Pollination is a fundamental ecosystem service that enables sexual reproduction in plants, playing a crucial role in maintaining biodiversity, ecosystem functioning, and food security [1]. It is essential in both natural and human-managed ecosystems, supporting the regeneration of wild plant populations and the production of fruits, seeds, and vegetables [1, 2]. More than 75% of the world’s leading food crops, including many fruits, vegetables, nuts, and oilseeds, rely on varying degrees of animal pollinators, predominantly insects [3]. Globally, more than 300 commercial crops benefit from animal-mediated pollination, and approximately 84% of these are pollinated primarily by insects [1, 4]. Among insect pollinators, honeybees (Apis mellifera) are the most efficient and widely managed pollinators. Their contribution is immense, as they are responsible for pollinating 70–80% of insect-pollinated crops, accounting for approximately 35% of global food production [1, 5].

The economic value of pollination services provided by honeybees is substantial. In the United States of America alone, the annual contribution of honeybee pollination to agriculture is estimated at USD 3.65 billion [6], and globally, the economic value of insect pollination has been estimated at approximately €153 billion annually, which represents 9.5% of the total value of agricultural food production worldwide [7]. In addition to increasing crop yields, honeybee pollination also enhances seed quality, size, and uniformity [8, 9]; therefore, honeybee pollination is increasingly regarded as a vital agricultural input on par with fertilizers, labor, and crop protection products [10].

Carrot (Daucus carota L.) is a biennial, cross-pollinated root vegetable that is widely grown in tropical and subtropical regions. It is valued for its high content of alpha- and beta-carotene, which are precursors of vitamin A and are thus essential for human vision and immune function [11]. Owing to its floral biology, where anthers release pollen before the stigma becomes receptive (protandry), carrot plants require cross-pollination for effective seed set [8]. Honeybee pollination has been found to be crucial for commercial carrot seed production [12, 13].

In Ethiopia, carrot cultivation is expanding rapidly due to increasing demand in urban and peri-urban markets. Recent estimates indicate that total production has reached 12,345.8 metric tons cultivated on approximately 2,215 hectares [11]. However, domestic seed production remains minimal due to inadequate pollination, leading to low seed yields. Consequently, the country depends heavily on imported carrot seeds, primarily from France, the Netherlands, and Denmark [14]. The high cost of import, which amounted to approximately €106,183 in 2004 [15], exerts significant pressure on national foreign exchange reserves and poses challenges for sustainable agricultural development.

To reduce reliance on imported seeds and support local seed sovereignty, enhancing pollination, particularly through the utilization of managed honeybee colonies, is a promising solution. Therefore, the current study was designed to investigate the impact of honeybee pollination on the yield and germination capacity of carrot seeds and to assess the diversity and abundance of pollinators visiting carrot flowers under Ethiopian conditions.

Study area

The study was conducted in Walmera District, central highlands of Ethiopia. The study location was 9°03′N, 38°30′E, with an elevation of 2450 masl and a bimodal rainfall pattern. The main rainy season is from June to September, with a mean annual precipitation of 1150 mm.

Plant material

Seeds of carrot variety Haramaya I were recieved from Holeta Agricultural Research Center, Holeta, Ethiopia.

Experimental design and agronomic managment

This study was carried out to evaluate the effects of insect pollinators, particularly honeybees, on carrot seed yield and germination capacity under different pollination treatments. The experiment utilized the released carrot variety, Haramaya I, which was selected for its proven adaptability to medium to high altitudes ranging from 1600 to 2400 m above sea level.

The seeds of Haramaya I were sown on plots measuring 3 m by 3 m, following the recommended agronomic guidelines. A seed rate of 3–5 kg per hectare was employed, along with the application of 46 kg/ha phosphorus (P₂O₅) and 64 kg/ha nitrogen (N) as basal fertilizer. The experiment was conducted in a randomized complete block design (RCBD) to minimize the effects of field variability. Each treatment was replicated three times to ensure statistical reliability.

Throughout the experimental period, all standard agronomic practices necessary for optimal carrot growth were implemented. These included timely weeding, appropriate watering, and routine monitoring for pest and disease incidence, which were managed accordingly to avoid interference with pollination activities [12].

Treatments

Three distinct pollination treatments were applied to evaluate the impact of different pollination scenarios on carrot seed production:

Honeybee only pollinated (T1): In this treatment, plots were enclosed in plastic mesh cages, and a medium-strength honeybee (Apis mellifera) colony housed in a standard Zander hive was introduced inside each cage (Fig. 1). The colonies were provided with sugar syrup to sustain them until the flowering phase ended, and the cages were removed. Since the enclosed environment restricts honeybees’ access to natural floral resources, the sugar syrup serves as a necessary supplemental energy source to maintain colony health and activity during the experimental period. While this artificial feeding could slightly alter natural foraging behavior by reducing their motivation to search for nectar, it ensures colony survival and consistency of pollination activity in the absence of alternative food sources within the cages. This controlled feeding approach is commonly used in pollination experiments to balance honeybee welfare with experimental integrity [4].

Insect pollinator exclusion (T2): Plots were similarly enclosed with plastic mesh cages but without introducing any pollinators. This treatment was designed to exclude all insect visitors, thereby representing self-pollination or wind pollination only [16].

Open pollination (T3): These plots were left open and accessible to all natural insect visitors. The insect orders observed during the pollination study were Hymenoptera (bees and wasps), Diptera (flies), Lepidoptera (butterflies and moths), and Coleoptera (beetles). No cages were used, allowing for natural pollination under open field conditions [17]

Experimental setup and status of carrots under field conditions

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Pollinator observation and insect sampling

Pollinator activity was assessed during the peak flowering period of the crop. Insect visitation was monitored in a standardized 1 m² area within each plot. Observations were conducted over five consecutive days, with data collection starting at 9:00 and continuing until 18:00 at three-hour intervals each day (9:00, 12:00, 15:00, and 18:00). During each time interval, the number of insect visiting flowers within the designated area was counted over a 10 min period.

To complement the observational data, visiting insects were also captured via a standard insect sweep net. The collected samples were preserved at Holeta Bee Research Center using alcohol (70% ethanol) and later identified to the species or morphogroup level by a qualified entomologist at the Holeta Bee Research Center. This allowed for the assessment of pollinator diversity and the specific role of honeybees relative to other insect visitors.

Calculation of yield advantage (% increment)

The yield advantage of one treatment over another can be calculated via the following formula:

Yield Advantage (%) =  *100 [17].

Whereas, treatment A represents the seed yield from either honeybee-pollinated or open pollinated plots, while treatment B represents the seed yield from either self-pollinated (pollinator-excluded) or honeybee-pollinated plots, depending on the comparison being made.

1. (a)

   Honeybee vs. self-pollination: 

2. (b)

   Open vs. self-pollination: 

3. (c)

   Open vs. Honeybee only:   

Finally, The data on seed yield, thousand seed weight, and germination percentage were analyzed using one-way ANOVA using R software to evaluate differences among treatments whereas the data of the insect visitors were quantified via simple frequency tabulation using SPSS.

Seed yield per plant

The seed yield per plant exhibited substantial variation across the different pollination treatments, reflecting the vital influence of insect-mediated pollination. The highest seed yield per plant was recorded under open pollination conditions, reaching 193.20 ± 18.97 seeds (Table 1). This treatment allowed access to a diverse array of insect flower visitors, including honeybees, wild bees and flies, which likely contributed to more effective and thorough pollination. The treatment involving honeybees alone also performed well, producing 150.47 ± 13.35 seeds per plant. The yield difference between these two treatments was not statistically significant, as indicated by their shared letter grouping (a). These findings suggest that honeybees alone are sufficiently efficient in facilitating pollination to maintain high seed production levels per plant. In stark contrast, the exclusion of insect pollinators led to a sharp decline in seed yield, with only 59.53 ± 6.68 seeds per plant statistically and inferior to the other treatments. This significant reduction highlights the critical importance of insect pollinators, particularly honeybees, in maximizing reproductive success and yield at the individual plant level.

Seed yield per umbel

The pattern observed in seed yield per umbel mirrored the trends observed at the whole-plant level, further reinforcing the importance of insect pollinators. The open pollination treatment resulted in the highest seed yield per umbel, with an average of 5.16 ± 0.44 seeds (Table 1). This superior performance is likely attributable to the synergistic effect of multiple pollinator species, which enhance pollen transfer and increase the likelihood of complete fertilization across umbels. The honeybee only treatment yielded 4.04 ± 0.34 seeds per umbel was similar to that of open pollination. These findings suggest that honeybees can independently ensure effective pollination of umbels, providing reliable service even in the absence of other pollinators. However, the treatment excluding insect pollinators produced only 1.50 ± 0.16 seeds per umbel, a significantly lower yield, indicating poor pollination efficiency. This finding underscores the strong reliance of crops on biotic pollination agents to achieve optimal seed set within floral structures.

Mean seed yield per hectare

At the broader, field-scale level, the mean seed yield per hectare displayed a consistent and revealing pattern. Open pollination resulted in a mean yield of 561.97 ± 41.08 kg/ha (Table 1), against the 559.22 ± 42.17 kg/ha obtained under honeybee only pollination. These two means were not significantly different, confirming that honeybee pollination alone can support crop productivity nearly as effectively as the full complement of insect pollinators. On the other hand, the exclusion of insect pollinators led to a dramatic yield reduction, with only 144.45 ± 17.13 kg/ha recorded. This represents a loss of more than 70% compared with the insect-pollinated treatments, clearly demonstrating the indispensable role of insect pollination in agricultural productivity.

Yield advantages among treatments

The comparison of yield among the different pollination treatments clearly demonstrated the vital role of honeybee pollination in enhancing carrot seed production. When carrot plants were pollinated exclusively by honeybees, the seed yield increased by 287.14% (Table 2), which is approximately 2.87 times greater than that observed under self-pollination conditions. This substantial yield advantage indicates that honeybee activity alone can nearly triple carrot seed productivity, underscoring their efficiency and effectiveness as pollinators.

Similarly, under open pollination, where plants are exposed to a combination of pollinators, including honeybees, wild insects, and possibly wind, the yield was 289.04% greater (approximately 2.89 times greater) than that in self-pollinated plots. This result further confirms the critical importance of external pollination agents in maximizing seed output. However, the marginal yield difference of only 0.49% (approximately 0.0049 times) between the open pollination and honeybee only pollination treatments suggests that honeybees contribute almost entirely to pollination services in carrot fields. In other words, the contribution of other insect pollinators or abiotic factors, such as wind, is minimal in comparison to that of honeybees.

These findings highlight the overwhelmingly dominant role of honeybees in carrot seed production and suggest that maintaining a healthy population of managed or wild honeybees is crucial for ensuring high yields. The minimal additional benefit from other pollinators indicates that without honeybees, carrot seed production could be severely affected, regardless of the presence of other potential pollinators. Therefore, targeted strategies for the conservation, enhancement, and sustainable management of honeybee populations should be prioritized in carrot-producing regions. This includes providing diverse and abundant floral resources, minimizing pesticide exposure, and protecting the nesting habitats of pollinators.

Thousand seed weight and germination percentage

The data presented in Table 3 clearly demonstrate that insect pollination, especially by honeybees, plays a crucial role in enhancing both the physical and physiological qualities of carrot seeds. Specifically, both the 1000 seed weight and germination percentage were significantly greater in the treatments involving pollination by honeybees alone or through open pollination than in the plots in which insect pollinators were excluded. The highest 1000 seed weight was observed under open pollination conditions (1.86 ± 0.12 g), followed closely by the honeybee only treatment (1.81 ± 0.91 g). These two treatments did not significantly differ from each other, as indicated by the shared statistical grouping (‘a’), suggesting that honeybees are the principal contributors to effective pollination under open conditions. In contrast, the absence of insect pollinators resulted in a notably lower seed weight (1.59 ± 0.0 g), which was statistically distinct, highlighting the adverse impact of pollinator exclusion on seed development.

A similar trend was observed for the percentage of seed germination. Seeds from open pollinated plots (96.10 ± 2.8%) and those pollinated by honeybees only (92.5.11 ± 2.8%) presented significantly higher germination rates than did seeds from plots without insect pollination (40.53 ± 2.31%). The latter group was significantly different and presented reduced seed viability, likely because of insufficient fertilization during flowering. These findings underscore the importance of insect-mediated pollination in ensuring not only seed formation but also the development of seeds with high vigor and potential for successful seed development for plant growth.

Insect flower visitors

The observation data revealed that insect visitors belong to four major orders, Hymenoptera, Diptera, Coleoptera, and Lepidoptera, with Hymenoptera being the most dominant group, accounting for 58.2% of the total 430 insect visitors (Table 4). Among these pollinators, honeybee (Apis mellifera) was the most common pollinator, accounting for 32.7% of all visits, highlighting its critical role in pollination. Stingless bees (Meliponula beccarii) were the second most common within this order, contributing to 14.8% of the visits. Other unidentified hymenopterans and wasps (Vespula germanica) contributed 9.5% and 1.2%, respectively, to the population, suggesting a diversity of native and wild pollinators that supplement pollination services. Diptera, represented by Eristalis spp. (hoverflies), were also significant, making up 20.5% of the total visitors. These flies often mimic bees and are effective pollinators of open or shallow flowers, particularly under cooler or early-morning conditions when bee activity is low. Coleoptera, represented by Lamprima aurata, accounted for 11.4% of the visits. Although they are generally less efficient and messier pollinators, their presence indicates that their floral structure may be suitable for beetle pollination. Vanessa cardui (butterfly) was accounted for 7.7% of floral visits of carrot variety Haramaya I (Table 4).

Foraging intensity of flowering insects

Figure 2 shows the diurnal activity patterns of various flowering insects on the carrot variety Haramaya I on the basis of their mean number per 10 min observation period at four different times of the day: 09:00, 12:00, 15:00, and 18:00. Among the recorded species, Apis mellifera was the dominant flower visitors throughout the day, with its activity steadily increasing from approximately three individuals at 09:00 to a peak of approximately 15 individuals at 15:00, before dropping sharply to near zero by 18:00. Meliponula beccarii was the second most active flower visitors, showing no activity at 09:00, peaking at approximately 12:00 with approximately eight individuals, and then slightly declining by 15:00 before also ceasing activity by 18:00.

Other pollinators presented lower and more variable activity levels. Eristalis spp. presented a slight increase in activity during the afternoon, peaking at approximately 15:00. Vanessa cardui followed a similar pattern, with its highest activity occurring between 12:00 and 15:00. Lamprima aurata was observed only in the morning and around noon, suggesting that it is primarily an early-day forager. Vespula germanica was a minor pollinator, with low numbers throughout the day and a slight peak at noon.

Diurnal activity patterns of various insect pollinators on the carrot variety Haramaya I

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Seed yield and yield advantages of Carrot variety Haramaya I

Both the open pollination and honeybee only pollination treatments resulted in significantly greater seed yields than did the plots that were caged to exclude all the insect pollinators. This trend supports the findings of Free [13], who highlighted the importance of insect pollinators, particularly honeybees, in carrot seed production and noted that reliance on honeybees alone may not maximize seed yield because of factors such as floral preferences and limited cross-plant movement. Similarly, Howlett et al. [18] and Howlett [19] demonstrated that nonbeekeeping insects, such as blowflies (Calliphora vicina), can be as effective as honeybees in pollinating hybrid carrot crops, especially under open pollinated conditions.

The use of cages, while necessary for isolating specific pollination treatments, can alter the microenvironment, particularly in terms of light intensity, temperature, and humidity. These changes may affect both plant physiology (e.g., nectar production, flower opening) and pollinator behavior (e.g., foraging activity, flight patterns).

Moreover, confinement may influence honeybee foraging dynamics, potentially leading to increased visitation rates due to restricted space or, conversely, reduced motivation to forage if resources are limited or environmental conditions become suboptimal. While we attempted to mitigate these effects by using mesh cages that allow air circulation and natural light penetration, we acknowledge that such conditions do not perfectly replicate open field environments.

The reduced yield in the honeybee only treatment in the current study, despite the presence of honeybees, can be attributed to the confined conditions inside the mesh cages. Confinement restricts the honeybees’ natural foraging behavior, flight paths, and access to diverse floral resources, likely inducing stress and reducing their pollination effectiveness. This finding corroborates those of Delaplane and Mayer [20], who reported that honeybee performance is significantly influenced by environmental conditions and physical constraints.

Moreover, the proximity of an apiary (within a 1 km radius) to the experimental plots likely contributed to the high honeybee density observed in the open pollinated treatments, increasing pollination efficiency and seed yield. Garibaldi et al. [21] reported that wild and managed pollinators together significantly increase fruit set in crops, reinforcing the idea that proximity to bee sources and pollinator diversity are key drivers of successful pollination.

The results of the present study indicate a significant increase in carrot seed yield under insect-assisted pollination compared with self-pollination, with particularly strong effects observed in the honeybee and open pollination treatments. Specifically, the seed yield increased by approximately 2.87 times with only honeybee pollination and 2.89 times under open pollination relative to self-pollination. These findings align well with recent studies that underscore the critical role of flowering insects in improving both the quantity and quality of seed yield in various crops, including carrots [1, 13].

Desha et al. [22] reported a substantial increase in seed yield for Brassica carinata when plots were caged with honeybees, with a yield of 24.01 quintals/ha compared with only 17.08 quintals/ha in plots where insect access was excluded, a 34.8% increase. These findings support the notion that honeybees serve as highly efficient pollinators, enhancing reproductive success through effective pollen transfer. Similarly, in a study on Nigella sativa, Tesfaye et al. [23] reported that honeybee-pollinated plots presented significantly greater capsule numbers and seed set than those without insect visitation did, further highlighting the productivity gains facilitated by insect pollination.

The slight yield advantage observed under open pollination conditions over honeybee only pollination (an increase of approximately 0.0049 times) suggests that a diverse pollinator community may provide marginal but meaningful benefits. Research by Gaffney et al. [24] emphasized that while honeybees are dominant pollinators, the effectiveness of pollination can vary with insect behavior and pollen carrying capacity. They noted that frequent visitors to hybrid carrot flowers were not always effective pollen carriers, highlighting the importance of evaluating pollinator efficacy rather than just visitation rates.

Thousand seed weight and germination capacity of carrots

The findings on the thousand seed weight and germination capacity of the carrot variety Haramaya I, which showed no statistically significant differences between open pollination and honeybee only pollination but significantly greater values than self-pollination, were consistent with recent studies highlighting the vital role of flowering insects, particularly honeybees, in enhancing seed quality. Honeybees (Apis mellifera) are efficient pollinators for carrot crops because of their frequent foraging behavior and ability to facilitate cross-pollination [25]. Compared with self-pollinated seeds, cross-pollination is known to increase genetic diversity and reduce inbreeding depression, which often results in heavier seeds and greater germination potential [26]. In Carrot variety, Haramaya I, the similarity between open and honeybee only pollination outcomes indicates that honeybee pollination is efficient to ensure optimal seed development. This observation aligns with the broader literature. For example, Klein et al. [1] emphasized that insect pollination, especially by honeybees, plays a key role in improving seed quantity and quality in many fruit and vegetable crops, including carrot. Garibaldi et al. [20] further showed that even in the presence of honeybees, contributions from wild pollinators significantly increase crop yields, indicating the importance of pollinator diversity. Roulston and Goodell [27] noted that reliance on a single pollinator species may increase vulnerability to pollination failure due to environmental stresses or diseases; thus, maintaining a diverse pollinator community is essential for resilience.

Flowering insects of the Carrot variety Haramaya I

The most important flowering insects of the Haramaya I carrot variety were bees, particularly honeybees and stingless bees, which together made up nearly half of all insect visits. Hoverflies also played a significant role, especially when bee activity was low, while beetles and butterflies contributed marginally to the pollination system.

These results affirm the critical role of bees, especially Apis mellifera and stingless bees, in carrot pollination while also highlighting the complementary contributions of diverse wild pollinators. This aligns with the growing body of literature emphasizing the importance of both managed and wild pollinators in agroecosystems. For example, Garibaldi et al. [20] demonstrated that wild pollinators often provide unique and essential services that complement honeybee activity, increasing fruit and seed set across many crops. Similarly, Rader et al. [28] emphasized the need for pollinator diversity to ensure the stability and resilience of pollination services, especially under variable environmental conditions. The presence of hoverflies and beetles, which are less efficient than bees but still functional, supports findings from Orford et al. [29] that non-bee insects can make significant contributions, particularly in cooler or bee-scarce contexts.

Foraging intensity of flowering insects

The observed peak in pollinator activity between 12:00 and 15:00 underscores the importance of this midday window for effective pollination services in the studied agroecosystem. This pattern is consistent with findings from multiple studies, which report that many pollinators, particularly bees, exhibit diurnal foraging behavior influenced by temperature, light intensity, and floral resource availability [8, 30]. These abiotic factors are often optimal at midday, enhancing nectar secretion and the visibility of floral cues, thus stimulating greater foraging activity [31].

The detection of multiple pollinator species foraging at different times of the day suggests a case of temporal complementarity, a phenomenon where different pollinators utilize floral resources at different times, reducing interspecific competition and increasing overall pollination efficiency [32]. This temporal resource partitioning increases the functional diversity of the pollinator community, making the pollination system more resilient to environmental variability and species-specific declines [33]. For example, solitary bees may forage earlier or later than honeybees do, and butterflies or hoverflies may be more active during overcast periods when bees reduce their foraging [34].

Moreover, such temporal complementarity has been shown to stabilize pollination services over time, as asynchronous activity among species ensures that flowers receive visits throughout the day [20]. This can be particularly beneficial for plants with long anthesis periods or those that require repeated visits for effective fertilization.

From a management perspective, the identification of peak pollinator activity periods has crucial implications [35]. Avoiding pesticide applications, mechanical weeding, or other disruptive practices during the 12:00–15:00 window can significantly reduce pollinator mortality and protect the integrity of the pollination process [36]. Many studies have shown that pesticide exposure during foraging can result in sublethal effects, such as impaired navigation, reduced learning ability, and a decrease in colony level, particularly in bees [37, 38]. Therefore, aligning farm practices with pollinator activity rhythms supports both biodiversity conservation and crop productivity.

Limitations of the study: Specifically, the research was conducted at a single geographic location over a two-year period, which may limit the generalizability of the findings to broader ecological or agricultural contexts. Variations in climate, vegetation types, pollinator communities, and management practices across regions and years could influence pollination dynamics and crop responses.

Our study demonstrated that the carrot variety Haramaya I is highly dependent on insect pollination, particularly by honeybees. Open pollination resulted in an average seed yield of 561.97 ± 41.08 kg/ha, which was not significantly different from the 559.22 ± 42.17 kg/ha yield observed under honeybee only pollination. In contrast, the exclusion of all flowering insects led to a substantial reduction in seed yield of Carrot variety Haramaya I, with only 144.45 ± 17.13 kg/ha produced. Seed germination rates were also significantly higher under both open and honeybee only pollination compared to self-pollination. Besides honeybees, key flowering insects observed under central highland conditions in Ethiopia included Eristalis spp., Meliponula beccarii, Lamprima aurata, Vanessa cardui, and Vespula germanica. On the basis of these findings, placing honeybee colonies near carrot fields during the flowering period is recommended to ensure effective pollination, higher seed yield, and improved seed quality for better germination and market. Additionally, further multi-site studies are needed to validate and expand these findings across different agroecological zones.