Impacts of honeybee density on crop yield: A meta-analysis

There is increasing recognition that pollination deficits are limiting crop yields world-wide. However, management strategies for optimal insect pollination are still unclear for most crops. Current management focuses on providing high densities of honeybees, but recommended densities are highly variable, even within single crops and cultivars. We performed an extensive literature search to record honeybee densities (colony density and/or flower visitation rates) and crop productivity (fruit set, seed set, fruit weight and/or yield). Effect sizes were represented as the difference in crop productivity between the two most extreme levels of honeybee densities. Out of 795 reviewed studies, only 22 analysed the effect of at least two levels of honeybee densities on crop productivity (reporting 60 resulting effect sizes in total). Moreover, few recommendations for crop pollination management are based on results from controlled experimental designs, and with comparable methodology. We found that both colony density and visitation rates increased all the productivity variables. However, effects were nonlinear for visitation rates, suggesting that there is an optimum (mean of 8-10 visits per flower) beyond which more honeybees are not beneficial (and can even be detrimental) for crop productivity. Effect sizes for visitation rates were greater than that for colony densities, suggesting that visitation rates are a more direct measure of the pollination process. Data on the relation between colony density and visitation rates are lacking. Interestingly, effect sizes for visitation rates were greater for crops with separate sexes than those with hermaphroditic flowers; therefore, the benefits of honeybee pollination vary according to the crop biology.Synthesis and applications. Current practices for crop pollination assume that more honeybees are always better for crop yield, even if the effect of this management on crop production still unclear. In contrast, our analyses suggest that there is an optimum for honeybee densities. Despite the importance of honeybees and pollinator-dependent crops world-wide, there is a lack of studies designed for finding such an optimal level of crop pollination. Our analyses further suggest that visitation rates could be used as a proxy to guide management recommendations such as colony density and spatial arrangement. Foreign Language AbstractResumen Los deficits de polinizacion estan limitando la productividad de los cultivos en todo el mundo. Para sustentar el servicio de polinizacion en zonas de agricultura intensiva, el manejo actual consiste en saturar los cultivos de flores con abejas meliferas proveyendo altas densidades de colmenas. Sin embargo, se sabe muy poco sobre la eficiencia de este manejo para poder alcanzar una polinizacion optima y existe controversia respecto las densidades recomendadas. Realizamos una sintesis global de la literatura cientifica para registrar la densidad de abejas meliferas (tasa de visitas o densidad de colmenas) y la productividad de los cultivos (cantidad de frutos o de semillas por flor, peso del fruto, o rendimiento por hectarea o planta). Los tamanos de efecto se calcularon como la diferencia en la productividad entre los dos niveles mas extremos de densidades de abejas. De los 795 estudios revisados, solo 22 analizaron el efecto de al menos dos niveles de densidad de abejas sobre la productividad de los cultivos (resultando en 60 tamanos de efecto en total). Ademas, pocos estudios se basan en los resultados de disenos experimentales controlados y con una metodologia comparable. Encontramos que tanto la tasa de visita como la densidad de colmenas aumentaron todas las variables de productividad. Sin embargo, el efecto de la tasa de visita fue curvilineo, lo que sugiere que hay un optimo (8-10 visitas por flor) mas alla del cual mas abejas no es beneficioso (o incluso perjudicial) para la productividad de los cultivos. Los tamanos de efecto para la tasa de visitas fueron mayores que para la densidad de colmenas, lo que sugiere que la tasa de visitas es una medida mas directa del proceso de polinizacion. Faltan datos sobre la relacion entre la tasa de visitas y la densidad de colmenas. De modo interesante, el tamano de efecto de la tasa de visitas fue mayor para cultivos con sexos separados que para aquellos con flores hermafroditas, lo que sugiere que los beneficios de la polinizacion por la abeja melifera dependen de la biologia floral. Sintesis y aplicaciones. El manejo actual para la polinizacion de los cultivos asume que mas abejas siempre aumenta la productividad de los cultivos. En cambio, nuestros analisis sugieren que existe un optimo para la tasa de visita de abejas y que esa variable podria usarse como un proxy para guiar las recomendaciones de manejo, como la densidad de colmenas y su disposicion espacial. Current practices for crop pollination assume that more honeybees are always better for crop yield, even if the effect of this management on crop production still unclear. In contrast, our analyses suggest that there is an optimum for honeybee densities. Despite the importance of honeybees and pollinator-dependent crops world-wide, there is a lack of studies designed for finding such an optimal level of crop pollination. Our analyses further suggest that visitation rates could be used as a proxy to guide management recommendations such as colony density and spatial arrangement.