human land use and wild bee visitation to crops
Contrary to our expectations, we found no strong associations between land-use intensity (at either local or landscape scale) and wild bee visitation to crops (Table 3). The best models were statistically significant for only two of our eight data sets, and none was significant after correcting for multiple comparisons.
Natural history traits such as sociality and nesting requirements can determine how bees respond to land use (Klein, Steffan-Dewenter & Tscharntke 2003a; Steffan-Dewenter et al. 2006), and variation in traits among species could lead to findings of no significant effect for the bee community as a whole. However, our analyses by natural history trait revealed only one pattern not found at the community scale: solitary species were positively associated with the abundance of weedy flowers in the farm field. Even obligatorily wood-nesting bees did not have strong associations with woodland cover at either the local or the landscape scales.
Previous studies of crop visitation by wild pollinators have found negative effects of human land use at the local and/or landscape scale (Klein et al. 2007; Kremen & Chaplin-Kramer 2007). Why then did land-use intensity have such weak effects in our study? We suggest four possible reasons, which are not mutually exclusive. First, we considered the possibility that we were unable to detect the true effects of human disturbance because our data sets were too small and/or variable, especially given the known variability of wild bee populations (Williams, Minckley & Silveira 2001). This may have been the case for our smaller data sets from 2004. However, the statistical models for the more extensive 2005 data sets showed even less association between wild bees and land use than those from 2004. In particular, our 2005 watermelon data set included 23 sites, 3828 wild bee visits to 15 888 watermelon flowers, and 1221 collected specimens, yet all variables relating to land-use intensity were highly non-significant. In contrast, many studies finding significant effects of land use on wild bees in other systems had smaller or similar sample sizes, e.g. 104 wild bee visits to grapefruit in Argentina (Chacoff & Aizen 2006); 615 wild bee visits to coffee in Costa Rica (Ricketts 2004); and 3349 wild bee visits to watermelon in California (Kremen, Williams & Thorp 2002; Kremen et al. 2004). Furthermore, for our 2005 watermelon data set we considered the range of values for the number of wild bee visits per flower per day that were included within the 95% confidence intervals for the slope in single regressions against each of our metrics of woodland cover (this approach is preferable to power analysis; Colegrave & Ruxton 2005). Across the gradient, the lower 95% CI prediction was 38–108 visits per flower per day (for proportion woodland) or 65–109 (for distance to woodland), both of which are more than the number of visits required for full fruit set (10–40 visits; R.W., unpublished data). This means that, even when we consider the range of possible slopes that might be consistent with our data, wild bees provide sufficient visitation to supply plants with crop pollination services across the entire land-use gradient.
Second, we may have found few differences between organic and conventional farm management because, in our system, many of the features often associated with organic farming (Hole et al. 2005) are common to both management categories. Organic and conventional farms did not differ significantly in farm field size (mean ± SD for organic 4789 ± 4475 m2, conventional 6525 ± 4048 m2; t-test, t = 0·92, P = 0·37), number of crops grown (organic 2·0 ± 2·4 different crops per 1000 m2, conventional 0·7 ± 0·4 per 1000 m2; Wilcoxon test, χ2 = 1·0, P = 0·32), weedy flower density (organic 68 ± 80 cm flowers per 600 cm, conventional 41 ± 35 cm flowers per 600 cm; Wilcoxon test, χ2 = 0·45, P = 0·50), or the density of weedy flower species (organic 6·0 ± 2·6 species per 600 cm, conventional 6·6 ± 2·4 species per 600 cm; t-test, t = 0·50, P = 0·62). Synthetic pesticide, herbicide and fertilizers are used only on the conventional farms, and some of the synthetic pesticides used in our area are known to be highly toxic to bees (e.g. malathion and permethrin). However, organic farms are also permitted to use certain non-synthetic pesticides. Overall, our findings are consistent with the suggestion of Benton, Vickery & Wilson (2003) that the local habitat heterogeneity resulting from factors such as weediness and field size may be more important than organic farming per se in supporting biodiversity. Our results are also consistent with previous findings that farm management exerts a stronger effect on insect diversity in homogeneous landscapes (Tscharntke et al. 2005; Rundlöf & Smith 2006), whereas our landscapes were heterogeneous.
Third, the phenology of floral resources in our study system may be complementary between woodlands and human-disturbed habitats (Heinrich 1976). In our study system, flowers and pollinators are abundant in spring woodlands, but by the time the forest canopy closes in June, there is little bloom and few pollinators (R.W., unpublished data). In contrast, by June many species are flowering in agricultural areas, old fields, and gardens, and such habitats can continue to provide floral resources through the autumn. Our data set was dominated by bee species with long flight seasons [e.g. Bombus, Lasioglossum (Dialictus), Halictus, Ceratina], which could take advantage of this complementarity over time. Several other studies in temperate forest ecosystems have also found that although forests support certain bee species, they support lower bee densities than human-disturbed habitats (Banaszak 1992, 1996; Klemm 1996; Steffan-Dewenter et al. 2002; Winfree et al. 2007a).
Fourth, high dispersion of natural habitat fragments and high habitat heterogeneity throughout our study system may make it better for many bee species. Habitat heterogeneity is a key factor promoting biodiversity in agricultural landscapes (Tscharntke et al. 2005; Rundlöf & Smith 2006). Bees may benefit from habitat heterogeneity because their foraging, nesting and overwintering resources are often located in different habitat types (Westrich 1996). One indication of high heterogeneity in our study system is the large range of variation in terms of the proportion of woodland cover in the landscape surrounding each farm at a 2 km radius (8–60%; all metrics were calculated for our 2005 watermelon data set), compared with the small range of variation in distance to the nearest patch of woodland (18–343 m). Furthermore, these two measures are uncorrelated (Pearson's r = −0·28, P = 0·19). Thus a farm site could have very low proportional woodland in the surrounding landscape, but still have a patch of woodland within tens of metres of the farm site. Our system contrasts with California's Central Valley, where several studies finding a negative effect of habitat loss on bees have been carried out (Kremen, Williams & Thorp 2002; Kremen et al. 2004; Greenleaf & Kremen 2006a, 2006b ). In California, the range of variation in the proportion of natural habitat in the surrounding landscape is similar to ours (0–62%), but the distance to the nearest natural habitat patch also varies greatly (35–5980 m; C.K., unpublished data), and is highly negatively correlated with landscape cover (Spearman's ρ = −0·93, P < 0·0001). This comparison suggests that there is local-scale heterogeneity in the New Jersey/Pennsylvania system across the entire landscape gradient, whereas in the California system local-scale heterogeneity is found only in the landscapes with most natural habitat.
Two other measures related to heterogeneity can be contrasted between our system and other studies that found negative effects of human land use on bees. In the work of Morandin & Winston (2005), crop field sizes were at least two orders of magnitude larger than those in our study; in studies that reported the maximum distance to the nearest patch of natural habitat, these distances ranged from 900 to 1600 m (Klein, Steffan-Dewenter & Tscharntke 2003a, 2003b; Ricketts 2004; Chacoff & Aizen 2006), compared with 318 m in our study.
Habitat heterogeneity in our system can also be compared with studies relating landscape-scale heterogeneity to biodiversity of other taxa in agricultural systems. In a study of butterflies, ‘heterogeneous’ agricultural landscapes were defined as those for which pasture constitutes a large proportion (on average 19%) of all agricultural lands (Rundlöf & Smith 2006). In our system, pasture constitutes 22% of all agricultural lands (USDA-NASS 2004). Furthermore, in our system hay fields constitute 44% of all non-pasture croplands (USDA-NASS 2004). Heterogeneity is further added to our system by suburban/urban development, which ranged from 11 to 73% at a 2-km radius. Other studies have found suburban/urban areas to support diverse bee faunas (Cane et al. 2006; Winfree et al. 2007a). Another definition that has been used in the published literature is that complex or heterogeneous agricultural landscapes are those containing ≥20% non-crop habitat (Tscharntke et al. 2005). Our entire study system meets this criterion, because the maximum proportion of agriculture was 66%.
crop visitation by managed vs. unmanaged bees
Most of the pollinator visitation to summer vegetable crops in our study region is by wild bee species. This is a striking finding from a farm management perspective, because most of the farmers in our region rent honeybees to pollinate their crops, and few are aware of the pollination provided by wild species.
Our study contributes to the growing literature demonstrating the importance of crop pollination by wild bees (Kremen & Chaplin-Kramer 2007), and is notable for finding that wild, native bees provide more visitation than managed or feral Apis mellifera, being responsible for 62% of the flower visits over the entire study system. Previous studies of canola (Morandin & Winston 2005) and coffee in Indonesia (Klein, Steffan-Dewenter & Tscharntke 2003b, 2003a) found that wild bees (which include wild, native Apis species for coffee) contributed >98% of the flower visits. All other studies have found that wild bees contribute a smaller proportion of visits than we found, when summed over all sites in the system (although particular sites can have higher visitation than the means presented here). Wild bees accounted for 59% of visits to coffee in Costa Rica (Ricketts 2004); 51% of visits to longan in Australia (Blanche, Ludwig & Cunningham 2006); about 37% (Heard & Exley 1994) or 0% (Blanche, Ludwig & Cunningham 2006) of visits to macadamia in Australia; 34% of visits to watermelon in California (Kremen, Williams & Thorp 2002; Kremen et al. 2004); 28% of visits to sunflower (Greenleaf & Kremen 2006b) in California; 2–30% of visits to a variety of crops in Poland (Banaszak 1996); and 3% of visits to grapefruit in Argentina (Chacoff & Aizen 2006). Although flower visitation rate is not equivalent to pollination, which also depends on per-visit pollen deposition, visitation is the most important predictor of actual pollination (Vázquez, Morris & Jordano 2005).
Lastly, the wild bee communities visiting watermelon and tomato crops were distinct (Fig. 3), even when we controlled for farm and for the differential attractiveness of the two crops. This result lends credence to the argument that conservation of diverse communities is necessary in order to retain the full range of ecosystem services (Tilman 1999).
conclusions and management recommendations
In contrast to previous studies of crop pollination by wild bees, in our system neither local- nor landscape-scale land use affected wild bee visit frequency to crop flowers. Organic farming was not associated with wild bee diversity or abundance, but in our system organic and conventional farming are not distinct in terms of field size, crop diversity or the abundance of flowering weeds. Our study therefore supports the hypothesis that these farm-site characteristics are more important than organic farming per se (Benton, Vickery & Wilson 2003). Our entire study system has high habitat heterogeneity compared with some other study systems, where negative effects of human land use on crop visitation by wild bees have been found. This might explain why wild bees are abundant and diverse, even in areas with a low proportion of natural habitat. It may also explain the weak effect of organic farm management (Tscharntke et al. 2005; Rundlöf & Smith 2006).
Currently, there is debate over the most effective way to restore biodiversity in agricultural landscapes (Kleijn et al. 2006). Agri-environment schemes and similar programmes, such as those administered by the US Department of Agriculture, cost nearly 4 billion annually in Europe and North America (Donald & Evans 2006). Our findings suggest that restoration of habitat heterogeneity is important and should remain a goal of such programmes. Our findings also suggest that such programmes should target intensively used, homogeneous landscapes for restoration, given that heterogeneous landscapes already appear to support diverse pollinators. Maintaining such landscape heterogeneity is also important to prevent them from crossing thresholds past which they no longer support this critical ecosystem service.
The bee communities we found visiting crops were dominated by species with long flight seasons, which need floral resources spanning the entire growing season. Such resources may be provided by the habitat heterogeneity in our system. In other, more homogeneous agricultural landscapes, growers may want to actively manage for hedgerows and buffer plantings that flower at times of year, when crops are not in bloom, a practice that is widely believed to increase pollinator populations (Vaughan et al. 2004). This recommendation is supported by our finding that even weeds co-flowering with crops did not appear to draw pollinators away from crops; indeed, for solitary bees we found a significant positive effect of co-flowering weeds on crop visitation.
Lastly, wild bees were responsible for the majority of crop flower visitation to three of the four summer vegetable crops we studied, even though most farmers in our system own or rent domesticated honeybees for pollination purposes. Furthermore, different bee communities were found on different crops, suggesting that maintaining diverse bee communities leads to more complete pollination services. These are striking findings with regard to the ecosystem services delivered by wild species.