Identifying key knowledge needs for evidence-based conservation of wild insect pollinators: a collaborative cross-sectoral exercise

In response to evidence of insect pollinator declines, organisations in many sectors, including the food and farming industry, are investing in pollinator conservation. They are keen to ensure that their efforts use the best available science. We convened a group of 32 ‘conservation practitioners’ with an active interest in pollinators and 16 insect pollinator scientists. The conservation practitioners include representatives from UK industry (including retail), environmental non-government organisations and nature conservation agencies. We collaboratively developed a long list of 246 knowledge needs relating to conservation of wild insect pollinators in the UK. We refined and selected the most important knowledge needs, through a three-stage process of voting and scoring, including discussions of each need at a workshop. We present the top 35 knowledge needs as scored by conservation practitioners or scientists. We find general agreement in priorities identified by these two groups. The priority knowledge needs will structure ongoing work to make science accessible to practitioners, and help to guide future science policy and funding. Understanding the economic benefits of crop pollination, basic pollinator ecology and impacts of pesticides on wild pollinators emerge strongly as priorities, as well as a need to monitor floral resources in the landscape.

The utility of aerial pan-trapping for assessing insect pollinators across vertical strata

Insect pollinators provide a critical ecosystem service by pollinating many wild flowers and crops. It is therefore essential to be able to effectively survey and monitor pollinator communities across a range of habitats, and in particular, sample the often stratified parts of the habitats where insects are found. To date, a wide array of sampling methods have been used to collect insect pollinators, but no single method has been used effectively to sample across habitat types and throughout the spatial structure of habitats. Here we present a method of ‘aerial pan-trapping’ that allows insect pollinators to be sampled across the vertical strata from the canopy of forests to agro-ecosystems. We surveyed and compared the species richness and abundance of a wide range of insect pollinators in agricultural, secondary regenerating forest and primary forest habitats in Ghana to evaluate the usefulness of this approach. In addition to confirming the efficacy of the method at heights of up to 30 metres and the effects of trap color on catch, we found greatest insect abundance in agricultural land and higher bee abundance and species richness in undisturbed forest compared to secondary forest.

Persistent reduced ecosystem respiration after insect disturbance in high elevation forests

Amid a worldwide increase in tree mortality, mountain pine beetles (Dendroctonus ponderosae Hopkins) have led to the death of billions of trees from Mexico to Alaska since 2000. This is predicted to have important carbon, water and energy balance feedbacks on the Earth system. Counter to current projections, we show that on a decadal scale, tree mortality causes no increase in ecosystem respiration from scales of several square metres up to an 84 km2 valley. Rather, we found comparable declines in both gross primary productivity and respiration suggesting little change in net flux, with a transitory recovery of respiration 6–7 years after mortality associated with increased incorporation of leaf litter C into soil organic matter, followed by further decline in years 8–10. The mechanism of the impact of tree mortality caused by these biotic disturbances is consistent with reduced input rather than increased output of carbon.

New age estimates for the Palaeolithic assemblages and Pleistocene succession of Casablanca, Morocco

Marine and aeolian Quaternary sediments from Casablanca, Morocco were dated using the optically stimulated luminescence (OSL) signal of quartz grains. These sediments form part of an extensive succession spanning the Pleistocene, and contain a rich faunal and archaeological record, including an Acheulian lithic assemblage from before the Brunhes–Matayama boundary, and a Homo erectus jaw from younger cave deposits. Sediment samples from the sites of Reddad Ben Ali, Oulad J’mel, Sidi Abderhamane and Thomas Quarries have been dated, in order to assess the upper limits of OSL. The revision of previously measured mammalian tooth enamel electron spin resonance (ESR) dates from the Grotte des Rhinocéros, Oulad Hamida Quarry 1, incorporating updated environmental dose rate measurements and attenuation calculations, also provide chronological constraint for the archaeological material preserved at Thomas Quarries. Several OSL age estimates extend back to around 500,000 years, with a single sample providing an OSL age close to 1 Ma in magnetically reversed sediments. These luminescence dates are some of the oldest determined, and their reliability is assessed using both internal criteria based on stratigraphic consistency, and external lithostratigraphic, morphostratigraphic and independent chronological constraints. For most samples, good internal agreement is observed using single aliquot regenerative-dose OSL measurements, while multiple aliquot additive-dose measurements generally have poorer resolution and consistency. Novel slow-component and component-resolved OSL approaches applied to four samples provide significantly enhanced dating precision, and an examination of the degree of signal zeroing at deposition. A comparison of the OSL age estimates with the updated ESR dates and one U-series date demonstrate that this method has great potential for providing reliable age estimates for sediments of this antiquity. We consider the cause of some slight age inversion observed at Thomas Quarries, and provide recommendations for further luminescence dating within this succession.

Avoiding a bad apple: insect pollination enhances fruit quality and economic value

Insect pollination is important for food production globally and apples are one of the major fruit crops which are reliant on this ecosystem service. It is fundamentally important that the full range of benefits of insect pollination to crop production are understood, if the costs of interventions aiming to enhance pollination are to be compared against the costs of the interventions themselves. Most previous studies have simply assessed the benefits of pollination to crop yield and ignored quality benefits and how these translate through to economic values. In the present study we examine the influence of insect pollination services on farmgate output of two important UK apple varieties; Gala and Cox. Using field experiments, we quantify the influence of insect pollination on yield and importantly quality and whether either may be limited by sub-optimal insect pollination. Using an expanded bioeconomic model we value insect pollination to UK apple production and establish the potential for improvement through pollination service management. We show that insects are essential in the production of both varieties of apple in the UK and contribute a total of £36.7 million per annum, over £6 million more than the value calculated using more conventional dependence ratio methods. Insect pollination not only affects the quantity of production but can also have marked impacts on the quality of apples, influencing size, shape and effecting their classification for market. These effects are variety specific however. Due to the influence of pollination on both yield and quality in Gala, there is potential for insect pollination services to improve UK output by up to £5.7 million per annum. Our research shows that continued pollinator decline could have serious financial implications for the apple industry but there is considerable scope through management of wild pollinators or using managed pollinator augmentation, to improve the quality of production. Furthermore, we show that it is critically important to consider all production parameters including quality, varietal differences and management costs when valuing the pollination service of any crop so investment in pollinator management can be proportional to its contribution.

Reversing insect pollinator decline

Pollination by insects enables the reproduction of flowering plants and is critical to UK agriculture.1 Insect pollinators have declined globally, with implications for food security and wild habitats. This POSTnote summarises the causes for the recent trends, gaps in knowledge and possible strategies for reversing pollinator decline.

Contribution of insect pollinators to crop yield and quality varies with agricultural intensification

Background: Up to 75% of crop species benefit at least to some degree from animal pollination for fruit or seed set and yield. However, basic information on the level of pollinator dependence and pollinator contribution to yield is lacking for many crops. Even less is known about how insect pollination affects crop quality. Given that habitat loss and agricultural intensification are known to decrease pollinator richness and abundance, there is a need to assess the consequences for different components of crop production. Methods: We used pollination exclusion on flowers or inflorescences on a whole plant basis to assess the contribution of insect pollination to crop yield and quality in four flowering crops (spring oilseed rape, field bean, strawberry, and buckwheat) located in four regions of Europe. For each crop, we recorded abundance and species richness of flower visiting insects in ten fields located along a gradient fromsimple to heterogeneous landscapes. Results: Insect pollination enhanced average crop yield between 18 and 71% depending on the crop. Yield quality was also enhanced in most crops. For instance, oilseed rape had higher oil and lower chlorophyll contents when adequately pollinated, the proportion of empty seeds decreased in buckwheat, and strawberries’ commercial grade improved; however, we did not find higher nitrogen content in open pollinated field beans. Complex landscapes had a higher overall species richness of wild pollinators across crops, but visitation rates were only higher in complex landscapes for some crops. On the contrary, the overall yield was consistently enhanced by higher visitation rates, but not by higher pollinator richness. Discussion. For the four crops in this study, there is clear benefit delivered by pollinators on yield quantity and/or quality, but it is not maximized under current agricultural intensification. Honeybees, the most abundant pollinator, might partially compensate the loss of wild pollinators in some areas, but our results suggest the need of landscape-scale actions to enhance wild pollinator populations.

Density of insect-pollinated grassland plants decreases with increasing surrounding land-use intensity

Pollinator declines have raised concerns about the persistence of plant species that depend on insect pollination, in particular by bees, for their reproduction. The impact of pollinator declines remains unknown for species-rich plant communities found in temperate seminatural grasslands. We investigated effects of land-use intensity in the surrounding landscape on the distribution of plant traits related to insect pollination in 239 European seminatural grasslands. Increasing arable land use in the surrounding landscape consistently reduced the density of plants depending on bee and insect pollination. Similarly, the relative abundance of bee-pollination-dependent plants increased with higher proportions of non-arable agricultural land (e.g. permanent grassland). This was paralleled by an overall increase in bee abundance and diversity. By isolating the impact of the surrounding landscape from effects of local habitat quality, we show for the first time that grassland plants dependent on insect pollination are particularly susceptible to increasing land-use intensity in the landscape.

A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators

There is evidence that in Europe and North America many species of pollinators are in decline, both in abundance and distribution. Although there is a long list of potential causes of this decline, there is concern that neonicotinoid insecticides, in particular through their use as seed treatments are, at least in part, responsible. This paper describes a project that set out to summarize the natural science evidence base relevant to neonicotinoid insecticides and insect pollinators in as policy-neutral terms as possible. A series of evidence statements are listed and categorized according to the nature of the underlying information. The evidence summary forms the appendix to this paper and an annotated bibliography is provided in the electronic supplementary material.

Adding value to the urban lawnscape: insect abundance and diversity in grass-free lawns

Insect diversity may be declining even more rapidly than in plants and vertebrates, particularly in areas where indigenous habitats are replaced by an anthropogenic one. The most common component of anthropogenic greenspace is the ornamental lawn. Intensively managed and offering limited habitat opportunities for both plants and insects, lawns are biodiversity poor and ecologically insensitive. An alternative lawn format that positively influences biodiversity and reduces management requirements would be a useful tool in eco-friendly urban greenspace management. In investigating the potential for a forb-only alternative to the grass lawn we sampled both trial grass-free lawn formats and turf lawns to identify any influence that lawn composition and grass-free lawn specific mowing regimes might have on the abundance and diversity of insect families. In addition to the mowing regimes, both the composition and origin of lawn flora were found to significantly influence insect abundance and diversity and these factors rarely interacted. Native-only and mixed origin grass-free lawns hosted greater numbers of adult insects than found in turf and an equivalent diversity of insect families, however the mowing regime applied was distinct from traditional turf lawn management by being substantially less intensive and our results suggest that there is the potential for even greater abundance and diversity via the grass-free format that may offer additional resources to insectivorous garden species such as birds. When the composition of grass-free lawns included native forbs the diversity of insect families was found be sufficiently different from turf lawns to form distinct assemblages and in so doing contribute to beta diversity within urban greenspace. In sum, grass-free lawns may be a useful and aesthetically appropriate tool for adding value to the generally biodiversity poor urban lawnscape.

Utilizing insect behavior in chemical detection by a behavioral biosensor

Traditionally, biosensors have been defined as consisting of two parts; a biological part, which is used to detect chemical or physical changes in the environment, and a corresponding electronic component, which tranduces the signal into an electronically readable format. Biosensors are used for detection of volatile compounds often at a level of sensitivity unattainable by traditional analytical techniques. Classical biosensors and traditional analytical techniques do not allow an ecological context to be imparted to the volatile compound/s under investigation. Therefore, we propose the use of behavioral biosensors, in which a whole organism is utilized for the analysis of chemical stimuli. In this case, the organism detects a chemical or physical change and demonstrates this detection through modifications of its behavior; it is the organism's behavior itself that defines the biosensor. In this review, we evaluate the use and future prospects of behavioral biosensors, with a particular focus on parasitic wasps.

Insect pollination reduces yield loss following heat stress in faba bean (Vicia faba L.)

Global food security, particularly crop fertilization and yield production, is threatened by heat waves that are projected to increase in frequency and magnitude with climate change. Effects of heat stress on the fertilization of insect-pollinated plants are not well understood, but experiments conducted primarily in self-pollinated crops, such as wheat, show that transfer of fertile pollen may recover yield following stress. We hypothesized that in the partially pollinator-dependent crop, faba bean (Vicia faba L.), insect pollination would elicit similar yield recovery following heat stress. We exposed potted faba bean plants to heat stress for 5 days during floral development and anthesis. Temperature treatments were representative of heat waves projected in the UK for the period 2021-2050 and onwards. Following temperature treatments, plants were distributed in flight cages and either pollinated by domesticated Bombus terrestris colonies or received no insect pollination. Yield loss due to heat stress at 30°C was greater in plants excluded from pollinators (15%) compared to those with bumblebee pollination (2.5%). Thus, the pollinator dependency of faba bean yield was 16% at control temperatures (18 to 26°C) and extreme stress (34°C), but was 53% following intermediate heat stress at 30°C. These findings provide the first evidence that the pollinator dependency of crops can be modified by heat stress, and suggest that insect pollination may become more important in crop production as the probability of heat waves increases.

From insect to man: Photorhabdus sheds light on the emergence of human pathogenicity

Photorhabdus are highly effective insect pathogenic bacteria that exist in a mutualistic relationship with Heterorhabditid nematodes. Unlike other members of the genus, Photorhabdus asymbiotica can also infect humans. Most Photorhabdus cannot replicate above 34°C, limiting their host-range to poikilothermic invertebrates. In contrast, P. asymbiotica must necessarily be able to replicate at 37°C or above. Many well-studied mammalian pathogens use the elevated temperature of their host as a signal to regulate the necessary changes in gene expression required for infection. Here we use RNA-seq, proteomics and phenotype microarrays to examine temperature dependent differences in transcription, translation and phenotype of P. asymbiotica at 28°C versus 37°C, relevant to the insect or human hosts respectively. Our findings reveal relatively few temperature dependant differences in gene expression. There is however a striking difference in metabolism at 37°C, with a significant reduction in the range of carbon and nitrogen sources that otherwise support respiration at 28°C. We propose that the key adaptation that enables P. asymbiotica to infect humans is to aggressively acquire amino acids, peptides and other nutrients from the human host, employing a so called “nutritional virulence” strategy. This would simultaneously cripple the host immune response while providing nutrients sufficient for reproduction. This might explain the severity of ulcerated lesions observed in clinical cases of Photorhabdosis. Furthermore, while P. asymbiotica can invade mammalian cells they must also resist immediate killing by humoral immunity components in serum. We observed an increase in the production of the insect Phenol-oxidase inhibitor Rhabduscin normally deployed to inhibit the melanisation immune cascade. Crucially we demonstrated this molecule also facilitates protection against killing by the alternative human complement pathway.