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Assessing pollinators use of floral resource subsidies in agri-environment schemes: An illustration using Phacelia tanacetifolia and honeybees Rowan Sprague 1, Stéphane Boyer 1,2, Georgia M. Stevenson
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Assessing pollinators use of floral resource subsidies in agri-environment schemes: An illustration using Phacelia tanacetifolia and honeybees Rowan Sprague 1, Stéphane Boyer 1,2, Georgia M. Stevenson 3 and Steve D. Wratten 1 1 Bio-Protection Research Centre, Lincoln University, Christchurch, New Zealand 2 Environmental and Animal Sciences, Unitec Institute of Technology, Auckland, New Zealand 3 Department of Ecology, Lincoln University, Christchurch, New Zealand Submitted 27 June 2016 Accepted 12 October 2016 Published 15 November 2016 Corresponding author Rowan Sprague, Academic editor Giovanni Benelli Additional Information and Declarations can be found on page 11 DOI /peerj.2677 Copyright 2016 Sprague et al. Distributed under Creative Commons CC-BY 4.0 ABSTRACT Background: Honeybees (Apis mellifera L.) are frequently used in agriculture for pollination services because of their abundance, generalist floral preferences, ease of management and hive transport. However, their populations are declining in many countries. Agri-Environment Schemes (AES) are being implemented in agricultural systems to combat the decline in populations of pollinators and other insects. Despite AES being increasingly embedded in policy and budgets, scientific assessments of many of these schemes still are lacking, and only a few studies have examined the extent to which insect pollinators use the floral enhancements that are part of AES and on which floral components they feed (i.e., pollen and/or nectar). Methods: In the present work, we used a combination of observations on honeybee foraging for nectar/pollen from the Californian annual plant Phacelia tanacetifolia in the field, collection of pollen pellets from hives, and pollen identification, to assess the value of adding phacelia to an agro-ecosystem to benefit honeybees. Results: It was found that phacelia pollen was almost never taken by honeybees. The work here demonstrates that honeybees may not use the floral enhancements added to a landscape as expected and points to the need for more careful assessments of what resources are used by honeybees in AES and understanding the role, if any, which AES play in enhancing pollinator fitness. Discussion: We recommend using the methodology in this paper to explore the efficacy of AES before particular flowering species are adopted more widely to give a more complete illustration of the actual efficacy of AES. Subjects Agricultural Science, Biodiversity, Ecology, Science Policy Keywords Apis mellifera, Honeybee foraging behaviour, Agroecosystems, Pollen preference, Floral enhancements, Pollinator health strategies INTRODUCTION As many as 70% of crop species worldwide benefit directly or indirectly from pollination by animals (Klein et al., 2007), with insects contributing the most to this ecosystem service (ES). Of these pollinators, honeybees (Apis mellifera L.) are used most frequently in agriculture for pollination services because of their abundance, generalist floral How to cite this article Sprague et al. (2016), Assessing pollinators use of floral resource subsidies in agri-environment schemes: An illustration using Phacelia tanacetifolia and honeybees. PeerJ 4:e2677; DOI /peerj.2677 preferences, ease of management and transport of hives, and revenue-generating by-products (Tautz, 2008; Aizen & Harder, 2009; Potts et al., 2010a). Although the significance of unmanaged insects in crop pollination has been increasingly recognised (Winfree et al., 2008; Rader et al., 2009; Woodcock et al., 2013), reliance on honeybees has increased in recent decades in response to rising pollination needs and overall population declines of pollinators (Aizen et al., 2008; Breeze et al., 2011). While demand for this ES is high, honeybee populations are declining in many countries, including the United States, Canada, the UK and Germany (Potts et al., 2010a; Potts et al., 2010b; van der Zee et al., 2012; vanengelsdorp et al., 2012). No single cause of this decline has been identified; rather, several factors are involved, notably varroa mites (Varroa destructor) (Sammataro, Gerson & Needham, 2000; Shen et al., 2005), pathogens such as American foulbrood (caused by the bacterium Paenibacillus spp.) (Genersch, 2010), fungal parasites such as Nosema (Potts et al., 2010a; Pettis et al., 2013), loss of biodiversity and associated floral resources in agricultural systems (Kremen et al., 2007; Klein et al., 2007; Potts et al., 2010a), and the use of neonicotinoid pesticides (vanengelsdorp & Meixner, 2010; Potts et al., 2010a; Goulson, 2013). Agri-environment schemes (AES) have been developed to mitigate some of these declines in ES, and this paper provides an illustration of how the value of such schemes for pollinators can be better assessed. What are agri-environment schemes, and how effective are they? In response to pollinator population declines, the European Commission has recommended programmes aimed at improving pollinator fitness and efficacy as part of the wider fiscal policy of AES. Originating from the 1980s to protect biodiversity and important cultural areas in England, these schemes attempt to inform landowners and policy makers on methods to manage land sustainably and enhance ES (Natural England, 2012). Included in this policy are methods that claim to benefit pollinators such as bees and butterflies (Natural England, 2013a; Natural England, 2013b). The methods recommended to improve pollinator fitness and efficacy do not usually involve crops which need to be pollinated by insects, but rather are usually a mix of wildflowers selected because of their high nectar and/or pollen quality planted in the field margins beside crops. AES have evolved over time to incorporate more tractable ways for farmers to become involved and to include more management recommendations to enhance a range of multiple ES; examples include beetle banks or habitats for beetles (Thomas, Wratten & Sotherton, 1992) and buffer strips of wildflowers between croplands (Department for Environment, Food Rural Affairs & UK Government, 2014). By 2009, about 66% of England s agricultural land was managed as part of AES agreements (Natural England, 2009). Other countries are also attempting to address the issue of pollinator decline. Recently the US Federal Government also proposed the Pollinator Health Strategy 2015, which seeks to improve the health of honeybees and native pollinators, and restore land to be used as pollinator habitat. Differing from the AES Environmental Stewardship Handbooks which guide farmers on how to implement AES, this report acknowledged the Sprague et al. (2016), PeerJ, DOI /peerj /15 elements in its strategy which need to be researched before the government can recommend more effective policies (Vilsack & McCarthy, 2015). Despite AES being increasingly embedded in policy and budgets, scientific assessments of many of these schemes still are lacking, such as quantifying the type, extent and quality of ES actually delivered (Kleijn & Sutherland, 2003; Kleijn et al., 2006; Whittingham, 2007). Also, few studies have examined the extent to which insect pollinators use the floral enhancements and whether the added resources serve as shelter, nest sites or pollen/nectar resources. In a study by Holland et al. (2015), researchers found that farm management, such as establishing florally-enhanced grass areas, and the amount of uncropped habitats can positively affect the species richness and abundance of insect populations. An example of an AES approach which specifically targets pollinators is that by Pywell et al. (2006), who found that bumblebees (Bombus spp.) benefited from wildflower mixes and mixes of flowers with known high-quality pollen and nectar through increased abundance and species richness. However, this study did not examine how the Bombus spp. used the added floral resources and whether the bumblebees preferred the added flowers. This raises a key issue with studies of insect pollinators through floral enhancement schemes. These schemes often lack comparisons of how these insects use the added floral resources compared to the other surrounding flowers. For example, there need to be more studies assessing the extent to which pollinators prefer particular added flowers, their relative use of pollen and nectar on each plant species visited, diurnal and seasonal use of the resource, the value of the added flowers for other beneficial arthropods, and any associated ecosystem disservices (e.g., weediness potential) if these potential AES are to be adopted (Zhang et al., 2007; Wielgoss et al., 2014). Our study aims to addresses a key part of this issue, that of examining how and to what extent honeybees use the Californian annual plant Phacelia tanacetifolia (Bentham: Borginaceae; tansy leaf). Farmers and policy makers need to have a clear and straightforward way to assess the values of AES implemented on farms. In the present work, we used a combination of observations on honeybee foraging for nectar/pollen from Phacelia tanacetifolia and collection of pollen pellets from nearby hives to assess the value of adding phacelia to an agro-ecosystem to benefit honeybees. Honeybees as the study organisms Honeybees were used here not only because of their agricultural importance, but also because of their distinct foraging behaviours. Individuals collect pollen by gathering the grains from the anthers of flowers and they use nectar to keep the grains together. They carry the pollen in pollen baskets (corbiculae) on their hind legs, forming pellets of pollen grains (Tautz, 2008). These bees demonstrate floral constancy, meaning that individual foraging bees will visit only one species of flower on any one day, sometimes even over several days (Free, 1963). As a result of this constancy, there is a 95 99% likelihood that a pellet will comprise pollen from only one species (Tautz, 2008). There are a few studies that explore the use of AES by honeybees and the potential ways in which they benefit from them. Couvillon, Schürch & Ratnieks (2014) examined Sprague et al. (2016), PeerJ, DOI /peerj /15 honeybee waggle dance patterns to determine where they forage in landscapes containing different types of AES, as well as areas without any such stewardship measures. They found that these insects showed a significant foraging preference for Higher Level Stewardship sites, or sites that met more complex requirements to address local needs and provide more than one ES (Couvillon, Schürch & Ratnieks, 2014). However, this study did not explore whether or not this preference was correlated with the type and quantity of floral resources available. Balfour et al. (2015) also examined honeybee waggle dance patterns and the surrounding available flowers for pollinators to determine where honeybees were foraging and which habitat and flower types in which they were most abundant. They found that honeybees were mostly found in field margins and hedgerows and that they foraged mainly for agricultural weeds. This study did not examine specifically whether honeybees preferred certain flowers over others and it did not take place where flowers had been added to enhance honeybee fitness or efficacy. Carvell et al. (2007) found that bumblebee species abundance and diversity increased in response to field margins with legumes providing pollen and nectar, but they concluded that a more diverse mix of flowers should be planted to offer a range of blooming durations and flower phenology. Few studies have examined the foraging preference of honeybees, or lack thereof, for particular plant species providing floral resources in an agricultural context, and no studies have examined honeybee preference for floral resources in AES guidelines to test and better inform AES field and crop margin design. We did not study wild bees (native or bumblebees) in this study, as assessments of their preferences and colony fitness would be difficult due to their different life cycles and access to their nests compared to managed honeybee colonies. Here, we used phacelia as a potential supplementary floral resource because this species is commonly included in florally-enhanced field margins AES (Carreck & Williams, 2002; Decourtye, Mader & Desneux, 2010). It is a high-quality honey plant (Crane, Walker & Day, 1984) and a wide range of insect species forage on it (Carreck & Williams, 1997). Its pollen is said to have a high protein content (Trees for Bees, 2014) and its nectar and pollen improve the predation rate of insect biological control agents, including hoverflies (Diptera: Syrphidae) (Hickman & Wratten, 1996; Laubertie, Wratten & Hemptinne, 2012). For example, Laubertie, Wratten & Hemptinne (2012) compared how six different flowers (phacelia, buckwheat, coriander, alyssum, mustard, and marigold) commonly used as floral enhancements improved the fitness of hoverflies, and they found that phacelia overall improved fitness the most. For these reasons, we chose to use phacelia as our test flower species. MATERIALS AND METHODS Field site The field site was located on the Canterbury Plains, New Zealand within an agricultural landscape (latitude: , longitude: ). A single strip of P. tanacetifolia cv. Balo 8 m long and 1.5 m wide was sown every two weeks to ensure a continuous flowering period of at least six weeks. The honeybee hives used for this experiment were located about 25 m from the sown flowers. Two healthy hives with Sprague et al. (2016), PeerJ, DOI /peerj /15 queens of similar age of 1 2 years old (determined by the beekeeper) were chosen, as the age of queens affects the pollen demand of the colony and thus the extent of pollen foraging (Tautz, 2008). While the site was modelled after AES guidelines for the UK, recommendations of enhancing agricultural landscapes with wildflowers or known insect-beneficial flowers are similar throughout many countries. Therefore the results from this study should be generalizable to other countries. Pollen collection Pollen traps (Dimou & Thrasyvoulou, 2007) were installed on both hives. Pollen pellets were collected every day on which no rain had fallen and which had a maximum air temperature at or above 14 C (a total of twelve days between 7 November and 9 December 2014). Honeybees do not leave the hive to forage when the outside air temperature is below 11 C or it is raining (Dimou, Thrasyvoulou & Tsirakoglou, 2006). The main entrance of the pollen traps was closed at 11:00 h and opened again at 13:00 h to collect all the pollen which the foraging bees brought back to the hive during this 2-h period. This period was selected because honeybee foraging activity is high during the middle of the day (García-García, Ortiz & Dapena, 2004) and because this period was likely to include those plant species for which the bees foraged in the morning and the afternoon. The pollen pellets from each of the hives were collected at the end of the 2-h period and placed in separate 25 ml containers and stored at -20 C to eliminate fungal growth. The pollen pellets from one of the hives during one of the 2-h periods was considered to be one sample. Species identification from pollen samples The pellets in each sample were weighed together and counted. The purple ones were separated from the others using forceps and placed in individual tubes, as the purple colour is indicative of P. tanacetifolia pollen and no other known flowers in the area were thought to produce purple pollen. To confirm that the purple pellets collected really did comprise phacelia pollen, DNA barcoding with ITS primers was used to verify the species identity of the P. tanacetifolia pollen pellets. Observations of honeybees foraging on P. tanacetifolia The extent of the use of P. tanacetifolia by honeybees was examined through the pollen brought back to the hive and through the worker bees behaviour in the field. The numbers of honeybees foraging for nectar and pollen, respectively, were observed visually and counted in a 10 m 2 area over 5-min periods at 10:00, 12:00, and 15:00 for ten days between mid-december to end of January depending on weather conditions. Bumblebees were also visually counted to see whether other pollinators were also foraging on the phacelia. Twenty flowers of P. tanacetifolia were chosen randomly and the quantity of pollen on the anthers was scored; the scoring scale is shown in Table 1. The ages of the P. tanacetifolia flowers were also scored using the four stages defined by Williams (1997); this scoring scale is shown in Table 2. Sprague et al. (2016), PeerJ, DOI /peerj /15 Table 1 Scores for amount of pollen on P. tanacetifolia flowers. In brackets: percentage of the anther covered with pollen. Amount of pollen Score No visible pollen (0%) 0 Small amount of visible pollen (25%) 1 Some visible pollen (50%) 2 Large amount of visible pollen (75 100%) 3 Table 2 Score for maturity of P. tanacetifolia flowers (from Williams, 1997). Maturity of flowers Score Just-opened flower (Stage 1: curled filaments and style) 1 Mid-age flower (Stage 2: filaments uncurled and petals at about 60 ) 2 Mid-age-old flower (Stage 3: petals at about 20 60, styles longer than filaments) 3 Older flower (Stage 4: petals closing, some anthers may have fallen off the filaments) 4 Since the area of P. tanacetifolia flowers blooming changed throughout the experiment because of the sequential drilling, honeybee counts were divided by the area of flowers present on each date. Data analysis For the pollen pellet collection experiment, we analysed the count data to determine whether the total number of phacelia pollen pellets collected was significant compared to the total overall number of pellets. For our field observation experiments, to see if the number of honeybees foraging for nectar differed from the number of honeybees foraging for pollen, we used a paired two-tailed t-test. To test whether the number of honeybees foraging for nectar and for pollen varied with the time of day, the maturity of the flowers, and the amount of pollen on the flowers, a mixed effects linear model was used to account for the day on which the observations were taken. The data were bootstrapped to determine the 95% confidence intervals around the data. Likelihood Ratio Tests were used to determine which of these factors (if any) was significant for pollen and nectar foraging bees. We also used a mixed effects linear model to test whether the total number of bees foraging for both nectar and pollen was affected by the time of day, maturity of the flowers, and the amount of pollen on the flowers. We used a Likelihood Ratio Test again to determine whether these factors were significant overall. The R software program was used to explore and analyse the data (R Development Core Team, 2014). RESULTS Pollen collection experiment Only one P. tanacetifolia pollen pellet was found in a total of 23,431 pellets collected. The results of the DNA barcoding analysis confirmed that the purple pellet was from P. tanacetifolia. A preliminary DNA barcoding analysis of other pollen pellets showed that the honeybees also collected pollen from clover (Trifolium spp.), dandelion (Taraxacum spp.) and brassicas (Brassica spp.). No statistical tests for significance were run on these data as the number of P. tanacetifolia pollen pellets was negligible. Sprague et al. (2016), PeerJ, DOI /peerj /15 1.5 a Honeybees/sq meter/5 mins b Time 10:00 12:00 15: Nectar Pollen Nectar or Pollen Foraging Figure 1 Mean numbers of honeybees foraging for nectar and for pollen at 10:00, 12:00, and 15:00 (mean ± standard error; n = 12). Honeybees foraging on P. tanacetifolia in the field The virtual absence of P. tanacetifolia pollen collected by honeybees is supported by the observations of their foraging behaviour in the field. Using a two-tailed t-test, the number of honeybees foraging for pollen was significantly lower than the number of those foraging for nectar
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