Functional Ecology 2011, 25, 1–9 doi: 10.1111/j.1365-2435.2011.01885.x ‘X’ marks the spot: The possible benefits of nectar guides to bees and plants Anne S. Leonard* and Daniel R. Papaj Department of Ecology and Evolutionary Biology, Center for Insect Science, University of Arizona, 1041 East Lowell Street, Tucson, Arizona 85721, USA Summary 1. Many floral displays are visually complex, transmitting multi-coloured patterns that are thought to direct pollinators to nectar rewards. These ‘nectar guides’ may be mutually beneficial, if they reduce pollinators’ handling time, leading to an increased visitation rate and promoting pollen transfer. Yet, many details regarding how floral patterns influence foraging efficiency are unknown, as is the poten- tial for pollinator learning to alter this relationship. 2. We compared the responses of bumblebee (Bombus impatiens Cresson) foragers to artificial flowers that either possessed or lacked star-like patterns. By presenting each bee with two different foraging scenarios (patterned flowers rewarding ⁄ plain flowers unrewarding, plain flowers rewarding ⁄ patterned flowers unrewarding) on different days, we were able to assess both short- and long-term effects of pat- terns on bee foraging behaviour. 3. Bees discovered rewards more quickly on patterned flowers and were less likely to miss the reward, regardless of whether corollas were circular or had petals. Nectar guides’ effect on nectar discovery was immediate (innate) and persisted even after experience, although nectar discovery itself also had a learned component. We also found that bees departed patterned flowers sooner after feeding. Finally, when conditions changed such that flowers no longer provided a reward, bees visited the now-unre- warding flowers more persistently when they were patterned. 4. On the time-scale of a single foraging bout, our results provide some of the first data on how pollina- tors learn to forage efficiently using this common floral trait. Our bees’ persistent response to patterned flowers even after rewards ceased suggests that, rather than being consistently mutually beneficial to plant and pollinator, nectar guide patterns can at times promote pollen transfer for the plant at the expense of a bee’s foraging success. Key-words: Bombus, constancy, efficiency, foraging, handling time, learning, nectar discovery, pattern rotation, and configuration: Giurfa, Eichmann & Menzel 1996; Introduction Horridge 2000; Plowright et al. 2001; Avargue`s-Weber et al. Flowers display a remarkable variety of colourful patterns (Dafni, 2010), surprisingly few studies address whether and how the Lehrer & Kevan 1997; Fig. 1a–d). Theories on the function of presence of a nectar guide benefits plants and ⁄ or pollinators. this visual complexity date at least to the time of Sprengel Often, it is assumed that floral patterns are mutually benefi- (1793), who proposed that Saftmale (a German word translating cial to both plant and pollinator. Optimal diet theory (Pyke, Pul- as ‘juice marks’) guide pollinators towards the flower’s nectary. liam & Charnov 1977; Sih & Christensen 2001) predicts that Despite the ubiquity of such floral patterns (Kugler 1966; Penny foragers should be sensitive to the costs of acquiring particular 1983; Chittka et al. 1994), a good understanding of what fea- food items (nectar sources), adjusting their choices based not tures make them attractive (Knoll 1926; Daumer 1956, 1958; only upon energetic rewards, but also on the time or energy it Manning 1956; Free 1970; Jones & Buchmann 1974; Lunau takes to access those rewards. If pollinator fitness depends upon et al. 2006; Shang et al. 2010) and evidence that pollinators maximizing the rate of nectar collection (as in social bees: Pelle- perceive quite subtle aspects of their form (such as symmetry, tier & McNeil 2003; Burns 2005), then all else being equal, they should select flowers that have shorter handling times. Pollina- tors tend to spend less time using flowers that possess nectar *Correspondence author. E-mail: [email protected] Ó 2011 The Authors. Functional Ecology Ó 2011 British Ecological Society 2 A. S. Leonard & D. R. Papaj (a) (b) (c) (d) (e) (f) (g) Fig. 1. Animal-pollinated plants display a variety of floral patterns, which often function as nectar guides (a) Alstroemeria sp. with honey bee, Apis mellifera (b) Ipomoea ternifolia, (c) Lamiaceae, (d) Viola sp., (e) Circular and (f) Petaloid artificial flowers and patterns used in experiment. (g) Reflec- tance spectra for components of artificial flowers used in experiment; our colours mimic a natural situation in which foliage provides a grey-green background, flower petals are blue and nectar guide patterns are UV-blue. Photographs: A.S. Leonard. guides, suggesting that these patterns are indeed associated with of a single foraging trip, where a pattern is always associated foraging efficiency (Waser & Price 1983, 1985; Dinkel & Lunau with a reward. Because nectar availability of any one plant 2001; but see West & Laverty 1998). species can fluctuate (because of temporal changes in produc- Yet, we lack many basic details regarding how floral patterns tion or depletion by floral visitors: Heinrich 1979a), our multi- influence pollinator behaviour. For example, rather than explor- day experiment allowed us to examine how a floral pattern ing how patterns affect the sequence of behaviours on the flower, affected the capacity of bees to switch floral types when a pre- previous studies have focused on overall flower handling time, viously rewarding type becomes unrewarding. In this scenario, or even travel time between flowers. Additionally, the long-term the interests of the bee are in potential conflict with those of benefits of a guide remain unclear, because pollinators may the plant. The bee stands to benefit if the nectar guide on the acquire handling skills (e.g. Laverty 1994a) that allow them to once-rewarding floral type facilitates switching to a novel type, eventually forage equally efficiently without a guide. Although whereas the plant might benefit if the nectar guide impedes a naı¨ve bee’s preference for landing on patterned flowers is well- switching. Does experience using a nectar guide to locate a established (e.g. Lehrer, Wehner & Srinivasan 1985; Dafni, Leh- reward thus facilitate – or hinder – foraging on flowers that rer & Kevan 1997; Simonds & Plowright 2004), the effects of lack guides? patterns on foraging efficiency have apparently not been Our study explored two general aspects of the relationship assessed beyond the timeline of a single foraging bout. Perhaps between floral patterns and bumblebee (Bombus impatiens) nec- not surprisingly, nothing has been reported about how experi- tar foraging. First, we focused on possible handling time bene- ence shapes the guiding function of floral patterns, if at all. fits of a pattern. We examined the effects of a floral pattern not Understanding how the on-flower effects of a nectar guide only on nectar discovery but also on a bee’s decision to leave change with experience would provide a more precise descrip- the flower. Secondly, we also determined how pollinator experi- tion of the function(s) of this common floral trait. It might also ence affected nectar discovery in the context of floral patterns. yield a more informed perspective on the possible benefits of Whereas we hypothesized that a nectar guide would facilitate guides to plant and pollinator. In general, nectar guides are naı¨ve bees’ nectar discovery, we developed two opposing pre- presumed to benefit both plant and pollinator. A reduction in dictions for how the benefit of a guide might change with expe- nectar discovery time, for instance, might increase the rate at rience. If nectar guides aid bees in learning how to locate nectar which a bee acquires energy in the form of nectar (of benefit more effectively, then the relative time savings of a nectar guide to the bee) and simultaneously improve the rate at which the should grow over the course of a foraging trip. Alternatively, if bee transfers pollen (of benefit to the plant). Yet, most studies guides primarily benefit naı¨ve bees, the relative benefit of a examine pollinator responses to nectar guides on the time-scale guide should decrease. Ó 2011 The Authors. Functional Ecology Ó 2011 British Ecological Society, Functional Ecology, 25, 1–9 Nectar guides and bumblebee foraging 3 Materials and methods perimeter than the circle (surface area of circle: 19Æ63 cm2;petaloid: 15Æ75 cm2; perimeter of circle: 15Æ70 cm; petaloid: 23Æ80 cm; measured SUBJECTS AND PRE-TRAINING with Adobe Photoshop CS3, Adobe Systems, San Jose CA, USA). Shape differences may have altered the detectability of flower targets, as honey We used 30 B. impatiens workers as subjects, selected from a colony bees detect circular targets at a longer distance than petaloid targets (Ne’e- obtained from Koppert Biological Systems (Romulus, MI, USA). The man & Kevan 2001). On any given foraging trip, six of these flowers were colony was provided with pollen ad libitum and housed in a plastic box plain, and six had a light (human white; bee UV-blue), radially symmetri- (L · W · H: 22Æ0 · 24Æ0 · 12Æ0 cm). Experiments occurred in a room- cal, nectar guide pattern. The pattern was identical for both circular and pet- sized experimental chamber (L · W · H: 3Æ05 · 1Æ92 · 1Æ55 m), fitted aloid flowers. Although our artificial flowers were not modelled on a with a screen door to permit observation. The experimental chamber was specific species, many bee-pollinated flowers present a blue corolla with connected to the colony via a gated buffer box (L · W · H: light, UV-reflective radiating lines (e.g. Iris, Salvia, Ipomoea). Generally, 35Æ0 · 22Æ0 · 15Æ0 cm) that allowed us to release individual foragers, fit- chromatic contrast between pattern and corolla is important in guiding ted on the thorax with numbered tags (E.H. Thorne Ltd., Wragby, bumblebees’ orientation towards flowers (e.g. Lunau, Wacht & Chittka Lincolnshire, UK) for identification. The chamber was illuminated by 1996; Lunau et al.