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4.1 Introduction
In the previous chapter, the generalisation of the garden community suggested that flower visitors frequently exploit several plant taxa for the collection of floral rewards. This has been suggested to decrease their value as pollinators, as they may transfer higher quantities of heterospecific pollen between plants (Arceo-Gómez & Ashman, 2011). In this chapter, I measure the quantity and quality (diversity) of pollen from the bodies of flower visitors. These results reveal additional information about (i) flower visitor diet, and (ii) the potential value of these visitors as pollinators.
4.1.1 Visitor pollen loads provide a hidden history of flower visitation
Palynology (the study of pollen grains) is an important aspect of flower visitor interactions that surprisingly is often neglected from pollination studies. Quantitative analysis of pollen is of interest from both the plant and flower visitor perspective, because (i) it is the male gamete and its dispersal reflects male fitness, and (ii) it is offered as a protein- and lipid-rich reward to flower visitors. Either by active or passive collection, pollen grains adhere to the surface of flower visitors (particularly those that are very hairy) and may then be carried in the specialised structures present in bees (the corbicula, scopa or crop) and can remain on the body for several days (Courtney et al. 1982). From the perspective of flower visitors, pollen loads have been used to compare patterns in floral resource between species and over time (Kleijn & Raemakers 2008, Scheper et al. 2014, da Silva et al. 2017), the impact of introduced exotic plants (Lopezaraiza-Mikel et al. 2007, MacIvor et al. 2014) and in modelling flower visitor foraging behaviour (Marchand et al. 2015). Importantly, a palynological approach improves the resolution of flower visits in studies where observations are made to focal plants only, thereby increasing understanding of the importance of certain plant species (Bosch et al. 2009).
4.1.2 Pollen loads as a proxy for pollination
Previous studies have used the presence of conspecific pollen on a flower visitor as an indirect measure of pollination (e.g. Forup & Memmott 2005, Gibson et al. 2006), with the implicit assumption that greater pollen loads lead to more effective pollination. From the plant’s perspective, the size and heterogeneity of visitor pollen loads have been used to compare taxa in terms of their floral fidelity (Wilson et al. 2010, Rossi et al. 2015), the viability of the pollen carried (Rader et al. 2011) and, most importantly, to distinguish antagonistic from mutualistic visitors; for example Alarcón (2010) showed that many flower visitors carried no pollen, and were therefore deemed to be ‘cheaters’. Recently, pollen loads have been
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incorporated into flower visitation networks, so that the interactions represent total pollen transport (usually, a measure of pollen load x visit frequency). These studies have reported differences in the structure of pollen transport compared to visitation networks from communities in Mediterranean habitats (Bosch et al. 2009, Alarcón 2010), Arctic heathland (Olesen et al. 2011), arid grassland (Popic et al. 2013) and cloud forest (Ramírez-Burbano et al. 2017). Yet with the exception of Jędrzejewska-Szmek & Zych (2013) little is known about how pollen transport networks are structured in urban areas. Analysing the heterogeneity of pollen loads from the garden will shed light on the foraging preferences of visitors in communities where usually a large proportion of plants are exotics (Salisbury et al. 2015).
While pollen transport networks have become established as a more accurate measure of the value of flower visitors as pollinators, the effect on network specialisation has not been consistent between communities. In Alarcón (2010) and Popic et al. (2013), H2’ values
increased by up to 94% in the pollen transport network, while Bosch et al. (2009) and Ramírez- Burbano et al. (2017) reported a decline in specialisation. To fully understand the factors driving specialisation of plant-pollinator interactions, more pollen transport networks are needed in different habitats and across varied spatial and temporal scales. In light of global pollinator declines, it is important to understand whether the presence of pollen on the bodies of many flower visitor taxa represents functional redundancy or complementarity in terms of their role as pollinators. Furthermore, determining why the proportion of flower visitors that carry pollen varies between habitats will be a key aspect of future conservation efforts.
Using pollen transport as a proxy for pollination is not without limitations, and assuming that larger pollen loads equate to more effective pollination is problematic for two reasons. Firstly, not all of the pollen on an insect body will make it to the stigma as some is lost to the environment, groomed into specialised pollen carrying structures or used to provision nests between flower visits. Adler & Irwin (2006) found the quantity of Gelsemium sempervirens pollen on visitor bodies to be a poor predictor of that transferred to the stigma, while Larsson (2005) estimated that only 0.10% of all pollen removed from Knautia arvensis flowers was subsequently deposited on to stigmas, as many of the pollen-collecting solitary bees avoided flowers in the stigmatic phase. Secondly, some visitors may remove and transfer pollen at a high cost to the plant, so that their overall effect on plant fitness is negative when flower visitors with smaller pollen loads are present (Thomson & Goodell 2001, Lau & Galloway 2004).
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4.1.3 Downscaling from species to individuals in pollen load networks
In all networks, it is important to remember that each flower visitor node represents many individuals, with their own foraging preferences and behaviours. By recording visits made by individual Apis to Cirsium flower heads, Dupont et al. (2011) revealed that a small number of ‘scout’ bees visited many thistles, yet the majority of individual workers specialised on a much smaller number of flowers. Using a similar approach, Tur et al. (2013) analysed individual pollen loads from a diverse community of flower visitor taxa, and found downscaling substantially increased specialisation as many generalist species were composed of specialist individuals. What is not yet clear is whether this pattern holds true in gardens that are characterised by high and patchy floral diversity; to date, very little evidence has considered how planting in gardens should be shaped by the floral fidelity and opportunistic exploitation of floral resources by flower visitors. Although many plant varieties are recommended as ‘pollinator friendly’, it is unclear whether planting a larger diversity of plants in smaller patches is more beneficial than a reduced diversity in larger patches, and how this benefits different flower visitor taxa. From the plant’s perspective, high levels of individual specialisation are also likely to reduce heterospecific pollen transfer between flowers (Arceo-Gómez & Ashman 2011).
4.1.4 Flower visitor life history influences the quantity and quality of pollen loads
Using pollen load as a proxy for pollination implies that visitors carrying greater loads will be more effective pollinators. However, flower visitor life history is an important aspect of the quantity and quality of pollen carried, and shapes the structure of interactions in a network (Jordano et al. 2016); although many flower visitors feed on pollen, bees are the only insects that are entirely dependent on pollen as a source of protein for developing larvae (Thorp 2000). Consequently, most bees (>70% of species) are polylectic, actively collecting several species of pollen, and have evolved specialised structures for carrying pollen (Michener 2007). Pollen is usually collected on a pollen brush, located on the rear legs (e.g. Apis, Bombus and Halictidae) or beneath the abdomen (e.g. Megachilidae). Andrena species also collect pollen on the sides of the propodeum, while Hylaeus store pollen internally in their crops (Falk 2015). Although most bees collect dry pollen, Apis and Bombus can regurgitate nectar to moisten pollen so that it is stickier and easier to carry (Falk 2015). All these behaviours can greatly reduce the quantity of pollen reaching the stigma (Parker et al. 2015).
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In comparison to bees, Diptera do not actively collect pollen for brood provision, however many families do have hairs that trap pollen on their bodies, e.g. hoverflies in the tribe Eristalini (Ball & Morris 2013) and the non-syrphid Muscidae (Orford et al. 2015). Lepidopteran visitors are also covered in a fine brush of scales hairs, however very little pollen is normally found on the body (although see Epps et al. 2015) adhering instead to the proboscis and face (Courtney
et al. 1982). Therefore, while the pollen loads of non-bee visitors may be small in comparison,
these visitors could carry larger ‘free’ pollen loads that increase pollen deposition on to the stigma. However, the frequency of grooming and of flower visitation may be limiting factors.
4.1.5 Key questions
In this chapter I use pollen load and transport networks to examine the variation between flower visitors in the quantity and diversity of pollen carried. Evaluating pollination from the perspective of the male function of flowers, I ask: