Distance from forest edge affects bee pollinators in oilseed rape fields

Wild pollinators have been shown to enhance the pollination of Brassica napus (oilseed rape) and thus increase its market value. Several studies have previously shown that pollination services are greater in crops adjoining forest patches or other seminatural habitats than in crops completely surrounded by other crops. In this study, we investigated the specific importance of forest edges in providing potential pollinators in B. napus fields in two areas in France. Bees were caught with yellow pan traps at increasing distances from both warm and cold forest edges into B. napus fields during the blooming period. A total of 4594 individual bees, representing six families and 83 taxa, were collected. We found that both bee abundance and taxa richness were negatively affected by the distance from forest edge. However, responses varied between bee groups and edge orientations. The ITD (Inter‐Tegular distance) of the species, a good proxy for bee foraging range, seems to limit how far the bees can travel from the forest edge. We found a greater abundance of cuckoo bees (Nomada spp.) of Andrena spp. and Andrena spp. males at forest edges, which we assume indicate suitable nesting sites, or at least mating sites, for some abundant Andrena species and their parasites (Fig.  1 ). Synthesis and Applications. This study provides one of the first examples in temperate ecosystems of how forest edges may actually act as a reservoir of potential pollinators and directly benefit agricultural crops by providing nesting or mating sites for important early spring pollinators. Policy‐makers and land managers should take forest edges into account and encourage their protection in the agricultural matrix to promote wild bees and their pollination services.

Figure 1 Open in figure viewer PowerPoint Left, a Nomada sp male; right, an Andrena sp male. Caption Left, a Nomada sp male; right, an Andrena sp male.

Introduction

Pollinators play an important functional role in most terrestrial ecosystems and provide a key ecosystem service (Ashman et al. 2004 ). Insects, particularly bees, are the primary pollinators for the majority of the world's angiosperms (Ollerton et al. 2012 ). Without this service, many interconnected species and processes functioning within both wild and agricultural ecosystems could collapse (Kearns et al. 1998 ). Brassica napus (oilseed rape, OSR) represents the most widespread entomophilous crop in France with almost 1.5 Mha in 2010 (FAOSTAT August 10th, 2012). Results differ between varieties, but even though it seems that OSR produces 70% of its fruits through self‐pollination (Downey et al. 1970 in Mesquida and Renard 1981 ), native bees are also known to contribute to its pollination (Morandin and Winston 2005 ; Jauker et al. 2012 ). Bee pollination leads to improved yields (Steffan‐Dewenter 2003b ; Sabbahi et al. 2005 ) and to a shorter blooming period (Sabbahi et al. 2006 ), thus increasing the crop's market value (Bommarco et al. 2012 ). The most widely used species in crop pollination is the honeybee (Apis mellifera L) which is sometimes assumed to be sufficient for worldwide crop pollination (Aebi and Neumann 2011 ). However, this assertion has been questioned by different authors (Ollerton et al. 2012 ), and several studies show that many wild bees are also efficient pollinators of crops (Klein et al. 2007 ; Winfree et al. 2008 ; Breeze et al. 2011 ). Recently, Garibaldi et al. ( 2013 ) found positive associations of fruit set with wild‐insect visits to flowers in 41 crop systems worldwide. They demonstrate that honeybees do not maximize pollination, nor can they fully replace the contributions of diverse, wild‐insect assemblages to fruit set for a broad range of crops and agricultural practices on all continents with farmland. Unfortunately, not only are honey bees declining due to a variety of different causes (vanEngelsdorp et al. 2009 ), wild bee populations are also dwindling (Potts et al. 2010 ). Their decline has been documented in two Western European countries (Britain and the Netherlands) by comparing data obtained before and after 1980 (Biesmeijer et al. 2006 ). These losses have mostly been attributed to the use of agrochemicals, the increase in monocultures, the loss of seminatural habitat and deforestation (Steffan‐Dewenter et al. 2002 ; Steffan‐Dewenter and Westphal 2008 ; Brittain and Potts 2011 ). Several studies have shown the importance of natural or seminatural habitats in sustaining pollinator populations or pollination services close to fruit crops (Steffan‐Dewenter 2003a ; Kremen et al. 2004 ; Greenleaf and Kremen 2006a ; Carvalheiro et al. 2010 ). Morandin and Winston ( 2006 ) presented a cost–benefit model that estimates profit in OSR agroecosystems with different proportions of uncultivated land. They calculated that yield and profit could be maximized with 30% of the land left uncultivated within 750 m of field edges. Other studies have demonstrated a negative impact of the distance from forests on pollination services or bee abundance and richness both in tropical ecosystems (De Marco and Coelho 2004 ; Blanche et al. 2006 ; Chacoff and Aizen 2006 ) and in temperate ecosystems (Hawkins 1965 ; Taki et al. 2007 ; Arthur et al. 2010 ; Watson et al. 2011 ). These studies all suggest that natural or seminatural habitats are important sources of pollinators, probably because they provide “partial habitats” (Westrich 1996 ) such as complementary mating, foraging, nesting, and nesting materials sites that bees need to complete their life cycle. In this study, we focused on the effect of distance to forest edge on bee assemblages in OSR ecosystems. Forest edges could provide one or more important partial habitats for different bee species in agricultural landscapes, in particular when associated with a mass‐flowering crop such as OSR (Le Feon et al. 2011 ). For example, the availability of untilled soil and dead branches might provide ground‐nesting and cavity‐nesting bee species with numerous nesting sites. Moreover, during spring at least, the understory and the forest edge can provide cover containing flowering plants and wild trees such as Prunus spp, Castanea sativa, or Salix spp and thereby allow bees to find alternative floral resources. During spring 2010 and 2011, in two areas in France, we examined wild bee abundance and taxa richness both along forest edges and inside OSR fields at different distances from the forest. Like other taxa, bees respond to environmental variables according to their biologic traits that determine access and requirements for nesting, mating, and forage resources, species mobility or physiological tolerance. Specifically, we hypothesized that (1) bee abundance, species richness, and composition of bee communities within the crop field are dependent on the distance from the forest edge (where complementary floral resources, nesting sites, shelters, etc. can be found) and on the orientation of the forest edge; (2) the identity of bees in the crop is related to their foraging range which we measured with the ITD (Inter‐Tegular distance); (3) the forest edge may be the nesting or mating sites for cavity‐nesting or ground‐nesting bees such as Osmia spp or Andrena spp which are important groups of potential early spring pollinators for OSR.