3055
INTRODUCTION
Although nestmate recognition in social insects has been widely
studied, previous work has used a variety of methodologies and
social contexts. Bioassays to quantify the differential treatment of
nestmates versus non-nestmates range from presenting natural
guards at colony entrances with incoming foragers to observing
isolated non-guard individuals in containers and presenting them
with individuals who have been isolated from a colony since
eclosion. The use of these highly artificial contexts has the advantage
of affording greater control of the experimental conditions, and such
studies have generated significant advances in our understanding
of group-level behavioural discrimination (Breed, 1983; Getz and
Smith, 1983; Breed et al., 1988; Buchwald and Breed, 2005).
However, this may be at the expense of relevance to the actual
challenges faced by discriminators in nestmate recognition.
The theory of optimal acceptance thresholds predicts that a
discriminator will behave more or less permissively depending upon
the context, by trading off one error (reject nestmate) for the other
(accept non-nestmate) to minimize the total cost of all errors (Reeve,
1989; Couvillon et al., 2009; Jones et al., 2012). One such context
that affects recognition behaviour is the perceived threat: for example,
when honey bees face increased levels of conspecific robbing, the
guards’ threshold becomes less permissive, resulting in a lower
proportion of both non-nestmates and nestmates being accepted
(Downs and Ratnieks, 2000; Couvillon et al., 2008). Another context
is perceived proximity of the colony; paper wasps’ aggression varies
depending on the presence of a nestmate or a familiar nest fragment
(Starks et al., 1998). However, in spite of these data, many previous
studies that quantify recognition behaviour do not account for context.
Additionally, results obtained in different contexts are often compared
across studies (Johnson et al., 2011). If context is not considered,
such comparisons are rendered meaningless.
In this study we carried out bioassays on nestmate recognition
by guards in two species of eusocial bees, the honey bee Apis
mellifera Linnaeus 1758 and the stingless bee Tetragonisca
angustula (Latreille 1825). We systematically varied the naturalness
of the context from fully natural (guards at nest entrances) through
different degrees of unnatural (single versus two guards in a
container, with and without colony odour). If there is no effect of
context on guarding recognition behaviour (accept/reject an
introduced bee), we would expect guards to make similar recognition
errors under all treatments. Alternatively, if context does play a role,
then we would expect guards to make different recognition errors
between contexts. Specifically, we predicted that the lowest total
recognition errors would be at the natural nest entrance, with the
other contexts varying in their degree of error.
SUMMARY
Nestmate recognition studies, where a discriminator first recognises and then behaviourally discriminates (accepts/rejects)
another individual, have used a variety of methodologies and contexts. This is potentially problematic because recognition errors
in discrimination behaviour are predicted to be context-dependent. Here we compare the recognition decisions (accept/reject) of
discriminators in two eusocial bees, Apis mellifera and Tetragonisca angustula, under different contexts. These contexts include
natural guards at the hive entrance (control); natural guards held in plastic test arenas away from the hive entrance that vary
either in the presence or absence of colony odour or the presence or absence of an additional nestmate discriminator; and, for
the honey bee, the inside of the nest. For both honey bee and stingless bee guards, total recognition errors of behavioural
discrimination made by guards (% nestmates rejected + % non-nestmates accepted) are much lower at the colony entrance
(honey bee: 30.9%; stingless bee: 33.3%) than in the test arenas (honey bee: 60–86%; stingless bee: 61–81%; P<0.001 for both).
Within the test arenas, the presence of colony odour specifically reduced the total recognition errors in honey bees, although this
reduction still fell short of bringing error levels down to what was found at the colony entrance. Lastly, in honey bees, the data
show that the in-nest collective behavioural discrimination by ca. 30 workers that contact an intruder is insufficient to achieve
error-free recognition and is not as effective as the discrimination by guards at the entrance. Overall, these data demonstrate that
context is a significant factor in a discriminators’ ability to make appropriate recognition decisions, and should be considered
when designing recognition study methodologies.
Key words: Apis mellifera, Tetragonisca angustula, acceptance threshold, eusocial bee, social insects.
Received 13 January 2013; Accepted 14 April 2013
The Journal of Experimental Biology 216, 3055-3061
© 2013. Published by The Company of Biologists Ltd
doi:10.1242/jeb.085324
RESEARCH ARTICLE
Context affects nestmate recognition errors in honey bees and stingless bees
Margaret J. Couvillon
1,
*, Francisca H. I. D. Segers
1,2,3
, Roseanne Cooper-Bowman
1
, Gemma Truslove
1
,
Daniela L. Nascimento
2
, Fabio S. Nascimento
2
and Francis L. W. Ratnieks
1
1
Laboratory of Apiculture and Social Insects, School of Life Sciences, University of Sussex, Falmer, Brighton, BN1 9QG, UK,
2
Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo,
CEP 14040-901, Ribeirão Preto, SP, Brazil and
3
Laboratoire d’Ethologie Expérimentale et Comparée, EA4443, Université Paris 13,
Sorbonne Paris Cité, 99 Avenue J. B. Clément, 93430 Villetaneuse, France
*Author for correspondence (M.Couvillon@Sussex.ac.uk)
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