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Travel Optimization by Foraging Bumblebees Through Readjustments of Traplines After Discovery of New Feeding Locations Travel Optimization by Foraging Bumblebees through Readjustments of Traplines after Discovery of New Feeding Locations. Author(s): Mathieu Lihoreau, Lars Chittka, Nigel E. Raine Source: The American Naturalist, Vol. 176, No. 6 (December 2010), pp. 744-757 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/657042 . Accessed: 24/01/2011 13:57 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. 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The University of Chicago Press and The American Society of Naturalists are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org vol. 176, no. 6 the american naturalist december 2010 ൴ Travel Optimization by Foraging Bumblebees through Readjustments of Traplines after Discovery of New Feeding Locations Mathieu Lihoreau,1 Lars Chittka,1 and Nigel E. Raine1,2,* 1. Research Centre for Psychology, School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, United Kingdom; 2. School of Biological Sciences, Royal Holloway University of London, Egham, Surrey TW20 OEX, United Kingdom Submitted March 24, 2010; Accepted August 10, 2010; Electronically published October 25, 2010 Online enhancements: appendix figures. Navigation can be achieved using different mechanisms— abstract: Animals collecting resources that replenish over time such as directional compasses (e.g., Muheim et al. 2006), often visit patches in predictable sequences called traplines. Despite the widespread nature of this strategy, we still know little about how path integration (e.g., Mu¨ller and Wehner 1988; Chittka spatial memory develops and guides individuals toward suitable et al. 1995b), learned landmark sequences (e.g., Chittka et routes. Here, we investigate whether flower visitation sequences by al. 1995a; Zhang et al. 1996), or learned motor sequences bumblebees Bombus terrestris simply reflect the order in which flow- (e.g., Collett et al. 1993)—and often guides individual ers were discovered or whether they result from more complex nav- movements toward functional, if not optimal, routes. Be- igational strategies enabling bees to optimize their foraging routes. cause the complexity of routing problems increases ex- We analyzed bee flight movements in an array of four artificial flowers ponentially with the number of sites individuals have to maximizing interfloral distances. Starting from a single patch, we visit (Lawler et al. 1985), travel optimization becomes par- sequentially added three new patches so that if bees visited them in the order in which they originally encountered flowers, they would ticularly challenging for central-place foragers collecting follow a long (suboptimal) route. Bees’ tendency to visit patches in resources from multiple scattered patches. their discovery order decreased with experience. Instead, they opti- Bees, for example, are known to repeat foraging circuits, mized their flight distances by rearranging flower visitation se- visiting a particular set of flowers in a predictable non- quences. This resulted in the development of a primary route (trap- random order, referred to as trapline foraging in analogy line) and two or three less frequently used secondary routes. Bees with trappers checking traps on a regular basis (for a re- consistently used these routes after overnight breaks while occasion- view, see Ohashi and Thomson 2009). This strategy, al- ally exploring novel possibilities. We discuss how maintaining some level of route flexibility could allow traplining animals to cope with though first reported in pollinating insects (Heinrich 1976; dynamic routing problems, analogous to the well-known traveling Gilbert 1980), is widespread among animals and has been salesman problem. described in many vertebrates, such as bats (Lemke 1984; Racey and Swift 1985), birds (Davies and Houston 1981; Keywords: Bombus terrestris, pollination ecology, spatial cognition, Gill 1988), primates (Janson 1998; Watts 1998; Noser and trapline foraging, traveling salesman problem. Byrne 2010), and rodents (Reid and Reid 2005). In recent years, much attention has been focused on the adaptive value of traplining, highlighting that route fidelity can in- Introduction crease individual foraging performance in different ways, whether by allowing animals to (1) learn locations of the Animals exploiting resources within fixed areas or terri- most rewarding resources (Williams and Thomson 1998; tories have a set of navigational memories at their disposal Garrison and Gass 1999; Cunningham and Janson 2007), that allow them to encode spatial relationships between (2) set up optimal visitation schedules in relation to re- features of their environment and orient accurately as they sources replenishment rates (Possingham 1989; Ohashi gain experience (reviewed in Dolins and Mitchell 2010). and Thomson 2005), (3) increase travel speed and accuracy * Corresponding author; e-mail: [email protected]. of movements (Ohashi et al. 2007; Saleh and Chittka Am. Nat. 2010. Vol. 176, pp. 744–757. ᭧ 2010 by The University of Chicago. 2007), and/or (4) outcompete less experienced conspecifics 0003-0147/2010/17606-52035$15.00. All rights reserved. when exploiting overlapping areas (Gill 1988; Ohashi et DOI: 10.1086/657042 al. 2008). However, the question of how traplines develop Travel Optimization by Foraging Bees 745 remains surprisingly unexplored in comparison with other more efficient routes. We also investigated to what extent navigational strategies. individuals are consistent in their use of foraging circuits As pointed out by Anderson (1983), traplining animals after extended breaks, by observing bees in the same floral regularly cope with routing problems analogous to the array over two successive days. well-known traveling salesman problem in mathematics (finding the shortest multidestination route while visiting Methods each location only once). This problem remains time con- suming to solve using extensive computing power and still Experiments were carried out in a large flight room lacks an efficient general solution (Applegate et al. 2006; (length p 870 cm, width p 730 cm, height p 200 cm) Gutin and Punnen 2006). Traplining animals, especially set up in a greenhouse (temperature range: 15ЊϪ20ЊC; those with small brains such as pollinating insects (Menzel photoperiod: 12D : 12L), thus providing bees with eco- and Giurfa 2001; Chittka and Niven 2009), provide an logically realistic dimensions, to investigate large-scale tra- excellent opportunity to test simple heuristics and unravel plining behaviors (between-patch foraging). Greenhouse functional routing solutions (e.g., Bures et al. 1992; Cra- windows were obscured with white paint (Leyland, Bris- mer and Gallistel 1997). tol). Controlled illumination was provided by high- Two laboratory studies recently demonstrated that naive frequency fluorescent lighting (TMS 24F lamps with HF- bees foraging in stable floral arrays develop repeatable B 236 TLD [4.3 kHz] ballasts [Philips, The Netherlands] routes as they gain experience (Ohashi et al. 2007; Saleh fitted with Activa daylight fluorescent tubes [Osram, Ger- and Chittka 2007). Area fidelity allows them to establish many]), which simulates natural daylight above the bee long-term spatial memory and may favor the storage of flicker fusion frequency. Our subjects were workers from landmark sequences and/or motor commands necessary a commercially obtained Bombus terrestris colony (Syn- for accurate orientation (Collett et al. 1993; Menzel et al. genta Bioline Bees, Weert, The Netherlands), housed in a 2000). However, these results tell us little about the bipartite wooden nest box (length p 28 cm, width p 16 decision-making rules used by bees to develop stable vis- cm, height p 11 cm). The movements of bees from the itation sequences in relation to the spatial locations of nest box to the flight room could be carefully controlled flowers or flower patches. In particular, early descriptions using a series of shutters in the transparent entrance tube of trapline foraging in pollinating insects suggested that to the nest box. All workers were marked on their thorax the sequence in which individuals visit plants reflects the using individually numbered colored tags (Opalith tags, order in which they were initially incorporated into the Christian Graze KG, Germany) within a day of emergence route (the discovery order), even though this typically from pupae. The
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