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Density of Antennal Sensilla Influences Efficacy of Communication in a Social Insect
Author(s): Katherine P. Gill, Ellen van Wilgenburg, David L. Macmillan, and Mark A. Elgar,
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vol. 182, no. 6 the american naturalist december 2013
Natural History Note
Density of Antennal Sensilla Influences Efficacy
of Communication in a Social Insect
Katherine P. Gill, Ellen van Wilgenburg, David L. Macmillan, and Mark A. Elgar*
Department of Zoology, University of Melbourne, Melbourne, Victoria 3010, Australia
Submitted February 18, 2013; Accepted June 19, 2013; Electronically published October 9, 2013
Dryad data: http://dx.doi.org/10.5061/dryad.7c9q7.
abstract: Effective communication requires reliable signals and
competent receptors. Theoretical and empirical accounts of animal
signaling focus overwhelmingly on the capacity of the signaler to
convey the message. Nevertheless, the intended receiver’s ability to
detect a signal depends on the condition of its receptor organs, as
documented for humans. The impact of receptor organ condition
on signal reception and its consequences for functional behavior are
poorly understood. Social insects use antennae to detect chemical
odors that distinguish between nestmates and enemies, reacting ag-
gressively to the latter. We investigated the impact of antennal con-
dition, determined by the density of sensilla, on the behavior of the
weaver ant Oecophylla smaragdina. Worker aggression depended
upon the condition of their antennae: workers with fewer sensilla
on their antennae reacted less aggressively to nonnestmate enemies.
These novel data highlight the largely unappreciated significance of
receptor organ condition for animal communication and may have
implications for coevolutionary processes in animal communication.
Keywords: signal receiver, nestmate recognition, chemical commu-
nication, antennae, Oecophylla smaragdina, signal detection error.
Introduction
It is widely understood that effective communication re-
quires a combination of reliable signals and sensitive re-
ceptors, allowing the receiver to detect the signal precisely
and thus behave accordingly. At the organismic level, the
field has been largely dominated by an interest in the
degree to which signals provide accurate or honest infor-
mation about the signaler (Kotiaho 2001; Maynard Smith
and Harper 2003; Searcy and Nowicki 2005; Johansson
and Jones 2007; Botero et al. 2010; Sza´mado´ 2011; Stevens
and Ruxton 2012). While there have been some investi-
gations into how receiver strategies might act as a selection
pressure on signals (Johnstone 1994; Hailman 2008;
Broom and Ruxton 2011), the impact of the condition of
* Corresponding author; e-mail: m.elgar@unimelb.edu.au.
Am. Nat. 2013. Vol. 182, pp. 000–000. 䉷2013 by The University of Chicago.
0003-0147/2013/18206-54489$15.00. All rights reserved.
DOI: 10.1086/673712
the receptor organs on the capacity of the receiver to detect
and/or interpret the signal has rarely, if ever, been inves-
tigated in species other than humans (Roth et al. 2004;
Bovo et al. 2011), and much of this interest is at the genetic
and neurobiological level (e.g., Frasnelli et al. 2011).
The receptor component of visual and auditory sensory
systems deteriorates with age in humans and other ver-
tebrates, although the relative importance of senescence,
environmental damage, or both remains unclear (Roth et
al. 2004; Limburg and Keunen 2009; Bovo et al. 2011).
Less is known about the effect of these long-term processes
on olfactory sensory systems, despite their crucial role in
foraging and mating success, social interactions, and
avoidance of enemies, all of which depend upon the ac-
curate detection of chemical signals and cues (Wyatt2003).
The antennae of insects are essential for acquiring chemical
information, yet they are also subject to substantial wear
and tear (Seabrook et al. 1979). While neurophysiological
studies of insects reveal variation in response to chemical
signals with age (Seabrook et al. 1979; Blaney et al. 1986;
Vetter and Visscher 1997), this typically reflects the very
early days of adult life. Whether the condition of the re-
ceptor organ affects the individual’s ability to detect a
signal and respond appropriately is apparently unknown.
The profoundly cooperative behavior of social insects
relies on a combination of chemical and tactile signals,
typically detected through the antennae. In particular, so-
cial insects rely on chemical signals to distinguish between
colonymates and other enemies, thereby ensuring the in-
tegrity of the colony and preventing nonnestmates from
exploiting colony resources (Crozier and Pamilio 1996;
d’Ettorre and Lenoir 2010; van Wilgenburg et al. 2011;
Sturgis and Gordon 2012; van Wilgenburg and Elgar
2013). The chemical signals involved in colonymate rec-
ognition are nonvolatile cuticular hydrocarbons, com-
prising a mixture of alkanes, alkenes, and methyl-branched
alkanes (van Wilgenburg et al. 2011). An individual worker
discerns the identity of another individual by sweeping
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000 The American Naturalist
and/or brushing her antennae against the cuticle of her
counterpart, thereby obtaining information about the pro-
file and typically responding aggressively if it is not a nest-
mate (d’Ettorre and Lenoir 2010; van Wilgenburg et al.
2011; see also Brandstaetter et al. 2008).
It is widely recognized that there is both inter- and
intraspecific variation in the nature of the response of ants
to nonnestmate conspecifics, but the source of this vari-
ation has not been widely examined (Sturgis and Gordon
2012). The primary focus is how ecological and social
factors might modify workers’ response to nonnestmates,
including seasonal changes (Mabelis 1979; Ichinose 1991;
Katzerke et al. 2006), territoriality (Whitehouse and Jaffe
1995; Wenseleers et al. 2002), experimental design (van
Wilgenburg and Elgar 2013), and the number (Gordon et
al. 1993; Roulston et al. 2003; Sorrells et al. 2011), age
(Nowbahari and Lenoir 1989; van Wilgenburg et al. 2005),
and size (Nowbahari et al. 1999) of the workers. In con-
trast, Newey et al. (2010) propose that the variation in
worker response may derive from differences in signal per-
ception, which they suggest is the result of adaptive dif-
ferences in individual odor templates. An alternative ex-
planation, not favored by Newey et al. (2010), is that the
variation derives from recognition “error.”
The antennae of ants are covered by numerous che-
mosensory sensilla (Hashimoto 1990; Kleineidam et al.
2000; Renthal et al. 2003; Babu et al. 2011; Barsagade et
al. 2013) that detect specific odors, including those asso-
ciated with nestmate recognition (Ozaki et al. 2005). The
abundance and diversity of these sensilla begs the question
of whether the number or density of intact sensilla on the
antennae influences the capacity of ants to acquire chem-
ical information and respond as expected—in other words,
whether the observed variation in aggressive behavior is
influenced by the condition of the antennae.
The weaver ant Oecophylla smaragdina occurs in tropical
North Australia, equatorial Asia, and India (Schlu¨ens et
al. 2009; Crozier et al. 2010). Colonies of O. smaragdina
comprise up to 500,000 workers that inhabit numerous
leaf nests located on several neighboring trees. Weaver ants
may be polyandrous, with resulting relatively low levels of
relatedness within colonies (Schlu¨ens et al. 2009). There
are two morphologically distinct worker castes: smaller
minor workers that typically remain within the nest, tend-
ing the brood and queen, and larger, moreaggressive major
workers that forage outside the nest (Crozier et al. 2010).
The major workers of O. smaragdina use chemical signals
to distinguish between nestmates and conspecific non-
colonymates and other enemies, and they typically respond
aggressively to the latter (Ho¨ lldobler 1983; Elgar and Allan
2006; Gill et al. 2012). The smaller, minor workers remain
within the nest, tending to the queen and brood. Inter-
estingly, the antennae of minor workers have both fewer
antennomeres and fewer sensilla basiconica and sensilla
trichoidea curvata per antennomere than do major work-
ers; these differences may be linked to differences in the
behavior of the two castes (Babu et al. 2011).
We address two specific questions. First, we ask whether
the condition of a worker’s antennae, as reflected by the
density of sensilla, explain the variation in the level of
aggression directed toward conspecific workers from an-
other colony. Second, we ask whether any differences in
the condition of the antennae or the individual’s behavior
are related to the age of the worker.
Material and Methods
Behavioral Assays
We conducted standard nestmate recognition bioassays
(Dreier et al. 2007) and compared the observed level of
aggression with measures of the condition of both anten-
nae and mandibles, using the latter as an estimate of
worker age (Smeeton 1982; van Wilgenburg et al. 2005;
Massey and Hartley 2009).
We selected, at random, 24 colonies of Oecophylla smar-
agdina located on the campus of James Cook University
(Townsville, Australia), and each was individually identi-
fied. Numerous workers were removed from the nests of
each colony with forceps and held in 1-L plastic containers
lined with polytetrafluoroethylene (Fluon). Nests on
neighboring trees were deemed to be from different col-
onies if aggressive behavior was observed between major
workers (see Gill et al. 2012).
We conducted standard one-on-one nestmate recogni-
tion bioassays between workers from pairs of colonies,
following Gill et al. (2012). These assays took place in
plastic containers (8 cm diameter #3 cm high). One ant,
deemed the focal ant, was marked on her gaster with a
small dot of acrylic fluorescent paint 15 min before the
assay. The other ant remained unmarked and was gently
introduced into the container, and the pair was observed
for 3 min. We marked only the focal ant because we did
not want the paint to interfere with any chemical signals
produced by the other ant. We recorded the frequency of
four behaviors that are typical of interactions between
workers: grooming and trophallaxis, recoil and mandible
flare, nipping and gaster flexion, and biting and grappling.
Each of these four behaviors was weighted from 1 to 4,
respectively, providing a comparative, numerical aggres-
sion score (modified from Thomas et al. 1999). We cal-
culated an aggression index for each trial (following Dreier
et al. 2007; Gill et al. 2012):
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Antennal Condition and Signal Perception 000
AB
CD
Figure 1: Wear and tear on the antennae and mandibles of Oecophylla smaragdina and their effects on behavior: the distal funiculus of the
antennae illustrating limited (A) and extensive (C) wear and tear to the sensory hairs on the antennae and limited (B) and extensive (D;
with a broken first incisor) wear and tear of the mandibles.
4
冘(A#f)
ii
i
,(1)
N
where A
i
is the aggression score for each behavior i,f
i
is
the frequency of that behavior, and Nis the sum of the
frequencies of all behaviors in the 3-min trial.
We conducted four aggression bioassays for each ran-
domly allocated colony pair. The trials took place in the
field to minimize the time ants were removed from the
colony, and no ant was used more than once. At the end
of the trial, each worker was preserved in an individually
labeled vial for subsequent morphological measurements,
ensuring that the observer had no a priori knowledge of
the density of sensilla on the antennae of the observed
worker.
Morphological Measurements
The antennae of each marked worker were cut at the prox-
imal end from the head, laid flat on a clean slide, and
viewed under an Olympus BX51 light microscope attached
to a camera with #100 magnification. Several images of
the antennae were taken using SPOT (ver. 4.7.0) to obtain
a full segment length in focus, and Image-Pro Plus (ver.
6.3) was used to overlay the images and invert the final
image. We recorded the number of all types of sensilla
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000 The American Naturalist
Tabl e 1 : Summary statistics of worker traits across 12 colonies of Oecophylla smaragdina
Colony Antennae length (mm) Total sensilla per mm Mandible wear Aggression index
130 367.0 Ⳳ31.0 6.3 Ⳳ3.6 3.3 Ⳳ.3 1.6 Ⳳ.7
132 368.6 Ⳳ33.0 10.2 Ⳳ4.4 6.0 Ⳳ3.3 2.2 Ⳳ1.1
136 365.2 Ⳳ9.1 9.5 Ⳳ2.8 4.2 Ⳳ1.1 2.1 Ⳳ.2
145 355.5 Ⳳ14.8 6.1 Ⳳ2.1 4.1 Ⳳ.9 2.7 Ⳳ1.7
152 364.9 Ⳳ19.4 6.5 Ⳳ1.0 3.4 Ⳳ.2 1.4 Ⳳ.6
159 372.7 Ⳳ12.7 6.1 Ⳳ1.5 4.4 Ⳳ.9 2.3 Ⳳ1.0
166 363.3 Ⳳ12.7 8.0 Ⳳ1.2 4.2 Ⳳ1.1 2.1 Ⳳ.1
173 337.7 Ⳳ19.7 5.5 Ⳳ.6 3.6 Ⳳ.5 2.3 Ⳳ1.2
182 340.0 Ⳳ13.7 6.6 Ⳳ2.1 6.5 Ⳳ3.7 1.7 Ⳳ.6
185 389.3 Ⳳ11.0 5.9 Ⳳ2.4 4.9 Ⳳ1.5 1.4 Ⳳ.6
186 386.3 Ⳳ22.4 6.5 Ⳳ2.5 3.3 Ⳳ.3 1.6 Ⳳ.5
190 342.6 Ⳳ20.7 8.1 Ⳳ2.3 3.8 Ⳳ.8 1.9 Ⳳ1.2
Note: Values are mean ⳲSD for four ants per colony (except only two measures of mandible wear were obtained
for colony 186).
that were discernible (i.e., in focus) along the perimeter
of the most distal antennomere (segment) of the antennae.
The length of the segment to the most distal tip was also
measured (fig. 1A,1C). The number of sensilla was then
corrected for the length of the antennomere.
We used mandible wear as an estimate of worker age
(Smeeton 1982; Acosta et al. 1984; Gibb and Hochuli 2003;
van Wilgenburg et al. 2005; Massey and Hartley 2009).
The mandibles were dissected from the head of each ant,
placed on a slide so that the first incisor pointed upward,
and viewed under the light microscope (as described
above). Several images of the mandibles were taken using
SPOT (ver. 4.7.0) to obtain a full segment length in focus,
and Image-Pro Plus (ver. 6.3) was used to overlay the
images and invert the final image. We recorded the per-
pendicular distances of the first incisor and the total length
of the mandible from the outer edge of the first incisor
to the outer edge of the last incisor (fig. 1B,1D). Mandible
wear was calculated as the inverse of the ratio of incisor
length to mandible length (following Acosta et al. 1984;
van Wilgenburg et al. 2005).
Morphological measures of both antennae and man-
dibles were made blind to the individual’s aggression score
(see van Wilgenburg and Elgar 2013).
Statistical Procedures
The mean number of sensilla per antennal segment, the
mean mandible wear, and the mean aggression index score
were calculated for each colony. Residual scores were ob-
tained for each individual within a colony by subtracting
its raw score from the mean score for their respective
colony. We used regression analysis with JMP (ver. 7; SAS
Institute) to explore the impact of both residual antennal
and mandible wear on residual aggression index.
Results
In general, the ants behaved aggressively toward eachother,
with a mean aggression index across all trials of 1.9
( , ), although the entire range of be-SD p0.86 np48
haviors was observed. There was variation in both the
number of sensilla per micrometer of antennae and the
degree of mandible wear. The number of sensilla per mi-
crometer of antennae ranged from 3.1 to 14.9 (mean p
, , ), while the mandible wear index7.1 S D p2.6 np48
ranged from 2.9 to 12.0 ( , ,mean p4.3 SD p1.8 np
). There was significant variation between colonies in46
the number of sensilla per micrometer of antennae but
not in the level of aggression or mandible wear (table 1).
The capacity of workers to respond aggressively to non-
nestmates was significantly affected by the condition of
their signal receptor organ. The condition of the antennae
of workers varied (fig. 1A,1B), and workers whose an-
tennae had relatively fewer sensilla reacted less aggressively
to nonnestmates than did workers whose antennae had
relatively more sensilla (fig. 2A). This crucial behavioral
response does not appear to be age specific because the
level of aggressive behavior was not correlated with man-
dible wear (fig. 2B).
The data underlying table 1 and figure 2 are deposited
in the Dryad Digital Repository: http://dx.doi.org/10.5061
/dryad.7c9q7 (Gill et al. 2013).
Discussion
Our results highlight the largely unappreciated significance
of receptor organ condition for animal communication:
the level of aggression that ants direct toward nonnestmate
workers depended upon the condition of their antennae,
and ants with relatively fewer sensilla on their antennae
reacted less aggressively to nonnestmate enemies than did
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Antennal Condition and Signal Perception 000
-2
-1
0
1
2
-5-3-1135
-2.5
-1.5
-0.5
0.5
1.5
2.5
-3-115
Residual aggression
Residual aggression
Residual number of sensilla
Residual mandible wear
3
A
B
Figure 2: Residual level of aggression toward nonnestmates is pos-
itively correlated with the residual number of sensilla per micrometer
of antennae (A; , , ) but not with the
2
rp0.137 Fp7.298 P!0.01
1, 47
residual condition of the mandible (B;,).Fp0.877 P10.3
1, 45
those with more sensilla. The sources of variation in sen-
silla density may be due to intrinsic natural variation, ac-
cumulated damage through age, or damage that may de-
rive from engagement in a major conflict independent of
worker age.
It is perhaps surprising that the correlation between
antennal condition and functional behavior in Oecophylla
smaragdina is not influenced by our estimate of worker
age. Neurophysiological studies have reported age-related
changes in sensitivity to chemical social signals or envi-
ronmental cues (Seabrook et al. 1979; Blaney et al. 1986;
Vetter and Visscher 1997), although these studies com-
pared the response of very recently eclosed adults with
those that are a few days older. Older workers might be
expected to have antennae in poorer condition, simply
through ongoing wear and tear. Nevertheless, while it is
possible that our estimate of worker age is unreliable, any
potential influence of age is unlikely to be straightforward.
In theory, older workers might be more likely to engage
in defensive activities and react more aggressively to en-
emies because they are less valuable to the colony (van
Wilgenburg et al. 2005; see also Ho¨lldobler 1983). To be
effective in defense, these older workers should also have
superior sensory capabilities, enabling them to distinguish
accurately between nestmates and other enemies. How-
ever, such superior sensory capabilities may be more likely
found in younger workers, whose receptor organs have
had less exposure to the environment and thus may be in
better condition. If maintaining colony integrity is at a
premium, workers with antennae in good condition
should preferentially engage in nest defense, irrespective
of their age.
It seems likely that the pattern we observed would be
much stronger had we been able to identify and count
individual types of sensilla (e.g., using scanning electron
micrographs). Our present sample would have mostly in-
cluded the long and wispy sensilla trichoidea curvata, to-
gether with the shorter sensilla basiconica (see Babu et al.
2011). In the hymenoptera, both of these sensilla are sen-
sitive to olfactory cues, including pheromones (Hashimoto
1990). Both types of sensilla are especially numerous at
the distal end of the antennae in O. smaragdina (Babu et
al. 2011), with the numbers of each being broadly posi-
tively correlated across antenomeres 8–11 (Babu et al.
2011). Intriguingly, the number and density of olfactory
pore plate sensilla increases with body size in bumblebees,
and larger bumblebee workers respond correctly to much
lower odor concentrations than do small workers (Spaethe
et al. 2007).
Our results could have broader implications for animal
signaling. Animal communication reflects coevolutionary
processes involving both the signaler and the receiver, yet
theoretical and empirical studies rarely take into account
variation in the sensitivity or capacity of individuals to
detect signals (Johnstone 1994; Broom and Ruxton 2011).
This variation may derive from the quality of the receptor
organ, reflected in the number and density of intact sensilla
that may be due to either natural variation or environ-
mentally induced wear and tear. For example, variation in
receiver sensitivity arising from exposure to the environ-
ment might partly explain the maintenance of variation
in secondary sexual signals under intense sexual selection.
Some individuals may simply incorrectly judge a signal as
optimal and thus choose a mate of poorer quality. Ad-
ditionally, selection is thought to favor multiple signaling
across different modalities if it improves the capacity of
the receiver to discern accurate information (Bro-
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000 The American Naturalist
Jørgensen 2010). Perhaps multiple signaling is also more
common in species in which the receptor organs of one
modality are especially prone to damage from the envi-
ronment—in other words, olfactory and other signal mo-
dalities may be favored in species in which the antennae
is likely to be damaged during the life of the adult.
Acknowledgments
We thank the late R. Crozier, S. Robson, E. Schlu¨ens, and
H. Schlu¨ens for their hospitality at James Cook University;
J. Ratcliffe for help with fieldwork; R. Day for statistical
advice; A. Barron, K. P. Rajashekhar, and an anonymous
referee for helpful comments on the manuscript; and the
Australian Research Council (DP0879610) for financial
support.
Literature Cited
Acosta, F. J., J. V. M. Zorilla, and M. A. Cobelas. 1984. Experimental
study of polyethism in ants by noting mandible wear qualitative
part. Graellsia 39:143–155.
Babu, M. J., S. M. Ankolekar, and K. P. Rajashekhar. 2011. Castes of
the weaver ant Oecophylla smaragdina (Fabricius) differ in the
organization of sensilla on their antennae and mouthparts.Current
Science 101:755–764.
Barsagade, D. D., D. B. Tembhare, and S. G. Kadu. 2013. Microscopic
structure of antennal sensilla in the carpenter ant Camponotus
compressus (Fabricius) (Formicidae: Hymenoptera). Asian Myr-
mecology 5:113–120.
Blaney, W. M., L. M. Schoonhoven, and M. S. J. Simmonds. 1986.
Sensitivity variations in insect chemoreceptors; a review. Exper-
ientia 42:13–19.
Botero, C. A., P. Ido, J. Komdeur, and F. J. Weissing. 2010. The
evolution of individual variation in communication strategies.
Evolution 64:3123–3133.
Bovo, R., A. Ciorba, and A. Martini. 2011. Environmental and genetic
factors in age-related hearing impairment. Aging Clinical and Ex-
perimental Research 23:3–10.
Brandstaetter, A. S., A. Endler, and C. J. Kleineidam. 2008. Nestmate
recognition in ants is possible without tactile interaction. Natur-
wissenschaften 95:601–608.
Bro-Jørgensen, J. 2010. Dynamics of multiple signalling systems: an-
imal communication in a world in flux. Trends in Ecology and
Evolution 25:292–300.
Broom, M., and G. D. Ruxton. 2011. Some mistakes go unpunished:
the evolution of “all or nothing” signalling. Evolution 65:2743–
2749.
Crozier, R. H., P. S. Newey, E. A. Schlu¨ens, and S. K. A. Robson.
2010. A masterpiece of evolution—Oecophylla weaver ants (Hy-
menoptera: Formicidae). Myrmecological News 13:57–71.
Crozier, R. H., and P. Pamilo. 1996. Evolution of social insect col-
onies: sex allocation and kin selection. Oxford University Press,
Oxford.
d’Ettorre, P., and A. Lenoir. 2010. Nestmate recognition. Pages 194–
209 in L. Lach, C. L. Parr, and K. L. Abbott, eds. Ant ecology.
Oxford University Press, Oxford.
Dreier, S., J. S. van Zweden, and P. D’Ettorre. 2007. Long-term mem-
ory of individual identity in ant queens. Biology Letters 3:459–
462.
Elgar, M. A., and R. A. Allan. 2006. Colony specific mimicry of the
weaver ant Oecophylla smaragdina by the myrmecophilous salticid
spider Cosmophasis bitaeniata. Journal of Ethology 24:239–246.
Frasnelli, J., O. Collignon, P. Voss, and F. Lepore. 2011. Crossmodal
plasticity in sensory loss. Pages 233–249 in A. M. Green, C. E.
Chapman, J. F. Kalaska, and F. Lepore, eds. Enhancingperformance
for action and perception: multisensory integration, neuroplastic-
ity and neuroprosthetics. Vol. 191. Progress in Brain Research.
Elsevier, Amsterdam.
Gibb, H., and D. F. Hochuli. 2003. Nest relocation in the golden
spiny ant, Polyrhachis ammon: environmental cues and temporal
castes. Insectes Sociaux 50:323–329.
Gill, K. P., E. van Wilgenburg, D. L. Macmillan, and M. A. Elgar.
2013. Data from: Density of antennal sensilla influences efficacy
of communication in a social insect. American Naturalist, Dryad
Digital Repository, http://dx.doi.org/10.5061/dryad.7c9q7.
Gill, K. P., E. van Wilgenburg, P. Taylor, and M. A. Elgar. 2012.
Collective retention and transmission of chemical signals in a social
insect. Naturwissenschaften 99:245–248.
Gordon, D. M., R. E. Paul, and K. Thorpe. 1993. What is thefunction
of encounter patterns in ant colonies? Animal Behaviour 45:1083–
1100.
Hailman, J. P. 2008. Coding and redundancy. Harvard University
Press, Cambridge.
Hashimoto, Y. 1990. Unique features of sensilla on the antennae of
Formicidae (Hymenoptera). Applied Entomology and Zoology 25:
491–501.
Ho¨ lldobler, B. 1983. Territorial behavior in the green tree ant
(Oecophylla smaragdina). Biotropica 15:241–250.
Ichinose, K. 1991. Seasonal variation in nestmate recognition in
Paratrechina flavipes SMITH worker ants (Hymenoptera, Formi-
cidae). Animal Behaviour 41:1–6.
Johansson, B. G., and T. M. Jones. 2007. The role of chemical com-
munication in mate choice. Biological Reviews 82:265–289.
Johnstone, R. A. 1994. Honest signalling, perceptual error and the
evolution of all-or-nothing displays. Proceedings of the Royal So-
ciety B: Biological Sciences 256:169–175.
Katzerke, A., P. Neumann, C. W. W. Pirk, P. Bliss, and R.F. A.Moritz.
2006. Seasonal nestmate recognition in the ant Formica exsecta.
Behavioral Ecology and Sociobiology 61:143–150.
Kleineidam, C., R. Romani, J. Tautz, and N. Isidoro. 2000. Ultra-
structure and physiology of the CO
2
sensitive sensillum ampul-
laceum in the leaf-cutting ant Atta sexdens. Arthropod Structure
and Development 29:43–55.
Kotiaho, J. S. 2001. Costs of sexual traits: a mismatch between the-
oretical considerations and empirical evidence. Biological Reviews
76:365–376.
Limburg, H., and J. E. E. Keunen. 2009. Blindness and low vision
in the Netherlands from 2000 to 2020—modeling as a tool for
focused intervention. Ophthalmic Epidemiology 16:362–369.
Mabelis, A. A. 1979. Nest splitting by the red wood ant Formica
polyctena. Netherlands Journal of Zoology 29:109–126.
Massey, F. P., and S. E. Hartley. 2009. Physical defences wear you
down: progressive and irreversible impacts of silica on insect her-
bivores. Journal of Animal Ecology 78:281–291.
This content downloaded from 128.250.144.144 on Fri, 11 Oct 2013 00:31:20 AM
All use subject to JSTOR Terms and Conditions
Antennal Condition and Signal Perception 000
Maynard Smith, J., and D. G. C. Harper. 2003. Animalsignals. Oxford
University Press, Oxford.
Newey, P. S., S. K. A. Robson, and R. H. Crozier. 2010. Know thine
enemy: why some weaver ants do but others do not. Behavioral
Ecology 21:381–386.
Nowbahari, E., R. Feneron, and M. C. Malherbe. 1999. Effect of body
size on aggression in the ant, Cataglyphis niger (Hymenoptera;
Formicidae). Aggressive Behavior 25:369–379.
Nowbahari, E., and A. Lenoir. 1989. Age-related changes inaggression
in the ant Cataglyphis cursor (Hymenoptera, Formicidae) influence
on intercolonial relationships. Behavioural Processes 18:173–182.
Ozaki, M., A. Wada-Katsumata, K. Fujikawa, M. Iwasaki, F. Yokohari,
Y. Satoji, T. Nisimura, and R. Yamaoka. 2005. Ant nestmate and
non-nestmate discrimination by a chemosensory sensillum. Sci-
ence 309:311–314.
Renthal, R., D. Velasqueza, D. Olmosa, J. Hamptona, and W. P.
Sergin. 2003. Structure and distribution of antennal sensilla of the
red imported fire ant. Micron 34:405–413.
Roth, G. S., J. A. Mattison, M. A. Ottinger, M. E. Chachich, M. A.
Lane, and D. K. Ingram. 2004. Aging in rhesus monkeys: relevance
to human health interventions. Science 305:1423–1426.
Roulston, T. H., G. Buczkowski, and J. Silverman. 2003. Nestmate
discrimination in ants: effect of bioassay on aggressive behavior.
Insectes Sociaux 50:151–159.
Schlu¨ ens, E. A., B. J. Wegener, H. Schlu¨ens, N. Azuma, S. K. A.
Robson, and R. H. Crozier. 2009. Breeding system, colony and
population structure in the weaver ant Oecophylla smaragdina.
Molecular Ecology 18:156–167.
Seabrook, W. D., K. Hirai, H. H. Shorey, and L. K. Gaston. 1979.
Maturation and senescence of an insect chemosensory response.
Journal of Chemical Ecology 5:587–594.
Searcy, W. A., and S. Nowicki. 2005. Evolution of animal commu-
nication: reliability and deception in signalling systems. Princeton
University Press, Princeton, NJ.
Smeeton, L. 1982. The effect of age on the production of reproductive
eggs by workers of Myrmica rubra L (Hym. Formicidae). Insectes
Sociaux 29:465–474.
Sorrells, T. R., L. Y. Kuritzky, P. G. Kauhanen, K. Fitzgerald, S. J.
Sturgis, J. Chen, C. A. Dijamco, K. N. Basurto, and D. M. Gordon.
2011. Chemical defense by the native winter ant (Prenolepis
imparis) against the invasive Argentine ant (Linepithema humile).
PLoS ONE 6:e18717.
Spaethe, J., A. Brockmann, C. Halbig, and J. Tautz. 2007. Size de-
termines antennal sensitivity and behavioural threshold to odors
in bumblebee workers. Naturwissenschaften 94:733–739.
Stevens, M., and G. D. Ruxton. 2012. Linking the evolution andform
of warning coloration in nature. Proceedings of the Royal Society
B: Biological Sciences 279:417–426.
Sturgis, S. J., and D. M. Gordon. 2012. Nestmate recognition in ants
(Hymenoptera: Formicidae): a review. Myrmecological News 16:
101–110.
Sza´ mado´ , S. 2011. The cost of honesty and thefallacy of the handicap
principle. Animal Behaviour 81:3–10.
Thomas, M. L., L. J. Parry, R. A. Allan, and M. A. Elgar. 1999. Colony
recognition in Australian meat ants Iridomyrmex purpureus.
Naturwissenchaften 86:87–92.
van Wilgenburg, E., and M. A. Elgar. 2013. Confirmation bias in
studies of nestmate recognition: a cautionary note for research
into the behaviour of animals. PLoS ONE 8:e53548.
van Wilgenburg, E., M. R. E. Symonds, and M. A. Elgar. 2011. Evo-
lution of cuticular hydrocarbon diversity in ants. Journal of Evo-
lutionary Biology 24:1188–1198.
van Wilgenburg, E., E. van Lieshout, and M. A. Elgar. 2005. Conflict
strategies in the meat ant (Iridomyrmex purpureus): ritualised dis-
plays versus lethal fighting. Behaviour 142:701–716.
Vetter, R. S., and P. K. Visscher. 1997. Influence of age on antennal
response of male honey bees, Apis mellifera, to queen mandibular
pheromone and alarm pheromone component. Journal of Chem-
ical Ecology 23:1867–1880.
Wenseleers, T., J. Billen, and A. Hefetz. 2002. Territorial marking in
the desert ant Cataglyphis niger: does it pay to play bourgeois?
Journal of Insect Behavior 15:85–93.
Whitehouse, M. E. A., and K. Jaffe. 1995. Nestmate recognition in
the leaf-cutting ant Atta laevigata. Insectes Sociaux 42:157–166.
Wyatt, T. D. 2003. Pheromones and animal behaviour: communi-
cation by smell and taste. Cambridge University Press, Cambridge.
Natural History Editor: Mark A. McPeek
This content downloaded from 128.250.144.144 on Fri, 11 Oct 2013 00:31:20 AM
All use subject to JSTOR Terms and Conditions
