Introduction

Pollination is considered an essential and valuable ecosystem service for the production of an important variety of crops (Voeks and Rahmatian 2004; Macháč et al. 2021). The production and quality of fruits, for example, and therefore their commercial value and potential, depends on successful pollination (Klatt et al. 2013). Colonies of pollinating insects have been decreasing drastically during the last three decades (Potts et al. 2010; Ollerton et al. 2011). This trend is of concern not only to farmers, but also to governments. However, the exact causes of this decline are unclear and are still debated in academic circles. In some cases, pesticides appear to negatively affect the health of organisms that spend more time foraging in the fields, such as bumblebees, and this may, in turn, lead to low survival of entire colonies (Henry et al. 2012; Campbell et al. 2019). Landscape changes, due to intensive crops, human land management, or climate change, can be equally or even more harmful for pollinators than pesticides (Holzschuh et al. 2008; CaraDonna et al. 2018).

The absence of pollinators in the fields is beginning to cause additional costs to productors (Allsopp et al. 2008). However, the introduction of practices that favor the increase in pollinators has been shown to significantly increase productivity (MacInnis and Forrest 2019; Rollin and Garibaldi 2019).

Due to the relatively large size of fields in intensive farming, and their increased control by humans, pollinating insects often do not cover the entire production, creating an unmet need for farmers, who must devote additional monetary resources in order to harvest products that meet market expectations in terms of fruit size or seed number (Popak et al. 2019). In addition, organic food production cannot be ensured by focusing conservation efforts on only a few domesticated pollinator species, as it is well known that there are specific wild insect species needed to pollinate some plant species (Ollerton et al. 2011; Klatt et al. 2013). Through careful strategic landscape design growers could increase crop yields (Bravo-Monroy et al. 2015) and the presence of natural predators of pest insects (Karamaouna et al. 2019) which in turn could lead to reduced costs and therefore increased income. This systematic literature review aims to answer the following question: Have any successful practices been identified so far to attract pollinators to crops and increase their diversity, abundance, and quality?.

This work was carried out in Medellín Antioquia, Colombia, during 2021.

Methodology

This research follows the structure of a regular literary review but with changes in the way data is gathered, preserved, and analyzed. For a better understanding of the process, the methodology will be presented in phases:

Phase one

Defining keywords for TITLE-ABS-KEY equations search in Scopus, resulting in three different search equations limited by publication year after 2010. From the raw selection a prefilter was perform based on abstracts. The keywords used in each equation were:

  • “Promote” AND “pollinators” AND “regime”: resulting in 497 papers and 80 after filtering, from which 17 papers were selected.

  • “Promote” AND “pollinators” AND “regime “AND (LIMIT-TO (PUBYEAR, 2020) OR LIMIT-TO (PUBYEAR, 2019))

  • “Organic” AND “landscape” AND “benefit” AND “pollinators”: resulting in 86 papers and 28 after filtering, from which 10 papers were selected.

  • “Organic” AND “landscape” AND “benefit” AND “pollinators” AND (LIMIT-TO (PUBYEAR, 2020) AND (LIMIT-TO (DOCTYPE, “ar")) AND (LIMIT-TO (SUBJAREA, "AGRI") OR LIMIT-TO (SUBJAREA, "ENVI"))

  • “Pollinators” AND “landscape” AND “foraging”: resulting in 76 papers and 30 after filtering, from which 8 papers were selected.

  • “Pollinators” AND “landscape” AND “foraging” AND (LIMIT-TO (PUBYEAR, 2020)) AND (LIMIT-TO (SUBJAREA, "AGRI") OR LIMIT-TO (SUBJAREA, "ENVI"))

Additionally, from the review of the automatically detected papers, other 18 were selected from their references.

Phase two

The contents of the selected papers, their abstract, results, and conclusions were analyzed and consigned in a database along with their publication year, authors’ name, ISSN, Journal, Publisher, country, SCImago Journal Rank and SCImago Quartiles. The database purpose was to assemble and organize the information input for the software that would pick up the trends of keyword mentions through the entire document scope.

Phase three

The database was loaded into Vantage Point® 10.0 and its output was analyzed quantitatively and qualitatively.

Phase four

Vantage Point® displayed 32 keywords that were mentioned recurrently throughout the databases. From those, the ones that had direct relations with practices that could be implemented on fields were selected, and they were used as the basis for the analysis on graphs and tables.

The phases of the investigation, and some of their highlights are summarized in Fig. 1.

Fig. 1
figure 1

Source: self-elaboration

depicts all the stages of the research.

Full size image

Results and discussion

From the data that Vantage Point® yielded, as can be seen in Fig. 2, five countries: USA, Germany, the United Kingdom, Sweden, and South Africa, have produced 53% of the papers on this topic from 2010. Argentina and Mexico are the only Latin American countries that contribute to the publication of papers, one each.

Fig. 2
figure 2

Source: self-elaboration

Percentage of papers published by country. *Based on the institutional affiliation of the first author of the paper.

Full size image

The most mentioned keywords throughout the whole revision were “pollinators”, “landscape” and “crops”. However, since the objective of the review was to find the most common variables that affect the presence of pollinators, the first terms that would apply to management practices within crops had to be searched for. The most mentioned practices with positive outcomes were organic management, natural habitats, flower resources, and the presence of weeds or forbs inside or near croplands.

Through the review, it was observed that some words were related to each other. For example, “native trees” is directly linked to natural habitat, as well as “nesting opportunities”. Inside organic management practices “sowing regimes/grass management” and “organic fields” can be combined since these are commonly applied practices in this kind of crop fields administration type. The similarity between some of these practices resulted in four grouping categories of management practices that show promise for attracting pollinating insects to farmland. These categories and the practices they group together can be seen in Table 1. The contribution of each practice and each grouping category to the total number of mentions can be seen in Fig. 3. It is important to mention that these categories are not mutually exclusive. Many of them share elements, but they were proposed to try to create a classification that allows us to analyze the best practices for pollinator conservation in fields.

Table 1 Categorization of most recorded keywords and instances for every studied practice.
Full size table
Fig. 3
figure 3

Source: self-elaboration

Relevance of each managerial practice compared to total of mentions.

Full size image

As shown in Table 1 and Fig. 3, terms belonging to the category proximity to natural habitat were the most frequently mentioned throughout the review. A significant number of papers mentioned the relationship between this aspect and the increase in pollination levels in the different crops evaluated. Table 2 presents the category in which each paper consulted was classified according to the main managerial practice used or evaluated to attract pollinators, with a summary of the results. The classification obeys to the main category to which the article would belong, without meaning that it does not have elements of the other categories.

Table 2 Highlights of papers classified according to the main managerial practice used or assessed.
Full size table

Organic farming

In the results, a clear tendency of pollinators to frequent organic management fields, more than conventional farming ones, was observed. According to several cases, organic farming was not a better environment for pollinators due to lack of fertilizers or pesticides, but because their mowing regime was different, allowing more native weeds and flowers to be present near crops and this, in turn, attracted insects searching for forage or nesting (Holzschuh et al. 2008; Brittain et al. 2010; Carvalheiro et al. 2012; Power et al. 2012; Chateil and Porcher 2015). This supports the idea that there is coevolution between insect species and plants that should be studied and favored to improve the presence of pollinators in crops. It was clear that this kind of management holds sowing practices that do show beneficial externalities to pollinators because they result in abundant and diverse presence of vascular plants. (Berg et al. 2019).

Although no clear relationship between different fertilizers and nectar secretion by plants was detected in the literature review, this is an important variable that needs further investigation, since, for example, it is known that nitrogen can also negatively affect some floral properties important for pollinators (Banaszak-Cibicka et al. 2019).

Variables like land size has been reported as important, since insects are less likely to be found foraging in the middle of a field than in its border, closer to natural landscapes. Previous studies have shown that number of bumblebees in small organic managed fields may, in some cases, double those found in extensive, conventional configurations (Belfrage et al. 2005; Happe et al. 2018). Organic management seemed to have better results in general than conventional farming (Andersson et al. 2014; Power et al. 2016), and the effect is much greater when consecutive organically managed fields align together forming a protected area in such a way as to provide shelter and nesting opportunities as an extension of rural landscapes (Holzschuh et al. 2010; Hall et al. 2019).

Proximity to natural habitat

Carvalheiro et al. (2010) found that the number and variety of pollinators in the field declined rapidly with increasing distance from the natural habitat boundary. The researchers declared that these negative effects were difficult to overcome, even after implementing other positive practices such as not applying pesticides in fields. Investigators found that mango production began to decrease too about 500 m away from native habitat’s border because there was scarce cross pollination due to poor biodiversity. Caudill et al. (2017) found that the number of pollinator visits were higher in a coffee plantation in Costa Rica in the borders with natural habitat trees that provided shadow to insects. These frontiers also contained higher numbers of native species compared to the observed deep inside the crop fields, demonstrating the importance of keeping natural habitat intact to preserve an efficient species diversity.

While testing if pollination potential could be achieved in conventional management fields by using adjacent patches of flowers and bushes, Andersson et al. (2014) found that the measures did not work since flower beans have long corollary tubes which could not be pollinated by every insect species. Bumblebees could have pollinated the flowers, but these insects are usually attracted to seminatural grasslands, which this farm did not have. According to Andersson et al. (2014), bean yield is increased significantly by insect pollination as well, where plants grew higher number of pods and beans, but only on organic farms with increased landscape heterogeneity. These researchers concluded that complex crop rotations were not enough to attract pollinators or does not have the same impact than preserving natural habitat and reducing farming intensity.

Bravo-Monroy et al. (2015), conducted similar observations in a coffee plantation in Colombia. Native insect presence decreased significantly as distance to natural habitat increased. The paper mentions how pollinations increases coffee yield and suggests planting native plant patches inside coffee fields to form a kind of mutualism in which, at the same time, the native plants would provide shadows to the native bees and make foraging inside crop fields more appealing to insects. An interesting finding, however, was that honeybees were able to visit farms further away from natural habitat’s border than the native species. In one research, strawberries were separated from pollinators using plastic bags, resulting in fruits with more malformations and less mass, which led to the conclusion that the intervention of insects was necessary to improve the quality of the final product (MacInnis and Forrest 2019). They compared the effect between honey bees and native bees and found, similar to Bravo-Monroy et al. (2015) that the honey bees could travel larger distances than the natives but the latter, in turn, had higher pollination success and the plants visited by these species grew heavier fruits.

In China, Wu et al. (2019) measured the presence of pollinators in function to proximity to natural habitat in apple orchards, and their results complement those found in previously mentioned studies. Natural plant species in grasslands not frequented by humans are the preferred ground for native pollinators to nest and search for food. This, however, was impossible in the studied orchards since these were intensively managed by humans. The researchers also note that monospecific forests cultivated by farm managers were also ineffective in attracting insects. This might be because these forests had no important diversity of plants, and they were also very frequented by humans. There is also evidence that suggest that even if the required measures of natural habitat preservation are taken, adjacent farms management might also affect the presence of insects of a given field. According to Brittain et al. (2010) a field, even if it is managed organically, may not receive a significant number of pollinators because it may be completely separated from its natural habitat because it is surrounded by large plots of land managed conventionally. The creation of concatenated farms that maintain a degree of natural habitat can provide insects with connecting bridges in which pollinators can travel between patches of natural habitat, and this would in turn improve their presence in adjacent fields. Kehinde and Samways, (2012) also provide data that confirms the idea of connectivity but insist that this matter should be further investigated.

As for how much native habitat surrounding crop fields must be maintained without human manipulation to obtain pollination services, a study in California, USA, showed that almost negligible pollination services were obtained where fields were surrounded by 5% or less of natural habitat. However, increasing this percentage to at least 10% would stimulate insect visitation (Klein et al. 2012). Similar results were found by Holland et al. (2015) while trying to figure out what percentage of uncropped land must surround AES (Agri-Environmental Schemes) fields in order to make them more effective. They found that above 10% the abundance of pollinating insects quadrupled. On the other hand, very large natural habitats that provide sufficient foraging opportunities for pollinators may cause them to have no need to visit crops (Chateil and Porcher 2015). Proximity to natural habitat has been emulated before using patches of native herbaceous plants and trees within crop fields, but these have been found to deliver the desired ecosystem services in an effective area of roughly 100 m away from the native vegetations patch (Proesmans et al. 2019). This measure alone is not enough to provide good pollination to a whole parcel so some productors have considered inserting native forbs and flower corridors to improve insect survivability and thus density. However, some papers mentioned cases of agricultural products in which this tactic is not viable from a financial standpoint due to arable land decrease (Klein et al. 2012) and thus, should be evaluated carefully in each case to see if the increase in pollination services could compensate for the reduction in productive land.

The replacement of regular fences by live hedgerows seems like a good addition to most of crop yields, since these usually contain higher proportions of insect-pollinated forbs useful to bees as nesting and foraging places. At the same time, live hedgerows serve as connecting bridges that can be crossed by human managers and yet let the pollinators travel freely though different landscapes (Proesmans et al. 2019). Connectivity seems to be one of the most usual consequences of having a big proportion of native habitat land and should try to be emulated (Kehinde and Samways 2012). An organic farm, even if well managed, but lacking connectivity with native habitat because it is surrounded by conventional farms, may not have sufficient pollination services (Brittain et al. 2010). One of the biggest advantages of this practice is that it can be easily adapted in almost all kind of farms without harming arable land productivity. It has even shown good adaptation to intensively managed diary fields (Power et al. 2012). Live hedgerows may also contain trees which provide unique proteinic values the insects cannot always obtain from bushes and flowers. Additionally, it has been found that trees can provide food even in seasons in which flowering resources might be scarce (Donkersley 2019).

Some of the authors reviewed state that pollinating insects, such as butterflies (Zingg et al. 2019), native bees (Caudill et al. 2017; Cely-Santos and Philpott 2019), honeybees (Carvalheiro et al. 2010; Bravo-Monroy et al. 2015), stingless bees (Bravo-Monroy et al. 2015), wild bees (Holland et al. 2015; Hall et al. 2019; MacInnis and Forrest 2019; Wu et al. 2019; Steinert et al. 2020; Odanaka and Rehan 2020), hoverflies (Proesmans et al. 2019), and bumblebees (Shibata and Kudo 2020), are extremely sensitive to changes in the landscape. All species appear to have very different habitat requirements (Power et al. 2016), requiring producers to plan carefully, based on the species they may need (Hall et al. 2019). These researchers assert that species that thrive only in forested landscapes are the most threatened and least found in fields, which could generate low interest in their protection. Different pollinator species benefit plants in unique ways, and because of that, conservation efforts cannot focus on a single group. Ecological management practices that merge two or more landscape configurations into a mosaic pattern could have a higher success rate in conserving biodiversity. It is interesting, then, to study the ways of combining conservation strategies to find successful configurations, which poses a possible field for future research.

On intensely managed croplands, agri-environmental schemes, or BPA (Biodiversity Promotion Areas) proved to be effective. The later practice aims to prevent biodiversity decimation in fields by leaving some unaltered areas within or around them. By simply increasing BPA area from 5 to 15% an increase in density and variety of specific pollinator species from 22% up to 60% has been achieved (Zingg et al. 2019). This, however, has not been as successful with red listed specialist species that apparently need very particular and intricate landscape configurations and proves that insects have all very different habitat requirements. To avoid loss of pollinator groups, a heterogeneous configuration of the practices described above is recommended. Avoiding the use of herbicides allows the growth of native herbaceous plants, planting floral resources in fields can make crops attractive to native bees, and proximity to natural habitat (from 100 to 500 m depending on the species) can provide effective pollination services (Carvalheiro et al. 2010).

Seminatural grasslands

The influence on pollinators of seminatural grasslands were also a very recurrent topic throughout the revision. Several data have been found confirming that native grasses can maintain good living conditions for pollinators. This heterogeneous configuration allows for greater abundance and diversity of various insect communities by providing good foraging and nesting opportunities, creating suitable microhabitats for diverse pollinator groups (Power et al. 2016). Giuliano et al. (2018) defend that homogenization is one of the problems most related with biodiversity decrease. In their case, the fields with least frequent cutting regimes and rotating crops were the most biodiverse of all. They also found that sowing field margins with seed mixtures improved arthropod diversity and planting native herbs with flowers increased pollinator presence.

Karamaouna et al. (2019) found species that could be inserted into the field to increase yield and biodiversity. The planting of vegetation patches attracted greater numbers and more diverse populations of pollinators and at the same time attracted natural predators of pests. Researchers recommend using patches of native plants rather than exotics, as they can establish more easily in the field and genetic erosion is avoided. Bruppacher et al. (2016) reached similar conclusions when investigating the effect of slight modifications in mowing practices on the presence of butterflies in crop fields. The best results were obtained by postponing the mowing season nearly one month further the moment the butterfly reproductive cycle had ended, and by maintaining a patch of uncut shrubs after this process. The researchers observed a cumulative effect on diversity over time. Fields subjected to this management had up to 60% more diversity than traditionally mowed fields. From Giuliano et al. (2018) findings, it can be concluded that reducing the number of mowing from 2 to 1.5 per year can help species with low resistance to habitat destruction to recover.

Determining the appropriate mowing frequency is one of the most complex aspects of this practice, as it requires a thorough understanding of the nesting needs of each species. Not mowing periodically can be as detrimental to pollinator communities as mowing too often (Bruppacher et al. 2016). Berg et al. (2019) found that not mowing can cause a lot of bushes and trees to grow and cause pollinators to avoid these areas since they cannot obtain their needed amount of heat and sunlight. This means that planting processes must be further studied to create strategies that are adapted to each important group of pollinators and to find a balance point where their presence can be optimized.

Leaving grass plots untouched also helps larvae and, consequently, the entire insect community, recover more quickly. Farmers should delay mowing as long as possible in a compromise between production and biodiversity, and once mowed, should remove organic materials. Contrary to other recommendations, it has been proven that organic debris piled up after mowing can cause shade and humidity, changing the microclimate and not allowing new shrub growth. Pollinator abundance increased significantly approximately three years after mowing in the fields studied in Norway, which allows us to deduce how long it may take for a field to recover after mowing (Steinert et al. 2020).

Flowering resources

Numerous researchers have found that the presence of floral resources in fields is associated with increased pollinator populations. Flowering plants are beneficial for insects because their pollen is a source of carbohydrates, vitamins, minerals and amino acids, which is crucial for maintaining the health of pollinators. (Campbell et al. 2019; Topitzhofer et al. 2019). By measuring insect concentration at the boundaries between cereal fields and natural habitat, Marja et al. (2018) found that flower plantings generate a better distribution of pollinating insect visits. Holland et al. (2015) inserted flowering plants inside crop fields and found that these became more attractive as pollinators were distributed throughout the field. However, they insisted on further research to find a balance point where floral resources could be planted within crop fields without distracting insects from pollinating surrounding plants. Gilpin et al. (2019) investigated the effects of flower fields in Australia and concluded that it does not affect the pollination process of other native flowering plants outside the fields. In contrast, Hodgkiss et al. (2019) found that inserting flower resources into the fields did not affect insect visitation in an important statistical sense. They suggest that this may have occurred because, unlike much previous research, pollination services in these fields were already adequate. However, there was strong evidence to suggest that the use of floral resources increased the presence of natural enemies of strawberry pests, up to four times more than in previous measurements.

NFCA (Native Flower Conservation Areas) proved to have positive effects of mango yield in a study conducted by Carvalheiro et al. (2012). Flowers stimulate cross pollination of vegetal species which in turn improve fruits genetic codes. However, similar to distance to natural habitat, this ecosystem service begins to decrease as distance from the NFCA increases. Badillo-Montaño et al. (2019) concluded that inserting vast floral resources into the fields could also include nonnative species of crops into native pollinators diets. In some cases, it has been recognized that seminatural grasslands attract more pollination services to fields than the presence of floral resources, as it seems that its excess can distract pollinators from crops pollination (Galbraith et al. 2019). However, flower resources seem to be closely related to field attractiveness. During an experiment conducted by Topitzhofer et al. (2019) it was observed that one of the least visited species was a sterile hybrid carrot crop that did not offer sufficient floral resources and pollen to be attractive to pollinating insects. It was also growing in a more desert-like part of the landscape, without much more diverse floral species around it that could attract foraging. Species recognized for their pollen supply, such as meadowfoam and almond trees, were the most visited.

A variety of flowers has the potential to attract long-tongued pollinators, such as butterflies. Wix et al. (2019) found that planting a mix of plants in floral strips was more successful in attracting butterflies than the density or height of the plants themselves. Planting floral resources needs to be a strategically thought out process and targeted especially to the required pollinating insect groups to avoid loss of investment (Andersson et al. 2014).

Flower diversity and NFCAs should be implemented when possible. Not only for its potential attraction but also for achieving resilient pollinating communities. It has been proven that inserting floral arrangements or floral trees would improve pollen availability for insects, which helps them maintain good health, increased individual and colony weight, and reproductive success (Campbell et al. 2019). This helps colonies become more resistant to dangerous pests such as the mites, which seem to be more virulent and deathly on highly human-controlled apiaries (Dynes et al. 2020).

Conclusion

The analysis of the information compiled in the papers reviewed shows that the most important elements for improving the diversity, abundance and quality of pollinators are the proximity of the crop fields to natural habitats, the presence of flower resources and the degree to which the crop is combined with plant species native to the region. It was found that organic agriculture benefits the pollinator population more due to the heterogeneity of the plant resources present in the crops than to the non-use of chemical insecticides, although this aspect is still important.

Organic management practices such as preserving natural habitat, sowing flower resources in field, decreasing mowing frequency and using live hedgerows for landscape connectivity can lead to increased biodiversity in fields and better pollinating services for crops. Some of these practices are low cost and can be easily set up.

The proximity, connectivity and biodiversity of natural floral resources have a direct and positive relationship with the quality and quantity of pollinator colonies by increasing their sources of food, nesting, and protection. These resources also become barriers against the spread of insecticides and provide additional ecosystem services by harboring other beneficial insects and animals. However, it is important to carefully monitor the vegetation present to ensure compatibility between flowers and pollinators and that flowering plants receive, for example, adequate solar radiation to develop properly and abundantly.

The results of this research match with previous findings that warn that, although there are certain practices that stimulate the presence of pollinators in fields, there is no foolproof formula for attracting all the species required by agroecosystems. The requirements of a specific species must be carefully studied before making costly adjustments to landscape configurations. An interesting field for future research is, then, to study the ways of combining conservation strategies to find successful configurations of fields and natural habitats to preserve the diversity of pollinators.