Primary Article
Eukaryon, Vol. 8, March 2012, Lake Forest College
Biotic Resistance of Ants in Urban and Natural Environments
Susan Helford*
Department of Biology, Lake Forest College
as predation, competition, and diseases. However,
competition was a lower than expected factor in the success
of biotic resistance (Levine et al. 2004). Depending on the
spatial scale measured, different things account for biotic
resistance. When analyzed on a small scale, biodiversity
acts as a buffer for invasive species, but on a large-scale
there is a positive correlation between invasive species and
high biodiversity (Kennedy et al. 2002). Biotic resistance
probably does not completely repel invasions, but it can
make some difference (Kennedy et al. 2002). Though
relationships differ, the link between biodiversity and
invasive species is undisputed.
Urban areas are known to have low biodiversity
(Shochat et al. 2010). However, they are becoming one of
the most common habitat types in the United States and
worldwide. For this reason, it is important to understand
urban ecology. Future conservation efforts will need to focus
on urban systems (Dunn et al. 2006). High biodiversity can
act as a buffer to invasives, so non-diverse urban
environments could be particularly vulnerable to invasion.
One hypothesis postulated for the low biodiversity of urban
areas is that there is a high number of invasive species in
urban areas that outcompete native species; however, the
causal factor is difficult to determine (Shochat et al. 2010).
Habitat loss is clearly an important factor, but the
competition caused by invasive species may also negatively
affect native species. If biotic resistance is studied in urban
areas, efforts to conserve biodiversity can be more
knowledgeable about one of the most common habitat types.
Information on biotic resistance in urban areas could
contribute to conservation efforts. Past research
concentrates mostly on natural habitats (Shochat et al.
2010). Comparing biotic resistance in urban and natural
settings may help us to better understand how invasive
species affect both types of ecosystems.
With the increase in urban habitat, species that
interact often with humans are the most likely to persist
(Menke et al. 2010). Ants specifically take a role in the urban
ecosystem that can have some beneficial effects for
humans, like removal of food crumbs. Ants are common both
in natural and urban areas, and provide ecosystem
processes that are central to both types of ecosystems
(Menke et al. 2010). Invasive ant species, like Linepethema
humile (the Argentine Ant) can negatively affect native ant
species and have profound effects on the ecosystems they
Abstract
Invasive species can threaten the natural biodiversity of
ecosystems. Biotic resistance gives ecologists insight
into what prevents invasive species success. Urban
habitats are currently the most common and fastest
growing ecosystem on the planet, so understanding
biotic resistance in these areas is of particular
importance. Ants are a good study case for urban biotic
resistance since they perform important ecosystem
functions in both urban and natural habitats. We
compared the biotic resistance of urban and natural
habitats using data from existing papers and databases
of ant distributions in both natural and urban
environments. We also examined the effects of latitude
and ecosystem type on biotic resistance, and if biotic
resistance differs within different urban habitat types.
Biotic resistance was found to be higher in natural areas
than urban areas, and in a multiple regression, both
latitude and ecosystem types predicted two thirds of the
variance in biotic resistance. Urban habitat types were
found to differ among four non-mutually exclusive
groups, and biotic resistance of these habitats seemed
to follow a gradient from least man-made to most manmade. Human-caused change may be an important
variable to consider in future studies of biotic resistance
with vital implications for urban biodiversity.
Introduction
Invasive species are a worldwide problem that threaten
biological diversity. They can alter critical processes that
ecosystems rely on (Buczkowski & Bennett 2008). Many
factors effect how successful these invaders are, but
because of the complicated nature of ecosystems there is no
accurate way to predict how well invasive species will do in
new environments (Kennedy et al. 2002). There has been
some question of whether invasive species are the cause of
degraded ecosystems or simply “passengers” of noninteractive processes (MacDougall & Turkington 2005).
MacDougall & Turkington (2005) conducted experiments on
the importance of species competition for invasive success,
and found that although competition had some effect, the
more common causes of invasion were barriers and
environmental stressors that limit native species. A review by
Gurevitch & Padilla (2004) found that there is not enough
evidence to claim invasive species as the cause of lost
biodiversity. However, the relationship between
native
species decline and the introduction of invasive species is
often simultaneous. The relationship between invasive and
native species is important to understand for insight into
what makes an ecosystem vulnerable or resistant to
invasion.
Some ecosystems are better than others at
resisting invasion. When native species reduce the success
of invasive species, it is called biotic resistance (Levine et al.
2004). Not all invaders exposed to a new area are
successful. Many factors can reduce invasive success, such
________________________________________________
N
*This author wrote the paper for Biology 374: Biogeography taught by Dr. Sean
Menke.
Mean
Agriculture
10
.4110
.20354
Business
10
.3678
.24016
Greenway
9
.0869
.17303
Industrial
10
.5126
.27016
Park
10
.1874
.20240
Residential
30
.2971
.21972
Forest
10
.0000
.00000
Total
89
.2751
.25134
Table 1. Mean ratios by urban habitat types
80
Std. Deviation
Primary Article
Eukaryon, Vol. 8, March 2012, Lake Forest College
(I) Habitat
Agriculture
Business
Greenway
Industrial
Park
Residential
Forest
(J) Habitat
Business
Greenway
Industrial
Park
Residential
Forest
Agriculture
Greenway
Industrial
Park
Residential
Forest
Agriculture
Business
Industrial
Park
Residential
Forest
Agriculture
Business
Greenway
Park
Residential
Forest
Agriculture
Business
Greenway
Industrial
Residential
Forest
Agriculture
Business
Greenway
Industrial
Park
Forest
Agriculture
Business
Greenway
Industrial
Park
Residential
Mean
Difference (I-J)
.04319
*
.32415
-.10161
.22367
.11397
*
.41103
-.04319
.28096
-.14479
.18048
.07078
*
.36784
*
-.32415
-.28096
*
-.42576
-.10048
-.21019
.08688
.10161
.14479
*
.42576
*
.32528
.21557
*
.51264
-.22367
-.18048
.10048
*
-.32528
-.10971
.18736
-.11397
-.07078
.21019
-.21557
.10971
*
.29707
*
-.41103
*
-.36784
-.08688
*
-.51264
-.18736
*
-.29707
Std.
Error
.09314
.09570
.09314
.09314
.07605
.09314
.09314
.09570
.09314
.09314
.07605
.09314
.09570
.09570
.09570
.09570
.07916
.09570
.09314
.09314
.09570
.09314
.07605
.09314
.09314
.09314
.09570
.09314
.07605
.09314
.07605
.07605
.07916
.07605
.07605
.07605
.09314
.09314
.09570
.09314
.09314
.07605
Sig.
.999
.018
.929
.211
.745
.001
.999
.063
.711
.462
.966
.003
.018
.063
.001
.940
.123
.970
.929
.711
.001
.013
.081
.000
.211
.462
.940
.013
.777
.416
.745
.966
.123
.081
.777
.003
.001
.003
.970
.000
.416
.003
Table 2. Tukey HSD comparisons
between the biotic resistance of these two types of
ecosystems, as well as habitat types within urban systems.
We also chose to examine latitude with climate change in
mind. Changing climates will affect the abiotic factors, like
temperature by latitude, which can affect species
assemblages and vulnerability to invasion (Chapin III et al.
2000). One example of this climate change effect is the
Argentine Ant, which is limited in its northern range by soil
temperatures. Should the temperatures increase on a
latitudinal gradient, this harmful species may move further
north (Brightwell et al. 2010).
Our first hypothesis will be to determine if there is
a difference between the biotic resistance in urban and
natural areas. Our second hypothesis will be to see if biotic
resistance varies by latitude. Our third hypothesis will be to
determine if there is a difference in biotic resistance between
invade (Buczkowski & Bennett 2008). Additionally, many
invasive ant species have significant effects on their
ecosystems, and are a target of pest control and
conservation efforts (Buczkowski & Bennett 2008).
Since ants are present in and central to both urban and
natural environments, they are a good study system for
comparing biotic resistance between these two ecosystems.
We chose to use ants to examine the factors that
determine the success of invasions. We lookied at both
biotic resistance as a biotic factor and latitude as a correlate
for abiotic factors. Biotic resistance is often studied in natural
systems, but less commonly in urban systems. For example,
different natural ecosystems have differing levels of biotic
resistance that are documented, but urban habitat types
have not been extensively studied (Shochat et al. 2010). We
wanted to determine if there was a significant difference
81
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Eukaryon, Vol. 8, March 2012, Lake Forest College
Habitat
Forest
N
1
2
3
4
10
.0000
9
.0869
.0869
Park
10
.1874
.1874
.1874
Residential
30
.2971
.2971
.2971
Business
10
.3678
.3678
Agriculture
10
.4110
.4110
Industrial
10
Greenway
.5126
Figure 1. Map of urban and natural data points This figure shows
the datum points analyzed. Blue circles represent urban habitat data
points and red circles represent natural habitat datum points.
Table 3. Tukey HSD groups
different types of habitats within urban ecosystems. To
quantify biotic resistance, we use ratios of the number of
invasive species to the number of total species in an area.
By looking at both biotic resistance and how it interacts with
latitude, we hope to learn more about the factors that
promote invasion.
also conducted a multiple regression model of latitude and
ecosystem on transformed ratios. To test our third
hypothesis, we ran a one-way ANOVA test comparing the
transformed ratios of different habitat types. We ran a posthoc Tukey HSD test after finding the ANOVA significant.
Results
Hypothesis 1. Urban ecosystems averaged significantly
more invasive species per total species than natural
ecosystems (0.45 ± 0.21SD, 0.07 ± 0.11SD respectively)
(t18 = 5.18, p < 0.0005) ( Fig. 1).
Hypothesis 2. We ran a regression of latitude on transformed
ratios, which was non-significant, R2=.003, F1,87-0.261,
p=.611. We ran a multiple regression of latitude and habitat
type on the transformed ratios, which was found to be
significant, R2=0.673, F2,17=17.474, p<.0005. In this model,
ecosystem type was a significant factor (t=-5.545, p<0.0005)
and latitude was marginally significant (t=-1.964, p=0.066)
(Fig. 2).
Hypothesis 3. We ran a one-way ANOVA to see if invasive
species/ total species ratio varied by urban habitat type (Fig.
3). There were large differences in the ratios of different
habitat types (Table 1, Fig. 4). The ANOVA was
Methods
Data Collection
As a class, we requested data from 13 articles on urban ant
distributions. The data we requested was presence /
absence matrices for every species of ant recorded and
GPS coordinates of all sites where ant data were collected.
Not all papers kept track of the specific data. Many of the
papers did not have GPS coordinates for sites, and so
presence/absence matrices were calculated by city. Our
study required both city wide data, and within city data for
analyses. We looked at the combined data collected by the
class to choose what was appropriate for analysis. We
eliminated data that did not have GPS coordinates, as well
as data from papers that only collected samples in more
natural areas, like forests. This left us with data on 10 cities
from eight different papers (Appendix A). We submitted the
latitude values of each city to our professor, Dr. Sean
Menke, and he provided us with presence / absence data on
ants in natural habitats for similar latitudes. This left us with
10 urban data sites and 10 natural data sites.
For the data on different urban habitat types, we
used only data from the paper on Raleigh, NC (Menke, et al.
2010). We chose to use only this data because the habitat
types were the best recorded, and it had the most data
points. We had no method to compare what one paper
labeled a park to what another paper labeled a park, so we
kept our data to one paper for consistency.
Data Analysis
For all cities, the number of invasive species was
counted. Invasive species were determined using data for
North America (Menke et al. 2010; Invasive Species). We
then created a ratio of the number of invasive species in an
area to the total number of species in an area. Since we
planned on using parametric tests, we transformed the data
using the equation: ArcSine(Square root(#invasive species/
# total species)), to create the variable which we labeled
“transformed ratio.”
To test our first hypothesis, we ran an independent
samples t-test on the mean transformed ratios comparing
urban and natural data. To test our second hypothesis, we
ran a linear regression of latitude on transformed ratios. We
Figure 2. Multiple regression for latitude and ecosystems
Regression lines for latitude and ecosystem type on the transformed
invasive species/ total species ratio. Blue points represent urban
ecosystems, and green points represent natural ecosystems.
Y=0.903-0.013x1-0.383x2, r2=0.673.
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Eukaryon, Vol. 8, March 2012, Lake Forest College
predict biotic resistance of an area. We also found some
significant differences between the mean biotic resistances
of different urban habitat types. All of these findings support
our three hypotheses.
The findings on our first hypothesis are not
surprising. The natural areas had higher biodiversity in
general than the urban areas. Since our data were collected
in a series of small studies at the site level, it makes sense
that this biodiversity served as a buffer of sorts to the
success of invasive species. These results, however, could
have been an artifact of the data collection methods. Since
urban habitats are studied less often than natural habitats,
the data may have simply been less thorough, resulting in
lower diversity. However, despite sampling techniques, the
number of invasive species in urban environments was
much higher than that in natural environments.
Our regression model gave some interesting
results. Latitude alone was not a significant predictor of biotic
resistance. This could have been due to low power, since we
only had 10 sites for each type of ecosystem, resulting in a
total of 20 samples. However, we decided to run a second
multiple regression to include both ecosystem and latitude.
The regression model was highly significant and a good
predictor of transformed ratios, accounting for two thirds of
the variation in biotic resistance among ants. The
significance of this model revealed why the first model may
have been different. Though latitude seemed to have an
effect, the overall starting point for biotic resistance ratios in
urban areas was higher (Fig. 2). This detail makes sense in
light of the results of our first hypothesis. With increasing
latitudes, biotic resistance seemed to be strengthened. The
slopes of
the lines did not appear to differ significantly. This
information gives us some insight to a possible latitudinal
gradient in biotic resistance, in which latitudes higher north
have higher biotic resistance, shown by lower invasive
species: total species ratios. This gradient is interesting due
to the known diversity gradient in latitude, in which latitudes
farther north seem to have less overall diversity.
Our third hypothesis had some very illuminating
results. The data were limited in that it was collected in only
one city, so we must be cautious when drawing conclusions.
However, the biotic resistance in the urban area almost
seems to follow a gradient of more urban-like to more
natural-like environments. The order of biotic resistance from
lowest resistance to highest resistance is: industrial,
agricultural, business, residential, park, greenway, forest.
When one sees the category agricultural field, it does not
seem to fit in as an urban-like environment. However, when
one takes into account the level of man-made change in
each ecosystem, agriculture ranks higher, close to industrial.
This result shows that not only does biotic resistance differ
between urban and natural areas, but also within different
urban habitat types. Additionally, the level of man-made
change in an area may possibly have an effect on the
success of invasive species there. The Tukey HSD test
showed that not every environment differed significantly from
the others, however, the significant differences also showed
the urban-natural gradient (Table 2). For example, industrial
habitats differed significantly from park, greenway, and forest
habitats, the three areas with the highest biotic resistance.
The interesting result that our data yields is that
man-made change in an ecosystem could be a factor in
determining the success of invasive species. Examining this
factor could be a productive research direction for the field.
While the findings of this study are interesting, it is important
to note methodological limitations. We did not collect the
data ourselves, so discrepancies in data collection methods
between studies may have affected the data. Ideally, all
Figure 3. Map of urban habitat types: This figure represents all
datum points for urban habitat types. Green points represent
agricultural habitats, blue points represent business habitats, pink
points represent forest habitats, red points represent greenway
habitats, orange points represent industrial habitats, yellow points
represent park habitats, and purple points represent residential
habitats.
significant and post-hoc Tukey HSD tests were
run
(F6,89=7.70, p<.0005) (Table 2). Post-hoc Tukey HSD tests
showed four non-mutually exclusive groups. Group 1
included forest, greenway, and park. Group 2 included
greenway, park, and residential. Group 3 included park,
residential, business, and agriculture. Group 4 included
residential, business, agriculture, and industrial (Table 3, Fig.
5).
Discussion
We found a significant difference between the means of
biotic resistance in urban and natural areas. Additionally, we
discovered that latitude alone did not predict biotic
resistance, but that latitude and ecosystem together can
Figure 4. Mean transformed ratio by habitat type: This graph
shows the transformed invasive species: total species ratios for each
urban habitat type. The green bar represents agricultural habitat
types, the blue bar represents business habitat types, the red bar
represents greenway habitat types, the orange bar represents
industrial habitat types, the yellow bar represents park habitat types,
the purple bar represents residential habitat types, and the pink bar
represents forest habitat types.
83
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Eukaryon, Vol. 8, March 2012, Lake Forest College
Invasive species: Information, images, videos, distribution maps.
2011. Center for Invasive Species and Ecosystem Health
http://www.invasive.org/species/insects.cfm
areas would have been equally sampled using the same
Kennedy, T.A., Naeem, S., Howe, K.M., Knops, J.M.H., Tilman, D. &
Reich, P. 2002. Nature 417: 636-638.
Levine, J.M., P.B. Adler & S,G. Yelenik. 2004. A meta-analysis of
biotic resistance to exotic plant invasions. Ecology Letters 7: 975-989.
MacDougall, A.S, & R, Turkington. 2005. Are invasive species the
drivers or passengers of change in degraded ecosystems? Ecology
86: 42-55.
Menke, S.B., W. Booth, R.R. Dunn, C. Schal, E.L. Vargo, & J.
Silverman. 2010. Is it easy to be urban? Convergent success in urban
habitats among lineages of a widespread native ant. PLoS ONE 5: 18.
Menke, S.B., B. Guenard, J.O. Sexton, M.D. Weiser, R.R. Dunn, & J.
Silverman. 2010. Urban areas may serve as habitat and corridors for
dry-adapted, heat tolerant species; an example from ants. Urban
Ecosystems 14:135-163.
methods for sampling ants. We also were only able to
Shochat, E., S.B. Lerman, A.M. Anderies, P.S. Warren, S.H. Faeth, &
C.H. Nilon. 2010. Invasion, competition, and biodiversity loss in urban
ecosystems. BioScience 60: 199-208.
Figure 5. Groups designated by Tukey HSD test This graph shows
the results of the Tukey HSD test. The green bars represent
agricultural habitat types, the blue bars represent business habitat
types, the red bars represent greenway habitat types, the orange bar
represents industrial habitat types, the yellow bars represent park
habitat types, the purple bars represent residential habitat types, and
the pink bar represents forest habitat types. Post-hoc Tukey HSD
tests showed four non-mutually exclusive groups. Group 1 includes
forest, greenway, and park. Group 2 includes greenway, park, and
residential. Group 3 includes park, residential, business, and
agriculture. Group 4 includes residential, business, agriculture, and
industrial.
Appendix A
Clarke, K.M., B.L. Fisher, & G. LeBuhn. 2008. The influence of urban
park characteristics on ant (Hymenoptera, Formicidae) communities.
Urban Ecosystems 11:317–334.
Field, H.C., W.E. Evans Sr., R. Hartley, L.D. Hansen, & J.H. Klotz.
2007. A Survey of Structural Ant Pests in the Southwestern U.S.A.
(Hymenoptera: Formicidae). Sociobiology 29:1-14.
employ correlational analyses, so we cannot attribute causeeffect relationships to these variables. Additionally, we did
not include all known data on urban ant distributions
because of missing information from some of the studies,
like GPS coordinates. With proper resources, large-scale
data sampling of urban and natural environments on similar
latitudes in the future would be a good way to reanalyze our
hypotheses. Even better would be an experimental
manipulation of the level of man-made change or
“urbanness” of an area to see if a causal relationship is
involved. Examining this variable may lead to further
knowledge on how invasive species establish success in an
ecosystem. The more we can learn about invasive species,
the more knowledgeable conservation efforts targeting these
species will be.
Forys, E.A & C.R. Allen. 2005. The Impacts of Sprawl on Biodiversity:
the Ant Fauna of the Lower Florida Keys. Ecology 79:2041-2056.
Menke, S.B., B. Guenard, J.O. Sexton, M.D. Weiser, R.R. Dunn, & J.
Silverman. 2010. Urban areas may serve as habitat and corridors for
dry-adapted, heat tolerant species; an example from ants. Urban
Ecosystems 14:135-163.
Pecaravic, M., J. Danoff-Burg, & R.R. Dunn. 2010. Biodiversity on
Broadway-Enigmatic Diversity of the Societies of Ants (Formicidae)
on the Streets of New York City. PLoS ONE 5: 1-8.
Sanford, M.P., P.N. Manley, & D.D. Murphy. 2008. Effects of Urban
Development on Ant Communities: Implications for Ecosystem
Services and Management. Conservation Biology 23:131-141.
References
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Brightwell, R.J., P.E. Labadie, & J. Silverman. 2010. Northward
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Note: Eukaryon is published by students at Lake Forest
College, who are solely responsible for its content. The
views expressed in Eukaryon do not necessarily reflect
those of the College. Articles published within Eukaryon
should not be cited in bibliographies. Material contained
herein should be treated as personal communication and
should be cited as such only with the consent of the author.
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84