Do Queens of Bumblebee Species Differ in Their Choice of Flower Colour Morphs of Corydalis Cava (Fumariaceae)?
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Apidologie Original article * INRA, DIB and Springer-Verlag France, 2014. This article is published with open access at Springerlink.com DOI: 10.1007/s13592-014-0326-x Do queens of bumblebee species differ in their choice of flower colour morphs of Corydalis cava (Fumariaceae)? Łukasz MYCZKO, Weronika BANASZAK-CIBICKA, Tim H. SPARKS, Piotr TRYJANOWSKI Institute of Zoology, Poznań University of Life Sciences, Wojska Polskiego 71C, 60-625, Poznań, Poland Received 6 June 2014 – Revised 18 September 2014 – Accepted 6 October 2014 Abstract – Bumblebee queens require a continuous supply of flowering food plants from early spring for the successful development of annual colonies. Early in spring, Corydalis cava provides essential nectar and pollen resources and a choice of flower colour. In this paper, we examine flower colour choice (purple or white) in C. cava and verify the hypothesis that bumblebee queens differ in their choice of flower colour. A total of 10,615 observations of flower visits were made in spring 2011 and spring 2014 near Poznań, western Poland. Our results suggest that Bombus lucorum/cryptarum used purple flowers less, while Bombus terrestris used purple flowers more and Bombus hortorum showed no preference. Therefore, the colour morphs of C. cava are probably co- evolutionary adaptations to the development of another part of the insect community which has different colour preferences. Bombus lucorum / Bombus cryptarum / Bombus terrestris / Bombus hortorum / foraging behaviour / colour choice 1. INTRODUCTION (Wilson 1971; Oster and Wilson 1978). A strong selection is evident, partly caused by ergonomic Pollinators are often considered crucial species restrictions due to mismatching functional traits of in ecosystems (Williams and Osborne 2009; plants and insects (Wilson 1983). For the devel- Winfree 2010). Bumblebees pollinate a wide opment of their annual colonies, bumblebees re- range of plants in both agricultural and natural quire a continuous supply of flowering food plants habitats (e.g. Heinrich 2004; Goulson 2010; from early spring to late summer, as is usually Osgathorpe et al. 2012). They live in annual col- provided in perennial semi-natural habitats onies that are founded by single queens (Heinrich (Fussell and Corbet 1991;Corbet1995). 2004; Goulson et al. 2002). When a queen The melliferous flowers of the herb Corydalis emerges from hibernation in spring, she feeds on cava (L.) Schweigg and Koerte (Fumariaceae) pollen and nectar until her ovaries develop. She appear directly before tree foliation. They precede then tries to find a suitable nesting site. Early and supplement shrub and tree flowering, so can colony development is in fact a critical period be an important food supply for pollinators in characterised by a high rate of colony failure early spring. The complex flower morphology of the species indicates a co-evolution with Electronic supplementary material The online version of specialised pollinators (Fenster et al. 2004). The this article (doi:10.1007/s13592-014-0326-x) contains flowers have long and narrow corolla tubes and supplementary material, which is available to authorized require large-bodied, long-tongued bees for polli- users. nation. Anthophora plumipes (Pallas, 1772) Corresponding author: Ł. Myczko, (Hymenoptera: Apoidea: Apiformes) is a com- [email protected] mon pollinator of C. cava within the core of the Manuscript editor: James Nieh plant’s range, e.g. Austria, and its proboscis is Ł.Myczkoetal. long enough to reach the nectar legitimately. 1981), variability of nectar content (Real 1981; Queens of the long-tongued Bombus hortorum Real et al. 1982), or the effects of density on (L.) are also common pollinators within the pollinator preferences for colour morphs plant’s central range. This species forages legiti- (Smithson and Macnair 1997). Previous studies mately both for nectar and pollen (Olesen and have mainly focused only on a single bee species. Knudsen 1994). Populations of C. cava at the Nevertheless, reality is more complicated because margins of the species range exist without their plants are pollinated by the whole pollinator com- principal evolutionary pollinators but persist munity. What is interesting is the pollinator-plant through an interaction with local opportunistic relationship, especially in early spring when there flower foragers, including bees and butterflies are limited food resources. In this paper, we ex- (Olesen 1992, 1996; Olesen and Knudsen 1994). amine the pollinator community of C. cava .The However, the flowers are visited mainly by freely purpose of our study was to verify the hypothesis foraging bumblebee queens. C. cava has two that bumblebee queens differ in choice of flower colour morphs (at least as recognised by humans): colour morphs of C. cava. purple and white. It is a well-known fact that flower colour is an 2. MATERIAL AND METHODS important signal to pollinators and might influ- ence pollinator behaviour (e.g. Waser and Price 2.1. Study organisms 1983; Welsford and Johnson 2012; Schiestl and Johnson 2013). When pollinators discriminate C. cava is a perennial spring forest herb with a among colours, this may influence patterns of complex flower. The plant grows in central and south- pollen transfer, and thus gene flow and evolution- ern Europe and has either purple or white flowered ary dynamics, within and between species individuals (see Supplementary Material). The terms (Hopkins and Rausher 2012). It is often assumed “purple” and “white” refer to human colour space. that many flowering plants owe much of their According to Olesen and Knudsen (1994), ultraviolet floral polymorphism in colour, shape and odour reflection from flower parts, nectar production, pollen to the combined effects of attracting different pol- traits and scent chemistry do not differ between the two linator species and to the spatio-temporal variation morphs. in the selection regimes they are subjected to Although the colour morphs co-occur throughout the (Ollerton et al. 2006). Many species of bumble- range of the species, their frequencies vary. The fre- bees have been shown to discriminate on the basis quency of white among populations ranges between 5 of floral colour (e.g. Waser and Price 1981, 1983; and 40 %, and within individual populations, white is Lunau 1991; Lunau et al. 1996). Colour appears often aggregated (Olesen and Knudsen 1994). to be particularly important for flower recognition Precocious flowering melliferous plants are of special (Menzel and Schmidta 1993;Schiestland importance, appearing directly before tree foliation. Johnson 2013). Both honeybees and bumblebees They precede and supplement shrub and tree flowering learn colours quickly when they are rewarded and are an important food supply for early spring bees. according to colour choice (Heinrich et al. 1977; The subgenus Bombus s. str. (syn. Terrestribombus ) Gumbert 2000;Ingsetal.2009). Recent work has includes four species (Bombus terrestris , Bombus also indicated that the strength of innate colour lucorum , Bombus cryptarum and Bombus magnus ), preferences can influence foraging performance in with an additional fifth species in Fennoscandia bumblebees under natural conditions (Raine and (Bombus sporadicus ). It is a group in which the classi- Chittka 2007). Intraspecific pollinator discrimina- fication of species is especially complicated (Bertsch tion may influence genotypic frequencies as well et al. 2004). The lucorum complex from central and as the reproductive success of colour morphs in northern Europe comprises three monophyletic bumble- plants. beetaxa(B. cryptarum , B. lucorum and B. magnus ), of There have been studies focusing on bumble- which B. lucorum is the most common of the lucorum bee preferences for colour morphs where morphs complex in Poland (Banaszak and Rasmont 1994). differ in nectar content (Heinrich et al. 1977;Real Because of the difficulty in separating the lucorum Bumblebee species and flower colour morph complex in the field even with freshly caught queens 2.3. Statistical analysis (e.g. in Scotland, Bertsch et al. 2005), we divided cap- tured bumblebees from subgenus Bombus s. str. into For each individual insect, the number and percentage B. terrestris and a second group of B. lucorum and of its visits to purple flowers were calculated. From each B. cryptarum . percentage, the appropriate site/year mean percentage of B. lucorum , B. cryptarum , B. terrestris , purple flowers was subtracted. This new variable, here- B. pratorum and B. lapidarius are short-tongued bum- after “colour bias”, indicates colour preference relative to blebees (Pekkarinen 1979). On C. cava ,thesespecies the site/year mean with positive values indicating more behave as nectar robbers, biting a hole in the back of the visits to purple flowers than expected and negative values corolla and inserting their proboscis through the hole to indicating more visits to white flowers. The colour bias collect nectar. C. cava is nectar robbed but also polli- for each species was compared to zero using one-sample nated by these short-tongued bumblebee queens t tests. Sparsely recorded species were not analysed. (Olesen and Knudsen 1994; Olesen 1996). A long- Differences between the three main species in colour bias tongued bumblebee, B. hortorum , entered flowers were examined using one-way ANOVA. through the front to collect nectar legitimately. The flower colour sequences of individual pollina- B. hortorum is widespread and abundant throughout tors were analysed