Intraspecific Thievery in the Ant Ectatomma ruidum is Mediated by Food Availability

Abstract

Animals modify their foraging strategies in response to environmental changes that affect foraging performance. In some species, cleptobiosis represents an alternative strategy for resource access. The environmental factors that favor the incidence or prevalence of cleptobiosis, however, are poorly described. The cleptobiotic Neotropical ant Ectatomma ruidum is characterized by a high frequency of thievery behavior, a specific type of intraspecific cleptobiosis, in which specialized thief workers insinuate themselves into nests of neighboring colonies and intercept food items brought into these nests. Here, we evaluate how colonies adjust thievery behavior in response to food availability. We supplemented food availability and measured how the incidence and intensity of thievery responded to resource availability. We found that the incidence and intensity of thievery decline in response to supplemental food, suggesting that thievery behavior is a response to resource limitation at the population scale. This finding indicates that the phenomenon of intraspecific thievery, although a rare strategy in among colonies of social animals, is a viable alternative foraging tactic in the context of competition and food limitation.

Full text

Intraspecific Thievery in the Ant Ectatomma ruidum is Mediated by Food Availability
Benoit Gu!
enard
1,2,4
,and Terrence P. McGlynn
3
1
Okinawa Institute of Science and Technology, Okinawa, Japan
2
Department of Biology and the Keck Center for Behavioral Biology, North Carolina State University, 127 David Clark Labs, Raleigh, NC,
27695, U.S.A.
3
Department of Biology, California State University, Dominguez Hills, 1000 E. Victoria Street Carson, CA, 90747, U.S.A.
ABSTRACT
Animals modify their foraging strategies in response to environmental changes that affect foraging performance. In some species,
cleptobiosis represents an alternative strategy for resource access. The environmental factors that favor the incidence or prevalence
of cleptobiosis, however, are poorly described. The cleptobiotic Neotropical ant Ectatomma ruidum is characterized by a high frequency
of thievery behavior, a specific type of intraspecific cleptobiosis, in which specialized thief workers insinuate themselves into nests of
neighboring colonies and intercept food items brought into these nests. Here, we evaluate how colonies adjust thievery behavior in
response to food availability. We supplemented food availability and measured how the incidence and intensity of thievery responded to
resource availability. We found that the incidence and intensity of thievery decline in response to supplemental food, suggesting that
thievery behavior is a response to resource limitation at the population scale. This finding indicates that the phenomenon of intraspecific
thievery, although a rare strategy in among colonies of social animals, is a viable alternative foraging tactic in the context of competition
and food limitation.
Abstract in Spanish is available in the online version of this article.
Key words: cleptobiosis; Ectatomma ruidum; food supplementation; foraging behavior; Formicidae; thievery.
FOOD RESOURCE AVAILABILITY CAN BE UNPREDICTABLE IN SPACE AND
TIME,WHETHER FOR HUNTER-GATHERER HUMANS, dung beetles, or
ants. This unpredictability has led to the evolution of strategies to
maximize the benefit of foraging and to minimize the cost associ-
ated with foraging. Costs include time and energy spent during
foraging (Fewell 1988, McGlynn et al. 2003), risk of predation
(Nonacs 1990), exposure to environmental hazards (Cerd!aet al.
1998), and interference competition (Traniello 1989). Because of
these costs, natural selection acts heavily on strategies to maxi-
mize food discovery and retrieval, and in some cases, the evolu-
tion of alternative foraging tactics involving less foraging effort
and risk may be favored (e.g., Mathot & Giraldeau 2008).
In social insects, foragers collect food items within a home
range and bring them to the nest. This leads to ‘central-place for-
aging’, where the ‘central place’is the nest where successful for-
agers converge with food resources. While central place foraging
may ameliorate the unpredictability of food resources (McGlynn
et al. 2003), it also may incur costs. Specifically, sedentary nests
are potentially susceptible to parasitic species that, rather than
forage for food, exploit the aggregation of resources within nest
sites (Buschinger 1986). Cleptobiosis is a particular form of social
parasitism, in which thieves intercept the food collected by
workers at areas around the nest or on trails used by foragers
(H€olldobler 1986, Richard et al. 2004, LaPierre et al. 2007, Breed
et al. 2012) and, in doing so, reduce their own foraging costs
(Curio 1976, Passera & Aron 2005). In ants, this behavior has
been described several times at an inter-specific level (H€olldobler
1986, Perfecto & Vandermeer 1993, Espadaler et al. 1995, Gras-
so et al. 2004, Richard et al. 2004). In at least two cases, however,
intraspecific cleptobiosis has been observed, in Messor aciculatus
(Fr. Smith) in Japan (Yamaguchi 1995) and in the Neotropical
Ectatomma ruidum (Roger) (Breed et al. 1990, 1992, 1999). A key
difference between cleptobiosis between species and that within
species, is that intraspecific cleptobiosis can be symmetrical,
which is to say that any given colony can be the villain and the
victim.
Ectatomma ruidum (Formicidae, Ectatomminae) is widespread
throughout the Neotropics, from Mexico to Brazil (Fern!andez &
Sendoya 2004). Colonies of this species are monodomous (single-
nested) and monogynous, containing 50–300 workers (Lachaud
et al. 1984, Breed et al. 1990, 1992, 1999, Schatz & Lachaud
2008, Lenoir et al. 2011). Nests have a single entrance, about
3–4 mm wide dug in the ground (Lachaud et al. 1984, Breed
et al. 1990). This species exhibits a unique form of intraspecific
cleptobiosis, which has been called thievery behavior, in which a
worker of one nest will enter a neighboring nest of the same spe-
cies, wait within the foreign nest, intercept food brought by a for-
ager, and then leave the foreign nest with the food and bring it
to its own nest (Breed et al. 1990, 1992, 1999). While resident
E. ruidum workers tend to repel foreign workers outside of their
nests and territories without injuries (Breed et al. 1990, 1992),
thieves are able to infiltrate colonies through chemical camouflage
and no specific aggressiveness is directed toward them (Breed
Received 22 August 2012; revision accepted 18 November 2012.
4
Corresponding author; e-mail: zeroben@gmail.com
ª2013 The Author(s) 497
Journal compilation ª2013 by The Association for Tropical Biology and Conservation
BIOTROPICA 45(4): 497–502 2013 10.1111/btp.12031

et al. 1992, Jeral et al. 1997). Thievery behavior is common within
populations of E. ruidum and has been noted at several locations
within the species’range (De Carli et al. 1998, Breed et al. 1999).
To date, studies of thievery have focused on a precise
description of the behavior (Breed et al. 1990, 1992, 1999, Jeral
et al. 1997) and the ecological consequences on foraging and nest
distribution for the different protagonists (Yamaguchi 1995). Lit-
tle is known about the factors that influence the frequency or
even simply occurrence of intraspecific cleptobiosis in ants. In
1990, Breed and collaborators hypothesized that thievery within
populations of E. ruidum might be a facultative response to high
colony densities or to food competition. Later on, it was shown
that the rate of thievery was independent of nest density (Breed
et al. 1999), but the possibility that thievery rates are related to
food supplies remains untested. Here, we hypothesize that food
supplementation will modify the intensity of thievery observed in
a population of E. ruidum. In this study, we modified food avail-
ability with daily additions of food and measured the foraging
responses of E. ruidum. We expect that, as a result of this manip-
ulation, colonies receiving supplemental food will experience a
reduction in the rate of thievery, as well as lower rates of thievery
relative to surrounding nests that do not receive supplemental
food.
METHODS
SITE LOCATION AND DESIGN.—Work was conducted in the arbore-
tum of La Selva Biological Station, Heredia Province, Costa
Rica in June 2008. Six sites were selected. Each site had an area
of 452 m
2
, comprised of a circle with a 12 m radius. Each plot
was separated from one another by at least 50 m, from edge to
edge, far greater than the maximal foraging distance of any E.
ruidum worker. For each site, a focal nest of E. ruidum was
located at the center of a 5 m radius circle in the middle of
the site and corresponded to the treated area receiving food
supplementation. Each inner circle was delimited with flagging
and each plot was exhaustively searched (for a minimum of
twenty person-hours) until all colonies of E. ruidum were found,
following a protocol involving direct searching for nests, feeding
foragers, and baiting, as conducted in previous work (McGlynn
et al. 2010). Nests outside the inner circle, when discovered,
were also marked (up to 12 m from the center) (Fig. 1). During
the food supplementation, any additional nests that were
detected were marked.
PRE-TREATMENT ASSAY.—Forty-eight hours after we completed the
establishment of sites with marked nests, six to seven study nests
per site were randomly selected to measure the rate of thievery.
Three to four nests were located within the inner circle areas,
and two to three were located outside the inner circle. In total,
twenty nests within treatment areas were measured for thievery
(including the focal nests), and nineteen were measured outside
treatment areas.
For each nest, ten food items (4-mm long cylinders of con-
densed white bread) were presented at the nest entrance. Over a
10-min duration, the number of items collected outside of the
focal nest was recorded. Three different events were observed
and recorded: (1) Collecting event—the food item was collected
by a resident worker and brought within the focal nest; (2) Col-
lecting and thievery events—the food item was collected and
brought by a resident worker within the focal nest, but then inter-
cepted within the focal nest by a thief which left the focal nest
and transport the food item into a different nest; and (3) Exploit-
ing event—the food item was collected by a worker from a for-
eign nest (later qualified as ‘exploiters’) which transport it to its
nest. The number of thieves departing the nest with the supple-
mental food was recorded and followed (by a second observer)
to the destination nest. For each thievery event, distances
between origin nests and destination nests were measured. For
each study nest, we calculated the proportion of food collected
(number of food items collected/number of food items offered)
and the proportion of thievery observed (number of food items
stolen within the nest by a thief/number of food items collected).
FOOD SUPPLEMENTATION PROCEDURE.—Over seven consecutive
days, about 3 mg of food was deposited daily adjacent to the
entrance of each nest present within the treated area (within the
5 m radius circle). The supplemental food was alternated, either a
mix of tuna and honey, or peanut butter, both of which are
known to be rich in proteins, lipids, and carbohydrates. Further-
more, to adjust for the possibility that we might have not
detected some nests within our treatment area, we added extra
food that could be exploited by all the nests present in the area.
Within the treated area, we added nine stations where food was
deposited daily. The stations were separated by 1.5 m from each
other within a square grid configuration (see Fig. 1). After a week
of food provisioning, 24 hr elapsed without any food provision-
ing before the commencement of the post-treatment assay.
POST-TREATMENT ASSAY.—Using the same methods as in the pre-
treatment assay, we measured thievery rate for areas inside and
outside our treatment area on the same study nests. Four study
FIGURE 1. Design of the treated area for one selected site.
498 Gu!
enard and McGlynn

nests (three inside and one outside the supplementation area) that
were used for pre-treatment measurements were not active or
had relocated to new positions, so these nests were excluded; to
accommodate this reduction in sample size, eight arbitrarily
selected nests that had not been measured during the pretreat-
ment assay were incorporated in the post-treatment measurement
(three inside and five outside).
THIEVERY OCCURRENCE.—Thievery was considered to occur if at
least one event of thievery was observed for the observed nest
during the 10 min period of our observation. We used a
chi-square test to compare the occurrence of thievery inside and
outside of the treated areas before and after the application of
treatments.
FOOD ITEMS COLLECTED BY FOREIGN WORKERS (EXPLOITERS).—We
monitored the number of food items that were collected by
exploiters while the food was standing outside of the focal nest
entrance. Exploiters are individuals foraging on the territory of
others, in this case at the vicinity of other nest entrances.
STATISTICAL ANALYSIS.—We evaluated the effect of food addition
on the different foraging behaviors observed in E. ruidum. All
our analyses used non-parametric Wilcoxon tests to compare the
effects of the treatments. Non-parametric tests were used on
account of ordinal and non-normally distributed data. We com-
pared the proportion of food collected before and after the food
addition for the areas located inside and outside the treated areas.
We then compared the rate of thievery observed before the treat-
ment between the treated areas and the non-treated areas. Simi-
larly, we compared the effect of food addition on thievery rate
after the food addition. Then we compared the rate of thievery
observed before and after the food addition within the two dif-
ferent treatments with matched-pairs Wilcoxon signed-rank tests.
Similar analyses were conducted on the proportion of total food
and the proportion of food collected by exploiters. For these
analyses, we used a subset of seventeen nests within the treated
areas and of 18 nests within the non-treated areas for which we
had data prior and after food supplementation. The larger dataset
(20 nests inside the treated areas and 23 nests within the non-
treated areas) included supplemental nests that did not have data
for both periods.
RESULTS
NEST DENSITIES.—Within our six treatment areas, the mean nest
density was 0.22 nest/m
2
(range: 0.10–0.37 nest/m
2
), which cor-
responds to a mean 17.3 nests per treated area (range: 8–29 nests
per 5 m radius area).
MEAN DISTANCE TRAVELED BY THIEF ANTS.—Forty-three thievery
events were observed in their entirety, to measure the distance
traveled by thieves. The distance traveled by thieves between the
origin and destination nests ranged from 40 to 480 cm
(mean !SD =148 !111 cm).
PERCENTAGE OF FOOD ITEMS COLLECTED.—Food supplementation
did not modify the proportion of food items collected before
and after within (mean !sd: Interior zone: X
before
=82.9 !
2.6; X
after
=71.3 !5.4; N=17; Z ="18.5; P=0.40, Wilco-
xon matched-pairs signed-ranks test) or outside (mean !SD:
Exterior zone: X
before
=89.2 !4.2; X
after
=82.3 !4.8; N=
18; Z ="9.5; P=0.54, Wilcoxon matched-pairs signed-ranks
test) the treated areas.
OCCURRENCE OF THIEVERY.—Thievery was observed from 67 per-
cent of the 39 nests surveyed prior to the application of food
supplementation. No difference between the nests inside and out-
side the treated areas was observed (N=39, v
2
=0.22,
P=0.63). After food supplementation, the overall occurrence of
thievery observed was lower, with only 42 percent of occurrence
observed. The twenty nests within the treated areas had a lower
thievery frequency (25%) than the 23 nests outside the treated
areas (57%) (N=43, v
2
=4.37, P=0.037).
INTENSITY OF THIEVERY.—Prior to food supplementation, no differ-
ence in the percentage of food robbed was observed (N=39;
Z="0.07; P=0.94) between the nests located inside or outside
the treated areas (mean !SD inside =19.4 !4.5;
outside =15.3 !4.9). After food supplementation, the percent-
age of food robbed was significantly lower (N=43; Z ="1.95;
P=0.05) for the nests located inside than outside the treated areas
(mean !SD inside =7.2 !4.1; outside =17.8 !5.2) (Fig. 2).
When comparing the proportion of food robbed before and after
food supplementation, we observed a significant decrease for the
nests located within the treated areas (N=17; Z ="27;
P=0.01, Wilcoxon matched-pairs signed-ranks test), but no
change in the nests located outside of the treated areas (N=18;
Z="4.5; P=0.36, Wilcoxon matched-pairs signed-ranks test).
FIGURE 2. Percentage of food items stolen per nest before and after the
treatment. In black are presented the nests located within the food-supple-
mented area and in light gray, the nests located outside the treated area. Sig-
nificant differences between pairs are represented by a star.
Food Limitation Enhances Thievery in Ants 499

FOOD ITEMS COLLECTED BY FOREIGN WORKERS (EXPLOITERS).—Prior
to food supplementation, the fraction of food items collected by
exploiters was greater inside the treated areas (N=39, Z =2.10,
P=0.04); as these areas were assigned independent of treatment,
this P-value below alpha presumably is an instance of Type I
error. After food supplementation, this difference was not
observed, with a similar effect size, and the fraction of stolen
items was not significantly different (N=43, Z =1.65;
P=0.10; Fig. 3). When comparing the percentage of exploiters
for a similar area before and after food supplementation, we
observed no difference between inside (N=17, Z =18.5;
P=0.40, Wilcoxon matched-pairs signed-ranks test) and outside
the treated areas (N=18, Z =9.5; P=0.54, Wilcoxon matched-
pairs signed-ranks test).
DISCUSSION
MANY ANT SPECIES HAVE THE CAPACITY TO EXPRESS FLEXIBILITY IN
THEIR FORAGING STRATEGIES,ACROSS SPACE AND TIME, as a function
of local conditions. Foraging decisions are context-dependent in
relation to the properties of food and environmental conditions
outside of the nest (Carroll & Janzen 1973, Traniello 1989). For
instance, ant colonies can adjust their foraging strategies to
optimize food intake on the basis of food quality or quantity
(Bernstein 1975, Breed et al. 1987), competition (Vepsäläinen &
Savolainen 1990, Andersen & Patel 1994, Cerd!aet al. 1998) or
predation pressure (Feener 1988, LeBrun 2005). The importance
of those factors has been highlighted over the past decades, but
their importance on the expression of social parasitism–such as
cleptobiosis–is still uncertain. In this study, we experimentally
demonstrated that the rate of cleptobiosis observed in popula-
tions of E. ruidum is directly related to food limitation.
Thievery was frequent among the nests of E. ruidum that we
surveyed. Prior to our treatment, under natural conditions, at least
two-thirds of the nests were experiencing some impact of thievery
from workers of surrounding nests. These results are similar to
those of Breed and collaborators who found that 7 of 10 nests
suffered from thievery (1990). After only a week of food addition,
and while no difference in foraging activity (number of food items
collected per nest) was observed, the frequency of thievery
decreased to be observed in only a quarter of the nests surveyed.
Non food-supplemented nests maintained a similar rate of thiev-
ery to that observed prior to the experiment. Similar to frequency,
thievery intensity responded negatively to food addition (Fig. 2).
Fifteen to twenty percent of the food items collected by foragers
were stolen in areas without food supplementation, but thievery
rate was reduced by half in areas with food supplementation.
The nest density of E. ruidum found in our study of 0.22
nest/m
2
is similar, although in the lower tail of other studies
reporting nest density for E. ruidum (Table 1). Despite this rela-
tively low density of nests, thievery behavior was common in the
population surveyed, further indicating that, as suggested by
Breed et al. (1999), thievery is not limited to populations with
high nest density.
In Mexico, E. ruidum had a strong predatory effect on the
insect community in a coffee plantation, with a daily estimate per
hectare of 150,000 insects collected (Lachaud et al. 1990). If rate
of thievery is constant and estimated to be 15 to 20 percent of
the prey brought to the nest as our results indicate, this could rep-
resent 22,000 to 30,000 prey items that could be stolen each day
in similar conditions. As indicated by previous studies and our
results, however, thievery rate is not uniform among colonies of
E. ruidum (Breed et al. 1990) or as observed for the other known
intraspecific cleptobiotic species M. aciculatus (Yamaguchi 1995),
and this asymmetry could lead to strong difference in colony
growth performance between colonies within a population. Two
different evolutionary strategies could emerge within the popula-
tion. First, colonies may invest in foraging and defensive strategies
to protect the food collected from thieves; and second, colonies
may invest more in thievery and less in foraging. In this context,
thievery and foraging behaviors in E. ruidum relate to the pro-
ducer-scrounger game developed for other organisms such as
birds. In bird population, some individuals find food resources
(producer tactic), while other individuals exploit their discoveries
(scrounger tactic) (Barnard & Sibly 1981, Giraldeau & Beauchamp
1999). The expression of one of these strategies can be individ-
ual-dependent (Morand-Ferron et al. 2011, David & Giraldeau
2012) or context-dependant (Coolen 2002, Barta et al. 2004). As a
counterpoint to work on birds, thievery in E. ruidum represents a
great social insect model to study evolutionary aspects of foraging
and of alternative strategies, and the factors that determine the
use of thievery by specific colonies. In this regard, our results
tend to show that the use of thievery as an alternative strategy is
reduced by an increase of food within the population.
The mean distance covered by a thief to its destination nest
was about 1.5 m with a maximum distance observed of 4.8 m.
This corresponds to the foraging distance observed in other
FIGURE 3. Mean number per nest of items stolen by exploiters outside the
nest entrance before and after the treatment. In black are presented the nests
located within the food-supplemented area and in light gray, the nests located
outside the treated area. Significant differences between pairs are represented
by a star.
500 Gu!
enard and McGlynn

study of about 3 m although occasional distance up to 30 m has
been noted (Lachaud et al. 1984). Several authors have noticed
that the high nests density should favor the overlapping of
foraging territory (Lachaud et al. 1984, Breed et al. 1999, Schatz
& Lachaud 2008), with the exception of the results of Breed and
collaborators (1990) who found that only few workers foraged
outside of their territories. Here, we confirm those observations
with the demonstration of a consequent percentage of food items
(10–30%) collected by exploiters directly at the vicinity of other
nest entrances. Our results indicate that the addition of food did
not modify the intensity of exploiters and so we did not see a
switch from thievery (collection of food inside the nest) to
exploiting (collection at the vicinity of other nest entrance).
Future studies focusing on worker polyethism, perhaps through
the use of marking techniques and in laboratory colonies, should
emphasize the flexibility of workers to exploit food within their
environment either as thieves or exploiters.
In conclusion, colonies of E. ruidum use a complex foraging
strategy mixing social parasitism and exploitative competition,
which is responsive to the availability of food in the environment.
The rarity of intraspecific thievery, compared with heterospecific
food robbing, remains a conundrum. We propose that the evolu-
tion of intraspecific thievery may not be favored when encounters
between thief and victim result in injury or death. In most social
insects, interactions between workers from separate colonies at
the nest site typically result in major aggression, although this is
not the case in most Ectatomma species (Breed et al. 1990, 1992,
Zinck et al. 2008), nor in M. aciculatus where intraspecific cleptobi-
osis is common (Yamaguchi 1995). The new question posed by
our findings is to understand how thievery represents an evolu-
tionarily stable strategy, and whether this phenomenon functions
as a form of parasitism or a form of mutualism.
ACKNOWLEDGMENTS
We thank Stephanie Mattingly, Lauren Valbracht and Gilbert Lam
for assistance in fieldwork. We also thank Rob Dunn for useful
comments on the manuscript, and Melody Castellon and Roder-
ick Castro for their assistance in translating the abstract. Finally,
we thank three anonymous reviewers for their insightful com-
ments on previous version of the manuscript. Work was con-
ducted under support of the National Science Foundation
(OISE-0854259 and OISE-1130156), a CSUDH Sally Casanova
Memorial RSCAAP Fellowship to TPM, and a Harkema Award
offered through the NCSU Department of Biology to BG.
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