BEHAVIOURAL
-IN
CASTES AND THEIR CORRELATES
THE PRIMITIVELY
MARGINATA
(LEP.)
K. Chandrashekara
EUSOCIAL
WASP, ROPALIDIA
(HYMENOPTERA:
VESPIDAE)
and Raghavendra Gadagkar
Centre for Ecological Sciences
Indian Institute of Science,
Bangalore 560 012, India
INTRODUCTION
Insects living in groups comprising of individuals from more than one
generation,
most of whom give up reproduction in favour of one or a few
members of their group, but cooperate in rearing the resulting brood are
termed eusocial (Michener,
1969; Wilson, 1911). In the highly eusocial
insects such as all termites, most ants and .some bees and wasps the
non-reproductives
are morphologically
distinct castes who have little or no
reproductive opportunities. Such morphological differences often extend to
subcastes among workers as well. This leads to efficient division of labour
and a stable social organisation.
Such morphologically
distinct castes are
however absent in most primitively eusocial bees and wasps. Here adult
wasps or bees are considered totipotent because the social roles, including
that of the egg layer, that members of a colony can undertake are flexible.
In the absence of morphological
castes why do certain individuals accept
the role of workers
and how are the division
of labour and social
organisation achieved?
Pardi (1948) suggested
that social interactions
involving dominance
behaviour results in the most dorr11nant -female becoming the queen who
monopolises egg laying while the subordinates
accept worker roles. This
pattern seems to hold for most species of primitively eusoci'al wasps studied
since (West-Eberhard,
1969; Jeanne, 1972). A recent study by Gadagkar
and Joshi (1982, 1983) focussed on inter-individual
behavioural variability
among colony members of the primitively eusocial tropical wasp Ropalidia
marginata.
Constructing
time-activity
budgets for commonly
occurring
behaviours and using principal components analysis they identified three
behavioural castes viz., Sitters. Fighters and Foragers.
How is social organisation
and division
of labour achieved
by
behavioural
caste differentiation?
What is the pattern of task allocation
among members of these castes? Is there any task specialization
among
members of the three castes? Th~sEt are some of the questions we have
attempted to answer in this paper. We do This by exploring the behavioural,
Social Insects ..An Indian Perspective (eds.) G.K Veeresh, A.A. V. Kumar and
T. Shivashankar,
Published by IUSSI-lndian Chapter, Bangalore (1990).
153
-"
morphological
and anatomical correlates of the behavioural castes in the
primitively eusocial tropical wasp R. marginat~. Our results show that the
extra-nidal task of foraging is primarily performed by the Foragers while
most of the intra-nidal tasks are shared by Sitters and Fighters. Sitters and
Fighters have better developed ovaries and hence may be treated as
potential queens. We failed to discover any morphological correlates of the
behavioural castes, reinforcing the idea of relative flexibility in social roles
that adult wasps of a colony may adopt.
MATERIALS
AND
METHODS
The results presented here are based on observations conducted on
12 post-emergence
colonies of R. marginata between January 1986 and
May 1987. Seven of these colonies were located In Bangalore (13.00' N
and 77"32' E) and five were in Mysore (12.25' Nand 76.50' E), India.
i
I
1. Sampling
methods
All adult wasps on a nest were marked with unique spots of quick- drying
paint to enable individual identification. Quantitative data on behaviour was
obtained by observing each colony for a period of 20 h over six days. Two
sampling
methods namely, "instantaneous
scans" and "recording
all
occurrences
of rare behaviours " (Altmann, 1974) were used in the study.
Each observation se$sion comprised of 17 "instantaneous
scans" and 24
"all occurrences"
sessions of five min duration and thus amounted to 3 h
and 20 min. Three such observation sessions beginning 0800 h, 1120 h
and 1440 h on three successive days covered the entire period between
0800 hand 1800 h when wasps are most active. The cycle was repeated
once again on the following three days to complete the observations. Data
for each colony was th us based on a total of 102 "instantaneous
scans"
and 144 "all occurrences" sessions. Data on Colony 6 alone was however
based on 51 scans and 72 "all occurrences" since the nest was attacked
by the predatory hornet Vespa tropica and the observations could not be
completed. The results presented in this paper are thus based on"230 h of
observations
on 12 natural colonies. Data from the instantaneous
scans
were used to construct ti~-activity
budgets while those from the all
occurences
sessions were used to compute the frequency per hour at
which a behaviour was performed_by each animal. In all colonies only one
individ ual was ever seen laying eggs and she was designated as the queen.
Data on nest contents and the numbers of males and females present
on the nest was obtained by collecting the nests after completion
of
observations.
All female wasps from each colony thus collected were
measured and dissected under a binocular dissection microscope to obtain
data on body size and ovarian condition. The dissected wasps were oven
dried at 80.C to estimate dry weight and the non-structural
fat content of
each wasp following the method of Folch et al. (1957).
154
2. Variables
used
Twenty variables were used in this study. They are, the proportions of
time spent in five common behaviours,
(1) Sit and Groom, (2) Raise
Antennae, (3) Walk, (4) In cells, (5) Absent from nest, and the frequencies
per hour of 11 rare behaviours,
(6) Dominance behaviour, (7) Subordinate
behaviour, (8) Bring food, (9) Snatch
(12) Bring building material,
(13)
building material, (15) Extend walls
Total number of oocytes, (18) Wing
Non-structural
fat content (mg).
food, (10) Lose food, (11) Feed larva,
Snatch building material,
(14) Lose
of cells, (16) Build new cells; and (17)
length, (19) Dry weight (mg) and (20)
3. Data Analysis
The method of principal components analysis (Frey and Pimentel, 1978)
was used as described by (Gadagkar and Joshi, 1983,1984) to analyse the
Trme-activity budgets constructed from data on proportions of time spent
in five common behaviours. The positions of wasps were plotted as points
in the space of the first two principal components.
These points fell into
three distinct clusters as confirmed by the nearest centroid method (see
Gadagkar and Joshi, 1983, 1984). Principal components
analysis and
identification
of the clu~ters were performed separately for each colony.
Using the method of Logistic regression
analysis each of the 20
variables used in the study was modelled to test its influence on the
probability of an animal being a Sitter, a Fighter or a Forager such that,
In(p1/P3)
= a1 + 131X
In(p2/P3) = a2 + 132X
where P1, P2 and P3 are the probabilities of being a Sitter, a Fighter or
a Forager respectively (p1 + P2 + P3 = 1), a 1 an a2 are intercepts, 131and
132 are regression coefficients
and X is the independent variable. The
regression
equations:
P1 = P3 [exp(a1 + 131X)]
P2 = P3 [exp(a2 + ~2X)]
P3 = 1 -P1 -P2
were solved
criterion:
by an iterative
L =
k
(0
i=1
procedure
m
P1) (0
P2)
i=k+ 1
155
using the maximum
n
(0 P3)
i=m+ 1
likelihood
where L is the likelihood, 1 to k are Sitters, k+ 1 to m are Fighters and
m+1 to n are Foragers (For further details see, Shanubhogue
and Gore,
1987; Gadagkar, et at., submitted; Cox and Snell, 1989). This analysis was
carried out by pooling all the data from 12 colonies.
RESULTS
Time-activity budgets constructed for all individually identified animals
from 12 colonies of the tropical wasp R. marginata revealed that female
wasps spend 69% .100% (mean :t S.D. = 94.61 :t 5.23) of their time in the
five common behaviours,
Sit and Groom, Raise Antennae, Walk, In Cells
and Ab.sent from Nest (Variables 1-5 in the list of variables ). The manner
in which each wasp allocated her time between these five behaviours was
however highly variable (data not shown). In order to discern a pattern in
differential allocation of time by individuals in the five common behaviours
we subjected the time-activity
budgets of wasps from each colony to
principal components analysis. Our results show that the first two principal
components together account for 97.9% -99.7% of the variance in the input
data. In colony 1, which we use in this paper to illustrate the results of
principal
components
analysis,
the first two principal
components
accounted for 99.5% of the variance in the input data (Table 1). The position
of each wasp is therefore plotted as amplitudes in the space of the first two
principal components
(Figure 1) and the points resolve into three distinct
clusters. The boundaries of the three clusters were always confirmed by
the nearest centroid criterion, so that each point was closer to its own
centroid than to the centroid of any other cluster (Gadagkar and Joshi,
1983). The results were identical for all the 12 colonies with the wasps
falling into three distinct clusters.
Results
Table 1.
of Principal components
-PC:t
Sit and Groom
analysis
PC II
-0.6985
0.5024
Raise Antennae
0.0406
-0.6741
Walk
Q.0293
-0.1337
In Cells
-0.0114
Absent from nest
0.7138
Eigen value
0.1457
Variance
96.67
Cum. Variance
-0.0201
-0.5242
0.0042
2.77
99.44
156
Following Gadagkar and Joshi (1983) we constructed mean behavioural
profiles for animals in each cluster. The cluster with the highest mean
proportion of time spent in Sit and Groom was labelled Sitters, the cluster
with the highest mean proportion of time spent in Raise antennae or the
highest frequency
of Dominance behaviour was labelled Fighters and
similarly the cluster with the highest mean propor1ion of time spent in Absent
from nest was labelled Foragers.
:: 0.6
z
L4J
z
~0.4
~ ~~:7
0
~
~,~
~
0 0
~ 0.2
L;)
51
Fa
FI
z
it:
0.. 0
-0.8
-0.4
0
PRINCIPAL
0.4
COMPONENT I
Fig. 1. Behavioural castes of female wasps in colony 1 as identified by principal
components analysis. Each open circle denotes a wasp, plotted as a point in the
coordinate space of the first two principal components. The centroids of each cluster
are indicated by closed circles. The cluster of Sitters, Fighters and Foragers are
indicated by letters 51, FI and Fa respectively.
By what other attributes can we characterize
Sitters, Fighters and
Foragers? In other words, are they different from each other, and if so, can
we distinguish between them with respect to other variables used in the
study? We use the method of logistic regression analysis to show patterns
of task allocation among the three behavioural castes.
Making pairwise comparisons
between castes for each variable we
found that Foragers brought food significantly more often than either Sitters
or Fighters (p < 0.05) and Fighters did so significantly
more often than
Sitters (p < 0.05, Table 2). Fighters showed significantly higher frequencies
of Dominance behaviour than either Sitters or Foragers (p < 0.05) and
Sitte's did so significantly
more often than Foragers (p< 0.05, Table 2).
Sitters and Fighters showed significantly higher frequencies of Snatch food,
Feed larva and Extend walls of cells than Foragers (p < 0.05, Table 2).
These three variables however did not permit us to distinguish between
Sitters and Fighters.
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Sitters and Fighters had the most well developed ovaries in comparison
to Foragers (p < 0.05). Other variables nam~ly, Wing length, Dry weight
and Fat content did not differ significantly between castes.
DISCUSSION
In the absence of morphologically distinct castes how is division of
labour achieved in primitively eusocial insects? In an attempt to answer this
question Gadagkar and Joshi (1983) constructed time-activity budgets ot
wasps and an~lysed them using multivariate statistical techniques such as
principal components analysis and cluster analysis and established the
presence of three behavioural castes. Using the data on other behaviours
such as -Bring food, Dominance behaviour and Egg laying, they named
these clusters as Sitters, Fighters and Foragers. Since the colonies of R.
marginata are perennial they argued that some individuals from among
either Sitters or Fighters could become queens in future and that Foragers
had very little chance of becoming queens. Our results are based on a
larger data set and confirm these basic findings.
The main objective of thjs study was to identify correlates of the
behavioural castes and thereby understand how division of labour and
socia! organisation are achieved in R. marginata. The results clearly
suggest that division of labour and social organisation are built around
behavioural caste differentiation. The risky task of foraging is performed by
Foragers who also have the most poorly developed ovaries. Such
individuals with poorly developed ovaries are out of reckoning to become
queens in future. On the other hand Sitters and Fighters both share the
intra-nidal tasks such as feeding larvae and nest building. In additton the
Fighters seem to perform an important role of keeping the colony members
active and working by being aggressive towards other members of a colony.
It is in fact quite common to see long periods of inactivity being broken by
some individuals showing dominance towards others who left the nest and
quite often were seen to return with food (unpublished observations).
Queen supercedure which is common in colonies of R. marginata'
provides opportunities for other individuals to become queens. The
individuals most likely to become queens in future are among the Sitters
and Fighters since both have equally developed ovaries. Such potential
queens however are not morphologically different from the rest. The lack
of any morphological difference among queens and workers in primitively
eusocial species leaves room for flexibility in social roles that the individuals
can undertake. The lack of any morphological differences among the
behavioural castes adds to this flexibility.
159
i
SUMMARY
In the absence of a morphologically
distinct worker caste, the primitively
eusocial wasps achieve division of labour by differential allocation of their
time into various activities. Analysis of time-activity budgets using principal
components analysis permitted us to classify all female wasps in a colony
of Ropalidia marginata
into three behavioural
castes namely, Sitters,
Fighters and Foragers. The method of logistic regression analysis was used
to explore behavioural,
morphological
and anatomical correlates of these
castes. Results of preliminary analysis show that Foragers perform most
of the risky task of foraging and have the most poorly developed ovaries.
Both Sitters and Fighters perform most of the intra-nidal tasks but the
Fighters show most of the dominance
behaviour.
Queens are almost
always among the Sitters. Both Sitters and Fighters have well developed
ovaries and may be treated as hopeful queens. Indices of body size such
as wing length and dry weight are not correlated with the behavioural caste
of an animal.
ACKNOWLEDGEMENTS
We thank A. Shanubhouge
and A.P. Gore for the computer
used to perform logistic regression analysis.
program
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