als did no e lec he ex en o pollu ion
(Lindenmaye e al. 2000).
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294
Ca abids ha e been commonly s udied o e alua e he ecological e ec s o indus y
emissions and ag icul u e chemicals. The below examples demons a e he po en ial
o ca abids o also ac as indica o s o ecologically sus ainable a ming, en i onmen al
eco e y and ‘ecosys em heal h’. The u ili y o ca abids as indica o s in hese cases e-
lies on he inadequa ely es ed assump ion ha o he , o en mo e se e ely h ea ened,
axa simila ly espond o hese pollu an s and chemicals. This issue conce ns he o he
indica o ca ego ies as well.
Se e al case s udies all sugges ha hea y me als in he soil signi ican ly and nega-
i ely a ec ca abids (e.g., E mako 2004; Gongalsky e al. 2004; Belskaya and Zi-
no ie 2007). Mo eo e , cadmium and zink a ec he g ow h and body calo ic alue
o Poecilus cup eus indi iduals (Ma yański e al. 2002). Ca abids ha e also been used
o assess he eco e y o ecosys ems a e pollu ion e en s (e.g., Schwe k e al. 2006;
Cá denas and Hidalgo 2007).
In ag o-ecosys ems, pes icide and e ilize impac s on ca abids ha e been s udied
(e.g., D i schilo and E win 1982; Basedow 1990; K omp 1990; La sen e al. 1996;
Bou assa e al. 2008). Ca abids espond nega i ely o dime hoa e (commonly-used
pes icide) sp ayings bu hei numbe s may eco e wi hin a ew weeks (Huusela-Veis-
ola 1996). Fe ilize and he bicide impac s ha e o en been mino , bu may a ec
ca abids indi ec ly h ough changes in he ege a ion (K omp 1999).
Also cumula i e impac s may appea common. Fo example, he in ensi y o ca -
abid esponse o pollu an s and chemicals depends on addi ional s esso s, such as ood
sca ci y and chemicals. S one e al. (2001) s udied adul s o P e os ichus oblongopunc a-
us a a ch onically pollu ed mining a ea in Poland. They collec ed indi iduals a si es
wi h di e en le els o soil me als and subjec ed hese bee les o ood sho ages and an
insec icide (dime hoa e) in he labo a o y. Ca abid dea h a es, caused by hese s ess-
o s, we e highe he mo e se e ely he collec ing si e had been con amina ed by me als.
To de e mine whe he hese esponses we e gene ically based o esul ed di ec ly om
soil con amina ion, Lagisz and Laskowski (2007) collec ed addi ional indi iduals a
S one e al.‘s (2001) si es, and ea ed a second gene a ion in he labo a o y. These labo-
a o y specimens we e subjec ed o ood sho ages and he same insec icide, and esul s
showed ha he collec ing si e o he pa en indi iduals had no e ec on dea h a es
o he second gene a ion. Thus, he in e ac ion was no gene ically based in his case.
Recen ad ances in ag o-ecosys ems conce n gene-manipula ed (GM) o ansgen-
ic plan s ha can be conside ed ‘gene ic pollu an s’, as e idenced by he hyb idiza ion
o na i e and GM co n in Mexico (Quis and Chapela 2000). GM echniques ha e
been apidly adop ed in o ag icul u e o inc ease he c op plan s’ pes and disease ol-
e ance, yield and/o nu i ional alue, bu manipula ing he gene ic ma e ial o hese
plan s is suspec ed o lead o unwan ed consequences (e.g., Dunwell 1999). Fo ex-
ample, he use o GM plan s migh di ec ly o indi ec ly a ec non- a ge o ganisms,
including ca abids. Non- a ge in e eb a es we e gene ally li le a ec ed by GM co n
and co on, as compa ed wi h non- ansgenic e sions o hese plan s, bu we e mo e
a ec ed by he use o pes icides (Ma ie e al. 2007). Simila ly, GM c ops had a mi-
no e ec on adul ca abids locally (Lopez e al. 2005; Szeke es e al. 2006; Floa e e
Ca abid bee les as use ul model o ganisms, indica o s, o bo h? 295
al. 2007). Howe e , Wal z (2009) summa ized he e ec s o GM c ops on insec s and
epo ed d as ic e ec s on, e.g., bu e ly la al dea h a es. Hence, expe imen s on he
la al de elopmen o seed-ea ing ca abids in GM and con en ional c op ields would
signi ican ly con ibu e o his a ea o esea ch.
Dominance indica o s
Dominance indica o s make up much o he o al biomass o he numbe o indi idu-
als in an a ea o in e es (Lindenmaye e al. 2000) and p edic pa icula ecosys ems o
assemblages. Fo example, ce ain ee species o m much o he biomass and b oadly
e lec habi a ype in o es s. Simila ly, ca abid dominance indica o s should e lec
pa icula habi a ypes, deg ees o dis u bance and ecosys em eco e y, ho -spo s o
a e species o pa icula habi a ypes o conse a ion in e es . The use o ca abids in
his sense has aced ce ain di icul ies ha migh be o e come.
In e eb a es a e seldom used in en i onmen al assessmen s because o he high ex-
pe ise equi ed (Ande sen 1999; bu see Ande sen and Maje 2004). While s ongly
ad oca ed he e (see "Ca abids as model o ganisms"), species-le el app oaches usually e-
qui e conside able in es men s o expe ise, ime and money in o educa ion, sampling
and analysis (Lango and Spence 2006). Hence, in apid biodi e si y assessmen s (e.g.,
Wa d and La i iè e 2004), nume ical o biomass dominance migh be al e na i e op ions.
Niemelä (1993b) showed ha bo eal- o es ca abid assemblages consis o a ew
abundan (easily iden i iable) and se e al sca ce (o en mo e di icul o iden i y) spe-
cies. In hese o es s, ea ly successional phases can be nume ically domina ed by P e -
os ichus nige , while closed phases a e o en domina ed by Cala hus mic op e us (e.g.,
Koi ula e al. 2002). Howe e , as hese species a e gene alis s o o es succession (Nie-
melä e al. 2007) and occu in many o es ypes (Lind o h 1985, 1986), hei p esence
may no indica e aspec s use ul o conse a ion o managemen .
Ca abid body size has been linked o ce ain ecological p ocesses, such as u baniza-
ion and succession (e.g., Magu a e al. 2006b). The Mean Indi idual Biomass (MIB)
app oach equi es only sampling, coun ing, weighing and using a simple equa ion
de eloped by Szyszko e al. (2000). MIB is p edic ed o inc ease along g adual succes-
sional changes in ege a ion ha subsequen ly al e s he ca abid auna, om smalle
open-habi a (Ama a, Bembidion, e c.) o la ge closed- o es (Ca abus, Cych us, e c.)
species (Szyszko e al. 2000). An inc ease in MIB should hus indica e condi ions ap-
p oaching la e successional s ages.
MIB is ad oca ed as an easy ool o policy make s o assess he s a e o he en-
i onmen . The me hod assumes a linea ela ionship be ween MIB and ime since
dis u bance, which seems o hold h ough ea ly successional phases, du ing which he
ca abid auna changes apidly (Szyszko e al. 2000; Koi ula e al. 2002). Howe e ,
a leas in bo eal sp uce o es s he ca abid assemblage s uc u e − and consequen ly
MIB − changes li le be ween 30 and 100 yea s ollowing clea -cu ing (Koi ula e al.
2002; M. Koi ula unpubl.), sugges ing a pla eau in he end. Fo o es s olde han
Ma i J. Koi ula / ZooKeys 100: 287–317 (2011)
302
Assume you a e in e es ed in he impac o a e ilize on meadow biodi e si y, and
you would like o s udy i ca abids espond o he added e ilize as an ea ly wa n-
ing indica o , i.e., be o e i can be de ec ed by in en o ying plan s. You migh ha e a
eason o expec ing some ca abid species o be able o do so (see Me i ee e al. 2006).
You decide o explo e sligh di e ences in assemblage composi ion using pi all aps.
The s udy can be done by sampling, o example, (i) se e al ea ed ( e ilize add-
ed) and un ea ed (no e ilize added; con ol), andomly-assigned sub-plo s wi hin
one o a ew meadows. Such a p o ocol would be sui able o de ec ing small-scale
phenomena, such as a ia ion wi hin meadows; (ii) se e al (say >10) meadows ea ed
wi h di e en le els o he e ilize . This p o ocol migh be ine o assessing h eshold
condi ions by using non-linea eg ession modeling o e alua e, e.g., i he h eshold
o abundance change occu s ea lie o ca abids han o plan s; (iii) mul iple meadow
pai s o which one is ea ed and he o he is no ; o (i ) sepa a e, ea ed and un ea ed
meadows (see, e.g., Unde wood 1997).
Assume ha you end up using he las -men ioned op ion. A con incing demon-
s a ion o you case would equi e a leas he ollowing.
a. Selec meadows ha a e ini ially as simila as possible bu s ill dis inc i e.
b. Es ablish a leas 3–4 ea ed and 3–4 un ea ed meadows o be able o calcula e
means and a iances o bo h. The mo e meadows he be e , as mo e na u al a i-
a ion will be co e ed and he mo e p ecise he es ima e o mean. I possible, sample
be o e and a e he addi ion o he e ilize o be e accoun o ini ial a ia ion
(Unde wood 1992). Conce ning you s udy ques ion, hese meadows (no aps in
hem, i espec i e o how hey a e placed) a e you eplica es: you a e in e es ed in
a phenomenon ha scales o a ia ion be ween meadows.
c. Spa ially dis ibu e you eplica es e enly. They should no o m ea men -speci ic
clus e s.
d. The eplica es should be sepa a e, i.e., unlikely o a ec each o he ecologically.
Sec ions o di e en habi a ypes be ween you s udy meadows help con ince
you colleagues ha he meadows a e indeed ecologically independen om each
o he .
e. Synch onize he sampling, i.e., sample a e e y meadow o e he same pe iod.
. Collec mul iple samples om each meadow (see poin 5 abo e).
g. Sample o e a pe iod long enough o ep esen a i ely collec ca abids, and also o
see i he plan assemblage esponds o he ea men . I he plan s, o any o he
axa o he han ca abids, do no espond o he ea men , you ha e ailed o ind
an ea ly wa ning indica o , wha e e you esul o ca abids. The ollow-up may
easily ake se e al yea s o p oduce use ul in o ma ion.
A lack o p ope eplica ion is su p isingly common in ecology, conside ing he amoun
o li e a u e on his issue. In he abo e example, you migh ha e selec ed only one
ea ed and one un ea ed meadow and se 10 aps in each, pe haps 15–20 m apa o
sample independence (Digweed e al. 1995). Bu you would hen ha e no eplica ion

Ca abid bee les as use ul model o ganisms, indica o s, o bo h? 303
o he ac o o in e es , iz. he addi ion o e ilize , which ope a ed a he meadow
scale. As a solu ion you migh ea each ap as a eplica e in you analysis, bu you
would hen in oduce pseudo- eplica ion because samples om a gi en meadow a e in-
e -dependen h ough ecological in e ac ions be ween he plo s wi h aps (Hu lbe
1984). Likewise, in a labo a o y expe imen wi h wo cages (con ol and ea men ),
you migh conside each indi idual in a cage a eplica e, bu you would ha e di icul y
o con ince o he s ha i was no some cha ac e is ic o he cage ha p oduced he e-
sul . Ano he example is o use spa ially clumped ea men s: he e, clus e s o meadows
wi h simila ea men . Now, unde lying en i onmen al g adien s o local condi ions
could d i e he esul , no necessa ily he e ilize addi ion. Simila ly, you should no
compa e mois Du ch meadows wi h d y Belgian meadows i you aim is o s udy
he e ec o mois u e on ca abids. The only excep ions o no p ope ly eplica ing
ea men s conce n s udies on excep ionally a e (o dange ous) axa, habi a ypes o
phenomena.
Sugges ions o u he esea ch
Ca abidologis s ha e much o con ibu e o indica o s udies. Fi s o all, he esea che
mus adop he conse a ionis s’ iew on wha is an indica o . Second, he esea ch mus
be p ope ly ca ied ou (see "Indica o hun : common sense e isi ed"). Thi d, i he
esul s sugges ha ca abids eliably e lec a ia ion o high conse a ion ele ance, he
esea che should desc ibe (i) he a iables o he assemblage ha bes e lec his a ia-
ion, (ii) he s udy condi ions (con ex ), (iii) he p ecision and accu acy o ca abids in
e lec ing his a ia ion based on, e.g., pe cen o e lap, peak di e ence and con idence in-
e als, and (i ) he species o condi ions ha could no be easily obse ed wi hou using
ca abids. Fou h, as he ca abid ecological li e a u e is as (see "Ca abids as model o gan-
isms"), and o inc ease he powe o analyses, ca abidologis s should mo e on om wo-
ailed null hypo hesis es ing owa d ou inely o mula ing explici , di ec ional hypo h-
eses − no jus in indica o esea ch bu in modeling biological phenomena in gene al.
The a ious indica o ca ego ies ("E alua ion o ca abids as indica o s") p o ide
po en ial o de eloping powe ul managemen and conse a ion ools. Taxon, pollu-
ion, en i onmen al and managemen indica o s migh be ound by mo ing on om
applying o al ichness owa d using single-species abundances o hei mo phological/
gene ic a ia ion, g oups o specialis s, unc ional g oups, o s uc u al cha ac e is ics o
assemblages (as e lec ed by, e.g., a ini y indices; Magu a e al. 2006a; Dé i e al. 2010).
A di e en way o app oach he indica o issue migh be o s udy i he p esence o ce -
ain species would indica e he lack o conse a ion alues a a gi en si e (‘nega i e indi-
ca o s’). Keys one indica o s, on he o he hand, migh be ound h ough expe imen s
wi h mul iple ophic le els and manipula ed abundances o po en ial compe i o s.
Ea ly wa ning indica o s a e endy because o hei po en ial in assessing la ge-
scale en i onmen al al e a ions, bu he concep could also be examined h ough eco-
logical in e ac ions and a smalle spa ial scales. Fo example, esponses o ca abids o
Ma i J. Koi ula / ZooKeys 100: 287–317 (2011)
304
changes in combina ions o empe a u e, soil chemis y and/o expansion o u ban a -
eas may be ui ul (see Knowl on and G aham 2010). The mic o scale appea s equally
p omising: ca abids a e physiologically ex emely sensi i e o suga s, sal s, amino acids,
pH and empe a u e (Me i ee e al. 2004, 2005, 2008; Mus e al. 2006). Thus, physi-
ological al e a ions due o changes in hese ac o s migh unc ion as ea ly wa ning
signals o cu en ly mino en i onmen al a ia ion, such ha canno be obse ed by
isual inspec ion o he en i onmen . Some o hese aspec s could also be explo ed us-
ing a ini y indices.
Conclusions
No wo species can p ecisely e lec each o he , and one mus be p epa ed o unce ain y
and e o when using an indica o . The compe i i e exclusion p inciple (Ha din 1960)
pos ula es ha membe s o a guild mus be ecologically a leas sligh ly di e en om
one ano he o co-occu in e ms o e.g. popula ion dynamics, habi a and o aging e-
qui emen s, aspec s o ep oduc ion and en i onmen al g ain size. De ining accep able
imp ecision is a poli ical ques ion, bu esea ch can only de e mine con idence limi s.
Indica o s a e assessmen ools in ended o be used in si ua ions when habi a s
and species a e los , o condi ions al e ed. Because humans will con inue o u ilizing
he en i onmen , some dec ease in habi a a ea and, a some loca ions, quali y is in-
e i able: biology compe es wi h economics and social issues in policy. De ec ing a eas
o si es o high conse a ion alue assis s in de ining conse a ion p io i ies. S ill, he
conse a ionis may ha e o ask whe he he /his s a is ically signi ican esul is bio-
logically o economically impo an , o whe he a non-signi ican esul is i ele an .
Fo example, i h ea ened o a e species a e in ol ed, he p ecau iona y p inciple
should apply (e.g., Haag and Kaupenjohann 2001): i a pa icula en i onmen al im-
pac is unde e alua ion, s a is ical non-signi icance should no be conside ed equal o
no e ec o ze o di e ence (McGa ey 2007), and an indica o should be allowed o
p o ide occasional ‘ alse posi i es’. The la e is impo an in p o ec ing me apopula-
ions, wi h bo h occupied and p esen ly unoccupied habi a pa ches being necessa y
o he long- e m pe sis ence o an o ganism (Hanski 1999). Likewise, wi hin a gi en
a ea, local popula ions o ca abids may di e in hei ep oduc i e capaci y and o he
quali ies, and consequen ly luc ua e pa ly independen ly (e.g., den Boe 2002).
To be use ul in conse a ion, an indica o mus ha e high and consis en p edic-
i e powe ha ela es o pa icula condi ions and/o a e species. We s ill lack he
i s clea -cu case showing ca abids o eliably p edic en i ies o high conse a ion
and managemen in e es . To ill his gap, (a) knowledge on he ela ionship be ween
ca abids and o he axa mus be g ea ly inc eased, and (b) s ic es s mus be applied
o e alua e indica o unc ioning as ou lined abo e. We should soon be able o de ine a
‘niche’ o ca abids in en i onmen al assessmen s. Cases o ca abids ul illing c i e ia o
be use ul indica o s will possibly be documen ed in he nea u u e, bu he indica o
unc ioning o pa icula axa may always emain con ex speci ic.
Ca abid bee les as use ul model o ganisms, indica o s, o bo h? 305
Acknowledgemen s
I would like o hank he o ganize s o he XIV ECM o in i ing me o he cong ess
as a plena y speake ; his pape is based on my cong ess p esen a ion. Bob O’Ha a,
Hanna Koi ula, Johan Ko ze and h ee anonymous e iewe s p o ided cons uc i e
commen s o an ea lie e sion o his pape .
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