Flower Colours Along an Alpine Altitude Gradient, Seen Through the Eyes of Fly and Bee Pollinators
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Arthropod-Plant Interactions (2009) 3:27–43 DOI 10.1007/s11829-009-9056-9 ORIGINAL PAPER Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators Sarah E. J. Arnold Æ Vincent Savolainen Æ Lars Chittka Received: 23 June 2008 / Accepted: 30 January 2009 / Published online: 17 February 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Alpine flowers face multiple challenges in higher altitude. However, although there was a slight terms of abiotic and biotic factors, some of which may increase in bee-blue-green flowers and a decrease in bee- result in selection for certain colours at increasing altitude, blue flowers with increasing elevation, there were no sta- in particular the changing pollinator species composition, tistically significant effects of altitude on flower colour as which tends to move from bee-dominated at lower eleva- seen either by bees or by flies. Although flower colour is tions to fly-dominated in high-alpine regions. To evaluate known to be constrained by evolutionary history, in this whether growing at altitude—and the associated change in sample we also did not find evidence that phylogeny and the dominant pollinator groups present—has an effect on elevation interact to determine flower colours in alpine the colour of flowers, we analysed data collected from areas. the Dovrefjell National Park in Norway. Unlike previous studies, however, we considered the flower colours Keywords Flower colour Á Pollinator diversity Á according to ecologically relevant models of bee and fly Insect vision Á Alpine flowers Á Pollination colour vision and also their physical spectral properties independently of any colour vision system, rather than merely looking at human colour categories. The shift from Introduction bee to fly pollination with elevation might, according to the pollination syndrome hypothesis, lead to the prediction that Plants growing in mountainous regions are faced with a flower colours should shift from more bee-blue and UV- range of challenges. As well as having to contend, poten- blue flowers (blue/violet to humans, i.e. colours tradition- tially, with high winds, desiccation and extremes of cold, ally associated with large bee pollinators) at low elevations they also face increased ultraviolet exposure and pollinator to more bee-blue-green and green (yellow and white to limitation when the temperatures and winds grow too humans—colours often linked to fly pollination) flowers at extreme for pollinating insects to fly (Totland et al. 2000). Many strategies employed for dealing with such habitats have already been investigated in depth (Totland et al. Handling editor: Neal Williams 2000), but what still warrants further investigation is how S. E. J. Arnold (&) Á L. Chittka flowers at high altitude might exhibit specific adaptations Research Centre for Psychology, School of Biological and in terms of their pigmentation. Chemical Sciences, Queen Mary University of London, Mile Why might some colours in high-alpine habitats be more End Road, London E1 4NS, UK beneficial than others? Flower colour is under selection by e-mail: [email protected] pollinators (Kevan and Baker 1983; Rodriguez-Girones V. Savolainen and Santamaria 2004; Tastard et al. 2008; Waser 1983; Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK Whibley et al. 2006). There are indeed several studies associating shifts in flower colours with shifts in pollinator V. Savolainen Imperial College London, Silwood Park Campus, type (Altshuler 2003; Bradshaw and Schemske 2003). In Ascot, Berks SL5 7PY, UK alpine areas the numbers of pollinators present will 123 28 S. E. J. Arnold et al. decrease overall with increasing altitude, and will change tended to consist of a higher proportion of white and yel- in composition; some insect groups are less able to function low species. McCall and Primack (1992) observed that at very high elevations than others (Kearns 1992; Totland purple and yellow flowers were the most visited colours in 1992). Therefore, different pollinator guilds dominate at lowland woodland, whilst yellow and white were the two different elevations and therefore the selective forces on most visited colours in alpine tundra, with blue–purple flower traits might be expected to differ. The pollination flowers being much less frequently visited. Some of these syndrome hypothesis, which has been used as the basis for earlier studies, however, contain primarily observational studies of pollination systems for many years (Faegri and recordings that are not well supported by statistical power. van der Pijl 1978), postulates a strong association between More importantly, perhaps with the exception of Kevan different pollinator guilds and particular suites of floral (1972), some of these studies have considered flower col- characteristics, in particular aspects of morphology and our principally from the human perspective, without fully colour (e.g. the zygomorphic, closed and blue/purple ‘‘bee taking into account the more recent understanding of pol- flowers’’; large, white ‘‘moth flowers’’ with long corolla linator visual systems and how these differ from human tubes). Based on this framework, a changing pollinator eyes (Chittka and Kevan 2005; Chittka and Menzel 1992; composition at different elevations may be expected to lead Menzel and Shmida 1993). to different colours prevailing at different altitudes These differences are fundamental: all insects so far depending on the dominant pollinator types and the colours extensively tested have UV receptors with a maximum that appeal to them. sensitivity between around 330 and 375 nm (i.e. in the UV For example, the ability of flies to forage at higher range where human eyes have no sensitivity)—this elevations than bees (Kearns 1992;La´zaro et al. 2008; includes bees and other hymenopterans, lepidopterans, Totland 1993) might perhaps lead us to expect that the coleopterans, hemipterans, dipterans, etc. (Briscoe and flower colours traditionally thought to be associated with Chittka 2001). Bees, the most important pollinators in fly pollination (appearing white and yellow to humans) Norway at all but the high-alpine elevations (La´zaro et al. would be more abundant at high altitudes. Flowers 2008), also have blue and green receptors, but typically appearing white (and also pink) to humans are mostly lack red receptors (Peitsch et al. 1992) (see Fig. 1a). Other blue–green for bees and other trichromatic insects (Kevan insects, including many butterflies and flies, have rather et al. 1996), whereas yellow flowers can be either green or different colour vision systems, in some cases more com- UV-green, depending on their UV reflectance, to such plex than those of bees or humans (Briscoe and Chittka insects (Chittka et al. 1994). 2001; Morante and Desplan 2008). Figure 1b shows the Bees appear to be especially dominant at low to medium spectral sensitivities of the four photoreceptors contribut- elevations (i.e. below the treeline, in sub-alpine habitats) ing to colour vision in the blowfly, Lucilia sp. (La´zaro et al. 2008), their large body size allowing foraging We investigated whether the flower community growing in the relative cold, but the high energetic requirement at high altitude has a different pollinator-relevant colour demanded by maintaining their flight muscles at a high composition to that of lower altitude areas, by using a data enough temperature perhaps restricting their activities at set collected along a transect in the Norwegian Dovrefjell very high elevations (Arroyo et al. 1982). Bees of many mountains from 700 m to 1,600 m elevation. This is of species have an innate preference for UV-blue and blue especial interest in light of the recent study by La´zaro et al. flowers (Giurfa et al. 1995; Raine et al. 2006), leading (2008), in which plant communities at different elevations perhaps to an expectation based on the pollination syn- in southern Norway were surveyed for floral colour and drome hypothesis that where bees dominate as pollinators morphology, and this was combined with visitation data. (e.g. below the treeline in mountainous regions), bee-blue The study found evidence of association between traits and UV-blue flower species should be more numerous. (including colour) and pollinator, showing that flowers in However, this preference is modifiable by learning, as are alpine areas generally seem to be visited by pollinators that the innate preferences in many other pollinating insects could be predicted according to the pollination syndrome such as hoverflies and butterflies (Lunau and Maier 1995). hypothesis. Thus, it seems that the predominance of pol- There have been previous attempts to document the linator types (and subsequently the main foraging strategies effects of altitude on flower colours present (see Totland in evidence) varies with elevation and could potentially et al. (2000) for a summary)—Weevers (1952) observed have strong effects on which flower species are most that there were more blue flower species in upland areas abundant. than in lowland areas (both in Switzerland above 1,100 m In our study we consider flower colours as seen by their and Java above 1,500 m), and Kevan (1972) and Savile pollinators, firstly using the well-studied model of bee (1972) observed that flowers in alpine areas and arctic colour vision, secondly using a model of fly colour vision, regions (which are climatically similar to alpine areas) and also using the raw reflectance spectra of the flowers, 123 Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators 29 flowers, when growing at particular elevations, to exhibit particular colours more often. Materials and methods Study sites and data collection The study site was located in the Dovrefjell–Sunndalsfjella National Park (formerly Dovrefjell National Park) in Norway, near to Oppdal. Data were collected in June 1992 in the altitude range 700–1,600 m a.s.l. (sub-alpine to high- alpine), using Kongsvoll Biological Station (62° 180N, 9° 360 E, 900 m above sea level) as a basis.