Multifactorial Causes For Pollinator Decline Biology Essay

When one considers the term pollinator, the vast majority of people will picture a bee of some description; hymenopterans, specifically bees, are the chief pollinators of many large scale agricultural crops (Breeze et al. 2011); there are several favourable factors which single them out as proficient pollinators, these are both physiological and behavioural advantages. Physically, their hairy bodies facilitate the attachment of pollen to a greater degree than other insects; and their body size, structure and shape allow the bees to feed on, and collect pollen from many different plants (Williams 2002). This allows honeybees in particular to be large scale generalists (polylectic), feeding from many plants within their home range; bumblebees and solitary bees are also largely generalists, with a few specialist (oligolectic) species dispersed between both orders (Goulson and Darvill 2004; Biesmeijer et al. 2006).

Due to the significance of these species this review will focus, chiefly, on the plight of our agriculturally important hymenopteran pollinators, with particular focus paid to Apis mellifera and Bombus terrestris, as their ecological and economic contributions are many times greater than other pollinating species within the UK, and indeed the world. Despite the overall importance of many Bombus spp. the vast majority of research into them has been performed on the Buff-tailed bumble bee Bombus terrestris, in light of this, the rest of the information presented in this review will focus on this particular species from Bombus, but may be taken as an indicator for the genus as a whole.

2.4. Multifactorial causes for pollinator decline

Implicated in the decline of pollinator species, the world over, are a number of different causes ranging from parasitic infestations, such as Varroa destructor or Nosema ceranae (Rosenkranz et al. 2010; Pettis et al. 2012), to agricultural intensification and pesticide use (Thompson 2010; Cresswell 2011; Ricketts et al. 2008). Obviously for different species of bees there will be different circumstances leading to population decline; Apis mellifera, the European honey bee, is particularly affected by Colony Collapse Disorder and the Varroa destructor mite. Whereas bumble bees, Bombus spp. seem to be more susceptible to land use intensification and pesticide bioaccumulation (Thompson 2001; Cresswell et al. 2012). Indeed bees themselves can also be the root cause of the decline of related species, with the intrusion of non-native, foreign species leading to the decline of some native species in regions where they are imported for commercial applications (Ings et al. 2006).

3. Primary managed and wild pollinators in the United Kingdom

3.1. British pollinator diversity

If one were to consider the entirety of insects which actively pollinate flowering plants and dependent crops, there are several thousand species found within the UK, which all fertilise various plant species to a differing degree. These chiefly include Hymenopterans (honeybees, bumblebees and solitary bees); with smaller contributions coming from Lepidopterans (butterflies and moths), Dipterans (hoverflies), and Coleopterans (beetles). The contribution of species from outside of the Hymenopteran family cannot be overlooked, with 59 species of native and migratory butterflies Rhopalocera; more than 2,400 species of moth Heterocera; around 250 species of hoverfly Syrphidae (Kevan and Baker 1983); but very few Coleopterans contribute towards pollination in the UK. Of the few that do, the majority are specialists, such as soldier beetles Cantharidae, which pollinate sunflowers Helianthus annuus.

3.2. Hymenopteran pollinators

Behaviourally all three of our main, native types of bee show distinct and diverse pollination activities; for instance, the honeybee will embark upon long trips, during which it will limit its gathering behaviour to one specific species of flower. Bumble bee harvesting methods are similarly complex, incorporating scent marking and recognition to actively label, or avoid, flowers which have already been harvested(Goulson et al. 2000); this ensures that the bumble bee, which has a high metabolic rate, does not waste valuable energy reserves foraging from "used" flowers. They also demonstrate significant flight distances, with most bumble bee workers frequently achieving distances from the nest of anything from two to five kilometres(Goulson et al. 2002; Hagen et al. 2011), or further; with each of these foraging trips limited to one species of flowering plant.

Both Bombus spp. and Apis mellifera are obligate, social organisms; with the efforts of an individual contributing to a much greater, whole-colony interaction with the local environment. This "superorganism" can have significant beneficial effects in the ecosystem, and the losses of one or more of these colonies will clearly have significant negative effects on the immediate environment.

If one were to consider the pollination capacity of solitary bees, for example the red mason bee Osmia rufa, which is sufficiently capable of pollinating orchards and fruit crops, even in significantly reduced numbers compared to a single honey bee colony (Williams 2002). These bees are no doubt effective pollinators, within suitable settings, but due to their need for specialised nesting sites within close proximity to their foraging areas, they are rarely found on crop plants (Williams 2002); as such they are often limited, in commercial terms, to early flowering fruit crops which coincide with the bees comparatively short flying and foraging seasons (Williams 1996).

4. Pollination: an ecosystem service

4.1. Benefits of Pollination

Ecosystem services are defined as the beneficial goods and services that humanity derives, directly or indirectly, from natural ecosystem functions (Costanza et al. 1997); pollination is one such example of this, and is evidently one of the most vital ecosystem services that nature bestows upon mankind. Indeed 87 out of 115 globally important crops are heavily reliant upon insect pollination (Klein et al. 2007); this accounts for around one third of the world’s food crops (Richards 2001), chiefly the most commercially lucrative non-staple crops such as fruits (apples, pears etc.), nuts and crops for biofuels. The benefits, of insect pollination, range from simply increasing the yield and quality of products to an increase in genetic diversity (Hajjar et al. 2008; Breeze et al. 2011), ensuring that the crop species are significantly more diverse than monoculture, self-pollinating crops.

4.2. Current Knowledge

Despite pollination being generally recognised as one of the key supporting ecosystem services, there is a marked disparity between the levels of research committed to it from an agricultural perspective, and from an ecological standpoint (Dixon 2009). Essentially, Dixon implies that there is an increased emphasis on securing pollination services in agriculture, but a significant dearth of knowledge which can be applied to a natural, unfarmed ecosystem. This inequality has arisen chiefly through the increased prevalence of both Colony Collapse Disorder (Evans et al. 2009) and Varroa destructor infestation (Rosenkranz et al. 2010), in farmed colonies of the European honeybee Apis mellifera. The significant and rapid decline of these managed populations has prompted substantial efforts to understand and hopefully counteract the issues at hand. Unfortunately, this had led to the disparity which Dixon (2009) refers to, with vast amounts of research focused on the domesticated species, and fewer studies committed to understanding wild bees.

4.3. Managed pollinators

In essence both wild pollinators, in sufficient numbers, and managed species of bees are equally capable of pollinating crops to a desirable level. Supplementary pollination of crops by wild pollinators may be adequate in smaller farming environments, such as rural smallholdings and farms (Belfrage et al. 2005; Kasina et al. 2009); however larger monoculture-based plantations, such as those found in the USA, require the application of managed pollination (Gill 1990). Gill goes on to state that managed hives are also employed, to great effect, in areas where the natural pollinator population is insufficient or non-existent. Pollination in general has a positive effect on the economic value of crops; studies conducted on a smallholding in Kenya demonstrated that 40% of the net value of crops was down to incidental pollination (Kasina et al. 2009). In regions, or plantations, where managed pollinators are actively sought to either supplement incidental pollination, or provide a singular source of pollination, they contribute vastly to the economy; in the USA alone the annual benefits to the economy are estimated at $1.6 billion for incidental pollination benefits and $8.3 billion for single pollination species (ESA 2013). However, any monetary values applied to these services must be done so cautiously due to the fluctuating nature of the local and global economy.

4.4. Importance of wild pollination services within the United Kingdom

Previous studies have identified benefits to crop yield associated with wild pollinators, indeed within the UK it has been observed that despite a decrease in farmed A. mellifera colonies by 54% in the years from 1985 to 2005, there had been an overall increase of insect pollinated crop yields by ~54% since 1984 (Breeze et al. 2011). Breeze et al. tentatively suggest that the maximal pollination due to managed honeybee colonies could be as low as 11.7% of the total annual yield. Various factors must be accounted for when considering this figure as only around 2% of managed colonies within the UK are actively bred for pollination services (Breeze et al., 2011), with the vast majority of British beekeepers working in an amateur capacity, or solely focusing on honey production. Therefore it is reasonable to assume that the stated figure could, in reality, be much lower. The vast majority of the remaining 88.3% of annual yield of insect pollinated crops can therefore be cautiously attributed to wild pollinator species, which goes some way to indicate the significance of these often overlooked, and currently threatened, creatures.

4.5. Conflicting views

Arguments have been brought forward (Allsopp et al. 2008), stating that the fears over global food security are unfounded, with the vast majority of staple food crops (two thirds of global food production) being wind-, or self-pollinated and thereby having no relationship with the state of pollinator species (Ghazoul 2005). Food derived from pollinated crops allows the supplementation of the human diet with much more than just staple sustenance; pollinated crops are also utilised as fodder, for the dairy and livestock industries (Richards 2001), providing humanity with the means to produce vast amounts of meat and dairy produce to supplement our diets with many vital vitamins and minerals. Therefore, it may be true to an extent that the current fears of global food shortages are being exaggerated, but without the supplementary foods provided directly and indirectly by pollination, the human diet would be far less nutritious.

5. Pesticides: Agricultural aide or ecological inhibitor?

5.1. The application of pesticides within the UK

5.1.1 Plant protection products

DEFRA classifies any pesticides with agricultural applications as "plant protection products", and as these compounds are applied to food crops they are strictly regulated (DEFRA 2011). There are a multitude of diverse classes of pesticides currently under strict licence within the UK; these can broadly be divided into different categories by their purposes within the agricultural environment, and further by their specific action. The three primary forms of pesticide used globally are insecticides (44% of annual global pesticide consumption), herbicides (30%), and fungicides (21%), with other forms of pesticide accounting for the remaining 5% (Aktar et al. 2009). Within the United Kingdom the distribution of pesticide consumption is somewhat different, with fungicides covering 38% of total pesticide treated agricultural land, 30% covered by herbicides, and 9% covered by insecticides; the rest of the treated land is covered by chemical compounds ("other" in Figure 5.1.) mainly includes measures used to control "slugs and potato cyst nematode" (Hillocks 2012).

Figure 5.1. A comparative view of the consumption of different pesticide classes, as a percentage of the total usage per annum (Aktar et al. 2009; Hillocks 2012)

5.1.2 Main pesticides in British agriculture

Herbicides and fungicides are the most widely used pesticides within the UK, covering 68% of treated arable land; the most common crop on treated land is wheat Triticum aestivum with an average coverage of 58% (Hillocks 2012), therefore the most widely used herbicides and fungicides are aimed at pests and weeds found within wheat fields, and indeed cereal crops, which occupied 70.66% of all arable farmland in the UK in 2010 (AgriStats 2010). In general, farming practices commonly involve higher levels of crop spraying in the autumn than in the spring, and individual crops can typically be sprayed with several or more different chemical compounds (Thomas et al. 1996; Robinson and Sutherland 2002).

5.2 Variable effects of pesticides on pollinators

5.2.1Herbicides & Fungicides

Several herbicides find particular use in the British farmland environment, for example Topik®, with its active ingredient clodinafop-propargyl, is used to control the major problem of Black-grass Alopecurus myosuroides in cereal fields (produced by Syngenta AG). Most herbicides in use today pose very little threat to native pollinators, with only a few recorded incidences of bee poisoning linked directly to herbicides, such as paraquat (Greig-Smith et al. 1994). The effects of herbicides on bees; both A.mellifera and Bombus species, can be more nuanced and subtle; a reduction in local floral variability and pollen resources (Potts et al. 2010; Holzschuh et al. 2007) may lead to a reduction in individual and colonial fitness.

Crop diseases, such as powdery mildew caused by Blumeria graminis, on winter wheat fields (Fitt et al. 2006), are dealt with via the application of fungicide compounds and generally, at the legally permissible levels set out under European Union regulation number 1107/2009 (HSE 2011), they are of little to no risk to bee health (Ladurner et al. 2005). Indeed it was only at unnaturally high levels that the fungicides applied to A. mellifera by Ladurner et al. (2005) began to demonstrate negative effects; Neem oil, a naturally occurring compound used in organic farming, directly affected survival levels with contact application. Propiconazole, a DNA demethylation inhibitor, displayed delayed and acute toxicity effects in A. mellifera, when administered in high concentrations. However, at environmentally acceptable levels there was no indication of any negative effects to the bees.

5.2.2 Synergistic effects of herbicides & fungicides

Despite their generally safe reputation, fungicides and herbicides respectively can "assist" the toxicity towards, and damage to, bees by other chemical compounds. This toxicity pathway is well known in other organisms and is given the term "synergistic effects"; a synergistic effect is brought about through the combined action of multiple agents, working in unison to produce an effect which is significantly greater than the effect of either compound individually (Hertzberg and MacDonell 2002). Whereas increased toxicity towards an individual organism can occur simply through the bioaccumulation of multiple, similar compounds (Boedeker et al. 1993), resulting in additive effects; the process behind synergy is much more complex in its mechanisms. Synergistic relationships involve the alteration of a chemicals normal action by another compound; the effects may change the activation, specific site of action, or detoxification rate of the effected chemical (Thompson 1996; Cohen 1984). Thompson (1996) identifies the alteration of pesticide-metabolising enzymes, within an organism, as potentially the greatest accommodating factor for synergistic activities to occur.

It has become increasingly apparent over the past few decades (Thompson 1996) that our native and managed pollinators are not immune to these reactions (Pilling et al. 1995; Gill et al. 2012; Chauzat et al. 2009). The vast majority of research into the effects of multiple pesticide synergisms in hymenopterans has mainly been focused around A. mellifera (Chauzat et al. 2009; Schmuck et al. 2003), due to being seen as a good indicator of environmental pollution, through its generalist foraging behaviour, and particulate uptake, via body hairs (Porrini et al. 2003). Previous studies have found synergistic relationships occurring between of fungicides and insecticides which display very high levels of toxicity, relative to the intensities observed in mono-pesticide dosages (Pilling et al. 1995; Gill et al. 2012). And despite this synergistic relationship not being universally applicable to any combination of fungicide and pesticide (Schmuck et al. 2003), the effects of such interactions were found to be significant.

One particularly well investigated relationship is that found between the pyrethroid pesticide, lambda-cyhalothrin, and various ergosterol biosynthesis-inhibiting (EBI) fungicides in the European honey bee (Pilling et al. 1995; Pilling and Jepson 2006). Toxicity levels, at recommended dosages (7.5g active ingredient. ha-1) defined by Pilling and Jepson (2006) as "hazard ratios", were found to be 110 for lambda-cyhalothrin alone, but in the presence of EBI-type fungicides it ranged from "366 with flutriafol to 1786 with propiconazole" (Pilling and Jepson 2006). This equates to a 16.2 fold increase in the toxicity of lambda-cyhalothrin towards A.mellifera.

Similar combinatorial effects can be observed in B. terrestris, with the inhibition of foraging behaviour and increased mortality greater in colonies dosed with imidicloprid and lambda-cyhalothrin (Gill et al. 2012). Gill et al. (2012) used concentrations of the pesticides which reflected the expected environmental levels of residues; when both pesticides were combined, the resulting damage to test colonies is of a higher severity than individual levels for either imidacloprid or lambda-cyhalothrin, and far greater than control colonies.

5.3 Insecticides

5.3.1 Specificity of pesticides used within the United Kingdom

Of all the pesticides used within agriculture, insecticides have the greatest capacity to inflict damage upon individual bees and whole colonies; broad-spectrum pesticides in particular have a heightened risk of harming non-target species (Epstein et al. 2000), as their mode of action is largely non-specific to a target species. Neonicotinoids and Pyrethroids are two such classes of broad-spectrum pesticides; narrow-spectrum pesticides are much less common and are focused directly on the target species, or group of organisms.

5.3.2 Risk factors and avenues of exposure

As such the vast majority of insecticides applied to crops within the UK, are broad-spectrum, and pose varying risks to foraging bees, depending upon the chemical’s propensity to bioaccumulate, amongst other factors, such as contact toxicity and toxicity arising from oral dosage (Goulson et al. 2008). Other factors must be taken into account when considering the effects of these chemicals on bees within a natural, non-laboratory environment; the expression of systemic pesticide molecules, such as imidacloprid, within the nectar of flowers frequented by B. terrestris is one such concern (Rortais et al. 2005). Another, spraying patterns and their seasonal and daily timing, must also be taken into account; with the foraging behaviours of the two main hymenopteran pollinators varying greatly (Thompson and Hunt 1999); with B.terrestris active in the morning and evening (prime crop spraying times) it may be difficult to adapt strategies to limit exposure.

5.3.3 Lethal and sub-lethal effects at individual and colony levels

Whilst the lethal and sometimes immediate effects of pesticide exposure may garner more attention from the media and subsequently the public eye; it can be the sub-lethal, cumulative effects of pesticides which can ultimately lead to greater, long term damage to a colony, or nested population (Bortolotti et al. 2003; Schneider et al. 2012; Cresswell 2011; Mommaerts et al. 2010). In general, lethal effects from neonicotinoid and pyrethroid pesticides commonly used within the UK are incredibly rare, when the chemicals are applied correctly, according to industry guidelines (Cresswell 2011; Whitehorn et al. 2012).

Sub-lethal effects have been recorded in both A. mellifera (Cresswell 2011) and B. terrestris (Mommaerts et al. 2010), commonly these effects manifest in the form of decreased overall foraging behaviour and at field-realistic pesticide concentrations this translates to a 6 – 20% decrease in honey bee performance (Cresswell 2011), at dietary concentrations of 0.7 – 10μg kg-1. However, these trace concentrations of imidacloprid have significantly more lethal effects on B. terrestris, with levels of 10μg kg-1 producing significantly greater levels of bumble bee mortality when compared to pesticide-free nests (Mommaerts et al. 2010; Cresswell et al. 2012). There is a clear disparity between the relative capacities for the two species to cope with this particular class of pesticide; as Cresswell et al. (2012) speculate, the separate evolutionary heritage of the two species may have inferred a selective advantage on A. mellifera, with its tropical origins inferring a resistance to alkaloid based compounds which are commonly found in plants from these hemispheres.

When sub-lethal effects are observed in B. terrestris, they have been identified at concentrations much lower than those observed in A. mellifera colonies (Cresswell et al. 2012); which indicates a greater sensitivity to the levels of insecticides one would expect to find in commercially treated fields. The application of these compounds during the spring months, when young queens are founding nests, is likely to impart a disadvantage on these colonies.

6. Other causes of pollinator decline

6.1. Encroachment from non-native bees

In the past few decades there has been an increased application of commercially reared bumble bees in industrial-scale greenhouses, particularly within the southern counties of England (Goulson et al. 2008; Ings et al. 2006), where the importation of around 10,000 colonies of B. terrestris dalmitinus, a subspecies from south-eastern Europe, occurs annually. Large-scale escapes have a precedent for occurring from these covered facilities (Goulson et al. 2002), and there is the capacity for these alien subspecies to spread non-native diseases and parasites to the native bumble bees, in the case of south-eastern England B. terrestris audax (Ings et al. 2006). Another threat posed to the native subspecies is the possibility of high levels of crossbreeding and subsequent hybridisation, which could lead to the very real prospect of the loss of a native subspecies (Raine et al. 2006; Ings et al. 2006).

6.2. Parasitism

6.2.1 General effects of parasitism

As with most free-living animals; the hymenopterans are subject to parasitism by various organisms (Holling 1959; Crofton 1971; Stoltz and Vinson 1979). Parasitic relationships, by definition, are detrimental towards the host organism, with a reduction in energy availability and overall fitness a common result. These effects occur at an individual level in most organisms, however, in colonial species, the decreased viability of multiple individuals can be reflected in a diminished fitness at the "superorganism", or colony, level (Rosenkranz et al. 2010). When one considers the negative effects of pesticide use, the additional stressors of parasitism can be an important contributory factor in the decline of pollinator species.

6.2.2 Varroa destructor – an endoparasitic mite

The most widely observed hymenopteran parasite is Varroa destructor, a mite which is endemic in A. mellifera colonies across the vast majority of the developed world, with the exception of Australia as of 2012 (Rosenkranz et al. 2010; Hafi et al. 2012); with colony losses reported only in the northern hemisphere as of 2010 (Neumann and Carreck 2010), as illustrated in Figure 6.1. V. destructor females feed on the haemolymph of adult bees in the phoretic stage of their lifecycle; juvenile females and males feed solely on the preimaginal stages of the honey bees within the sealed brood cells (Rosenkranz et al. 2010; Garedew et al. 2004). The effect of the mites can therefore be felt across multiple generations within the same hive; this pressure, not only on the adult workers, but also on the larval stages of new bees, facilitates a decrease in the overall fitness of the colony. Thus V. destructor has been implicated in increased colony failure and has also been spoken about in conjunction with Colony Collapse Disorder (Evans et al. 2009; Amdam et al. 2004).

Figure 6.1. A map produced by Neumann et al. (2010) after synthesising reports of V. destructor implicated in colony deaths from across the globe. What can be seen is a clear disparity between northern and southern hemispheres.

6.2.3 Locustacarus buchneri – a parasitic mite found on Bombus terrestris

The issue of parasitic mites within A. mellifera colonies is certainly a much more prominent and researched relationship within the field of Apiology; one only has to consider the sheer number of research papers published within the last decade or so, to recognise this disparity (Rosenkranz et al. 2010; Otterstatter and Whidden 2004). But in the light of recent research into the effects of commonly used insecticides on our most common wild pollinator (Cresswell et al. 2012; Whitehorn et al. 2012), any additional stressors related to B. terrestris health must be accounted for if efforts to aid their survival are to be successful.

L. buchneri rather like V. destructor feed on the haemolymph of their host; this is drawn from within the tracheal system of, initially, the founding queen and then later on, from workers (Otterstatter and Whidden 2004). This feeding behaviour, coupled with sufficiently high levels of infestation can lead to tracheal damage, and results in lethargic and impaired host activity (Alford 1975; Otterstatter and Whidden 2004). Generally the parasite load of foraging Bombus species from L. buchneri, is around 10% or less (MacFarlane et al. 1995) but has been observed at up to 50% in severely infested nests depending on the time of year, and host species (Otterstatter and Whidden 2004).

Prior studies into this organism have generally regarded it as a benign parasite, due to its apparently non-malignant nature and lack of impact on colony survival (Husband and Sinha 1970; Otterstatter et al. 2005). However, when a colony is under increased stress from various natural and synthetic stressors, the effects of the mites may be more pronounced; with the negative impact on single bees translating to a colony-wide decline in productivity and health, facilitated by the reduction of worker bee activity (Husband and Sinha 1970; Otterstatter et al. 2005). The increased proclivity of L. buchneri for pronounced colony damage, in the presence of additional stressors, raises issues which must be addressed by further research, namely into the combined effects of these mites and various common insecticides.

6.2.4 Nosema ceranae - a microsporidian parasite of Apis mellifera

Microsporidians are uniformly intracellular parasites, with the vast majority showing some resistance to the host immune system (Higes et al. 2006). A similar microsporidian, Nosema apis, is widely known and treated within colonies of A. mellifera. N. ceranae however, is a somewhat recent arrival in the scope of European beekeepers, reported in Spanish colonies of A. mellifera by Higes et al. in 2006; originally found on the Asian honeybee Apis cerana, this parasite infests the digestive system of infected bees, specifically in the ventriculus and midgut regions, occupying the epithelial layers of organ cells and leading to digestive disorders and increased mortality (Higes et al. 2006; Ritter and Escobar 2001). The transfer of this parasite from the original A. cerana host to A. mellifera has been hypothesised to have occurred in the past ten to fifteen years (Klee et al. 2007), with some reports pinpointing the exact origin, in Finland at least, as 1998 (Paxton et al. 2007); and rather like V. destructor, Klee et al. suggest that the large scale import and export of commercial A. mellifera colonies may have facilitated this host transfer.

Prevalence of this parasite, known as the "Asian variant" of N. apis infection, was quickly realised to be widespread across mainland Europe after initial identification, and subsequent tests in the UK, by the National Bee Unit (NBU) in the November of 2007, identified N. ceranae in 14 of 309 DNA samples taken from managed hives (Budge 2008), this equates to around 4.5% of samples collected. This initial figure is no doubt higher now, with the yearlong viability of spores ensuring that infection risk is high towards future generations in managed hives (BeeBase 2012).

Studies have reported higher mortalities in A. mellifera exposed to N. ceranae than those exposed to N. apis (Paxton et al. 2007), this effectively mirrors the effects seen in colonies exposed to V. destructor. As A. mellifera is a new host species, the resistance which the European honeybee had built up toward N. apis infection, is essentially rendered useless by this alien species, which generally leads to much more pronounced lethal effects in these vulnerable bees. Paxton et al. also found that the vast majority of Nosema-type infections in studied bees were caused by N. ceranae alone, or at a smaller level, in conjunction with N. apis which suggests a higher virulence can be attributed to this parasite.

Figure 6.2. Sperm counts taken from male bees with the B. terrestris colonies examined during the virulence studies conducted on N. bombi by Otti and Schmid-Hempel (2007). Error bars represent one standard deviation; with sample sizes given in brackets.

6.2.5 Nosema bombi - a microsporidian parasite of Bombus terrestris

Another unicellular Microsporidian is an important factor in pollinator decline, globally and within the UK; N. bombi, as the name suggests, is an obligate intracellular fungal parasite of bumble bees, with the vegetative state generally found in the mid-gut and Malpighian tubules of infected bees (Otti and Schmid-Hempel 2007). Observable effects, within the lab, on multiple Bombus species are somewhat severe, with the functional fitness of males (see Figure 6.2.) and young queens "reduced to zero", additionally the lifespan of the young males and worker bees is reduced (see Figure 4.) compared to control colonies (Otti and Schmid-Hempel 2007).

Figure 6.3. The mean proportion of dead worker bees found within B. terrestris colonies included in virulence studies of N. bombi by Otti and Schmid-Hempel (2007). Error bars represent 95% confidence intervals for binomial distributions; with sample sizes given in brackets.

N. bombi appears to reduce its own ability to reproduce within a colony through the severe negative effects it elicits on the infected nest. The damage is such that most of these nests would not survive in the natural environment (see Figure 6.3.), where other contributory factors such as pesticide exposure would increase the damage to the effected colony. Indeed another study conducted by Otti and Schmid-Hempel in 2008 verified this belief; they assessed the differences in damage to infected and control colonies of B. terrestris in the field. The results from this experiment broadly agreed with their prior work, with infected nests failing to produce any sexual offspring, and generally being much smaller, with fewer individuals per nest compared to the control colonies (Otti and Schmid‐Hempel 2008).

What we can see is the clear danger that N.bombi infection poses to colonies of our most important wild pollinator, with detection of N. bombi spores in the faecal matter of the control bees (Otti and Schmid‐Hempel 2008) indicating a viable means for horizontal transmission of the parasite, via infected faeces deposited on visited flowers. The parasite rules out its own vertical transmission as it effectively obliterates the infected colonies capacity to contribute towards the next generation’s gene pool entirely.

6.2.6 Aphomia sociella- The bee moth

One of the primary parasitic species associated with B. terrestris, in the UK, is the bee moth A. sociella; the lifecycle of this moth is such that it will bring about the damage of nests of Bombus colonies that are exposed to it. The females opportunistically lay eggs inside the nest, which will hatch into the larvae; subsequent damage occurs inside the Bombus nest due to the feeding activity of these larvae, systematically ingesting the wax cells, and structural regions of the nest; damage can also spread to larvae and the pupal cells.

These pests are more commonly found in suburban gardens than on agricultural land, so the threat to bumble bees nesting in farming environments is much less pronounced than in urban gardens. However what this indicates is that the greater floral diversity of suburban gardens accommodates a greater proportion of the B. terrestris population within the UK than monoculture farmland (Goulson et al. 2002). Whilst the greater infestation of A. sociella is no doubt a concern for urban populations of Bombus it serves as an indicator for an equally pressing concern, the relative lack of bumble bees in our countryside, which can be accounted for by the comparative destruction of the vast majority of natural grassland and hedgerow habitats in recent times (Goulson et al. 2002; Walker et al. 2004).

7. Agricultural intensification and landscape patterns

7.1 Agricultural intensification

7.1.1 Great Britain: a recent history of landscape alteration

One of mankind's most significant alterations to the global environment, is the expansion of agricultural land; from mostly subsistence farming towards an increasingly industrialised scale of production (Holderness 1985). In Britain, the first alterations to the countryside were made in earnest around c.6000 years ago, with the clearing of large areas of wild woods to accommodate the first arable crops and livestock. Over the ensuing centuries vast swathes of woodland and natural meadows were replaced with managed fields. Subsistence farming was the norm over these centuries, this changed between c.1600AD and c.1750AD, when increased labour requirements, and innovative inventions and techniques, led to farming on a larger scale (Tull et al. 1762; Wikipedia 2013); this increase in productivity was set to intensify after 1870, when stuttering cereal and land prices were outstripped by a rise in wages (Holderness 1985); this lead to a decrease in labour forces, and an inclination towards increased mechanisation (Zanden 1991).

Fertilisers and pesticides saw wide scale adoption after World War II, with the 1947 Agriculture Act passed by Clement Atlee’s post war government to promote increased crop production and food security, which coincided with improvements in plant breeding, and greater yields from important crops. In the search for greater yields and self-sufficiency, many thousands of miles of hedgerows were lost (Pollard et al. 1974; Petit et al. 2003), as were areas of natural woodland and grassland; vast swathes of natural habitats were converted to managed arable land, in changes supported by government policies and legislations, such as the 1951 Forestry Act, during the years between 1950 and 1970 (IPF 2011).

7.1.2 Implications of prior land management

With an increase in monoculture crops comes an expected decline in biodiversity within the immediate vicinity of these fields, as the numbers of plant species are reduced, so is the variety of vertebrate and invertebrate species which can survive there; thus the decline of bumblebee populations across Europe can be somewhat attributed to the removal of suitable habitat areas, for intensive agriculture (Osborne and Corbet 1994). The act of destroying vast stretches of hedgerows from the 1950s onwards, would have further reduced the area of viable habitats for native hymenopteran pollinators to scavenge; indeed between 1984 and 1990 it was estimated that the total length of hedgerows had declined by a further 23% (Hedgelink 2013). Ultimately these actions led to a deficit in biologically diverse areas and a reduced area of land within which to situate newer zones of diversity; one challenge for farmers and conservationists to overcome is how to promote increased biodiversity without significant costs, both in terms of productivity and finances.

7.2 Landscape patterns in agricultural Britain

7.2.1 Key landscape features

As we can see there has been an increase in highly managed farmland throughout the countryside (Walker et al. 2004), with fewer uninterrupted areas of natural habitat for bees to forage on and build nests in. Hedgerows, or field boundaries, have also seen a marked decline in recent decades (Petit et al. 2003), with their initial removal facilitating an expansion of arable land for crop planting (Petit et al. 2003); but efforts are being made to reverse this trend (Goulson et al. 2002). Thus, the increased provisioning of land (for agriculture) has led to a marked decline in suitable forage and nest building sites for many native pollinators, with B. terrestris amongst those affected. Clearly, within the unnatural, often barren expanses of farmed lands, the hedgerows and green lanes that intersperse these ecological deserts are a vital lifeline for our native pollinators (Croxton et al. 2002), and a pillar of biodiversity for other native species (Marshall and Moonen 2002).

7.2.2 Hedgerows and field boundaries – islands of biodiversity

Within agricultural landscapes field margins, or boundaries, are present at the edges of all managed fields (Marshall 1988; Marshall and Moonen 2002) and can be defined as man-made barriers designed to inhibit the free movement of livestock. Marshall and Moonen (2002) state that the three key components of any field margin are the boundary (i.e. hedges, fences, or walls), the crop edge, and a strip of land between the two which may serve multiple purposes, such as access or nature conservation.

In terms of UK wildlife, these field margins are well known as significant refuges for large reserves of both flora and fauna; with field edges containing the greatest diversity of flora in intensively managed lowland arable landscapes (Marshall and Moonen 2002). With the increased variety of flora comes an expected increase in the diversity of fauna which are supported by these man-made habitats. Invertebrates and vertebrates alike can be found within and around these sites (Duelli et al. 1991; Vickery et al. 1998), in much higher degrees of diversity and numbers than the ecologically barren, monoculture fields. This disparity in species dispersal, between closely situated habitats, is known as an ecotone (Forman 1995).

The 1st of June 1997 saw the introduction of the ‘Hedgerow Regulations 1997’ within the UK; this series of regulations protects around 70% of all countryside hedgerows, within Britain, which are over 30 years old or fall under the remit of another section of the guidelines (Hedgelink 2013). However there has been continued losses of hedgerows in the intervening years, due to poor management practices; with 402,000km (see Table 7.1.) of true hedgerows in England alone in 2007, down from 428,000km in 1998 (Carey et al. 2008), it is clear to see that such a significant expanse of beneficial habitat needs to be more effectively managed to ensure its continued existence.

Table 7.1. The length and standard error (‘000 km), and change in length of hedgerows in Great Britain between 1998 and 2007, constructed from data taken from CS2007 (Carey et al. 2008). Arrows symbolise a significant change (P < 0.05) in the direction shown.



1998 - 2007


Length (‘000 km)


(‘000 km)

Length (‘000 km)


(‘000 km)

Direction of changes
















Great Britain





7.2.3 Green lanes – transportation routes through arable landscapes

Defined by Dover et al. (2000) as "unmetalled tracks (free from bitumen) between fields of variable width… sunk below or raised above field level… bounded on both sides by grass banks, hedgerows or dry-stone walls"; green lanes provide areas of variable size which act as refuges for large swathes of animal and plant species (Croxton et al. 2002). Green lanes may act as vital refuges for bumble bees and other pollinator species, as they are somewhat more sheltered than field margins, and as such are less exposed to the chemical treatments which the more exposed hedgerows and margins are subject to; indeed Croxton et al. (2002) demonstrated that the vegetation communities are much more diverse within a green lane environment, than along a field margin. Their research also indicated that the greater degree of diversity within the vegetation was positively correlated with the density of local bumble bee populations. Green lanes within these arable, yet sparse, landscapes would therefore appear to be vitally important to the continued persistence of bumble bees and other pollinator populations.

7.2.4 Current landscape use strategies and their implications for pollinators

In light of recent reports pertaining to local and global pollinator declines (Goulson et al. 2008; Neumann and Carreck 2010; Potts et al. 2010), there has been a heightened interest in the possibility of combining the anthropogenic uses of landscapes with an increased provisioning of pollinator services (Goulson et al. 2010). To ensure that the agricultural landscape is a viable habitat for bumblebees there needs to be sufficient areas of two required environments: nesting habitats and foraging habitats (Westrich 1996; Walther‐Hellwig and Frankl 2000).

One particularly interesting study conducted into current farming practices and their influence over B. terrestris health, and subsequent pollination capacity, was performed by Goulson et al. in 2002. Within this study they looked into the comparative successes of B. terrestris nests situated within three distinct environments: suburban gardens, conventional unimproved farmland, and ecologically improved farmland (via conservation headlands, set-aside land etc). A particularly striking point raised by the research was the significantly greater success of bumblebee colonies situated within the suburban garden environment; this demonstrates somewhat the current importance of the suburban garden as a refuge for our native pollinators. With a considerably greater diversity of pollen available to workers, foraging in gardens contributes towards nests gaining biomass, and size, much more readily than the other two environments (Goulson et al. 2002).

Somewhat worryingly there was found to be very little difference between standard and improved farmland environments; with both habitats much less capable of ensuring that the nests could grow as rapidly as the suburban bees (see Graph 7.1.; Goulson et al. 2002). The disparity between the farmland and suburban environment occurs despite high levels of parasitism from A. sociella in the suburban nests (Goulson et al. 2002); which only serves to further emphasise the superiority of the non-farmland environment.

Evidently, the practices put in place to enrich farmland environments and improve their suitability for Bombus are not effective in the forms tested in the study; some of the schemes in question were aimed at encouraging the provisioning of annual flowers in regularly tilled soils, whereas other schemes which allowed for plant communities on untilled land were somewhat new at the time of study (Goulson et al. 2002). Both of these scheme types contributed towards unfavourable plant communities; which were not in the mid-successional stage of development which is favoured by B. terrestris amongst others (Steffan‐Dewenter and Tscharntke 2001; Goulson et al. 2002).

Graph 7.1. Changing masses of B. terrestris nests situated in three different habitats (± SE). Nests based in gardens were subject to high levels of parasitism from A. sociella (Goulson et al. 2002).

Environmental Stewardship was a government scheme introduced in March 2005 to incentivise and encourage the conservation of wildlife and biodiversity through the maintenance and enhancement of the landscape (DEFRA 2013). The three tiers of the scheme are focused on these key aims, at different levels of complexity and manipulation of the environment, with the simplest being Entry Level Stewardship (ELS), followed by organic ELS, and finally Higher Level Stewardship (HLS). One of the most important targets laid out in all of the tiers is the provisioning of natural floral communities in untilled field margins, allowing for mid-successional communities to arise (Goulson et al. 2002). Carvell et al. (2007) found that the application of a ‘legume based "pollen and nectar flower mix"’ recommended by the ELS schemes was capable of providing a richly diverse source of nutrition for multiple Bombus spp. This blend of floral species was preferable to sown grass mixtures, and when combined with the additional measures put in place with the HLS measures would be capable of providing diverse floral ecosystems, with perennial plants capable of supporting a significant range of pollinators (Carvell et al. 2007).

8. Discussion

8.1. The relative importance of different pollinator species within the UK

It is apparent from the current research that there is a clear disparity between the importance of managed A. mellifera colonies on a global scale, and their relative significance towards the ecosystem within the United Kingdom (Breeze et al. 2011). In countries such as the United States, the provisioning of managed colonies of honeybees near to food crops is vital towards ensuring that pollination levels are sufficient enough to guarantee that harvested yields are high, and of good quality (Gill 1990; Kremen et al. 2004; Losey and Vaughan 2006). Within the United Kingdom, it is the actions of wild colonies of native bees which influence the overall success of food crops. This is made quite clear when we consider the rise in insect pollinated crop areas of around 57.5% since 1984, covering 848,946 hectares in 2007 (Breeze et al. 2011). It is clear therefore, that within the UK we must endeavour to focus more on ensuring the continued prevalence of our native pollinators; with more research needed into the current status of not only B. terrestris, but also other members of Bombus and solitary bees, and feral colonies of honeybees.

British Melittology would seemingly achieve more on a national scale; if there was a concerted shift in focus away from A. mellifera towards a more dedicated and broad-reaching attempt to investigate our native pollinators and their potential threats. Ultimately it would be most beneficial to maintain a high degree of biodiversity within our native pollinators; not just in an agricultural sense, where their input is economically vital, but also socially and culturally where their actions improve the aesthetic quality of our parks and gardens. This target, of maintaining a high level of biodiversity, would also ensure that any population crashes, within one species, would not have a hugely significant effect on the overall levels of pollination across the nation.

8.2. Recommendable courses of action to ensure the persistence of UK pollinators

8.2.1. Changes to insecticide policies

One need only look at the increasing evidence against the safety of neonicotinoid insecticides to agree that their continued large-scale application, within the agricultural environment, is to the detriment of both B. terrestris and managed colonies of A. mellifera (Mommaerts et al. 2010; Cresswell et al. 2012). Indeed the actions of the European Union, in attempting to ban their use, are commendable and if successful, will no doubt alleviate a considerable strain on these vital pollinator species (Hillocks 2012; McCarthy 2013). Alternative insecticide measures are readily available to farmers which have reduced effect on beneficial insects; one such example is a range of man-made chemicals known as Insect Growth Regulators (IGRs). These chemicals actively prevent the development of juvenile insects into the next stage of their lifecycle; and by preventing their progress to adulthood they are unable to breed, thereby limiting the numbers of pests in the long term (Staal 1975; Fox 1990). These chemicals do not kill the insect outright, but crucially, prevent its contribution to the next generation.

If a consensus cannot be achieved on the removal of neonicotinoids from the agricultural environment, then a compromise must be reached to ensure that their effects on bees are minimised. In terms of managed colonies of A. mellifera it could be as simple as facilitating greater levels of communication between farmers and local beekeepers, thereby enabling the removal of colonies from "at risk" areas. However, when it comes to bumblebees there is no such simple solution and it may come down to simply trying to minimise the negative effects of the insecticides.

A possible avenue of research into alleviating the effects of these compounds, is the inclusion of bumble bee scent marking homologues in spray mixtures; bumble bees regularly mark the flowers they have visited to ensure that other bees from their nest (and indeed other species of bumble bees) are aware that the nectar from this particular flower is depleted (Goulson et al. 2000). This incites avoidance behaviours in these bees, with less foraging activity taking place on the labeled flowers (Stout et al. 1998; Goulson et al. 2000). If a homologous compound based around heneicosane (a complex hydrocarbon extract from Bombus tarsal glands which elicited the strongest avoidance behaviours in lab tests) could be produced, then it would stimulate avoidance, or reduced foraging, behaviour in the bees (Goulson et al. 2000). If this was applied in conjunction with the insecticides then it may lead to an active reduction in foraging from the effected crops. Reduced levels of feeding from contaminated crops would result in the nests remaining stronger throughout the summer months and could feasibly eliminate most of the detrimental effects associated with prolonged insecticide exposure.