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- Materials and methods
1. The honeybee Apis mellifera is currently in decline worldwide because of the combined impacts of Colony Collapse Disorder and the Varroa destructor mite. In order to gain a balanced perspective of the importance of both wild and managed pollination services, it is essential to compare these services directly, a priori, within a cropping landscape. This process will determine the capacity of other flower visitors to act as honeybee replacements.
2. In a highly modified New Zealand agricultural landscape, we compared the pollination services provided by managed honeybees to unmanaged pollinator taxa (including flies) within a Brassica rapa var. chinensis mass flowering crop.
3. We evaluate overall pollinator effectiveness by separating the pollination service into two components: efficiency (i.e. per visit pollen deposition) and visit rate (i.e. pollinator abundance per available flower and the number of flower visits per minute).
4. We observed 31 species attending flowers of B. rapa. In addition to A. mellifera, seven insect species visited flowers frequently. These were three other bees (Lasioglossum sordidum, Bombus terrestris and Leioproctus sp.) and four flies (Dilophus nigrostigma, Melanostoma fasciatum, Melangyna novae-zelandiae and Eristalis tenax).
5. Two bee species, Bombus terrestris and Leioproctus sp. and one fly, Eristalis tenax were as efficient as the honeybee and as effective (in terms of rate of flower visitation). A higher honeybee abundance, however, resulted in it being the more effective pollinator overall.
6. Synthesis and applications. Alternative land management practices that increase the population sizes of unmanaged pollinator taxa to levels resulting in visitation frequencies as high as A. mellifera, have the potential to replace services provided by the honeybee. This will require a thorough investigation of each taxon’s intrinsic biology and a change in land management practices to ensure year round refuge, feeding, nesting and other resource requirements of pollinator taxa are met.
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- Materials and methods
The value of managed vs. wild pollinator services has recently been the focus of much attention (e.g. Allsopp, de Lange & Veldtman 2008), particularly with reference to global food crops and their pollination requirements (Klein et al. 2007; Aizen et al. 2008; Winfree 2008). Honeybee Apis mellifera Linnaeus, 1758 colony viability is now a serious concern because many agricultural crops are reliant on this single pollinator species and consequently, the contribution of this species to food production is high (Morse & Calderone 2000; Klein et al. 2007). This has sparked renewed interest in the function of unmanaged or wild pollinator taxa, particularly because of their provision of ‘pollination insurance’ (Winfree et al. 2007a).
Unmanaged pollinator taxa have proved to be superior pollinators when compared with honeybees in some crop species. For example, in a study of watermelon pollination in North America, native bees were responsible for a significantly greater number (62%) of flower visits than honeybees and pollen deposition at flowers was strongly correlated with native bee visitation, but not with honeybee visitation (Winfree et al. 2007a). Similarly, an increased abundance and diversity of native bees significantly improved fruit set in coffee plantations (Klein, Steffan-Dewenter & Tscharntke 2003) and seed set in canola (Morandin & Winston 2005). These ‘free’ wild pollinator services, however, are ostensibly at risk from land use modification and pesticide use (Watanabe 1994; Stokstad 2006). The perceived value of these services to global food production, however, has been questioned (Watanabe 1994; Allen-Wardell et al. 1998; Ghazoul 2005a; Steffan-Dewenter, Potts & Packer 2005; Stokstad 2007; Aizen et al. 2008; Allsopp et al. 2008) leading to, in some respects, the understatement of their potential services to global crop production (Ghazoul 2005a; Allsopp et al. 2008).
This premise has developed from two critical concerns: the first is that a majority of global food production does not in fact depend on animal pollination and hence the attention directed toward declining wild pollinators is currently not warranted (Ghazoul 2005a). The assumption that pollinator declines have yet to be translated into decreased food production is supported by a study by Aizen et al. (2008) which compared rates of yield increase between pollinator-dependent and pollinator-independent crops over the last 45 years. The second concern arises from the fact that studies that have assessed the value of wild pollinators, often fail to compare the managed and the unmanaged components to arrive at a balanced view of the net worth of their services (Allsopp et al. 2008). There is a need for empirical studies directly comparing managed and unmanaged pollinator services (Ghazoul 2005a,b; Steffan-Dewenter et al. 2005) in order to demonstrate unequivocally the relative significance of their services in pollinating global food crops (Allsopp et al. 2008).
Two components of pollination need to be assessed in order to directly compare the overall effectiveness of managed and unmanaged pollinator services, pollen transfer efficiency and visitation frequency. Pollen transfer efficiency describes the proficiency with which individual pollinators remove and transport pollen to conspecific stigmas (Primack & Silander 1975; Herrera 1987; Harder & Wilson 1998). Visitation frequency is a function of both the abundance of the pollinator and the number of flowers it visits in a given time interval (Herrera 1987, 1989; Vazquez, Morris & Jordano 2005; Madjidian, Morales & Smith 2008). The most effective insect pollinator would therefore be one that is present in high numbers and moves rapidly from flower to flower (i.e. has a high visitation rate). It would also frequently contact the stigma, transferring many pollen grains (i.e. has high pollen transfer efficiency). Conversely, the least effective insect pollinator would have low abundance and move relatively slowly from flower to flower (i.e. have a low visitation rate). It would rarely contact the stigma while visiting a flower and transfer few pollen grains when it did (i.e. have low pollen transfer efficiency).
The lack of studies comparing managed and unmanaged services in situ, in intensive agricultural systems, is surprising as there is a clear link between diverse pollinator guilds and improved pollen loads, high fruit and seed set and increased offspring vigour (Schemske & Pautler 1984; Herrera 1987; Klein et al. 2003; Gomez et al. 2007). Intensive agricultural systems that support diverse unmanaged pollinator assemblages co-existing with managed honeybee hives prior to honeybee decline, are ideal systems to identify potential alternative taxa that might be used if honeybees decline.
We use a highly modified landscape in the Canterbury region of New Zealand, to ask the following questions: (1) Does pollen transfer efficiency (as measured by stigmatic pollen loads and the proportion of visits in which the stigma is contacted) differ between the honeybee and other flower-visiting taxa? (2) Does the rate of flower visitation (measured as both visitor abundance per number of available open flowers, and the number of flower visits per minute) differ between the honeybee and other taxa? (3) How do these differences translate into overall pollinator effectiveness? (4) Are any of the alternative pollinator taxa directly, or as a group, capable of replacing honeybee services in a mass flowering crop?
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- Materials and methods
In total, we observed 31 species attending flowers of B. rapa (Table 1). In addition to A. mellifera, seven insect species visited flowers often enough to be included in analyses. These were three other bees: Lasioglossum sordidum (Smith, 1853), Bombus terrestris (Linnaeus, 1758) and Leioproctus sp.; and four flies: Dilophus nigrostigma (Walker, 1848), Melanostoma fasciatum (Macquart, 1850), Melangyna novae-zelandiae (Macquart, 1855) and Eristalis tenax Linnaeus, 1758 (Table 1).
Table 1. Taxa recorded visiting flowers in Brassica rapa fields in the Canterbury region, New Zealand
|Hymenoptera||Apidae||Apis mellifera Linnaeus, 1758 Bombus terrestris (Linnaeus, 1758)|
|Halictidae||Lasioglossum sordidum (Smith, 1853)|
|Diptera||Anthomyiidae||Delia platura (Meigen, 1826)|
|Anthomyia punctipennis (Weideman, 1830)|
|Bibionidae||Dilophus nigrostigma (Walker, 1848)|
|Calliphoridae||Calliphora hortona (Walker, 1849)|
|Calliphora quadrimaculata (Swedarius, 1787)|
|Calliphora stygia (Fabricius, 1794)|
|Calliphora vicina Robineau-Desvoidy, 1830|
|Lucilia sericata (Meigen, 1826)|
|Pollenia pseudorudis (Rognes, 1985)|
|Ephydridae||Unidentified species 1|
|Muscidae||Spilogona melas Schiner, 1868|
|Hydrotaea rostrata Robineau-Desvoidy, 1830|
|Syrphidae||Eristalis tenax Linnaeus, 1758|
|Melanostoma fasciatum (Macquart, 1850)|
|Melangyna novae-zelandiae (Macquart, 1855)|
|Helophilus hochstetteri Nowicki, 1875|
|Sarcophagidae||Oxysarcodexia varia (Walker, 1836)|
|Tachinidae||Pales usitata (Hutton, 1901)|
|Pales marginata (Hutton, 1901)|
|Coleoptera||Coccinelidae||Coccinella undecimpunctata (Linnaeus, 1758)|
|Hemiptera||Pentatomidae||Glaucias amyoi (Dallas)|
|Lepidoptera||Pieridae||Pieris rapae (Linneaus, 1758)|
Pollen transfer efficiency
In 63% of control (i.e. unvisited) flowers, there were no pollen grains on stigmas. In the remaining control stigmas, there were <2 pollen grains (mean = 1·96 ± 0·01). We thus have no reason to expect that pollen movement occurred without insect pollinators. There was no significant difference between emasculated flower stigmatic loads and intact flower pollen loads (t = −1·14, P = 0·27). This suggests pollen transfer estimated in stigmatic pollen load calculations was not likely to be self-pollen. In the absence of detailed data regarding pollinator behaviour, however, (i.e., extent of grooming, amount of self pollen carried on insect body (Harder 1990; Harder & Wilson 1998; Aizen & Harder 2007) we cannot verify with certainty that self-pollen was excluded from pollen transfer estimates in stigmatic pollen load calculations.
There were significant differences in the mean pollen load (log transformed) deposited onto stigmatic surfaces between species (F9,132 = 7·646, P < 0·0001, Fig. 1, Table 2). In comparisons between taxa representing the unmanaged component of pollinating fauna, A. mellifera transferred significantly greater amounts of pollen per stigmatic contact than four of the native species; Dilophus nigrostigma, Melanostoma fasciatum, Melangyna novae-zelandiae and Lasioglossum sordidum (Table 2, Fig. 1). Three species from the unmanaged assemblage were not different in this respect to A. mellifera; B. terrestris and Leioproctus sp. and the fly E. tenax, Fig. 1, Table 2).
Figure 1. Boxplot of stigma pollen loads per flower visit for each species. Box indicates quartiles with median marked as a horizontal line; points are outliers.
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The proportion of times that individuals contacted stigmatic surfaces when visiting flowers, differed between species (d.f. = 7, Wald = 434·405, P < 0·0001, Fig. 2). The honeybee and three unmanaged taxa (B. terrestris, Leioproctus sp. and E. tenax) contacted stigmatic surfaces on significantly more occasions than non-contact occasions. Stigma contact was low in the remaining taxa (Table 2, Fig. 2).
Figure 2. Boxplots of the proportion of stigma contact occasions per visit for 10 individual flower visits for each of n individuals. Box indicates quartiles with median marked as a horizontal line; points are outliers.
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Taxon level visitation frequency (visitor abundance per number of available flowers) varied significantly (F7,134 = 15·587, P < 0·0001, Fig. 3a). Honeybees visited flowers at a significantly higher rate than all other taxa (LSD tests: P < 0·0001). When taxa were grouped, honeybee visitation frequencies were still significantly higher than both fly and bee groups (F2,69 = 29·835, P < 0·0001).
Figure 3. Boxplots of visitation rates: (a) individual visitor frequencies (visits per flower) per 10 min period; (b) number of flowers visited per minute. Box indicates quartiles with median marked as a horizontal line.
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Visitation rate (no flower visits per min) also varied between taxa (F1,416 = 2·013, P = 0·052, Fig. 3b) but significance was marginal at P = 0·052. Post hoc analysis suggests that this effect is due to B. terrestris visiting significantly more flowers per minute than the honeybee (LSD test: P = 0·047) while other taxa did not differ from the honeybee in this respect (LSD test: P > 0·05; Table 3).
Table 3. Effectiveness of the eight most frequent flower visitors to 11 B. rapa fields in the Canterbury region, New Zealand
|Species||Visit frequency: visits flower−1 10 min−1 (mean ± SE)||Post-hoc comparisons with A. mellifera LSD test (P)||Visit rate: floral visits per minute (mean ± SE)||Post-hoc comparisons with A. mellifera LSD test (P)|
|Apis mellifera||2·35 × 10−2 ± 0·0001|| ||33·83 ± 3·07|| |
|Bombus terrestris||1·28 × 10−3 ± 0·00006||<0·001||69·12 ± 20·03||0·047|
|Leioproctus sp.||4·83 × 10−4 ± 0·00007||<0·001||64·31 ± 20·16||0·148|
|Lasioglossum sordidum||3·74 × 10−4 ± 0·00003||<0·001||10·03 ± 2·71||0·452|
|Eristalis tenax||3·39 × 10−3 ± 0·0003||<0·001||19·42 ± 1·71||0·457|
|Melangyna novae-zelandiae||2·92 × 10−3 ± 0·0003||<0·001||7·99 ± 1·07||0·286|
|Melanostoma fasciatum||1·87 × 10−3 ± 0·0006||<0·001||6·38 ± 1·39||0·295|
|Dilophus nigrostigma||4·08 × 10−3 ± 0·0003||<0·001||6·10 ± 1·67||0·394|
|All flies combined||8·20 × 10−3 ± 0·004||<0·001|| || |
|All bees combined (except Apis mellifera)||9·25 × 10−4 ± 0·004||<0·001|| || |
When both efficiency and visitation frequency were combined to produce an estimate of effectiveness (median stigma pollen load per visit × proportion of successful stigma contact × hourly rate of visitation), honeybees were the most effective single pollinator species. We estimated that honeybees accounted for the deposition of 7879 pollen grains per hour which is more than three times greater than the next highest pollinator taxa, (B. terrestris: 2247 pollen grains transferred per hour). The overall effectiveness of the remaining taxa was as follows in pollen grains transferred per hour: D. nigrostigma, 22; E. tenax, 968; L. sordidum, 2; Leioproctus sp., 300; M. fasciatum, 1; M. novae-zelandiae, 13.
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This study revealed a diverse unmanaged component of the pollinator assemblage in B. rapa crops. We found that in terms of pollen transfer efficiency, the unmanaged component of the pollinator assemblage includes taxa that are capable of providing pollination services equal to those currently performed by honeybees. First, we found that mean pollen loads deposited on stigmas of virgin flowers by two bee species, B. terrestris and Leioproctus sp. and one fly species, E. tenax, were not significantly different to that deposited by the honeybee (Table 2, Fig. 1). Secondly, these three species were as likely to touch stigmatic surfaces when attending flowers as A. mellifera (Table 2, Fig. 2).
Rate of visitation is an important component affecting pollination success and determining the overall contribution of individual taxa to total pollination services (Vazquez et al. 2005). In this study, we consider both visitation frequency (abundance per number of available flowers) and visitation rate (number of flower visits per min) separately for the purpose of demonstrating the potential of alternative pollinator taxa. Although honeybees visited flowers at significantly higher frequencies than any of the other visitors, they did not differ significantly in the number of flowers visited per minute when compared with all other taxa. We suggest that in the above measures of pollen transfer efficiency and floral visits per min, several alternative taxa are equal to the honeybee but are not common enough to make them more effective overall.
A higher abundance of honeybees ultimately resulted in overall greater effectiveness of honeybees as a single taxon. This result is similar to a study by Madjidian et al. (2008) in Argentina comparing a native and exotic bumblebee species. The higher visitation frequency of the exotic bumblebee Bombus ruderatus resulted in it being a more effective pollinator than the native bumblebee B. dahlbomii, even though the native bumblebee was more efficient.
The higher abundance of honeybees per number of available flowers relative to unmanaged taxa probably reflects managed and unmanaged status. By definition, honeybee populations are managed to maintain high population sizes, whereas unmanaged taxa are not. This does not necessarily preclude currently unmanaged taxa from performing the same services. It is possible that even though the effectiveness of unmanaged taxa was lower, it may still result in maximum seed set. In the absence of seed set data, we cannot test this assumption.
If lower effectiveness results in lower seed set, unmanaged pollinators would need to be managed in order to increase population sizes in accordance with those of the honeybee, beyond that which exists naturally at this time in this system.
Managing a range of naturally existing pollinators in-situ is likely to be challenging for several reasons; First, we have become accustomed to ‘mobile’ as opposed to ‘in-situ’ pollination services. Honeybees are efficient, versatile and easily managed within transportable hives (Morse & Calderone 2000; Klein et al. 2007; Winfree 2008). In contrast, unmanaged pollinators are not as transportable and hence not as versatile (at present). Nonetheless, the effectiveness of flies (Syrphidae in particular) as crop pollinators is becoming increasingly evident (e.g. Feldman 2006; Pontin et al. 2006). For example, pollination by E. tenax was shown to improve the shape and weight of sweet peppers in Canada (Jarlan, De Oliveira & Gingras 1997) while Episyrphus balteatus (also Syrphidae) significantly increased seed set and yield of an oilseed rape crop in cage experiments when compared with control cages (Jauker & Wolters 2008).
Secondly, managing alternative pollinator taxa in situ to achieve high densities is challenging as it requires a thorough investigation of each taxon’s intrinsic biology (Cane et al. 2006). For instance, in this study system (and across most of New Zealand) the indigenous pollinating fauna lacks large social bees and is dominated by solitary bees and flies (Lloyd 1985; Donovan 2007). Solitary bees in particular have a short, fixed flying season, which is synchronized with the flowering time of certain host plants (Minckley et al. 1994; Westerkamp & Gottsberger 2000). This means that timing may not always be compatible with the flowering crop in need of pollination. In contrast, eusocial bees are capable of recruiting foragers quickly to high quality resources (Brosi et al. 2007; Winfree 2008).
Fundamental research into the intrinsic biology and life history traits of both solitary bees and flies is currently lacking in this, and most other systems (Klein et al. 2007). In order to understand which resources are needed for these taxa to maintain stable populations in agricultural landscapes we need to first understand their role and function in their current system.
In conclusion, the results of this study demonstrate that three species that currently exist as part of the unmanaged pollinator assemblage of B. rapa in the South Island of New Zealand are equally as efficient as the honeybee in providing pollination services. Effectiveness was higher in honeybees but this probably reflects the higher population sizes of a managed species giving rise to higher rates of visitation in honeybees. Our results suggest that there is potential for other species to fulfil the pollination role of honeybees under management strategies that increase local population sizes and thus visitation rates.