Pollinator exclusion by bagging female flowers caused plants to abort the fruit. By contrast, all hand-pollinated female flowers matured to seed-bearing fruits (419±17 s.e. seeds per fruit, n=9). We found on average 2.72±0.33 pumpkin flowers in the surroundings of each pumpkin plot (n=14). In total, 633 bee individuals from 25 species and nine genera were caught, belonging to the subfamilies Anthophorinae, Apinae, Halictinae, Megachilinae and Xylocopinae.
The pumpkin pollinator community was strongly determined by the habitat and environmental variables. Bee species richness increased significantly with the weather PCA axis (increasing temperature and light intensity, decreasing humidity; likelihood ratio=7.06, p=0.008), and the resources PCA axis (increasing density and diversity of floral resources; likelihood ratio=8.31, p=0.004). Although both of these variables differed across habitat types, habitat type itself did not significantly add any explanatory power (likelihood ratio=3.01, p=0.557), and was thus removed from the minimal model. Conversely, the only significant predictor in the minimal model for bee abundance was habitat type (likelihood ratio=11.26, p=0.024); abundance was significantly higher in open area habitats (21.33±4.06 individuals, n=3) compared with all other habitat types (natural forest: 3.56±2.87, n=3; low intensity: 6.23±3.86, medium intensity: 6.08±3.80, high intensity: 10.58±3.80 individuals per flower and sampling (pollination rate), n=4).
Bee species richness was the only significant predictor variable in the model for seed set per fruit (r2=0.452, F1,13=19.24, p=0.022; ) whereas bee abundance did not significantly correlate with seed set (r2<0.01, F1,13=0.13, p=0.74). Mean number of seeds per fruit from plots with high species richness (10 bee species) reached almost that of hand-pollinated control flowers (), whereas low richness (four species) led to just 50% of the seed set found in control flowers. Number of seeds per fruit was correlated with fruit size (Spearman: R2=0.635, p=0.015), which is the economically most important trait for measuring this ecosystem service. However, we found no correlation between fruit size and the bee community (abundance: r2<0.001, F1,3=0.043, p=0.85; species richness: r2=0.05, F1,3=8.29, p=0.064) in contrast to seed set as the response variable. Habitat type, surrounding pumpkin flowers, humus thickness, slope and canopy cover did not influence seed set significantly ().
Figure 1 Mean number of seeds per fruit per pumpkin patch in relation to the number of bee species per pumpkin patch. Results for open-pollinated flowers are shown with filled circles and solid line and that for hand-pollinated bagged control flowers in nine plots (more ...)
Seed set in relation to predictor variables tested with GLM. (Italic numbers indicate significant effects.)
Species differed in their spatial resource use (height of flowers: r2
<0.001), with Nomia concinna
preferring the lowest, and Xylocopa nobilis
preferring the highest flowers (, ). Pollinating height in one high-intensity plot was significantly lower (0.26±0.04) compared with two open area plots (0.59±0.03, 0.59±0.05; r2
=0.0001), independent of habitat type (r2
=0.177). Temporal species turnover showed even stronger differences, as almost all species differed significantly from each other in their preferred time of visitation (r2
<0.001). The species that visited flowers the earliest were Apis cerana
, X. dejeani
and X. confusa
, whereas X. nobilis
and Ceratina cognata
appeared significantly later (, ). Flower visitation in one low-intensity cacao plot was on average earlier (08.16±10) when compared with one medium-intensity (09.19±11), high-intensity (09.14±6) and open area plot (09.05±5; r2
<0.001) and habitat had no influence (r2
=0.49). Species identity explained minor variance of the overall model for preferred flower size (r2
=0.0047), and as only A. cerana
=18) differed from C. cognata
=17) and Lasioglossum
=137) in preferred flower size, we did not include flower size for classification into functional guilds.
Figure 2 Height and time of flowers preferred by each bee species. Arithmetic means±s.e. are given. For mean values, standard error and significance levels, see . Numbers represent species identity: 1, N. concinna; 2, Lasioglossum sp.; 3, A. cerana (more ...)
Body size was closely related to pollinating behaviour and each size class showed consistent patterns. Duration of a single flower visitation was significantly longer for small bees compared with very small and very large bees (r2
<0.001; ). Body size classes also differed in the number of flowers they visited. Very large bees checked two or three flowers mostly in their preferred height range, whereas small bees fed for a very long time but only on one flower. The amount of pollen transferred per flower visit was a consequence of species-specific anatomical characteristics, because larger bees had larger pollen-transporting surfaces such as the plumose ventral section of the abdomen and the dorsal part of the thorax or femur (). Within-flower movements are generally responsible for pollen distribution on the stigma (Chagnon et al. 1993
). Owing to their size, large and very large bees entered the flower directly and remained between the petal and anther or pistil, while rubbing the pollen-carrying ventral part of the abdomen on the pistil of a female flower, or picking up pollen in male flowers. High pollen transfer was restricted to a part of the pistil, as large bees could not move around the pistil as did small and very small bees (). Small and very small bees landed on the petal, anther or pistil and then walked for a long time on anthers or pistil while feeding on pollen or nectar and thus distributing pollen. Very large bee species such as X. dejeani
and X. confusa
appeared very early in the morning, transferring large amounts of pollen, whereas Lasioglossum
sp., C. cognata
sp. appeared significantly later, mainly providing the distribution of the pollen that was already transferred by other species (e.g. Xylocopa
) on the stigma owing to their activity within the flower.
There was no clear pattern relating body size to pollinating height, even though very small species pollinated significantly lower flowers (r2
=209) than small (0.672
=178), large (0.523±0.048, n
=62) or very large species (0.544±0.04, n
=91). By contrast, small bees pollinated significantly higher flowers compared with medium-sized bees (0.368±0.042, n
=64). We found that medium-sized (08.25±6
=64), large (08.40±7
=60) and very large (08.37±6
=90) bees occurred significantly earlier compared with small (09.02±3
=178) and very small bees (09.11±3
According to the differences between the bee species in the three functional traits of pollination, we could identify eight functional pumpkin pollinator groups ().
In a model where bee species richness was included first, after abundance was factored out, only bee species richness was significantly positively correlated with seed per fruit. However, when functional guild diversity was included ahead of richness in a type I (sequential) sum of squares (SS) model, species richness became non-significant. In a type I SS model, variance that is shared by two predictors is attributed to the first predictor to enter the model (Schmid et al. 2002
). This demonstrates that richness and functional guild diversity are strongly correlated, making it impossible to attribute the shared variance to either predictor. However, functional guild diversity explained much more of the variance in seed set (r2
=0.45) when it was first in the model, compared with richness (r2
=0.32; , ), making functional diversity a stronger predictor of seed set.
Bee species richness and functional guild diversity in relation to the residuals of seed set after correlation with bee abundance. (Italic numbers indicate significant effects.)
Number of guilds per plot (based on differences in ) in relation to the number of pumpkin seeds. Seed set increases with increasing number of functional groups.