Distinct types of foragers in the ant Ectatomma ruidum: Typical foragers and furtive thieves

Abstract

A principal benefit of social living is the communal defence of resources. However, in the ant Ectatomma ruidum, specialized thieves often circumvent detection by conspecific non-nestmates, and those detected are peacefully expelled. Colonies can gather food through typical foraging (opportunistically tracking prey or nutrients in the home range) or by robbing (entering a conspecific nest, waiting for, and then removing a newly arrived food item carried in by a forager). Here, we conducted behavioural assays to determine whether robbers (or 'thieves'), carrying purloined food, manifest behaviours that minimize the probability of detection relative to nonthieving individuals. We found several lines of evidence that individuals carrying stolen food behave distinctly from normal nonthieving foragers. When returning to their home nest with a stolen food item, thieves had fewer encounters with conspecifics, were more likely to pause during movement, and were more likely to release food when grasped. Thieves walked faster while travelling in the victim's home range, compared to their own home range. When experimentally perturbed, thieves were more likely to reverse their direction of movement, while normal foragers continued moving in the same direction. Because the carbon and nitrogen stable isotope composition, as well as the C:N ratio, was the same for both thieves and nonthieves, we conclude that both groups were accessing the same food sources, using different behaviours to repartition a common resource. We conclude that, although thieves are morphologically indistinguishable from nonthieving foragers, their food retrieval behaviours are distinct in a manner that reduces the probability of detection and aggressive interactions with other conspecifics. We propose that thieves are a distinct caste of forager in E. ruidum.

Full text

Distinct types of foragers in the ant Ectatomma ruidum: typical
foragers and furtive thieves
Terrence P. McGlynn
a
,
*
, Russell Graham
a
, Jane Wilson
b
, Jeremy Emerson
a
,
Jennifer M. Jandt
c
, A. Hope Jahren
d
a
Department of Biology, California State University Dominguez Hills, Carson, CA, U.S.A.
b
Columbine Middle School, Montrose, CO, U.S.A.
c
Department of Zoology, University of Otago, Dunedin, New Zealand
d
Department of Geology and Geophysics, University of Hawaii at Manoa, Honolulu, HI, U.S.A.
article info
Article history:
Received 10 April 2015
Initial acceptance 18 May 2015
Final acceptance 6 August 2015
Available online
MS. number: A15-00300R
Keywords:
ant
colony defence
conspecific thievery
Ectatomma ruidum
food pilferage
foraging
kleptoparasitism
nestmate recognition
social living
A principal benefit of social living is the communal defence of resources. However, in the ant Ectatomma
ruidum, specialized thieves often circumvent detection by conspecific non-nestmates, and those detected
are peacefully expelled. Colonies can gather food through typical foraging (opportunistically tracking
prey or nutrients in the home range) or by robbing (entering a conspecific nest, waiting for, and then
removing a newly arrived food item carried in by a forager). Here, we conducted behavioural assays to
determine whether robbers (or ‘thieves’), carrying purloined food, manifest behaviours that minimize
the probability of detection relative to nonthieving individuals. We found several lines of evidence that
individuals carrying stolen food behave distinctly from normal nonthieving foragers. When returning to
their home nest with a stolen food item, thieves had fewer encounters with conspecifics, were more
likely to pause during movement, and were more likely to release food when grasped. Thieves walked
faster while travelling in the victim's home range, compared to their own home range. When
experimentally perturbed, thieves were more likely to reverse their direction of movement, while
normal foragers continued moving in the same direction. Because the carbon and nitrogen stable isotope
composition, as well as the C:N ratio, was the same for both thieves and nonthieves, we conclude that
both groups were accessing the same food sources, using different behaviours to repartition a common
resource. We conclude that, although thieves are morphologically indistinguishable from nonthieving
foragers, their food retrieval behaviours are distinct in a manner that reduces the probability of detection
and aggressive interactions with other conspecifics. We propose that thieves are a distinct caste of
forager in E. ruidum.
©2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Food often limits fitness, and animals in want of food may rob it
from other individuals (Breed, Cook, &Krasnec, 2012; Brockmann &
Barnard, 1979). A critical function of social groups is the collective
defence of shared food resources. Food robbing is commonly
known to occur when an individual of one species robs from
another species, but intraspecific food robbing is observed in a
variety of lineages as well (Steele &Hockey, 1995).
The selective pressure for food robbing is typically matched
with the evolution of strategies to detect, deter and punish in-
dividuals that attempt to rob food (Breed et al., 2012). For example,
in the honeybee Apis mellifera, behaviourally specialized guard
workers monitor the nest entrance to screen individuals entering
the colony and will engage in potentially mortal combat if in-
dividuals from other colonies are detected at the nest entrance
(Mann &Breed, 1997; Moore, Breed, &Moor, 1987). Conspecific
food-robbing events occurs between honeybee colonies, but as
food scarcity and thieving attempts increase, successful rejections
of non-nestmates also increase (Couvillon et al., 2008; Downs &
Ratnieks, 2000).
In ants, mechanisms that prevent food robbing are so effective
that intraspecific thievery has only been documented in two spe-
cies: Messor aciculatus (Yamaguchi, 1995) and Ectatomma ruidum
(Breed, Snyder, Lynn, &Morhart, 1992; Perfecto &Vandermeer,
1993). Intraspecific food robbing remains undetected in other ant
species, despite extensive observation of many other species.
Nevertheless, in E. ruidum, intraspecific thievery among adjacent
*Correspondence: T. P. McGlynn, Department of Biology, California State
University Dominguez Hills, Carson, CA 90747, U.S.A.
E-mail address: terry.mcglynn@gmail.com (T. P. McGlynn).
Contents lists available at ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
http://dx.doi.org/10.1016/j.anbehav.2015.08.024
0003-3472/©2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Animal Behaviour 109 (2015) 243e247

colonies is readily observed (Gu!
enard &McGlynn, 2013). Ectatomma
ruidum thieves specialize in stealing food from another colony (i.e.
the ‘victim nest’); the cuticular hydrocarbon profile of thieves is
intermediate between the colony to which they are bringing food
and the colony from which they are removing food, presumably
obfuscating nestmate recognition cues, and thieves are not known
to switch to a nonthieving foraging habit (Breed et al., 1992; Jeral,
Breed, &Hibbard, 1997). Thievery is thought to be evolutionarily
stable only at low frequencies (Brockmann &Barnard, 1979; Ruxton
&Broom, 1999), but thieving is a common activity in E. ruidum
colonies, at least in Costa Rica and Panama (Breed, McGlynn, Stocker,
&Klein, 1999). Like other social insects, colonies of E. ruidum are less
vigilant against interlopers when food is relatively abundant in the
environment (Gu!
enard &McGlynn, 2013).
Thievery in E. ruidum is uniquely overt and widespread, and is
undetected in other ant species. Intraspecific kleptoparasitic
behaviour in E. ruidum persists despite the fact that colonies are
more vigilant against thieves when more thieving occurs (Jandt,
Hunt, &McGlynn, 2015). It is broadly accepted that the ecological
success of social insect colonies emerges from the collective ability
to acquire resources and defend them from competitors. Thievery
within E. ruidum suggests very poor abilities in protecting resources,
but this species is nevertheless among the most widespread and
locally abundant ants in the Neotropics (Schatz &Lachaud, 2008). To
address this apparent contradiction, we wish to understand how
foragers that act as thieves and collect resources from the insides of
neighbouring nests are distinct from ‘normal’(nonthief) foragers
that collect resources from the surrounding leaf litter.
Here we tested whether intraspecific thieves are behaviourally
and physiologically distinct from nonthieves, in addition to their
obvious specialization in acquiring purloined food items. Anecdotal
evidence from prior investigations suggested that thieves are
sneaky: they are fast, they hide, and they drop food and switch
course, making them more difficult to follow (Jandt et al., 2015). If
thieves that remove food from other colonies function as a distinct
type of forager, then thieves should engage in a particular set of
behaviours after retrieving stolen materials to avoid being ‘caught
in the act’of thieving. Alternatively, if thieves are not behaviourally
distinct from other foragers (i.e. they are only different from non-
thieves with respect to the location of food collection), then in-
dividuals that retrieve food from a victim nest should show the
same behaviours as other foragers. We also investigated whether
thieves and nonthieves are compositionally different from one
another, using stable isotope composition to evaluate differences in
the food source of tissue. All together, we explored whether or not
thieves can be considered a separate group, or caste, from normal
foragers.
METHODS
We studied E. ruidum, an omnivorous ground-nesting ant spe-
cies, with workers measuring about 7 mm in length. Colonies
contain up to a few hundred workers, and the diets of colonies
typically consist of arthropods and nectar. The pattern of thievery in
this species was described by Breed et al. (1992), Jeral et al. (1997)
and Perfecto and Vandermeer (1993). Each colony receives food
from a relatively small number of thieves (less than 10 individuals),
each of which specializes on removing food items from a particular
colony nesting in the vicinity of their home colony. The relative
concentrations of hydrocarbon compounds on the exoskeletons of
E. ruidum serve as nestmate recognition pheromones, and the hy-
drocarbons found on the thieves are intermediate between the
colonies from which they are delivering food and those from which
they are removing food (Jeral et al., 1997). Thieves may be distin-
guished from nonthieves by being observed in the act of removing
food from the nest of one colony and carrying it towards the nest of
a different colony. As E. ruidum is a monodomous species, the field
identification of thieves from their behaviour is straightforward.
Fieldwork was conducted during JuneeAugust 2014 at La Selva
Biological Station, located in a lowland tropical wet forest in the
Caribbean slope of Costa Rica. La Selva receives a mean annual
rainfall of about 4 m, with the majority occurring during
MayeDecember. Work was conducted on colonies nesting within
the arboretum of the research station. This area has an open un-
derstory and a shallow leaf litter layer that has also facilitated
previous experiments on E. ruidum (Gu!
enard &McGlynn, 2013;
Jandt et al., 2015; McGlynn, Dunn, Wayman, &Romero, 2010).
We established four sites, in which all colonies of E. ruidum were
detected through exhaustive searching and baiting (N¼58 col-
onies). We arbitrarily selected 24 colonies and delineated home
ranges by following the movements of foragers, after the meth-
odology of Breed et al. (1999) and McGlynn, Shotell, and Kelly
(2003). We conducted field assays to quantify the behaviour of
individuals while carrying a food item (8 mm
3
piece of ham). Each
food item was readily handled by foragers in a way that did not
disrupt movement and was equivalent to a high-quality, although
modestly sized, item of prey that might be collected by foragers. To
establish home ranges, we provided food items to ants using for-
ceps, which immediately elicited food-carrying behaviour back to
the home nest.
Rates of Travel and Encounters with Conspecifics
We determined the rate of travel by measuring the time and
distance for an individual to carry a food item from the site of
presentation to the entrance of a nest. For nonthieves, food was
presented about 50 cm from the nest entrance. For trials involving
thieves, individuals were observed as food was carried out from the
victim nest for a distance of 50 cm towards their home nest. All
replicates of 47 thieves and 84 nonthieves were standardized to the
rate of cm/s; in three observations, the distance was less than 50 cm
before the thief reached its home nest. In the 13 colonies with
mapped home ranges, we divided the data into rates of travel
outside and inside the home range. In these colonies, workers were
followed the entire route to their home nest.
We recorded the number of encounters with conspecifics, the
number of pauses and the duration of pauses that ensued post-
encounter while the focal individual (thief or nonthief) travelled
back to its home nest. An encounter was recorded if an antenna of
the focal individual touched another conspecific ant, or if an antenna
of the conspecific ant touched the focal individual. A pause was
recorded if the ant stopped forward movement for more than 2 s.
Response to Perturbation
We conducted a bioassay to compare the response of thieves
and nonthieves to external perturbation. The tool we used for
perturbation was a freeze-killed E. ruidum worker mounted on the
tip of a 25 cm piece of wire (i.e. ‘conspecific target’). The individual
used for this target was collected hundreds of metres from any of
our sites (and therefore, unlikely to have been a member of the
home or the victim colony used in the assay). As in the assays for
rate of travel, for nonthieves, we presented food to arbitrarily
selected wandering individuals in the leaf litter within the home
range, and for thieves, we observed individuals as food was carried
out from the victim nest. We identified an active focal individual
(thief or nonthief) and followed her for at least 20 cm. We waved
the conspecific target in front of the focal ant four times for 1 s, at a
distance of about 3 mm from her antennae. We observed the
behaviour of the focal ant and scored two nonexclusive responses:
T. P. McGlynn et al. / Animal Behaviour 109 (2015) 243e247244

pause (lack of forward movement for a minimum of 2 s), and
change in direction (change in direction of movement >90
"
). After
the focal individual recommenced carrying the food item back to
the nest for a minimum of 15 cm, we picked the ant up by its legs
with forceps and recorded whether the ant dropped the food item
as a result. This protocol was immediately repeated for a pairwise
comparison, with thieves and nonthieves from the same colony.
Isotope Analysis
Individuals from the external perturbation bioassay were
collected for stable isotope analysis to infer differences in diet, by
using the relative proportion of
13
C and
15
N comprising the tissue of
thieves and nonthieves. Individuals were oven-dried for 24 h at
50
"
C, legs were removed, and about 1 mg of leg material was
weighed on an analytical balance and enclosed in a tin capsule
(Costech Analytical Technologies, Valencia, CA, U.S.A.). Samples
were analysed for carbon and nitrogen stable isotope and total
mass composition using a Eurovector Elemental Analyzer config-
ured with a Delta V Stable Isotope Ratio Mass Spectrometer; carbon
and nitrogen stable isotope values are reported in standard delta-
notation relative to the standards Vienna Pee Dee Belemnite
(VPDB) and air, respectively (Post et al., 2007). When we compared
the carbon and nitrogen isotopic composition, as well as the C:N
mass ratio, of 50 individuals sampled within our study.
Assessment of carbon and nitrogen stable isotope composition
of arthropod tissues is an established method used to perform diet
analysis, to reconstruct food webs and to examine feeding behav-
iour (Hood-Nowotny &Knols, 2007) that has a long and useful
history of application within ant ecology (e.g. Blüthgen, Gebauer, &
Fiedler, 2003; Fisher, Sternberg, &Price, 1990; Tillberg, 2004).
There are developmental distinctions in isotopic composition of
ants that have not yet been accounted for by differences in diet, as
adult worker ants show higher
d
13
C and
d
15
N values than brood
(Tillberg, McCarthy, Dolezal, &Suarez, 2006). Ottonetti, Tucci,
Chelazzi, and Santini (2008) found that
d
15
N value was signifi-
cantly correlated with multiple indices of ecological performance.
Statistical Analyses
We compared the frequency of pauses and encounters using
ordinal logistic regression, and we evaluated movement rates of
thieves inside and outside the home ranges using matched-pairs
tests. All other analyses were conducted using a generalized
linear model, using a binomial response for response variables with
two categories. Rates of travel were log transformed prior to
analysis to normalize distributions. Statistical analyses were con-
ducted using JMP 11.0 (SAS Institute, Cary, NC, U.S.A.).
RESULTS
Rates of Travel and Encounters with Conspecifics
As thieves were removing experimentally introduced food from
a colony, their movements differed from those of nonthieves that
were traversing the same distance and carrying an equivalent
experimental food item (Fig. 1). Over a distance of 50 cm, thieves
paused more frequently (GLM: c
2
1
¼24.2, N¼124, P<0.0001;
Fig. 1) and encountered fewer individuals (c
2
1
¼12.5, P¼0.0004)
than nonthieves. Even though thieves paused more frequently,
their mean ±SE rate of movement in the home range of the nest
from which food was removed was 1.77 ±0.20 cm/s, compared to a
mean rate of 1.36 ±0.17 cm/s after crossing the border into their
own home range (matched-pairs test: t
12
¼2.37, P¼0.035).
Response to Perturbation
Thieves responded differently to the perturbation assay than
nonthieves (Fig. 2). Relative to nonthieves, thieves reversed direc-
tion more frequently (32% versus 77%; GLM: c
2
1
¼14.5, P<0.0001)
and paused more frequently (59% versus 89%; c
2
1
¼8.26, P¼0.004).
Among individuals that paused, the mean ±duration of the pause
was longer in thieves (14.5 ±1.6 s) than in nonthieves (6.25 ±1.3 s)
(c
2
1
¼12.5, P¼0.0004). After individuals were picked up with
forceps at the end of a trial, thieves dropped their food item 67% of
the time, while nonthieves dropped the food item 36% of the time
(c
2
1
¼5.36, P¼0.021).
Isotope Analysis
We observed no difference in isotopic measures between
thieves (
d
13
C¼#26.6 ±0.6
‰
SD;
d
15
N¼8.1 ±0.6
‰
;
C:N ¼3.65 ±0.06 ; N¼23) and nonthieves (
d
13
C¼#26.5 ±0.5
‰
;
d
15
N¼8.3 ±0.5
‰
; C:N ¼3.60 ±0.03; N¼27). The
d
13
C values that
we observed were similar to those seen in large-scale studies across
arthropod families (e.g. Halaj, Peck, and Niwa (2005) sampled 22
species within 22 arthropod families and found
d
13
C values ranging
from #27
‰
to #21
‰
) and indicative of a reliance upon C3 plant
tissue, across various stages of decomposition (Dawson, Mambelli,
Plamboeck, Templer, &Tu, 2002), after taking into account the
widely accepted values of isotopic enrichment during tissue
100
50
25
Frequency (%)
Frequency (%)
0
100
75
25
0
2
Number of encounters over 50 cm Number of
p
auses over 50 cm
345 1 2 3 4 5
Thieves
Nonthieves
Thieves
Nonthieves
75
1
50
Figure 1. Mean frequency of the number of individuals encountered and the number of pauses made by E. ruidum thieves and nonthieves after experimental provisioning of a food
item and 50 cm of travel (see Results for statistical analyses).
T. P. McGlynn et al. / Animal Behaviour 109 (2015) 243e247 245

synthesis after dietary assimilation (i.e. Feldhaar, Gebauer, &
Blüthgen, 2010; McCutchan, Lewis, Kendall, &McGrath, 2003).
The
d
15
N values that we observed are consistent with other
terrestrial ants foraging for arthropod prey, consistent with soil
organic matter as a food source (Natelhoffer &Fry, 1988). Ponsard
and Arditi (2000) found that the
d
15
N value of soil macro-
invertebrates commonly reflects the local
d
15
N value of leaf litter,
and the values that we found were similar to those reported for
Tetramorium sp. studied by Penick, Savage, and Dunn (2015).
DISCUSSION
Every colony of E. ruidum simultaneously maintains individuals
that collect the same type of food item, but with two distinct
foraging strategies. Workers of these foraging types are behav-
iourally distinct from one another but rely upon a common pool of
food resources. The disparate behaviours that make up these two
strategies effectively serve to repartition the original pool of re-
sources gained during primary foraging. The first foraging strategy
is ‘normal’, with workers that collect food from within their terri-
tories. These individuals find food within the home range, walk in a
straight line back to the nest, encounter other ants along the way,
interact with them, and carry on in a nonchalant fashion. The
second foraging strategy is thievery, in which workers collect food
from inside a colony that is outside their own colony's home range.
These individuals walk more slowly, pause more frequently and
avoid encountering conspecifics en route. These individuals are also
more prone to reverse direction when perturbed and to drop their
pilfered food items when grabbed.
The presence of distinct foraging strategies in E. ruidum is
notable because individual differences in social insects are more
often recognized with respect to reproductive potential or divi-
sion of labour. The identification of a distinct foraging strategy,
but for the same type of food, is uncommon. Polybia occidentalis
wasp foragers specialize on either pulp or prey/nectar (O'Donnell
&Jeanne, 1990) and honeybee (A. mellifera) foragers specialize on
either pollen or nectar (Page, Rueppell, &Amdam, 2012), but
these examples describe individuals that have different foraging
preferences. The predilection for specialized foraging behaviours
also occurs in E.ruidum, as foragers may be subdivided into in-
dividuals that attack prey by stinging and those that transport
food that has already been killed (Schatz, Lachaud, &Beugnon,
199 6).
Like soldiers and workers in other species of ants, thieves and
foragers are nonreproductive individuals. However, unlike soldiers
and workers, thieves are not morphologically different from for-
agers. Aside from behaviours that may be characterized as ‘sneaky’,
such as ducking under nearby leaves, trying to outrun an
approaching pair of forceps or dropping their food, thieves and
foragers are indistinguishable. The lack of differentiation extends to
diet, as the carbon and nitrogen compositions of thieves and non-
thieves do not differ. The etiology of thievery in E. ruidum remains
enigmatic, and it is not known whether it is a learned behaviour.
The lack of overt dietary differences provides an additional piece of
evidence for investigation into the development of thieves. It does
not appear that thieves are fed a different food source during
development or consume a different food source than other
members of the colony. Their distinct behavioural repertoire
merely repartitions resources primarily gained through initial
foraging.
The apparent rarity of conspecific thievery in ants leads us to ask
whether any properties of E. ruidum may have facilitated the evo-
lution of thievery. Colonies can incur a reduction in productivity
when thieves are present in the population, although this cost is
reduced in denser populations (Jandt et al., 2015). The cost of
detection is very low for thieves: they are physically removed from
the victim colony environment unharmed, but they soon return to
steal from the same colony again. The lack of lethal aggression
against detected thieves must influence the costebenefit trade-offs
of thieving and vigilance against thieves. The genetic structuring of
populations may have caused low levels of intercolonial aggression,
as is known in the congener Ectatomma tuberculatum (Zinck, Hora,
Ch^
aline, &Jaisson, 2008). Ectatomma ruidum is known for nesting
in open environments and in high density (Schatz &Lachaud,
2008), which may influence the success of food robbing and facil-
itate the rapid egress of thieves (Paulson, 1985). Most species of
ants, especially those in the tropics, are not subjected to intense
colony-level behavioural experimentation, and it may be that
thievery is not a rare phenomenon, but one that is widely
undocumented.
Acknowledgments
This work was supported by the National Science Foundation
(OISE-1261015; HRD-1302873) and the CSUDH Office of Under-
graduate Research, Scholarship and Creative Activity. We thank the
100
50
25
0Thief
Reversed direction Paused Dro
pp
ed food
Nonthief Thief Nonthief Thief Nonthie
f
Frequency (%)
75
Figure 2. Percentages of E. ruidum thieves and nonthieves that reversed direction, paused or dropped food after encountering a conspecific target (a freeze-killed ant mounted on a
probe). Black bars indicate the frequency of behaviours (see Results for statistical analyses).
T. P. McGlynn et al. / Animal Behaviour 109 (2015) 243e247246

staff of La Selva Biological Station for logistic support, particularly
Bernal Matarrita and Danilo Brenes. The project was conceived by
T.P.M. and designed by T.P.M., J.M.J., J.W., J.E. and R.G. Fieldwork was
conducted by R.G., J.W. and J.E. Statistical analyses were conducted
by T.P.M. and A.H.J. The manuscript written by T.P.M. with contri-
butions from J.M.J. and A.H.J.
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