JAE538.
fm Page 875 Wednesday, August 22, 2001 8:46 AM
et al. dynamics of carabid predation on slugs
Spatial
Journal of Animal FORUM
Blackwell
Oxford,
Journal
JAE
British
520021-8790
70
538
J.001
Mair Ecological
of
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AnimalSociety,
Ltd
Ecology2001
Ecology 2001
70, 875 – 876 Spatial dynamics of predation by carabid beetles on slugs
JACQUI MAIR, MARK D. F. SHIRLEY, STEPHEN P. RUSHTON and
GORDON R. PORT
Department of Agricultural and Environmental Science, University of Newcastle upon Tyne, Newcastle upon Tyne
NE1 7RU
In a recent issue of Journal of Animal Ecology, Bohan
et al. (2000), presented data from a field survey ana-
lysing the distribution of slugs and a slug predator
Pterostichus melanarius (Illiger) through time and over
a range of spatial scales. Slugs were sampled at 0·25, 1,
4 and 16 m scales with beetles being sampled at 4, 8 and
16 m scales. The distributions of the two main slug
species (Deroceras reticulatum (Müller) and Arion
intermedius Normand) were found to be spatially
independent at all spatial scales; however, total slug
distribution at the 16 m scale was found to be aggre-
gated in June and random in July. The distribution of
P. melanarius was aggregated at the 16 m scale and
random at the 4 and 8 m scales in June, whilst in July
distributions were random at all spatial scales. Patterns
of beetle and slug distributions were therefore compared
at the 16 m scale in June and July using spatial analysis
by distribution indices (SADIE) algorithms. The pat-
tern of P. melanarius distribution was not associated
with either slug species, but to ‘all slugs’. ELISA tests
were carried out on individual P. melanarius to deter-
mine whether they had consumed slug tissue and 11%
overall were found to be sero-positive for slug protein.
The authors develop a hypothesis concerning the
impact of beetle predatory activity on slug popula-
tions; namely that predation by P. melanarius was ‘not
opportunistic, but direct and dynamic.’ We analyse the
data further and evaluate the extent to which the
hypotheses developed by the authors are supported by
the results of their analyses. We then present alternative
explanations of the observed patterns by consideration
of analyses at scales other than those presented.
First, we question why comparisons between spatial
patterns of carabids and slugs were only made at the
16 m scale, given that associations were also detected at
the 4 m scale where beetle and slug sampling also coin-
cided. If we consider their analyses at the 16 m level,
then the data presented by Bohan et al. indicate that
there was a significant association in the pattern of dis-
tribution between slugs that were larger than 50 mg
and beetles that were sero-positive to slug antibody in
June. This association was not obvious in July. They
Correspondence: Dr J. Mair, Department of Agricultural &
Environmental Science, University of Newcastle, Newcastle
© 2001 British upon Tyne, NE1 7RY. Tel: 0191-222-6599/5952. E-mail:
Ecological Society jacqueline.mair@ncl.ac.uk
Graphicraft Limited, Hong Kong
000
used this difference and the decline in slug numbers
between these two periods as evidence of significant
predation of slugs by beetles.
It is implicit in this study that slug numbers have
declined between the two months; however, no actual
data of this type are given. We have therefore inter-
polated from the density maps the change in ‘large’ slug
populations between June and July by analysing the
data presented in their Fig. 3a,b. Consideration of the
data shows that where a decline in slug numbers
occurred, there was an average reduction of 56·9%.
Even allowing for our interpretation of the inter-
polated maps, we believe that this observed reduction in
the numbers of ‘large’ slugs is unlikely to be due solely
to predation by P. melanarius; and that there must be
alternative explanations for the observed patterns. In
order to refute the predation hypothesis, we compare
estimates of slug population size for the two periods
with the population density of potential predators. We
then use these figures to estimate the per capita rate of
predation required to lead to the observed decline in
slugs, given the levels of sero-prevalence in the beetle
populations. If the beetles are responsible for the
observed reduction in the slug population – of approx-
imately 57% in 1 month (28 days) – and if there are ini-
tially 120 slugs m–2 (a density in the mid-range of those
observed), then 2·4 slugs m–2 must be killed each night.
An average of 11% of the beetles caught on each sam-
pling occasion in June and July tested positive; how-
ever, since beetles remain ELISA-positive for slug
protein for 2·5 days, only 4·4% of the beetles can be
assumed to have killed slugs on any given night.
With this estimate of 4·4% of beetles killing slugs
each night, the beetle density necessary to cause the
observed decline would have to be 55 m–2. Densities of
P. melanarius in the field have been found to range from
0·25 to 11 m–2 (Thiele 1977; Scheller 1984; Ayre 1995;
Kromp 1999). We conclude therefore that this density
of 55 m–2 is unrealistic, indicating that the decline in
slug populations observed is unlikely to be due to
beetles alone.
The authors suggested that beetles remain satiated
for up to 23 days following feeding, to account for the
static distribution of carabids over the sampling
period. It is highly unlikely that P. melanarius will
remain satiated for such a long period of time. P.
melanarius will kill slugs even when satiated (Thiele
JAE538.fm Page 876 Wednesday, August 22, 2001 8:46 AM
876 1977); however, generalist carabids are known to be
Forum voracious feeders consuming at least their own body
weight daily (Thiele 1977; Kromp 1999) and up to three
times their body weight per day in the case of P.
melanarius (Thiele 1977). As beetles feed every day, if
P. melanarius was strongly motivated to feed on slugs
as suggested by Bohan et al. we would expect beetle dis-
tribution to closely match the slug spatial distribution.
However, the beetle distributions did not change
between months and the decrease in the numbers of
large slugs was not significantly related to the distribu-
tion of P. melanarius (P = 0·055). In July many sero-
positive beetles were found in areas with few large
slugs. This was interpreted as beetles consuming all the
large slugs in that particular location in June and
remaining present in the area because they were sati-
ated. However, for beetles to be sero-positive for slug
proteins in the July samples they must have consumed
slug tissue in the previous 2·5 days, indicating that
beetles were not only feeding on ‘large’ slugs.
There are several possible alternative explanations to
the patterns observed. First, whilst Bohan et al. have
included the effects of environment in their initial
hypotheses, they refuted the hypothesis that relative
humidity and temperature had any effects on slug popu-
lations. We contend that whilst they undertook the
tests, their ability to test the hypotheses was restricted
by the quality of the data they had available, resulting
in Type II errors for the tests undertaken. Secondly, we
would contend that the environmental data used were
collected at inappropriate spatial and temporal scales.
Small-scale (less than 1 cm) variations in surface
topography mean that the soil microclimate varies at a
scale similar to that of the size of an adult slug. Coarse
samples at the scale taken are unlikely to be able to
resolve the differences in soil moisture content that
could generate patterns or clumping in the distribution
of animals. Thirdly, the time scale between samples of
these environmental data provide only a simple snap-
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
875–876
shot that is unlikely to be an indicator of the range in
moisture or environmental conditions encountered by
the slug during the intersample period. Finally, the
authors did not consider the possibility that clumped
distribution patterns might arise as a result of the
highly localized nature of birth and recruitment into
the population. Slugs lay large egg masses. This means
that the spatial pattern of eggs in the environment is
inevitably highly clumped. One might expect that this
clumping would persist into the juvenile stages of slugs,
as the ranging abilities of slugs is bound to be related to
size. As slugs grow bigger they can move farther. Thus,
as slugs age they would tend to move further apart and
become less aggregated, all things being equal.
We suggest as our alternate hypothesis, that the
observed distributions of slugs reflects the demographic
features, such as egg distribution patterns, and that any
congruence between spatial patterns of beetles and
slugs was purely fortuitous or determined by environ-
mental parameters with which both were correlated.
References
Ayre, K. (1995) Evaluation of carabids as predators of slugs in
arable land. PhD Thesis, University of Newcastle upon
Tyne, Newcastle upon Tyne.
Bohan, D.B., Bohan, A.C., Glen, D.M., Symondson, W.O.C.,
Wiltshire, C.W. & Hughes, L. (2000) Spatial dynamics of
predation by carabid beetles on slugs. Journal of Animal
Ecology, 69, 367 – 379.
Kromp, B. (1999) Carabid beetles in sustainable agriculture: a
review on pest control efficacy, cultivation impacts and
enhancement. Agriculture, Ecosystems and Environment,
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Scheller, H.V. (1984) The role of ground beetles as predators
on early populations of cereal aphids in spring barley.
Zeitschrift für Angewandte Entomologie, 97, 451–463.
Thiele, H.U. (1977) Carabid beetles in their environments: a
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behaviour. Springer-Verlag, Berlin.
Received 21 December 2000; accepted 1 May 2001