Insectes Sociaux
https://doi.org/10.1007/s00040-021-00810-y
Insectes Sociaux
RESEARCH ARTICLE
Tandem communication improves ant foraging success in a highly
competitive tropical habitat
S. M. Glaser1
· R. M. Feitosa2 · A. Koch3 · N. Goß1 · F. S. do Nascimento4 · C. Grüter1,5
Received: 25 August 2020 / Revised: 10 January 2021 / Accepted: 6 February 2021
© The Author(s) 2021
Abstract
Tropical ants experience intense intra- and interspecific competition for food sources, which influences their activity pattern
and foraging strategies. Even though different ant species can coexist through spatial and temporal niche partitioning, direct
competition for food cannot be avoided. Recruitment communication is assumed to help colonies to monopolize and exploit
food sources successfully, but this has rarely been tested under field conditions. We studied if recruitment communication
helps colonies of the Neotropical ant Pachycondyla harpax to be more successful in a highly competitive tropical environment. Additionally, we explored if temporal and spatial niche differentiation helps focal colonies to avoid competition.
Pachycondyla harpax competed with dozens of ant species for food. Mass-recruiting competitors were often successful in
displacing P. harpax from food baits. However, when foragers of P. harpax were able to recruit nestmates they had a 4-times
higher probability to keep access to the food baits. Colonies were unlikely to be displaced during our observations after a
few ants arrived at the food source. Competition was more intense after sunset, but a disproportionate increase in activity
after sunset allowed focal colonies to exploit food sources more successfully after sunset. Our results support the hypothesis
that recruitment communication helps colonies to monopolize food sources by helping them to establish a critical mass of
nestmates at large resources. This indicates that even species with a small colony size and a slow recruitment method, such
as tandem running, benefit from recruitment communication in a competitive environment.
Keywords Ant · Competition · Pachycondyla harpax · Recruitment · Tandem running
Introduction
* S. M. Glaser
simone-glaser1@gmx.de
1
Institute of Organismic and Molecular Evolution, Johannes
Gutenberg University, Hanns-Dieter-Hüsch-Weg 15,
55128 Mainz, Germany
2
Departamento de Zoologia, Universidade Federal do Paraná,
Caixa Postal 19020, Curitiba, PR 81531-980, Brazil
3
Animal Comparative Economics Laboratory, Department
of Zoology and Evolutionary Biology, University
of Regensburg, 93053 Regensburg, Germany
4
Depto. de Biologia da Faculdade de Filosofia, Ciências e
Letras de Ribeirão Preto, Universidade de São Paulo (USP),
São Paulo, Brazil
5
Present Address: School of Biological Sciences, University
of Bristol, 24 Tyndall Avenue, Bristol BS8 1TQ, UK
The tropics are home to thousands of ant species, some
forming colonies containing millions of ants. Collectively,
their biomass exceeds the biomass of all wild mammals
combined (Bar-On et al. 2018) as they fulfill vital ecological
roles as predators, herbivores or soil architects (Hölldobler
and Wilson 1990; Davidson et al. 2003). Competition for
food sources among colonies can be intense, but intra- and
interspecific competition is often reduced through a variety
of mechanisms (Hölldobler 1981). Often species occupy
particular dietary niches, e.g. by exploiting different food
types (sugars, carrion, excrements, seeds, and live prey)
or food sizes (Torres 1984; Houadria et al. 2015). Additionally, species can show temporal activity patterns that
allow them to avoid competitors (Torres 1984; Stuble et al.
2013; Houadria et al. 2016; Rosumek 2017). For instance,
nocturnal species like some Myrmecia or Polyrhachis ants
have adapted to low light levels by developing large eyes
and efficient navigational strategies (Narendra et al. 2013a,
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S. M. Glaser et al.
b, 2017). On the other hand, activity patterns of tropical
species are also dependent on moisture gradients (Kaspari
and Weiser 2000).
Despite these mechanisms of niche differentiation, competition cannot be avoided entirely. The foraging strategies
used by the different species are likely to have a strong
impact on the ability of colonies to monopolize and exploit
food sources fast and efficiently (Traniello 1987, 1989a;
Lach et al. 2010; Drescher et al. 2011; Grevé et al. 2019). In
particular, communication and recruiting other nestmates to
food sources should increase a colony’s chances of displacing competitors and gaining long-term access to food.
Communication among nestmates is widespread in ants
and other social insects (Beckers et al. 1989; Hölldobler
and Wilson 1990; Jarau and Hrncir 2009; Almeida et al.
2018; Glaser and Grüter 2018; Grüter and Czaczkes 2019).
It allows the members of a colony to exchange information about their environment, such as the locations of food
sources or the presence of predators and competitors (Kendal et al. 2004; Dawson and Chittka 2014; Lanan 2014).
During communication, ants may use tactile signals (e.g.
antennation, drumming or vibrations (Hölldobler 1999;
Franklin 2014)) or chemical signals (e.g. alarm or trail
pheromones (Hölldobler 1976, Traniello 1989b, Lach et al.
2010; Czaczkes et al. 2015)). Ant species with large colony
sizes often use chemical mass-recruitment with short- or
long-lasting trails, trunk trails, and mass-raids (Beckers
et al. 1989, Traniello 1989a, Hölldobler and Wilson 1990,
Lanan 2014; Czaczkes et al. 2015). Species with smaller
colonies use recruitment strategies like tandem running or
group recruitment (Möglich et al. 1974; Beckers et al. 1989;
Liefke et al. 2001).
In tandem running, an informed ant returns to the nest
after finding a good nest site or a rewarding food source that
is too large to be exploited by a single ant. In the nest, she
releases a pheromone to attract a potential recruit (Möglich
et al. 1974). When the pair walks towards the resource,
the follower antennates the leader’s gaster and hind legs
to maintain cohesion (Franklin 2014). Although ants in a
tandem run-walk slower than ants walking alone, tandem
recruitment could save time if resources are hard to find by
independent search (Franks and Richardson 2006). Many
species (e.g. in Temnothorax or Pachycondyla) use tandem
running for both nest emigrations and foraging recruitment
(Colin et al. 2017; Grüter et al. 2018), whereas others (e.g.
Neoponera or Diacamma) perform tandem runs only during
colony migrations, but not during foraging (Fresneau 1985;
Kaur et al. 2017). This raises the question whether and how
tandem running might improve foraging success and, in particular, whether tandem recruitment might improve foraging
success when the competition is intense.
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Tropical ants with small colony sizes might be particularly prone to direct competition, so-called interference competition, because they have to compete with mass-recruiting
species that use pheromone trails to recruit large numbers
of foragers and soldiers that are specialized to fight (Dejean
et al. 2005; Czaczkes et al. 2011, 2015; Czaczkes and Ratnieks 2012). It seems highly plausible that communication
helps mass-recruiting colonies to monopolize food sources,
but it remains unclear whether this is also the case in species
with small colonies that use slower forms of communication,
such as tandem running. So far, only very few studies have
assessed the role of communication in foraging competition
in ants. One such study by Dejean et al. (2005) found that
Pheidole megacephala (Fabricius, 1793) increases recruitment when they perceive competitors near food sources.
Most ponerine ants live in small colonies (often just a couple
of hundred individuals or less), they are important generalist
arthropod predators and show a diversity of foraging strategies (Nascimento et al. 2012; Schmidt 2013), one of which
is tandem recruitment (Grüter et al. 2018).
Here, we tested if recruitment communication helps colonies to be more successful in a highly competitive tropical
environment. As a model system, we studied Pachycondyla
harpax (Fabricius, 1804), a common Neotropical species
that usually uses tandem running to recruit nestmates to
newly discovered food sources (Grüter et al. 2018). A previous study observed that P. harpax foragers are often displaced at food sources by aggressive competitors, mainly
Pheidole (Grüter et al. 2018). First, we described and quantified the main competitors of P. harpax in a Brazilian environment. Second, we tested our main prediction that tandem
recruitment helps colonies to access food sources that would
otherwise be monopolized by competitors. Third, we tested
if P. harpax might follow a strategy of temporal and spatial
niche differentiation to avoid competition, e.g. by foraging
in locations and during times when competition for food is
lower.
Materials and methods
Study site and study species
Experiments were performed in March 2018 and February/
March 2019 on the campus of the University of São Paulo
in Ribeirão Preto, Brazil. Our study species Pachycondyla
harpax forages for dead and living insects and plant seeds
(Grüter et al. 2018). If scouts detect food items, they cannot carry home by themselves, e.g. beetle larvae or caterpillars, they often initiate tandem runs to recruit nestmates
to the food source. This species is common in the study
area and nests underground (Grüter et al. 2018). Colony
Tandem communication improves ant foraging success in a highly competitive tropical habitat
sizes range from 15 to 100 individuals that aggressively
defend food sources against many smaller ants (Wheeler
1900).
Experimental setup and procedure
All experiments were conducted in the field in three different locations on the campus, where P. harpax occurred.
We located and marked colonies by following foragers
who return to their nest after offering them small pieces
of cheese (mozzarella or “queijo minas”).
Part 1: interspecific competition depending on food types,
daytime and territory
We first attempted to identify competitors of P. harpax
and explored whether our focal species has a preference
for different baits. We consider other ant species that forage at the same time and collect the same food type to be
competitors. This does not imply aggressive interactions,
i.e. interference competition since also non-aggressive
species can reduce the foraging success of focal colonies
via exploitation competition (Human and Gordon 1996;
Lach 2005). Furthermore, we checked if P. harpax face
different levels of competition at different food types and
distances from the colony entrance. We tested 15 colonies with four different food sources: we used honey and
pieces of mango (approx. 1 cm3) as carbohydrate baits and
cheese cubes (approx. 1 cm3) or meat (pieces of sausage
or mealworms) as protein-rich food sources. Food baits
were placed at two different distances from the colony
entrances: either at 30 cm (“inner territory”) or at 100 cm
(“outer territory”). Previous research has shown that most
food items are collected < 100 cm from the nest entrance
(Grüter et al. 2018).
Furthermore, we tested if P. harpax face stronger competition during the daytime or at night. We offered food
baits (cubes of cheese, approx. 1 cm3) during the morning
(9.00–12.00 h) and after sunset (18.30–21.00 h). Due to the
low activity of P. harpax in the afternoon, we did not test for
competition during that time. We again tested the influence
of distance from the nest.
After providing a food source, we recorded the number
of different ant species (competitors) at the food bait during
and at the end of a 10-min observation period. In case an ant
species could not be identified by the observer, specimens
were collected for later identification. Ants were identified
by comparison with the species of the Entomological Collection Padre Jesus Santiago Moure, Universidade Federal
do Paraná, Curitiba, Brazil (DZUP), where the vouchers
were deposited.
Part 2: exploitation and recruitment depending
on competition
We provided food baits to 42 individual foragers of P. harpax (31 colonies). After they accepted the food and, thus,
were the first species at the food source (treatment bait, without competition at the beginning), we provided a second
food source as a control bait approx. 30 cm from the first
food source and at a similar distance to the nest. The second
food source was normally discovered quickly by competitors but could also be found by P. harpax. The second bait
allowed us to perform a paired comparison between the two
baits near a colony. As soon as the food sources were placed,
we started filming (JVC GZ-GX1 camcorder) the immediate
surroundings of the two food baits. In some trials, we made
still images of the control bait. We recorded at least one
image per minute. Additionally, both baits were regularly
inspected. Each trial was filmed for approx. 60 min. Observations ended earlier if other ant species displaced P. harpax
from the first bait. It was not possible to quantify the number
of food that was removed from the bait without disturbing
the experiments. We frequently observed single foragers, to
breaking-off bits and to walk away and transporting it back
to the nest.
During video analysis, we recorded the distance of each
bait from the nest (whenever possible), the probability of
recruitment by P. harpax colonies, the maximum number
of P. harpax foragers at the bait (at the same time), whether
and for how long P. harpax foragers had access to the bait,
the time until competitors found the bait and if there was a
takeover (within 60 min after initial discovery P. harpax did
not have access anymore) by competitors. P. harpax foragers were considered to have access to the food source (yes
or no) when the individuals of a colony had access to the
food source for at least 15 min and were able to collect and
exploit the food bait, even if there were other non-aggressive
ant species present. We considered a takeover by another ant
species to have occurred when P. harpax could no longer
feed at the bait.
Part 3: daily activity of Pachycondyla harpax
We observed that P. harpax appeared to be more active after
sunset (unpublished data; see also García-Pérez et al. 1997).
To confirm this, we observed 15 colonies at various locations on the campus during several days (14 March 2019–21
March 2019), from 9.30 h in the morning until 20.00 h in
the evening. Each colony was observed for one minute and
all P. harpax individuals in an area of one meter around
the nest entrance were recorded. If we found no focal ant,
the colony was considered to be inactive. After sunset, we
explored the surrounding of the nest entrance using the light
of headlamps.
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S. M. Glaser et al.
Part 4: food exploitation success depending on daytime
Results
To compare the foraging success of P. harpax during the
daytime (9.30–12.00 h) and after sunset (18.30–21.00 h),
we tested 15 colonies in both time periods and provided
cheese baits for individual P. harpax foragers. Every five
minutes during a 45-min observation period we performed
a scan-sampling and checked whether foragers from the
focal colony still had access and recorded the maximum
number of foragers that were simultaneously present at
the food source. This allowed us to explore the competitive performance of colonies during the day and at night.
Interspecific competition depending on food types
and territory
Overall, we identified almost 40 different ant species at our
baits during the 10-min observation periods (Table 1). The
most common competitors of P. harpax were mass-recruiting Pheidole species (mostly Pheidole oxyops Forel 1908),
Odontomachus sp.; rarely, we found Atta or Camponotus
at a food bait (Fig. 1). A similar number of ant species
Statistical analysis
Table 1 Competing ant species observed at different food baits during our observations
All tests were performed in R 3.5.3 (R Development Core
Team 2019). We performed linear mixed-effect models
(LMEs) for normally distributed response variables and
generalized linear mixed-effect models (GLMMs) for
response variables with a binomial or Poisson distribution (Zuur et al. 2009). For the competition and food
exploitation experiments, colony ID was used as a random effect to account for the potential non-independence
of observations from the same colony. Location was used
as a random factor for the recruitment experiments (Zuur
et al. 2009). For the activity analyzes, we used colony and
date as random factors. In part 1, we tested the role of the
fixed effects “daytime”, “colony territory” (inner vs. outer)
and “food type” on the presence of competitors and P.
harpax activity. In part 2, to test the influence of recruitment on the foraging success, we used the fixed effects
“maximum number of P. harpax foragers at the baits” and
“recruitment” (yes or no) to test if they predicted whether
P. harpax had access (yes or no) to the food bait. Since
these predictors are linked, we explored their importance
separately. With a McNemar’s test we analyzed if the probability to recruit was higher at the treatment than at the
control feeder. To test for significant interactions among
the fixed-effects, we used likelihood ratio tests (LRT)
and compared the model without the interaction with the
model containing the interaction. Non-significant interactions were removed from the model. In part 3, we tested
if colony activity (ants vs. no ants) depended on the time
of the day. In part 4, we quantified the foraging activity of
focal colonies depending on the time interval during the
45-min observation period.
Subfamily
Species
Dolichoderinae
Dolichoderus bispinosus
Linepithema gallardoi
Brachymyrmex sp.
Camponotus (Myrmaphaenus) sp. 1
Camponotus (Myrmaphaenus) sp. 2
Camponotus ager
Camponotus atriceps
Camponotus substitutus
Sericomyrmex mayri
Acromyrmex sp.
Apterostigma gr. pilosum
Atta sexdens
Crematogaster erecta
Nesomyrmex sp.
Pheidole angusta
Pheidole gertrudae
Pheidole oxyops
Pheidole sensitiva
Pheidole sp. 1
Pheidole sp. 2
Pheidole sp. 3
Pheidole sp. 4
Pheidole aff radoszkowskii sp. 1
Pheidole aff radoszkowskii sp. 2
Pheidole aff subarmata
Solenopsis decipiens
Solenopsis sp.
Mycetomoellerius sp.
Wasmannia auropunctata
Hypoponera sp.
Neoponera verenae
Neoponera villosa
Odontomachus chelifer
Odontomachus sp.
Pachycondyla striata
13
Formicinae
Myrmicinae
Ponerinae
Tandem communication improves ant foraging success in a highly competitive tropical habitat
Fig. 1 Study species and competitors at food baits. a Pachycondyla
harpax defending the food source against Wasmannia auropunctata.
b Atta sexdens picking up and carrying away the cheese bait. c Work-
ers and soldiers of mass recruiting Pheidole oxyops (Photo by Tomer
Czaczkes). d Odontomachus chelifer carrying away a small piece of
cheese
discovered the different types of food during the 10-min
observation period, irrespective of the distance from the
P. harpax focal colony (range = 30–100 cm, 2.68 ± 1.20
species [mean ± sd]). There was a borderline significant
difference between the total number of species that discovered honey compared to meat, with more species collecting honey than meat (GLMER: inner vs. outer territory: z = − 0.792, p = 0.428; food sources: meat vs. honey:
z = 2.080, p = 0.038; meat vs fruit: z = 0.816, p = 0.415; meat
vs. cheese: z = 0.931, p = 0.352; cheese vs. honey: z = 1.190,
p = 0.234; cheese vs. fruit: z = − 0.095, p = 0.924; fruit vs.
honey: z = 1.252, p = 0.211). At the end of the 10-min observation period, the number of ant species at the food baits
decreased to 1.36 ± 0.76 species and there was no difference between food types (GLMER: inner vs. outer territory: z = − 0.643, p = 0.520; food sources: meat vs honey:
z = 1.500, p = 0.134; meat vs fruit: z = − 0.067, p = 0.947;
meat vs. cheese: z = 0.420, p = 0.675; cheese vs. honey:
z = 1.104, p = 0.269; cheese vs. fruit: z = − 0.479, p = 0.125;
fruit vs. honey: z = 1.536, p = 0.211). This reduction is likely
due to the displacement of weakly competitive species by
competitively superior species.
Exploitation and recruitment depending
on competition
We found that after offering P. harpax foragers a bait, a substantial proportion of ants initiated tandem recruitment. In
42.9% (18 out of 42) of all trials, at least one forager started
recruiting. The control bait was found in 38.1% (16 out of 42)
of all trials by at least one P. harpax forager. Tandem recruitment to the control bait occurred in 37.5% (6 out of 16) of
these trials (14.3% of all trials). Overall, tandem recruitment by P. harpax foragers was significantly more likely at
the treatment bait than at the control bait (McNemar’s test:
χ2 = 6.050, df = 1, p = 0.014). The distance between the nest
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S. M. Glaser et al.
and the food source did not influence recruitment probability
(GLMER: z = 1.052, p = 0.293). When comparing the number of P. harpax foragers at the two baits, we found no correlation between the maximum number of ants at the treatment and control feeder (GLMER: z = − 0.653, p = 0.514). A
positive correlation might have been expected if the number
of ants at the two paired baits would have been the result of
the colony size of the focal colony or reflected the level of
competition in the area of the focal colony. Furthermore,
competitors found the treatment and control feeder equally
fast (treatment: 1.66 ± 2.28 min vs. control: 2.05 ± 1.79 min
(mean ± sd); GLMER: z = − 1.318, p = 0.187) and there was
no correlation of time of discovery by competitors (GLMER:
z = 1.526, p = 0.127).
We predicted that recruitment would lead to an increase
in ants at the bait and, in turn, a higher probability to have
access to the food bait. The results show that significantly
more ants reached the food source when recruitment took
place (Fig. 2a) (GLMER: z = 5.942, p < 0.001). Thus, when
ants performed more tandem runs, the maximum number of ants that were present at a bait increased (GLMER:
z = 4.486, p < 0.001). During a trial, individual foragers were
often seen walking to the nest with small pieces of food
and, subsequently, return to the food source in a tandem run
or alone. We found that recruitment was associated with
a more than 4-times higher probability to have access to
the food source (no recruitment: 20.8% vs. recruitment:
88.9%) (Fig. 2b) (GLMER: z = 2.723, p = 0.006). Related
to these two findings, we predicted that colonies are more
likely to keep access if more ants are at the food source. We
found that the probability of having access increased significantly with an increasing number of foragers at the food bait
(Fig. 2c) (GLMER: z = 2.723, p = 0.006): P. harpax colonies
had a 100% access chance when at least three ants were at
the food source.
When competitors took over the food source at any time
during the 60-min observation period, P. harpax stopped
recruiting. We tested if an increasing number of foragers at
the food source lowered the chance of a takeover by another
species and indeed found this to be the case (GLMER:
z = − 3.087, p = 0.002). When there were at least five ants of
P. harpax at the food bait, takeover was extremely unlikely
(Fig. 2d).
Activity cycle
We found in the first experiments that P. harpax has
an increased activity after sunset (~ 6.30 pm) (see also
García-Pérez et al. 1997). Therefore, we quantified the
activity of 15 colonies from early morning (sunrise ~ 6.15
am) until after sunset (9:30 h to 20:00 h) over eight days
(Fig. 3). There was substantial variation in activity
throughout the day. As described by García-Pérez et al.
13
(1997) in a different area, activity was generally low during the day and increased in the evening around 17.00 h up
to 18.30 h (GLMER: χ2 = 84.133, df = 7, p < 0.001). While
observing the colony activity, we also measured the temperature throughout the day. The morning counts ended
around 11 am (26.88 °C ± 1.63 °C). The afternoon counts
lasted from 12:30 pm until 5 pm (28.70 °C ± 1.72 °C).
Sunset was typically around 6:30 pm. This is when our
evening measurements started (24.70 °C ± 1.34 °C). The
temperature was always measured a few cm above the
ground in shaded areas.
Interspecific competition depending on daytime
and territory
One explanation for the increased activity at night could be
that colonies face less competition than during the daytime.
Thus, we compared the number of ant species at food baits
in the morning vs. the evening. Contrary to our expectation, we observed that significantly more competitor species
discovered the bait after sunset (Fig. 4a) (LME: t = − 2.355,
p = 0.024). There was also a tendency for more ant species to discover the bait closer to the nest entrance (LME:
t =− 1.753, p = 0.087).
The probability that P. harpax foragers would discover
the baits during the 10-min observation period was higher
at night than during daytime (Fig. 4b) (GLMER: z = − 2.332,
p = 0.020). This probability did not depend on the distance
of the cheese bait from the nest entrance of the focal colonies
(GLMER: z = − 0.354, p = 0.724). There was a borderline
non-significant trend that P. harpax were more likely to still
have access to the food at night compared to daytime at the
end of the 10-min observation period, (GLMER: daytime:
z = 1.910, p = 0.056; territory: z = − 0.363, p = 0.716). The
most frequent and successful competitor was the massrecruiting Pheidole oxyops (present in 62.2% experiments)
(Fig. 1c).
Food exploitation and access depending on daytime
We then presented individual P. harpax foragers with cheese
baits to explore whether time of day affected their ability to
maintain access to the food source during a 45-min observation period. During daytime, the number of foragers at
the bait remained constant and low, whereas the number
of P. harpax at the food increased after sunset (Fig. 5a, b)
(GLMER: morning vs. evening: z = − 8.056, p < 0.001; time:
morning: χ2 = 10.033, df = 8, p = 0.263; evening: χ2 = 27.66,
df = 8, p < 0.001).
Not all colonies were able to keep access to the food bait
over the 45 min. After sunset, more colonies kept access to
the food source than in the morning (morning: 18.5% vs.
Tandem communication improves ant foraging success in a highly competitive tropical habitat
Fig. 2 Maximum number of ants (a) and the probability of ants at the
food source (b) depending on whether our focal colony performed
tandem recruitment. Probability of access (c) and of a food takeover
by a competitive ant species (d) depending on the maximum number
of ants at the food source. Access refers to a period of exploitation
of at least 15 min during the observation period. Takeovers occurred
when focal colonies were displaced during the 60 min observation
period. Boxplots show median, 25th and 75th quartile and the 5th and
95th percentile. Bar plots show means and SE. Note that all values
in (c) and (d) are either 1 or 0 but that jitter was used to better visualize the data points. Grey areas show the 95% confidence interval.
***p < 0.001
evening: 58.6%) (Fig. 5c, 5d (GLMER: morning vs. evening:
z = − 8.056, p < 0.001; time: morning: χ2 = 3.2 × 1010, df = 8,
p < 0.001; evening: χ2 = 801.82, df = 8, p < 0.001).
Discussion
Our results support the hypothesis that recruitment communication by tandem running increases access to food
sources and, thus, foraging success in Pachycondyla harpax. Competition in this Brazilian habitat was intense for
all types of food as almost 40 different ant species discovered and exploited our baits during our observations. This
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S. M. Glaser et al.
Fig. 3 The probability of colony
activity of P. harpax foragers
during daytime over 8 days
(n = 15). Sunset was around
18.30
Fig. 4 Number of different competitors (a) and the probability (b) that P. harpax would discover the bait during 10 min depending on the time
of day and the distance from the entrance of the focal colony (territory). Sample sizes refer to the number of trials. n.s. not significant, *p < 0.05
intense competition is not surprising given that P. harpax
is a generalist forager, like many other Neotropical ant species. Confronted with big food items, foragers attempted to
cut off small pieces of food and transport them back to the
nest. However, they were frequently displaced by competitor species. Although several different species can discover
a food source, only a few of them remain at the food bait
over longer time periods. This reduction is likely due to
displacement by competitively superior species. The most
abundant competitors were Pheidole spp. (Table 1; 94.6%
of all observations), which are very efficient and aggressive
mass-recruiters (Czaczkes et al. 2011; Czaczkes and Ratnieks 2012). While it was not possible to collect data on the
number of competing individuals at baits, the observations
13
on the dominance of Pheidole spp. suggest that the number
of competing ants affects the ability of P. harpax to access
and defend food items. In some cases, however, a single
individual of Odontomachus or Neoponera could banish
their competitors, demonstrating that there is not always a
straightforward relationship between the number and dominance of competitors. Different competitors could also fight
against each other and thereby give a third party the opportunity to have access and exploit a food bait.
It is often assumed that mass-recruitment via pheromone
trails helps colonies to monopolize food sources (de Biseau
et al. 1997; Detrain and Deneubourg 2008; Drescher et al.
2011). Accordingly, Pheidole megacephala scouts start
recruiting more nestmates and soldiers to a food source
Tandem communication improves ant foraging success in a highly competitive tropical habitat
Fig. 5 Number of individual P. harpax workers and the probability of colony presence at food baits during the 45-min period in the morning (a,
c) and evening (b, d). n.s. not significant, ***p < 0.001
if pheromones from competing colonies are encountered
(Dejean et al. 2005). Our results support and extend this
view by showing that also species with small colonies
employing relatively slow recruitment mechanisms are
likely to benefit from recruitment communication. When
P. harpax foragers had an opportunity to recruit nestmates
to a food source, their foraging success was much higher:
focal colonies with recruitment were 4 times more likely
to keep access to the food during our observations. This is
likely to allow more foragers to recruit further ants, leading
to positive feedback and a larger number of ants at the food.
The bait was unlikely to be taken over by competitors when
about five or more P. harpax foragers were at the food source
(Fig. 2d). When P. harpax foragers found the food source by
chance, they were often not able to exploit it for longer time
periods if competitors were already present and prevented
other P. harpax ants to recruit nestmates. When focal foragers discovered the bait before competitor species, as was
the case at the treatment bait, tandem recruitment was much
more frequently observed compared to the control bait (43%
vs. 14%), which was randomly placed in the vicinity of the
same nest. Thus, finding a food source first, before competitor species, is of critical importance to foraging success. The
recruitment probability in P. harpax is comparable or higher
13
S. M. Glaser et al.
than in other species that use recruitment methods other than
chemical trails. For example, about 10% of returning honeybee foragers perform a waggle dance (Seeley 1995) and ~ 10
to 30% of ant foragers lead tandem runs to food sources in
Cardiocondyla venustula and Temnothorax nylanderi (Wilson 1959; Glaser and Grüter 2018).
Competition might be less intense in some areas, allowing more P. harpax foragers to have access for longer and to
recruit nestmates to exploit the food source. A large number
of P. harpax at a bait might also indicate a large colony
size. In both cases, we would expect a positive correlation
between the paired treatment and control baits in terms of
the number of P. harpax foragers exploiting them. In other
words, the two baits in the proximity of a particular nest
should be similar in the number of P. harpax foragers. However, this was not the case in our study as the number of P.
harpax foragers at the treatment feeder was unrelated to the
number at the paired control feeder. Additionally, there was
no correlation in how quickly competitors found the treatment and control feeder. This finding, in combination with
our other findings, suggests that the number of ants at a bait
is largely the result of discovering a food source first, followed by successful recruitment. Colony size might still be
an important factor for competitiveness. When a colony is
larger, more individuals can scout or be recruited to a food
source. Hence, larger colonies are probably more successful
during foraging compared to smaller colonies (Dornhaus
et al. 2012). In addition, foragers from larger colonies might
also be more aggressive (Oster and Wilson 1978), which
would further affect access to food sources.
One possibility to avoid competition might be to forage during different times of the day, as is the case with
nocturnal and diurnal species (Rosumek 2017). In a study
on grassland ants, for example, different species foraged
at different times of the day depending on air temperature
(Albrecht and Gotelli 2001). This temporal niche partitioning can help subdominant species to avoid dominant species (Stuble et al. 2013). Stingless bees, likewise, shift their
activity to avoid the presence of other, mainly aggressive
species (Nagamitsu and Inoue 1997, Keppner and Jarau
2016). In the tropics, species also can adapt to different seasons, e.g. by being more active during the rainy seasons
(Baumgartner and Roubik 1989), whereas others are active
during both seasons. In accordance with a previous study
(García-Pérez et al. 1997), we observed that the activity of P.
harpax increases in the afternoon and is highest after sunset.
Thus, we hypothesized that this shift in activity is due to the
competition being less intense after sunset. Contrary to this
expectation we found that competition seemed to be even
stronger after sunset than during the morning/daytime: we
found a 33% increase in the number of competitor species
at the food baits after sunset. A possible explanation might
be that most ant species start becoming more active when
13
temperatures are going down and humidity increases to prevent water loss (Schilman et al. 2007). The > 100% increase
in P. harpax activity after sunset (Fig. 3) more than compensated for the increase in competitor species after sunset
(Fig. 4) and, as a result, P. harpax colonies were better able
to defend and exploit food sources after sunset (Fig. 5). After
45 min, only 18.5% of the colonies maintained access to the
food during the morning compared to 56.6% after sunset.
This suggests that P. harpax might be more successful during the night because they increase their activity at a higher
rate than other ant species. As a result, we observed an
increase in the number of foragers at the food bait over time
after sunset, but not during daytime. This increase is most
likely due to ants being recruited via tandem runs (personal
observation) in combination with a higher rate of independent discoveries at night.
Conclusions
It is often assumed that recruitment communication in social
insects is beneficial for foraging success (but see DechaumeMoncharmont et al. 2005, I’Anson Price et al. 2019). One
key benefit could be that recruitment allows colonies to
monopolize food sources in a competitive environment by
building up a critical mass of nestmates to defend a large
resource. However, evidence for this has been scarce. In
our study, we show that Pachycondyla harpax is likely to
improve their foraging success thanks to tandem recruitment. The results also indicate that foragers have better
access to food sources at night, most likely aided by recruiting nestmates. This highlights the potential influence of
communication on foraging success and efficiency in ants,
including those species with small colony sizes and slow,
direct recruitment communication.
Supplementary Information The online version contains supplementary material available at https://doi.org/10.1007/s00040-021-00810-y.
Acknowledgements We thank the Department of Behavioural Ecology and Social Evolution, Johannes Gutenberg-University Mainz for
feedback and advice.
Author contributions SMG and CG designed the experiments; RMF
identified ant species; SMG, AK, NG, and CG performed experiments. SMG analyzed the data and wrote the primarily manuscript.
All authors contributed critically to the drafts and gave final approval
for publication.
Funding Open Access funding enabled and organized by Projekt
DEAL. C.G. and S.G. were funded by the German Research Foundation (DFG: GR 4986/1-1). N.G. was partly funded by the FeldbauschStiftung. R.M.F. was supported by the Conselho Nacional de Desenvolvimento Científico (Grant 302462/2016-3). F.S.N. was funded by a
Tandem communication improves ant foraging success in a highly competitive tropical habitat
Fapesp grant (2019/01148-8). Collection permits were obtained prior
to field collection (Sisbio-ICMBio 26649).
Data availability statement Data deposited in the supplement.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval All applicable institutional and/or national guidelines
for the care and use of animals were followed.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
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