Behav Ecol Sociobiol (2008) 62:1643–1653 DOI 10.1007/s00265-008-0593-5
ORIGINAL PAPER
Nest site selection in the open-nesting honeybee Apis florea Benjamin P. Oldroyd & Rosalyn S. Gloag & Naïla Even & Wandee Wattanachaiyingcharoen & Madeleine Beekman
Received: 10 February 2008 / Revised: 24 March 2008 / Accepted: 8 April 2008 / Published online: 5 June 2008 # Springer-Verlag 2008
Abstract We studied nest site selection by swarms of the red dwarf honeybee, Apis florea. By video recording and decoding all dances of four swarms, we were able to determine the direction and distances indicated by 1,239 dances performed by the bees. The bees also performed a total of 715 nondirectional dances; dances that were so brief that no directional information could be extracted. Even though dances converged over time to a smaller number of areas, in none of the swarms did dances converge to one site. As a result, even prior to lift off, bees performed dances indicating nest sites in several different directions. Two of four swarms traveled directly in what seemed to be the general direction indicated by the majority of dances in the half hour prior to swarm lift off. The other two traveled along circuitous routes in the general direction indicated by the dances. We suggest that nest site selection in A. florea has similar elements to nest site selection in the better-studied Apis mellifera. However, the observation that many more locations are indicated by dances prior to lift off also shows that there are fundamental differences between the two species. Keywords Apis florea . Red dwarf honeybee . Apis mellifera . Swarming . Nesting . Decentralised decision-making . Hymenoptera
Communicated by M. Giurfa B. P. Oldroyd (*) : R. S. Gloag : N. Even : M. Beekman Behaviour and Genetics of Social Insects Laboratory, School of Biological Sciences A12, University of Sydney, Sydney, NSW 2006, Australia e-mail:
[email protected] W. Wattanachaiyingcharoen Department of Biology, Faculty of Science, Naresuan University, Phitsanulok 65000, Thailand
Introduction Finding a new nest site is one of the most important decisions an insect colony must make, for its reproductive success will be greatly enhanced if the site is a superior one and compromised if the site is a poor one (Franks et al. 2002). For example, if seeking a cavity, it must be of sufficient size to allow full development of the colony while the opening should be sufficiently small that it affords protection from predators and the elements (Seeley and Buhrman 2001; Franks et al. 2003). In many species, the colony makes considerable investment in the nest site, furnishing it with combs and lining the interior with protective barriers (Seeley and Morse 1976; Hepburn 1986; Roubik 2006), meaning that it is costly to abandon a site should it turn out to be a poor one. Not surprisingly, therefore, many social insect species have evolved elaborate mechanisms to search for new nest sites, evaluate their relative merits and to decide on the best site possible (Seeley et al. 2006; Visscher 2007). The decision making process is achieved via a non-hierarchical distributed network that often involves hundreds of individuals but never the entire colony (Camazine et al. 2001). The nature of these mechanisms is particularly interesting because they can provide inspiration for new ways of decision making in human systems, which tend to employ centralised hierarchical systems (Bonabeau and Meyer 2001) and insight into how complex group behaviour can evolve even in animals with relatively simple nervous systems like bees and ants (Anderson 2002). In the western hive bee, Apis mellifera, the process of swarming and nest site selection is well understood (Lindauer 1955; Winston 1987; Seeley and Visscher 2004a; Visscher 2007). A reproductive swarm issues from the colony and clusters a few tens of metres from it. Scout
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bees then begin searching for suitable cavities in which to construct the colony’s new home. Successful scouts report the location of suitable nesting cavities to other bees by performing communication dances on the surface of the swarm cluster (Lindauer 1955) and thus can recruit dance followers to their discovery (Camazine et al. 1999; Seeley and Buhrman 1999). (In the following, we simply refer to both scouts and recruits as ‘bees’; it is important to realise that these bees are only a small subset of all bees in the swarm as the majority will remain quiescent within the swarm cluster.) Both the number of dances performed by a bee and the number of circuits per dance are positively correlated with the bee’s perception of nest site quality. With each visit to the potential site, the number of dance circuits performed by an individual bee declines linearly, but bees that have rated their site as being of high quality start with more dance circuits per dance than those that have visited a poor quality site (Seeley and Buhrman 1999; Seeley 2003). As a result, sites of high quality are advertised for longer than sites of low quality. The outcome of this process is an increase in the number of bees visiting and dancing for sites of good quality and a decreasing number of bees dancing for sites of poor quality (Seeley 2003). Eventually, one site comes to dominate in visitation and dancing (Lindauer 1955; Seeley and Buhrman 1999), a process that may take several days (Villa 2004). When one site under consideration is being visited by a sufficient number of bees, the bees at the new nest site sense that a quorum has been reached (Seeley and Visscher 2004b). Once the quorum has been achieved, bees that have sensed the quorum return to the swarm and signal the end of the decision-making process by producing an auditory signal— piping. This signal informs the quiescent bees of the cluster that they should prepare themselves metabolically for flight (Seeley and Tautz 2001; Donahoe et al. 2003; Seeley et al. 2003). The final signals for flight are ‘buzz running’ in which a scout runs in zigzags over the swarm, vibrating its wings every second or so (Lindauer 1955; Rittschof and Seeley 2008). The swarm then takes flight and flies to its chosen home, most likely guided by the bees that know of the location of the new nest site, and which streak through the flying swarm in the direction of travel (Janson et al. 2005; Beekman et al. 2006). The red dwarf honeybee, Apis florea, is endemic to Southeast Asia, India and eastern regions of the Middle East (Oldroyd and Wongsiri 2006). In contrast to cavitynesting A. mellifera, an A. florea colony builds a small nest comprised of a single comb about 20×20 cm (Rinderer et al. 1996), suspended from a twig of a shrub or tree in the open (Akratanakul 1977). For a cavity-nesting honeybee species like A. mellifera, there is likely to be only a limited number of potential nest sites located by a swarm. In contrast, for an open-nesting species like A. florea, it seems
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that there is an almost infinite number of shaded twigs that would be equally suitable for building a nest. This would remain true even if factors such as proximity to food, water or other nests of A. florea caused certain areas of the general environment to be favoured as nesting sites. In A. mellifera, the relative quality of potential nest sites is critical to the process of decision making (Seeley and Buhrman 2001). Given that there must be hundreds of thousands of equally good twigs within flying distance of most A. florea swarms, how does A. florea select a new nest site? Does the swarm simply fly off, landing at the first suitable site encountered? Or does A. florea employ scouts that search the surroundings for potential nest sites and report their locations in the form of recruitment dances in a process similar to that found in A. mellifera? And if so, what criteria do the scouts use to select one site over another? Here, we explore aspects of the nest site selection process of swarms of A. florea. A. florea is part of the most basal clade of honeybees (Raffiudin and Crozier 2007) and so characters present in them, and also in other more derived species, are most likely the ancestral condition. We, therefore, contrast the behaviour of A. florea swarms with that of the derived cavity nesting species A. mellifera, thus providing insights into the evolution of nest site selection in the honeybee.
Methods Recording the behaviour of swarms In May–June 2007, we created four combless swarms of A. florea on the grounds of Naresuan University in Phitsanulok, Thailand. Our site contained grassy areas, isolated trees, some secondary regrowth (approximately 2 m high), rows of ornamental trees on three sides and an ornamental lake on the fourth side. To establish a swarm, we lightly smoked a wild colony, which caused the adult bees to contract into a tight cluster near the top of the comb. We, then, cut the twig holding the nest and gently transferred it into a muslin bag for transport. We suspended the twig holding the colony in a convenient location and removed the bag. After the colony had rested for several hours, we sprayed it liberally with water to reduce defensiveness and, using a pencil to push the curtain of bees aside, searched for the queen, which we placed in a wire gauze cage (3.5×3×1 cm). We, then, suspended the caged queen in a screened box (20×22×18 cm) and dumped all adult bees into the box. The caged colony was then fed sucrose syrup (1:1 by volume, granulated sucrose/ water) ad libitum for 3–4 days until the workers began to produce wax scales (Seeley and Buhrman 1999). Confining the queen and her workers to a cage while feeding the bees
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copious amounts of sucrose syrup is known to induce normal nest site selection behaviour in A. mellifera. Because of this feeding and the fact that the bees started to produce wax scales, we assume that our swarms behaved as a reproductive swarm in a temporary cluster. However, we recognize that our swarms were not natural and may have behaved like an absconding swarm after leaving an established nest in response to a dearth of food or attack by predators (Combs 1972). Such absconding swarms probably go through a nest site selection process similar to a reproductive swarm but may also migrate before finally settling down as does the related Apis dorsata (Koeniger and Koeniger 1980; Dyer and Seeley 1994). We used an isolated tree in the middle of the site as a place to establish all four swarms. At a convenient height for making video recordings, we suspended a 1.5 m long, 1.5 cm diameter stick horizontally from the tree’s trunk to make a support for the swarms. To set up a swarm, we tied the cage containing the queen to the stick at dusk and then shook the workers from the screen cage. Without exception, the workers quickly joined their queen and formed a swarm cluster. To prevent ants from harassing our swarms, we placed a thick layer of axle grease around the supporting stick. The location we chose was shaded, similar to natural nest sites of A. florea. The only difference was that this location was closer to the ground to allow us to film the dances. The queens were released from their cage either just after dawn the next morning (swarms 2–4) while the queen of swarm 1 was released an hour prior to lift off. We made video recordings of every dance on the surface of each swarm until it departed. Most dances took place on the horizontal plane formed by the bees clustered on the top of the stick. Because the bees had been fed ample sugar solution while caged, we could be assured that most, if not all, dances were for potential nest sites and not for forage. This assumption was confirmed by the absence of any dancers carrying pollen or any dancers offering food to other workers during dances. A magnetic compass was positioned so that it was visible throughout the recordings. We regularly recorded the time of day on the audio track of the video. We also recorded the departures of the swarms and, where possible, observed the behaviour of queens as the swarms took off. After the swarms departed, we followed them as far as was possible. In two cases, we were able to observe where the swarm clustered. Decoding the dances Descriptions of the components of the dance (waggle phase and return phase) are given in Weidenmüller and Seeley (1999). During freeze-frame playback, we aligned a circular
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protractor similar to that described by von Frisch (1967) along the axis of a dancing bee and recorded the deviation of the bee’s body from straight up the screen during its waggle phase to the nearest degree. Dances were only measured if the dance included four consecutive waggle phases, and the direction of the dance was decoded as the mean of the 4+ consecutive waggles. Using the image of the compass, we then converted these readings into the compass direction that the worker had faced during her waggle phases. We also measured the duration of the waggle phase of each dance to the nearest 1/10 s. The dance of a honeybee worker contains information about the direction and distance to the goal that the worker is indicating (Dyer 2002). The duration of a waggle phase of the dance indicates the distance to the goal (von Frisch 1967). Short waggle runs indicate nearby goals, whereas long ones indicate more distance goals. Three calibration curves that relate duration of the dance circuit to distance to feeder have been determined empirically for A. florea (Lindauer 1956; Koeniger et al. 1982; Dyer and Seeley 1991). These three calibration curves include the duration of the return phase of the dance: the time it takes the dancing bee to return to its original position before performing the next waggle phase. However, we noticed that particularly in protracted dances, the duration of the return phase was highly variable between each waggle phase of the same dance. Often, the dancing bee had to force her way through other bees before she could resume dancing. We, therefore, did not include the return phase in our measurement but added a fixed return phase of 1.5 s (Gardner et al. 2007) to all our dances to obtain a relative measure of the distance of the advertised sites. The published curves relating distance to dance circuit duration (Lindauer 1956; Koeniger et al. 1982; Dyer and Seeley 1991) are quite variable. This is not surprising because distance perception by flying bees is heavily influenced by the visual environment (Srinivasan et al. 2000; Esch et al. 2001; Barron and Srinivasan 2006). Because we were interested in visualising the relative location of the sites advertised on the swarms rather than their absolute position, we used an average of the three published curves to estimate the distances that the dances were indicating. The equation relating circuit duration to distance we used was: circuit duration = 1.5 + 0.0068 (distance). By combining the distance and direction information for each dance, we were able to deduce the polar coordinates of the site being advertised by each dancing bee. We present our data in radial plots in which each point represents a dance, as has been done previously for foraging A. mellifera (e.g. Visscher and Seeley 1982; Beekman and Ratnieks 2000). In all swarms, a large number of dancers performed dances that were not fully formed figure of eight
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dances. Bees either waggled without otherwise moving forward or, more commonly, waggled throughout the dance in rather random circles but with more vigorous wagging in one direction or with abdomen raised in a particular direction only. Because of the short duration of those dances, we could not discern information about distance even though they do contain directional information (Sen Sarma et al. 2004). We recorded them as ‘round’ dances and show their numbers in Fig. 1.
directions that were significantly from random (Zar 1996). In addition, in the final 30 min before swarm lift off, we used a one-sample test for the mean angle (Zar 1996) to test the null hypothesis that the mean vector indicated by the dances differed significantly from the direction actually traveled by the swarm.
Statistical analysis
Reaching a decision
For each 1-h period in which observations were made, we used a Rayleigh’s test to determine if dances indicated
Figure 1 shows how the popularity of different sites waxed and waned over time. In all cases, the directions of new nest
Results
Swarm 1 z=0.26, P=0.07
z=8.24, P
