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

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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.
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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
conspecic thievery
Ectatomma ruidum
food pilferage
foraging
kleptoparasitism
nestmate recognition
social living
A principal benet of social living is the communal defence of resources. However, in the ant Ectatomma
ruidum, specialized thieves often circumvent detection by conspecic 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 conspecic 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 conspecics, 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 conspecics. 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 tness, 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 intraspecic 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). Conspecic
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 intraspecic thievery has only been documented in two spe-
cies: Messor aciculatus (Yamaguchi, 1995) and Ectatomma ruidum
(Breed, Snyder, Lynn, &Morhart, 1992; Perfecto &Vandermeer,
1993). Intraspecic food robbing remains undetected in other ant
species, despite extensive observation of many other species.
Nevertheless, in E. ruidum, intraspecic 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 prole 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. Intraspecic 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 intraspecic 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 difcult 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 actof 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 eld
identication 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 eld 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 Conspecics
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 conspecics, 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 conspecic ant, or if an antenna
of the conspecic 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. conspecic 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 identied an active focal individual
(thief or nonthief) and followed her for at least 20 cm. We waved
the conspecic 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 cong-
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 signi-
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 Conspecics
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 reects 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 rst foraging strategy
is normal, with workers that collect food from within their terri-
tories. These individuals nd 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 conspecics 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 identication 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 conspecic 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 inuence the costebenet 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 inuence 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 Ofce 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 conspecic 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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... Many social insects that rely on solitary stealth maneuvers have evolved behavioral strategies for overcoming this challenge (Matsuko 1984;Gronenberg 1996;Jackson and Pollard 1996;Murphy and Patek 2012). For example, Ectatomma ruidum are facultatively solitary foragers, enabling the use of a prolonged stealth approach to capture food items from heavily defended colonies of other social insects (Lima and Antonialli-Junior 2013;McGlynn et al. 2015;Schatz and Wcislo 1999). ...
... This apparent preference for feeding on social insects is also common in other species of Ectatomma (Lima and Antonialli-Junior 2013;Schatz and Wcislo 1999). Individual behavioral specialization on different foraging strategies has been demonstrated in Ectatomma ruidum, where foragers may preferentially perform either Btypical foraging^or Bthievery^ (McGlynn et al. 2015). Ambush predation entails similar behaviors and may represent another valuable foraging strategy employed by a behavioral sub-caste of Ectatomma foragers. ...
Article
Social insect colonies are high-value foraging targets for insectivores, prompting the evolution of complex colony defensive adaptations as well as specialized foraging tactics in social insect predators. Predatory ants that forage on other social insects employ a diverse range of behaviors targeted at specific prey species. Here, we describe a solitary foraging strategy of the ant Ectatomma tuberculatum, on nest guards of the stingless bee Tetragonisca angustula. We observed multiple instances of E. tuberculatum ambushing and successfully capturing the hovering and standing guards of T. angustula near nest entrances. The unique hovering behavior of the guard caste of this bee species, an adaptation to frequent cleptoparasitism by other stingless bees, may make these guards particularly vulnerable to ground-based, ambush attacks by E. tuberculatum. Likewise, the behavior of the foraging ants appears to adaptively exploit the defensive formations and activity patterns of these bees. These observations suggest an adaptive and targeted predatory strategy aimed at gathering external guard bees as prey from these heavily fortified nests.
... Here, we focus on defences against parasites that directly take advantage of the sociality of their hosts, i.e. social parasites. Many social parasites are social themselves, such as the slavemaking ants [12], cleptoparasitic ants and bees [13][14][15] or ants, wasps and bees that sneak into other nests to reproduce [16][17][18], while others have social ancestors, such as many workerless ant inquilines [19]. We will restrict our discussion to these cases. ...
... Social parasites are often closely related to their hosts (referred to as 'Emery's rule') [64,65], which distinguishes these host-parasite interactions from those of microbial or viral parasites and their multicellular hosts. In cases of intraspecific parasitism, colonies are parasitized by workers or queens of the same species [14,16,18,28,51,52,66,67] or sub-species [17,29] that attempt to raid resources or reproduce. Even in interspecific relationships, such as in the workerless ant inquilines (table 1), they are often their hosts' sister species [19,30]. ...
Article
Insect societies face many social parasites that exploit their altruistic behaviours or their resources. Due to the fitness costs these social parasites incur, hosts have evolved various behavioural, chemical, architectural and morphological defence traits. Similar to bacteria infecting multicellular hosts, social parasites have to successfully go through several steps to exploit their hosts. Here, we review how social insects try to interrupt this sequence of events. They can avoid parasite contact by choosing to nest in parasite-free locales or evade attacks by adapting their colony structure. Once social parasites attack, hosts attempt to detect them, which can be facilitated by adjustments in colony odour. If social parasites enter the nest, hosts can either aggressively defend their colony or take their young and flee. Nest structures are often shaped to prevent social parasite invasion or to safeguard host resources. Finally, if social parasites successfully establish themselves in host nests, hosts can rebel by killing the parasite brood or by reproducing in the parasites' presence. Hosts of social parasites can therefore develop multiple traits, leading to the evolution of complex defence portfolios of co-dependent traits. Social parasites can respond to these multi-level defences with counter-adaptations, potentially leading to geographical mosaics of coevolution. This article is part of the Theo Murphy meeting issue ‘Evolution of pathogen and parasite avoidance behaviours’.
... Further studies and extended sampling are needed to test the link between local biotic and abiotic factors and CHC variation in this group. ~ 41 ~ The colonies of E. ruidum reach extremely high densities (Pratt 1989;Schatz and Lachaud 2008) and these ants exhibit intraspecific thievery, where specialized individuals consistently "forage" by stealing food from neighboring colonies De Carli et al. 1998;McGlynn et al. 2015). Although in some populations these ants have a relatively permissive non-nestmate acceptance threshold De Carli et al. 1998;Jandt et al. 2015), high nest density and thievery might have promoted stricter acceptance thresholds in other populations. ...
Thesis
To describe and understand biodiversity, the identification of species is essential. Because some species diversify without revealing any morphologic change, the use of different taxonomic tools is highly recommended. Among the advantages of employing different traits for species classification, one of the most remarkable is that at the same time we obtain information about which traits have been involved in the diversification of species. In this study I investigated the variation observed in the ant species Ectatomma ruidum as an evidence of different taxa. E. ruidum is a widely distributed ant from the Neotropics and in previous studies based on mitochondrial sequences the species was proposed to include at least four different taxa. The geographic distribution patterns of the putative species shows that some of them are restricted to small areas, without any apparent geographic barrier separating populations, which raised the question about which mechanisms separated them. By analyzing recognition cues, acoustic signals, morphological acoustic traits and DNA sequences (mitochondrial DNA COI gene, 3RAD and UCE) I provide evidence supporting the separation for most of the previously proposed species. Additionally, the combination of phenotypic and genetic information unveiled that recognition cues may have had a very important role in the diversification of the species complex. Overall, this study adds evidence in favor of the use of a multi trait approach for the delimitation of closely related specie
... The colonies of E. ruidum reach extremely high densities (Pratt 1989;Schatz and Lachaud 2008) and these ants exhibit intraspecific thievery, where specialized individuals consistently "forage" by stealing food from neighboring colonies (Breed et al. 1990;De Carli et al. 1998;McGlynn et al. 2015). Although in some populations these ants have a relatively permissive non-nestmate acceptance threshold (Breed et al. 1990;De Carli et al. 1998;Jandt et al. 2015), high nest density and thievery might have promoted stricter acceptance thresholds in other populations. ...
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In social insects, chemical communication is the main communication mode among colony members, which use the blends of cuticular hydrocarbons as recognition cues to discriminate between nestmates and non-nestmates and to prevent the exploitation of their nest resources by aliens. The aim of this study was to assess the variation of nestmate recognition cues in the ant Ectatomma ruidum, a species complex with a considerably conserved morphology and one of the few ant species where intraspecific thievery, a form of cleptoparasitism, has been reported. We analyzed the cuticular hydrocarbon profiles of ants collected from a number of geographically separated populations and examined DNA sequence data to assess their species identity. We focused on one species of the complex, E. ruidum sp. 3–4, whose species delineation remains controversial. We documented that several quantitative and qualitative traits of the cuticular hydrocarbon profiles varied significantly between populations, indicating that this species harbors more cuticular chemical phenotypic diversity than expected within a single species. In particular, there was a striking divergence among populations in the proportion of methylalkanes, alkenes, alkadienes and odd-chain components, which likely play a major role in nestmate/non-nestmate discrimination, a process which might have been crucial in these cleptobiotic ants. Further investigations are needed to test the hypothesis that biotic pressures, such as the need to discriminate conspecific intruders and limit thievery, could have played an important role in promoting the evolutionary divergence between populations in this ant species complex.
... These individuals should also have more flexible learning abilities and rely more on personal information. Foragers who vary in their foraging strategies as in Ectatomma ruidum (McGlynn et al., 2015) or in their resource specialization as in Formica aquilonia (Iakovlev and Reznikova, 2019) should also vary in their personality traits and cognitive abilities. Since the task repertoire of individual ants changes with age, further studies are also required to understand whether personality traits of individuals remain constant across their lifetimes and how this affects their task choice and task performance at different stages of their life. ...
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Animals live in heterogeneous environments where food resources are transient and have to be exploited rapidly. Ants show a wide range of foraging strategies and this activity is tightly regulated irrespective of the mode of recruitment used. Individual foragers base their decision to forage on information received from nestmates (social information). Transmission of information can be in the form of direct physical interactions such as antennation or indirect exchange of information such as laying of pheromone trails. Foragers also rely on information from their internal states or experience (personal information). The interaction between these two sources of information gives rise to plasticity in foraging behavior. Recent studies have examined the role of personality (consistent inter-individual variation in behavioral traits) during ant foraging. Since colonies differ from each other in the distribution of personalities of their members, colonies may consistently differ in behavioral traits, giving rise to colony level personality. However, the interaction between information use and personality, especially at the individual level, remains unexplored. Here, we briefly summarize the literature on the effect of social and personal information on the regulation of ant foraging and the effect of personality on this behavior. We point out that a more focused examination of the interplay between personality and information use will help us understand how behavioral plasticity in the context of foraging is shaped at the colony and individual levels.
... Whether the thieves maintain this speed all the way back to their nest was not examined in the current study, but we expect this not to be the case as the density of foreign ants would be lower. Increase in the speed of thieves while in the home range of the victim colony was also reported in E. ruidum ants ( McGlynn et al., 2015). The average length of the body of an adult female D. indicum ant is about 1 cm. ...
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Theft of resources is ubiquitous in the animal kingdom. An evolutionary arms race between thieves and their victims is expected. Although several studies have documented inter- and intraspecific theft of resources in different taxa, studies that delve into the behaviour of thieves and the factors that influence their behaviour have not been undertaken. In the current study on the primitively eusocial ant Diacamma indicum, we caught brood thieves red-handed: we observed them in the act of stealing brood and examined their behaviour. Thieves were persistent in their attempts despite facing aggression in the victim colony. Experiencing aggression or failure to steal in the previous attempt negatively impacted a thief’s drive to reattempt. To avoid the risks associated with theft, successful thieves exited from victim nests about three times faster than others who were procuring brood from unguarded nests. In a series of experiments examining factors that caused thieves to increase their exit speed, we found that indirect cues of a foreign colony’s presence, such as odour or the presence of foreign ants, did not induce these changes in thieves. Thus, we conclude that these ant thieves only respond to the direct threat posed by aggressive foreign ants. In this comprehensive study using behavioural experiments, we reveal the simple rules of engagement between victims and brood thieves.
... In contrast, in compound nests two ant species share a nest space or nest close to one another and occasionally interact, but they keep and rear their brood separately (Wasmann 1891;Wheeler 1901;Hölldobler and Wilson 1990). Interactions in compound nests range from commensalism, where one species benefits from the nest environment of a host species and occasionally feeds on food scraps of the host species, to parasitic interactions, where the parasite feeds on host brood or is fed by the host via trophallaxis (Table 1) (Hölldobler and Wilson 1990;Breed et al. 2012;Kanizsai et al. 2013;Gallego-Ropero and Feitosa 2014;McGlynn et al. 2015). Traditionally, interactions between ant species living in compound nests were categorized with a set of Hellenistic terms (Forel 1898(Forel , 1901Wheeler 1901Wheeler , 1910 (Table 1). ...
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Over 40 years ago, the dacetine ant Strumigenys arizonica was discovered in a nest of the fungus-growing ant Trachymyrmex arizonensis at Madera Canyon in the Santa Rita Mountains of the southwestern United States. This discovery suggested that the two species form compound nests, but this hypothesis has not been investigated. Here, we characterize this symbiosis through an analysis of collection records supplemented by recent field and laboratory observations. Our observations show that S. arizonica and T. arizonensis form compound nests that are a type of commensalistic symbiosis. Individuals of S. arizonica forage in galleries and tunnels of T. arizonensis nests but do not steal fungus or brood. Instead, individuals of S. arizonica hunt collembolans in the internal refuse piles of T. arizonensis nests. Interestingly, S. arizonica was never found independent of its host T. arizonensis over a significant portion of the geographic range of T. arizonensis. These results suggest a tight but asymmetric association where compound nesting is obligate for S. arizonica and facultative for T. arizonensis.
... Our data were collected in second-growth tropical dry forest, which has a relatively low and open/broken canopy (Murphy and Lugo 1986), and day-foraging E. ruidum workers may have experienced higher temperatures than the weather station data indicated (Kaspari et al. 2014;Scheffers et al. 2016). E. ruidum is a widespread, often abundant and conspicuous species that occurs in a wide range of habitats and life zones (McGlynn et al. 2015;Aguilar-Velasco et al. 2016). Future studies could assess whether E. ruidum worker diel thermal tolerance differences occur in other habitats. ...
Article
Physiological constraints can limit thermal niche breadth in organisms, particularly for small-bodied ectotherms. Daily temperature fluctuations often surpass annual (seasonal) temperature variation in the tropics, suggesting diel temperature cycles could drive thermal specialization by individuals that are active at different times of the day. We used foraging workers of the Neotropical ant Ectatomma ruidum to assess whether diurnally and nocturnally active workers differed in thermal tolerance. We compared critical thermal maxima (CTmax) of nocturnal and diurnal foraging workers to explore thermal niche specialization over the diel cycle. We predicted that diurnally active workers would have higher CTmax because they occupy a warmer thermal niche. As predicted, diurnal foragers exhibited significantly higher CTmax (mean 1.1 °C difference) than nocturnal foragers. Diurnal and nocturnal foragers were similar in body size, and there was no relationship between worker size and CTmax. We discuss possible mechanisms for this pattern, and the implications of within- versus between-colony differences in CTmax.
... Our data were collected in second-growth tropical dry forest, which has a relatively low and open/broken canopy (Murphy and Lugo 1986), and day-foraging E. ruidum workers may have experienced higher temperatures than the weather station data indicated (Kaspari et al. 2014;Scheffers et al. 2016). E. ruidum is a widespread, often abundant and conspicuous species that occurs in a wide range of habitats and life zones (McGlynn et al. 2015;Aguilar-Velasco et al. 2016). Future studies could assess whether E. ruidum worker diel thermal tolerance differences occur in other habitats. ...
Article
Full-text available
Physiological constraints can limit thermal niche breadth in organisms, particularly for small-bodied ectotherms. Daily temperature fluctuations often surpass annual (seasonal) temperature variation in the tropics, suggesting diel temperature cycles could drive thermal specialization by individuals that are active at different times of the day. We used foraging workers of the Neotropical ant Ectatomma ruidum to assess whether diurnally and nocturnally active workers differed in thermal tolerance. We compared critical thermal maxima (CTmax) of nocturnal and diurnal foraging workers to explore thermal niche specialization over the diel cycle. We predicted that diurnally active workers would have higher CTmax because they occupy a warmer thermal niche. As predicted, diurnal foragers exhibited significantly higher CTmax (mean 1.1 °C difference) than nocturnal foragers. Diurnal and nocturnal foragers were similar in body size, and there was no relationship between worker size and CTmax. We discuss possible mechanisms for this pattern, and the implications of within- versus between-colony differences in CTmax.
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Understanding the ecological relevance of variation within and between colonies has been an important and recurring theme in social insect research. Recent research addresses the genomic and physiological factors and fitness effects associated with behavioral variation, within and among colonies, in regulation of activity, cognitive abilities, and aggression. Behavioral variation among colonies has consequences for survival and reproductive success that are the basis for evolutionary change.
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For diverse communities of omnivorous insects such as ants, the extent of direct consumption of plantderived resources vs. predation is largely unknown. However, determination of the extent of “herbivory” among ants may be crucial to understand the hyperdominance of ants in tropical tree crowns, where prey organisms tend to occur scarcely and unpredictably. We therefore examined N and C stable isotope ratios (d15N and d13C) in 50 ant species and associated insects and plants from a tropical rainforest in North Queensland, Australia. Variation between ant species was pronounced (range of species means: 7.1‰ in d15N and 6.8‰ in d13C). Isotope signatures of the entire ant community overlapped with those of several herbivorous as well as predacious arthropods. Variability in d15N between ants was not correlated with plant d15N from which they were collected. Ant species spread out in a continuum between largely herbivorous and purely predacious taxa, with a high degree of omnivory. Ant species’ d15N were consistent with the trophic level predicted by natural feeding observations, but not their d13C. Low d15N levels were recorded for ant species that commonly forage for nectar on understorey or canopy plants, intermediate levels for species with large colonies that were highly abundant on nectar and honeydew sources and were predacious, and the highest levels for predominantly predatory groundforaging species. Colonies of the dominant weaver-ants (Oecophylla smaragdina) had significantly lower d15N in mature forests (where preferred honeydew and nectar sources are abundant) than in open secondary vegetation. N concentration of ant dry mass showed only very limited variability across species and no correlation with trophic levels. This study demonstrates that stable isotopes provide a powerful tool for quantitative analyses of trophic niche partitioning and plasticity in complex and diverse tropical omnivore communities.
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Most social animals have mechanisms to distinguish group members from outsiders, in part to prevent the exploitation of resources reserved for members of the group. Nevertheless, specialized thieves of the Neotropical ant, Ectatomma ruidum, also known as the 'thieving ant', regularly enter and steal resources from distinct, neighboring colonies. Here, we examine the mechanisms and consequences of thievery in a population of E.ruidum. We show that (1) individuals from nearby colonies were accepted more often than those from farther colonies; (2) rejection rates decreased as individuals interacted more with non-nestmates from the same source colony; and (3) colonies that were experimentally treated to reduce thievery rates had improved productivity. The boost in productivity with thievery reduction was greater in low density populations than in high density populations. We conclude that, as in other species, thievery has negative fitness costs to E.ruidum. However, greater acceptance of neighbors than non-neighbors and increased acceptance after habituation to non-nestmates suggest a proximate explanation for the presence of thievery. Moreover, lower fitness costs of thievery at high nesting density, combined with observations of extraordinarily high densities of E.ruidum throughout its range, suggest there is little selection pressure among these ants to guard against thieves, thus providing an ultimate explanation why thievery persists among litter-foraging ants.
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Intraspecific kleptoparasitism among Kelp Gulls (Lams dominicanus) was studied at four sites in the southwestern Cape Province of South Africa. Sites included: (1) undisturbed foraging habitats; (2) a sandy beach and a rocky shore; and (3) areas where supplementary food was available - a fishing harbor and a refuse dump. Simple food-choice experiments were used to test hypotheses generated from field observations. Among-site variation in the rate and success of kleptoparasitism was related to prey attributes, of which prey size and handling time were the most important. In food-choice experiments, gulls selected small prey with short handling times. Prey with long handling times were the most likely to be stolen and the rate of keptoparasitism was higher when prey were dispersed than when they were clumped. There were marked age-related differences in the rate, although not the success, of kleptoparasitism among Kelp Gulls. Juvenile (first-year) gulls attempted kleptoparasitism significantly more often than expected and adults significantly less often. Subadults kleptoparasitized in proportion to their abundance in the population. If an age-related dominance hierarchy exists, it mediates kleptoparasitic behavior in Kelp Gull assemblages through older birds avoiding kleptoparasitic attacks rather than initiating them. Simple mathematical models, based on data collected during field observations, were used to investigate the conditions explaining the rate of intraspecific kleptoparasitism within Kelp Gull populations. Either few individuals can kleptoparasitize relatively frequently, or many individuals can kleptoparasitize infrequently. Apparently, both mechanisms operate within Kelp Gull populations because individuals attempt kleptoparasitism relatively frequently when they are juveniles and inefficient hunters, but infrequently once they are adult and efficient hunters. The viability of facultative intraspecific kleptoparasitism as a foraging technique relies on stolen prey being larger on average than the prey captured by hunting.
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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.
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Animals reflect the stable isotope ratios (delta(15)N and delta(13)C) of their diet, with a slight enrichment in N-15 that allows the use of delta(15)N as a trophic-level indicator Stable isotope contents were measured for the litter, soil, and macro-invertebrates of three temperate deciduous forest sites, in spring, summer, and autumn, to study the trophic structure of this community. No distinct trophic structure could be derived from measurements of delta(13)C. In contrast, when the delta(15)N values of all animal species were grouped together, the hypothesis of an isotopically similar diet was rejected. Therefore, the community spreads over more than one trophic level and was subdivided into detritivores and predators. The potential detritivore food sources in the forest litter and soil showed a variety of isotopic ratios. Despite this fact. the variance of the isotopic ratios of the detritivorous species was nor larger than what could be expected from interspecific variability of trophic isotopic enrichment alone. This was also the case for the predators in most of the sample sets. However, in some cases this variance was significantly larger, due to a small number of species with high delta(15)N values. The delta(15)N values of the detritivores indicated that the mean delta(15)N value of their food was close to that measured for the superficial litter layers. The difference in delta(15)N between detritivores and predators was highly significant and never significantly different from the value expected fur one trophic transfer (3.4 parts per thousand), although often slightly higher. Most of the litter macro-invertebrate community we studied can therefore be described as belonging to two trophic levels, one feeding on the superficial litter layers (or on soil fractions that have a similar delta(15)N value), and a second trophic level feeding on the first, with some indication of intraguild predation among the predators. Between-site differences of up to 7 parts per thousand were found for delta(15)N in the litter, and the delta(15)N values of the whole animal community were shifted in accordance with the local value of the litter delta(15)N. Therefore, the trophic structure must be studied in relation to the local isotopic content of the litter. Seasonal differences in isotopic ratios of the litter or animal samples were neither large nor consistent. These findings indicate similar trophic structure of the communities at the three sites and during the three sampling periods.
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The authors used δ15N and δ13C measurements to study formation and decay of soil organic matter in surface soils of two oak (Quercus spp.) forests in Wisconsin. There were two controls of soil isotopic compositions: new litter inputs and overall isotopic fractionation during decomposition. Litter inputs lowered soil δ15N and δ13C values while decomposition increased δ15 and δ13C values. Field experiments showed that low surface soil δ15N and δ13C values resulted when litter inputs were high. Laboratory experiments showed that overall isotopic fractionation during decomposition left residual soil N and C enriched in 15N and 13C, and could explain the high δ15N and δ13C values observed in deeper forest soils.
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