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Colour Preferences of Tetragonula Carbonaria Sm. Stingless Bees For University of Groningen Colour preferences of Tetragonula carbonaria Sm. stingless bees for colour morphs of the Australian native orchid Caladenia carnea Dyer, Adrian G.; Boyd-Gerny, Skye; Shrestha, Mani; Garcia, Jair E.; van der Kooi, Casper J.; Wong, Bob B M Published in: Journal of Comparative Physiology A DOI: 10.1007/s00359-019-01346-0 IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2019 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Dyer, A. G., Boyd-Gerny, S., Shrestha, M., Garcia, J. E., van der Kooi, C. J., & Wong, B. B. M. (2019). Colour preferences of Tetragonula carbonaria Sm. stingless bees for colour morphs of the Australian native orchid Caladenia carnea. Journal of Comparative Physiology A, 205(3), 347-361. https://doi.org/10.1007/s00359-019-01346-0 Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 27-09-2021 Journal of Comparative Physiology A (2019) 205:347–361 https://doi.org/10.1007/s00359-019-01346-0 ORIGINAL PAPER Colour preferences of Tetragonula carbonaria Sm. stingless bees for colour morphs of the Australian native orchid Caladenia carnea Adrian G. Dyer1,4 · Skye Boyd‑Gerny2 · Mani Shrestha2,3 · Jair E. Garcia1 · Casper J. van der Kooi5 · Bob B. M. Wong2 Received: 18 October 2018 / Revised: 8 May 2019 / Accepted: 13 May 2019 / Published online: 29 May 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Innate colour preferences promote the capacity of pollinators to fnd fowers, although currently there is a paucity of data on how preferences apply to real fowers. The Australian sugarbag bee (Tetragonula carbonaria Sm.) has innate prefer- ences for colours, including UV-absorbing white. Sugarbag bees are pollinators of the terrestrial orchid Caladenia carnea R.Br., which has both white and pink morphs. In laboratory conditions, we tested fower-naïve bees with the white and pink fower morphs revealing a signifcant preference for the white morph, consistent with experiments using artifcial stimuli. In experiments to understand how bees may select food-deceptive orchids following habituation to a particular colour morph, we observed a signifcant increase in choices towards novel white fowers. We also observed that the presence of a UV- refecting dorsal sepal signal signifcantly increased bee choices compared to fowers that had the UV signal blocked. Our fndings demonstrate that innate preference testing of insect pollinators with artifcial stimuli is replicated in a biologically signifcant scenario with fowers. The fndings also underscore how food-deceptive orchids can receive sufcient pollinator visits to ensure pollination by having diferent morphs that draw on the innate preferences of bees and their ability to make decisions in a complex ecological setting. Keywords Flower · Orchids · Pollination · Innate preferences · Ultraviolet Introduction 2011; Reser et al. 2012; Hempel de Ibarra et al. 2014) infu- ence how fowers visited by bees may have evolved specifc Plant–pollinator interactions provide important insights into signals (Chittka and Menzel 1992). Darwin (1877) postu- how complex biological partnerships exist (Barth 1985; lated that innate preferences could allow fower visitors to Sargent and Ackerly 2008; Mitchell et al. 2009). Bees, in more easily fnd fowers, and testing using artifcial stimuli particular, are an important model in neuroethology for in several species of bees has revealed innate colour prefer- understanding how the building blocks of sensory percep- ences that could act to infuence bee choices (Giurfa et al. tion (Frisch 1914; Srinivasan and Lehrer 1988; Dyer et al. 1995; Gumbert 2000; Rohde et al. 2013; Dyer et al. 2016a). However, there is currently a paucity of data on how col- * Adrian G. Dyer our preferences observed in bees for artifcial stimuli might [email protected] represent the actual choices for real fowers. Understanding these principles is important for building a better under- 1 School of Media and Communication, RMIT University, standing of how sensory perception of bee pollinators may Melbourne, VIC 3001, Australia shape plant communities. 2 School of Biological Sciences, Monash University, Clayton, Colour perception requires the presence of multiple pho- VIC 3800, Australia toreceptors, and bees have been shown to have a phylogenet- 3 Faculty of Information Technology, Monash University, ically conserved trichromatic visual system based on ultra- Clayton, VIC 3800, Australia violet-, blue- and green-sensitive photoreceptors (Briscoe 4 Department of Physiology, Monash University, Clayton, and Chittka 2001). In this respect, fowers in both the North- VIC 3800, Australia ern (Chittka and Menzel 1992; Arnold et al. 2009; Shrestha 5 Groningen Institute for Evolutionary Life Sciences, et al. 2014) and Southern Hemispheres (Dyer et al. 2012; University of Groningen, Groningen, The Netherlands Vol.:(0123456789)1 3 348 Journal of Comparative Physiology A (2019) 205:347–361 Bischof et al. 2013; Shrestha et al. 2013) are typically char- and perceptual biases of Hymenopteran pollinators (Wong acterised by spectral signatures with marker points at about and Schiestl 2002; Peakall 2007; Phillips et al. 2009; Gaskett 400 and 500 nm, which closely match the optimal colour 2011). In this regard, the role of colour signals in orchids processing of bee trichromats (Helversen 1972; Chittka and that use food mimicry to achieve pollination remains poorly Menzel 1992). However, there is strong evidence that the understood (Jersáková et al. 2012, 2016). Bees, including colour vision of diferent pollinators signifcantly infuences the sugarbag bee, are known pollinators of the terrestrial what colour fowers evolve. For instance, in South America, orchid Caladenia carnea (Adams et al. 1992; Kuiter 2016), both white and red hummingbird-pollinated fowers difer a widespread species endemic to south-eastern Australia. from bee-pollinated fowers in their refection properties Caladenia carnea is believed to be a food-deceptive orchid for ultraviolet (UV) light (Lunau et al. 2011). Specifcally, that achieves pollination through colour mimicry of food- red fowers lack UV signals and, thus, the predominately rewarding fowers. Interestingly, the species is also colour long wavelength signals do not modulate the trichromatic polymorphic, with both white and pink forms of the fower vision of bees, whereas hummingbird-pollinated white fow- present in the same environment (Jones 2006 and Pers. obs ers do refect UV, which results in achromatic stimuli that authors). Both the orchid’s pollination syndrome and its are difcult to detect since bees do not process brightness striking colour polymorphism make C. carnea an excellent diferences (Kevan et al. 1996; Spaethe et al. 2001; Dyer model with which to investigate foral exploitation of the vis- et al. 2007; Lunau et al. 2011; Ng et al. 2018). For common ual system and behaviour of bee pollinators. Due to the lack poppy (Papaver rhoeas) fowers, it was found that in the of any obvious resemblance to nectar-producing models, it Middle East where it is pollinated by a red-sensitive beetle has been suggested that most food-deceptive Caladenia spe- the fowers refect only red light, but in Europe, where it is cies, including C. carnea, are likely to be using non-model pollinated by bees, the fowers also refect ultraviolet light mimicry to attract generalist food-seeking insects (Phillips (van der Kooi and Stavenga 2019). Thus, UV signalling from et al. 2009; but see Dixon and Christenhusz 2018). broadband natural colours can be complex and depend on In the current study, we frst used laboratory-based testing which wavelengths of UV are refected, and it is important to of sugarbag bees to investigate if previously observed innate test diferent animals to understand how the building blocks preferences for UV-absorbing white artifcial stimuli might of perception may take efect in biological systems (Kemp apply when considering colour morphs of cultivated C. et al. 2015). carnea orchid fowers sourced from the Australasian Native Recently, there has been increased interest in stingless Orchid Society. In our lab-based study, we additionally bees and how these insects interact with their environment tested if the dorsal sepal that refected UV radiation infu- in a way that enables successful pollination (Hrncir et al. enced bee choices if the UV signal was blocked. Our analy- 2016). The sugarbag bee (Tetragonula carbonaria Sm.), is ses of spectra also considered modulation of green receptor a small (1.13 ± 0.02 mm intertegulae span; mean ± SD; Dyer contrast, since that factor has previously been shown to be et al. 2016a, b) native Australian bee that lives in colonies
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