Bridging the Gap between Field Experiments and Machine Learning: The EC H2020 B-GOOD Project as a Case Study towards Automated Predictive Health Monitoring of Honey Bee Colonies.

Honey bee colonies have great societal and economic importance. The main challenge that beekeepers face is keeping bee colonies healthy under ever-changing environmental conditions. In the past two decades, beekeepers that manage colonies of Western honey bees (Apis mellifera) have become increasingly concerned by the presence of parasites and pathogens affecting the bees, the reduction in pollen and nectar availability, and the colonies' exposure to pesticides, among others. Hence, beekeepers need to know the health condition of their colonies and how to keep them alive and thriving, which creates a need for a new holistic data collection method to harmonize the flow of information from various sources that can be linked at the colony level for different health determinants, such as bee colony, environmental, socioeconomic, and genetic statuses. For this purpose, we have developed and implemented the B-GOOD (Giving Beekeeping Guidance by computational-assisted Decision Making) project as a case study to categorize the colony's health condition and find a Health Status Index (HSI). Using a 3-tier setup guided by work plans and standardized protocols, we have collected data from inside the colonies (amount of brood, disease load, honey harvest, etc.) and from their environment (floral resource availability). Most of the project's data was automatically collected by the BEEP Base Sensor System. This continuous stream of data served as the basis to determine and validate an algorithm to calculate the HSI using machine learning. In this article, we share our insights on this holistic methodology and also highlight the importance of using a standardized data language to increase the compatibility between different current and future studies. We argue that the combined management of big data will be an essential building block in the development of targeted guidance for beekeepers and for the future of sustainable beekeeping.

Uncovering the significance of the ratio of food K:Na in bee ecology and evolution.

Bees provide important ecological services, and many species are threatened globally, yet our knowledge of wild bee ecology and evolution is limited. While evolving from carnivorous ancestors, bees had to develop strategies for coping with limitations imposed on them by a plant-based diet, with nectar providing energy and essential amino acids and pollen as an extraordinary, protein- and lipid-rich food nutritionally similar to animal tissues. Both nectar and pollen display one characteristic common to plants, a high ratio of potassium to sodium (K:Na), potentially leading to bee underdevelopment, health problems, and death. We discuss why and how the ratio of K:Na contributes to bee ecology and evolution and how considering this factor in future studies will provide new knowledge, more accurately depicting the relationship of bees with their environments. Such knowledge is essential for understanding how plants and bees function and interact and is needed to effectively protect wild bees.

The conserved and high K-to-Na ratio in sunflower pollen: Possible implications for bee health and plant-bee interactions.

Sodium (Na) concentrations are low in plant tissues, and its metabolic function in plants is minor; however, Na is a key nutrient for plant consumers. Previous studies have thus far focused on Na concentration. Nevertheless, a balanced potassium (K) to Na ratio (K:Na) is more important than Na concentration alone since food with high K:Na has detrimental effects on consumers irrespective of Na concentration. Therefore, plants may actively regulate K:Na in their tissues and products, shaping plant-insect interactions. Studies considering nutritional aspects of plant-insect interactions have focused on nonreproductive tissues and nectar. In this study, we consider pollen as serving a primary reproductive function for plants as well as a food of pollinivores. Plants might regulate K:Na in pollen to affect their interactions with pollinivorous pollinators. To investigate whether such a mechanism exists, we manipulated Na concentrations in soil and measured the proportion of K, Na, and 13 other nutrient elements in the pollen of two sunflower (Helianthus annuus) cultivars. This approach allowed us to account for the overall nutritional quality of pollen by investigating the proportions of many elements that could correlate with the concentrations of K and Na. Of the elements studied, only the concentrations of Na and K were highly correlated. Pollen K:Na was high in both cultivars irrespective of Na fertilization, and it remained high regardless of pollen Na concentration. Interestingly, pollen K:Na did not decrease as pollen increased the Na concentration. We hypothesize that high K:Na in pollen might benefit plant fertilization and embryonic development; therefore, a tradeoff might occur between producing low K:Na pollen as a reward for pollinators and high K:Na pollen to optimize the plant fertilization process. This is the first study to provide data on pollen K:Na regulation by plants. Our findings broaden the understanding of plant-bee interactions and provide a foundation for a better understanding of the role of the soil-plant-pollen-pollinator pathway in nutrient cycling in ecosystems. Specifically, unexplored costs and tradeoffs related to balancing the K:Na by plants and pollinivores might play a role in past and current shaping of pollination ecology.

Phenology and production of pollen, nectar, and sugar in 1612 plant species from various environments.

To predict the quantity and quality of food available to pollinators in various landscapes over time, it is necessary to collect detailed data on the pollen, nectar, and sugar production per unit area and the flowering phenology of plants. Similar data are needed to estimate the contribution of plants to the functioning of food webs via the flow of energy and nutrients through the soil-plant-nectar/pollen-consumer pathway. Current knowledge on this topic is fragmented. This database represents the first compilation of data on the various food resources produced by 1612 plant species belonging to 755 genera and 133 families, including crop plants and wild plants, annuals and perennials, animal- and wind-pollinated plants, and weeds and trees growing in different ecosystems under various environmental conditions. The data set consists of 103 parameters related to the traits of plant species and geographical and environmental factors, allowing for precise calculations of the amounts of nectar, pollen, and energy provided by plants and available to consumers in the considered flora or ecosystem on a daily basis throughout the year. These parameters, gathered by us and extracted from the available literature, describe pollen, nectar, and sugar production (where applicable, in mass, volume, and concentration units), honey yield, the timing and duration of flowering, flower longevity, number of plants and flowers per unit area, weather conditions (temperature and precipitation), geographical location, landscape, and syntaxonomy. The data were obtained from various, mostly European, pedoclimatic zones, and the majority of the data were available for plant species and communities present in Central Europe, especially in Poland, where research on floral resources has a long tradition. These data are representative of the whole continent and may be used as a reference for plant communities occurring on continents other than Europe since the database allows for the consideration of differences in the production of resources by a single plant species growing in different communities. This data set provides a unique opportunity to test hypotheses related to the functioning of food webs, nutrient cycling, plant ecology, and pollinator ecology and conservation. The data are released under a CC-BY-NC-SA license, and this paper must be properly cited when using the database.

Unravelling the dependence of a wild bee on floral diversity and composition using a feeding experiment.

We investigated nutrition as a potential mechanism underlying the link between floral diversity/composition and wild bee performance. The health, resilience, and fitness of bees may be limited by a lack of nutritionally balanced larval food (pollen), influencing the entire population, even if adults are not limited nutritionally by the availability and quality of their food (mainly nectar). We hypothesized that the nutritional quality of bee larval food is indirectly connected to the species diversity of pollen provisions and is directly driven by the pollen species composition. Therefore, the accessibility of specific, nutritionally desirable key plant species for larvae might promote bee populations. Using a fully controlled feeding experiment, we simulated different pollen resources that could be available to bees in various environments, reflecting potential changes in floral species diversity and composition that could be caused by landscape changes. Suboptimal concentrations of certain nutrients in pollen produced by specific plant species resulted in reduced bee fitness. The negative effects were alleviated when scarce nutrients were added to these pollen diets. The scarcity of specific nutrients was associated with certain plant species but not with plant diversity. Thus, one of the mechanisms underlying the decreased fitness of wild bees in homogenous landscapes may be nutritional imbalance, i.e., the scarcity of specific nutrients associated with the presence of certain plant species and not with species diversity in pollen provisions eaten by larvae. Accordingly, we provide a conceptual representation of how the floral species composition and diversity can impact bee populations by affecting fitness-related life history traits. Additionally, we suggest that mixes of 'bee-friendly' plants used to improve the nutritional base for wild bees should be composed considering the local flora to supplement bees with vital nutrients that are scarce in the considered environment.

Stoichiometric niche, nutrient partitioning and resource allocation in a solitary bee are sex-specific and phosphorous is allocated mainly to the cocoon.

Life histories of species may be shaped by nutritional limitations posed on populations. Yet, populations contain individuals that differ according to sex and life stage, each of which having different nutritional demands and experiencing specific limitations. We studied patterns of resource assimilation, allocation and excretion during the growth of the solitary bee Osmia bicornis (two sexes) under natural conditions. Adopting an ecological perspective, we assert that organisms ingest mutable organic molecules that are transformed during physiological processes and that the immutable atoms of the chemical elements composing these molecules may be allocated to specific functions, thereby influencing organismal fitness and life history. Therefore, using the framework of ecological stoichiometry, we investigated the multielemental (C, N, S, P, K, Na, Ca, Mg, Fe, Zn, Mn, Cu) compositions of six components of the bee elemental budget: food (pollen), eggs, pupae, adults, cocoons and excreta. The sexes differed fundamentally in the assimilation and allocation of acquired atoms, elemental phenotypes, and stoichiometric niches for all six components. Phosphorus, which supports larval growth, was allocated mainly (55-75%) to the cocoon after larval development was complete. Additionally, the majority (60-99%) of the Mn, Ca, Mg and Zn acquired during larval development was allocated to the cocoon, probably influencing bee fitness by conferring protection. We conclude that for holometabolous insects, considering only the chemical composition of the adult body within the context of nutritional ecology does not provide a complete picture. Low ratios of C to other nutrients, low N:P and high Na concentrations in excreta and cocoons may be important for local-scale nutrient cycling. Limited access to specific nutritional elements may hinder bee development in a sex-dependent manner, and N and P limitations, commonly considered elsewhere, may not play important roles in O. bicornis. Sexual dimorphism in nutritional limitations due to nutrient scarcity during the larval stage may influence bee population function and should be considered in bee conservation efforts.

The Scarcity of Specific Nutrients in Wild Bee Larval Food Negatively Influences Certain Life History Traits.

Bee nutrition studies have focused on food quantity rather than quality, and on details of bee biology rather than on the functioning of bees in ecosystems. Ecological stoichiometry has been proposed for studies on bee nutritional ecology as an ecosystem-oriented approach complementary to traditional approaches. It uses atomic ratios of chemical elements in foods and organisms as metrics to ask ecological questions. However, information is needed on the fitness effects of nutritional mismatches between bee demand and the supply of specific elements in food. We performed the first laboratory feeding experiment on the wild bee Osmia bicornis, investigating the impact of Na, K, and Zn scarcity in larval food on fitness-related life history traits (mortality, cocoon development, and imago body mass). We showed that bee fitness is shaped by chemical element availability in larval food; this effect may be sex-specific, where Na might influence female body mass, while Zn influences male mortality and body mass, and the trade-off between K allocation in cocoons and adults may influence cocoon and body development. These results elucidate the nutritional mechanisms underlying the nutritional ecology, behavioral ecology, and population functioning of bees within the context of nutrient cycling in the food web.

Sexual Dimorphism in the Multielemental Stoichiometric Phenotypes and Stoichiometric Niches of Spiders.

Nutritional limitations may shape populations and communities of organisms. This phenomenon is often studied by treating populations and communities as pools of homogenous individuals with average nutritional optima and experiencing average constraints and trade-offs that influence their fitness in a standardized way. However, populations and communities consist of individuals belonging to different sexes, each with specific nutritional demands and limitations. Taking this into account, we used the ecological stoichiometry framework to study sexual differences in the stoichiometric phenotypes, reflecting stoichiometric niches, of four spider taxa differing in the hunting mode. The species and sexes differed fundamentally in their elemental phenotypes, including elements beyond those most commonly studied (C, N and P). Both species and sexes were distinguished by the C:N ratio and concentrations of Cu, K and Zn. Species additionally differed in concentrations of Na, Mg and Mn. Phosphorous was not involved in this differentiation. Sexual dimorphism in spiders' elemental phenotypes, related to differences in their stoichiometric niches, suggests different nutritional optima and differences in nutritional limitation experienced by different sexes and species. This may influence the structure and functioning of spider populations and communities.

A Better Understanding of Bee Nutritional Ecology Is Needed to Optimize Conservation Strategies for Wild Bees-The Application of Ecological Stoichiometry.

The observed decline in wild bees may be connected to the decreasing diversity of flowering plants. Changes in floral composition shape nutrient availability in inhabited areas, and bee larvae need food rich in body-building nutrients to develop into adults. Adult food, mainly composed of energy-rich nectar, differs from larval food, mainly composed of pollen, and adult bees forage on different plant species for nectar and pollen. Defining bee-friendly plants based on the quantities of food produced, and on the visitation rates of adult pollinating insects leads to the planting of bee habitats with poor-quality food for larvae, which limits their growth and development, and negatively affects the population. Consequently, failing to understand the nutritional needs of wild bees may lead to unintended negative effects of conservation efforts. Ecological stoichiometry was developed to elucidate the nutritional constraints of organisms and their colonies, populations, and communities. Here, I discuss how applying ecological stoichiometry to the study of the nutritional ecology of wild bees would help fill the gaps in our understanding of bee biology. I present questions that should be answered in future studies to improve our knowledge of the nutritional ecology of wild bees, which could result in better conservation strategies.

Predation Cues in Solitary bee Nests.

Predation at the nesting site can significantly affect solitary bees' reproductive success. We tested female red mason bees' (Osmia bicornis L.) acceptance of potential nesting sites, some of which were marked with cues coming from predated conspecifics (crushed bees) or from a predator itself (rodent excreta). In our experiment, females did not avoid nests marked with either of the two predator cues. We suggest that bee females do not recognize these two cues as risky. Alternatively, costs of abandoning natal aggregation might be too high compared with any perceived predation risk of staying. Moreover, the presence of crushed bees can provide positive information about the presence of conspecifics and, possibly, information about a nesting aggregation that may be preferred by bees when choosing a nesting site.

Ecological stoichiometry of the honeybee: Pollen diversity and adequate species composition are needed to mitigate limitations imposed on the growth and development of bees by pollen quality.

The least understood aspects of the nutritional needs of bees are the elemental composition of pollen and the bees' need for a stoichiometrically balanced diet containing the required proportions of nutrients. Reduced plant diversity has been proposed as an indirect factor responsible for the pollinator crisis. We suggest stoichiometric mismatch resulting from a nutritionally unbalanced diet as a potential direct factor. The concentrations and stoichiometric ratios of C, N, S, P, K, Na, Ca, Mg, Fe, Zn, Mn, and Cu were studied in the bodies of honeybees of various castes and sexes and in the nectar and pollen of various plant species. A literature review of the elemental composition of pollen was performed. We identified possible co-limitations of bee growth and development resulting mainly from the scarcity of Na, S, Cu, P and K, and possibly Zn and N, in pollen. Particular castes and sexes face specific limitations. Concentrations of potentially limiting elements in pollen revealed high taxonomic diversity. High floral diversity may be necessary to maintain populations of pollen eaters. Single-species crop plantations, even if these species are rich in nectar and pollen, might limit bee growth and development, not allowing for gathering nutrients in adequate proportions. However, particular plant species may play greater roles than others in balancing honeybee diets. Therefore, we suggest specific plant species that may (1) ensure optimal growth and production of individuals by producing pollen that is exceptionally well balanced stoichiometrically (e.g., clover) or (2) prevent growth and development of honeybees by producing pollen that is extremely unbalanced for bees (e.g., sunflower). Since pollen is generally poor in Na, this element must be supplemented using "dirty water". Nectar cannot supplement the diet with limiting elements. Stoichiometric mismatch should be considered in intervention strategies aimed at improving the nutritional base for bees.

Sedentary antlion larvae (Neuroptera: Myrmeleontidae) use vibrational cues to modify their foraging strategies.

Learning abilities are exhibited by many animals, including insects. However, sedentary species are typically believed to have low capacities and requirements for learning. Despite this view, recent studies show that even such inconspicuous organisms as larval antlions, which employ an ambush predation strategy, are capable of learning, although their learning abilities are rather simple, i.e., limited to the association of vibrational cues with the arrival of prey. This study demonstrates, for the first time, that antlion larvae can use vibrational cues for complex modifications of their foraging strategies. Specifically, antlion larvae rapidly learn to differentiate between the vibrational cues associated with prey of different sizes, and they save resources by ignoring smaller prey in favour of larger, more energetically profitable prey. Moreover, antlion larvae can learn to associate vibrational cues with the loss of their prey, and they respond by burying their victims under the sand more often and more rapidly than do individuals with no opportunities to form such associations. These findings provide not only new insights into the cognitive abilities of animals but also support for the optimal foraging strategy concept, suggesting the importance of maximizing fitness output by balancing the costs and benefits of alternative foraging strategies.

How to make a beetle out of wood: multi-elemental stoichiometry of wood decay, xylophagy and fungivory.

The majority of terrestrial biomass is wood, but the elemental composition of its potential consumers, xylophages, differs hugely from that of wood. This causes a severe nutritional imbalance. We studied the stoichiometric relationships of 11 elements (C, N, P, K, Ca, Mg, Fe, Zn, Mn, Cu, Na) in three species of pine-xylem-feeding insects, Stictoleptura rubra, Arhopalus rusticus (Coleoptera, Cerambycidae) and Chalcophora mariana (Coleoptera, Buprestidae), to elucidate their mechanisms of tissue growth and to match their life histories to their dietary constraints. These beetles do not differ from other Coleoptera in their absolute elemental compositions, which are approximately 1000 (N), 100 (P, Cu) and 50 (K, Na) times higher than in dead but undecayed pine wood. This discrepancy diminishes along the wood decay gradient, but the elemental concentrations remain higher by an order of magnitude in beetles than in highly decayed wood. Numerical simulation of the life history of S. rubra shows that feeding on nutrient-poor undecayed wood would extend its development time to implausible values, whereas feeding on highly decomposed wood (heavily infected with fungi) would barely balance its nutritional budget during the long development period of this species. The changes in stoichiometry indicate that the relative change in the nutrient levels in decaying wood cannot be attributed solely to carbon loss resulting from decomposer respiration: the action of fungi substantially enriches the decaying wood with nutritional elements imported from the outside of the system, making it a suitable food for wood-eating invertebrates.