Declines in forage availability for bumblebees at a national scale
Introduction
Resource availability is often a critical factor in determining the distribution and abundance of species, and it is recognised that reductions in habitat quality as well as quantity are likely to cause population declines (Schultz and Dlugosch, 1999). Many social bumblebee (Bombus Latr.) species have undergone serious declines in recent decades across Europe and North America (Williams, 1982, Rasmont, 1988, Buchmann and Nabhan, 1996). Several factors have been suggested as possible contributors to these declines, including competition from the honeybee (Apis mellifera), changes in climate and the effects of predators and parasites (Williams, 1986). However, the principal factor is likely to have been the loss and degradation of habitats and critical food resources due to changes in land-use and agricultural practices (Goulson et al., 2005, Williams, 2005).
In Britain, as in other parts of Europe, the intensification of agricultural practices since the 1940s has resulted in the fragmentation, degradation and loss of semi-natural habitats (Robinson and Sutherland, 2002). For example, the area of unimproved lowland grassland in Britain is reported to have declined by over 90% between 1932 and 1984 (Fuller, 1987). Bumblebees forage for the colony as well as themselves, but only store several days’ worth of reserves, so therefore require an almost continuous supply of food resources (nectar and pollen) within foraging distance from the nest throughout the period of colony activity (Prŷs-Jones and Corbet, 1991). Flower-rich, extensively managed vegetation is therefore considered an essential component of the agricultural landscape for bumblebees, providing foraging resources as well as nesting, mating and hibernation sites (Banaszak, 1992, Williams, 1986).
Analyses of change in the distributional ranges of British bumblebees have highlighted the likely extent of declines during the 20th Century. By the 1980s, only six of Britain’s 19 Bombus species remained throughout their pre-1960 range (Williams, 1982). Three species are now considered to have become extinct, four (Bombus distinguendus, B. humilis, B. ruderatus and B. sylvarum) are currently on the UK Biodiversity Action Plan as priorities for conservation and others remain under threat (UK Biodiversity Group, 1998). This situation may threaten the pollination of many wild flowers and entomophilous crops (such as field bean, clover and various fruits) for which bumblebees are especially important (Corbet et al., 1991). They are therefore a key component of agricultural and semi-natural ecosystems that require urgent conservation.
The causes of rarity and decline among British bumblebees have recently been discussed by Goulson et al., 2005, Williams, 2005. They concluded that a combination of factors including a species’ proximity to the edge of its European range and degree of food-plant or habitat specialization are likely to determine its sensitivity to environmental change, but noted that further studies on the rarer bumblebee species are still required. While these ecological factors continue to be debated, evidence of specific changes in abundance of essential habitat components, namely forage plants which provide nectar and pollen resources, has been largely anecdotal or derived at local scales. At the scale of individual sites, there is a link between the abundance and diversity of bumblebees and that of their preferred forage plant species (Bäckman and Tiainen, 2002, Carvell, 2002). More specifically, the abundance of the most rewarding forage plants at a site seems to be more important for many bee species than overall flowering plant diversity (Williams, 1989). Rasmont (1988) suggested that the loss of Fabaceae, historically sown as fodder crops, from grassland systems in France and Belgium was the major driver of declines in the longer-tongued bumblebees. However, quantitative evidence for declines or increases in forage plant abundance at national scales and over relevant time periods is so far lacking. It is important to understand the extent and direction of these changes in order to design appropriate measures to conserve bumblebee populations.
Attempts to quantify large-scale changes in biodiversity are often hindered by the quality and availability of data on species distributions (Thomas et al., 2004). However, repeated and systematic surveys in Britain over the past 30–50 years have generated two datasets which allow national changes in range and abundance of vascular plant species to be assessed. The New Atlas of the British and Irish Flora can be used to study change in number of occupied 10-km squares between 1930–1969 and 1987–1999 (Preston et al., 2002). This spans the likely period of most serious decline in bumblebee species (Williams, 1982). At a more detailed scale, the Countryside Surveys of Britain recorded the changing presence of all vascular plant species in fixed plots within 259 1-km squares between 1978 and 1998 (Haines-Young et al., 2000). These changes in species frequency have been used to infer changes in plant abundance between the two survey periods (Smart et al., 2005). The Countryside Surveys are likely to have covered the later phase of the period of bumblebee declines, but offer the most useful measure of national scale change in habitat quality.
In this paper we collate a number of datasets documenting bumblebee visitation to specified plant species in Britain, to produce a list of important nectar and pollen sources. We analyse changes in range and frequency of these forage plant species to quantify changes in resource availability for bumblebees at a national scale. We also consider whether the magnitude of such changes may help to explain 20th Century declines in British bumblebees. The forage species list is not exhaustive, and does not include entomophilous crops or garden flowers, but represents the collective findings of available surveys which meet particular criteria. Furthermore, the analysis is restricted to native species and long-established aliens (archaeophytes) (Preston et al., 2004), both because the value of recently introduced plant species (neophytes) as forage plants is less well known, and because numerical estimates of the spread of invasive plant species are influenced to a greater degree than natives by changes in recording practice.
Section snippets
Collation of bumblebee forage plant data
A number of datasets containing information on bumblebee forage plant visitation across Britain were collated. Data from both published and unpublished studies were used but, in order to ensure consistency, the following criteria were applied.
- (a)
All studies presented data as the number of bumblebee visits to a specified list of flowering plant species from one site (where more than one site was sampled during a study, datasets were considered separately). Studies conducted in gardens alone were
Bumblebee forage plants and the ‘forage index’
A total of 145 plant species were identified as forage resources for bumblebees at the 14 study sites from which datasets were collated (Table 1). Of these species, 43% represented the Fabaceae (15%), Asteraceae (15%) and Lamiaceae (13%) and the majority were perennial or biennial. Plants with the highest overall forage index included Ballota nigra, Centaurea nigra, Teucrium scorodonia and Lamium album, though the latter two species were only visited by bees at one site. The long-tongued Bombus
Discussion
This study was designed to broadly quantify 20th Century changes in availability of forage resources for bumblebees at a national scale using the best available data. Overall, a large proportion of forage plants declined in both large-scale range and local-scale frequency between the two survey periods of the New Atlas and Countryside Survey (CS). These changes were of greater magnitude than changes in other native and long-established plant species, reflecting serious reductions in the quality
Acknowledgements
This work was funded by the Department for Environment, Food and Rural Affairs (BD1617) and Natural Environment Research Council. The authors thank all those who provided additional data on forage plant visitation, Tim Sparks for statistical advice and Matt Heard, Paul Williams and two anonymous referees for helpful comments on earlier versions of the manuscript.
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