Introduction
Biological invasions are important drivers of global change and pose a
major challenge to biodiversity and human
welfare (Vitousek 1990,
exotic species differ from native species is central to the study of
invasion biology (Lemoine 2016,
understanding why some exotic species excel at dominating recipient
communities requires a biogeographical comparison between the native and
introduced ranges of exotic
species (Hierro 2005).
The biotic resistance hypothesis has been widely cited to explaining
invasive species success, as regions with high species diversity are
thought to be more resistant to exotic species than depauperate regions
such as island communities (Elton 1958).
The reason for this is that exotic species are less likely to have
access to available niche space in recipient
communities (Shea 2002). Evidence for
biotic resistance by native ant communities, however, has been mixed. In
the introduced range of Linipithema humile, climatic and habitat
factors have been attributed to the expansion range of L.
humile populations in
California (Roura-Pascual 2009,
in the introduced range of Australia studies have found that native ant
resistance by Irodomyrmex species constrained L.
humile populations in Australia
The impact of exotic ants on native biodiversity has been widely
documented in the literature (Holway
2002, Lach 2009). Consequences of exotic
ant invasions in the introduced range include the local displacement and
reduction of native ant
diversity (Wittman 2014).
Interspecific competition is a major driving factor structuring
ecological communities and regarded as an important determinant for
invasive success (Hölldobler
1990, Sakai 2001) . One
mechanism through which exotic ants can affect recipient ant communities
is through resource competition(Kenis
2008). In native ant communities, resource trade-offs are thought to
lead to species coexistence in which some ant species excel at resource
discovery while others thrive at dominating
resources. (Fellers 1987,
ant species in displacing local ant species has been attributed to their
superior discovery and dominance
abilities (Holway 1998,
the invasive little fire ant Wasmannia auropunctata, showed no
significant differences in resource discovery and dominance abilities
between its native and introduced range (Yitbarek et al. in press).
Understanding how exotic ants are organized within local ant assemblages
in their native range can allows us to make predictions about their
invasion success in the introduced
range (Calcaterra 2016). Relatively
few studies have examined biotic interactions within the native range of
exotic ant species which have mainly focused on L. humile and
S. invicta
populations.(Suarez 1999,
lack studies comparing the invasion dynamics of other globally important
exotic species in their native and introduced ranges. It’s especially
important that we examine how exotic ants are organized within local
species assemblages.
W. auropunctata is considered to be a globally important exotic
ant species, posing a serious threat to biodiversity and human health as
well as being a major pest species in agricultural
ecosystems(Breton 2003,
decades invaded tropical and subtropical regions of the world including
Caribbean and Pacific islands, the United States (Florida), and Western
parts of Africa (Gabon and Cameroon)
spread to parts outside of the tropics such as in the Mediterranean
region of Israel, suggesting that a tropical species can successfully
adapt to colder climates (Vonshak
2009). The evolutionary history of W. auropunctata suggests that
two genetically distinct clades within W. auropunctata
populations coincided in central Brazil, with clade A distributed to
Central America and the northern parts of South America while clade B
was distributed to the southern parts of South America
suggests that Caribbean populations are non-native and likely underwent
multiple introductions presumably from the northern regions of South
America (Foucaud 2010). Within the
native range of W. auropunctata, demographic and reproductive
differences distinguish between dominant clonal populations occupying
human-disturbed habitats and non-dominant sexual populations that occur
in natural
forests (Fournier
2005, Foucaud 2009,
populations have all been found to be clonal and originate from native
dominant populations (Foucaud 2010).
While the success of W. auropunctata has been partially
attributed to its clonal reproductive system, we lack a comparative
ecological analysis of how W. auropunctata ranks relative to
native competitors in invaded regions and areas of origins.
The aim of this study was to compare the ecological dynamics of W.
auropunctata populations in shaded agricultural coffee ecosystems
between their native range of Mexico and introduced range of Puerto
Rico. Shaded agricultural coffee ecosystems represent a useful
replicated model system for comparing invasion patterns because they
have similar vegetation patterns around the globe and are situated
within important biodiversity
hotspots (Moguel 1999,
(Yitbarek et al. in press) found no differences in resource discovery
rates in W. auropunctata populations between Mexico and Puerto
Rico. However, that study did not address the community context of
species interactions.
We studied the competitive interactions between W. auropunctata
and native competitors in recipient communities. We compared the
foraging behavior and competitive interactions around food baits during
short-term (80 minutes) and long-term (14 days) experiments. Within the
context of biotic resistance, the expectation is that competitively
dominant native species in Mexico will inhibit W. auropunctata
populations from expansion. In contrast, we expect that in the
introduced range of Puerto Rico W. auropunctata will
competitively displace local ant species. Comparing the relative rank of
exotic species in local assemblages will allows us to make predictions
about invasion patterns.
Materials and Methods
\label{materials-and-methods}
Study Sites
\label{study-sites}
This study was conducted on an organic shaded agricultural coffee
ecosystems within the native range of W. auropunctata populations
in Mexico and in the introduced region of Puerto Rico. Both regions
experience annual wet and dry seasons, as is common in many tropical
regions. Data were collected during the wet season (summer) between the
months of June and July in 2012, 2013, and 2014. In the Mexico site, a
45-ha plot was surveyed to map the spatial distribution of W.
auropunctata colonies in a medium shaded organic coffee farm in the
state of Chiapas in southern Mexico (15.1735835, -92.3382748), a 30-h a
plot was surveyed in a low-shade conventional coffee farm (15.172465,
-92.3301377), and finally a 6-ha plot was surveyed in a rustic part of
the coffee farm with relatively high shade levels. We observed a total
of 4 colonies in the 45-ha plot and 1 colony in the 30-ha plot ranging
from 0.25-1 ha in size (Figure 1). In Puerto Rico we surveyed 10 small
coffee farms (mostly < 5 ha) in the mountainous regions of
Puerto Rico within the municipalities of Orocovis, Lares, Adjuntas, and
Utuado (18.175850 -66.4155700). The largest coffee farm (5-ha)
where W. auropunctata populations occurred was located in
Orocovis and this farm had the highest shade level (Figure 2).
Field surveys
\label{field-surveys}
Surveys were conducted to map the spatial distributions and abundance of
dominant ant species. We walked dense trail systems by placing tuna
baits on coffee plants approximately every 4 meters. Baits were checked
every 30 minutes for the presence of ant species. A total of 1181 baits
were placed within the 45-ha plot, 992 baits within the low-shade coffee
farm, and another 229 baits within the rustic 6-ha plot (Figure 1).
Detailed descriptions of the 45-ha coffee farm in Mexico have been
reported elsewhere (Vandermeer
2010).
In Puerto Rico, we placed a total of 664 baits across all 10 coffee
farms (32 baits per ha, approximately 20 ha in total farm size). Site
locations in both Mexico and Puerto Rico were selected so that native
ant species, both arboreal and ground foraging ants, overlapped in their
ranges with W. auropunctata populations. Our baiting method did
not set out to sample the entire community, but instead focused on
dominant species that engage in competitive
interactions (Armbrecht
2003). Differences in farm size reflected the fact that coffee farms in
the Soconoscu regions of Mexico are relatively large in size (300-ha) as
compared to the central region of Puerto Rico, where the average farm
size is considerably small (2-5 ha).
Short-term competition
experiment
\label{short-term-competition-experiment}
We conducted short-term competition experiments between W.
auropunctata and native ant species. In Mexico, competition experiments
were performed on the ground between W. auropunctata and native
ants Solenopsis geminata and Pheidole protensa. Arboreal
competition experiments in turn were conducted with Solenopsis
picea and Pheidole synanthropica species. In Puerto Rico, we
conducted short-term experiments between W. auropunctata and the
native ground-foraging ant Solenopsis invicta.
For our terrestrial competition experiments, we recorded the timing of
resource discovery, recruitment, and the total number of individual
workers at baits by placing ten baits (i.e. tuna) in a 1-m line right at
the border between ant colonies and subsequently checked the baits at
30-sec intervals for up to 80 minutes
was separated by 10 cm within sites where species co-occurred. The
intent of this experimental setup was to sample right at the border
between monospecific patches were competition took place. For our
arboreal competition experiments in the field, we placed five baits on
bamboo branches between coffee trees inhabiting ant nests. Each of the
five sites was separated by 10 cm located between arboreal nesting
sites. We recorded the discovery time, recruitment time, and the total
number of individual workers at baits.
\label{section}
Long-term competition
experiments
\label{long-term-competition-experiments}
For the long-term competition experiments in Mexico, we used platforms
to connect plastic containers inhabiting W. auropunctata and
S. picea nests in a common foraging arena for 14-days. Holes were
drilled in the plastic containers to allow ants from leaving the nest to
the platform were the resources were placed. To prevent ants from
escaping we placed the containers in a water bath. Prior to our
laboratory experiment, we conducted field trials to identify potential
dominant arboreal ants in the field. We selected S. picea nests
due to their dominance in coffee plants and relative ease of nest
collection. Caution was taking to collect nests that had sufficient
amount of queens, workers, and brood in order to keep the nests viable
in the lab. Each day the ants were supplied with sugar water and tuna in
the lab to enable both species to compete for resources. We used 6
replicates in the experiment with different pairs of unique nest that
had not previously been exposed to each other. Controls consisted of
nests pairs that were not connected (n =2 pairs) with a platform. In
Puerto Rico, we followed the same protocol for assessing the long-term
competitive dynamics between W. auropunctata and the arboreal ant
L. iniquum . We used 8 connected pairs of W. auropunctata
and L. iniquum nests in the experiment and 2 pairs that served as
control replicates.
Analysis
\label{analysis}
For all the competition experiments, we analyzed the differences among
species with respect to total number of workers at baits. Prior to
conducting statistical analyses, we plotted the data to test for
normality using the Shapiro-Wilk test. Because of the non-normality, we
used the non-parametric Kruskal-Wallis rank sum test with the library
stats(R Core Team 2013). Nemenyi’s post-hoc tests were applied for
pairwise multiple comparisons using the PMCMR package in R, v. 2.15.
ANOVA analysis was performed to detect differences in the number of live
ant workers found between treatments in the long-term competition
experiments.
\label{section-1}
Results
\label{results}
Within the native range, we found a low overall abundance of W.
auropunctata surveyed in Mexico relative to its introduced range of
Puerto Rico, where W. auropunctata was found to occur in much
higher abundances. In the 45-hectare plot in Mexico (medium-shade
organic coffee), we documented a total of 84 morpho-species, 3.4 % of
which consisted of W. auropunctata found at baits. In the
30-hectare plot (low-shade conventional farm), we documented a total of
58 morphospecies of which only 0.4% occupied baits by W.
auropunctata. In the 6-hectare plot (rustic coffee, within high shaded
coffee), we detected W. auropunctata at 7.9 and 3.9%
respectively at arboreal baits, whereas ground-baits occupancy by
W. auropunctata was only 0.5%. While W. auropunctata
distribution on the farm was limited in the native range, we detected a
large cluster of W. auropunctata colonies that presumably make up
part of a larger super-colony (Figure 1). In Puerto Rico, we detected a
total of 16 morpho-species throughout our surveys on 10 smaller-sized
coffee farms (ranging from 1-6 ha). On average, we found 41.7 % of
arboreal trees occupied by W. auropunctata. In most cases,
W. auropunctata was widely distributed across all farms reaching
high densities in patches it dominated thereby excluding other ant
species from occupying nearby trees.
Overall, we found that W. auropunctata was patchily distributed
between Mexico and Puerto Rico. The main difference, however, is that
patches dominated by W. auropunctata included a greater diversity
of native ant species in Mexico. For example, native species diversity
in the largest patch (1 ha) ranged anywhere from 30-50 native ant
species, with only 40 % of baits occupied by W. auropunctata
(Figure 1). In Puerto Rico, farms had on average less than 20 native ant
species present, with the largest patch only containing 2 dominant
arboreal ant species (Figure 2).
Short-term competition: Mexico and Puerto
Rico
\label{short-term-competition-mexico-and-puerto-rico}
Competition between W. auropunctata and native ant species
revealed important differences during contests. Interactions with
S. geminata showed that W. auropunctata was able to
rapidly recruit workers to baits during the first 20 minutes of the
experiment (Figure 3 a), after which S. geminata took over and
dominated the majority of baits by the end of the experiment
(\(x^{2}=\)55.976, p < 0.0001). Competitive interactions
between W. auropunctata and P. protensa revealed
oscillatory dynamics (Figure 3 b). W. auropunctata rapidly
increased at baits within the first 25-minutes after which P.
protensa dominated for some time until getting surpassed by W.
auropunctata (\(x^{2}\)=15.641, p < 0.0001). Arboreal
competitive interactions between W. auropunctata and S.
picea were equally intense. S. picea initially dominated the
baits but was overtaken by W. auropunctata after 30-minutes
(Figure 3 c). Despite S. picea maintaining a constant recruitment
rate throughout the experiment, W. auropunctata steadily
increased recruitment of workers enabling it to dominate most baits
(\(x^{2}\)= 9.8396, p=0.0017). However, the arboreal ant P.
synanthropica was competitively superior against W. auropunctata
(Figure 3 d) during the experiment resulting in the complete dominance
of baits (\(x^{2}\)= 69.03, p < 0.0002). In Puerto Rico,
we compared competitive dynamics with W. auropunctata and the
dominant ant competitors S. invicta and L. iniquum.
W. auropunctata initially increased its recruitment rate in
response to S. invicta but was quickly overtaken by S.
invicta as more of its workers dominated baits. Although we didn’t
detect a significant interaction in the competition experiment
(\(x^{2}=\)3.485, p=0.062) S. invicta held on to more baits and
its rapid recruitment of workers to baits enabled them to push out
W. auropunctata workers (Figure 4).
Long-term competition: Mexico and Puerto
Rico
\label{long-term-competition-mexico-and-puerto-rico}
W. auropunctata workers were superior against S. picea
during the long-term experiment in Mexico (Figure 5). We observed
greater survival of W. auropunctata workers in the 14-day
experiment (F=5.43, p=0.013). During the first couple of days, S.
picea recruited higher number of workers to the foraging arena and
displaced W. auropunctata workers at baits in the majority of
replicates. As aggression intensified, S. picea preempted
W. auropunctata workers from accessing resources. In response,
small groups of W. auropunctata workers attacked S. picea
individuals from the arena. In most of the replicates, we observed that
W. auropunctata had a clear numerical advantage over S.
picea. In five of our replicates, W. auropunctata invaded the
nest boxes of S. picea resulting in a high worker density of
W. auropunctata including many brood and queens. In one replicate
(#3), we observed a nest invasion by W. auropunctata workers
into a S. picea nest, with queens and brood moved into the
invaded nest. Further inspection into nests with a tiny camera revealed
that W. auropunctata workers frequently dispersed their brood and
queens within nests. In Puerto Rico, the number of live W.
auropunctata workers was not significantly higher than L.
iniquum (F=1.87, p=0.17). In the first two days, L. iniquum was
much faster at recruiting workers to baits compared to W.
auropunctata. In about one quarter of the replicates, few L.
iniquum workers were found alive in the nest boxes as they were killed
by W. auropunctata workers. We did observe occasional fighting
between species, but L. iniquum was quick enough to avoid
W. auropunctata workers in the foraging arena (Figure 6).
\label{section-2}