This study used data on three plant species, at five field sites, to construct visitation and pollen transport webs, which provide a quantitative community-level approach to understanding the pollinator requirements of rare plant species. We found that spatial variation appears to be greater than temporal variation. The implications of this work for the conservation of these species, for rare plants in general and for the study of plant–pollinator communities are discussed below, along with the limitations of our approach.
The interaction-based approach used in this study has provided information about the pollinator requirements of rare plants that would be extremely difficult to gather using other methods. As predicted, the rare plants share pollinators with more common species, making their survival at least in part dependent on those species. This pattern is seen in all five of the communities sampled, despite large differences in plant and insect abundance and diversity between sites (Figs 1–4). Furthermore, our data show that neither the most abundant visitors nor pollen carriers of a rare plant, nor the species carrying the largest quantities of the plant species’ pollen, are necessarily its most important pollinators.
In agreement with previous studies on plant–pollinator networks (Bond 1994; Memmott 1999; Dicks 2002; Olesen & Jordano 2002), our results show that Galeopsis angustifolia, Silene gallica and Torilis arvensis are generalists with respect to pollination, and that their visitors also show a relatively high level of generalization. Pollen transport data reveal greater levels of generalization in plant–pollinator communities than suggested by the visitation data alone. For example, Silene gallica only had nine observed visitor species but 11 species carried its pollen. Equally, not all visitors carry pollen. For example only four of 22 visitors to Galeopsis angustifolia at GA1, and three of nine at GA2, actually carried any Galeopsis angustifolia pollen.
The most accurate method for determining which species are the most effective pollinators of each rare plant species would be to conduct bagging experiments (Klein, Steffan-Dewenter & Tscharntke 2003), allowing access by specific insect species, and excluding all others right up to seed set. However, this was not practical at our field sites, as each of the rare plants was visited by numerous insect species (some up to 25 species), making the experimental exclusion of each species impossible. Instead a probabilistic method was used, with limitations such as the necessary assumption that pollen fidelity and relative abundance are equally influential on a pollinator's overall efficiency, and are not influenced by each other.
Plants may interact via shared pollinators in negative as well as positive ways. Competition between plant species via pollinators can occur, for example through improper pollen transfer resulting in pollen loss by the donor and stigma clogging, exploitation, or chemical or physical interference by pollen, all of which can lower seed set in the recipient (Feinsinger 1978; Waser 1978), or simply through competition for pollinator visitation (Rathcke 1983). However, there is evidence to suggest that sequentially flowering species that compete for pollination can simultaneously facilitate each other's pollination by providing the resources necessary for the survival of adequate numbers of pollinators throughout the year, in a form of ‘effective mutualism’ (Waser & Real 1979), supporting our assumption that the more abundant plant species facilitate the pollination of the rarer plants in their communities. Indeed, seed set may increase even if there is competition for visitation by pollinators (i.e. a reduction in visitation rates), as long as the quality of each visit is high (Rathcke 1983).
Relatively small numbers of insects were used to calculate PI values for some of the insect species (Table 2). This problem was unavoidable because with such large-scale studies there is an inevitable trade-off between the number of sites and species sampled, and the sampling intensity at each site.
Our method effectively shortens the list of potential pollinators and gives us a fair indication of the species pollinating each plant species. It is on this basis that we provide the management recommendations outlined below for the particular study sites as examples of a more general approach to the management of rare plants.
Galeopsis angustifolia appears to rely very heavily on Bombus pascuorum for pollination at GA1 and therefore this relationship should be considered essential for the maintenance of this population of Galeopsis angustifolia. The only other plant used with any frequency by Bombus pascuorum at GA1 is Odontites vernus (55% of the pollen on Bombus pascuorum was probably from this species). The early death by mildew of all Galeopsis angustifolia in the plot (Table 1), which thus eliminated the main source of food for Bombus pascuorum, emphasizes the importance of maintaining Odontites vernus as a resource for Bombus pascuorum during periods when Galeopsis angustifolia is not in flower. To conserve Bombus pascuorum (and thereby Galeopsis angustifolia) at this site, Odontites vernus should be encouraged and protected as far as practically possible. There are few data on the foraging ranges of bumblebees (Osborne et al. 1999), although it is known that some individuals forage over distances of up to 2 km (Walther-Hellwig & Frankl 2000). However, Bombus pascuorum appears to prefer resources closer to the nest, if they are available (Kreyer et al. 2004), and is thought to stay mainly within 500 m of the nest (Walther-Hellwig & Frankl 2000).
The most important pollinator of Galeopsis angustifolia at GA2 is probably the syrphid Sphaerophoria scripta. Web data show that Sphaerophoria scripta visits and carries pollen of one or both Senecio (Asteraceae) species (Senecio viscosus and Senecio jacobaea) at the site. We recommend therefore that efforts be made to conserve these plant species. Galeopsis angustifolia appears to have an extremely low level of pollen transport at GA2. Considering the increased risks of extinction through reduced pollinator visitation for small populations of plants (Spira 2001), the planting of ex-situ propagated plants from seeds collected at the site to increase the current population size should be considered in the management of Galeopsis angustifolia at this site.
For Silene gallica, management plans should incorporate measures to ensure the maintenance of Sphaerophoria scripta. Sphaerophoria scripta appears to feed on a wide variety of plant species, including Hypericum pulchrum, and therefore we suggest that the population of this plant be maintained at this site. Interestingly, no species other than Sphaerophoria scripta visits this plant species or carries its pollen at site SG, so it is vital not only for Silene gallica but also for Hypericum pulchrum that the importance of Sphaerophoria scripta as a pollinator at this site is recognized and acted upon.
Chloromyia formosa may be of particular importance in the pollination of Torilis arvensis at TA1 because of its apparent specialization on the flowers of this species. If so, Torilis arvensis must be maintained in high numbers at this site in order to provide sufficient resources to support an adequate population of Chloromyia formosa. Chloromyia formosa is specialized for feeding on Torilis arvensis according to criteria defined by Reed (1995), who suggested that to be considered specialized for feeding on a particular plant, an insect must be caught more than eight times on the same plant species at the same site. The cut-off point of eight times helps to avoid confusing low abundance with specialization, and we consider it a useful, if slightly arbitrary, measure of specialization.
Some of the other most frequent visitors to Torilis arvensis at TA1 also visit Sinapis arvensis and Epilobium tetragonum frequently, and so these plant species should be considered an important resource for potential pollinators of Torilis arvensis. We recommend therefore that Sinapis arvensis and Epilobium tetragonum be protected and maintained at this site, and planted alongside Torilis arvensis at any new sites. However, given the wide range of plants visited by the potential pollinators of Torilis arvensis, it would be advisable to manage the site to maintain the diversity of plant species currently present.
At site TA2 Chloromyia formosa was caught on Euphorbia exigua (Euphorbiaceae) and so is not a true specialist at a national scale. This result emphasizes the value of replicating the study of the pollination of rare plants in geographically separate populations. However, this local specialization of Chloromyia formosa on Torilis arvensis could be important in terms of pollination, as it could result in high levels of pollen fidelity in calculating PI values for this insect species.
Torilis arvensis was not visited frequently at TA2, and so it is particularly important that the plant species supporting the insect populations are at least maintained, and ideally increased. The seemingly low visitation rate at this site is probably partly the result of the reduced sampling effort at this site (which was the result of the harvesting of the crop; Table 1), but even allowing for this, insect abundance at this site seems low. The potential pollinators of Torilis arvensis at TA2 utilize a wide range of plant species, and it is therefore recommended that this site is managed for as diverse an assemblage of plant species as possible, preferably containing Lapsana communis, Rubus fruticosus agg. and Medicago lupulina, as these are the three most generalized plant species and therefore provide resources for potential pollinators of many of the plant species at the site.
Our limited data suggest that the pollinator fauna of rare plants can vary considerably across their geographical range, while showing far less variation at a given site from 1 year to the next. While the small number of field sites studied for the rare plant species limits the extent to which generalized statements can be made regarding their pollinator fauna, given the substantial spatial variation found in these systems it is clear that measures aimed at conservation of the pollinators of these plants should be tailored to each community in which they are found rather than based on assumptions of their similarity between sites.
The data we present on the plants and pollinators at each field site are not exhaustive surveys of the species present, nor are they intended to be; rather, they are quantitative samples of the community context in which the interactions between rare plants and their pollinators take place. This approach has allowed us to identify the probable key pollinators of rare plant species, and to make specific recommendations for management of the plant–pollinator communities in which they are found. Interestingly, our three arable sites (GA1, TA1 and TA2) had higher numbers of both plants and insects (both species and abundance) than the two non-arable sites (GA2 and SG). This can be seen clearly by comparing the size of the visitation webs (Figs 1–4), which are drawn to the same scale, showing that agro-ecosystems can be important for the conservation of biodiversity.
Our results and management recommendations can play a vital part in protecting rare plant species, but we are also aware that the management of arable land for conservation can conflict with the growing of crops. For example, at site TA2 managers have found it hard to maintain the diversity of arable plants without sacrificing the success of their cereal crop (Marren 1999). There is hope, however, for the continued growth of arable weeds on some of Britain's farms, as a result of new agri-environment schemes (DEFRA 2005) that provide subsidies to farmers for employing environmentally beneficial practices such as wide, unsprayed field margins, beetle banks and less intensive hedgerow management. Indeed, arable plants are increasingly recognized as essential for maintaining farmland biodiversity (Altieri 1999; Marshall et al. 2003). The seeds of arable insect-pollinated species such as Stellaria media (Caryophyllaceae) and Sinapis arvensis (Brassicaceae) form a major part of the diet of most farmland bird species (Marshall et al. 2003), many of which are currently in decline (Siriwardena et al. 1998; Stephens et al. 2003; Butler, Bradbury & Whittingham 2005). Galeopsis spp. are also a component of farmland bird diets (Marshall et al. 2003). In turn, the insects that feed on arable plants, both herbivores and flower feeders, provide an important food source for the chicks of many of these bird species (Wilson et al. 1999). In addition, certain arable plants play an important role in maintaining complexes of beneficial insects, which provide invaluable services to farmers in limiting insect pest populations (Altieri 1999). The financial incentives of government agri-environment schemes, and the growing awareness among farmers of the ecosystem services that arable plants can provide, are important steps towards their protection. However, it is essential that we target each species’ specific ecological needs if we are to manage them effectively (Fox 2004). If future agricultural policies are devised with this in mind, using information on vital ecological interactions such as pollination, it may yet be possible for rare arable plants to flourish in the British countryside once again.