Christopher Dyer 707585 Y3 dissertation

Christopher Dyer (707585): ZoologyThe flower preferences of insect pollinators

The flower preferences of insect

pollinators

Christopher Dyer (707585)Wallace Building

Swansea UniversitySwanseaSA2 8PP

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Figure 1: Volucella zonaria on Cirsium


: Abstract Insect flower visitors (or pollinators) are essential animals: they are

economically important to humans, and also support proper ecosystem function for natural communities. Pollinator groups have preferences for certain flowers, usually based on colour and morphology. Despite their importance the flower preferences of many insect pollinator groups are largely unknown and understudied. With current declines observable in many insect groups it is vital that not only are the preferences of these

groups understood but also the impact that increasing urban cover has on them. This study provides a general overview of the flower preferences of the most common insect flower visitors in the United Kingdom (UK), and

assesses the change in abundance of such groups across a suburban-rural gradient.

The general preferences of the four main insect pollinator orders (Diptera, Hymenoptera, Coleoptera and Lepidoptera) are described, as well as the

preferences of four insect groups that made up 80% of all insects recorded. The importance of the most visited flower group (the

Umbellifers) is also given notice. Although most groups were recorded at lower abundances at more urban sites, the limited amount of data

collected means the impact of urbanisation on insect abundance can only be speculated. It is clear, however, that different insect groups are

impacted in different ways, and that standardisation in sample sites is needed to reliably assess impact of urbanisation. Much research is still

needed to fully understand all of the factors that govern the flower preferences of insect flower visitors.

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Contents : Abstract 1: Introduction

o 1-1: History of pollination and its studyo 1-2: Pollination as an ecosystem serviceo 1-3: Insect pollinatorso 1-4: Study goals

2: Materials and methodso 2-1: Sampling siteso 2-2: Sampling protocolo 2-3: Identification of pollinators and blossomso 2-4: Environmental variableso 2-5: Statistics

3: Resultso 3-1: Insect groups recordedo 3-2: Plant groups visitedo 3-3: Sites and site comparisonso 3-4: Analysis of the main pollinator orders

4: Discussiono 4-1: Analysis of the Umbelliferso 4-2: Flower preferences of the Dipterao 4-3: Flower preferences of the Hymenopterao 4-4: Flower preferences of the Coleopterao 4-5: Flower preferences of the Lepidopterao 4-6: The impact of urban cover of insect abundanceo 4-7: Flaws and limitations

5: Conclusions and recommendations 6: References 7: Appendix 8: Acknowledgements 9: Project log and forms

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1: Introduction and background1-1: History of pollination and its studyPollination biology is the study of how, when and why plants are pollinated (a “what” component may also be added where anthecology [study of pollinators] is involved, Baker, 1983). The study of pollination is a highly ecliptic field including elements of botany, anatomy, zoology, evolutionary biology and phenology.

Plants (Kingdom Plantae) are among the most important living organisms on planet earth: they produce the oxygen that is used by nearly all heterotrophic life on earth. Pollination is the first step in the process by which most angiosperms reproduce and has been studied by botanists for hundreds of years, although interest in the biology of pollination is almost as old as agriculture (Real, 1983).

The vast majority of plants are pollinated by animals (pollinators). Around 78% of plants are pollinated by animals in temperate zones, rising to 94% in tropical ecosystems: most of which are insects (Ollerton, Winfree & Tarrant, 2011). Insect pollination (entomophily) was first discovered by the “fathers” of pollination biology, Koelreuter and Sprengel (Faegri & Pijl, 1971). They independently proved the sexual nature of flower parts (see previous citation), described flower parts and discovered different types of pollination, including entomophily. The complex relationships between plants and their pollinators are only just starting to be explored.

1-2: Pollination as an ecosystem servicePollination is a supporting ecosystem service, which benefits mankind through proper functioning of ecosystems and related processes (Daily,

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1997). Ecosystem services are often commoditized in order to express their importance to policymakers and the public (De Groot, 1987; Peterson et al. 2010). Ecosystem services globally are worth more than the value of all human produce in one year (Costanza et al. 1998; Pearce, 1998). Insect pollination alone is worth US$215 billion to the global economy annually (Gallai et al. 2009), and is estimated to be worth UK£400 million annually to the United Kingdom (Breeze et al. 2011).

These figures make the current trend of decline across many insect pollinator groups an issue that needs to be tackled, especially as demand for insect pollinator services increases (Potts et al. 2010; Aizen & Harder, 2009). This is likely due to an increasing demand for crops worldwide (Tilman et al. 2011) as the global population increases.

Despite the focus on ecosystem services as valuable to humans, these services also support proper ecosystem function for all wildlife (Rapport et al. 1998). Entomophily provides humans with resources, and also maintains biodiversity not just of plants but of all the animals that utilise the plants pollinated by insects.

1-3: Insect pollinatorsThe most important pollinating insect orders are the Diptera, Hymenoptera (particularly the Apoidea), Coleoptera, and Lepidoptera. These four orders comprise the vast majority of pollinating insects, and each order (and groups within the orders) have different foraging niches and flower preferences. These preferences can often be related to morphology of the pollinator or the flower, or the needs of the insect: whether it takes nectar, pollen or both (Syafaruddin et al. 2006).

Many pollinators also display flower constancy; a preference to certain plant species even if it involves ignoring potentially more profitable flowers (Goulson, 2000; Chittka, Thomson & Waser, 1999). Preferences for constancy may show intraspecific variation (Barth, 1985). Charles Darwin hypothesised that constancy is due to the limited capacity of insect

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memory, but this traditional idea has been largely rejected (Goulson, Stout & Hawson, 1997). Flower constancy may aid in finding flowers in large patches of similar plants, increasing foraging efficiency as the pollinator only visits flowers with known rewards (Goulson, 2000).

Pollination syndromes are a suite of traits possessed by groups of flowers that make them suitably adapted to be pollinated by certain pollinator clades (Ollerton et al. 2009). This idea is somewhat beneficial as it categorises pollinators based on general preference trends, however it is too simplistic to fully describe pollinators as many have a generalist nature with regards to flower foraging (Fenster et al 2004; Johnson & Steiner, 2000).

An attempt has been made below to summarise the general foraging preferences of the four major groups of insect pollinators, although it should be noted that these are very broad summaries.

1-3-1: DIPTERA AS POLLINATORSThe Diptera (true flies) are the largest insect order in the UK (5200 species, Proctor, Yeo & Lack, 1996) and have been known as pollinators since the late 19th century. Knuth (1906-09) lists a large diversity of dipteran pollinators from many families alongside the more well-known pollinators.

Syrphid flies are among the most important insect pollinators. The larvae of many species are aphidophagous which makes them useful as both pollinators and biological control agents (Ankersmit et al. 1986). Over 250 species are found in the UK (Stubbs & Falk, 2002). Superficially resembling bees and wasps, many species have been shown to have a preference for white and yellow blossoms (Lunau & Maier, 1995). The short proboscises of most syrphids are thought to limit them to feeding on flowers with short corollas (Gilbert, 1981; Goulson & Wright, 1997). Syrphid flies are one of the few fly groups known to show floral constancy (see Section 1-3) which is a rare trait among the Diptera (Ellis & Johnson, 2012).

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Bee flies (Bombyliidae) are also important dipteran pollinators, evolved for more efficient nectar collecting than syrphids due to their longer proboscises (Faegri & Pijl, 1971). Only one species is native to the UK: Bombylius major (Stubbs & Drake, 2001). The majority of the other families of Diptera contain pollinators; however these groups have not been extensively studied as flower visitors and their preferences are largely unknown (Larson, Kevan & Inouye, 2001).

1-3-2: HYMENOPTERA AS POLLINATORSThe Hymenoptera are among the most effective pollinators of flowers, especially the Apis and Bombus, although other bee and wasp species can be important as pollinators (Herrera, 1987). Pollination by the Formicidae is rare: likely due to the antibiotic secretions of ants inhibiting pollen function (see Beattie et al. 1984). Many bee species show flower constancy, likely aiding in their efficiency as pollinators of certain flowers (Grant, 1950; Free, 1970).

Honeybees are highly efficient pollinators with a widespread distribution, able to exploit a variety of pollen and nectar sources which are used to feed the colony (Winston, 1991). They have a preference for zygomorphic, deep corolla flowers often with nectar guides, and have been shown to have sophisticated colour vision and innate colour preference, as well as the capacity to learn (Giurfa et al. 1995; Menzel & Muller, 1996). Honeybee flower preferences are the most researched due to their economic importance (Southwick & Southwick Jr, 1992).

Bumblebees (Bombus), much like honeybees, have a preference for deep flowers with long corollas (Campbell et al. 2012). They are also thought to have a preference for blue flowers (Lunau & Maier, 1995). Experiments that strong corolla colour is important in attracting bumblebees to blossoms (Lunau, 1990).

Solitary bees can be locally important pollinators (Gathmann & Tscharntke, 2002), and also wasps, notably members of Agaonidae which have co-evolved with Ficus species (Herre, 1989).

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1-3-3: COLEOPTERA AS POLLINATORSPollination by the Coleoptera is more common in tropical regions, possibly due to greater biodiversity in these regions creating more niches for pollinators. This likely affects the study of beetle pollination, and little is known about the flower preferences of beetle species. Delpino (1868-75) distinguished two types of common flowers pollinated by beetles: inflorescences, and large single flowers. Certain species of the Magnoliaceae are mainly pollinated by beetles (Dieringer et al. 1999), but whether this represents an actual preference in the Coleoptera is not clear.

1-3-4: LEPIDOPTERA AS POLLINATORSMembers of the Lepidoptera are spurious pollinators: for adult Lepidoptera feeding is not always a necessity (Faegri & Pijl, 1971); however when they do forage it is often for nectar rather than pollen. They tend to forage on blossoms with deep corollas (Herrera, 1993), and are also sensitive to flower scent (Andersson, 2002). Beyond these broad trends the Lepidoptera do not seem to show a general preference; instead preference for certain flowers seems to vary between species (Tudor et al. 2004).

1-4: Pollinator declineValuing pollination as an ecosystem service has highlighted the importance of insect pollinators which are currently in decline. Because of their importance a lot of attention has been paid to honeybee decline, with one report suggesting as much as a 45% decline in honeybee numbers in 50 years in Europe (Potts et al. 2010). Due to the focus on honeybees it is possible that declines in other pollinator groups have gone unnoticed.

The causes of pollinator decline have been widely and extensively debated. Numerous studies have demonstrated the negative effects of pesticides on beneficial invertebrate groups (Henry et al. 2012; Desneux,

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Decourtye & Delpuech, 2006): however urbanisation is likely the main cause of biodiversity decline (Winfree et al. 2009). Urbanisation is linked to habitat loss and homogenisation (McKinney et al. 2006). Species richness is significantly reduced in urban cores, but individual species response to suburban (moderate) levels of urbanisation varies (McKinney, 2008). Amount of homogenisation in land use is also a factor in pollinator abundance: agricultural areas are often more homogenous in terms of plant varieties, and bee species tend to decline more rapidly in agricultural areas (Bates et al. 2011) due to a low tolerance for homogeneous plant communities.

The impact of urbanisation on species is largely dependent on local factors such as land use and urban habitat structure (Smith et al. 2006; Sattler et al. 2010), but most research is united in stating the negative impacts of urbanisation on various invertebrate taxa (McKinney, 2008). Due to the importance of pollinators, it is vital that their habitat and foraging preferences are understood, and that direct action is taken to encourage pollinators in urban areas and increase abundance of these insects.

1-4: Rationale and study aimsThere are large knowledge gaps regarding the preferences of the most common insect pollinator groups within the UK (the exception being bees). This study aims to: Describe the general flower preferences of these groups in regards to

flower colour and morphology using gathered data and previous research.

Analyse how increasing levels of urban cover may impact insect pollinator groups.

By understanding how insect pollinators are impacted by urbanisation, appropriate legislation can be created in order to aid in preserving these groups. Knowledge of their flower preferences can also aid in the creation

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of urban green spaces that are “pollinator friendly”, which could potentially contribute to combating pollinator decline.

2: Materials and methods 2-1: Sampling sites

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Before actual sampling begun, prospective sites were identified and carefully monitored for pollinating insects, to ensure the site would yield enough data. Only scrubland and grassy sites were chosen, and each site was required to have at least a 10m2 area with 60% or greater flowering plant cover (a single species was not allowed to cover more than 40% of the sample site). These measures were an effort to standardise the sample sites and reduce the affect that quality of sample site and diversity of flora had on the overall results. This also ensured a variety of pollinators were recorded. All of the sample sites were located within the Bristol region (ST6). Figure 2 shows the four sample sites.

In order to explore the impact of urbanisation on the abundance and diversity of pollinators recorded, the method used by Geslin et al. (2013) was utilised: sites with greater than 50% cover of grassland and trees were categorised as semi natural (rural), sites with 25% to 50% building or road cover were categorised as suburban, and sites with greater than 50% building cover were categorised as urban.

Land use/type for a 300 metre radius from the centre of each sample site was assessed using a modified version of the phase one habitat mapping system (Joint Nature Conservation Committee, 2010), in which category

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Figure 2: The four sample sites (circled in red on the photographs) and surrounding land. Images taken from www.gridreferencefinder.com


J3.6 (buildings) was expanded to include residential buildings (J3.6.1, represented by a hashed grey area), and commercial buildings (J3.6.2, represented by a dotted grey area). Category J6 was also created for roads, represented by two thick grey parallel lines. This expansion of phase one habitat mapping has many potential applications in similar studies as well as for landscape planners, conservationists and economists.

Table 1 shows the phase 1 habitat mapping categories utilised, as well as whether that particular category symbolised urban or green cover. The results of the mapping are displayed below in Table 2: sites 1 and 2 were designated suburban, whilst sites 3 and 4 were designated urban.

2-2: Sampling protocolSampling took place between July 21st 2014 and August 20th 2014. The

summer months are the optimal time for studies such as this as the largest diversity of insects and flowers can be found during summer. Each site

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Table 2: Results of the phase one habitat mapping, with designations for each sample site

Table 1: The phase 1 categories used to determine percentages of urban and green cover at sample sites

Phase 1 category

Urban/green

A GreenB GreenG GreenJ1.1 GreenJ1.2 GreenJ3.6.1* UrbanJ3.6.2* UrbanJ4 UrbanJ6* Urban

Site Grid ref Urban cover

Green cover

Designation

S1 ST6187480406 46 54 SuburbanS2 ST6273481720 26 74 SuburbanS3 ST6122378129 73 27 UrbanS4 ST6162678747 74 26 Urban


was sampled a minimum of twice and a maximum of four times. Due to destruction of the sites, sample sites 3 and 4 could not be sampled as many times as sites 1 and 2.

The initial experimental design used a stationary camera focussed on a single flower for a ten minute period, with a photograph taken every time an insect visited the flower. A trial run of this methodology revealed it to be flawed as few pollinators were actually recorded. This method also severely limited the amount of data that could be collected.

The sampling protocol used is as follows. A digital single-lens reflex camera (Alpha 290, Sony. Sony Europe, The Heights Brooklands, Weybridge, Surrey KT13 0XW) fitted with a zoom lens (30-300mm zoom A17s, Tamron. Tamron Europe GmbH, Robert Bosch Strabe 9, 50769, Koln, Germany) was used to take photographs of any insect that landed on a flower in a 15m2 area within the study site in a 30 minute time period. At least two pictures were taken of every insect where possible; one focussed on the abdominal markings and one focussed on the wing venation as these features are key to identifying between many insect families, particularly the syrphid flies (Stubbs & Falk, 2002). A two minute habituation period was used (Campbell et al. 2012). Insects smaller than 3 millimetres were discounted due to the length of time it took to focus on such small animals with the equipment being used. Figures 3-8 show some of the photographs taken during the study.

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2-3: Identification of pollinators and blossomsA variety of methods were used to identify the species present, including books, taxonomic keys, dichotomous keys, online resources, images and professional and enthusiast knowledge (Stubbs & Falk, 2002; Gilbert, 1993; Lee & Purslow, 2011; K state parasitology laboratory; Naturespot; Bumblebee conservation trust; Help save bees; Tachinid recording scheme; UK hoverflies; Insects of Britain and Northern Europe)

Different groups of insects were identified to different levels: many insect species cannot be identified solely from images. Lepidoptera and Coleoptera were identified down to species level due to the distinct characteristics of species from these groups. Hoverflies (Syrphidae) were also identified to species level as they differ greatly in appearance from the rest of the Diptera, and many UK species have distinctive features (Ball & Morris, 2012). The exceptions to this were hoverflies of the genus Sphaerophoria as species from this genus in the UK are difficult to confidently identify without examination of specimens. All other remaining species were identified to family level at the least. Specimens were not taken as this was deemed too intrusive for this type of study. The flowering plants were identified to genus level (Rose, 2006; Stace, 2010).

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Figures 3-8: Examples of photographs taken during sampling. Clockwise from top left: Bombus species, Tachinidae, Maniola jurtina, Apis species, Rhagonycha fulva, Eristalis tenax


2-4: Environmental variablesCertain environmental conditions were measured before sampling, and sampling was only conducted within certain parameters of these variables (Bates et al. 2011), as environmental conditions can have a large impact on the local abundance of insects and the nectar concentrations within flowers (McCall & Primack, 1992; Williams, 1961; Corbet, 1978).

Air temperatures were measured using a mercury thermometer left to acclimatise to local temperature for two minutes before a reading was taken. These readings were also checked against the Bristol meteorological office forecast for accuracy. A subjective measure of cloud cover was taken (the percentage of the visible sky obscured by cloud was recorded). Wind speed was measured using the subjective Beaufort scale (Frost, 1966), as a device for accurately measuring wind speed was not available. Sampling was only conducted between temperatures of 18-30C, cloud cover of no more than 80%, wind speed of <4 on the Beaufort scale (<15Km) and when it was not raining (see Bates et al. 2011).

2-5: Statistical analysisData were analysed using a variety of statistical methods. Linear regression analysis was conducted to determine whether a significant correlation existed between the number of pollinators recorded and the time of year (date). Chi square tests were used to determine whether different pollinator groups were recorded on different plant groups statistically more often than others.

Correlations were used to determine the strength of the relationship between percentage of urban cover and the average number of pollinators per sample session.

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3: Results 3-1: Insect groups recordedA total of 514 insect pollinators were recorded across 13 sampling sessions from 55 different groups (family, genus or species). Only seven of these groups were ubiquitous across all the sample sites: Andrena, Apis, Bombus, Calliphoridae, Eristalis tenax, Rhagonycha fulva, and Tachinidae.

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The temperature range across all the sample sessions was 16-25C, whilst wind speed ranged from 0-29Km.

The largest of the four main pollinator orders was the Diptera, which accounted for 58.56% of the insects recorded. The second largest of the four main orders was the Hymenoptera (28.4% of total), followed by the Coleoptera (7.39% of total), and finally the Lepidoptera (5.06% of total): Figure 9 displays the number of insects from each of these four orders.

Tachinidae and Calliphoridae were the two largest groups, accounting for almost a quarter (24.90%) of all the insects recorded. Apart from the four main pollinator orders four further groups were identified as being important groups: the calypterate flies (families Calliphoridae, Muscidae, Sarcophagidae, and Tachinidae), Bombus species, Apis species and Syrphidae, which together accounted for 79.18% of the insects recorded.

Three of the insects recorded did not fall into any of these orders. These included one member of the Chrysopidae (order Neuroptera) and two members of the Nabidae (order Hemiptera). Due to the small number found, these insects were excluded from further analysis.

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Figure 9: Pie chart displaying the abundance recorded of each of the four main orders


3-2: Plant groups visitedThe 514 insects were recorded visiting 16 different flowering plant groups. Several very similar species of plant with white umbels of small flowers were recorded during the study period, the majority from the genus Daucus. All of the white umbel species were grouped together under the category Umbellifers, as they were all very anatomically similar and had very similar species assemblages visiting them. Table 2 displays the 16 different plant groups recorded. Apart from the Umbellifers group, they were all genera of flowering plants.

Family Plant group Common name ColourASTERACEAE Achillea Yarrow Various

Calendula Marigold Yellow/orangeCirsium Thistle PurpleHypochaeris Cat's ear YellowJacobea Ragwort YellowPulicaria Fleabane White + yellowSenecio Ragwort & Groundsel YellowSonchus Sow thistle YellowTaxaracum Dandelion YellowTragopogon Goatsbeard YellowUmbellifers Umbellifers White

CAPRIFOLIACEAE Dipsacus Teasel PurpleCONVOLVULACEAE Calystegia Bindweed White

Convolvulus Morning glory WhiteFABACEAE Melilotus Sweet clover YellowROSACEAE Rubus Blackberry White

Over a quarter (39.69%) of insects were recorded on Umbellifers. Figure 10 shows the numbers of different groups found on Umbellifers: the Diptera accounted for 73.53% of the insects recorded on this flower group.

Senecio and Cirsium were the second and third most visited plant groups (15.95% and 15.56% respectively). Senecio was most visited by the

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Table 3: The 16 plant groups recorded, along with common names and colour of flowers


Diptera (mainly the Syrphidae), whilst Cirsium was most visited by the Hymenoptera.

3-3: Sites and site comparisonsAs mentioned in Section 2-2, some of the sites could not be sampled as much as was desired. Only the two suburban sites (1 and 2) had four sampling sessions. The most urban sample site (site 4) could only be sampled twice: a total of 64 pollinating insects were recorded at this site. In order to remove the impact of different numbers of sample sessions at each site, a mean number of insects was calculated for each site.

Table 3 shows the number of insects recorded during each sampling session. The two urban sites had the lowest mean number of pollinators. Site two had the lowest urban cover (26%), but not the highest mean number of pollinators per sample: site one had the highest number of pollinators (mean of 50.25), and had a total urban cover of 46%.

There was a moderate negative correlation between the average number of pollinators per site and percentage of urban cover (r=-0.48, N=4, P=0.525), which was not statistically significant.

Sample site

Urban cover (%)

Sample 1

Sample 2

Sample 3

Sample 4

Mean (±SD)

S1 46 52 60 50 39 50.25 (±8.66)S2 26 28 42 46 32 37 (±8.41)S3 73 26 38 37 N/A 33.67 (±6.66)S4 74 30 34 N/A N/A 32 (±2.83)

Linear regressions were conducted to determine the degree of correlation between date and number of pollinating insects recorded. Regressions were only conducted on the data from sample sites one and two. Regression results show a moderate positive relationship between date and number of pollinators at sample site one (r2=0.536, F=2.314, P=0.268. See figure 3), and a very weak positive relationship between

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Table 4: Number of insects recorded during each half hour sampling session


date and number of pollinators at sample site two (r2=0.12, F=0.272, P=0.654). However neither of these regressions were statistically significant so will not be discussed further in this study (see Figure 11)

Figure 12 shows the proportional abundances of eight insect groups at each sample site. For most of these groups the most individuals were found at sample site one: the exceptions to this are the Coleoptera and the Bombus, which were found at the highest number in site two. The calyptrate flies had the most “even” distribution of these eight groups, with 31.25% recorded at sites one and two, and 28.4% recorded at site three. The majority of Apis and Syrphidae were recorded at site one.

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Figure 11: Correlation between number of pollinators and date at sample site one.


Half of these groups were recorded in their lowest abundance at site four, and no group was recorded in its highest abundance at site four.

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3-4: Analysis of the main pollinator ordersEach of the four main pollinator orders (and the four other groups identified as important pollinators) were analysed separately using chi square tests to determine if differences in their visitation rates to the different plant groups were statistically significant. In order to correct for the problem of conducting multiple chi squared tests, a Bonferroni correction was used (Cabin & Mitchell, 2000), which resulted in an altered probability threshold of 0.00625 for these statistical tests during analysis.

Chi squared tests showed a highly statistically significant (P=<0.001) differences in visitation to the different plant groups in the Diptera,

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Figure 12: Proportional abundances of eight pollinator groups across the urban-rural gradient of this study. S2 is the most rural site, S4 is the most urban


Hymenoptera and Coleoptera, but not in the Lepidoptera (2=6.85, DF=6, P=0.33). Highly statistically significant (P=<0.001) chi squared results were also gained from the Apis, Bombus, Syrphidae and calypterate flies with regards to visitations to the different plant groups (see Appendix for the results of all chi squared tests).

Figure 13 displays all of the pollinator groups recorded during the course of the study, with incidental sightings removed (groups recorded at an abundance of one). Of the 55 total groups 21 were incidentally recorded. Figure 13 shows that nine of the 10 most recorded groups were either Diptera or Hymenoptera, with two of these being species or genera of hoverfly.

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Figure 13: Graph displaying the abundances of the different insect groups recorded. The bars are colour coded as follows: Diptera, Hymenoptera, Coleoptera, Lepidoptera, other.


3-4-1: DIPTERAAlmost half (49.83%) of the Diptera recorded were found on Umbellifers. Calypterate flies made up the majority of the Diptera recorded (58.47%); 85.23% of the calypterate flies recorded were found on Umbellifers.

A total of 124 hoverflies (Syrphidae) were recorded from 16 genera: accounting for almost a quarter (24.12%) of all pollinators recorded. The three most recorded hoverfly species were: Eristalis tenax, (38), Sphaerophoria sp (16), and Eristalis pertinax (11). Eristalis species were the most recorded genus of hoverfly, whilst four genera were only recorded once.

Over a quarter (28.23%) of the hoverflies found were recorded on flowers from the genus Senecio, and 48.39% of hoverflies were recorded on genera with yellow flowers (hoverflies made up the majority of Diptera found on yellow flowers, see Figure 14). Chi square tests conducted on the visitations to different plant groups of the four most recorded hoverfly species (Eristalis tenax, Sphaerophoria species, Eristalis pertinax and Episyrphus balteatus) were conducted: only the test conducted on the data for E.tenax was statistically significant (χ2=17.61, df=4, P<0.001).

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3-4-2: HYMENOPTERAThree groups of Hymenoptera accounted for 83.56% of those recorded: Apis, Bombus and the Tenthrenidae. The only other Hymenoptera group with more than 10 individuals recorded were the Andrena.

Tenthrenidae were found exclusively on Umbellifers. The Icheumonidae were also recorded exclusively on Umbellifers but were overall in a lower abundance than the Tenthrenidae.

Apis and Bombus species made up a significant portion of the Hymenoptera recorded, and were the third and fourth largest groups respectively overall. The Bombus species were mostly recorded on the two purple flower groups (Cirsium and Dipsacus): 84.91% of Bombus visitations were on purple flowers. The two flower groups most visited by Apis species were Senecio and Cirsium respectively (75.92% of visitations). None of the other flower genera were visited more than three times by the Apis.

3-4-3: COLEOPTERAFour species of Coleoptera were recorded: Rhagonycha fulva, Oedemera nobilis, Cetonia aurata and Ischonomera cyanea; the last two were only

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Figure 14: Abundance of different groups found on yellow flower genera (Hypochaeris, Jacobea, Melilotus, Senecio, Sonchus, Taxaracum and Tragopogon)

































recorded incidentally. 30 of the 38 Coleoptera recorded were R.fulva, of which 70% were found on Umbellifers. All of the beetle visitations to Cirsium were by R.fulva.

3-4-4: LEPIDOPTERAA total of 26 butterflies were recorded from 11 species making them the least recorded of the four main orders. No one species made up a majority of the number recorded and only five species were recorded more than twice. The two most recorded species were Thymelicus sylvestris (six), and Polyommatus Icarus (four). Lepidopterans were recorded on seven of the 16 plant groups, and were found most on the two purple groups (Cirsium, seven and Dipsacus, five) and Taxaracum species (five), although no one plant group made up the majority of visitations in the Lepidoptera.

4: Discussion

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4-1: Analysis of the UmbellifersThe Umbellifers were the most popular plant group, with a high abundance (40% of total) and diversity (69% of the groups) recorded on this flower group. In particular Umbellifers were important for the Diptera, especially the calyptrate flies, which has been noted before (Pérez-Bañón, Petanidou & Marcos-García, 2007; Memmott, 1999). Like in this study, Lamborn and Ollerton (2000) observed Coleoptera, Hymenoptera and a range of Diptera visiting the Umbellifer Daucus carota. The role of the dark central floret in this species has long been the subject of debate. Eisikowitch (1980) claimed that the dark floret attracted flies by mimicking a resting fly, which would explain the abundance of calyptrate flies found on Umbellifers. Conversely Polte and Reinhold (2013), discarded its role in attracting pollinators altogether.

Whilst it is possible that the dark floret functions to attract insect visitors (in particular Diptera species); the diversity of insect visitors to Umbellifers observed here is likely due to the open design of the umbel, and the shallow structure of the flowers allowing for many generalist (such as Calyptrate flies) as well as specialised flower visitors to forage from them. This theory would explain the diversity of insects observed on Umbellifers in this and other studies. Being pollinated by a variety of different species is likely highly beneficial for Umbellifers as it increases the potential for a large dispersal range for pollen.

4-2: Flower preferences of Diptera4-2-1: FLOWER PREFERENCES OF CALYPTRATE FLIESThe Diptera were by far the largest order recorded (58.56% of total). Whilst the role of Syrphidae in pollination is well known, the calyptrate flies that account for a large proportion of the insect pollinators recorded here (and in general; Proctor, Yeo & Lack, 1996), are often largely understudied. Proctor & Yeo (1973) comment on the role of the Tachinidae, Sarcophagidae and Calliphoridae as frequent flower visitors,

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and also claim the Muscidae to be the most important dipteran pollinators in the UK after the Syrphidae. By contrast this study found the Muscidae to be the least recorded of all the fly families. The reason for this is unknown, though it could be due to the sites sampled.

The Tachinidae were the largest group recorded overall, and were ubiquitous across the sample sites. Like many of the well-known pollinator groups such as the Bombus species, members of this family often have bristly bodies which potentially make them efficient pollinators (Larson, Kevan & Inouye, 2001). Despite being known as flower foragers this family and its relationship with flowers is largely unknown (see previous citation).

The calyptrate flies showed a clear preference for Umbellifers over the other plant groups, with 70.45% of calyptrate fly visitations recorded being to Umbellifers. This observation is supported by significant statistical testing (χ2=55.73, DF=7, P=<0.001). This seems to support the previously mentioned theory that the central black floret found in some members of this group plays a role in attracting insect visitors (Eisikowitch, 1980). Despite this strong preference alongside previous research, this study cannot reliably suggest the reasoning for why Umbellifers are so popular with the calyptrate flies.

4-2-2: FLOWER PREFERENCES OF THE SYRPHIDAEThe Syrphidae accounted for almost a quarter of all the insects recorded: this study has shown the importance of syrphid flies as flower visitors.

Statistical testing on the four most recorded syrphid species (Eristalis tenax, Sphaerophoria species, Eristalis pertinax and Episyrphus balteatus), found that only E.tenax (the drone fly) spent significantly significant periods of time on different flowers (2=17.61, DF=4, P=<0.001), and was found the most on Senecio and other yellow flowers. This indicates a strong preference for yellow in this species, which has been noted by many other researchers previously (Ilse, 1949; Lunau & Wacht, 1994).

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It is assumed that this innate yellow preference is true for all Syrphid flies; however no research has thus far tested the preferences of other species. In this study only E.tenax (out of the four most recorded syrphid species) was recorded the most on a yellow flower genus: Sphaerophoria species was recorded the most on white flowers, and Eristalis pertinax was recorded the most on Umbellifers. The data presented here suggest that the assumed preference for yellow in this family may be an over-generalisation of the innate preference shown by E.tenax (Lunau & Wacht, 1994). Branquart and Hemptinne (2000) suggested that many hoverfly species do not show strong colour preference, instead short corolla, open flower species are favourable. This theory seems to be supported by this study, with genera belonging to the Asteraceae being the most visited by hoverflies (see previous citation).

4-3: Flower preferences of HymenopteraHoneybees (Apis) accounted for 10.5% of all the insects recorded, and are often described as the most important group of insect pollinators (Free, 1993). Conversely, Breeze et al. (2011) presented evidence that although Honeybee numbers have declined in the past 30 years, the yield from insect pollinated crops has risen by 54% since 1984. This, along with the data presented here, suggests that Honeybees are not as important as traditionally thought.

During this study they were recorded the most on Senecio (42.59% of Apis recorded on Senecio. Individual honeybees collect both nectar and pollen (Robinson & Page Jr, 1989), and Proctor, Yeo & Lack (1996) commented on the tendency for honeybees to visit flowers that provide both, such as the Asteraceae (which includes Senecio).

Hill, Wells & Wells (1997) found that honeybees show very strong flower constancy, even if doing so meant sub-optimal rewards, and that the bees would most often become constant on blue or yellow flowers: Apis species may have innate preferences for yellow and blue flowers. Daumer (1956)

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proved trichromatic vision exists in Apis, with wavelength sensitivity peaking at ultraviolet, blue and yellow: however it is extremely difficult to study innate preferences in honeybees, due to the constant stream of information from experienced to inexperienced worker bees influencing the preferences of naïve workers (Lunau & Maier, 1995). Apis were only recorded on Senecio more than once (in this study) at site one, whereas at site four there were recorded nine times on Cirsium and only once on Senecio. Butler (1951) found blue and yellow to be more attractive to honeybees than other colours (as did Hill, Wells & Wells, 1997) which strongly suggests an innate preference for these two colours in honeybees. However it is possible that a combination of the flowers that are locally available and the advanced learning capabilities of honeybees could alter this apparent innate preference in Apis species. For example an abundance of Cirsium at site four could have altered the preference of nearby honeybee hives so that they became constant on Cirsium, though much research would be needed to further support this claim.

The bumblebees (Bombus species) are similar to Apis species: both groups are social, both have sophisticated visual capability (Daumer, 1956), floral scents are important to both groups (Manning, 1957), and both can show strong flower constancy (Waddington, Allen & Heinrich, 1981). One of the key differences between the two genera is that Bombus species on average have longer tongues (Brian, 1957), which leads them to prefer larger flowers and inflorescences with deeper flowers (Ohashi & Yahara, 1998; Comba et al. 1999). Over 80% of visitations by bumblebees (Bombus) in this study were to the purple flowers (Dipsacus and Cirsium), which would suggest a preference for purple in the bumblebees: however these two flower genera had the largest flowers in this study. Therefore it appears that morphology is more important than flower colour for Bombus species.

The Tenthrenidae (a family of sawfly) are notable in this study as the only group that had over ten individuals recorded to be found exclusively on one plant group (the Umbellifers). Sawflies (particularly females) are

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known to occasionally feed on nectar and pollen (Benson, 1950), and some sawfly species are pollen vectors for certain plants particularly the Orchidaceae (Nilsson, 1981), but the species that they have been observed pollinating are not closely related to Umbellifers such as D. carota which they were recorded on in this study. Lamborn & Ollerton (2000) also observed members of the Tenthrenidae visiting Umbellifers, but found that they were not feeding on flower substances but were instead predating on other flower visitors (Gauld & Bolton, 1988).

4-4: Flower preferences of ColeopteraThe abundance of beetles in this study is disproportionate to the taxonomic diversity of the order within the UK. Beetles are likely unimportant as pollinators in the UK: cantharophily is more common in other regions of the world (see Gottsberger, 1989; Maia & Schlindwein, 2006; Dafni et al. 1990)

Rhagonycha fulva (common red soldier beetle) was by far the most common beetle species recorded, and the seventh largest group overall. Their role as occasional generalist pollinators has been noted in the past (Bernhardt. 2000). The majority (70%) of R.fulva recorded were found on Umbellifers. Soldier beetles are known as regular visitors to Umbellifers such as Daucus carota (Lamborn & Ollerton, 2000). Soldier beetle species often mate on flowers (Harde, 2000), and indeed often during the study multiple individuals of R.fulva were found on the same umbel. Therefore it is likely that the visitations of R.fulva to Umbellifers within this experiment were likely for mating opportunities, though still potentially contributes towards pollination. The flowers most visited by the Coleoptera in this study (Umbellifers and Cirsium) seem to validate Delpino’s (1868-75) description of two main types of flowers pollinated by beetles (inflorescences and large flowers).

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4-5: Flower preferences of LepidopteraLepidoptera were the least recorded of the four main orders in this study, accounting for only 5.06% of the total. Whilst this may create the assumption that the Lepidoptera are unimportant as flower visitors, the diurnal nature of the experimental design of this study excludes a large percentage of the Lepidoptera as many species of moth and some species of butterfly are nocturnal. Moths can be effective pollinators (Young, 2002; Raguso & Pichersky, 1995); therefore in order to gain a more complete understanding of the Lepidoptera as pollinators both diurnal and nocturnal species have to be considered.

The Lepidoptera were the only group that did not visit the different plant groups statistically differently (2=6.85, DF=6, P=0.33). In general butterflies prefer flowers with deeper corollas as they forage almost exclusively for nectar (Herrera, 1993; Corbet, 2000; Scoble, 1992), but colour preference seems to vary between species. In this study Thymelicus sylvestris visited Cirsium species the most, whilst Polyommatus icarus visited Taxaracum species most. Butterflies are tetra chromatic (Hovis, 1999), and many can see ultraviolet light wavelengths. Individual species also appear have different peaks in sensitivity in the visible light spectrum (Lunau & Maier, 1995), which means that each species likely has differing colour preferences. These findings serve to illustrate the sophisticated nature of vision in butterflies, and also explain the lack of statistically significant findings for the Lepidoptera in this study.

4-6: The impact of urban cover on insect abundanceA general trend can be observed across the urban-rural gradient of the sample sites in this study: the four main insect pollinator orders (plus the Apis, Bombus, Syrphidae and calyptrate flies) were all found in lower abundances at the more urban sites. Whilst there was moderate negative

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correlation between increased levels of urban cover and flower visitor abundance, statistical testing found no significant relationship (r=-0.48, N=4, P=0.525), likely due to the limited amount of data collected. These different groups are impacted by increased urban cover differently: hoverflies can be significantly reduced with increased urban cover (Geslin et al. 2013), some species of Coleoptera decline in urban areas (Niemelä et al. 2002), and butterflies are often severely reduced in urban areas (Blair & Launer, 1997). Conversely the Apis and Bombus may not be significantly impacted by urbanisation depending on land use: quality of available foraging is more important (Hostetler & McIntyre, 2001; Matteson, Ascher & Langellotto, 2008; Geslin et al. 2013). The Calyptrate flies seemed to be the group least affected by urbanisation as they were found at high abundances (50-55) at sites one, two and three. This is likely due to the close associations between certain fly species, Musca domestica for example, and urban environments (Robinson, 1996).

Whilst steps were taken to standardise the sample sites (see Section 2-1), the amount of different flowers at each sample site clearly had an impact. Site one had an abundance of yellow flowers particularly Senecio, Jacobea and Taxaracum. The majority of the Apis were found at site one; this genus has a preference for yellow (Butler, 1951). Eristalis tenax also has an innate preference for yellow flowers (Ilse, 1949) and over 75% of recordings for this species were at site one. As previously discussed Bombus species have a preference for larger flowers and were recorded most at site two, the only site where the large Dipsacus species were found.

Whilst there does appear to be a general decrease in abundance in insect flower visitor groups with increased levels of urban cover, different groups react differently and the floral assemblage present may also influence the abundance of different groups. This highlights the importance of standardisation in sample sites when analysing the impact of urbanisation on animal groups. This also means that caution must be taken when

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applying the results of this study (or any study on urbanisation and insect abundance) to other areas.

4-7: Flaws and limitationsDuring analysis and research a number of flaws with the experimental design were uncovered.

Half hour sampling sessions possibly led to individuals being recorded multiple times during the same session: shorter sampling sessions are recommended for future studies. Hymenoptera species have much shorter feeding times than most Diptera species which may have also contributed to multiple recordings of certain species as they may spend more time than others foraging.

Moving within the sample site likely disturbed insects despite the two minute habituation period (Campbell et al. 2012). It was noticed that some of the insect groups (for example butterflies) had longer flight initiation distances (FID, see Cooper Jr & Frederick, 2007) than some of the other groups (for example the Coleoptera and calyptrate flies). No research on FID in insects exists and its impact cannot be quantified within this study, but it is possible that this negatively impacted the abundance of butterflies seen.

Visitation to a flower does not equal pollination of said flower. Some of the beetles recorded, for example Cetonia aurata and the Oedemeridae, are destructive flower feeders so likely do not pollinate the flowers they visit (Proctor & Yeo, 1973; Hobby, 1933). Whilst taking photographs during sampling all insects were photographed in order to maximise the amount of data collected, which made it difficult to separate actual pollinators from general flower visitors during the study. Despite this, insects such as the Tenthrenidae and R.fulva which do not collect pollen can still potentially contribute to pollen distribution of certain flowers, due to accidental pollen transfer.

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5: Conclusion and recommendations This study has demonstrated the general preferences of several of the most important pollinator groups in the UK. Table 4 summarises the main findings of this study.

Insect group

General flower preference

Coleoptera Umbellifers due to the open flower structure Do not forage for pollen or nectar, some species

feed destructively on soft flower parts (Proctor & Yeo 1973; Hobby 1933)

Lepidoptera Deep corolla flowers due to the long proboscis length of most species

Each species may have a different colour preference based on the peaks in spectral sensitivity in their eyes across the visible light spectrum (Lunau & Maier 1995)

Bombus species

Preference based on morphology: prefer larger flowers and deep corollas (Ohashi & Yahara 1998; Comba et al 1999)

Apis species Innate preference for yellow (Butler 1951) Preference may change based on available floral

resources near their hiveEristalis tenax Innate preference for yellow (Lunau & Wacht 1994)

This species’ preference seems to have been assumed to be the preference for all hoverflies

Calyptrate flies Umbellifers due to the open flower structure. The central black floret of many Umbellifers could

be an attractant for flies (Eisikowitch 1980)

The Lepidoptera do not appear to have a general colour preference: no one colour of flower accounted for the majority of visitations. Hoverflies were previously thought to have an innate preference for yellow (Lunau & Wacht, 1994) but this study finds this to be largely untrue. Branquart and Hemptinne (2000) theorise that hoverflies prioritise flower morphology

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Table 5: Summary of the main study findings


over colour, which seems to be supported by this study however further research would be needed to test this.

Past research has reliably shown an innate preference for yellow in Apis species (Butler, 1951), however hive preferences could potentially change based on locally available flowers. The calyptrate flies are clearly important flower visitors but they are vastly understudied compared to most other pollinator orders. This limits the capacity to discuss the results of this study regarding these fly families, although the strong preference for umbellifers in these families cannot be disputed, based on the results of this and several other studies (Eisikowitch, 1980; Proctor, Yeo & Lack, 1996; Pérez-Bañón, Petanidou & Marcos-García, 2007; Memmott, 1999).

The Umbellifers are clearly important species for a wealth of insect flower visitors (Lamborn & Ollerton, 2000), although the reason for this is still the subject of debate (Polte & Reinhold, 2013). Umbellifers could potentially be planted in more urban environments to encourage a diverse assemblage of insect flower visitors (Zych, Niemczyk & Niemirski, 2007) and contribute towards combating decline in many pollinator groups.

It is likely that the Hymenoptera are not as important as pollinators as traditionally thought (Free, 1993; Breeze et al. 2011). Whilst their uses in agriculture make them important economically (Southwick & Southwick Jr, 1992); in natural systems the Diptera (particularly the Syrphidae) seem to be the most important flower visitors.

Due to the limited amount of data collected, this study cannot make any significant new observations regarding the relationship between levels of urban cover and abundance of insect flower visitors. Different insect groups are clearly affected by urbanisation in different ways. Local factors (floral assemblage, environment) play a large role in abundances, and this study strains the importance of standardisation of sample sites when assessing the impact of urbanisation. Further studies would be needed to further assess the impact of these variables on abundances of insect groups. This information is vital if the impact of urbanisation on insects is to be fully quantified, understood and combated.

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7: Appendix

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Common name

Plant species Bombus Apis SyrphidaeCalypterate

fliesYarrow Achillea 0 1 6 9

Marigold Calendula 2 2 0 1

Bindweed Calystegia 0 1 4 0Thistle Cirsium 14 18 20 10Morning glory Convolvulus 0 0 2 0Teasel Dipsacus 31 1 3 0Cat's ear Hypochaeris 0 0 2 0Ragwort Jacobea 1 0 5 13Sweet clover Melilotus 0 3 0 0Fleabane Pulicaria 0 0 2 0Blackberry Rubus 0 2 1 0Ragwort & Groundsel Senecio 1 23 35 16

Sow thistle Sonchus 0 0 0 1Dandelion Taxaracum 3 2 15 2Goatsbeard Tragopogon 1 0 3 0Umbell ifers Umbellifers 0 1 26 124

Common name

Plant speciesTOTAL

NUMBERDiptera Hymenoptera Coleoptera Lepidoptera Other

Yarrow Achillea 18 15 1 2 0 0Marigold Calendula 8 1 7 0 0 0Bindweed Calystegia 6 4 1 1 0 0Thistle Cirsium 80 31 36 6 7 0Morning glory Convolvulus 2 2 0 0 0 0Teasel Dipsacus 46 3 35 3 5 0Cat's ear Hypochaeris 3 2 0 1 0 0Ragwort Jacobea 21 18 0 1 2 0Sweet clover Melilotus 3 0 3 0 0 0Fleabane Pulicaria 6 2 0 0 3 1Blackberry Rubus 3 1 2 0 0 0Ragwort & Groundsel Senecio 82 51 28 0 3 0

Sow thistle Sonchus 1 1 0 0 0 0

Dandelion Taxaracum 27 17 5 0 5 0

Goatsbeard Tragopogon 4 3 1 0 0 0

Umbellifers Umbellifers 204 150 27 24 1 2

Tables 5+6: Raw data regarding visitations of different insect groups to different flower groups. The groups are coloured according to their flower colour. The green and blue bars represent the proportional abundance of each group in relation to the other groups.


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Table 7: Chi square test results with regards to group visitation to the different flower groups

Order 2 DF PDiptera 973.94 14 P<0.001Hymenoptera 164.71 10 P<0.001Coleoptera 77.68 6 P<0.001Lepidoptera 6.85 6 0.33Bombus 101.92 6 P<0.001

Apis 108.59 9 P<0.001Syrphidae 152.15 12 P<0.001Calypterate flies 550.73 7 P<0.001

Eristalis tenax 17.61 4 P<0.001Sphaerophoria species

8.5 6 0.2

Eristalis pertinax 3.09 4 0.54Episyrphus balteatus 1 4 0.91


8 : Acknowledgements I would like to thank my dissertation tutor Dr Wendy Harris for her excellent support and aid in constructing this dissertation. I would also like to thank Dr Dan Foreman for his support and suggestions, and also Dr James Bull for his assistance during statistical analysis.

I would like to thank Amy Schwartz, Will Townsend, Carly Green, and the people of the Facebook groups “Insects of Britain and Northern Europe” and “UK Hoverflies” for their aid identifying insects and plants recorded during sampling.

Finally I would thank Emma-Louise Cole, Georgie Davies and Zoe Edwards for their support and constructive criticism throughout.

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Christopher Dyer 707585 Y3 dissertation