An energetics-based honeybee nectar-foraging model used to assess the potential for landscape-level pesticide exposure dilution

Abstract

Estimating the exposure of honeybees to pesticides on a landscape scale requires models of their spatial foraging behaviour. For this purpose, we developed a mechanistic, energetics-based model for a single day of nectar foraging in complex landscape mosaics. Net energetic efficiency determined resource patch choice. In one version of the model a single optimal patch was selected each hour. In another version, recruitment of foragers was simulated and several patches could be exploited simultaneously. Resource availability changed during the day due to depletion and/or intrinsic properties of the resource (anthesis). The model accounted for the impact of patch distance and size, resource depletion and replenishment, competition with other nectar foragers, and seasonal and diurnal patterns in availability of nectar-providing crops and wild flowers. From the model we derived simple rules for resource patch selection, e.g., for landscapes with mass-flowering crops only, net energetic efficiency would be proportional to the ratio of the energetic content of the nectar divided by distance to the hive. We also determined maximum distances at which resources like oilseed rape and clover were still energetically attractive. We used the model to assess the potential for pesticide exposure dilution in landscapes of different composition and complexity. Dilution means a lower concentration in nectar arriving at the hive compared to the concentration in nectar at a treated field and can result from foraging effort being diverted away from treated fields. Applying the model for all possible hive locations over a large area, distributions of dilution factors were obtained that were characterised by their 90-percentile value. For an area for which detailed spatial data on crops and off-field semi-natural habitats were available, we tested three landscape management scenarios that were expected to lead to exposure dilution: providing alternative resources than the target crop (oilseed rape) in the form of (i) other untreated crop fields, (ii) flower strips of different widths at field edges (off-crop in-field resources), and (iii) resources on off-field (semi-natural) habitats. For both model versions, significant dilution occurred only when alternative resource patches were equal or more attractive than oilseed rape, nearby and numerous and only in case of flower strips and off-field habitats. On an area-base, flower strips were more than one order of magnitude more effective than off-field habitats, the main reason being that flower strips had an optimal location. The two model versions differed in the predicted number of resource patches exploited over the day, but mainly in landscapes with numerous small resource patches. In landscapes consisting of few large resource patches (crop fields) both versions predicted the use of a small number of patches.

Keywords: Depletion; Energetic efficiency; Flower strips; Foraging; Honeybee; Landscape ecology; Nectar content; Pesticide exposure; Resource selection; Semi-natural habitats.

Figure 1. Map of the case-study area.

Oilseed rape fields (ochre), alternative crop fields (lilac) and off-field resource patches (green) as used in the scenario simulations.

Figure 2. Choice of resources depends on net energetic efficiency.

The choice between resources at equal distance depends on their value for EI/EE (Eq. (22b)). This ratio increases asymptotically with nectar acquisition rate gaF to the limit value 1/c × e_R∕e_F. With larger e_R, e.g., for clover compared to OSR, EI/EE will level off at a higher value. When flower density is much higher, the resulting value of EI/EE may still be larger for the resource with the lower e_R. Curves refer to resources at 200 m and 1 km. Values for clover and OSR as specified in Table 2 and used in the scenarios are indicated.

Figure 3. Attractive flower strips and off-field habitats may dilute exposure.

Flower strips can lead to high exposure reduction, when present in large numbers (A). For the RL-model, the width of the strips has no impact on this dilution; for 2, 5 and 10 m wide strips, the graphs are very similar (not shown). Off-field habitats can have similar impact (B, C) as flower strips. When quality is low (D) few off-field habitat patches are selected resulting in little dilution. Note that flowers strips are identical to medium quality off-field habitat patches. All graphs refer to RL-model.

Figure 4. The number of daily exploited patches depends on the foraging patch selection model.

With the SO-model an increase in the number of exploited patches indicates that depletion of the optimal patch plays a role. This may occur for narrow flower strips (A) and for off-field habitats that are mostly small-sized (C), and is determined by patch size not by its ‘quality’. For the RL-model the number of exploited patches is linearly related to their abundance. Depletion is unlikely and patch size has no impact on patch selection (B). Instead patch ‘quality’ is important (D) as patches need to have a sufficiently high NEE to be considered and promoted for in the recruitment process.

Figure 5. On an area-base flower strips are more effective than off-field patches.

To obtain the same degree of dilution, much more area is required of managed off-field habitat patches (B), compared to flower strips (A) with identical properties. This is related to landscape characteristics and a consequence of off-field patches being in general further away from target crop field and hive location.