Behavioral Ecology Vol. 11 No. 3: 315-318
© 2000 International Society for Behavioral Ecology
Queen transport during ant colony emigration: a group-level adaptive behavior
Centre for Mathematical Biology and Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
Address correspondence to A. B. Sendova-Franks, Faculty of Computer Studies and Mathematics, University of the West of England, Frenchay Campus, Coldharbour Lane, Bristol BS116 1QY, UK. E-mail: ana.sendova-franks{at}uwe.ac.uk .
Received 24 July 1999; revised 30 September 1999; accepted 1 October 1999.
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ABSTRACT |
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Ant colonies emigrate frequently from one nest site to another. Emigrations, however, are dangerous, particularly for colonies with a single queen. The queen is a "vital organ" of the colony, and emigrations expose her to grave peril. The optimal strategy for a monogynous ant colony, therefore, should be that the queen moves during the middle of the emigration so that she is transferred swiftly from the protection of half of the colony in the old nest to the protection of the other half colony in the new nest. In the ant Leptothorax albipennis, the queen is carried during colony emigration. We tested the null hypothesis that the queen has a random position in the sequence of transport events during an emigration. The result of 32 emigrations demonstrated, for the first time, that the transport serial number of the queen [calculated relative to the total number of all transport events (i.e., of brood and adult ants together), brood transport events, or adult ant transport events] is not random and furthermore occurs in the middle of the transport sequence. This result represents a colony strategy because we found that the relative transport serial number of the queen was related neither to emigration distance nor to colony size. Transporting queens in the middle of emigrations is a strategy probably favored by selection and is an aspect of colonies behaving as group-level adaptive units.
Key words: ants, colony emigration, group-level adaptive unit, Leptothorax, queen, risk minimization.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Ant colonies emigrate much more frequently than previously assumed (Hölldobler and Wilson, 1990
; Partridge et
al., 1997). During emigrations the queen is exposed to danger. She
is vulnerable to predation or might become lost. Therefore, the stage at which
the queen should be moved during an emigration is an essential strategic issue
for the colony. This important issue of risk minimization during emigration
has received little attention.
In certain species, dense groups of workers, called queen retinues, guard
the mother queen as she moves from one nest to another
(Hölldobler
and Wilson, 1990). In extreme cases, particularly in large,
monogynous colonies, such as in weaver ants (Oecophylla), the entire
body of the queen is covered by a seething shell of guards
(Hölldobler
and Wilson, 1983). In ecitonine army ants, the retinue extends 1 m
in front of the queen and 2 m behind her and contains up to five times the
number of workers found in an ordinary 3-m section of the column of emigrating
ants (Rettenmeyer et al.,
1978). The formation of such retinues suggests that the queen is
protected as a uniquely important member of the colony.
In many species, including our study species Leptothorax
albipennis, the queen is carried to the new nest by a worker rather than
walking unaided (Abraham and Pasteels,
1980;
Möglich,
1978;
Möglich and
Hölldobler, 1974). Such queen
transport is often part of adult transport, which occurs in addition to brood
transport, during colony emigration in the majority of ant species,
particularly those belonging to the two largest subfamilies, the Myrmicinae
and the Formicinae
(Hölldobler
and Wilson, 1990).
Stereotyped techniques of communication and recruitment during emigration
by Leptothorax and other genera have been extensively documented
(e.g.,
Möglich,
1978;
Möglich and
Hölldobler, 1975), and task
allocation during this emergency has also been investigated (e.g.,
Abraham and Pasteels, 1980;
Möglich and
Hölldobler, 1974;
Sendova-Franks and Franks,
1995b). This study, however, is the first detailed analysis of the
relative timing of queen movement during emigration.
In monogynous ants, the queen is a "vital organ" of the
society, and her movement during an emigration is likely to occur when the old
nest is no longer suitable for the colony and the new nest is incomplete and
not fully fortified. Therefore, we hypothesized that the queen should move
during the middle of the emigration so that she moves swiftly between the
protection afforded by half of the colony in the old nest site and half of the
colony in the new nest site. Numbers of workers are likely to be of great
importance for ants in defensive situations
(Franks and Partridge,
1993).
We tested the null hypothesis that the queen has a random position in the
sequence of transport events during an emigration, and, alternatively, if her
position is not random, that it is not in the middle of the emigration
sequence. To test these hypotheses we studied 32 emigrations of colonies of
the ant L. albipennis at four different emigration distances under
controlled conditions in the laboratory. In statistics, the term "serial
number" is used to specify the position of a particular event in a
sequence (Cox and Lewis, 1968).
Henceforth, we refer to the position of the queen in the sequence of transport
events as the queen's transport serial number.
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METHODS |
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The experiments were carried out on eight colonies of the ant Leptothorax albipennis (Curtis) collected from rock crevices in Dorset, England. The colonies were housed in nests made from a pair of microscope slides separated by a thin cardboard perimeter (the details of the method used to culture colonies under laboratory conditions followed Sendova-Franks and Franks, 1995c
). Such nests mimic the natural geometry of nests in the
field. The number of adult workers in the colonies varied from 37 to 103 and
the number of brood items from 66 to 127.
Each of the eight colonies emigrated 4 times, giving a total of 32
emigrations. We provoked emigrations simply by removing the roof of the
current nest site in the presence of another complete nest site nearby which
the ants could colonize (Sendova-Franks
and Franks, 1995b). The four emigrations of each colony took four
consecutive 48-h periods beginning with the opening of the old nest. The 16
emigrations of colonies 1-4 were carried out from 3 June to 14 July 1996. The
remaining 16 emigrations of colonies 5-8 were carried out from 26 May to 28
June 1997. The emigration distance (the distance between the old nest and the
new nest) was varied in colonies 1-4. Each of the four colonies was emigrated
at each of the following four emigration distances: 6 cm, 12 cm, 24 cm, and 48
cm. The experiment followed a Latin-square design
(Sokal and Rohlf, 1995). The
emigration distances were permutated so that any possible effects of
emigration distance, sequential number of consecutive emigration, and colony
identity were dissociated. We chose the permutations at random: for colony 1,
out of the 24 possible; for colony 2, out of the remaining 9 permutations that
did not contain any of the 4 distances in the same position they were in the
permutation already chosen for colony 1; for colony 3, out of the remaining 2
permutations satisfying the condition of nonrepeatability of position; for
colony 4, the single remaining permutation. In colonies 5-8 the emigration
distance was kept constant at 6 cm.
We recorded the transport of brood, workers, and the queen to the new nest on videotape. The time of arrival at the new nest, transport serial number, and identity of each transported item were extracted from the video for each of the 32 emigrations. The total number of transported items thus analyzed was 4537.
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RESULTS |
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Our objective was to test the null hypothesis that the queen's transport serial number occurs at random within the complete set of possible transport serial numbers. Furthermore, we wanted to test this hypothesis separately for brood transport and adult ant transport in case there was a tendency for either brood or adult ants to be transported first. To this end, we established the serial number of the queen in the sequence of (1) all transport events (i.e., of brood and adult ants together); (2) brood transport events; and (3) adult ant transport events and in each case calculated the queen's transport serial number relative to the total number of events.
According to the null hypothesis, the frequency distribution of the queen's serial number as a proportion of total number for each of (1) all transport events, (2) brood transport events, or (3) adult ant transport events should not be significantly different from a uniform distribution. The reason for this is that under the null hypothesis the queen's transport serial number occurs at random within the complete set of possible transport serial numbers. For example, in a series of 150 transport events the queen will be equally likely to occupy any of the positions 1-150. The distribution of the serial numbers 1-150 (as well as the distribution of these serial numbers, calculated relative to the total number of transport events, 150) follows a uniform distribution. Therefore, under the null hypothesis, a representative sample of the queen's serial number during transport over many emigrations should also follow a uniform distribution.
The null hypothesis that the transport serial number of the queen is random
was rejected in each of the three cases by a Chi-square test. The frequency
distribution of the queen's serial number relative to the total number for
each of: all transport events (Figure
1a), brood transport events
(Figure 1b), or adult ant
transport events (Figure 1c)
was significantly different from a uniform distribution. When the distribution
values were classified into five categories, the numbers of entries in these
categories were significantly different in each of the three cases
(Table 1). Not only did the
queen's transport serial number not occur at random within the complete set of
possible transport serial numbers, but it tended to be in the middle of the
transport sequence. Thus, the category with the highest contribution to the
final Chi-square value was the middle (third) category, containing values from
0.4 to 0.6 (cases 1 and 2, Table
1) or the second category, containing values from 0.2 to 0.4 (case
3, Table 1). There was no
significant difference among the three cases (heterogeneity test for cases
1-3, 
2 = 5.591, df = 8). This result is not simply an artifact
of particular experimental conditions but represents a robust colony-level
strategy. We found that the queen's transport serial number was related
neither to emigration distance (Table
2) nor to colony size (Table
3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We have demonstrated for the first time for any social insect that the queen's serial number in the series of transport events during colony emigration is not only nonrandom but occurs in the middle of the transport sequence. Moreover, it is related neither to emigration distance nor to colony size. These results are consistent with the hypothesis that the optimal strategy for a monogynous ant colony is to minimize the danger for the queen by providing her with the protection of the majority of colony members at any one time.
In an established nest, the queen occupies a central spatial position in
the radially symmetrical structure of the colony population
(Sendova-Franks and Franks,
1995a). After the initial crisis following the destruction of
their current nest site, the majority of colony members also settle down into
a radially symmetrical structure with the queen in the center (Franks and
Sendova-Franks, personal observations). This spatial organization protects the
queen because of the sheer numbers of workers and brood placed between her and
any potential enemy. The odds of her being predated should be much reduced by
this strategy.
Moving the queen too early to the new nest during colony emigration
endangers her both in terms of the possibility of her becoming lost (the
choice of new nest might not yet be final because different scouts might
choose different nest sites before a single one is eventually selected) and in
terms of leaving her with the minority of colony members. Moving the queen too
late endangers her by the increased chance of predation both due to the length
of exposure and again in terms of leaving her with the minority of colony
members. When an old nest breaks up, L. albipennis ants are
vulnerable to predation by larger ants such as Lasius niger and
various Myrmica species (Franks and Sendova-Franks, personal
observations). Even though L. albipennis workers may not actively
defend colony members against these species, by surrounding the queen with a
large number of either brood or workers, the colony should minimize the risk
that this unique individual would be predated
(Franks and Partridge, 1993,
Hamilton, 1971). The mechanism
underlying the decision-making process that determines when during the
emigration the queen should be moved is not yet understood but it is under
investigation.
The occurrence of queen transport in the middle of these emigrations is a
colony-level phenomenon. It is, therefore, a new example of social insect
colonies acting as group-level adaptive units
(Bourke and Franks, 1995;
Seeley, 1997).
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ACKNOWLEDGEMENTS |
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We are very grateful to Sarah Backen, Liz Langridge, Eamonn Mallon, Stephen Pratt, and Andrew Spencer for their comments on an earlier version of this paper. We acknowledge the Leverhulme Trust for their support.
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REFERENCES |
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Sendova-Franks AB, Franks NR, 1995c. Spatial relationships within nests of the ant Leptothorax unifasciatus (Latr.). and their implications for the division of labour. Anim Behav 50: 121-136.
Sendova-Franks AB, Franks NR, 1995a. Demonstrating new social interactions in ant colonies through randomization tests: separating seeing from believing. Anim Behav 50: 1683-1696.
Siegel S, Castellan NJ, 1988. Nonparametric statistics for the behavioral sciences, 2nd ed. London: McGraw-Hill.
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