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Nectar Properties of the Sunbird-Pollinated Plant Impatiens Sakeriana: a Comparison with Six Other Co-Flowering Species ⁎ M

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Nectar Properties of the Sunbird-Pollinated Plant Impatiens Sakeriana: a Comparison with Six Other Co-Flowering Species ⁎ M Available online at www.sciencedirect.com South African Journal of Botany 78 (2012) 63–74 www.elsevier.com/locate/sajb Nectar properties of the sunbird-pollinated plant Impatiens sakeriana: A comparison with six other co-flowering species ⁎ M. Bartoš a,b, , Š. Janeček b, E. Padyšáková a,b, E. Patáčová b, J. Altman a,b,M.Pešata b, J. Kantorová b, R. Tropek a,c a Faculty of Science, University of South Bohemia, Branišovská 31, CZ-370 05 České Budějovice, Czech Republic b Institute of Botany, Academy of Sciences of the Czech Republic, Dukelská 135, CZ-379 82 Třeboň, Czech Republic c Institute of Entomology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, CZ-370 05 České Budějovice, Czech Republic Received 20 December 2010; received in revised form 9 May 2011; accepted 11 May 2011 Abstract Adaptations of the nectar traits in bird-pollinated flowers are amongst the most discussed aspects of floral evolution. In the case of sunbird- pollinated plants, data on nectar traits originate almost exclusively from the South African region and are very scarce for tropical Africa, where paradoxically the highest sunbird diversity occurs. Here we present a study on the nectar properties of a sunbird-pollinated plant, Impatiens sakeriana, growing in the West African mountains, including the nectar production, diurnal changes in the nectar standing crop, the nectar concentrations, the nectar volumes, total sugar amounts and sugar composition. Moreover we compare the nectar traits of I. sakeriana with six other co-flowering insect-visited plant species. Our results showed that many nectar properties, including high volume (approx. 38 μL in flowers unvisited by sunbirds), low sugar concentration (approx. 30% w/w) and high sucrose content (95%), are specific to I. sakeriana, compared to the insect-visited plants. These are in accordance with the most recent theory that nectar properties of the sunbird-pollinated plants are similar to those pollinated by hummingbirds. © 2011 SAAB. Published by Elsevier B.V. All rights reserved. Keywords: Cameroon; Impatiens sakeriana; Nectar; Pollination; Sunbird 1. Introduction Plants pollinated by birds are expected to produce higher volumes of more diluted nectar than insect-pollinated plants Nectarivory in birds is a widespread phenomenon, especially (Bolten and Feinsinger, 1978; Nicolson and Fleming, 2003a; in the tropical and subtropical areas with long flowering Goldblatt and Manning, 2006). The higher nectar amount is seasons. It has been estimated that around 10% of all bird believed to be related to the high energetic requirements of the species may use nectar as a resource (Wolf and Gill, 1986). The birds (Heinrich, 1981). The function of low sugar concentration most famous nectar feeders in the New World are humming- in the bird-pollinated flowers is much more debatable. Two birds, representing the most specialised bird pollinators (Stiles, hypotheses have been offered to explain the low concentrations 1978; Arizmendi and Ornelas, 1990; Stiles and Freeman, 1993; in regard to the evolution of the most appropriate nectar Schuchmann, 1999). In the Old World the most specialised properties for the birds. Baker (1975) noticed that nectar with a nectarivorous birds are sugarbirds, flowerpeckers, sunbirds and low sugar concentration has also a low viscosity, which spiderhunters (Cheke et al., 2001). facilitates more efficient extraction from flowers. Calder (1979) suggested that the dilute nectars can support bird water requirements in warm to hot environments, but at the same time ⁎ Corresponding author at: Tel.: +420 384721156; fax: +420 384721136. he pointed to possible problems with excessive water input E-mail address: [email protected] (M. Bartoš). under lower temperatures. More recent studies show that just 0254-6299/$ - see front matter © 2011 SAAB. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.sajb.2011.05.015 64 M. Bartoš et al. / South African Journal of Botany 78 (2012) 63–74 the excess water from dilute nectars represents the prevailing evaporation (Plowright, 1987). Pyke and Waser (1981) speculated osmoregulatory challenge to nectar-feeding birds. As a on the hypothesis that nectar properties evolved to affect pollinator consequence, the potential advantages related with more diluted foraging behaviour. nectars of bird-pollinated plants are debatable (Martinez del Rio The relation of the nectar sugar composition to the pollinator et al., 2001). The daily water intake of birds feeding on dilute class has also been repeatedly questioned (e.g. Galetto and nectar can be several times higher than their body weight Bernardello, 2004; Chalcoff et al., 2006; Wolff, 2006; Schmidt- (McWhorter and Martinez del Rio, 1999; Lotz and Nicolson, Lebuhn et al., 2007). A long-standing paradigm has been that 1999). The nectar-feeding birds are well adapted for elimination hummingbirds and passerine birds differ in preferences of of surplus water. A South American hummingbird, Sephanoides nectar sugar composition in the plants pollinated by them. sephanoides, can regulate the redundant water by decreasing Hummingbirds were generally regarded as sucrose-dominant water reabsorption in its kidneys (Hartman Bakken and Sabat, nectar consumers in comparison with the Old World nectar- 2006). Another studied nectarivorous bird, the Palestine sunbird ivorous birds, which prefer hexose-dominant nectar (Bruneau, (Nectarinia osea), is moreover able to regulate intestinal water 1997; Baker et al., 1998; Nicolson and Fleming, 2003a; absorption (McWhorter et al., 2003; McWhorter et al., 2004). Schmidt-Lebuhn et al., 2007). The hypothesis on this The higher ability of the Whitebellied Sunbird (Nectarinia dichotomy is however controversial, as there are large groups talatala) to produce highly diluted cloacal fluid when feeding of sunbird-pollinated plants in the Old World which produce on a dilute sucrose solution was manifested by Fleming and sucrose-rich nectar (Vos et al., 1994; Barnes et al., 1995). The Nicolson (2003). Besides avoiding over-hydration during the broader synthesis of Nicolson and Fleming (2003a) showed that feeding on more diluted nectars, the nectar-feeding birds face the passerine-pollinated plants embody a bimodal pattern with a dehydration during times of fasting (naturally during the night) high number of plants with high sucrose content and many (Hartman Bakken et al., 2004; Hartman Bakken and Sabat, species with hexose-rich nectar. Moreover, the dichotomy was 2006; Fleming et al., 2004a). Different bird groups solve this also put into doubt by several experimental studies showing that dilemma in different ways: whereas sunbirds are able to produce the specialised Old World passerines are able to absorb sucrose concentrated cloacal fluid (Fleming and Nicolson, 2003), effectively (Lotz and Nicolson, 1996; Downs, 1997; Jackson hummingbirds conserve water balance only by remarkable et al., 1998) and did not prefer hexoses (or in extremely diluted reduction of their glomerular filtration rate (Hartman Bakken solutions only) using equicaloric (Fleming et al., 2004b; Brown et al., 2004; Hartman Bakken and Sabat, 2006). Dehydration et al., 2008) or equiweight (Lotz and Nicolson, 1996; Brown during the day activity is rather improbable as the birds can et al., 2008) solutions. Recently, Johnson and Nicolson (2008) consume supplementary water (Nicolson and Fleming, 2003b). have proclaimed this dichotomy as false, and suggested a more Nevertheless the plants produce nectar to increase their fitness useful distinction between specialised (i.e. including just and not to satisfy altruistically birds' requirements (Pyke, 1981; hummingbirds or sunbirds) and generalised (i.e. including Pyke and Waser, 1981; Martinez del Rio et al., 2001). In bulbuls, weavers, orioles and others) bird pollination systems. consequence, we need to consider the nectar properties as a Moreover, recent experiments show that the generalist avian compromise between plant and bird concerns. This could be the nectarivores prefer hexose solutions of concentrations similar as reason why the plants specialised to opportunistic nectarivores those found in the plants adapted to these birds (Fleming et al., produce relatively less concentrated nectar (8–12%) than plants 2008; Odendaal et al., 2010; Brown et al., 2010a,b). specialised to specialist nectarivores (15–25%), as they need to The theories on the nectar properties of the Old World plants satisfy the highly different requirements of their pollinators pollinated by specialised sunbirds can be nevertheless strongly (Johnson and Nicolson, 2008; Botes et al., 2008; Symes et al., affected by unbalanced geographical data acquisition. In most 2008; Brown et al., 2010a,b; Odendaal et al., 2010; Symes et al., of the synthesising studies the data predominates from the South 2010). On the other hand, it has been shown that plants pollinated African region (Baker et al., 1998; Johnson and Nicolson, by specialised birds produce a bit more diluted nectar than 2008), which represents just a marginal area of sunbird expected from the birds' preferences (Tamm and Gass, 1986; distribution (Cheke et al., 2001). Only a few studies have Roberts, 1996; Blem et al., 1997; Blem et al., 2000; Johnson et al., been done on the plant nectar properties in tropical Africa (Vos 2006). This disproportion can be explained considering that a et al., 1994; Burd, 1995; Evans, 1996; Johnson and Brown, different force other than ornithocentricity can modify the 2004; Ley and Claßen-Bockhoff,
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