Translating research into action; bumblebee conservation as a case study

Abstract

Bumblebees belong to the genus Bombus, which comprises about 250 species, largely confined to the temperate Northern Hemisphere. They are wholly dependent on flowers for their energetic and developmental requirements. Most are social species, with nest sizes varying from 50 to 400 workers. As such, they have attracted considerable attention regarding their role as pollinators. There is a growing body of evidence that bumblebees have declined in Europe, North America and Asia in recent decades because of multiple causes probably including habitat loss, impacts of pesticides, competition from non-native species and the introduction of non-native diseases (Goulson, Lye & Darvill 2008a; Williams & Osborne 2009). Recent health problems affecting honeybees and a perception that other pollinators may be declining has led to serious concern that we might be facing a global ‘pollination crisis’ affecting pollination of crops and wildflowers (e.g. Aizen & Harder 2009). The global value of crop pollination by bumblebees is unknown; Gallai et al. (2009) estimate that for the EU25 countries in 2005, the value of insect pollination of agricultural crops was €14·2 billion, with a large (but unquantified) proportion of this coming from bumblebees. Most crop pollination delivered by bumblebees is because of a handful of common species, so that from an economic viewpoint there may be no need to conserve a diversity of bumblebee species. However, bumblebees also provide pollination services to natural ecosystems, with numerous wild plant species largely or entirely dependent on bumblebees for pollination. As bumblebee species each occupy distinct (albeit often overlapping) niches with regard to their patterns of floral visitation (e.g. Goulson, Lye & Darvill 2008b), it is probable that many bumblebee species are needed to maintain functionality of natural ecosystems (Williams & Osborne 2009). Bumblebee nests also support a diversity of parasitic and commensal organisms. For these reasons, it can be argued that bumblebees are ‘keystone species’, upon which the survival of many other organisms depend (Goulson, Lye & Darvill 2008a). Perhaps as a result of perceived declines, academic interest in bumblebees has risen markedly in recent decades. This can be simply illustrated by plotting the number of papers in Thomson’s ISI Web of Knowledge which have Bombus in the abstract or key words (Fig. 1). Over the last 20 years the number of papers published per year has grown steadily from 12 to 144, a 12-fold increase (for comparison, studies concerning two other pollinator groups, Lepidoptera or Syrphidae, have each increased by a factors of c. 2·5 over the same period, Fig. 1). The studies of bumblebees encompass diverse topics from ‘pure’ research of, for example, social structure, foraging behaviour, population genetics, pheromones and navigation, to applied studies addressing how particular land management methods influence bumblebee numbers. There is no doubt that we understand far more about the biology of bumblebees than we once did, although there remains much more to learn (for example mating behaviour of many species has rarely been seen, and because natural nests are hard to find we know little about the factors affecting their survival and success). The number of publications in Thomson’s ISI Web of Knowledge which have Bombus, Lepidoptera or Syrphidae in the abstract, key words or title, plotted against year of publication. Numbers for Lepidoptera are divided by 10 for ease of comparison. Recent papers on bumblebees (and many grant applications) often start by summarizing evidence for bumblebee declines, the implication being that the research may contribute to our understanding of the causes of decline and so help us to reverse them. However, publishing a paper, no matter how good the science may be, does not in itself improve the fortunes of a single bumblebee. It is only when the research reaches the right audiences and is translated into practical action that it makes any difference. Very few farmers, gardeners, politicians or nature reserve wardens sit down of an evening to read a scientific journal, nor should we expect them to. If they did, they might struggle to make sense of most of it. Academics must take some of the blame for this situation; many researchers make little effort to communicate their work beyond the traditional use of scientific journals, publications which are all but incomprehensible to the layman. This in turn is largely because the traditional criteria used for judging academic success (publications and grant income) pay little attention to the impact of the research. In some areas of science the breakdown of communication between scientists and the public may not be too disastrous, but in conservation this matters profoundly, because if conservation research is not communicated to those who might implement it, then the research effort (and funds) were wasted. Yet there remains a yawning gulf between the research consensus and practical on-the-ground habitat management, and it is not clear whose job it is to bridge this gap. This applies both at the level of rare species conservation (arguably the territory of conservation NGOs) and at the more basic level of maintaining healthy pollinator populations. The Bumblebee Conservation Trust (BBCT, http://www.bumblebeeconservation.org) was founded in the UK in 2006 by academics (Goulson & Darvill), with the specific aim of linking science and practice by translating our growing understanding of bumblebee ecology into well-informed practical conservation measures, which would halt and hopefully reverse declines in bumblebee populations. It provides an example of one possible route by which conservation research can usefully feed directly into on-the-ground conservation. We discuss, in turn: What recent research has revealed about the conservation needs of bumblebees; how this has fed into the strategy of BBCT; current knowledge gaps with regard to bumblebee ecology of relevance to conservation; and barriers facing the more widespread implementation of research in conservation. Six key points have emerged in recent years: Population size. Recent studies have demonstrated that the social nature of bumblebees renders them particularly sensitive to habitat fragmentation. Their effective population size is c. 1·5 times the number of successful nests, for each nest contains just one breeding female and the sperm she has stored from a (single) haploid male. Although some species remain widespread and hence have large populations, others thrive only in areas containing high densities of their favourite forage plants. Because of habitat loss, mainly attributable to agricultural intensification, these flower-rich areas are now often small and fragmented. Most nature reserves in the UK might only support a handful of nests of a rare bumblebee species, and are thus far too small to support viable populations. For example, Ellis et al. (2006) estimated that surviving UK populations of the rare Bombus sylvarum contained between 26 and 48 nests, and that the remaining populations are isolated from one another. Such tiny populations are unlikely to be viable in the long term, and it seems likely that a breakdown of metapopulation structure has already led to the UK extinction of B. subterraneus (Goulson, Lye & Darvill 2008a). Genetic studies have demonstrated that the rarer species such as B. sylvarum, B. muscorum and B. distinguendus are genetically depauperate compared to more common species (e.g. Ellis et al. 2006). There is a real risk that surviving populations of rare species will disappear in the near future because of stochastic effects, inbreeding, or both. Dispersal abilities. Recent research has revealed marked differences in the dispersal ranges of the sexual stages of bumblebees, suggesting that some bumblebee groups such as the subgenus Pyrobombus (which includes B. pratorum, B. jonellus, B. hypnorum and B. monticola) may have relatively high dispersal abilities. In contrast the Thoracobombus group seem to be relatively sedentary (e.g. Darvill et al. 2010); this group includes B. pascuorum, B. sylvarum, B. humilis, B. rudararius and B. muscorum, of which all but B. pascuorum have undergone marked declines. Differences in dispersal ability dictate the scale of habitat fragmentation which an individual species can withstand. Foraging range. The foraging range of worker bees determines the area which a nest can exploit. It is hard to quantify, and there have been many attempts, but it seems highly likely that there are important differences between species, with foraging ranges varying from c. 400 m to 1·5 km (e.g. Osborne et al. 2008a). Species with long foraging ranges such as B. terrestris will be able to cope with more patchy availability of floral resources than those with shorter foraging ranges (thought to include B. pascuorum, B. muscorum and B. sylvarum). Bumblebees do not store large quantities of nectar or pollen which means temporal and spatial patchiness in local forage availability is more difficult for species with short foraging ranges to withstand. Forage use. Studies suggest that bumblebees do not require a high floral diversity to survive (e.g. Carvell et al. 2007). There is high dietary overlap between species, but most bumblebee species could be catered for throughout most of the season by providing a plentiful supply of 10 or fewer suitable plants. Fabaceae appear to be very important in providing protein-rich pollen for bumblebees, and it is likely that the large scale loss of species-rich grasslands and clover leys (habitats characterized by high densities of Fabaceae) are primary drivers of bumblebee declines in Europe (Goulson, Lye & Darvill 2008a). Trifolium pratense and its close relatives appear to be particularly important sources of both nectar and pollen for many long-tongued bumblebee species such as B. distinguendus, the UK’s rarest species and a UK Biodiversity Action Plan priority species. Nevertheless, where available, bumblebees are known to forage from (and pollinate) a great diversity of flowering plants. Hence, bumblebees benefit from a diverse flora, and vice versa. The value of agri-environment schemes. Simple agri-environment scheme options are available in many EU countries and the USA; for example pollen and nectar strips in field margins can be very effective in providing forage for bumblebees in the UK (Carvell et al. 2007). Schemes promoting the restoration and creation of species-rich grasslands also have the potential to greatly benefit bumblebees. There is now a wealth of information on how best to establish and manage both short and long-term pollen and nectar strips or species-rich grasslands (e.g. Pywell et al. 2002; Carvell et al. 2007). However, even in non-competitive, entry-level schemes uptake of these options can be poor. In total only 6000 ha of pollen and nectar mix has been sown in England, which has a total area of over 13 million ha (0·05%). Farmland areas under agri-environment schemes but not incorporating these targeted options are often no better for bumblebees than conventional farmland (e.g. Lye et al. 2009), indicating the need for interventionist measures where these are not currently available. If food prices rise in the future, as seems probable, agri-environment schemes may become less attractive to farmers, and in Europe, future Rural Development Programme funding could have a significant impact on the menu of fundable measures. Urban areas. It has become clear that both gardens and brownfield sites in urban areas support higher densities of bumblebees and bumblebee nests than do typical farmed areas (Osborne et al. 2008b). In some cases these urban areas can also support rare and declining species (e.g. B. sylvarum and B. humilis in the Thames Estuary). Brownfield sites are often under threat as legislation prioritizes them for development. A number of practical messages have emerged from bumblebee research. From our growing knowledge of bumblebee population structure, it is clear that conservation measures need to focus on enhancing the size and connectivity of extant populations of the rare species, which otherwise are likely to go extinct one by one. Nature reserves are too small to support viable populations, so conservation measures need to target the wider countryside, i.e. farmland. Stepping-stone habitat is needed to link existing populations, and this is likely to be particularly critical for the more sedentary species. Studies of foraging range suggest that some species forage much further afield than others. For the species with shorter foraging ranges, nests will only survive if there are patches of suitable flowers available through the season within a c. 400 m radius of the nest. However, even for the less mobile species, patches of floral resources clearly need not be contiguous and could readily be incorporated into most farming systems as patches of flowers interspersed among much larger areas of crops. Suitable conservation measures include: (i) maintenance of flower-rich sites; (ii) restoration of species-rich grasslands; (iii) sowing pollen and nectar mixes; (iv) encouraging clover ley crops and a return to crop rotations as an alternative to the use of fertilizers; (v) promoting wildlife-friendly gardening. As bumblebees are found throughout the UK, these activities have some value wherever they take place; as a minimum they will help to boost populations of the common species. However, to conserve rare species and prevent further bumblebee extinctions, activities need to be targeted at appropriate sites close to or within areas where rare species persist. It is clearly not possible for a small NGO to buy and manage sufficient land to make any significant impact on bumblebee populations at a national scale, so the challenge is to persuade land owners and managers to change their practices. The key stakeholders here are farmers, local councils, gardeners, and those involved in the management of nature reserves, national parks and other protected areas. Land management can also be improved indirectly by influencing government policy. 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