Effect Of Honeybee On Native Bee Pollinators Biology Essay


Animal pollination plays an important role in the reproduction and fruit set of many cultivated, flowering crop plants and wild plant communities. Bees comprise an estimated 25,000-30,000 species worldwide, all obligate flower visitors. Animal pollination is effected by many different species ranging from vertebrates (e.g., bats) to invertebrates such as insects and intensity or quality of pollination may be affected if pollinator species change. Introduction of non-native (exotic) pollinators might have impact on both native plants and pollinators communities. Thus, the introduction of non-native bees may cause direct and indirect ecological impacts.

1. Introduction

The flowering plants (angiosperms), comprise approximately one-sixth of the total number of described species (250,000 species) and insects about two-thirds. These groups thus dominate the flora and fauna of Earth's terrestrial habitats, and interactions between them are dominant components of all terrestrial ecosystems (1). One of the most ecologically important of these interactions is that between flowering plants and pollinator insects (2). Most of these flowering plants - in some studies estimates are as high as 90% (3) - including many important agricultural species, are pollinated by animals, mainly insects (4); the rest of angiosperms rely on abiotic agents such as wind or water. Animal pollination plays an important role in the reproduction and fruit set of many cultivated, flowering crop plants (5, 6 7) and wild plant communities (8, 9, 10, 11). It contributes to the maintenance of plant diversity, in terms of species number, genetic variation and richness of functional groups (12, 13).

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Pollination is defined as the transfer of pollen from anther (the male part of a flower) to a stigma (female part of a flower) of the same or different flower, thus enabling fertilization to take place (14). Self-pollination occurs when the anther and stigma are from the same flower, from different flowers on the same plant, or from flowers on different plants of the same cultivar (15). Cross-pollination is the transfer of pollen from one cultivar to the flower of a different cultivar of the same species. Bees are the main pollinating group in many climate zones and in most geographic regions (16). Bees comprise an estimated 25,000-30,000 species worldwide, all obligate flower visitors. Adding these species to other obligate or facultative pollinators such as flies, butterflies and moths, beetles, and birds, the total number of flower-visiting species worldwide is estimated to be nearly 300,000 (3).

Pollinators are one of the important ecosystem elements and well known to provide key ecosystem services to both natural and agro-ecosystems. An ecosystem is a unit of interdependent organisms that interact with each other and with abiotic factors. Ecosystems are considered functional groups composed of elements (structures) and processes (functions). The ecosystem structures are the biotic components (biological species) which can be organized according to the functions they have in the system (i.e. their trophic level). The ecosystem processes, or functions, refers to mechanistic processes such as decomposition, productivity and nitrogen fixation (17). Ecosystem services are natural functions that benefit human populations (18, 19). These services include soil formation, nutrient cycling, gas regulation, climate regulation, pollination as well as recreation and cultural. Hence, understanding the interaction of pollinators is important to improve our understanding of ecosystem services and functions.

Insect pollinators are thought to contribute between 15% and 30% of the human food supply (20) and bees are documented to be the most important pollinating taxon (21). However, the bulk of the world's staple foods are wind-pollinated, anemophilous (self-pollinated) or propagated vegetatively (22). The value of honeybee (Apis mellifera) pollination in the US ranges from $1.6 to $5.7 billion a year (23), and increased to reach $14.6 billion in 2000 (24); in Europe is estimated to worth approximately €4.25 billion, and pollination by other taxa worth around €0.75 billion (21). For global agriculture, the estimated value is around $200 billion (3).

Animal pollination is effected by many different species ranging from vertebrates (e.g., bats) to invertebrates such as insects and intensity or quality of pollination may be affected if pollinator species change. It is widely documented that pollinators and the services they provide are under increasing threat from anthropogenic sources (25, 26). Some of the most important threats recognized include: fragmentation of habitat, habitat isolation, agrochemicals, agricultural intensification, parasites, diseases, climate change, introduced non-native plants and competition with managed pollinators (21). Threats to managed pollinators such as honeybees are also recognized and some studies reported significant losses due to disease and competition between managed honeybees and Africanised honeybees (3).

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Introduction of non-native (exotic) pollinators such as the honeybee, will affect both native plant and pollinator communities. Such effects may be positive or negative for the communities' species. If the efficiency of exotic pollinators, in term of pollen transportation, is more than it in the native pollinator, then native and exotic plants will subsequently increase their fruit and seeds production compared with native plants not pollinated by the exotic species. On the other hand, if the efficiency of native pollinators is higher than the exotic pollinator in pollinating a specific plant, then this may reduce seed set (27).

Honeybees are thought to use less than a third of the available flowering species and substantially fewer species are in use in an intensive manner (28). Therefore, there are variable impacts of foraging by honeybees depending on the plants used, and subsequently on native fauna that use the same resources. If a minor proportion of pollen or nectar are consumed by honeybees, minimal effects on floral and fauna can be expected; if they consume a substantial amount of these resources, impacts may be more significant (29) (figure 1).

Figure 1. The variable impacts of honeybee foraging on native flora and fauna. Thicker arrows represent a potential for stronger effects (28).

Some studies assumed that nectar and pollen feeders, especially bees (Hymenoptera: Apoidea) are strongly affected by interspecific competition for the high-quality food resources provided by the floral community to attract pollinators (30, 31). It is thought that, on oceanic islands, the impact of the introduced honeybee upon native pollinators might have been more severe, and that most likely because native pollinator faunas on oceanic islands lack social bee species, which are frequently abundant pollinators on the continent (32). However, even in Europe, where A. mellifera is a native species, species richness and abundance of wild bees might have affected by invasion impacts of high local densities of A. mellifera (33).

An increase in competitive effects may occur after: the introduction of new competitors, (ii) changes in environmental conditions, and (iii) increased abundance of a competitor. The introduction of non-native pollinators may cause direct and indirect ecological impacts. The direct impacts include competition for floral and nesting resources with native organisms; indirect impacts include the transmission of parasites and/or pathogens to native organisms, and changes in pollination systems of native and exotic floral communities (34).

2. Direct impacts of honeybees:


Competition between honeybees and wild bees (interspecific competition) is thought to be a key factor in structuring foraging communities on flowers (35, 36). Thus, honeybees may compete with native bees for resources, leading to reduced species diversity of pollinators, especially when resources are limited. Interference competition occurs when an organism physically excludes another from an access to food sources. Exploitative competition occurs when reduction of resources by one organism leads it to deprive others of the benefits to be gained from those resources (36).

2. 1. 1. Interference competition

While most studies support the fact that interference competition by aggressive exclusion does not frequently occur between honeybees and native insects during foraging (37), an extremely rare study reported aggression behaviour by Apis toward other bees (28). However, interference by honeybees during robbing has been recognized under certain conditions. In Japan, Sakagami (1959) reports aggressive interactions between introduced A. mellifera and native Apis cerana during the flower dearth period of autumn since all the A. cerana workers were expelled within 2 days by A. mellifera. A. cerana frequently attacks A. mellifera, but A. melliferas was found to be more resistant to hive robbing than A. cerana (38). This interaction is widely cited to be evidence for interspecific aggression by honeybees by many authors, and it may the behaviour responsible for the reduction in population size seen for A. cerana in Japan (28). Aggressive behaviour of some other species of bees such as stingless bees has been recognized. For example, Johnson (1981) studied the aggressive defence of two stingless bee species, Trigona silverstriana and Trigona corvin,g and found that T. silverstriana had almost completely excluded T. corving within three hours of the start of the experiment (39).

2. 1. 2. Exploitative competition

The introduced honeybee is an example of a species that can compete with native bees for floral resources. Honeybees Apis mellifera might competitively displace native pollinators from both floral resources and geographic areas (40). Nevertheless, the degree to which this introduced species modifies native communities remains debatable, reflecting ongoing uncertainty over the results of the resource competition as a mechanism responsible for population changes of native pollinators (41).

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Honeybees begin foraging at lower temperatures than most other pollinators and have first use of most floral resource. This behaviour in foraging activity gives the introduced honeybee an advantage in any competitive interaction, particularly if floral resources are available mainly in the morning before temperature rises (40). For some plants, honeybees can remove up to 30-90% of the nectar and pollen from flowers (42) before native bees start foraging.

Several studies have indicated that introduced honeybees decrease the foraging success of native pollinators as a result of competition for resources. For example, Ginsburg (1983) in New York suggested that interspecific competition between honeybees and native bees affects the distribution of foragers on flower clusters of various sizes, and was greater in the spring (43). Paton (1993) also found interspecific competition between honeybees and Australian native bees and reported that native bees spend twice as long collecting food in the absence of honeybees, implying that the net effect of introducing honeybees might be to increase the numbers of native bees working flowers at one time (29). Moreover, Roubik et al. (1986) have documented a direct competition for pollen or nectar between African honeybees and native stingless bees in Panama (44). Thomson (2004) in California demonstrated negative effects of non-native honeybees on native bumblebees. She found that proximity to honeybee hives significantly reduced the foraging rates and reproductive success of Bombus occidentalis colonies (41). Thomson (2006) found significant niche overlap between foraging preferences of native bumblebees and introduced honeybees, which was as high as 80- 90% during periods of resource scarcity (45). Schaffer et al (1979) studied competition among three species of bees (Apis mellifera, Bombus sonorus, and Xylocopa arizonensis) on several habitats of Agave schottii in Arizona. They found that abundance of Apis was greatest at the most productive habitat, Bombus at intermediate stands and Xylocopa at the least productive habitat (46). Benest (1976) studied foraging by honeybees and three species of bumblebees in France. Data show bees of the same species foraged together on one flowers, but bees avoided mixed-species foraging on the same flower, and honeybees are more tolerant of joint foraging than are bumblebees (47). Paini et al. (2005) have performed a replicated Before-After Control-Impact (BACI) experiment to study the putative impact of feral honeybees on an undescribed species of Australian solitary bee (Megachile sp. M323/F367), and they found a large resource overlap occurred between the two species (48).


Although the above studies show that honeybees have substantial overlap in resource use with some native pollinators, it is hard to confirm the importance of resource competition as a limiting process for population changes without evidence of population-level changes in natural habitats. Yet, no clear evidence has been found of long-term declines of native bees due to competition with non-native honeybees in natural habitats (49). This may be due to the difficulty of carrying out convincing studies of competition between such mobile organisms. The only way to clearly examine the effect of competition for floral resources as the limiting factor for the abundance of natives is by artificially manipulating the introduced bee species, and the population size of native species is then noted. If there is a significant increase in the population size in the absence of exotic bees, then competition is occurring. This task is very hard to accomplish (50).

An alternative technique is to study the correlation between patterns of diversity of native bees and abundance of exotic bees without manipulating their distribution. Kato et al. (1999) studied oceanic islands in the northwest Pacific, and found that honeybees were dominant and native bees were rare or absent on islands (32). Aizen & Feinsinger (1994) related the fragmentation of forests in Argentina with a decline in native pollinators and an increase in honeybee populations (51). Thomson (2004) in California found that proximity to honeybee hives significantly reduced reproductive success of Bombus occidentalis colonies (41). Pleasants (1981) reported negative correlations between Apis and bumblebee abundance (52). Not all studies, however, support this hypothesis. For example, Steffan-Dewenter and Tscharntke (2000) demonstrated that there is no significant correlation between interspecific competition by honeybees and the abundance and species richness of wild bees (53). Minckley et al. (2003) also reported no negative impact of number of honeybees on species richness and abundance of all native bees in the deserts of North America (54).

Therefore, drawing conclusions from these studies is problematic due to the conflicting results, and the lack of indisputable evidence that introduced bees have had a significant impact, via competition, on a population of native pollinators.

Although the different assessments by which competition between honeybees and native bees can be measured, such as floral resource overlap, visitation rates and nest sites, are indirect and might not result in a detrimental impact on native bees being detected, investigating these indirect measurements of competition is nevertheless valuable, as they indicate the potential for competition between honeybees and native bees. The only way to determine a negative impact unequivocally, however, is by assessing direct measurements such as individual survival, fecundity or population numbers (55) (Fig. 2).

alternative floral resource

honey bee

native bee

1. Floral resource


2. Reduced native bee visitation rates

unchanged native bee visitation rates

3. Reduced resource harvesting

unchanged resource harvesting


4b. Reduced fecundity

4a. Reduced survival

4c. Reduced population size/extinction


Figure 2. Shows the different measurements that have to be assessed to determine whether competition is occurring between honeybees and native bees. Although all these measurements can used to determine competitive incidence, only measurements 4a - c can cause a negative impact on native bees, whereas measurements 1-3 have either no impact or a negative impact on native bees (55).

3. Indirect impacts of honeybees:


Introduced pathogens have been recognized as a significant threat to biodiversity, and are associated with the extinction or dramatic decline of various wildlife populations (56). In eusocial insect colonies, the vigour of the pathogen depends on both the ability to infect and spread between insects within a colony and on the ability to spread to new individuals in other colonies. Vertical transmission is thought to be the most important way of pathogen infection of new colonies (57). Horizontal transmission of pathogens can occur through a number of routes such as: contact between individuals (or between individuals and infectious materials) during robbing, contact between infected and uninfected individuals from different colonies during foraging, contact with infectious material from the environment, such as flowers (57). Due to the behaviours of bees foraging, pollinators could run the risk of acquiring infections if pathogens can be horizontally transmitted through shared use of flowers (58).

Species introduced to new regions are likely to transport many pathogens (59). Consequently, for example, the honeybee diseases chalkbrood, caused by the fungus Ascosphaera apis, foulbrood, caused by the bacteria Paenibacillus larvae, the microsporidian Nosema apis, and the mite Varroa destructor now occur throughout the world (50). Goka et al. (2001) discovered that the commercially introduced colonies of European bumblebees are infested with a European race of the endoparasitic mite Locustacarus buchneri (60). Small hive beetles, Aethina tumida, are reported to have been transported into California, North America with the transport of honeybee hives, where they serves as a potential threat to native bumblebees colonies (61). Furthermore, as reviewed by Goulson (2003), the parasitic nematode and three mite species hosted by bumblebees in New Zealand are thought to have come from the U.K. with the imported bees (50). In Europe, bumblebees (Bombus. pascuorum) has been infected by a honeybee pathogen, deformed wing virus (DWV), raising the concern of transmission of viruses from introduced honeybees to native bumblebees and the serious threat this may pose to bumblebee populations (62). On the other hand, not all of the honeybees and other bee diseases are cross-infective. For instance, in the case of Nosema species, Nosema apis infects honeybees but not bumblebees, while Nosema bombi does not infect honeybees but is a pathogen for bumblebees (63). Also, the understanding of the susceptibility of native bees to the parasites and pathogens that have been transmitted by non-native bees is still weak (50).

4. Conclusion and future perspectives

Honeybees have been shown to display a competitive interaction with several bee species for floral resources such as nectar and pollen. Interspecific competition interactions with honeybees have an effect on foraging success of native pollinators. Honeybees might also competitively displace native pollinators from both floral resources and geographic areas. In addition, honeybees do not use interference competition during foraging, although robbing behaviour may take place under certain condition. Although, species richness and abundance of wild bees might have been affected by the invasion of A. mellifera, there is no incontrovertible evidence, however, to indicate that the introduction of honeybees has caused decreased population sizes or extinction of any native pollinators.

Despite the fact that parasites and pathogens are one of the causes of pollinators decline worldwide, and that introduced bees may transmit pathogens to native pollinators, susceptibility of native bees to the parasites and pathogens that have been transmitted by non-native bees is still ambiguous. Yet, there is no clear evidence that enemies carried by introduced bees have impacted native bee populations. In contrast, Donovan (1980) concluded that introduced bees (leafcutting bees) bees are attacked by native bee enemies, but that the converse was not reported (64).

However, the absence of experimental evidence does not necessarily mean that populations or ecosystem processes are not affected by introduced species. I will perform experiments involving manipulative experiments and 'Before-After Control-Impact (BACI)' studies to determine whether honeybees do substantially impact upon native pollinator communities. Given the complexity of such studies, in terms of numbers of species and ecological interactions, ecosystem models may also be valuable to predict the potential consequences on the ecosystem in term of the pollination services they provide.