A novel method to measure hairiness in bees and other insect pollinators

Hairiness is a salient trait of insect pollinators that has been linked to thermoregulation, pollen uptake and transportation, and pollination success. Despite its potential importance in pollination ecology, hairiness is rarely included in pollinator trait analyses. This is likely due to the lack of standardized and efficient methods to measure hairiness. We describe a novel methodology that uses a stereomicroscope equipped with a live measurement module software to quantitatively measure two components of hairiness: hair density and hair length. We took measures of the two hairiness components in 109 insect pollinator species (including 52 bee species). We analyzed the relationship between hair density and length and between these two components and body size. We combined hair density and length measures to calculate a hairiness index and tested whether hairiness differed between major pollinator groups and bee genera. Body size was strongly and positively correlated to hair length and weakly and negatively correlated to hair density. The correlation between the two hairiness components was weak and negative. According to our hairiness index, butterflies and moths were the hairiest pollinator group, followed by bees, hoverflies, beetles, and other flies. Among bees, bumblebees (Bombus) and mason bees (Osmia) were the hairiest taxa, followed by digger bees (Anthophorinae), sand bees (Andrena), and sweat bees (Halictini). Our methodology provides an effective and standardized measure of the two components of hairiness (hair density and length), thus allowing for a meaningful interpretation of hairiness. We provide a detailed protocol of our methodology, which we hope will contribute to improve our understanding of pollination effectiveness, thermal biology, and responses to climate change in insects. Hairiness is a fundamental functional trait in pollinator ecology related to thermoregulation and pollination effectiveness. Surprisingly, there is a lack of standard methods to measure this trait. We provide an effective method to quantitatively measure hairiness to contribute to filling an important gap in pollinator data bases and to improve our understanding of the ecology and evolution of a threatened group of organisms that provide an essential ecosystem service

Management trade‐offs on ecosystem services in apple orchards across Europe: Direct and indirect effects of organic production

Apple is considered the most important fruit crop in temperate areas and profitable production depends on multiple ecosystem services, including the reduction of pest damage and the provision of sufficient pollination levels. Management approaches present an inherent trade‐off as each affects species differently. We quantified the direct and indirect effects of management (organic vs. integrated pest management, IPM) on species richness, ecosystem services, and fruit production in 85 apple orchards in three European countries. We also quantified how habit composition influenced these effects at three spatial scales: within orchards, adjacent to orchards, and in the surrounding landscape. Organic management resulted in 48% lower yield than IPM, and also that the variation between orchards was large with some organic orchards having a higher yield than the average yield of IPM orchards. The lower yield in organic orchards resulted directly from management practices, and from higher pest damage in organic orchards. These negative yield effects were partly offset by indirect positive effects from more natural enemies and higher flower visitation rates in organic orchards. Two factors other than management affected species richness and ecosystem services. Higher cover of flowering plants within and adjacent to the apple trees increased flower visitation rates by pollinating insects and a higher cover of apple orchards in the landscape decreased species richness of beneficial arthropods. The species richness of beneficial arthropods in orchards was uncorrelated with fruit production, suggesting that diversity can be increased without large yield loss. At the same time, organic orchards had 38% higher species richness than IPM orchards, an effect that is likely due to differences in pest management. Synthesis and applications. Our results indicate that organic management is more efficient than integrated pest management in developing environmentally friendly apple orchards with higher species richness. We also demonstrate that there is no inherent trade‐off between species richness and yield. Development of more environmentally friendly means for pest control, which do not negatively affect pollination services, needs to be a priority for sustainable apple production.info:eu-repo/semantics/publishedVersio

Management trade-offs on ecosystem services in apple orchards across Europe : Direct and indirect effects of organic production

Apple is considered the most important fruit crop in temperate areas and profitable production depends on multiple ecosystem services, including the reduction of pest damage and the provision of sufficient pollination levels. Management approaches present an inherent trade-off as each affects species differently. We quantified the direct and indirect effects of management (organic vs. integrated pest management, IPM) on species richness, ecosystem services, and fruit production in 85 apple orchards in three European countries. We also quantified how habit composition influenced these effects at three spatial scales: within orchards, adjacent to orchards, and in the surrounding landscape. Organic management resulted in 48% lower yield than IPM, and also that the variation between orchards was large with some organic orchards having a higher yield than the average yield of IPM orchards. The lower yield in organic orchards resulted directly from management practices, and from higher pest damage in organic orchards. These negative yield effects were partly offset by indirect positive effects from more natural enemies and higher flower visitation rates in organic orchards. Two factors other than management affected species richness and ecosystem services. Higher cover of flowering plants within and adjacent to the apple trees increased flower visitation rates by pollinating insects and a higher cover of apple orchards in the landscape decreased species richness of beneficial arthropods. The species richness of beneficial arthropods in orchards was uncorrelated with fruit production, suggesting that diversity can be increased without large yield loss. At the same time, organic orchards had 38% higher species richness than IPM orchards, an effect that is likely due to differences in pest management. Synthesis and applications. Our results indicate that organic management is more efficient than integrated pest management in developing environmentally friendly apple orchards with higher species richness. We also demonstrate that there is no inherent trade-off between species richness and yield. Development of more environmentally friendly means for pest control, which do not negatively affect pollination services, needs to be a priority for sustainable apple production

Management-dependent effects of pollinator functional diversity on apple pollination services: A response–effect trait approach

Data available via the Dryad Digital Repository https://doi.org/10.5061/dryad.63xsj3v39 (Roquer-Beni et al., 2021).Functional traits mediate the response of communities to disturbances (response traits) and their contribution to ecosystem functions (effect traits). To predict how anthropogenic disturbances influence ecosystem services requires a dual approach including both trait concepts. Here, we used a response–effect trait conceptual framework to understand how local and landscape features affect pollinator functional diversity and pollination services in apple orchards. We worked in 110 apple orchards across four European regions. Orchards differed in management practices. Low-intensity (LI) orchards were certified organic or followed close-to-organic practices. High-intensity (HI) orchards followed integrated pest management practices. Within each management type, orchards encompassed a range of local (flower diversity, agri-environmental structures) and landscape features (orchard and pollinator-friendly habitat cover). We measured pollinator visitation rates and calculated trait composition metrics based on 10 pollinator traits. We used initial fruit set as a measure of pollination service. Some pollinator traits (body size and hairiness) were negatively related to orchard cover and positively affected by pollinator-friendly habitat cover. Bee functional diversity was lower in HI orchards and decreased with increased landscape orchard cover. Pollination service was not associated with any particular trait but increased with pollinator trait diversity in LI orchards. As a result, LI orchards with high pollinator trait diversity reached levels of pollination service similar to those of HI orchards. Synthesis and applications. Pollinator functional diversity enables pollinator communities to respond to agricultural intensification and to increase pollination function. Our results show that efforts to promote biodiversity provide greater returns in low-intensity than in high-intensity orchards. The fact that low-intensity orchards with high pollinator functional diversity reach levels of pollination services similar to those of high-intensity orchards provides a compelling argument for the conversion of high-intensity into low-intensity farms.This research (EcoFruit project) was funded through the 2013–2014 BiodivERsA/FACCE-JPI joint call (2014-74), Spanish MinECo (PCIN-2014-145-C02), German BMBF (PT-DLR/BMBF, 01LC1403) and Swedish Research Council Formas (2014-1784) by Formas (2013-934 to M.T.), Stiftelsen Lantbruksforskning (H1256150 to M.P.), INIA (RTA2013-00039-C03-00 to G.A. and M.M.), MinECo/FEDER (CGL2015-68963-C2-2-R to D.G.), FI-AGAUR (to L.R.-B.) and MinECo (RYC-2015-18448 to X.A.)

Predatory arthropods in apple orchards across Europe: Responses to agricultural management, adjacent habitat, landscape composition and country

Local agri-environmental schemes, including hedgerows, flowering strips, organic management, and a landscape rich in semi-natural habitat patches, are assumed to enhance the presence of beneficial arthropods and their contribution to biological control in fruit crops. We studied the influence of local factors (orchard management and adjacent habitats) and of landscape composition on the abundance and community composition of predatory arthropods in apple orchards in three European countries. To elucidate how local and landscape factors influence natural enemy effectiveness in apple production systems, we calculated community energy use as a proxy for the communities’ predation potential based on biomass and metabolic rates of predatory arthropods. Predator communities were assessed by standardised beating samples taken from apple trees in 86 orchards in Germany, Spain and Sweden. Orchard management included integrated production (IP; i.e. the reduced and targeted application of synthetic agrochemicals), and organic management practices in all three countries. Predator communities differed between management types and countries. Several groups, including beetles (Coleoptera), predatory bugs (Heteroptera), flies (Diptera) and spiders (Araneae) benefited from organic management depending on country. Woody habitat and IP supported harvestmen (Opiliones). In both IP and organic orchards we detected aversive influences of a high-quality surrounding landscape on some predator groups: for example, high covers of woody habitat reduced earwig abundances in German orchards but enhanced their abundance in Sweden, and high natural plant species richness tended to reduce predatory bug abundance in Sweden and IP orchards in Spain. We conclude that predatory arthropod communities and influences of local and landscape factors are strongly shaped by orchard management, and that the influence of management differs between countries. Our results indicate that organic management improves the living conditions for effective predator communities.info:eu-repo/semantics/acceptedVersio

Ecological, environmental, and management data indicate apple production is driven by wild bee diversity and management practices

Climate, landscape composition, management practice, and wild bee pollination are all variables thought to play significant roles in commercial apple production. However, how these variables affect production efficiency under field-realistic conditions has not been investigated at large geographical scales. We combined intensive standardized field surveys (using netting and pan traps) with structural equation models to explore the relative impact of biotic and abiotic variables on bee diversity, apple yield and fruit quality, and their ability to represent reliable proxies of apple production. Here we show that apple yields are mainly driven by management practice, without evidence for a significantly superior contribution by managed honey bees. Total wild bee diversity, while negatively correlated with honey bee dominance, promoted apple quality by enhancing seed set number. Our study demonstrates that even across a broad geographical range there is potential to harness wild bee diversity as nature-based solution and as a substitute to an exclusive reliance on honey bees in the context of commercial apple production

Opportunities to reduce pollination deficits and address production shortfalls in an important insect pollinated crop

Pollinators face multiple pressures and there is evidence of populations in decline. As demand for insect-pollinated crops increases, crop production is threatened by shortfalls in pollination services. Understanding the extent of current yield deficits due to pollination and identifying opportunities to protect or improve crop yield and quality through pollination management is therefore of international importance. To explore the extent of ‘pollination deficits’, where maximum yield is not being achieved due to insufficient pollination, we use an extensive dataset on a globally important crop, apples. We quantified how these deficits vary between orchards and countries as well as compare ‘pollinator dependence’ across different apple varieties. We found evidence of pollination deficits and in some cases, risks of over-pollination were even apparent where fruit quality could be reduced by too much pollination. In almost all regions studied we found some orchards performing significantly better than others, in terms of avoiding a pollination deficit and crop yield shortfalls due to sub-optimal pollination. This represents an opportunity to improve production through better pollinator and crop management. Our findings also demonstrate that pollinator dependence varies considerably between apple varieties in terms of fruit number and fruit quality. We propose that assessments of pollination service and deficits in crops can be used to quantify supply and demand for pollinators and help target local management to address deficits although crop variety has a strong influence on the role of pollinators

Pollinator communities and pollination services in apple orchards: a trait-based approach

La biodiversitat està amenaçada arreu del món a conseqüència d’activitats humanes com el canvi d’usos del sòl, l’explotació de recursos o el canvi climàtic. Durant els darrers 20 anys, les aproximacions basades en trets s’han anat incorporant de manera creixent en estudis que relacionen la biodiversitat, l’estructura de les comunitats i el funcionament ecosistèmic, com a alternativa a les aproximacions taxonòmiques. La pol·linització és un servei ecosistèmic cabdal que contribueix a la reproducció sexual de més del 85% de les espècies d’angiospermes al món. A més, els pol·linitzadors proveeixen d’un servei ecosistèmic cabdal a través de la seva contribució a la producció agrícola i a la nutrició humana. Tanmateix, la diversitat de pol·linitzadors està experimentant forts declivis a Europa. La intensificació agrícola és una de les principals causes d’aquests declivis. Els trets funcionals determinen les respostes dels pol·linitzadors (individus o espècies) a les alteracions ambientals (trets resposta) i, al mateix temps, contribueixen al funcionament ecosistèmic (trets efecte). Les aproximacions basades en trets ja fa temps que s’utilitzen en plantes i, en canvi, no tant en animals vertebrats. Per molts grups d’invertebrats terrestres encara falta consens sobre quins trets cal mesurar, com, i quin poder predictiu tenen. Diversos estudis han analitzat els efectes de la intensificació agrícola sobre la composició funcional, i d’altres han analitzat el rol de la composició funcional sobre el servei de la pol·linització. Tot i això, són pocs els estudis que utilitzen un marc de trets resposta-efecte. L’objectiu d’aquesta tesi és entendre millor els mecanismes que relacionen la composició funcional amb la provisió del servei de la pol·linització en camps de pomera. Per fer-ho, vaig mesurar diferents trets de pol·linitzadors en 109 espècies de per tal d’estudiar el rol funcional individual i a nivell d’espècie. També vaig utilitzar aquests trets per estudiar com la composició funcional de pol·linitzadors responia a factors agrícoles a escala local i de paisatge i com, a la vegada, aquests trets afectaven al servei de la pol·linització a nivell de comunitat. Primer, vaig desenvolupar un mètode estandarditzat per mesurar quantitativament la pilositat, un tret important en l’ecologia de la pol·linització. El mètode proposat considera dos components de la pilositat (la llargada i la densitat dels pèls) i es va utilitzar en 109 espècies pertanyents a diferents grups de pol·linitzadors. Segon, vaig determinar quins trets dels pol·linitzadors promovien l’eficàcia pol·linitzadora i vaig explorar si pol·linitzadors amb eficàcies pol·linitzadores similars compartien també trets similars. Vaig observar que l’eficàcia pol·linitzadora no depenia d’un únic tret sinó de diversos trets morfològics i de comportament. Els trets que tenien més efecte sobre l’eficàcia pol·linitzadora van ser el comportament intrafloral, la mida corporal i la durada de les visites. Tots els pol·linitzadors eficients s’aproximaven a les flors des de dalt però, a banda d’això, no compartien necessàriament altres trets. Finalment, vaig analitzar com factors locals i de paisatge afectaven al servei de la pol·linització mitjançant canvis en la composició funcional en 110 camps de pomes de diferents zones d’Europa. El servei de la pol·linització va incrementar amb la diversitat funcional de pol·linitzadors, però només en camps de gestió poc intensiva. Així, camps poc intensius amb una alta diversitat funcional van assolir nivells de serveis de pol·linització similars als dels camps de gestió intensiva.La biodiversidad está siendo amenazada en todo el mundo a consecuencia de actividades humanas como el cambio de los usos del suelo, la explotación de recursos o el cambio climático. Durante los últimos 20 años, las aproximaciones basadas en rasgos se han ido incorporando de manera creciente en los estudios que relacionan la biodiversidad, la estructura de las comunidades y el funcionamiento ecosistémico, como alternativa a las aproximaciones taxonómicas. La polinización es un servicio ecosistémico clave que contribuye a la reproducción sexual de más del 85% de las especies de angiospermas del mundo. Además, los polinizadores proveen un servicio ecosistémico clave a través de su contribución a la producción agrícola y a la nutrición humana. Asimismo, la diversidad de polinizadores está experimentando fuertes declives en Europa. La intensificación agrícola es una de las principales causas de estos declives. Los rasgos funcionales determinan las respuestas de los polinizadores (individuos o especies) a las alteraciones ambientales (rasgos respuesta) y, al mismo tiempo, contribuyen al funcionamiento ecosistémico (rasgos respuesta). Las aproximaciones basadas en rasgos ya hace tiempo que se utilizan en plantas y, en cambio, no son tan utilizadas en animales vertebrados. En muchos grupos de invertebrados terrestres aún falta consenso sobre qué rasgos es necesario medir, cómo, y qué poder predictivo tienen. Diversos estudios han analizado los efectos de la intensificación agrícola sobre la composición funcional y otros han analizado el rol de la composición funcional sobre el servicio de la polinización. En cambio, son pocos los estudios que utilizan un marco de rasgos respuesta-efecto. El objetivo de la presente tesis es entender mejor los mecanismos que relacionan la composición funcional con la provisión del servicio ecosistémico de la polinización en campos de manzana. Para ello, medí 10 rasgos de polinizadores en 109 especies de grupos diferentes para estudiar el rol funcional individual y a nivel de especie. También utilicé los rasgos para estudiar cómo la composición funcional de polinizadores respondía a factores agrícolas tanto a escala local como de paisaje y de cómo, a la vez, estos rasgos afectan al servicio de la polinización a nivel de comunidad. Primero, desarrollé un método estandarizado para medir cuantitativamente la pilosidad, un rasgo importante en ecología de la polinización. El método propuesto tiene en cuenta dos componentes de la pilosidad (la longitud y la densidad de los pelos) y se utilizó en 109 especies pertenecientes a diferentes grupos de polinizadores. Esperamos que este método incentive la inclusión de la pilosidad en bases de datos de polinizadores y contribuya al conocimiento sobre la importancia de este rasgo en la ecología de la polinización. Segundo, determiné qué rasgos de los polinizadores promueven la eficacia polinizadora y exploré si polinizadores con eficacias similares compartían también rasgos similares. Observé que la eficacia polinizadora no depende de un único rasgo sino de varios rasgos morfológicos y de comportamiento. Los rasgos que afectaron más a la eficacia polinizadora fueron el comportamiento intrafloral, el tamaño corporal y la duración de las visitas. Todos los polinizadores eficientes se aproximaban a las flores desde arriba, pero no compartían necesariamente otros rasgos. Finalmente, analicé cómo factores locales y de paisaje afectan al servicio de la polinización mediante cambios en la composición funcional en 110 campos de manzana de diferentes zonas de Europa. El servicio de la polinización incrementó con la diversidad funcional de polinizadores, pero solo en campos de gestión poco intensiva. Así, campos poco intensivos con una diversidad funcional alta obtuvieron niveles de polinización similares a los campos de gestión intensiva. La relación entre los rasgos respuesta y efecto se vio más influenciada por la diversidad funcional que no por rasgos funcionales concretos.Biodiversity is being threatened worldwide as a result of human activities such as land use change, exploitation of resources or climate change. During the last 20 years, trait-based approaches have been increasingly incorporated in studies linking biodiversity, community structure and ecosystem functioning, as an alternative to taxonomy-based approaches. One crucial ecosystem function is pollination, which contributes to the sexual reproduction of more than 85% of angiosperm species worldwide. In addition, pollinators provide a crucial ecosystem service through their contribution to agricultural production and human nutrition. However, pollinator diversity is experiencing strong declines in Europe and North America. Agricultural intensification is considered one of the main drivers of these declines. Functional traits mediate the responses of pollinators (individuals or species) to environmental disturbances (response traits) and, at the same time, contribute to ecosystem function (effect traits). Trait-based approaches have long been used in plant studies and, to a lesser extent, studies on vertebrate animals. However, for many groups of terrestrial invertebrates there is still a lack of consensus on which traits should be measured, their predictive value and how they should be measured. Several studies have addressed the effects of agricultural intensification on pollinator functional composition and others have addressed the role of functional composition on pollination service. However, of studies analysing both processes simultaneously using a response-trait effect framework remain very scarce. The aim of this thesis is to better understand the mechanisms linking functional composition with pollination service provision in apple orchards. To do so, I measured 10 pollinator traits in 109 species of different pollinator groups to study pollinator functional performance at individual and species level. I also used these traits to study how pollinator functional composition responded to agricultural local and landscape features and how, in turn, these traits affected pollination service at the community level. First, I developed a standardized method to quantitatively measure hairiness, a salient trait in pollination ecology. The proposed methodology accounts for the two components of hairiness (hair length and hair density) and was used on 109 species from different pollinator groups. Hopefully the method will foster the inclusion of hairiness in pollinator data bases and contribute to our understanding of the relevance of this trait in pollination ecology. Second, I determined which pollinator traits promote pollination effectiveness and explored whether pollinators with similar pollination effectiveness share similar traits. I found that pollination effectiveness was not dependent on a single trait but on a variety of behavioural and morphological traits. The main traits affecting pollination effectiveness were flower handling behaviour, body size and visit duration. All effective pollinators were top-workers, but otherwise did not necessarily share similar traits. Third, using a response-trait framework, I analysed how local and landscape features affected pollination service through changes in functional composition in 110 apple orchards across Europe. Pollination service increased with pollinator functional diversity, but only in low-input orchards. As a result, low-input orchards with high pollinator functional diversity reached levels of pollination service similar to those of high-input orchards. The relationship between response and effect traits was better mediated by functional diversity rather than specific functional traits. Functional diversity enabled pollinator communities to better respond to management and landscape intensity and to increase pollination function through complementarity.Universitat Autònoma de Barcelona. Programa de Doctorat en Ecologia Terrestr

Data matrix used for structural equation model

The data matrix includes all variables included in the structural equation model analysed in the paper. The variable descriptions and the statistical code is found in the README-fil