Flower traits (e.g., self-compatibility) determine pollinator dependence, and thereby seed production and mating. But crop research often overlooks how specific flower traits influence pollination quantity and quality and, consequently, yield. Our study addresses this oversight by investigating how the under-studied phenomenon of premature pollen development (PPD)—where pollen germinates inside the anther before dispersal—affects pollinator dependence in soybean, a globally important crop. Soybean exhibits both PPD and variable pollinator dependence. To link these two factors, we conducted a four-week study across 15 experimental plots within a 24-hectare soybean plantation in Central Argentina. We collected 186 flowers and pollinator visitation data to analyze how PPD and visitation frequency affected pollen tube growth in the style. Our findings indicate that PPD limits autonomous self-pollination while simultaneously increasing pollinator dependence. Interestingly, small wild pollinators appear to be more effective at pollen transfer than managed honeybees. This work highlights the potential consequences of PPD on soybean yield and suggests the critical role of wild pollinators when PPD is present. Our findings underscore the need to preserve pollinator habitats to maintain high productivity, even in seemingly self-pollinating crops. They also raise questions about the role and consequences of PPD in plant reproduction beyond agriculture.
Insect-mediated pollination enhances global production of many crops, and evidence highlights that insect pollination can also improve crop quality. The link between insect-mediated pollination and crop quality is driven not only by insect pollinators, but by a complex of interactions between pollinators, plant genotype, levels of cross pollination, plant physiology, environmental conditions, farm management, etc. To further optimize food production, the link between insect-mediated pollination and crop quality requires additional examination. In this study, we used a dataset of 260 sites across multiple production regions to explore how flower visitation of honey bees and wild bees drives fruit quality in highbush blueberry, measured as fruit weight. Our hypothesis was that bee visitation mediates fruit quality through fruit set and seed set. These effects were evaluated using both linear and structural equation modeling (SEM). Our analyses show that seed set mainly influences fruit quality and SEM analyses reveal a positive cascading effect of wild bee visitation on fruit quality, mediated via seed set. Similar effects of fruit set or honey bee visitation on fruit quality were not detected. This study highlights that bee visitation mainly affects blueberry fruit quality via seed set and that analyses beyond the pollinator visitation-crop quality relation can inform pollination research and management. Possible measures to improve crop quality by enhancing pollinator visitation by means of farm management or landscape management are discussed.
Nitrogen (N) and phosphorus (P) fertilisers are widely used in agro-ecosystems but can endanger the diversity of beneficial soil-borne biota. This study aimed to determine the impact of long-term N and P fertilisation on arbuscular mycorrhizal fungi (AMF), a group of symbiotic soil fungi, by distinguishing between the effects of individual and combined nutrient applications. We examined the impacts of long-term (i.e. 19 years) N and P fertilisation at two developmental crop stages: V6 (six fully expanded leaves) and R1 (initiation of flowering, after N addition). We measured mycorrhizal colonisation to test the plant-AMF relationship and used Illumina MiSeq sequencing of 18S rRNA gene from rhizospheric soil to evaluate AMF diversity. N and P fertilisation resulted primarily in additive effects rather than interactive effects. N fertilisation greatly increased alpha diversity (e.g. + 38
Blueberry cultivation requires insect-mediated pollination for optimal fruit formation. Studies have shown that improving the efficiency of pollen exchange during flowering increases both the quantity and quality of fruit. Blueberry flowers have a unique anther structure that facilitates pollen release through a specialised interaction called 'buzz pollination', which is performed by wild bee species rather than Apis mellifera. The study aims to assess the effects of pollination management, weed management, and landscape heterogeneity on pollinator communities, and their interaction with the crop and blueberry fruit set. Nine blueberry plots were studied to investigate the influence of including Bombus pauloensis hives, the presence of inter-row vegetation, and landscape heterogeneity on pollinator abundance, richness, visitation rate, and fruit production. Generalised linear mixed models (GLMM) were used to analyse the relationship between these factors. No significant differences in fruit formation were found between plots receiving pollination services from Apis mellifera and those with a combination of A. mellifera + B. pauloensis hives. However, inter-row vegetation had a positive effect on pollinator abundance and visitation rate to blueberry flowers. The increase in cultivated areas had a negative effect on the visitation rate of both managed and native pollinators. Conversely, more diverse landscapes had a negative and significant effect on A. mellifera abundance within the plots. These findings suggest the importance of implementing wild pollinator-friendly management practices, carefully assessing honeybee densities, and managing resources at both local and landscape scales to enhance bee visitation and blueberry fruit production.
Animal pollination is essential to guarantee the economic viability of pollination-dependent crops, and honeybees (Apis mellifera L.) play a central role as the most used species worldwide for pollination service management. Despite its importance, recommendations on honeybee hive stocking density are based on rules of thumb that assume hives as standardized units and do not consider the contingencies of the crop's pollen deposition demand. We developed a mechanistic simulation model to assess the consequences of variant hive quality and stocking density scenarios for blueberry productivity per hectare. To do so, we used Bayesian models, field experiments and secondary information to parametrize the simulation and estimate flower visitation rate, pollen deposition, and fruit production at the crop level. We found that maximizing pollen deposition at the crop level can be achieved with seven high quality-hives ha(-1) (20000 bees colony(-1)), whereas reaching similar levels of pollination with conventional hives (10000 bees colony(-1)) would require 20 hives ha(-1). Also, optimal hive stocking densities to maximize blueberry yield ha(-1) needs four high quality-hives ha(-1), whilst similar levels of productivity could be reached with 20 conventional colonies ha(-1). From an economic and productive perspective, a lower unit rental price for conventional hives compensates for the use of less, but more expensive, high quality hives. Therefore, deciding using either low or high-quality hives should be based on, for instance, the logistic implications of using similar to 2.5 more hives ha(-1) and the consequences of using colonies with a poorer sanitation state for pollination service stability. Our work set the basis for a more biological and evidence-based protocol for honeybee hive management in blueberry crops. Indeed, integrating honeybee and blueberry pollination ecology, we provide a pragmatic approach to maximize crop productivity based on the minimum beehive stocking densities that optimize pollen deposition and crop yield ha(-1) depending on hive's quality. Knowing such a minimum allows for reduced operation costs for farmers, lower uncertainty of pollinators contribution to crop productivity and the risk of undesirable pollination scenarios, and helps to limit the potential negative impacts of saturating ecosystems with honeybees.
Animal pollination is crucial for the reproduction and economic viability of a wide range of crops. Despite the existing data, the extent to which citrus crops depend on pollinators to guarantee fruit production still needs to be determined. Here, we described the composition of potential pollinators in citrus (Citrus spp.) from the main growing areas of Argentina; moreover, we combined Bayesian models and empirical simulations to assess the contribution of animal pollination on fruit set and yield ha-1 in different species and cultivars of lemons, grapefruits, mandarins, and oranges. Honeybee (A. mellifera L.) was the most commonly observed potential pollinator, followed by a diverse group of insects, mainly native bees. Regardless of citrus species and cultivars, the probability of flowers setting fruit in pollinated flowers was 2.4 times higher than unpollinated flowers. Furthermore, our simulations showed that about 60% of the citrus yield ha-1 can be attributable to animal pollination across all species and cultivars. Therefore, it is crucial to maintain environments that support pollinator diversity and increase consumer and to producer awareness and demand in order to ensure the significant benefits of animal pollination in citrus production.
In Argentina, food production is the basis of economic and social development. Several crops depend on entomophilous pollination. However, wild and managed pollinators are threatened by conventional agricultural management practices. In this work, we evaluate the economic value attributed to entomophilous pollination (EEV) of the main crops between 2013 and 2018. Our study focused on analyses of crops with varying degrees of pollinator dependence in terms, their harvested area, yield and total economic value (EV). The EEV attributed to pollinators and the vulnerability of each crop category were estimated. The EEV attributed exclusively to entomophilous pollination, in the 27 crops analyzed, was US$ 4.437 million, representing a contribution of the pollinators of 21,83% of the EV and 13,8 million tons of agricultural products. The EEV in decreasing order is industrial crops, fruit trees, vegetables, nuts and citrus. In industrial crops, where managed pollinators are not used, the contribution of pollinators was high, reaching US$3.655 million. Fruit trees and vegetables are the most vulnerable to an eventual decrease or absence of pollinators with estimated vulnerability rates of 68 and 38% respectively. These results show the economic contribution of the pollinators to the country's agriculture, the high vulnerability of agroecosystems and the effects in quantitative terms of a potential reduction in food production due to a pollination deficit. Finally, this work may be useful to guide decision-making and establish public policies aimed at promoting diversification and sustainability of agricultural models to guarantee food security.
Highbush blueberry production has expanded worldwide in recent decades. To safeguard future yields, it is essential to understand if insect pollination is limiting current blueberry production and which insects contribute to pollination in different production regions.We present a systematic review including a set of meta‐analyses on insect‐mediated pollination in highbush blueberry. We summarize the geographic distribution of research, the abundance of different pollinator taxa and their relative pollination contributions. Using raw data from 21 studies, totalling 496 site replicates, we determine the degree of pollination service and pollen limitation (i.e. combining open pollination levels with experimental bagged and/or hand pollination treatments), as well as the contribution of honeybees and wild bees to pollination (i.e. observational, open pollination).Most studies originate from North America, focusing on only a few cultivars. Honeybees are the dominant pollinator, and wild bees are occasionally abundant. Wild bees are more efficient pollinators on a single‐visit basis compared to honeybees, which increases their relative pollination contribution compared to their relative abundance.Insect‐mediated pollination services increased blueberry fruit set, berry weight and seed set (R2 values: 64.8%, 75.9% and 75.2% respectively). We often detected pollen limitation, indicated by an increase in fruit set, berry weight and seed set (R2: 10.1%, 18.2% and 21.5%, respectively), with additional hand pollination. Increasing visitation of honeybees and wild bees contributed to blueberry pollination by increasing fruit set (R2: 5.4% and 3.5%), berry weight (R2: 6.5% and 2.8%) and seed set (R2: 6.4% and 3.8%) respectively. Bee contributions to fruit set and berry weight were variable across regions.Synthesis and application: A diverse community of insects, primarily bees, contributes to highbush blueberry pollination and yield. However, pollination deficits are common. The finding that both honeybees and wild bees enhance pollination highlights the possibility of adopting different management strategies that utilize honeybees, wild bees or both depending on the specific context and region. This further emphasizes the general importance of conserving pollinator health and diversity. Our synthesis highlights data gaps and areas for future research to better understand the pollination contribution of different pollinators to crops that are expanding globally.
Pest responses to landscape complexity show variable patterns globally, primarily related to species traits and specific managed habitats. Leaf-cutting ants (LCAs) are native insects and important pests of plantation forests in South America. We evaluated the responses of LCA nests in young Eucalyptus plantations to different spatial contexts: land uses, interfaces (adjacent land use pairs), agroecosystems, and landscapes. We selected 30 sites in the littoral region of Argentina representing three types of land uses neighboring Eucalyptus plantations: adult eucalypt plantations, citrus plantations, and semi-natural habitats. At each site, we quantified and identified LCA nests and characterized landscape composition and configuration in circles of 250 m radius. LCA nest abundance and presence were similar across different land uses, interfaces, and agroecosystems. Nest presence decreased in landscapes with increasing mean perimeter/area ratio and citrus coverage, whereas LCA abundance showed a similar trend. This indicates that heterogeneous landscapes and those with greater citrus plantation coverage were less likely to have LCA nests. Our findings suggest that landscape configuration was the main predictor of the LCA presence. Understanding the dynamics of LCAs populations and their complex associations with landscape components will contribute to developing successful environmental pest management strategies for plantation forests.
Ecological intensification has been embraced with great interest by the academic sector but is still rarely taken up by farmers because monitoring the state of different ecological functions is not straightforward. Modelling tools can represent a more accessible alternative of measuring ecological functions, which could help promote their use amongst farmers and other decision-makers. In the case of crop pollination, modelling has traditionally followed either a mechanistic or a data-driven approach. Mechanistic models simulate the habitat preferences and foraging behaviour of pollinators, while data-driven models associate georeferenced variables with real observations. Here, we test these two approaches to predict pollination supply and validate these predictions using data from a newly released global dataset on pollinator visitation rates to different crops. We use one of the most extensively used models for the mechanistic approach, while for the data-driven approach, we select from among a comprehensive set of state-of-the-art machine-learning models. Moreover, we explore a mixed approach, where data-derived inputs, rather than expert assessment, inform the mechanistic model. We find that, at a global scale, machine-learning models work best, offering a rank correlation coefficient between predictions and observations of pollinator visitation rates of 0.56. In turn, the mechanistic model works moderately well at a global scale for wild bees other than bumblebees. Biomes characterized by temperate or Mediterranean forests show a better agreement between mechanistic model predictions and observations, probably due to more comprehensive ecological knowledge and therefore better parameterization of input variables for these biomes. This study highlights the challenges of transferring input variables across multiple biomes, as expected given the different composition of species in different biomes. Our results provide clear guidance on which pollination supply models perform best at different spatial scales – the first step towards bridging the stakeholder–academia gap in modelling ecosystem service delivery under ecological intensification.
The condition called "river disease" (MDR by its acronym in Spanish) is an intoxication in immature stages of honey bees caused by a compound from the genus Sebastiania Spreng and concentrated in the exudates of Epormenis cestri Berg. Our objective was to determine the temporal dynamics of the life cycle of E. cestri, its association with the predominant vegetation components and the influence of the Uruguay river on the size of its populations. With this aim, we selected 5 sites in the vicinity of the Uruguay river where populations of E. cestri were sampled using the Stem-tap technique modified for this purpose. The effect of landscape components on the abundance of E. cestri was evaluated using GLMM. It was determined that the hatching of the E. cestri eggs was in mid-October, finding a staggered distribution of its phenophases. In addition, we found significantly negative effects of the Espinal forest cover and the increase in the distance from the banks of the Uruguay river on the total abundance of E. cestri. This work shows some first clues for the understanding of how the components of the landscape structure the populations of E. cestri, allowing to predict the critical moment of incidence of MDR.
Latin America (LA) plays an important role in the global food supply and dedicates a significant part of its surface to croplands. Current losses of wild and managed pollinators are a threat to agricultural production because the productivity of many crops depends on entomophilous pollination; thus, consequences could be significant for the development of regional economies. We assess the current importance of pollination service for the main crops of Argentina, Brazil, Chile, Mexico, and Uruguay, which represent approximately 74% of the total surface of LA. Our study focused on three aspects, i) analyses of crops with varying degrees of pollinator dependence in terms of the harvested area and its yield, ii) estimation of economic value attributed to pollinators (EEV) and the vulnerability of each crop category, iii) characterization of the pollinator services provided by managed bees. Regional-level analyses showed that 58% of crops have essential and high dependence levels on insect pollination. LA produced 228.1 million tons of food that can be attributed directly to insect pollination, and an additional 33.9 million tons corresponds to crops that are not directly used for human food. The total production economic value of all crops dependent on pollination was US$ 77.82 billion, of which the economic value attributable to insect pollination was US$ 22.95 billion. Industrial crops and fruits were the leading crop category in the value of entomophilous pollination, followed by beverages, vegetables, hybrid seeds, citrus, and nuts. Crops occupy an area of 64.8 million hectares, 80% of which is used for soybean production, a clear sign of poor agricultural diversification, with Chile and Mexico being the countries with the highest degree of diversification. We estimated that hybrid seeds, fruits, and beverages whose productivity reached 44 million tons, are the most vulnerable to pollinator decline with 90, 64, and 44% vulnerability ratios. Our valuation demonstrates the vulnerability of agrosystems production, socioeconomic, and ecological terms.
Landscapes dominated by conventional agriculture reduce and simplify natural habitats, with negative consequences for ecosystem regulating services. We examined differences in structure and composition of bee com-munities across biotic and abiotic gradients to investigate how these communities respond to land-use changes associated with agriculture. Studies like ours which evaluates the relative effect of different components of spatial heterogeneity remain uncommon and are important to conserve pollinator fauna. The diversity of floral resources and habitat richness including the configuration and composition of landscape heterogeneity have been shown to influence the diversity of wild bees on a landscape scale. In this study, we examined how wild bee communities respond to landscape heterogeneity in a semi-arid productive region of Entre Rios Argentina. We modeled the effect of landscape heterogeneity on wild bee community abundance, species richness, and Chao-1 diversity. We sampled bees using pan traps in four common land-uses in the region (forest plantations, pasture/ croplands, mixed use areas and native espinal savanna) for five months in the spring-summer of 2014-2015. We identified 96 bee species among 3407 bees collected in the four habitat types. Pasture/croplands along with native espinal savanna supported the highest abundance, richness, and diversity of bees. Species composition of wild bee communities differed between land uses, with numerous species unique to each land use. Across all land use types, diversity of flower resources consistently supported more abundant and diverse wild bee communities. The richness of habitats along with the diversity of floral resources acted synergistically over wild bee com-munities. Our findings further clarify the relationship between land-use and wild bee communities, which provide valuable pollination services to crops and native plants. Continued expansion of large-scale monoculture forest plantations will likely come at the expense of the native floral resources, which are a key component to support regional bee species richness. Promoting landscapes with a diversity of crops and flower resources are important for the conservation of pollinators that are key for the functioning of ecosystems.
Seventy five percent of the world's food crops benefit from insect pollination. Hence, there has been increased interest in how global change drivers impact this critical ecosystem service. Because standardized data on crop pollination are rarely available, we are limited in our capacity to understand the variation in pollination benefits to crop yield, as well as to anticipate changes in this service, develop predictions, and inform management actions. Here, we present CropPol, a dynamic, open, and global database on crop pollination. It contains measurements recorded from 202 crop studies, covering 3,394 field observations, 2,552 yield measurements (i.e., berry mass, number of fruits, and fruit density [kg/ha], among others), and 47,752 insect records from 48 commercial crops distributed around the globe. CropPol comprises 32 of the 87 leading global crops and commodities that are pollinator dependent. Malus domestica is the most represented crop (32 studies), followed by Brassica napus (22 studies), Vaccinium corymbosum (13 studies), and Citrullus lanatus (12 studies). The most abundant pollinator guilds recorded are honey bees (34.22% counts), bumblebees (19.19%), flies other than Syrphidae and Bombyliidae (13.18%), other wild bees (13.13%), beetles (10.97%), Syrphidae (4.87%), and Bombyliidae (0.05%). Locations comprise 34 countries distributed among Europe (76 studies), North America (60), Latin America and the Caribbean (29), Asia (20), Oceania (10), and Africa (7). Sampling spans three decades and is concentrated on 2001-2005 (21 studies), 2006-2010 (40), 2011-2015 (88), and 2016-2020 (50). This is the most comprehensive open global data set on measurements of crop flower visitors, crop pollinators and pollination to date, and we encourage researchers to add more datasets to this database in the future. This data set is released for non-commercial use only. Credits should be given to this paper (i.e., proper citation), and the products generated with this database should be shared under the same license terms (CC BY-NC-SA).
While the cultivated area of pollinator-dependent crops is increasing, pollinator availability is decreasing, leading to problems in many agroecosystems. For this reason, pollinator-dependent crop growers often rent beehives to support their pollination requirements to sustain fruit productivity. However, the efficiency of those pollination systems has not been extensively studied. Here, we compared the effect of "precision" pollination (i.e., application of pesticides coordinated with growers, audit of hives, dietary supplementation and individual distribution of hives) with conventional practices (i.e., pesticides applications without coordination with growers and no audit of hives, low maintenance of hives and hives distributed in large groups) on the mean level of pollination and fruit production and quality in blueberry crops. In nine blueberry fields, we measured bee visitation rate to flowers, fruit set, fruit firmness and fruit weight. On average, precision-pollinated plots had 70% more bee visits to flowers and produced 13% more fruits that were 12% heavier and 12% firmer than those obtained through conventional practices. These results showed that pollination efficiency could be improved if key management related to bee strength, distribution and health care are taken into account. Due to these results, we encourage growers and beekeepers to include precision pollination practices to both increase the productivity of blueberry fields and the wellbeing of honey bees within agroecosystems.
Understanding how bees use resources at a landscape scale is essential for developing meaningful management plans that sustain populations and the pollination services they provide. Bumblebees are important pollinators for many wild and cultivated plants, and have experienced steep population declines worldwide. Bee foraging behavior can be influenced by resource availability and the bee’s lifecycle stage. To better understand these relationships, we studied the habitat selection of Bombus atratus by tracking 17 queen bumblebees with radio telemetry in blueberry fields in Entre Ríos province, Argentina. To evaluate land use and floral resources used by bumblebees, we tracked bees before and after nest establishment and estimated home ranges using minimum convex polygons and kernel density methods. We also classify the pollen of their body to determine which botanical resources they use from the floral species available. We characterized land use for each bee as the relative proportion of GPS points inside of each land use. Bumblebees differed markedly in their movement behavior in relation to nest establishment. They moved over larger areas and mostly within blueberry fields before to nest establishment, in contrast to after establishing the nest that they preferred the edges near forest plantations and changed the nutritional resources by wild floral species. Our study is the first to track queen bumblebee movements in an agricultural setting and relate movement change across time and space with pollen resource availability. This study provides insight into the way bumblebee queens use different habitat elements at crucial periods in their lifecycle, showing the importance of mass flowering crops like blueberry in the first stages of queen’s lifecycle and how diversified landscapes help support bee populations as their needs changes during different phases of their lifecycle.
Understanding how bees use the resources provided by crops of massive flowering is essential to develop meaningful agricultural management of plans to maximize the potential of pollination service. We assessed the effect of the pollination carried out by native species Bombus pauloensis and Apis mellifera on the production and quality of blueberry fruits. In this context, we tested the prediction that pollinator assemblages benefit fruit yield. Four treatments were performed: open pollination, B. pauloensis pollination, A. mellifera pollination, and autogamy. For each treatment, the frequency of floral visitors, fruit setting, yield, and quality were evaluated. The results showed that Vaccinium corymbosum L. ‘Emerald’ is highly dependent on entomophilous pollination to obtain optimal production and high-quality fruit, and that pollination with A. mellifera generated the highest proportion of fruit setting (0.80 ± 0.03). The highest seed number was found in open pollinated fruits. This study highlights the effect of the interactions among wild and managed pollinators on the productivity of commercial blueberry fields, and is the first report of B. pauloensis use in blueberry pollination.