Interrogating an insect society

Abstract

Insect societies such as those of ants, bees, and wasps consist of 1 or a small number of fertile queens and a large number of sterile or nearly sterile workers. While the queens engage in laying eggs, workers perform all other tasks such as nest building, acquisition and processing of food, and brood care. How do such societies function in a coordinated and efficient manner? What are the rules that individuals follow? How are these rules made and enforced? These questions are of obvious interest to us as fellow social animals but how do we interrogate an insect society and seek answers to these questions? In this article I will describe my research that was designed to seek answers from an insect society to a series of questions of obvious interest to us. I have chosen the Indian paper wasp Ropalidia marginata for this purpose, a species that is abundantly distributed in peninsular India and serves as an excellent model system. An important feature of this species is that queens and workers are morphologically identical and physiologically nearly so. How then does an individual become a queen? How does the queen suppress worker reproduction? How does the queen regulate the nonreproductive activities of the workers? What is the function of aggression shown by different individuals? How and when is the queen's heir decided? I will show how such questions can indeed be investigated and will emphasize the need for a whole range of different techniques of observation and experimentation.

Fig. 1.

A typical nest of the Indian paper wasp, R. marginata (Photo: Sujata Kardile).

Fig. 2.

Behavioral castes of R. marginata. Twenty wasps are shown as points in the coordinate space of the amplitudes associated with the first 2 principal components. The points fall into 3 clusters (or castes) by the criterion of nearest centroid. Dots indicate centroids. Q = queen. [Redrawn with permission from ref. (Copyright 1983, Elsevier).]

Fig. 3.

A typical queen removal experiment showing the frequencies per hour of dominance behavior shown by the queen (blue bars), PQ (pink bars), maximum workers (green bars), and mean worker (yellow bars) on days 1–3. Bars that carry different letters are significantly different from each other (P < 0.05 or less) within each day, bars that carry different numbers are significantly different from each other (P < 0.05 or less) among the 3 days. Comparisons are by the 2-tailed Wilcoxon matched-pairs signed-rank test. [(Copyright 1995, Oxford University Press).] (Inset) Dominance acts per nest mate per hour shown by replacement queens from the day of takeover up to 10 days after queen replacement. Means and 1 SD are shown for 9 nests for days 1–7 and 6 nests on day 10. [Redrawn with permission from ref. (Copyright 1996, Elsevier).]

Fig. 4.

A typical mesh experiment. Mean and SD of the frequency per hour of dominance behavior of the queen (Q), PQ1 and PQ2 on day 1 (unmanipulated colony), day 2 (after dividing the colony), and day 3 (after exchanging the queen) (n = 12 colonies). Comparisons are by Wilcoxon matched-pairs signed-ranks test and significantly different values (P < α, where α is set to 0.0023 after Bonferroni correction) are indicated by different letters. [Redrawn with permission from ref. (Copyright 2008, Springer).]

Fig. 5.

Frequency per hour of dominance behavior (DB) shown by the PQ within 30 min of queen removal as compared with her own levels of dominance in the queen right colony. Wilcoxon matched-pairs, signed-ranks test; n = 50, P = 0.000. [Redrawn with permission from ref. (Copyright 2007, Elsevier).]

Fig. 6.

Mean and SD of the frequency per hour of RA shown by the queen (blue bar), Max worker (the worker showing the highest value among workers in the colony; green bar), and Min worker (the worker showing the lowest value among workers in the colony; black bar). n = 8 colonies. Comparisons are by Wilcoxon matched-pairs, signed-ranks test; bars with different letters are significantly different (P < 0.05) from each other. [Redrawn with permission from ref. (Copyright 2007, Elsevier).]

Fig. 7.

Foraging, feeding larvae, and unloading in a typical queen removal experiment. (Upper) Frequencies per hour of food brought per individual per hour and feeding larvae per individual per hour are not significantly different on days 1–3, as can be seen from the identical letters on the bars. (Lower) Frequencies at which foragers were unloaded and the proportion of the feeding of larvae done by foragers on days 1–3. For each behavior, bars with different letters are significantly different from each other. All comparisons are by 2-tailed Wilcoxon matched-pairs signed-rank tests. [Redrawn with permission from ref. (Copyright 1995, Oxford University Press).]

Fig. 8.

Excess feeding experiment. Comparisons of bring food, feed larvae, and dominance behavior among workers and dominance received by foragers, on day 1 (normal colony) and day 3 (1 day after excess feeding). Bars shown are the means and SDs across 11 nests. For all variables, values on day 1 are significantly greater than the corresponding values on day 3 (two-tailed Wilcoxon matched-pairs, signed-rank tests; P < 0.05). [Redrawn with permission from ref. (Copyright 2006, Elsevier).]

Fig. 9.

Food deprivation experiment. Comparison of mean and SD of frequency per hour of dominance behavior, foraging attempts, and bring food on day 1 (normal colony), day 2 (food deprived by preventing foraging), and day 3 (foraging permitted). Different numbers indicate a significant difference between the bars (two-tailed, Wilcoxon matched-pairs test; n = 8). [Redrawn with permission from ref. (Copyright 2008, Springer).]

Fig. 10.

A schematic diagram postulating physiological effects of aggression in the aggressor and the victim (Right) and the absence of aggression in a lone wasp (Left).

Fig. 11.

The queen (Q)–PQ exchange experiment. (Upper) A typical experiment in which the PQ1 was the cryptic successor. The frequency per hour of dominance behavior exhibited by the queen, PQ1, and Max worker (defined as the worker showing maximum aggression) on day 1 in the normal colony and on the queen-right and queenless fragments in the 3 sessions on day 2 are shown. (Lower) A typical experiment in which the PQ2 was the cryptic successor. The frequency per hour of dominance behavior exhibited by the queen, PQ1, PQ2, and Max worker on day 1 in the normal colony and on the queen-right and queenless fragments in the 3 sessions on day 2 are shown. [Redrawn with permission from ref. (Copyright 2008, The Royal Society).]