Managed honeybees decrease pollination limitation in self-compatible but not in self-incompatible crops

1. Introduction

The agricultural area devoted to pollinator-dependent crops is growing worldwide [1,2], while the stock of managed honeybees (Apis mellifera L.), the main pollinator in most agroecosystems, is growing at a slower rate than its demand [3]. In parallel, wild bees and other non-bee pollinators are declining because of different and pervasive human disturbances [4–7]. This uneven scenario of high pollinator demand and low availability might represent a ‘pollination service bottleneck’, limiting the quantity and/or the quality of the fruits and seeds produced by many crops. However, the extent to which pollinator-dependent crops are pollination-limited at a global scale remains unknown.

Pollination limitation occurs when inadequate pollen transfer, either in quantitative or qualitative terms, limits sexual plant reproduction [8–10]. As a result, fewer seeds and/or fruits are produced than those that can be potentially produced given either available ovules or resources [11]. Inadequate quantity and/or quality of pollen transfer in pollinator-dependent crops can arise because of pollinator shortages and/or the presence of inefficient pollinators [9]. Different types of human disturbances, particularly the replacement of natural habitats by croplands and widespread use of pesticides, have caused declines in the abundance and/or diversity of pollinators at local, regional and global scales [5,7,12–14]. As a consequence, agriculture increasingly depends on managed bees.

The managed honeybee represents the most economically important pollinator for a wide variety of agricultural crops [15–17], being also the most abundant crop pollinator worldwide [18,19]. Honeybees have been historically the main pollinators for many crops due to their highly developed social behaviour, their generalist diet and large populations [20,21]. Farmers around the globe expend large amounts of money every year for their pollination services [22,23]. Surprisingly, and despite its relevance, the impact of managed bees, in general, and of honeybees in particular on alleviating pollination limitation has not been assessed.

The magnitude of pollination limitation is also expected to vary with a plant's compatibility system, which determines whether ovules can be successfully fertilized by self-pollen, outcross pollen or pollen from either source [24,25]. Self-incompatibility is a mechanism that prevents self-fertilization in hermaphroditic flowering plants based on the discrimination of self- versus outcross pollen in the pistil during pollen germination on the stigma or pollen-tube growth in the style or ovary [26]. Animal-pollinated crops exhibiting self-incompatibility (SI crops, hereafter) require the transfer of outcross pollen for successful ovule fertilization and seed formation and thus are expected to be highly dependent on pollinators. Therefore, the cultivation of SI crops commonly requires the planting of at least two varieties within a field and the presence of efficient pollinators for pollen transfer between them [27]. From an agricultural perspective, an efficient pollinator for a SI crop should be one that shows a low constancy to a single variety, limits geitonogamous pollination by visiting few flowers per plant and promotes cross-fertilization by flying relatively long distances between consecutive visits. Instead, crops exhibiting self-compatibility (SC crops, hereafter) do not possess a genetic-based mechanism to prevent selfing, showing variable dependence on pollinators based on their relative capacity to self-pollinate autonomously and achieving successful fertilization after self-pollination. Therefore, SC crops can be cultivated in monovarietal plantations usually without experiencing a significant yield reduction due to the transfer of self-pollen, a feature that also increases management options for efficient pollination [28]. Because of the high pollination demands and limited pollinator alternatives to maximize yield in SI crops together with the challenges of managing different varieties within the same plantation, selection for SC crop varieties in traditionally SI crops has been a priority in crop breeding programmes [29–31].

In this study, we present a global synthesis of the extent to which pollinator-dependent crops experience pollination limitation. Because the area devoted to pollinator-dependent crops is increasing while wild pollinators are declining and managed honeybees are growing but at a slower pace than their demand [2,3], we expected to find widespread pollination limitation in crops. After proving that pollination limitation in crops is the rule rather than the exception, we evaluated whether the use of domesticated honeybees, the most important and ubiquitous managed pollinator, mitigates pollination limitation. Given that the honeybee is a super-generalist pollinator and is being actively managed to pollinate most pollinator-dependent crops [32], we predicted lower levels of pollination limitation in crops with managed honeybees than in those crops without them. Then, we assessed if the magnitude of pollination limitation differed between SI and SC crops. Since SI crops require that pollinators transport outcross pollen for successful ovule fertilization, whereas SC crops can set seeds or fruits after receiving either outcross or self-pollen, we predicted higher levels of pollination limitation in SI than SC crops. Finally, we compared the extent to which managed honeybees may alleviate pollination limitation in SI versus SC crops (i.e. an interaction between presence/absence of managed honeybees and crop compatibility system). Because honeybees tend to favour the transfer of self-pollen by moving short distances between consecutive visits and visiting many flowers within the same plant (e.g. [33,34]), we expected active honeybee management to reduce pollination limitation more strongly in SC than SI crops. To address all these hypotheses, we conducted a meta-analysis using data from published literature covering phylogenetically diverse pollinator-dependent crops from studies distributed worldwide.

2. Material and methods

3. Results

We retrieved data assessing crop pollination limitation from 52 studies conducted around the world (figure 1), encompassing 30 different pollinator-dependent crops, 18 SC and 13 SI (one of the crops studied, Prunus dulcis, has SC and SI varieties), which belong to 19 families (see electronic supplementary material, table S2 and figure S2). Our dataset included many economically important crops like apples, almonds, coffee, oil seed rape, sunflower and blueberries, among others. From these 52 studies, we estimated a total of 107 individual effect sizes. In terms of the magnitude of pollination limitation, we observed an average of 34.2% increase in yield when flowers were supplemented with outcross pollen (95% CI (18.53–51.43%), p < 0.001, figure 2). Model-adjusted mean effect sizes varied between an approximately 20% decrease to an approximately 80% increase in yield after pollen supplementation. Only one of the 107 individual estimates was negative (indicating lower yield after pollen supplementation), and nearly 95% of the 95% CIs associated with the 107 estimated positive effect sizes did not overlap with zero (electronic supplementary material, figure S3).

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Deployment of managed honeybees tends to circumvent pollination limitation. Without managed honeybees, pollen supplementation increased yield by an average of 44.5% (95% CI (24.8–67.19%), p < 0.001, figure 2), whereas crops with active honeybee management showed no evidence of pollination limitation as the 95% CIs around the mean yield increase in pollen-supplemented flowers overlapped with zero (18.4%, 95% CI (–2.26% to 43.47%), p = 0.084, figure 2). Therefore, the use of managed honeybees tended to reduce the extent of pollination limitation (Q_b = 2.75, d.f. = 1, p = 0.09).

Both SI and SC crops showed signs of pollination limitation, although the effect was higher in SI crops. SC crops showed, on average, a 22.2% increase in yield when supplemented with pollen (95% CI (7.89–38.26%), p = 0.001, figure 2), whereas SI crops showed a much higher value, estimated in 49.7% (95% CI (29.56–73.32%), p < 0.001, figure 2). Therefore, yield was significantly more pollination-limited in SI than in SC crops (Q_b = 5.91, d.f. = 1, p = 0.01).

Interestingly, honeybee management decreased pollination limitation significantly in SC but not in SI crops. In fact, SC crops with active honeybee management showed no evidence of pollination limitation as the 95% CIs around the mean yield increase in pollen-supplemented flowers overlapped with zero (8.3%, 95% CI (−11.08% to 31.91%), p = 0.42, figure 3). Instead, pollen supplementation translated into an average increase of 34.1% in yield among SC crops when no bee management was involved (95% CI (13.87–58.2%), p < 0.001, figure 3). On the contrary, SI crops with management of bees showed a 43.7% increase in yield when supplemented with pollen (95% CI (7.14–93.09%), p = 0.01, figure 3), which was similar to the estimated yield average increase of 54.5% observed without bee management (95% CI (30.34–83.30%), p < 0.001, figure 3). We actually detected an overall differential response to pollen supplementation between SC and SI crops depending on the use of managed honeybees (Q_b = 8.12, d.f. = 3, p = 0.04). These results indicate that deployment of honeybees in fields cultivated with SI crops would not be enough to circumvent pollination limitation.

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4. Discussion

The findings of our meta-analysis based on 30 crops represent the first demonstration of a global scenario of pollination limitation among pollinator-dependent crops. Specifically, we found evidence of pollination limitation in about 94% of all estimated effects sizes, with pollen supplementation increasing crop yield by an average of approximately 35%. These results demonstrate that pollination limitation is widespread among pollinator-dependent crops and an important factor curtailing yield. Agreeing with our global results, pollination limitation has also been reported to be regionally widespread among several important crops across the United States [49]. We also found that the deployment of domesticated honeybees in crop fields and the cultivation of SC crops could ameliorate pollination limitation. However, while honeybee management seems to reduce pollination limitation in SC crops, it has a negligible effect in diminishing the large pollination deficits observed among SI crops. Therefore, our findings are indicative that the use of honeybees, the most widespread managed bee for crop pollination [16,19], will not be enough to decrease unrealized yields associated with pollination limitation in many crops, particularly in those that depend on cross-pollination to sustain high yields (e.g. almond, cacao, coffee and apples, among others). Even though the results of our quantitative review are of an associative nature, they agree with hypothetical expectations based on basic biological knowledge of how a pollinator's foraging behaviour can interact with a plant's compatibility system to determine the extent of quantitative and qualitative pollination limitation. Particularly, our results agree with the expectation that the use of a pollinator like the honeybee, which visits many flowers of the same plant in a row during the same foraging bout, cannot reduce pollination limitation to any large extent despite high stigmatic pollen receipt because of the preponderant transfer of self-pollen [10].

The pervasive pollination limitation revealed here implies that current regimens of biotic pollination are inadequate to maximize agricultural yield. This could be interpreted as evidence that pollination demands exceed the global pollination capacity [3]. In fact, it is expected that this pollination gap has been widening during the last decades as a consequence of a worldwide decline in pollinator abundance and diversity [7,16,50–52] driven, among other factors, by agriculture expansion and intensification [2,53]. Therefore, it is relevant to contrast the magnitude of pollination limitation in crops with estimates from wild plants [8,9]. Contrary to our expectations, the magnitude of pollen limitation we estimated here for crops, in terms of increase in reproductive output after pollen supplementation (i.e. approximately 34%), was somewhat lower than those estimated in wild plants (approx. 42% in Ashman et al., [8] and approx. 75% in Knight et al., [9]). Even though agricultural landscapes tend to be more depauperate of wild pollinators than those remaining landscapes dominated by natural and seminatural vegetation [4,54], the lower average magnitude of pollination limitation among crops could be reflecting the use of external pollinator subsidies such as the deployment of honeybee hives as well as the lower pollinator-dependence nature of most crops in comparison with wild plant communities. It has been estimated that only 10% of all crops would suffer a complete reproductive collapse in the absence of pollinators [9,55], which contrasts with the 30% estimated for wild plant species [56]. In any event, our results suggest that pollination is a key factor limiting yield of most animal-pollinated crops under different agricultural settings.

To minimize pollination inefficiencies and maximize yields, farmers pay for the service provided by managed bees, mostly honeybees, representing a key species for agriculture [15,16,18,19,22]. Our review shows that although the use of managed honeybees does not fully circumvent unrealized yields caused by pollination limitation, it significantly decreases its magnitude. In fact, deployment of managed honeybee hives reduced pollination limitation to almost one half (figure 2). On the one hand, this result validates the importance of managed honeybees and their contribution to global agriculture [3,57,58]. But, on the other hand, it suggests that single-species management (i.e. the honeybee) is not sufficient to compensate for the lack of wild pollinators (see also [19]). Diverse pollinator assemblages can increase pollination efficiency and reduce pollination limitation through several mechanisms, including increased spatial and temporal niche complementarity, likelihood to include one or more effective pollinator, and interference competition between pollinators promoting inter-plant movement and outcrossing [59–62]. Additionally, overstocking fields with managed bees may promote honeybee spill over into natural ecosystems, with negative consequences for wild plants and other pollinators [63,64]. Therefore, our findings call for an integrated pollinator management to sustain high yields. This integrated management should consider the use of domesticated pollinators, together with the fostering of diverse wild pollinator assemblages through enhancing habitat heterogeneity and floral and nesting resources at different spatial scales [65].

Our findings also demonstrate that a crop's compatibility system, as a proxy of mating system and outcrossing requirements, is a key trait determining the extent of pollination limitation and thus of realized yield. Specifically, we found that pollination limits the yield of SI crops twice as much as the yield of SC crops (figure 2). This result could be explained by the fact that, in SI crops, pollen needs to be transferred between plants, more commonly between different varieties, for successful pollination [27]. SC crops, on the other hand, do not have strict barriers to self-fertilization, which reduces the pollen transfer distance for effective pollination, for example, within a flower and between flowers within a plant [66]. Also, SC crops exhibit variable dependency levels on animal pollinators based on their differential capacity to self-pollinate autonomously, as it has been shown in new SC varieties of almond trees [30].

Most interestingly, we demonstrated that the deployment of managed honeybee hives in crop fields ameliorates pollination limitation depending on a crop's compatibility system. Specifically, the use of honeybees could circumvent pollination limitation and maximize yield among SC crops but not among SI crops. This latter result could be explained by the foraging behaviour of Apis mellifera. First, in agricultural contexts, honeybees tend to forage on single plant rows [34,67,68], while SI crops are typically sown planting a different variety in each row [20]. This fact also points to the relevance of population genetic aspects of crop pollination management, particularly the inter-compatibility of the different admixed varieties and how these varieties are spatially intermixed [69–72]. Second, honeybees show high floral constancy depending on flower rewards [59,73], morphology [74,75] and colour ([76] and references therein), and crop varieties may differ strongly in these traits (see for example [77]). An extreme example of honeybee constancy related to phenotypic differences can be found in kiwi, where male plants offer pollen as a reward to floral visitors while female plants do not, generating a strong preference for male flowers by honeybees [78]. This example represents only one out of many examples of honeybees foraging behaviour, showing that honeybees rarely move between varieties because of their high constancy, which decreases the transfer of outcross pollen [34,67,68].

Fortunately, research has shown that honeybee constancy can be disrupted when other pollinators are present, increasing their pollination efficiency [34,59]. Consequently, the presence of both wild and managed pollinators in crop fields could be important for increasing cross-pollination because of either their additive or interactive effects. On the other hand, the use of just one all-purpose species of managed pollinator like the honeybee will have a negligible effect in reducing pollination deficits, particularly in SI crops. Moreover, reliance on a single pollinator species for crop pollination will increase enormously the risk of sudden yield collapses [79].

5. Concluding remarks

Modern agriculture is becoming increasingly pollinator-dependent, and animal-pollinated crops account for the majority of the expansion in agricultural area [1,2]. However, the increasing demand of pollination services has not been attended with proper agricultural management practices that promote diversity in terms of pollen sources (i.e. varieties/cultivars) and pollinators. On the plant side, even though the effects of enhancing genetic diversity within plantations had been relatively unexplored, Kron & Husband [80] showed that increasing the diversity of pollen donors could decrease pollination limitation by enhancing the number of ovules fertilized with high-quality pollen (see also [10]). More specifically, well intermixed multi-varietal plantations, particularly of SI crops, may diminish pollination limitation by decreasing the chance of morphological and phenological flowering mismatches, thus increasing the effective availability of alternative sources of compatible pollen. On the pollinator side, here we show that single-species management (i.e. honeybees) does not completely solve yield losses associated with pollination limitation for many crops. This limitation could be circumvented by the application of well-developed protocols to diversify pollinator options (see [65]), such as the enhancement of wild pollinator assemblages through restauration of natural and seminatural habitats. Overall, our study suggests that crop pollination management for increasing yield should consider the joint diversification of both the plant and pollinator sides as positive synergistic effects could derive from such an integrative approach.

Data accessibility

Data are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.rfj6q57ct [81].

Authors' contributions

A.S.: conceptualization, data curation, formal analysis, writing—original draft; R.A.: data curation, formal analysis, writing—review and editing; L.A.: data curation, writing—review and editing; G.G.: formal analysis, writing—review and editing; C.L.M.: conceptualization, data curation, writing—review and editing; A.T.: writing—review and editing; M.A.A.: conceptualization, writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Competing interests

We declare we have no competing interests.

Funding

This work was supported by the National Scientific and Technical Research Council (CONICET) – Argentina; CONICET (PIP 2015-0371); FONCyT (PICT 2016-0764; PICT 2019-1897) and SURPASS2 ‘Safeguarding pollination services in a changing world’, project funded under the Newton Fund Latin America Biodiversity Programme: Biodiversity–Ecosystem Services for Sustainable Development, grants awarded by the NERC, Great Britain [NE/S011870/1] and CONICET, Argentina [RD 1984/19].