# Quantifying the production of plant pollen at the farm scale

Ellen K Wright, Thomas P Timberlake, Mathilde Baude, Ian P Vaughan,

Jane Memmott

► To cite this version:

Ellen K Wright, Thomas P Timberlake, Mathilde Baude, Ian P Vaughan, Jane Memmott. Quantifying the production of plant pollen at the farm scale. New Phytologist, 2024, 242 (6), pp.2888 - 2899. 10.1111/nph.19763. hal-04661010

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# Quantifying the production of plant pollen at the farm scale

Ellen K. Wright¹,², Thomas P. Timberlake¹ ID, Mathilde Baude³,⁴, Ian P. Vaughan⁵ ID and Jane Memmott¹

¹School of Biological Sciences, University of Bristol, Bristol Life Sciences Building, 24 Tyndall Avenue, Bristol, BS8 1TQ, UK; ²Cabot Institute, University of Bristol, Royal Fort House, Bristol, BS8 1UH, UK; ³Université d'Orléans, Château de la Source, BP 6749, Orléans Cedex 2, 45067, France; ⁴Institut d'Ecologie et des Sciences de l'Environnement (IEES-Paris), Sorbonne Université, UPEC, Université Paris Cité, CNRS, IRD, INRAE, Paris, 75005, France; ⁵Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff, CF10 3AX, UK

Author for correspondence:
Thomas Timberlake
Email: thomas.timberlake@bristol.ac.uk

Received: 27 January 2024

Accepted: 27 March 2024

New Phytologist (2024) **242**: 2888–2899

doi: 10.1111/nph.19763

**Key words:** agroecology, farmland, floral longevity, floral resources, flowering phenology, landscape ecology, nectar, pollen, pollinator.

## Summary

* Plant pollen is rich in protein, sterols and lipids, providing crucial nutrition for many pollinators. However, we know very little about the quantity, quality and timing of pollen availability in real landscapes, limiting our ability to improve food supply for pollinators.

* We quantify the floral longevity and pollen production of a whole plant community for the first time, enabling us to calculate daily pollen availability. We combine these data with floral abundance and nectar measures from UK farmland to quantify pollen and nectar production at the landscape scale throughout the year.

* Pollen and nectar production were significantly correlated at the floral unit, and landscape level. The species providing the highest quantity of pollen on farmland were *Salix* spp. (38%), *Filipendula ulmaria* (14%), *Rubus fruticosus* (10%) and *Taraxacum officinale* (9%). Hedge-rows were the most pollen-rich habitats, but permanent pasture provided the majority of pollen at the landscape scale, because of its large area. Pollen and nectar were closely associated in their phenology, with both peaking in late April, before declining steeply in June and remaining low throughout the year.

* Our data provide a starting point for including pollen in floral resource assessments and ensuring the nutritional requirements of pollinators are met in farmland landscapes.

## Introduction

Floral resources (pollen and nectar) are the primary food source for most pollinators and thus a major factor limiting their populations (Roulston & Goodell, 2011; Woodard & Jha, 2017). Decades of agricultural intensification have led to a decline in the quantity, diversity and temporal continuity of floral resources (Baude et al., 2016; Hemberger et al., 2023), likely contributing to parallel rates of decline in many pollinator taxa (Biesmeijer et al., 2006; Powney et al., 2019). Reversing pollinator declines requires us to understand more about where floral resources are located – both in time and in space – and how pollinators are using them so that we can manage landscapes to increase the quantity, quality and seasonal continuity of food for pollinators (Sponsler et al., 2023).

Farmland covers approximately half of the world's habitable land area and > 70% in some countries such as the UK (FAO, 2018). Agricultural expansion and intensification is thought to be the leading driver of pollinator declines (Potts et al., 2010; Goulson et al., 2015; Powney et al., 2019), and yet, it is in our agricultural landscapes that we rely most directly on pollinators, through the services they provide to crop pollination (Klein et al., 2007). Improving agricultural landscapes for pollinators is therefore a high priority and has the potential to deliver

simultaneous benefits for biodiversity and food production. Most pollinator conservation schemes, including those in the UK, focus on increasing the number of flowers in farmland landscapes, often incentivising farmers through payments schemes (Carvell et al., 2007; Natural England, 2009). However, without knowing the existing quantities of pollen and nectar provided by farmland through the year, or the species and habitats that provide these resources, it is difficult to design targeted management interventions that meet the food requirements of pollinators throughout the year (Ogilvie & Forrest, 2017; Timberlake et al., 2019; Sponsler et al., 2023). This may lead to seasonal gaps in their annual forage needs (Timberlake et al., 2019, 2021; Guezen & Forrest, 2021; Jachuła et al., 2021), or potential shortfalls in some of the specific nutrients they require (Vaudo et al., 2015; Filipiak, 2019; Jones & Rader, 2022).

Broadly speaking, pollinators require two types of food from flowers: nectar and pollen. Nectar primarily consists of sugars, which provide much of the energy required by pollinators for flight and thermoregulation, though a range of other important compounds are also found in trace amounts (Willmer, 2011). Pollen, however, is a much more complicated mixture of proteins, lipids, vitamins and minerals (Vaudo et al., 2015). The proteins found in pollen are essential for the growth and development of bee larvae (Ruedenauer et al., 2016; Moerman
et al., 2017), while lipids are required in the formation of phos-
pholipid bilayers, which are important structural features of all
cells (Furse et al., 2023a). If either of these essential nutrients are
in low supply during development, this can lead to negative
effects on adult bee physiology and offspring performance (Kä
mper et al., 2016; Bukovinszky et al., 2017; Rotheray
et al., 2017; Woodard & Jha, 2017). Proteins and lipids comprise
a large proportion of pollen mass, but their relative concentration
differs considerably amongst plant species (Buchman, 1986;
Roulston & Cane, 2000; Donkersley et al., 2014; Vaudo
et al., 2020; Furse et al., 2023b). This variation in the protein:
lipid ratio of pollen is thought to be a major driver of foraging
behaviour in bees (Vaudo et al., 2020, 2024). Despite the
well-established role of pollen in supporting pollinator nutrition
and driving foraging behaviour in bees, we still know very little
about the quantity and phenology of pollen availability in real
landscapes, greatly limiting our ability to improve its supply for
pollinators.

While there are a small number of studies on landscape-level nectar supplies (e.g. Baude et al., 2016; Hicks et al., 2016; Timberlake et al., 2019; Langlois et al., 2020; Tew et al., 2021; Barnsley et al., 2022), equivalent studies on landscape-level pollen supply are lacking (but see Jachuła et al., 2022 for a landscape-level pollen assessment in Poland). This is largely due to the fact that pollen is much harder to measure than nectar. Nectar is a relatively simple sugar solution secreted over time to ensure the replenishment of flowers, so measurements of nectar productivity can be standardised by recording the production of sugar per 24 h, providing a simple common currency for measuring this resource (e.g. Baude et al., 2016). In comparison with nectar, pollen production is much more challenging to measure for two primary reasons. First, it is a solid rather than a liquid, so cannot be easily extracted and quantified. Second, unlike nectar, it is not replenished by flowers but is a finite resource produced only once by each flower and irreversibly depleted when pollinators collect it. This means that in order to quantify daily pollen productivity and avoid double-counting the same pollen from 1 d to the next, it is necessary to measure both the amount of pollen produced by a flower and the number of days the flower remains open (i.e. its floral longevity). Only then can you calculate landscape-level pollen availability per unit time and express it in a way that is relevant to pollinators.

By combining pollen production data and floral longevity
measurements with floral abundance estimates from replicate
farms, our study aimed to quantify farmland pollen production
at the species level, the habitat level and the landscape level
throughout an entire flowering season and compare this with
equivalent values for nectar availability. There were three speci-
fic objectives to our work: (1) measure pollen production
values of farmland plant species and compare these with values
for nectar production; (2) identify the species and habitats that
provide the greatest proportion of farmland pollen throughout
the year and compare these with equivalent values for nectar;
and (3) quantify the phenology of pollen supply at the land-
scape level and compare this with the phenology of nectar
supply.

**Materials and Methods**

The primary goal of our fieldwork was to quantify pollen produc-
tion at the species level, the habitat level and the landscape level,
throughout an entire flowering season. To achieve this, we first
quantified the volume of pollen produced by individual flowers
of a range of common farmland plant species. We then recorded
the floral longevity of each of these plant species to establish how
long the pollen from each flower remains available to pollinators
so that pollen values could be expressed per unit time. We com-
bined these species-level pollen values with floral abundance data
from different farmland habitats on replicate UK farms to calcu-
late pollen availability at the habitat level. Finally, we scaled up to
the landscape level to quantify the phenology of pollen availabil-
ity throughout the year at a whole-farm scale.

Study sites and species

There were two sets of field sites used in this study: one set for
collecting data on species-level pollen production and floral long-
evity, and another set for measuring the phenology of floral abun-
dance in different farmland habitats throughout the year. The
data on species-level pollen production and floral longevity were
collected in various phases from 2011 to 2022 at 24 field sites
located within an 8 km radius of Bristol, UK. These sites were
chosen as they provided a wide range of habitats including pas-
ture, field margins, hedgerows, arable fields, woodlands, public
green space and private gardens, and therefore a wide range of
plant species. The pollen production and floral longevity of a
plant's flowers are less variable traits than a plant's floral abun-
dance or phenology, which are highly influenced by the location
and the time of year; thus, pollen and floral longevity measure-
ments did not need to be made at the same time or location as
the floral abundance measurements. The floral abundance data
were collected in 2017 on three medium-sized (140-280 ha)
mixed (dairy, sheep and arable) farms in Somerset, all located
within a 30 km radius of Bristol, UK. The three farms had
slightly different habitat compositions, but the dominant habitat
types were pasture and arable crops, with hedgerows separating
the fields. Two of the farms contained woodland and two con-
tained field margins, but all other habitat elements (pasture,
hedgerows and arable fields) were present on all three farms (Sup-
porting Information Table S1). Further details of the three farms
can be found in Timberlake et al., 2019, and the floral resource
supply of these sites was found to be broadly representative of the
wider region, falling within the interquartile range of floral
resource supply on 12 farms across the west of England (Timber-
lake et al., 2021).

Quantifying the pollen production and floral longevity of
plant species

The plant species for which we measured pollen production and
floral longevity were selected from the list of species recorded on
the three floral abundance farms in Somerset. To keep the work-
load manageable, we selected the species that contributed 98% of
all floral units across the three farms, resulting in a list of 73 plant species to sample (Table S2). This captured all of the common species while avoiding the labour-intensive sampling of scarce species, which contribute very little to farm-scale floral abundance. One species of 73 (Fallopia japonica Houttuyn) was dropped as only female plants are found in the UK, therefore producing no pollen (this species contributed 1% of all floral units across the three farms). For the remaining 72 plant species (comprising 97% of all floral units), we measured the pollen production and floral longevity of each species at multiple sites across the 24 sampling sites.

**Measuring species-level pollen production** For the 72 common farmland plant species selected in our study, we recorded the total volume of pollen produced by each individual floral unit. This was done by collecting at least 10 stems of unopened flowers in the field, transferring them to a beaker of water in the laboratory to allow them to open in a sterile environment, and then harvesting 25–150 pollen-laden anthers (depending on anther size) from a range of newly opened flowers. For each species, we calculated the mean number of anthers per floral unit, the mean number of pollen grains per anther and calculated the volume of each pollen grain. We then multiplied up these values to calculate the total volume of pollen produced by each floral unit. Although we measure only the volume of each pollen grain, and not the mass, values of pollen volume could theoretically be converted to approximate values of pollen mass using a typical density value for pollen. We define a ‘floral unit’ as one or multiple flowers that can be visited by insects without flying (Carvalheiro *et al.*, 2008); for example, a composite flower head of daisy, *Bellis perennis* L. See Notes S1 for full details of the pollen sampling methodology.

**Measuring species-level floral longevity** For each of the 72 plant species, we recorded the floral longevity of 10–20 individual flowers in two different field sites (though in a few cases, only one site was possible). Flowers were identified while in bud and tagged before opening. If the flower was a composite head containing many individual flowers (e.g. a daisy), individual flowers on multiple flower heads were marked using a permanent marker pen. After marking the flowers, return visits were made to the flower 5 d a week (Monday–Wednesday and Friday–Saturday) to measure their lifespan. Each flower was inspected to determine whether the anthers had dehisced (i.e. when pollen becomes available) and then checked daily to identify the point at which the flower died or dropped its anthers (pollen no longer available). Floral longevity was calculated as the number of days from the anthers dehiscing to the point at which the flower died, or the anthers dropped off – this corresponds to the number of days over which the flower’s pollen is available to pollinators.

**Quantifying daily pollen production** Daily pollen production is defined as the volume of pollen that is available to a pollinator over a 24-h period. This was calculated by dividing the total volume of pollen produced by a floral unit by the mean floral longevity of the species (measured in days). This provides a *per unit time* measure for pollen, which is comparable to the daily

nectar production values listed in Baude *et al.* (2016), Timberlake *et al.* (2019). These daily pollen or nectar values can be multiplied up by daily estimates of floral abundance to calculate the total supply of pollen or nectar at a landscape level.

Recording landscape-level floral abundance

From March to October 2017, each of the three floral abundance farms was visited once per week to record the number of open floral units in each type of semi-natural habitat (permanent pasture, semi-natural woodland, hedgerows and field margins). On each sampling occasion, six 50-m transects were randomly placed in each semi-natural habitat type (e.g. 24 transects in total, for a farm with four habitat types). Ten quadrats of 1 m² were distributed along the transect length at 5-m intervals and the number of open floral units of each flowering plant species within or directly above each quadrat was recorded. For trees and shrubs, all floral units in a 5-m vertical column above the quadrat were counted. Above this, the tree's height within the vertical column was estimated with a clinometer and the floral abundance values were multiplied up accordingly (Baude *et al.*, 2016). Floral abundance values per metre squared were multiplied by the area of each habitat within the sampling sites to provide an estimate of each species' floral abundance at a landscape level. For each plant species, a generalised additive model (GAM) in the R package *MGCV* (Wood, 2010), was used to model a smooth, nonlinear trend in floral abundance over time, allowing floral abundance values to be estimated for all species on any day of the year. A thin-plate regression spline was used to model day of the year, with the degree of smoothing selected using the default generalised cross-validation method (Wood, 2010). These daily floral abundance estimates were then multiplied by the daily pollen production values for each species to calculate the total volume of pollen produced by each plant species over time at the habitat or landscape level.

Addressing the three objectives

**Objective 1: Measure pollen production values of farmland plant species and compare these with values for nectar production** To evaluate the relationship between per-floral-unit nectar and pollen production of the 72 farmland plant species, we regressed daily nectar values (from Baude *et al.*, 2016; Timberlake *et al.*, 2019) against the daily pollen values calculated in this study. A general linear model was used to test for a relationship between the two floral resources and assess the extent to which pollen production can be predicted from nectar production (or vice versa).

**Objective 2: Identify the species and habitats that provide the greatest proportion of farmland pollen throughout the year and compare these with equivalent values for nectar** For each plant species in each habitat, we multiplied their daily pollen production value by their daily floral abundance value to calculate the total volume of pollen produced. These values were then summed across the whole year and across all habitats on the farm to calculate the total annual pollen production of each species at the farm scale. For
each species, we calculated its percentage contribution to total farm-scale pollen production, enabling us to identify the most important species at the landscape level. We repeated this analysis using nectar production values to compare the sets of species, which are most important for the provisioning of each resource. Finally, to compare the resource value of different farmland habitats through the year, we summed the habitat-level pollen production values across all species within a habitat to provide an estimate of the total volume of pollen produced by the plant community of that habitat at a given point in time. Again, this analysis was repeated for nectar data as well, to compare the two resources.

**Objective 3: Quantify the phenology of pollen supply at the landscape level and compare this with the phenology of nectar supply** To quantify the phenology of pollen supply at the landscape level throughout the year, we summed the pollen production values from all habitats on each farm to give an estimate of total landscape-level pollen supply at each sampling time point. Combining values from all three farms, a GAM in the R package *MGCV* (Wood, 2010), was used to model a smooth, nonlinear trend in pollen supply over time. A thin-plate regression spline was used to model day of the year, with the degree of smoothing selected using the default generalised cross-validation method (Wood, 2010). To compare the phenological pattern of pollen and nectar supply at the landscape level, we repeated this analysis using the nectar production values of each plant species. For comparison, we also modelled the phenology of floral abundance alone. The phenological pattern of these three different measures of floral resources (pollen supply, nectar supply and floral abundance) was visually compared to assess their degree of similarity. All analyses were carried out in R, v.3.5.1 (R Core Team, 2022).

## Results

A total of 1316 measurements of floral longevity were recorded from 72 species across the 24 sites. The species recorded were from 23 different families, with Asteraceae making up the largest proportion of these (n = 13). Mean floral longevity values of each species ranged from 1 to 8 d, but the flowers of most species remained open for just 1–4 d and only five species had a mean floral longevity of >5 d; the mean and median values were 2.6 ± 1.4 SD and 2.3 d, respectively (Fig. 1). We collected pollen data from these same 72 species and combined the two data sets to calculate their daily pollen production values; all values are provided in Table S2. Across the three floral abundance farms, we recorded a total of 235 322 floral units from 125 flowering plant species and 97% of these floral units were from our 72 target species. The pollen production data and floral abundance measurements were combined to address the three objectives.

### Objective 1: Measure pollen production of individual farmland plant species and compare them with nectar production values

The mean daily pollen production of the 72 plant species was 16.2 mm³ FU⁻¹ d⁻¹; however, this varied amongst species by

<figure><img src="image_3.png" /><figcaption>**Fig. 1** Floral longevity of most species was between 1 and 3 d, with a mean of 2.6 (vertical dashed line) and only five species with a mean floral longevity value > 5 d. Approximately 10–20 floral longevity records were collected for each species (72 species in total), and a mean value was taken for each species, which is the data summarised in this histogram.</figcaption></figure>

five orders of magnitude, with a standard error of 15.4. The species that produced the highest volume of pollen per floral unit (FU) per day were *Salix* spp. at 1110 mm³ FU⁻¹ d⁻¹, *Heracleum sphondylium* L. (8.6 mm³ FU⁻¹ d⁻¹), and *Cirsium vulgare* L. (6.4 mm³ FU⁻¹ d⁻¹) (Table 1). See Table S2 for a full list of pollen production values. At a floral unit level, there was a significant positive association between the daily pollen and nectar production values of the 72 farmland plant species for which both pollen and nectar data were available (linear model, F₁,₇₁ = 35.33, *P* < 0.001, adjusted R² = 0.326; Fig. 2). This indicates that on average, species that produce large quantities of nectar also produce large quantities of pollen, likely because both resources are broadly correlated with flower size, that is large flowers will produce large amounts of both pollen and nectar. While there is a general positive relationship between pollen and nectar production, there are nevertheless some notable exceptions. For example, *Salix* spp. produced far more pollen than expected based on its nectar production, while *Myosotis arvensis* L. and *Allium ursinum* L. produced far less pollen than expected based on their nectar values. Three species produced no nectar, but still produced pollen: *Filipendula ulmaria* L., *Corylus avellana* L. and *Tripleurospermum inodorum* L.

### Objective 2: Identify the species and habitats that provide the greatest proportion of farmland pollen throughout the year and compare these with equivalent values for nectar

On the three farms, *Salix* spp. produced a mean of 38.2% (± 32.3% SE) of all farm-scale pollen throughout the year.
<table><caption>**Table 1** Daily pollen production per flower and per floral unit (FU) of the top 25 species recorded in the field sites.</caption><thead><tr><th>Plant taxon</th><th>Common name</th><th>Pollen per flower d<sup>-1</sup> mm<sup>-3</sup></th><th>Flowers FU<sup>-1</sup></th><th>Pollen FU<sup>-1</sup> d<sup>-1</sup> mm<sup>-3</sup></th></tr></thead><tbody><tr><td>Salix spp.</td><td>Willow</td><td>4.156</td><td>267.0</td><td>1109.716</td></tr><tr><td>Heracleum sphondylium</td><td>Hogweed</td><td>0.029</td><td>295.6</td><td>8.577</td></tr><tr><td>Cirsium vulgare</td><td>Spear thistle</td><td>0.048</td><td>133.4</td><td>6.378</td></tr><tr><td>Calystegia sepium</td><td>Hedge bindweed</td><td>4.484</td><td>1.0</td><td>4.484</td></tr><tr><td>Arctium agg.</td><td>Lesser burdock</td><td>0.163</td><td>27.2</td><td>4.436</td></tr><tr><td>Sambucus nigra</td><td>Elderflower</td><td>0.016</td><td>224.8</td><td>3.518</td></tr><tr><td>Centaurea nigra</td><td>Common knapweed</td><td>0.062</td><td>53.8</td><td>3.321</td></tr><tr><td>Taraxacum officinale</td><td>Dandelion</td><td>0.014</td><td>216.4</td><td>3.134</td></tr><tr><td>Filipendula ulmaria</td><td>Meadowsweet</td><td>0.050</td><td>57.0</td><td>2.828</td></tr><tr><td>Rosa canina</td><td>Dog rose</td><td>2.194</td><td>1.0</td><td>2.194</td></tr><tr><td>Anthriscus sylvestris</td><td>Cow parsley</td><td>0.016</td><td>119.5</td><td>1.966</td></tr><tr><td>Cirsium palustre</td><td>Marsh thistle</td><td>0.025</td><td>59.6</td><td>1.470</td></tr><tr><td>Rubus fruticosus</td><td>Bramble</td><td>1.339</td><td>1.0</td><td>1.339</td></tr><tr><td>Impatiens glandulifera</td><td>Himalayan Balsam</td><td>1.338</td><td>1.0</td><td>1.338</td></tr><tr><td>Cerastium fontanum</td><td>Mouse-ear chickweed</td><td>1.284</td><td>1.0</td><td>1.284</td></tr><tr><td>Cirsium arvense</td><td>Creeping thistle</td><td>0.010</td><td>113.4</td><td>1.173</td></tr><tr><td>Bellis perennis</td><td>Daisy</td><td>0.012</td><td>95.0</td><td>1.115</td></tr><tr><td>Lonicera periclymenum</td><td>Honeysuckle</td><td>1.038</td><td>1.0</td><td>1.038</td></tr><tr><td>Hypochaeris radicata</td><td>Catsear</td><td>0.014</td><td>57.8</td><td>0.828</td></tr><tr><td>Ranunculus ficaria</td><td>Lesser celendine</td><td>0.743</td><td>1.0</td><td>0.743</td></tr><tr><td>Epilobium hirsutum</td><td>Great willowherb</td><td>0.611</td><td>1.0</td><td>0.611</td></tr><tr><td>Sonchus oleraceus</td><td>Smooth sowthistle</td><td>0.005</td><td>116.9</td><td>0.567</td></tr><tr><td>Ranunculus repens</td><td>Creeping buttercup</td><td>0.552</td><td>1.0</td><td>0.552</td></tr><tr><td>Convolvulus arvensis</td><td>Field bindweed</td><td>0.354</td><td>1.0</td><td>0.354</td></tr><tr><td>Achillea millefolium</td><td>Yarrow</td><td>0.001</td><td>381.6</td><td>0.326</td></tr></tbody></table>

Species are listed in order of highest to lowest daily pollen production per floral unit.

<figure><img src="image_4.png" /><figcaption>**Fig. 2** Nectar and pollen production show a strong and significant association at the floral unit level ($F_{1,71} = 35.33, P < 0.001$, adj. $R^2 = 0.326$), likely because they both also correlate with floral unit size. Despite this relationship, a number of species (labelled individually by name) fall relatively far from the regression line (blue line ±95% confidence intervals) demonstrating the value of one resource cannot always be predicted from the other. Note the log scale on each axis, though the scale has been back-transformed to show absolute (rather than log-transformed) values for each resource. The regression equation is shown at the top left of the figure.</figcaption></figure>

However, this was highly variable amongst farms and very short-lived, being primarily limited to early April. After this, *Filipendula ulmaria*, *Rubus fruticosus* L. and *Taraxacum officinale* agg. (Weber) were the most important contributors to annual farm-scale pollen supply (Fig. 3); this was available for a longer period of the year and was more consistent amongst farms. The species that were most important for annual pollen provisioning were quite different from those that were most important for

nectar provisioning; however, *Rubus fruticosus*, *Taraxacum officinale* and *Centaurea nigra* L. were important providers of both resources at the farm scale (Fig. 3).

The habitats that provided the greatest proportion of pollen throughout the year varied depending on the scale at which pollen was expressed. Per square metre unit area, hedgerows provided the highest quantity of pollen, followed by field margins and woodland, with pasture providing the smallest amount
<figure><img src="image_5.png" /><figcaption>**Fig. 3** Plant species providing most of the pollen at a farm-scale differ from those which provide most of the nectar. Graph shows the percentage contributions of key plant species to annual farm-scale pollen (upper panel) and nectar (lower panel) supply. Values show a mean (±SE) across the three study farms. For clarity, only the top 20 species are shown for each resource.</figcaption></figure>

(Fig. 4). However, when scaled up to the level of the whole farm, pasture provided the majority of pollen, followed by woodland, hedgerows and field margins (Fig. 4). This difference occurs because pasture, while low in resources, covers by far the largest area of the farms (Table S1). Habitats varied in their pollen production value throughout the year; however, pasture remained the main provider of pollen at the farm scale throughout most of

the year, until the end of September when woodland habitats (with a high abundance of late-flowering ivy) became a major source of pollen (Figs 5, S1). The pollen and nectar production of different habitats show a similar pattern of relative importance on an annual basis (Fig. 4) and through the year (Figs 5, S1) – this is true at both the metre-squared scale and the whole-farm scale.
<figure><img src="image_6.png" /><figcaption>**Fig. 4** Farmland habitats show similar patterns of relative importance in their annual supply of pollen and nectar. Annual nectar production (top) and pollen production (bottom) of farmland habitats are expressed per metre-squared unit area (left) and per km² of farmland (right). Bars show the mean ± SE of the three study farms.</figcaption></figure>

<figure><img src="image_7.png" /><figcaption>**Fig. 5** Relative importance of each habitat in their provision of nectar (upper row) and pollen (lower row) differs substantially through the year, but remains relatively similar between the two resources. The left-hand column shows values at the metre-squared level while the right-hand row shows values at the km² (landscape level). Hedgerows provide the greatest contribution to pollen and nectar supply at the unit-area level while pasture provides the greatest contribution of both resources at the landscape level, due to its high coverage of the landscape. See Supporting Information Fig. S1 for the absolute values of pollen and nectar provided by each habitat through the year.</figcaption></figure>
Objective 3: Quantify the phenology of pollen supply at the landscape level and compare this with the phenology of nectar supply

Farmland pollen availability showed a strongly seasonal pattern with a large spring bloom peaking in April, followed by a steep decline in June and then remaining relatively low throughout the year (Fig. 6). The phenology of pollen and nectar supply were remarkably similar at a landscape level, which is not surprising given that the availability of both resources is largely driven by the abundance of flowers in the landscape (Fig. 6a). However, the magnitude of the peaks and troughs differed slightly between the two resources. After the spring peak of pollen and nectar production, pollen supply dropped more slowly than nectar,

buffered in part by the blooming of *Filipendula ulmaria*. This results in a less obvious 'June Gap' and more steady decline through to August, compared with a clear trough and then mini-peak in July for nectar production. These differences are driven by the specific identity of the flowering species, as while pollen and nectar are broadly correlated, there are exceptions to this (Fig. 2), and these exceptions will alter the magnitude of peaks and troughs. The phenology of floral abundance showed a similar pattern to both pollen and nectar supply, but there was a much more obvious peak in the late summer (September/October), which was largely driven by ivy, *Hedera helix* L., which produces a very large number of flowers, but relatively small amounts of nectar sugar and pollen per-flower.

<figure><img src="image_8.png" /><figcaption>**Fig. 6** Quantity of pollen, nectar and floral units all follow a similar seasonal pattern on farmland. Graph shows the phenology of three different measures of farmland floral resources: (a) number of floral units; (b) mass of nectar sugar and (c) volume of pollen, at a whole-farm scale throughout the flowering season. Points represent individual sampling events on the three study farms (Birches, Eastwood and Elmtree) and the data from all three farms are smoothed with a generalised additive model (±SE; dashed lines).</figcaption></figure>

Discussion

In this study, we recorded the pollen production of common farmland plant species and combined these data with floral longevity values and floral abundance data to characterise and quantify daily pollen production at the species, habitat and landscape scale. The results show that the flowers of most plant species produce pollen for between 1 and 4 d and that the daily pollen production of individual plant species is significantly correlated with their daily nectar production. Willows (*Salix* spp.) produced around one-third of all pollen at a landscape scale (perhaps because they are partially wind-pollinated), but this was very short-lived, and many other species were important for maintaining pollen supply through the year. Per unit area, hedgerows provided the highest quantity of both pollen and nectar, but at the landscape level, pasture and woodland provided the highest quantity due to their high landscape coverage. The phenology of pollen production at the farm scale showed a broadly similar trend to nectar production, though the 'June gap' (a period of relatively low nectar production reported by European beekeepers during June) was much less pronounced for pollen than for nectar. In general, landscape-level pollen and nectar availability are relatively good proxies for one another, though the species providing most of the landscape-scale pollen are not the same as those providing most of the nectar. In what follows, we consider the limitations of the study, put our results into the context of previous research in this field and consider some recommendations for management and possible future research directions.

Limitations

There are three main limitations to our research. First, the phenology work is based on 1 yr floral counts, and there is no measure of year-to-year variation in flowering, which may occur due to variation in weather conditions and farm management. The general patterns and dominant species are likely to be broadly conserved from year to year however (Timberlake *et al.*, 2019). Second, we only collected data on the *volume* of pollen and not the *mass* or nutritional *quality*. Pollen quantity alone may not provide the most relevant measure of pollinator requirements as pollen varies substantially amongst species in its nutritional value (Vaudo *et al.*, 2015). Data on the nutritional content of
pollen are currently limited for whole plant communities,
although it could be readily combined with these data when it
becomes available. Third, we do not include any wind-pollinated
species such as grasses in our assessments of pollen availability,
though pollinators are occasionally known to consume pollen
from these plants. Thus, our estimates of pollen availability may
represent a slight under-estimate of the true quantity of pollen
available to insects.

Pollen availability through the year

While there is very little floral longevity data for the UK, there
are some studies from the rest of the world. For example, Song
et al. (2022) collates information from over 416 papers, many of
which studied the floral longevity of species in Asia and the
Americas. Few of these studies include any pollen data though,
making it impossible to calculate daily pollen production.
Indeed, aside from a handful of studies, pollen production is
rarely quantified at all, despite being a vital component of polli-
nator nutrition. By recording both the pollen production and
floral longevity values of a whole community of common farm-
land plants, we are able to calculate their daily pollen production
values and quantify pollen resources at a landscape level. Similar
to the nectar production data reported by Timberlake
et al. (2019), our data show that that even though hedgerows pro-
duce the highest volume of pollen per unit area, their contribu-
tion to landscape-level floral resource production is relatively
low, due to their low coverage of the landscape. By contrast, pas-
ture has the lowest pollen production per unit area, but the high-
est landscape-level production of pollen, due to its high coverage
of UK farmland. Farmland pasture covers c. 40% of UK land
(GOV, 2015) and has become less florally diverse over time due
to increased fertiliser use and the shift from hay to sileage produc-
tion (Woodcock et al., 2014). This reduction in floral diversity
and abundance is thought to have played an important role in
reducing the abundance and diversity of pollinators on farmland
(Carvell et al., 2006; Wratten et al., 2012; Jönsson et al., 2015).
It should be noted that although we can quantify the supply of
pollen through the year, our understanding of pollen demand by
bees and other insects is highly limited, making it difficult to
infer anything about the limitation of this resource at different
times of year (Sponsler et al., 2023). In the absence of detailed
data on pollinator nutritional requirements, other approaches
can be used to assess resource limitation including foraging assays
(Sponsler et al., 2020) and pollen depletion studies (Harris
et al., 2023).

Comparing nectar and pollen availability

Nectar and pollen are broadly correlated at the floral-unit level,
likely due to their co-variance with floral unit size. The floral
organs that produce pollen and nectar are likely to be scaled up
in larger flowers, resulting in a greater production of both
resources. Moreover, in cases where floral units are comprised of
many individual flowers (such as *Salix* spp. and Asteraceae spp.),
both pollen and nectar are multiplied up by the number of

individual flowers, and will both therefore co-vary with flower
number. Despite this general pattern of association, there were
several species that did not conform closely to the regression line,
meaning the supply of one resource could not be reliably pre-
dicted from the other; these included *Salix* spp., *Myosotis arvensis*
and *Allium ursinum*. When scaling up to the landscape level, the
phenology of pollen and nectar supply were also closely corre-
lated due to the fact that both resources are largely determined by
floral abundance. Although our data enable us to quantify daily
pollen production at the landscape scale, the nutrient content of
pollen remains largely unknown, preventing a full assessment
of nutrient availability through the year. While there is some
information published on specific nutrients contained within pol-
len, for example by Todd & Bretherick (1942), Roulston &
Cane (2000), Vaudo *et al.* (2020), these studies focus on a small
subset of plant taxa and do not provide an overall picture of the
pollen nutrients available to foraging pollinators. Moreover,
many of the studies on pollen focus on the pollen collected by
bees, which is mixed with nectar and bee secretions and so does
not give an accurate estimation of its nutrient content (Kostić
et al., 2015; Taha, 2015; Li *et al.*, 2018). Looking forward,
improving our understanding of the nutrient content of pollen is
an important research area in need of further study.

Conservation implications

Management strategies implemented by the UK Government for
improving pollinator resources mainly focus on creating field mar-
gins planted with wildflowers and reduced mowing (Natural Eng-
land, 2012; DAERA, 2022). Although these areas do provide
floral-rich habitats, which have been found to improve pollinator
abundance (Haaland et al., 2011; Jönsson et al., 2015), they repre-
sent a tiny percentage of most farmland habitats and Baude
et al. (2016) report that they contribute a trivial amount of nectar.
Of the three study farms within this study, only Birches and Elm-
tree had field margins, and they comprised just 1% of the land on
the farms. Hedgerows provide high quantities of pollen and nectar
per unit area and have been found to support high bee richness as
well as facilitating the movement of pollinators across agricultural
landscapes (Cranmer et al., 2012; Dicks et al., 2015; Sardiñas &
Kremen, 2015). However, they also make up a very small percen-
tage of most farmland landscapes; in our case, c. 5% of each farm.
Focussing on improving pollinator resources in the widespread
habitats such as pasture may be a more effective way in increasing
the abundance of pollinators within farmland landscapes (Orford
et al., 2016; EIPWALES, 2021). Overall though, both the
improvement of existing habitats such as pasture and further devel-
opment of floral-rich field margins and hedgerows are key ways to
improve pollinator resource availability on farms. Our results show
that a few key species including *Salix* spp., *Filipendula ulmaria*,
*Rubus fruticosus* and *Taraxacum officinale* provide a very large pro-
portion of farmland pollen and may therefore offer particularly
important targets for conservation. Losing these species could have
profound consequences for the community of pollinators – parti-
cularly bees – which would likely lose a large proportion of their
protein and lipid supply. On the other hand, increasing the
abundance of these pollen-rich plant species on farmland – includ-
ing shrubs and trees such as willow – is likely to greatly benefit
populations of farmland pollinators.

Conclusion

Quantifying the pollen production, floral longevity and floral
abundance of a whole community of common farmland plants
throughout the year enabled us to conduct the first landscape-level
assessment of pollen supply in the UK. Looking ahead, this
approach – especially in combination with measures of pollen
nutritive value and information on the nutritional requirements of
pollinators – will provide more targeted approaches for conserving
pollinators and the pollination services they provide.

Acknowledgements

This work was supported by the Lady Emily Smyth Scholarship
Foundation from the University of Bristol and the UK Natural
Environment Research Council (NERC) through the NERC
GW4+ Doctoral Training Partnership (NE/L002434/1). We
thank the farmers and land owners who gave us permission to
survey their properties, and Vicky Palumbo for helping with the
pollen analysis for the field collected samples.

Competing interests

None declared.

Author contributions

JM, TPT and EKW conceived the ideas and designed the metho-
dology. EKW collected the floral longevity data. TPT collected
the floral abundance data. MB and EKW collected the pollen
data. EKW, TPT and IPV analysed the data. EKW and TPT led
the writing of the manuscript. All authors contributed critically
to drafts and gave final approval for publication.

ORCID

Thomas P. Timberlake ID https://orcid.org/0000-0001-8166-0825

Ian P. Vaughan ID https://orcid.org/0000-0002-7263-3822

Data availability

Fully reproducible R script and source data are available from:
https://github.com/tom-timberlake/farm_pollen. Pollen volume
and floral longevity values for all 72 plant species in this study are
available in Table S2.

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## Supporting Information

Additional Supporting Information may be found online in the Supporting Information section at the end of the article.

**Fig. S1** Phenology of pollen and nectar supply in each farmland habitat.

**Notes S1** Detailed methods for collecting and quantifying pollen volume.
**Table S1** Habitat composition of each of the three study farms.

**Table S2** Pollen volume and floral longevity values of all 72 plant species in the study.

Please note: Wiley is not responsible for the content or function-
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queries (other than missing material) should be directed to the
*New Phytologist* Central Office.