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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 affected 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 an impact on both native plants and pollinator communities. Thus, the introduction of non-native bees may cause direct and indirect ecological impacts. In this study I will test the hypothesis that introduced honeybees affect wild pollinators, pollination and plant reproduction by modifying foraging behaviour of wild pollinators through the competition, in order to understand the impacts of competition on ecosystem function and community structure.
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 (Buchmann and Nabhan, 1996). One of the most ecologically important of these interactions is that between flowering plants and pollinator insects (Klein et al., 2007). Most of these flowering plants - in some studies estimates are as high as 90% (Kearns et al., 1998) - including many important agricultural species, are pollinated by animals, mainly insects (Daily, 1997); the rest of the angiosperms rely on abiotic agents such as wind or water (Ackerman, 2000). Animal pollination plays an important role in the reproduction and fruit set of many cultivated, flowering crop plants (Nabhan and Buchmann, 1997, Kearns et al., 1998, Westerkamp and Gottsberger, 2000) and wild plant communities (Kearns and Inouye, 1997, Larson and Barrett, 2000, Ashman et al., 2004, Kremen et al., 2007). It contributes to the maintenance of plant diversity, in terms of species number, genetic variation and richness of functional groups (Fontaine et al., 2005, Ashworth et al., 2009).
Flowering plants form a mutualistic relationship with their flower-visiting pollinators. Mutualisms are defined as interspecific interactions between two participants, in which partners gain a net benefit (Bronstein, 1994). A competition interaction is one of the well-known instances of ecological and evolutionary consequences of species diversity within mutualistic interactions (Jason and Bruna, 2000, Stanton, 2003, Palmer et al., 2003). When mutualists share the same resource, competition for access to the resources or services its partners provide may be frequent (e.g., competition between pollinators for floral resources) and is important for understanding the mechanisms underlying host use by multiple species (Palmer et al., 2003)
Pollination is defined as the transfer of pollen from the 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 (Lovatt, 1997). Self-pollination occurs when the anther and stigma are from the same flower or from different flowers on the same plant (Mauseth, 2009). Cross-pollination is the transfer of pollen from one plant to another plant. Bees are the main pollinating group in many climate zones and in most geographic regions (Michener, 2000). 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 (Kearns et al., 1998).
Pollinators are one of the important ecosystem elements and are well known to provide key ecosystem services, specifically pollination, 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, refer to mechanistic processes such as decomposition, productivity and nitrogen fixation (De Marco and Coelho, 2004). Ecosystem services are natural functions that benefit human populations (Daily, 1999). These services include soil formation, nutrient cycling, gas regulation, climate regulation, biological control, pollination as well as recreation and cultural benefits. 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 (Greenleaf and Kremen, 2006) and bees are documented to be the most important pollinating taxon (Potts et al., 2006). However, the majority of the world's staple foods (e.g. wheat, rice, maize) are wind-pollinated (anemophilous), self-pollinated or propagated vegetatively (Allsopp et al., 2008). The value of honeybee (Apis mellifera) pollination in the US ranges from $1.6 to $5.7 billion a year (Vergara, 2008), and increased to reach $14.6 billion in 2000 (Morse and Calderone, 2003); in Europe it is estimated to be worth approximately â‚¬4.25 billion, and pollination by other taxa worth around â‚¬0.75 billion (Potts et al., 2006). For global agriculture, the estimated value is around â‚¬153Â billion (Gallai et al., 2009).
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 (Kremen and Ricketts, 2000, Kevan, 2001). 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 intra- and inter-specific competition with native and invasive species (Potts et al., 2006, Berenbaum, 2007). 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 (Kearns et al., 1998).
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 terms of pollen transportation, is higher than that of the native pollinator, then native and exotic plants will subsequently increase their fruit and seed production compared with native plants not pollinated by the exotic species. On the other hand, if the efficiency of native pollinators is higher than that of the exotic pollinator in pollinating a specific plant, then this may reduce seed set (Whittaker, 2007).
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 (Butz Huryn, 1997). 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 is consumed by honeybees, minimal effects on flora and fauna can be expected; if they consume a substantial amount of these resources, impacts may be more significant (Paton, 1993) (figure 1).
Figure 1. The variable impacts of honeybee foraging on native flora and fauna. Thicker arrows represent a potential for stronger effects (Butz Huryn, 1997).
Some studies assumed that nectar and pollen feeders, especially bees (Hymenoptera: Apoidea) are dynamically affected by interspecific competition for the high-quality food resources awarded by the floral community to attract pollinators (Eickwort and Ginsberg, 1980, Plowright and Laverty, 1984). It is thought that, on oceanic islands, the impact of the introduced honeybee upon native pollinators may be more severe, and that this is probably because native pollinator faunas on oceanic islands lack social bee species, which are frequently abundant pollinators on the continent (Kato et al., 1999). This is most likely due to the ability of social bee to communicate the presence, type and sometimes position of the food source and the large colony size that provide the social bee with a competitive ability advantage to that lacking social behaviour. However, even in Europe, where A. mellifera is a native species, species richness and abundance of wild bees might have been affected by invasion impacts of high local densities of A. mellifera (Walther-Hellwig et al., 2006).
An increase in competitive effects may occur after: "(i) the introduction of new competitors, (ii) changes in environmental conditions, and (iii) increased abundance of a competitor" (Steffan-Dewenter and Tscharntke, 2000). 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 (Nagamitsu et al., 2009).
Direct impacts of honeybees:
COMPETITION FOR FLORAL RESOURCES
Competition between honeybees and wild bees (interspecific competition) is thought to be a key factor in structuring foraging communities on flowers (Corbet et al., 1995, Denno et al., 1995). 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 (Denno et al., 1995).
While most studies find that interference competition by aggressive exclusion does not frequently occur between honeybees and native insects during foraging (Jha and Vandermeer, 2009), one study reported aggressive behaviour by Apis toward other bees (Butz Huryn, 1997). However, interference by honeybees during robbing has been recognized under certain conditions. In Japan, Sakagami (1959) reported 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. Apis cerana frequently attacks A. mellifera, but A. mellifera was found to be more resistant to hive robbing than A. cerana. This interaction is widely cited to be evidence for interspecific aggression by honeybees by many authors, and it may be the behaviour responsible for the reduction in populations of A. cerana in Japan (Butz Huryn, 1997). 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 silvestriana and Trigona corvina and found that T. silvestriana had almost completely excluded T. corvina within three hours of the start of the experiment.
Honeybees Apis mellifera might competitively displace native pollinators from both floral resources and geographic areas (Roubik, 1978). 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 (Thomson, 2004).
With some exceptions (e.g. bumblebees), honeybees begin foraging at lower temperatures than most other pollinators and have first use of most floral resource. This foraging activity gives the exotic honeybee an advantage in any competitive interaction, especially if rewards are available mostly in the morning before temperature rises (Roubik, 1978). For some plants, honeybees can remove up to 30-90% of the nectar and pollen from flowers before native bees start foraging (Lindenmayer, 2005).
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) suggested that interspecific competition between honeybees and native bees affected the distribution of foragers on flower clusters of various sizes in New York, and was greater in the spring. 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. Moreover, Roubik et al. (1986) have documented a direct competition for pollen or nectar between African honeybees and native stingless bees in Panama. Thomson (2004) in California demonstrated negative effects of non-native honeybees on native bumblebees. She found that foraging rates of Bombus occidentalis colonies were significantly reduced as a result of proximity to honeybee hives the. Schaffer et al. (1979) studied competition among three species of bees (Apis mellifera, Bombus sonorus, and Xylocopa arizonensis) on Agave schottii in several habitats 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. 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. Benest (1976) studied foraging by honeybees and three species of bumblebees in France. Data show bees of the same species foraged together on one flower, but bees avoided mixed-species foraging on the same flower, and honeybees are more tolerant of joint foraging than are bumblebees. Paini etÂ al. (2005) have performed a replicated Before-After Control-Impact (BACI) experiment to study the putative impact of feral honeybees on the reproductive success of an undescribed species of Australian solitary bee (Megachile sp. M323/F367), and they found a large resource overlap occurred between the two species. However, the change in the reproductive success of the native solitary bee Megachile sp was not significant.
EFFECTS ON POPULATION ABUNDANCE
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 an important 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 (Roubik and Wolda, 2001). 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 (Goulson, 2003).
An alternative technique is to study the correlation between patterns of diversity of native bees and abundance of introduced bees without manipulating their distribution. In a study in oceanic islands in the northwest Pacific, Kato (1999) reported that if honeybees were dominant, native bees were rare or absent on islands. Aizen and Feinsinger (1994) related the fragmentation of forests in Argentina with a decrease in indigenous pollinators and an increase in honeybee populations. Thomson (2004) in California found that proximity to honeybee hives significantly reduced reproductive success of Bombus occidentalis colonies. Pleasants (1981) reported negative correlations between Apis and bumblebee abundance. Not all studies, however, support that declines of native bees at the population level can result from the competition with non-native honeybees. 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 with different species of the following genera Andrena, Nomada, Lasioglossum, Sphecodes, and Bombus. 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.
Drawing conclusions from these studies is therefore problematic due to the conflicting results, and the lack of incontrovertible evidence that introduced bees have had a significant impact, through competition, on a population of native pollinators.
The different assessments, by which competition between honeybees and native bees can be measured, such as visitation rates floral resource overlap, and nest sites, are indirect and might not result in a detrimental effect on indigenous bees being detected. Examining these indirect measurements of competition is yet 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 (Paini, 2004) (Fig. 2).
Figure 2. The different measurements that have to be assessed to determine whether competition is occurring between honeybees and native bees. Although all these measurements can be 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 (Paini, 2004).
EFFECTS OF COMPETITION AMONG POLLINATORS ON PLANT POLLINATION AND PLANT PRODUCTIVITY
Many plants that reproduce sexually rely on animals for cross-fertilisation. To achieve successful cross-fertilisation, a plant must receive adequate pollinator visits, quantitatively and qualitatively. For successful pollination, pollinator visits should ideally lead to removal and deposition of a viable, compatible and a sufficient quantity of pollen grains at the proper period of pollination, i.e. the period of stigmatic receptivity. Removal and deposition of pollen, in the animal-pollinated plants, depends mostly on the foraging behaviours of the pollinator (e.g. visitation rate, handling time).
Despite the fact that few studies have been concerned with the impacts of the competition between the animal pollinators on plant reproductive success (Paton, 1993, Carmo et al., 2004), data from several studies, cited above, reported that honeybees have impacts on the foraging behaviours and/or population of other pollinators. Therefore, changes in the foraging behaviours or population size due to presence of the competitor may, in turn, affect pollination and fertilization by modifying plant-pollinator interactions and consequently plant reproduction success. For example Irwin and Brody (1999) found that depletion of floral resources by a nectar-robbing bumble bee, Bombus occidentalis, may change the behaviour of legitimate pollinators, and subsequently, the pollination and fertilization of the plant Ipomopsis aggregata. McDade and Sharon (1980) also reported that nectar robbers have adverse effects on fruit and seed set levels, by damaging plant reproductive structures, Since the effect of the nectar robbers on visitation by pollinators depend upon its impact on the reproductive structures and consequently the availability of floral rewards. Moreover, Reddy (1992) found that pollination and fruit set of 70% of the flowers of Vitex negundo were affected by wasps visitation. Roubik (1982) revealed that robber bees, Trigona ferricauda, aggressively deterred the sole pollinator of Pavonia dasypetala, the hermit hummingbird, leading to a reduction in their visitation, and thus, reduced seed production of the plant. Paton (1993) reported that increasing the number of honeybees competitively excludes the more effective pollinator, honeyeaters, from patches of Callistemon sp. leading to remarkably decreased fruit production. Carmo et al. (2004) reported that introduced honeybees have a detrimental effect on fruit and seed production of a Clusia arrudae tree, although the plant's attractiveness or the resource availability to its native pollinator, Eufriesea nigrohirta, was not affected.
Mechanisms for avoiding interspecific competition
Many authors concur that pollinators use different mechanisms to avoid competition (Pleasants, 1981, Eickwort and Ginsberg, 1980, Walther-Hellwig et al., 2006). Understanding the manner in which pollinators avoid competition will be useful for studying the competition among pollinators. Of the several mechanisms that have been suggested, the following mechanisms for competition avoidance have been well-documented (Palmer et al., 2003).
Environmental Heterogeneity and Trade-Offs
Results from previous experiments suggest that resource partitioning among species may be a common foraging strategy that lessens interspecific competition for resources and facilitates the coexistence of subordinate species (Brown and Wilson, 1956, Pianka, 1973, Friedlaender et al., 2009, Bowers, 1982). Competitors may partition their resources in at least three levels of variation: spatial, temporal, and/or floral. For example, Mayfield (1998) showed experimentally that each one of the two main insect visitors of Chapmannia floridana plant was found to forage on different vegetation densities and sites. In an experiment to determine whether resource utilisation by two species of bumblebees is altered by the presence of the other species, Inouye (1978) reported that each bumblebee species significantly preferred foraging on a different flower species. Heinrich (1976) found that patterns of resource utilization in the guild of bumblebees were associated with differences in the tongue length. Flowers with short corolla were visited mainly by short-tongued bumblebees and less visited by long-tongued one and those with deep corolla were visited primarily by long-tongued bumblebees. Moreover, Graham and Jones (1996) found that, among two species of bumblebees, the larger one, Bombus appositus, were more frequently visiting Delphinium barbeyi while the smaller one, B. flavifrons, preferred Aconitum columbianum. B. appositus gained more nectar from their preferred plant while there was no significant difference in nectar gained by B. flavifrons foraging on either plant. Therefore, they suggested that B. flavifrons were competitively displaced from the other floral resource by B. appositus. Morse (1977) demonstrated that Bombus ternarius workers avoided competition with B. terricola by shifting their foraging location to a distal part of flower clusters. Furthermore, Ginsberg (1983) have found that bee species tend to partition the available floral resources, mainly by foraging at different periods of the season.
Patch Dynamics and Competition-Colonization Trade-Offs
Patch dynamics, in which new patches of a limiting resource are continually being created (e.g. adding new floral resource into territorial habitat, or opening new flowers, in local habitat), are likely to facilitate coexistence within competing species (Kotler et al., 1993, Stanton et al., 2002, Palmer et al., 2003). This may result from differential abilities among species to explore the new resources. For example Roubik (1980) suggested that the relatively larger body size of Africanized honeybee allow them to discover new resource sooner than that of the social stingless bees, Trigona spp. Nagamitsu and Inoue (1997) found a differentiation, among aggressive social bees, in the ability for finding new resource with more aggressive bees discovering new baits slower than the less aggressive species. Furthermore, in a study of comparative foraging behaviour of six stingless bee species Hubbell and Johnson (1978) also found that the rapidity to discover new food was different among species, and it was as follow: Trigona fulviventris > T. silvestriana > T. testaceicornis > T. frontalis > T. buyssoni > T. fuscipennis.
Indirect impacts of honeybees:
TRANSMISSION OF PARASITES OR PATHOGENS TO NATIVE ORGANISMS
Introduced pathogens have been recognized as a significant threat to biodiversity, and are associated with the extinction or dramatic decline of various wildlife populations (Altizer et al., 2003). 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. In honeybees, vertical transmission has been suggested to be the most important route of pathogen infection of new colonies for some parasites, while horizontal transmission is more important for others (Fries and Camazine, 2001). 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, and the same, colonies during foraging, contact with infectious material from the environment, such as flowers (Fries and Camazine, 2001). Due to encounters during foraging, pollinators could run particular risks of acquiring infections if pathogens can be horizontally transmitted through shared use of flowers (Durrer and Schmid-Hempel, 1994).
Species introduced to new regions are likely to transport many pathogens (Torchin et al., 2003). 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 (Goka et al., 2000, Goulson, 2003). 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. Small hive beetles, Aethina tumida, are reported to have been transported into California, North America, with the transport of honeybee hives, where they serve as a potential threat to native bumblebees colonies (Evans et al., 2000). 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. In Europe, bumblebees (Bombus. pascuorum) have 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 (Genersch et al., 2006). 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 of bumblebees (Koppert Biological Systems, 2006). 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 (Goulson, 2003). Table 1 summarises evidence of transmitted pathogens and parasites among Bombus and Apis species.
Table 1. Evidences of transmitted pathogens and parasites among Bombus and Apis species; source: (Stout and Morales, 2009).
* Potential for transmission demonstrated, no evidence of host switch in the wild.
** Commercial colonies.
Honeybees have been shown to display competitive interactions with several bee species for floral resources, such as nectar and pollen. Interspecific competitive 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 (of stored food in other bee nests) may take place under certain conditions. 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 pollinator 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 upon native bee populations. In contrast, Donovan (1980) concluded that introduced bees (leafcutting bees) are attacked by native bee enemies, but that the converse was not reported. However, the absence of experimental evidence does not necessarily mean that populations or ecosystem processes are not affected by introduced species.
In this study I will test the hypothesis that introduced honeybees affect wild pollinators, pollination and plant reproduction by modifying foraging behaviour of wild pollinators through the competition, in order to understand the impacts of competition on ecosystem function and community structure.
Objectives of the work
The overall purpose of this study is to determine the competitive impacts of honeybees (Apis mellifera) on wild pollinators; and the potential impact this may have for the functioning of pollination and plant productivity. A variety of experimental approaches will be used to identify the effects of honeybees on native bee abundance, foraging behaviour and the dynamics of plant pollination.
Examine whether honeybees can transmit pathogens and/or parasites to bumblebees and vice versa. This goal will be achieved by monitoring the bees before and after they interact with each other. Microscopy and molecular techniques, i.e., RT-PCR will be used for this purpose.
In this study I will use greenhouse experiments and field experimental approaches to answer the following questions:
Does the behaviour of bumblebees depend purely on inter-specific competition, or also on intra-specific competition with bumblebees from other nests?
Does experimental increase in the density of honeybees affect bumblebee foraging behaviour?
Does the composition of available flowers (and thus reward availability) affect the interactions between honeybees and bumblebees?
Will competitive interactions between pollinators affect pollination and seed set?
Does proximity to honeybee hives affect wild bees' abundance and foraging behaviours?
Does the proximity to the hives affect pollination services provide by bumblebees?
I will include the following measurements to test the impacts of honeybees on bumblebee foraging behaviour and abundance, as these measurements should be affected as a result of competition (Inouye, 1980, Thomson, 2006, Sampson et al., 2009)
Visitation rates. The total number of pollinators observed for observation period. I will consider a flower to have been visited if a bee is seen to collect pollen and/or nectar from that flower (therefore excluding cases of just landing). Measurements of visitation rates can give valuable insight into the interaction amongst pollinators, and between pollinators, plants and subsequent seed set.
Handling time. The time spent visiting an individual flower. I will measure handling time by direct observation using stopwatch or by filming the bees with a video camera while speaking into the camera tape.
Forager abundance. The mean number of foragers per flower at patch scale, instead of the mean number of foragers per square metre, will be used in analyses of forager abundance. Thus abundance here is not comparable to population size but is a measure of the activities of bees at patch level. I will use data from Apis and Bombus forager abundance to test for a negative correlation between the numbers of Apis and Bombus observed at patch level.
Richness and abundance of foragers at patch level in the field. I will use UV-reflecting pan traps to sample pollinators and/or observe pollinators in patches of flowers directly.
Forager density = (forager abundance)/ (patch size)
Patch size = number of flowers in a patch
Pollen deposition = number of pollen grains deposited on a stigma.
Air temperature and general weather conditions will be considered at the time of observation, because they are likely to influence bee foraging behaviour.
To achieve different assessments of competitive impacts, I will perform two series of experiments. The first series of experiments will be conducted in a greenhouse to assess effects of honeybee density on the bumblebee foraging behaviour based on resource overlap, thus addressing questions 1-4. The second series of experiments will be performed in the field and aim to assess the competitive impacts based on correlations between the abundance of competitor pollinators, Apis and Bombus, thus addressing questions 5 and 6.
Study intra-specific competition
To examine the contribution of intraspecific competition within bumblebees on the changes in their foraging behaviour as a result of competition with honeybees, I will compare the foraging pattern of bumblebees with a gradually increased number of bumblebee hives and without honeybees, with their foraging behaviour when competing with honeybees. This experiment is to ascertain whether the intra-specific competition within bumblebees is a significant force in inter-specific competition with honeybees.
Inter-specific competition (resource overlap) experiments
It has been suggested that resource utilization by one pollinator may change the visitation pattern of the other pollinator (Irwin and Brody, 1999, Strauss and Irwin, 2004). To assess the competitive impacts, based on resource overlap, I will perform manipulative greenhouse experiments and 'Before-After Control-Impact (BACI)' studies in a greenhouse. I will study the foraging behaviour of bumblebees before and after introducing Apis nucleus hives. Then I will gradually increase the Apis populations in the addition treatment by adding new Apis nucleus hives with bumblebees held constant.
Resource overlap and availability measurements
To assess whether resource overlap affects interspecific competition, I will quantify availability of floral resources by measuring the number of the flowers at each patch. Overlap in plant use between Apis and Bombus will be quantified based on observations of plant visits by Apis and Bombus using a percent similarity index, after (Thomson, 2006), as follow: PS=100Ã-Î£ min(Ai,Bi), where Ai and Bi are the proportions of all Apis and all Bombus, respectively, observed visiting species i. PS is an index indicating the degree of overlap use, with 100 representing complete overlap in plant use.
Pollination and seed set affected by intraspecific competition, honeybee density and floral composition
In each of the above experiments (addressing questions 1-3) I will collect stigmas to count pollen deposition and let fruits mature to count seed set for a subset of the focal plants. This will make it possible to assess how pollination and seed set are affected by the factors manipulated in the experiments.
Field experiments on pollinator communities in relation to honeybee densities
For the competitive impacts, based on correlations between the abundance of Apis and Bombus, I will test whether proximity to Apis hives will lead to a corresponding change in Bombus foraging behaviours and forager numbers. I will monitor numbers of Apis and Bombus foragers in a set of floral patches placed along a distance gradient from the Apis hives site in four different directions to reduce the bias of environmental variation, such as wind direction). Since Apis workers have been documented, in general, to forage within a 1-km radius of the hive (Eickwort and Ginsberg, 1980), I will locate the patches at varying distances from the Apis hives with maximum distance 1000 m away. One floral patch will be located at each of five distances away from Apis site in four different directions, for a total of twenty floral patches.
In addition, cluster of pan traps with different colours, matching the colours of the flowers in the plant used in the study will be used, so that the trapped insects are likely to be a visitor to these plants. Pan trap will be placed near each floral patch point. The pans will be filled with water, a few drops of a detergent to reduce surface tension and a small amount of salt to act as a preservative. The traps will be held approximately 0.5 m above the ground. When possible, traps will be emptied every two days. Insects in the traps will be placed in containers containing 70% alcohol for later counting and identification. A cluster of traps will be placed at each floral patch point for a total of twenty clusters. Data from these traps will be used for analysis richness and abundance of bumblebees at the patch level.
Field experiments on pollination and seed set in relation to honeybee densities
One of the consequences of the presence of honeybees is that plants may not receive sufficient quantity of pollen to set seed (Gross, 2001). To determine whether competition between pollinators influences delivering pollination services, pollen grain deposition as a measure of this ecosystem service will be used. Pollen grain deposition will be measured by randomly collecting styles from the flowers from field experiments, stigmas will be removed from the flowers with a fine forceps. The pollen grains on the stigmas will then stained with basic fuchsin gelatin by pressing them into fuchsin gelatin previously melted on a glass slide to squash the stigmas and cover with a cover slip. The number of pollen grains will be counted using a compound microscope. Some flowers will be bagged and left to mature so that seed set can be measured. This technique will be used for addressing question 4 as well.
Research objective and activity
Full time statistics course /
Planting annual plants for greenhouse experiments
Inter-specific competition (greenhouse experiments)
Intra-specific competition (greenhouse experiments)
Pollen deposition counting / Analysis of the data / Pathogens/parasites diagnosis
Prepare field work / Planting annual plants for field experiments
Field (correlation) studies
Sorting of pan trap samples and data analysis