Using ants as bioindicators in land management: simplifying assessment of ant community responses potx

Journal of
A
pplied
Ecology 2002
39, 8– 17
Using ants as
bioindicators
in
land
management:
simplifying assessment
of ant
community
responses
ALAN N.
ANDERSEN*, BENJAMIN
D.
HOFFMANN*
,
WARREN
J.
MÜLLER†
AND
ANTHONY
D.
GRIFFITHS*
‡
*Tropical Savannas Cooperative Research Centre, Division of Sustainable Ecosystems,
CSIRO
Tropical
Ecosystems

Research Centre, PMB 44 Winnellie, NT 0822, Australia; and
†CSIRO
Mathematical and
Information
Sciences
,
GPO Box 664, Canberra, ACT 2601,
A
ustr
alia
Summary
1. The indicator qualities of terrestrial
invertebrates
are widely recognized in
the
context of detecting ecological change associated with human land-use. However, the
use
of terrestrial
invertebrates
as
bioindicators
remains more a topic of scientific
discourse
than a part of
land-management
practice, largely because their
inordinate
n
umbers
,

taxonomic challenges and general
unfamiliarity
make
invertebrates
too
intimida
ting
for most
land-management
agencies. Terrestrial
invertebrates
will not be
widely
adopted
as
bioindicators
in land
management
until simple and efficient
protocols have
been
developed that meet the needs of land
mana
gers
.
2. In
Australia,
ants are one group of terrestrial insects that has been
commonl
y

adopted as
bioindicators
in land
management,
and this study examined the reliability
of
a simplified ant assessment protocol designed to be within the capacity of a wide
r
ange
of land
mana
gers
.
3. Ants had previously been surveyed intensively as part of a comprehensive
assessment
of biodiversity responses to SO
2
emissions from a large copper and lead smelter at
Mt
Isa in the
Australian
semi-arid tropics. This intensive ant survey yielded 174 species
from
24 genera, and revealed seven key
patterns
of ant community structure and
composition
in relation to
habitat
and SO

2
levels.
4. We tested the extent to which a greatly simplified ant assessment was able
to
reproduce these results. Our simplified assessment was based on ant ‘bycatch’
from
bucket-sized (20-litre) pitfall traps used to sample vertebrates as part of the
br
oader
biodiversity survey. We also greatly simplified the sorting of ant morphospecies
b
y
considering only large (using a threshold of 4 mm) species, and
w
e
reduced sorting time
b
y considering only the presence or absence of species at each site. In this manner, the
inclusion
of ants in the assessment process required less than 10% of the effort
demanded by
the
intensive ant
surv
e
y
.
5. Our simplified protocol
reproduced
virtually all the key findings of the

intensi
v
e
survey. This puts effective ant
monitoring
within the capacity of a wide range of
land
mana
gers
.
Key-words:
environmental
assessment, land-use impacts,
monitoring,
sampling
protocols,
SO
2
Journal of Applied Ecology (2002) 39, 8– 17
© 2002
British
Ecological
Society
Correspondence:
Alan Andersen, Tropical Savannas
Cooper
-
ative Research Centre, Division of Sustainable
Ecosystems
,

CSIRO Tropical Ecosystems Research Centre,
PMB 44
Win-
nellie, NT 0822, Australia (e-mail
Alan.Andersen@csi r
o
.au).
‡Present address: Key Centre for Tropical Wildlife
Mana
ge-
ment,
Northern
Territory University, Darwin, NT 0909,
A
ustr
alia.
Intr
oduction
The indicator qualities of terrestrial
invertebrates
ar
e
widely recognized in the context of detecting
ecolo
gical
change associated with human land use
(R
osenber
g,
Danks & Lehmkuhl 1986). This

contrasts
with the
use
of
particular

in
v
erte
bra
te
groups as indicators of
gener
al
9
Simplified
ant
assessment
© 2002
British
Ecological
Society
,
Journal of
A
pplied
Ecology, 39
,
8–17
diversity

pa
tterns
(Pearson
&
Cassola
1992;
Kremen
1994), which has been widely disputed (Lawton et al.
1998; Kotze & Samways 1999).
Invertebrates
make
good
indic
- ators of ecological condition because they
are
highl
y diverse and functionally
important,
can
integrate
a
variety of ecological processes, are
sensitive to
envir
on-
mental change, and are easily
sampled (Greenslade & Greenslade 1984; Brown
1997; McGeoch 1998).
Despite these qualities, however, the use of
terr

estrial
invertebrates
as
bioindicators
remains more
a topic
of
scientific discourse than a part of
land-
mana
gement
practice. With few exceptions,
invertebrates
are
r
ou-
tinely ignored in land
monitoring
and assessment
pr
o-
grammes, largely
because their
inordinate
n
umbers
,
taxonomic
challenges and general
unfamiliarity

ar
e
too
intimidating
for most
land-management
a
gencies
(New 1996). This
contrasts
with the situation
in
aquatic systems, where relatively simple protocols f
o
r
assessing
macroinvertebrates
have been widely
a
pplied
in studies of river health (Hellawell 1978;
Norris & Norris 1995). Terrestrial insects and
other
in
v
erte-
brates will not be widely adopted as
bioindicators in
land
management

until simple and
efficient
pr
otocols
have been developed that meet the
needs of land
man-
agers (Andersen 1999).
In
Australia,
ants are one group of terrestrial
insects
that has been commonly adopted as
bioindicators in
land
management
(Majer 1983; Andersen 1997a).
In
particular,
ants have frequently been used by the
min-
ing industry as indicators of
restoration
success
(Majer
1984; Andersen 1997b). Ant species richness and
com-
position show predictable
colonization patterns
a

t
mine sites undergoing
rehabilitation
(Andersen 1993;
Majer & Nichols 1998; Bisevac & Majer 1999),
with
these
patterns
reflecting those of other
in
v
erte
bra
t
e
groups (Majer 1983; Andersen 1997b) and key
eco-
system processes (Andersen & Sparling 1997).
Mor
e
recently, ants have been used as indicators of
of
f-site
mining impacts (Read 1996;
Hoffmann,
Griffiths &
Andersen 2000) and for other land uses such as
f
o
r

estry
(York 1994;
Vanderwoude,
Andersen &
House 1997) and
pastoralism
(Landsberg,
Morton
&
James 1999;
Hoffmann
2000; Read & Andersen
2000). However,
in
virtually all these cases ant surveys
have involved
spe-
cialist
entomologists,
and
comprehensive ant
surv
eys
remain largely beyond the
capacity of most
envir
on-
mental
pr
actitioners

.
In any sampling
programme
there will inevitably
be
a trade-off between simplicity on one hand, and
r
eli-
ability on the other. When
endeavouring
to make
insect
surveys more accessible to land managers, there
is
no
point in developing simplified sampling
pr
otocols
if reliability is seriously
compromised.
This
stud
y examined the reliability of a simplified ant
assessment
protocol designed to be within the capacity
of a
wide
range of land
mana
gers

.
The study was conducted as part of a
compr
ehensi
v
e
assessment of biodiversity responses to SO
2
emissions
from a large copper and lead smelter at Mt Isa in
the
Table 1. Key findings of a comprehensive ant
sampling
programme
conducted as part of an assessment of
the
biodiversity impacts of SO
2
emissions from Mt Isa
mine
(Hoffmann,
Griffiths & Andersen 2000)
1. The two regionally
dominant
landforms (rocky
ridges
and alluvial plains)
supported
distinct ant
faunas.

2. Ant
abundance
declined with increasing levels of
SO
2
.
3. Species richness declined with increasing levels of
SO
2
.
4. Species composition varied systematically
with
increasing levels of
SO
2
.
5. Several common species showed clear
abundance
patterns
in relation to SO
2
, with some decreasing
and
others
incr
easing.
6. Ant functional group composition (
sensu
Andersen 1995)
showed relatively little change in relation to

SO
2
.
7. Ant responses varied according to
bio
geo
gr
a
phical
affinity, with the overall
abundance
of
Eyrean
(arid-adapted)
taxa increasing in relation to
SO
2
,
Torresian (tropical) taxa decreasing, and widespread
taxa
showing no
change
.
Australian
semi-arid tropics. Vegetation had been
dr
a-
matically affected immediately downwind from
the
smelter, and the influence of the smelter could

be
detected for at least 15 km (Griffiths 1998). A key
ques-
tion was whether or not faunal biodiversity was
sim-
ilarly affected. Routine vertebrate sampling indicated
tha
t
bird and reptile assemblages were significantly
influ-
enced by high SO
2
levels (up to 5 km from the
smelter),
with mammals providing too few records for
sta
tistical
treatment
(Griffiths 1998). A survey of ants,
on the
other
hand, revealed an effect of the smelter for
up to 35
km
(Hoffmann,
Griffiths & Andersen 2000).
Ants
w
e
r

e
therefore a far more sensitive indicator of
the effects
of
the smelter on faunal integrity than
v
erte
bra
tes
.
The ant survey was based on catches in
small
(4·5 cm) pitfall traps that were partly filled with
pr
e-
servative, which is the most widely used technique f
o
r
obtaining

quantitative
assessments of ant
communities
in open habitats (Andersen
1991;
Bestelmeyer &
W
iens
1996;
Fisher 1999). The survey yielded 174 species

from
24 genera, and revealed seven key
patterns
of ant
com-
munity structure and composition in relation to
ha
bi-
tat and SO
2
(Table 1). Our simplified protocol used
the
ant ‘bycatch’ from the bucket-sized pitfall traps used
to
capture
vertebrates,
which are routinely used in
wildlife surveys. We tested the extent to which our
simplified
ant assessment was sufficient to reproduce
the
se
v
e
n
key results of the intensive ant sampling
pr
o
g
r

amme
.
Methods
   
     
Mt Isa
is
located in
north-western
Queensland
(29°43′S
139°27′E),
Australia,
with its 400-mm average
ann
ual
rainfall being heavily
concentrated
within a
summer
wet season.
Temperatures
are high
year-round, with
mean monthly maxima ranging from about 25 °
C
(July) to 38 °C
(November),
and minima 10
°C

to
10
A.N.
Ander
sen
et
al.
© 2002
British
Ecological
Society
,
Journal of
A
pplied
Ecology, 39
,
8–17
24 °C (Bureau of
Meteorology,
Mt Isa). The
major
landforms in the region are erosional Tertiary
surfaces
with skeletal soils, rock
(sandstone,
shale and
quart-
zite)
outcrops

and alluvial plains. The
pr
edominant
vegetation is low open woodland
dominated
by
species of Eucalyptus, Acacia and Atalaya, with the
gr
ound-
layer
dominated
by hummock grass (Triodia
spp.)
on
skeletal soils and tussock grasses (species of
Aristida
and Cenchrus) on alluvial
loams
.
         
      
Biodiversity sampling at Mt Isa was stratified
accord-
ing to four SO
2
zones arranged along the direction
of
prevailing winds:
background
(soil sulphate levels

1– 5 p.p.m., 15 – 30 km upwind from the smelter),
lo
w
(10 – 30 p.p.m., 30 – 35 km downwind), medium (30
–
70 p.p.m., 7 –15 km downwind) and high (70 –120
p
.
p
.m.,
3 – 5 km downwind) (Griffiths 1998). The intensive
ant
survey was conducted at 40 sites, comprising four
r
ock
y ridge and four alluvial plain sites at each of the
lo
w
,
medium and high SO
2
zones, and eight sites from
each
habitat
in the
background
zone
(Hoffmann,
Griffiths & Andersen 2000). Ants were sampled using
4·5-cm diameter pitfall traps partly filled with

ethylene
gl
y
col
as a preservative. A 5
×
3 grid of
traps with
10-m
spac- ing was established at each site,
and operated f
or
48 h. All ants falling into traps were
sorted to species
,
iden- tified and
en
umer
a
ted.
Vertebrate pitfall traps (20-litre buckets,
28-cm
diameter) were installed at 14, 14, 21 and 16
sites
,
respectively, within the
background,
low, medium
and
high SO

2
zones,
distributed
amongst the three
major
habitat
types as follows: rocky ridges, 23 sites;
r
ock
y
plains, 20 sites; alluvial plains, 22 sites (Table 2).
These
sites included all those used in the intensive ant
surv
ey
,
except for eight from the
background
zone.
At
each
site, four pitfall traps (28-cm diameter plastic
b
uck
ets),
each with 10 m of drift fencing (height 30 cm),
w
e
r
e

randomly located within a 100
×
100-m plot.
Our
sim- plified protocol therefore considered ants from 220
(large) traps
distributed
across 65 sites,
compar
ed
with 600 (small) traps from 40 sites for the
intensi
v
e
ant survey. Ants were collected from vertebrate
tr
a
ps
early in the morning and late in the
afternoon
during 5
consecutive days between late October and
ear
l
y
December 1997. This was done within 2 weeks of
the
intensive ant survey. In addition to simplified
sampling
(i.e. using the ant bycatch from routine v

erte
bra
te
traps), we also greatly simplified the sorting
of
specimens in the
laboratory
by considering only
lar
ge
species. A 4-mm total length threshold was used
to
designate genera and species groups to
be
considered.
The taxa we considered were
Anoc
hetus
,
Bothroponera, Leptogenys,
Odontomac
hus
,
Rhytidoponera, Calomyrmex, Camponotus,
Opisthopsis
and Polyrhachis (i.e. all species within these
gener
a),
as well as the diversus species group of
Mer

anoplus
,
the mayri and purpureus groups of Iridomyrmex,
and
the bagoti and aeneovirens groups of
Melophorus
(nomenclature
follows
Andersen 2000).
The use
of
higher-level taxa
rather than a
strict size
criterion
avoided
potential
confusion caused
by
polymorphic
or
otherwise
variably sized
species in which
some
speci-
mens
fall below but
others are above
the

thr
eshold.
Sorting time was
further reduced
by considering
onl
y the presence
or absence of
species at each
site,
r
a
ther
than
their
abundance.
We did not
quantify it, but
esti-
mated that
our simplified
protocol required
less
than
10% of the
laboratory
time.
This was despite
the
sim-

plified
protocol
covering more
sites
.










was used to
analyse
abundance
data
in the
inten-
sive
ant study
(Hoffmann,
Griffiths &
Andersen 2000),
but an
alternative
analytical
strategy was

needed f
o
r
the
species by site presence/absence matrix from
our
simplified
protocol.
Each species had a binary
r
esponse
at each site, producing a number of
occupied
sites
out of a total possible number of
sites for
each
zone
×
habitat combination.
Our
anal
ytical

str
a
tegy
was to fit generalized linear
models
(GLM)

with bino- mial error and logit link
(Dobson 1990). These ana- lyses give rise to analysis
of
de
viance

tables.
When the residual deviance is
greater
than

one
,
extra-binomial
variation may be
present and
the
deviance ratios are
approximate
F-
ratios and can
be
tested for significance in a manner
similar to
F
-r
a
tios
in



.
When the residual
deviance is less than
or
equal to one, binomial
variation is assumed
and
testing for significance
is based on the deviance f
or
each term being
approxim- ately
distributed
as
a
chi-squared variate.
The outputs of such analyses
ar
e
lists of factors with
their deviances or deviance
r
a
tios
,
and their level of
significance. For significant
ter
ms

we provided
adjusted means and
standard
errors
where
appropriate.
The means were the
a
v
er
a
ge
proportions
of sites occupied by individual species
for all species in the
model.
Three sets of analyses were performed, fitting
indi-
vidual species, functional groups (Andersen
1995)
and
groups based on
biogeographical
affinities
(Andersen
2000) as factors, respectively. Five functional groups
w
e
r
e

common enough for analysis:
Dominant
Dolichoderinae
(species of Iridomyrmex),
Subordinate Camponotini
(primarily species of
Camponotus and
P
o
l
yrhac
his
),
Hot Climate
Specialists (species of Melophorus
and
Meranoplus),
Opportunists
(primarily species of
Rh
yti-
doponera) and Specialist
Predators
(primarily
species
of
Bothroponera and Leptogenys). Similarly,
three
bio-
geographical groups, Eyrean, Torresian and

widespr
ead,
were common enough for analysis.
Analyses were
also
conducted on the eight
individual species that
w
e
r
e
recorded from at least
15
sites
.
Patterns of species composition in relation to
ha
bita
t
and SO
2
were explored by
multivariate
analysis,
as
was the case for results from the
intensive
surv
ey
(Hoffmann,

Griffiths
&
Andersen
2000). Site species
da
ta
were combined within
habitat
types, and a
similarity
1
1
S
i
m
p
l
i
f
i
e
d

a
n
t

a
s
s

e
s
s
m
e
n
t
©

2
0
0
2

B
r
i
t
i
s
h
E
c
o
l
o
g
i
c
a

l

S
o
c
i
e
t
y
,

J
o
u
r
n
a
l

o
f

A
p
p
l
i
e
d

E
c
o
l
o
g
y
,

3
9
,
8
–
1
7
Table 2. Records of ant species across SO
2
zones and
habitat
type (RR, rocky ridge; RP, rocky plain; AP, alluvial plain). Data are numbers of sites at which species were recorded. Species codes follow
Hof
fmann,
Griffiths & Andersen (2000) (those not recorded by
Hoffmann,
Griffiths & Andersen 2000 are indicated by an asterisk). The functional group (FG; DD,
Dominant Dolichoderinae;
HCS, Hot
Climate
Specialist;

OPP,
Opportunist;
SC,
Subordinate Camponotini;
SP, Specialist
Predator)
and
biogeographical
affinity (BIOG; E, Eyrean; T, Torresian; W, widespread) of each species is also
giv
e
n
SO
2
zone
High Medium Low
Background
T
otal
Ha
bita
t
No.
sites
FG
BIOG
RR
7
RP
3

AP
6
RR
6
RP
8
AP
7
RR
5
RP
5
AP
4
RR
5
RP
4
AP
5
RR
23
RP
20
AP
22
Anochetus sp. C (armstrongi
gp)*
SP
T

1 1
Bothroponera sp. B (excavata
gp) SP
T
2 2 4
Leptogenys
adlerzi
SP
T
1 1 1 1 2 2
Odontomachus sp. A (ruficeps
gp)
OPP
T
1 1 2 1 1 1 4 2 1
Rhytidoponera
?
metallica
*
OPP
W
1 1
Rhytidoponera sp. nr.
r
eticulata
O
PP
T
1 1 1 3 2 2 4 2
Rhytidoponera sp. nr.

cornuta
O
PP
T
1 1 3 1 4 2 2 1 2 4 9
Rhytidoponera sp. nr.
rufithor
ax
OPP
E
7 1 4 3 5 4 4 2 2 4 5 16 12 13
Rhytidoponera sp. C (convexa
gp)
OPP
E
3 3 6
Meranoplus sp. C (diversus
gp)
HCS
E
1 1
Meranoplus sp. H (diversus
gp)
HCS
E
1 1
Iridomyrmex sp. nr.
mayri
DD
E

2 1 3 3 2 3 2 2 10 4
Iridomyrmex sanguineus
DD
E
2 1 1 1 1 1 1 3 2 3
Calomyrmex ?cyanea
SC
T
1 1 1 1 1 1
Camponotus
dr
omas
SC
E
1 1
Camponotus sp. A (denticulatus
gp)
SC
E
3 1 4 2 4 4 1 1 6 5 9
Camponotus fieldae
S
C
T
2 1 1 4 5 3 4 4 1 2 1 12 11 5
Camponotus sp. C (discors
gp)
SC W
1 2 2 1 2 2 6
Camponotus sp. D (novaehollandiae

gp)
SC
T
5 1 1 3 4 1 11 4
Camponotus sp. E (claripes
gp)
SC W
1 1 1 1
Camponotus sp. F (subnitidus g
p
)
S
C
E
2 2 3 1 2 1 1 1 1 1 4 5 6
Camponotus sp. H (sponsorum
gp)
SC
E
1 1 2 2 2
Camponotus sp. K (novaehollandiae
gp)*
SC
T
1 1 1 1
Camponotus sp. L (rubiginosus
gp)*
SC W
1 1 2
Camponotus sp. M (rubiginosus

gp)*
SC W
1 1
Camponotus sp. O (claripes
gp)*
SC W
1 1 1 1
Camponotus sp. P (rubiginosus
gp)*
SC W
1 1
Camponotus sp. Q (discors
gp)*
SC W
5 1 4 3 3 1 1 2 1 1 1 3 10 7 9
Melophorus bag
oti
HCS
E
1 3 2 2 2 6
Melophorus sp. AK (aeneovirens
gp)
HCS
E
1 1
Opisthopsis haddoni
SC
T
1 1 1 3 1 5
Opisthopsis ?rufoniger

SC
T
1 1
Opisthopsis
rufithor
ax
S
C
T
1 1 1 1 1 1
Table 2. continued
.
SO
2
zone
High Medium
Lo
w
Backgr
ound
T
otal
Ha
bita
t
No.
sites
RR
7
RP

3
AP
6
RR
6
RP
8
AP
7
RR
5
RP
5
AP
4
RR
5
RP
4
AP
5
RR
23
RP
20
AP
22
FG
BIOG
Polyrhachis inconspicua

Polyrhachis
pr
ometheus
*
Polyrhachis senilis
Polyrhachis sp. A (schwiedlandi
gp)
Polyrhachis sp. B (gravis
gp)
Polyrhachis sp. I (ammon
gp)*
Polyrhachis sp. J (ammon
gp)*
Polyrhachis sp. K (gab
gp)*
Total no.
r
ecords
Total no. species
Mean no. species
SC
S
C
S
C
SC
SC
SC
SC
SC

T
T
T
E
T
T
T
T
1 2 1 1
1
2 2
2
3 3 3
3
1 1 2
1
1
2
1
3
1
4
4
1
3
3
2
42
1 2
2

1 1
31 2 1
1
30
17
6·0
1
99
28
4·5
32
11
4·6
10
8
3·3
21
10
3·5
26
14
4·3
34
17
4·3
25
12
3·6
21
11

4·2
30
17
6·0
23
16
5·8
26
15
5·2
22
15
5·5
105
23
4·6
96
28
4·8
12
A.N.
Ander
sen
et
al.
© 2002
British
Ecological
Society
,

Journal of
A
pplied
Ecology, 39
,
8–17
matrix of
habitat
type/SO
2
zone
combinations
was
con-
structed using the Jaccard index, based on
pr
esence/
absence data for all species.
Habitat
type/SO
2
zone
combinations
were then
ordinated
using
semi-str
ong
hybrid
multidimensional

scaling
(SSH option of
the
PATN software package; Belbin
1994).
Results
           
        
A total of 41 species from 12 genera was recorded
b
y
our simplified
protocol,
with Camponotus (14 species)
and Polyrhachis (eight) collectively
contributing
half
of
all species (Table 2). Twelve (29%) species were
not
among the 174 species recorded during the
intensi
v
e
ant survey of
Hoffmann,
Griffiths & Andersen (2000).
This high
proportion
can be explained by the

gr
ea
ter
efficiency
of drift
fences
in capturing
uncommon
species
.
We did not consider
abundance
per se,
because
w
e
considered only presence/absence data.
However,
the
occurrence of species across sites can
be used as
an
abundance surrogate.
Considering all
species,
mean
occurrence decreased significantly
(deviance =
9·63,
d.f. = 3, P = 0·02) with increasing

levels of SO
2
,
and
mean site species richness showed
a similar
pattern,
although
this was not quite
statistically
significant
(P = 0·07, one-way


;
Fig.
1). Individual species exhibited a wide range of
responses in relation to
SO
2
(Fig. 2). Three of the
eight most common species showed statistically
significant responses (Table
3),
with the most marked
being shown by Camponotus
sp
.
A (denticulatus
group), which occurred primarily

a
t
higher SO
2
zones (Fig. 2d). Four of these eight species showed
significant
habitat
effects (Table 3). The
most
marked
was for Camponotus sp. D (no
v
aehollandiae
group),
which occurred primarily at rocky ridge
sites
and
was not recorded at all in alluvial plain
ha
bita
t
(Table
2).
The functional group–zone
interaction
was not sig-
nificant (deviance ratio =
1·51,
d.f. = 12,396, P > 0·05),
indicating that functional group composition was

r
el-
atively uniform across SO
2
zones. There was a
tendency
for specialist
predators
to favour low levels
of SO
2
(the
nine records occurred exclusively in the
low or
back-
ground zones; Table 2), but their
numbers were too
lo
w
to influence the overall analysis.
In
contrast,
the
bio-
geographical group–zone
interaction
was highly sig- nificant (deviance ratio =
4·57,
d.f. = 6,418, P < 0·001). The mean occurrence of
widespread species was

r
ela
t-
ively
constant,
but the
occurrence of Torresian species declined
systematically in relation to SO
2
, and
Eyrean
taxa
showed a curvilinear response (Fig.
3).
     
          
Multivariate ordination
showed strong
separation of
habitats according to species
composition,
with
r
ock
y
ridge and alluvial plain habitats at the two
e
xtr
emes
,

Occurrence
Occurrence
Richness
13
Simplified
ant
assessment
0·25
0·2
0·15
0·1
0·05
Occurrence Richness
8
6
4
2
0
0
H M L B
SO
2
zone
Fig. 1. Mean (+ SE) site occurrence and species richness of species at high (H), medium (M), low (L) and
background
(B)
SO
2
zones. A mean occurrence of 0·1 means that on average each species occupied 10% of sites. Only those species occurring at >
2 sites (n = 26) were considered for

occurr
ence
.
0·4
0·3
0·2
0·1
0
(a) Rhytidoponera sp. nr. cornuta
H M L
B
0·8
0·6
0·4
0·2
0
(b) Rhytidoponera sp. nr. ru
f
i
t
horax
H M L
B
0·4
0·3
0·2
0·1
0
(c) Iridomyrmex sp. nr. mayri
H M L

B
0·5
0·4
0·3
0·2
0·1
0
(d) Camponotus sp. A (denticulatus gp)
H M L
B
0·8
0·6
0·4
0·2
0
(e) Camponotus fieldae
H M L
B
0·4
0·3
0·2
0·1
0
(f) Camponotus sp. D (novaehollandiae gp)
H M L
B
0·5
0·4
0·3
0·2

0·1
0
(f) Camponotus sp. F (subnitidus gp)
H M L
B
0·8
0·6
0·4
0·2
0
SO
2
zone
(g) Camponotus sp. Q (discors gp)
H M L
B
Fig. 2. Occurrence
(proportion
of sites occupied) of common species at high (H), medium (M), low (L) and
background (B)
SO
2
zones
.
Table 3. Results of GLM tests of the effects of
habitat
type and SO
2
zone on the occurrence of the eight most common species
(those recorded from at least 15 sites). Data are P-values, with significant values indicated in

bold
Habitat type
SO
2
zone
Rhytidoponera sp. nr.
cornuta
0·02
0·08
Rhytidoponera sp. nr
rufithor
ax
0·74
0·16
Iridomyrmex sp. nr.
mayri
0·01
0·63
Camponotus sp. A (denticulatus
gp)
0·41
0·001
Camponotus fieldae
0·05
0·02
Camponotus sp. D (novaehollandiae
gp)
0·000
0·05
Camponotus sp. F (subnitidus

gp)
0·56
0·15
Camponotus sp. Q (discors
gp)
0·97
0·23
© 2002
British
Ecological
Society
,
Journal of
A
pplied
Ecology, 39
,
8–17
and rocky plains
intermediate
(Fig. 4). This was
sup-
ported by a highly significant
species–habitat inter-
action in GLM (deviance =
174·84,
d.f. = 80, P <
0·001). Similarly, SO
2
zones were also clearly evident

in
ordination
space (Fig. 4), and this was
supported
by
a
highly significant species–zone
interaction
in
GLM
(deviance = 222·18, d.f. = 120, P < 0·001).
Discussion
               
       
The intensive ant survey at Mt Isa, yielding 174 species
,
documented
seven clear responses of ant
communities
to variation in
habitat
and SO
2
(Table 1). Our
simplified
Occurrence
14
A.N.
Ander
sen

et
al.
0·25
0·2
0·15
Eyrean
T
orresian
0·1
0·05
0
H M L
B
SO
2
zone
Fig. 3. Mean (+ SE) occurrence
(proportion
of sites occupied) of eyrean and torresian
biogeographical
groups at high
(H),
medium (M), low (L) and
background
(B) SO
2
zones
.
1·5
1

Axis 2
Species composition varied with
SO
2
Multivariate
analysis of our results showed
clear
–1·5 –1
–
0·5
0·5
0
–
0·5
0 0·5
1
Axis 1
1·5
position, including distinguishing between low
and
background
zones
.
Several common species showed clear abundance
–1
–
1·5
stress = 0·2
The species commonly recorded by our
simplified

protocol showed a wide range of responses to
SO
2
.
© 2002
British
Ecological
Society
,
Journal of
A
pplied
Ecology, 39
,
8–17
Fig. 4.
Multivariate ordination
based on occurrence of
ant
species from rocky ridge (triangles), rocky plain (circles)
and
alluvial plain (squares)
habitats,
located in
background
(open
symbols), low (lightly shaded), medium (heavily
shaded)
and
high (closed) SO

2
zones
.
ant assessment protocol utilized the ant bycatch
from
routine vertebrate pitfall traps, with analysis
r
estricted
to the occurrence of larger species
.
It recorded 41
species
,
and required less than 10% of the effort
demanded
b
y the intensive ant sampling
programme.
How well did
it
reproduce the seven results of the
intensive ant
surv
ey?
Rocky ridge and alluvial plain habitats
suppor
ted
distinct ant
f
aunas

This was
demonstrated
by
multivariate
analysis of
the
results of our simplified
protocol,
where the two
ha
bi-
tats were clearly separated in
ordination
space based
on
ant species
composition.
In
addition,
our
simplified
protocol indicated that a third
habitat,
rocky
ridges
,
had
intermediate
species
composition.

Ant abundance declined with increasing
SO
2
Our simplified protocol only considered species
presence/absence, so we used mean occurrence as
a
surrogate of
abundance.
Mean occurrence
sho
w
e
d
a significant decline with increasing
SO
2
.
Species richness declined with increasing
SO
2
Our simplified protocol
reproduced
this
pattern,
bu
t
the variation was not quite statistically
significant.
Only one species,
Camponotus sp.

A (denticulatus
gp),
was
commonly
recorded in our
study as well as
in
the
intensive
survey, and in
both cases
abundance
clear
l
y increased
with increasing
SO
2
. None of our
other
common
species was
recorded
frequently
enough
in
the
intensive survey
to detect their
responses to

SO
2
.
Ant functional
group
composition
showed
relatively
little
change in
relation to
SO
2
From the results
of our simplified
protocol,
the
lack
of a
significant
functional
group–zone
interaction
indicated that
functional group
profiles were
r
ela
ti
v

e
l
y
uniform across
SO
2
zones
.
Ant
responses
varied
according
to
biogeograp
hical
affinity
As in the
intensive survey,
our results
revealed
tha
t
Eyrean and
Torresian taxa
showed
systematic
o
v
er
all

variation in relation to SO
2
, but that
widespread
taxa
did not. In both cases there were
marked declines
in
Torresian taxa with increasing
SO
2
. The intensive
surv
ey
showed marked increases in
Eyrean taxa with
incr
eas-
ing SO
2
, but this was only
weakly evident in our
da
ta.
In summary, our simplified protocol
reproduced
vir
- tually all the key findings of the intensive
survey.
This

was despite some differences in sampling
design.
Moreover, the protocol not only detected
r
a
ther
obvious
environmental variation,
such as
betw
een
major
habitat
types, and emission impacts in
the
imme-
diate vicinity of the smelter, but was
sensitive to
the
effects of low SO
2
levels up to 35 km
away. Such
ef
fects
15
Simplified
ant
assessment
© 2002

British
Ecological
Society
,
Journal of
A
pplied
Ecology, 39
,
8–17
on fauna were unable to be detected by
intensi
v
e
vertebrate
surv
e
y
.
Our simplified ant assessment protocol was
highl
y
effective at Mt Isa, but how widely applicable are
our
results to other regions? The reliability of our
pr
otocol
elsewhere depends on the suitability of the
envir
on-

ment for pitfall
trapping,
and the
abundance
and
di
v
e
r
- sity of the resident ant fauna. Pitfall
trapping is effective for sampling ants in relatively
open
envir
on-
ments (Andersen 1991; 1997c) but
becomes less
ef
fect-
ive as the complexity of the ground
layer increases,
and
is relatively ineffective in habitats
with dense leaf
litter
(Agosti et al. 2000). Our
protocol also relies on
a
diverse and
abundant
ant

fauna. As such it is
ideall
y suited for
Australia,
where
open habitats
pr
edominate
and the ant fauna is
exceptionally diverse. We and
our
colleagues have
used the protocol successfully to
sample
ants
throughout
inland Australia (Woinarski et
al.
2002). It is likely to be similarly effective in arid
lands
and the seasonal tropics
throughout
the world. On
the
other hand, it would be less effective in
cool–
temper
a
t
e

zones, where ant diversity is relatively low
and most
of
the
abundant
and speciose genera are
relatively
small
sized (e.g. Formica, Lasius and
Leptothorax
thr
ough-
out the Holarctic; Creighton
1950; Bolton 1995).
In
these regions, the body size
threshold of 4 mm
w
ould
have to be reduced in order
to cover sufficient
n
umbers
of species
.
      
            
Many authors have discussed the ideal
attributes
of

an
indicator group for assessing ecological change,
and
ants routinely perform well against these criteria
(Majer
1983; Greenslade & Greenslade 1984; Brown 1997).
Many of the
attributes
directly address a
tax
on
’
s
a
bility
to reflect general ecological change, and relate
to
their abundance,
diversity, functional
importance
and
sens-
itivity to
disturbance.
Ants clearly meet
these
criteria,
especially in Australia (Andersen
1990). However,
it

is also recognized that costs and
logistic
constraints
are
important
variables in the
design of
monitoring
programmes
(Spellerberg 1991).
Ants also perform
r
el-
atively well in this context. For
example, Brown (1997) scored 21 potential insect
indicator taxa in the
neo-
tropics according to a
variety of
attributes
r
ela
ting
primarily to their
practicality of use, and ants
r
a
ted
equal highest,
scoring 19 out of a possible 20

points.
Nevertheless,
ants still pose formidable challenges f
o
r
workers who
are inexperienced with insect
surv
eys
.
The simplified ant assessment protocol we
ha
v
e
tested here overcomes many of these challenges.
First,
it is readily
incorporated
into routine wildlife
surv
eys
,
such that ants can be reliably assessed without
speci-
fically sampling for them. Alternatively, if
v
erte
bra
t
e

trapping is not being
conducted,
it is
simple to
install
pitfall traps specifically for ants, as
this takes only a few minutes per trap. Secondly, by
considering only a
sub-
set of species it greatly reduces
laboratory
time
required
for the processing
and sorting of
specimens. Most
ant
species are
relatively small
(< 4 mm), so
most species
were ignored by
our
protocol.
Thirdly, large
species
ar
e
far
easier to sort

into
morphospecies
than are
small
species.
Throughout
the
world, small-
sized taxa
(such
as the myrmicine
genera Pheidole,
Cr
ematog
aster
,
Monomorium,
Leptothorax
and
Strumigenys) are
typic-
ally the
most demanding
ants
taxonomically,
and
require
considerable
experience for
them to be

r
elia
b
l
y sorted to
species level.
Most large
species can be
suc-
cessfully
sorted with only
limited
experience, such
tha
t
a focus on
large species
makes ants
accessible to a
wide
range of
users. Finally,
these efficiencies
mean that
a
greater number
of sites can be
surveyed. Despite
taking
only

about 10% of the
effort, in this
study our
pr
otocol
was
able to sample
65 sites
compared with
40 for
the
intensive
surv
e
y
.
Our sampling protocol has parallels with the
con-
cept of ‘taxonomic sufficiency’ (Ellis 1985),
w
hich
addresses the level of taxonomic resolution
at
w
hich
samples are most efficiently sorted and
analysed.
Both
approaches
focus on the resolution

required to
sa
tisfy
the objectives of the
monitoring
or assessment
pr
o-
gramme, as opposed to what is
required for a
compr
e-
hensive description of the
taxa under
in
v
estiga
tion.
Given that they comprise
a single taxonomic
famil
y
,
the question of
taxonomic sufficiency for ants is one
of
genus-level
analysis. Analysis of ant community data
a
t

genus
level can often reproduce species-level
pa
tterns
(Andersen 1997b; Pik, Oliver & Beattie 1999), but
the
reliability of genus as a surrogate for species in
ants
can
vary widely between regions (Andersen
1997a).
Our
protocol has the
advantages
of species-
level
pr
ecision,
and achieves efficiency through
‘sampling sufficiency’.
         
For 20 years scientists have been
promoting
the use
of
terrestrial
invertebrates
as
bioindicators,
but such

use
still largely remains a topic discussed by
scientists
rather than a practice embraced by land
managers.
In
the scientific arena,
attention
has
focused on
identifying
the most reliable indicator
taxon. However,
the
actual use of
invertebrates
by land managers is
not
limited by scientific
uncertainty
over which taxon
might
give
the most
precise results.
Rather,
it
is
limited by
gen-

eral
unfamiliarity
and inexperience with dealing
with
insects. The truth is that a number of
functionall
y
important invertebrate
groups can
provide v
alua
b
l
e
information
on ecological change
associated with
land
use. We suggest that research
directed at making
these
groups accessible to land
managers deserves
higher
priority than does
further assessment of the
r
ela
ti
v

e
merits of
different candidate taxa. Once
in
v
erte
bra
t
e
bioindicators
become engrained in
land-
mana
gement
culture, then it would be
appropriate
to
focus
a
ttention
on what might be the ‘best’ indicator
tax
on.
The main finding of our study does not really
con-
cern the details of our simplified sampling
pr
otocol.
16
A.N.

Ander
sen
et
al.
© 2002
British
Ecological
Society
,
Journal of
A
pplied
Ecology, 39
,
8–17
Rather,
it is the fact that comprehensive sampling
w
a
s
not required to reveal complex ant
comm
unity
responses to land use. Our study has
shown that a
r
el-
atively few
taxonomically
tractable

ants can say a
lot
about the
environment
in which
they occur, and
con-
siderably more than could
traditional
wildlife (v
erte-
brate) surveys. This is not
to decry the need for
detailed
studies of ants or other
invertebrate
groups as
part
of research into
ecological responses to land
use
.
However, the
requirements
of such research should
not
be confused
with those of routine
monitoring
pr

o-
grammes,
where the focus is not on the target
gr
oups
per se,
but on using them to provide
information
on
the
broader
environment.
The main issue in
envir
onmental
monitoring
is not whether or not
samples are
compr
e-
hensive, but whether they are
reliable, and we
ha
v
e
shown that simplified ant
sampling can provide
r
elia
b

l
e
r
esults
.
Ackno
wledgements
We thank Brandon Bestelmeyer,
Jonathan
Majer,
J
ohn
Woinarski and Rochelle Lawson for their helpful
com-
ments on the draft
manuscript.
This is CSIRO’s
T
r
op-
ical Ecosystems Research Centre
publication
n
umber
1170.
Reference
s
Agosti, D., Majer, J.D., Alonso, L.E. & Schultz, T.R. (2000)
Ants: Standard Methods for Measuring and
Monitoring

Biodiversity. Smithsonian
Institution
Press,
W
ashington,
DC.
Andersen, A.N. (1990) The use of ant communities
to
evaluate change in
A
ustr
alian
terrestrial ecosystems: a
r
e
view
and a recipe. Proceedings of the Ecological
Society
of
Australia, 16, 347–
357.
Andersen, A.N. (1991) Sampling communities of
gr
ound-
foraging ants: pitfall catches compared with
quadrat counts
in an
Australian
tropical savanna. Australian Journal
of

Ecology, 16, 273 –279.
Andersen, A.N. (1993) Ants as indicators of
r
estor
a
tion
success at a uranium mine in tropical
Australia.
Restoration
Ecology, 1, 156 –167.
Andersen, A.N. (1995) A classification of
Australian
ant
com-
munities, based on functional groups which parallel
plant
life-forms in relation to stress and
disturbance.
Journal
of
Biogeography, 22, 15 –
29.
Andersen, A.N. (1997a) Using ants as
bioindicators:
m
ultiscale
issues in ant community ecology. Conservation
Ecolog
y
[Online], 1,

8.
Andersen, A.N. (1997b) Ants as indicators of
ecosystem
restoration
following mining: a functional group
a
ppr
oach.
Conservation Outside Nature Reserves
(eds
P. Hale
&
D.
Lamb),
pp. 319 – 325. Centre For
Conservation
Biology,
The
Uni-
versity of Queensland, Brisbane,
A
ustr
alia.
Andersen, A.N. (1997c)
Functional
groups and
patterns of
organization
in
North

American ant communities:
a
comparison
with
Australia.
Journal of Biogeography, 24
,
433 –
460.
Andersen, A.N. (1999) My
bioindicator
or yours? Making
the
selection. Journal of Insect Conservation, 3, 1–
4.
Andersen, A.N. (2000) The Ants of Northern Australia: A
Guide to the Monsoonal Fauna. CSIRO Publishing,
Collingw
ood,
A
ustr
alia.
Andersen, A.N. & Sparling, G.P. (1997) Ants as
indica
tors
of
restoration
success:
relationship
with soil

micr
obial
biomass in the
Australian
seasonal tropics.
Restoration
Ecology, 5, 109 –114.
Belbin, L. (1994)
PATN.
Pattern Analysis Package
T
ec
hnical
Reference. CSIRO Wildlife and Ecology,
Canberr
a,
A
ustr
alia.
Bestelmeyer, B.T. & Wiens, J.A. (1996) The effects of land
use
on the structure of
ground-foraging
ant communities in
the
Argentine Chaco. Ecological Applications, 6, 1225 –
1240.
Bisevac, L. & Majer, J.D. (1999)
Comparative
study of

ant
communities of
rehabilitated
mineral sand mines and
hea
th-
land, Western
Australia.
Restoration Ecology, 7, 117 –126.
Bolton, B. (1995) A New General Catalogue of the Ants of
the
World.
Harvard
University Press, Cambridge,
MA.
Brown, K.S. Jr (1997) Diversity,
disturbance,
and
sustaina
b
l
e
use of
Neotr
opical
forests: insects as indicators
for
conserv
a
tion

monitoring.
Journal of Insect
Conservation, 1, 25 –
42.
Creighton, W.S. (1950) The ants of
North
America. Bulletin
of
the Museum of Comparative Zoology, 24, 1–
585.
Dobson,
A.J. (1990) An Introduction to Generalized
Linear
Models.
Chapman
& Hall,
London,
UK.
Ellis, D. (1985) Taxonomic sufficiency in pollution
assessment.
Marine Pollution Bulletin, 16,
459.
Fisher, B.L. (1999) Improving inventory efficiency: a
case
study of leaf-litter ant diversity in
Madagascar.
Ecological
Applications, 9, 714 –731.
Greenslade, P.J.M. & Greenslade, P. (1984)
Invertebrates

and
environmental
assessment. Environment and
Planning, 3
,
13
–15.
Griffiths, A.D. (1998) Impact of Sulphur Dioxide Emissions
on Savanna Biodiversity at Mt Isa, Queensland.
Unpub
lished
final report to Mt Isa Mines. CSIRO and
Tropical
Sa
v
annas
CRC, Darwin,
A
ustr
alia.
Hellawell, J.M. (1978) Biological Surveillance of Rivers:
A
Biological Monitoring Handbook. Water Research
Centr
e,
Stevenage,
UK.
Hoffmann,
B.D. (2000) Changes in ant species
composition

and community
organisation
along grazing gradients
in
semi-arid rangelands of the
Northern Territory.
R
ang
eland
Journal, 22, 171–189.
Hoffmann,
B.D., Griffiths, A.D. & Andersen, A.N. (2000)
Response of ant communities to dry sulfur
deposition
from mining emissions in semi-arid
northern
A
ustr
alia,
with implications for the use of functional groups.
A
ustr
al
Ecology, 25, 653 –
663.
Kotze, D.J. & Samways, M.J. (1999) Support for the
m
ulti-
taxa
approach

to biodiversity assessment, as shown by
epigaeic
invertebrates
in an
Afromontane
forest
archipelago.
J
ournal
of Insect Conservation, 3, 125 –143.
Kremen, C. (1994) Biological inventory using target taxa:
a
case study of the butterflies of
Madagascar.
Ecological
Applications, 4, 407–
422.
Landsberg,
J.,
Morton,
S. & James, C. (1999) A
comparison
of the diversity and indicator potential of
arthr
opods,
vertebrates and plants in arid rangelands
across
A
ustr
alia.

The Other 99%. The Conservation and
Biodiversity
of
Invertebrates (eds W. Ponder & D.
Lunney), pp. 111–120.
Transactions
of the Royal Society
of New South
W
ales,
Mosman,
A
ustr
alia.
Lawton, J.H., Bignell, D.E., Bolton, B., Bloemers,
G
.
F
.,
Eggleton, P.,
Hammond,
P.M.,
Hodda,
M., Holt,
R.D
.,
Larsen, T.B., Mawdsley, N.A., Stork, N.E., Srivastava,
D
.
S

.
& Watt, A.D. (1998) Biodiversity inventories,
indica
tor
taxa and effects of
habitat
modification in tropical f
o
r
est.
Nature, 391, 72
–76.
McGeoch, M.A. (1998) The selection, testing and
a
pplica
tion
of terrestrial insects as
bioindicators.
Biological Review, 73
,
181–
201.
Majer, J.D. (1983) Ants:
bio-indicators
of mine site
r
eha
bili-
tation, land-use,
and land

conservation.
En
vir
onmental
Management, 7,
375 –
383.
17
Simplified
ant
assessment
© 2002
British
Ecological
Society
,
Journal of
A
pplied
Ecology, 39
,
8–17
Majer, J.D. (1984)
Recolonisation
by ants in
r
ehabilita
ted
open-cut mines in
northern Australia.

Reclamation and
Revegetation Research, 2, 279 –
298.
Majer, J.D. & Nichols, O.G. (1998) Long-term
r
ecolonisa
tion patterns
of ants in Western
Australian
rehabilitated bauxite
mines with reference to their use as
indicators of
r
estor
a
tion
success. Journal of Applied
Ecology, 35, 161–182.
New, T.R. (1996) Taxonomic focus and quality control in
in
v
e
r
- tebrates surveys for biodiversity
conservation.
A
ustr
alian
Journal of Entomology, 35, 97 –106.
Norris, R.H. & Norris, K.R. (1995) The need for

biolo
gical
assessment of water quality: an
Australian perspective.
Australian Journal of Ecology, 20, 1–
6.
Pearson, D.L. & Cassola, F. (1992) World-wide species
rich-
ness
patterns
for tiger beetles
(Coleoptera: Cicindelidae):
indicator taxon for biodiversity and
conservation studies.
Conservation Biology, 6, 376 –
391.
Pik, A.J., Oliver, I. & Beattie, A.J. (1999) Taxonomic
suffi- ciency in ecological studies of terrestrial
in
v
erte
bra
tes.
Australian Journal of Ecology, 24, 555 –
562.
Read, J.J. (1996) Use of ants to monitor
environmental
impacts
of salt spray from a mine in arid
Australia.

Biodiversity and Conservation, 5, 1533 –1543.
Read, J.L. & Andersen, A.N. (2000) The value of ants as
ear
l
y
warning
bioindicators:
responses to pulsed cattle grazing
a
t
an
A
ustr
alian
arid zone locality. Journal of Arid
En
vir
onments
,
45, 231–
251.
Rosenberg,
D.M., Danks, H.V. &
Lehmkuhl,
D.M. (1986)
Importance
of insects in
environmental
impact
assessment.

Environmental Management, 10, 773 –783.
Spellerberg, I.F. (1991) Monitoring Ecological
Chang
e
.
Cambridge University Press, Cambridge,
UK.
Vanderwoude,
C., Andersen, A.N. & House, A.P.N. (1997)
Ant communities as
bioindicators
in relation to fire
man-
agement of spotted gum (Eucalyptus maculata
Hook.)
forests in south-east Queensland. Memoirs of the
Museum
of Victoria, 56, 671–
675.
Woinarski, J.C.Z., Andersen, A.N., Churchill, T.B. & Ash,
A.
(2002) Response of ant and terrestrial spider
assemblages
to
pastoral and military land use, and to
landscape
position,
in a tropical savanna woodland in
northern
A

ustr
alia.
Austral Ecology, 27, in
pr
ess.
York, A. (1994) The long-term effects of fire on forest
ant
communities:
management
implications for the
conserv
a-
tion of biodiversity. Memoirs of the Queensland
Museum
,
36, 231–
239.
Received 17 April 2001; final copy received 14 November 2001