Honey Bees ( Apis mellifera L . ) and Pollination Issues : Current Status , Impacts , and Potential Drivers of Decline

European honey bees (Apis mellifera L.) are important pollinators of many fruits, nuts, vegetables and field crops. Honey bees also pollinate different wild flowering plants and help to maintain the ecosystems. Currently, these pollinators are facing a number of threats including habitat destruction, pesticides, mites, parasites and loss of genetic diversity. Because of the decline in their number, there is a great loss of ecological services which impacts the world’s economy. This review of honey bee and pollination issues highlights the need of protection and conservation of these important pollinators. Research is required to quantify the synergistic effects of potential drivers for current colony loss and to identify the ecotypes and native species of honey bees which are more resistant to pests, pathogens and pesticides.

Flowering plants are very important to wildlife and humankind as they provide food, fiber and shelter (National Research Council, 2007).For the production of seeds, pollination is an essential step in the reproductive process of the world's nearly 300,000 species of flowering plants (Kevan & Viana, 2003).With the exception of grain crops and some vegetables, the major proportion of the global crop production mainly depends on biotic pollination (Klein et al., 2007;Ollerton et al., 2011).Insect mediated pollination provides direct and indirect benefits to human societies (Fisher et al., 2009) because insect pollination contributes to the yields of 75 percent of globally important crop species (Klein et al., 2007) including numerous wild plant species (Ollerton, Winfree, & Tarrant, 2011).One third of the food is derived from plants that are either dependent on or benefit from insect pollination (Oldroyd & Nanork, 2009), especially honey bees (Richards, 2001).
Bees represent the majority of insect pollinators (Kevan & Viana, 2003).There are about 17,000 described and 20,000 to 30,000 total estimated bee species in the world (National Research Council, 2007).The Food and Agriculture Organisation of the United Nations (FAO) estimates that out of some 100 crop species which provide 90% of food worldwide, 71 are bee-pollinated (http://www.fao.org/ag/magazine/0512sp1.htm).The European honey bee (Apis mellifera L.) is an important species of bees which pollinates a number of agricultural crops worldwide (Le Conte & Navajas, 2008;Klein et al., 2007;Rader et al., 2009) and have often been credited with pollination services that are actually performed by other bee species also (Parker, Batra, & Tependino, 1987;Richards, 1996).The role played by honey bees as pollinators also contributes to maintain biodiversity because there is a positive correlation between plant diversity and pollinator diversity (Heithaus, 1974;Del Moral & Standley, 1979).European honey bees have been managed along with other bees like eastern honey bees (Apis cerana F.), bumble bees such as Bombus terrestris L., solitary gregarious species such as leafcutter bees (Megachile rotundata F.) and mason bees (Osmia spp.) for crop pollination (Delaplane & Mayer, 2000).Wild and managed pollinators may have complementary behavioural relationships thus increasing the efficiency of pollination (Klein, Steffan-Dwenter, & Tscharntke, 2003) because the pollination by wild pollinators may be as important as that of managed pollinators for agricultural production (Veddeler, Olschewski, Tscharntke, & Klein, 2008;Klein, Steffan-Dwenter, & Tscharntke, 2003).
By collecting pollen and nectar from flowers, honey bees transfer pollen of most of the world's plants, providing an economically valuable pollination service to crops.According to Gallai, Salles, Settele, and Vaissiere (2009), the contribution of bees (mainly honey bees) and other insects to worldwide crop production for human food is about $190 billion each year as honey bees pollinate different types of crops (Table 1).The United States Department of Agriculture (USDA) also reports that honey bees provide pollination services for a number of food crops like almonds, apples, grapefruits, soybeans, strawberries (Del Moral & Standley, 1979;Williams, 1994).The bee pollinated agricultural crops, fruits and vegetables are valued at USD 20 billion a year in North America (Gallai, Salles, Settele, & Vaissiere, 2009;Klein et al., 2007;Morse & Calderone, 2000).Estimates by Canadian researchers on the annual value of honey bee pollination to Canadian agriculture have ranged from CAD 443 million to 1.2 billion (~ USD 413 million-1.12billion; Winston & Scott, 1984).In Australia, the annual benefits amounted to AUD 156 million (~ USD 147 million; Gill, 1990) while in US, benefits were estimated at USD 1.6 to 40 billion (Levin, 1983;Robinson, Nowogrodzki, & Morse, 1989;Morse & Calderone, 2000;E. E. Southwick & Jr L. Southwick, 1992).Source: Modified from Gill (1990).

Current Status and Trends of Honey Bee Loss
The number of honey bees is decreasing showing a trend towards future pollinator shortage (Bauer & Wing, 2010).In an effort to increase crop yield, honeybees, bumblebees and a few other bee species are purchased or rented by farmers in many countries (McGregor, 1976;Free, 1970;Olmstead & Wooten, 1987;Robinson, Nowogrodzki, & Morse, 1989;Dag, Zipori, & Pleser, 2006).

Impacts of Honey Bee Decline on Ecology and Economy
Honey bees as pollinators play an important role in maintaining an ecosystem, when we lose these pollinators, it leads to the collapse of other ecological components (Kearns & Inouye, 1997).Honey bees remain the most important managed pollinators for most crop monocultures worldwide (McGregor, 1976;Delaplane & Mayer, 2000).The effect of these pollinators decline is associated with decreased crop production (Bauer & Wing, 2010) leading to the loss in ecological components and economy.The ongoing trend of honey bee decline throughout the world have brought attention to the world food security (Westerkamp & Gottsberger, 2002;Holden, 2006).The reports of pollinator crisis are mainly the declines of crop-pollinating honey bees in North America, and bumble bees and butterflies in Europe (Ghazoul, 2005) which have been shown by the reports of decreased production of world's crops.In addition to pollination, honey bees also provide benefits for the plants they visit by the deposition of available nitrogen from their frass during foraging (Mishra, Alfik, Cabrea, Delaplane, & Mowrer, 2013) and they do not show any detrimental impacts on population abundances of any native animals or

Countries
plants (Huryn, 1997).They contribute to the biodiversity of many ecosystems while pollinating a variety of wild flowers (Corbet, Williams, & Osborne, 1991).The International Union for Conservation of Nature (IUCN) predicts a global loss of 20,000 flowering plant species within the next few decades; which will lead to the decline of the dependent pollinators like honey bees (Heywood, 1995).Also, the pollinator loss ultimately results in the decline of plant biodiversity (Biesmeijer et al., 2006;Thomas et al., 2004;Carvell et al., 2006, Pauw & Hawkins, 2011).Now, many nations are concerned about the recent declines of these pollinators.The global pollination crisis currently threatens agricultural productivity and has drawn intense interest among scientists, politicians, and the general public (Aizen, Garibaldi, Cumningham, & Klein, 2008;Holden, 2006).The farmers are aware of the economic benefit of honey bees pollination and they have started for colony rental of honey bees in the US (Sumner & Boriss, 2006) and Europe (Carreck, Williams, & Little, 1997).Because of their reduced number, the prices of honey bee colony rentals for pollination services are growing dramatically over the last few years (Burgett, Daberkow, Rucker, & Thurman, 2010;Caron, 2010).
The trend of declining honey bee shows that the value of pollination services has been significantly higher than current market prices for commercial pollination (Allsopp, De Lange, & Veldtman, 2008).Current decline in honey bees and other pollinators could seriously threaten the continued production of insect pollinated crops (Calderone, 2012).Hence, they are vital for economic benefits derived from sustainable agriculture and for food security.The current decline of honey bee populations emphasize the need to assess the potential loss in terms of economic value that may result from this trend.As a consequence of these pollinators decline, there will be a direct impact on economic losses by reduced crop yields as well as the lower productivity in the ecosystems.The main reason for crop yield reduction is due to pollinator's scarcity in combination with other environmental factors leading to reduced production of fruits, vegetables and nuts (Table 2).Source: Bauer and Wing (2010).

Potential Drivers of Honey Bees Declines
Recently the honey bees' population is decreasing rapidly which may be due to agricultural intensification, habitat alteration or fragmentation, pathogens, lack of nutrition, pesticides and the loss of genetic diversity (van Engelsdorp & Meixner, 2010;Cunningham, 2000;Kearns & Inouye, 1997;Ingram, Nabhan, & Buchmann, 1996;Cane, 2001).Still no records have been reported on the impacts of anthropogenic disturbances on honey bee abundance and species richness (Steffan-Dewenter, Potts, & Packer, 2005;Winfree, Aguilar, Vazquez, LeBuhn, & Aizen, 2009).Environmental factors like weather conditions, availability of nesting sites, food sources and chronic exposure to insecticides might cause CCD-like symptoms (Oldroyd, 2007).Similarly, the pathogens and parasites which have been demonstrated to be involved in colony losses in different regions of the world are considered current threats to honey bees and beekeeping (Genersch, 2010b).The possible causes of honey bee decline are as follows;

Habitat Fragmentation, Loss and Degradation
Degradation and discontinuity of habitats are responsible for changing pollinator populations (Thomas et al., 2004) because these activities cause genetic erosion by reducing gene flow and increase the chance of populations and species extinction (Barrett, Kohn, Falk, & Holsinger, 1991).Naug (2009) reported that nutritional stress due to habitat loss and foraging resources cause diseases and stress on honey bees and may cause collapse of colonies.Fragmentation and degradation of habitats can be detrimental to bee populations including honey bees (Rathcke, 1993;Kremen, Williams, & Thorp, 2002;Steffan-Dewenter, Klein, Gaebele, Alfert, & Tscharntke, 2006;Cane, Minckley, Kervin, Roulston, & Williams, 2006) due to the loss or dissociation of important resources for food and nesting (Hines & Hendrix, 2005;Potts et al., 2005).Habitat loss might be one of the biggest factors impacting honey bee declines and the agricultural landscape changes after the Second World War (Winfree, Aguilar, Vazquez, LeBuhn, & Aizen, 2009).Although, the pollinators including honey bees have been affected negatively with the loss of habitats when the proportion of semi-natural areas have decreased (Kremen, Williams, Bugg, Fay, & Thorp, 2004), there are no more reports of honey bee colony loss due to habitat loss.So, the loss in habitat is not a major driver for the recent colony loss.
It appears that Varroa acts both as disseminator and activator of some viruses like acute bee paralysis virus (ABPV), Kashmir bee virus (KBV) and Israeli acute paralysis virus (IAPV).Deformed wing virus (DWV) is a member of the Iflaviridae family and appears not only to be vectored by Varroa but also to replicate within the mite (Genersch & Aubert, 2010).DWV mainly causes covert, symptomless infections (Hails, Ball, & Genersch, 2008) and is transmitted vertically through drones and queens or horizontally through larval food (De Miranda & Fries, 2008;Yue, Schroder, Gisder, & Genersch, 2007).When transmitted to pupae through V. destructor, it causes infection resulting mainly deformed wings with other effects like shortened and bloated abdomen (Ball & Allen, 1988;Bowen-Walker, Martin, & Gunn, 1999;Yang & Cox-Foster, 2007) leading to the death of bees within less than 67 h after emergence (Yang & Cox-Foster, 2007).DWV has been reported as a potential cause for colony loss because it can act independently of Varroa mites (Highfield et al., 2009).Di Prisco et al. (2011) showed that the low temperature of winter increased the virus infection in honey bees and that the severity of DWV infection was positively correlated with V. destructor density.They also showed that host conditions are important on outcome of DWV showing honey bee morality rate.
IAPV has been identified as a marker or secondary agent of CCD (Cox-Foster & van Engelsdorp, 2009) and anti-viral treatment using IAPV-specific RNAi was able to silence IAPV and to reduce the symptoms of CCD (Maori et al., 2009).IAPV is prevalent in the Middle East, Australia and the USA but less frequently found in Europe (De Miranda, Cordoni, & Budge, 2010).Because of this, IAPV has been found to be associated with colony losses in USA (Cox-Foster et al., 2007) but so far not in Europe (Genersch, 2010b).The DWV should be considered as a major virus causing the loss of honey bee colonies.

Bacterial Pathogens
There are two main bacterial pathogens of honey bees and both are pathogenic to larvae but not to adult bees: Melissococcus plutonius, causing European Foulbrood (Bailey, 1956(Bailey, , 1957) ) and Paenibacillus larvae, causing American Foulbrood (Genersch et al., 2006;Genersch, 2010a).P. larvae is a spore forming bacteria which makes control more difficult than M. plutonius, which is not a spore forming bacterium.The bacteria enter the larvae through ingestion and proliferate in the larval midgut, assimilating much of the larval food and the infected larvae die from starvation (Bailey, 1983).There are few reports of colony loss due to bacterial pathogens around the world.

1) American Foulbrood
American foulbrood (AFB) is a bacterial disease of the bee brood.It is a notifiable disease in many countries.It is highly contagious, easily and rapidly spread within a colony and among colonies.Such colonies with AFB should be destroyed to prevent the disease from spreading further.AFB has had the greatest impact on the apiary industry.In 2000, the annual economic loss attributed to AFB infection in the US was $5 million (Eischen, Graham & Cox, 2005).It is considered to be more virulent than European foulbrood.

2) European Foulbrood
European foulbrood (EFB) has been reported from across every continent that honey bees inhabit (Matheson, 1993) and currently appears particularly prevalent and dramatically increasing in the UK (Wilkins, Brown, & Cuthbertson, 2007;Tomkies et al., 2009) and Switzerland (Forsgren, 2010;Belloy et al., 2007;Roetschi, Berthoud, Kuhn, & Imdorf, 2008).The bacteria cause the asymptomatic colonization of honey bee at first, until the time bees start to show symptoms of infections.Later on, bee larva die due to infection (Mckee, Goodman, & Hornitzky, 2004).EFB has not been reported from different countries and thus it is not believed to be a major factor to explain widespread colony loss.

Parasites 1) Varroa mite
Varroa mites could be the main reason for recent decline of honey bee colonies (Guzman-Novoa et al., 2010).V. destructor, causes a disease of honey bees called varrosis (Carreck, Ball, & Martin, 2010;Dahle, 2010;Martin, Ball, & Carreck, 2010) which appears from autumn to early spring during the overwintering phase.It causes general weakening and often complete losses of colonies.It is also a vector of a number of viruses which affect honey bee health and shorten the lives of infected bees under certain conditions.V. destructor does not have any free living life stages and completes all the life stages on honey bees.When a bee has been infested by this ectoparasite, it takes a longer time to return or even does not return to the colony (Kralj, Brockmann, Fuchs, & Tautz, 2007;Kralj & Fuchs, 2006).The V. destructor mite has an impact on the bee's immune system and on the susceptibility of honey bees towards various pathogens (Gregory, Evans, Rinderer, & De Guzman, 2005;Yang & Cox-Foster, 2005).V. destructor has been found to be responsible for colony losses especially in combination with virus infections (Ball, 1983;Ball & Allen, 1988;Delaplane & Hood, 1999;Hung, Adams, & Shimanuki, 1995;Martin, 2001;Todd, De Miranda, & Ball, 2007).So, V. destructor is responsible for the colony loss of A. mellifera.

Pesticides
There are different pesticides and other chemicals which can poison the honey bees influencing their health.These chemicals also affect plants in their productivity and eliminate nectar sources for pollinators and also deplete nesting materials (mainly flowers) for honey bees (Nabhan & Buchmann, 1996).The pesticides mainly neonicotinoids are responsible for the possible decline of honey bees (Cresswell & Thompson, 2012;Bernal et al., 2010).Neonicotinoids cause toxic effects as well as synergistically reinforce infectious agents such as N. ceranae which together can produce colony collapse (van der Sluijs et al., 2013).However, in some countries neonicotinoids are not regarded as the major risk factors associated with current colony losses (Fairbrother, Purdy, Anderson, & Fell, 2014) because there are no direct links between neonicotinoids and CCD (Hopwood et al., 2012).Also, dietary neonicotinoids do not cause the honey bee declines (Cresswell & Thompson, 2012).
In addition to neonicotinoids, other pesticides are also found to have negative effect on health of honey bees.Increased probability of Nosema infection was reported in bees that consumed pollen with a higher fungicide load (Pettis, Lichtenberg, Andree, Stitzinger, & Rose, 2013).Likewise, the residues of insecticide imidacloprid in nectar and pollen at high levels may be dangerous to bees (Laurent & Rathahao, 2003;Chauzat et al., 2006).Widespread losses of colonies in France is due to imidacloprid (Laurent & Rathahao, 2003).Similarly, other pesticides "acaricides" have also been found harmful for bees' health (Harz, Muller, & Rademacher, 2010).The acaricidal substances that were intentionally brought into the hives to control V. destructor are the most reported pesticides residues in honey bee colonies (Chauzat et al., 2006;Mullin et al., 2010;Johnson, Ellis, Mulli, & Frazier, 2010;Bernal et al., 2010).In most of the cases, the major pesticide contaminants in hives are the ones used by beekeepers and their residues have shown a number of sub lethal effects.The sub lethal effects of pesticides can have indirect effects including on foraging activity (Wu, Anelli, & Sheppard, 2011).
In Europe, a proposed pesticide ban has gathered scientific support with some additional field studies (Cressey, 2013).Pesticides and the techniques to use them represent one of the major uncertainties around the decline in honey bee numbers (Maini, Medrzycki, & Porrini, 2010).Some pesticides cause a wide range of sub lethal effects on honey bees with different traits and severities.It is difficult to observe sub lethal effects of pesticides on the health of honey bee colonies.The sub lethal pesticide residue concentrations found in nectar, pollen and bee bread are considered a potential factor resulting in delayed adverse effects on bee health (Chauzat et al., 2010).However, Bernal et al. (2010) found no correlation between sub lethal levels of pesticide residues in bee hives and colony mortality.There are major weaknesses of regulatory risk assessment and marketing authorisation of pesticides, particularly for neonicotinoids (Maxim & van der Sluijs, 2013).
In addition, there are reports of spray applications of pesticides in different countries, usually due to misuse of products, resulting in the contamination of nectar and pollen (Barnett, Charlton, & Fletcher, 2007;Thompson & Thorbahn, 2010).Exposure to neurotoxicants like imidacloprid in honey bee and their role with CCD remains to be determined (Mullin et al., 2010).Further field research would be needed to determine the sub lethal effects of neonicotinoids in bee health.

Diet and Honey Bees
Nutrition plays an important role to maintain the health and honey bee colonies (Brodschneider & Crailsheim, 2010).If honey bees have difficulty accessing sufficient pollen sources for all their essential amino acids they may be weakened and make them be more vulnerable to various pathogens and diseases.To maintain health, foraging bees need a variety of sources of natural nectar and pollen to prevent nutritional deficiency and to strengthen immune defences (Brodschneider & Crailsheim, 2010;Alaux, Ducloz, Crauser, & Le Conte, 2010;Pedersen & Omholt, 1993).Protection programs aimed at maintaining or enhancing plant diversity may help to provide better forage to bees and reduce the risk of malnutrition.

Relationship of Genetically Modified (GM) Crops and Honey Bee Decline
Initially the development of Genetically Modified Organisms (GMOs) was aimed to prevent the plants against the potentially adverse effects of pesticides and pests.The GMO crops with insecticidal properties could have a negative, sub-lethal, effect on bees.However, this concern of negative effect of GMOs have not been verified (Marvier, McCreedy, Regetz, & Kareiva, 2007;Duan, Marvier, Huesing, Dively, & Huang, 2008).The worker bees and colonies fed pollen from genetically modified Bacillus thuringiensis (Bt) corn did not have increased rates of mortality (Rose, Dively, & Pettis, 2007).To date, no strong evidence exists that GM crops cause acute toxicity to honey bees (Huang, Hanley, Pett, Langenberger, & Duan, 2004).

Weather and Climate in Honey Bee Decline
Climate variations have an important role for bee colonies.Extended periods of cold, rainy, and hot weather have been reported on severe, often unexplained, honey bee mortality in the past (Kauffeld, Everitt, & Taylor, 1976).Beekeepers also reported severe winter weather to be responsible for winter mortality in the US (van Engelsdorp, Hayes, Underwood, & Pettis, 2008).Weather might be important for colony productivity as higher temperatures tend to increase colony productivity because of reduced metabolic demands on foragers (Harrison & Fewell, 2002).The long periods of high temperatures and sufficient precipitation are both correlated to increased nectar production (Shuel, 1992), which in turn translates to increased colony productivity (Voorhies, Todd, & Galbraith, 1933).Mainly, the severe winter weather is found for colony mortality.

Loss of Genetic Diversity
Honey bee genetic diversity derives from multiple mating of a single queen with multiple males (polyandry).At the colony level, genetic variability has been shown to be important for disease resistance, homeostasis, thermoregulation and overall colony fitness (Tarpy, 2003;Jones, Myerscough, Graham, & Oldroyd, 2004;Graham, Myerscough, Jones, & Oldroyd, 2006;Mattila & Seeley, 2007).About 26 subspecies and numerous ecotypes of western honey bees (Apis mellifera) have been described, based upon behaviour, morphology, and molecular evidence and are grouped into five evolutionary lineages: A from Africa, C from the northern Mediterranean region and eastern Europe, M from northern and western Europe, O from the eastern Mediterranean and the Near and Middle East region, and Y from the east African country Ethiopia (Ruttner, 1988;Sheppard & Meixner, 2003).The performance of colonies in a number of resistance traits against pest, parasites and diseases may be considered for apicultural interest (Meixner et al., 2010).Recent researches increasingly bring the development of traits related to colony vitality into focus which have introduced and evaluated additional traits related to colony vitality, such as hygienic behaviour, mite infestation development and overwintering ability.To increase genetic diversity, several European countries, especially those with a tradition in the production of the commercially most desirable races (A. m. ligustica and A. m. carnica), have coordinated national breeding schemes.From these programs, thousands of queens are produced and exported across Europe and the world (Lodesani & Costa, 2003).The genetic variability of the US honey bee population is reduced compared to that of indigenous honey bee populations of Europe (Sheppard, 1988).In addition, it has been reported that as few as 500 breeder queens have been used to provide progeny for most of the commercial hives present in the US (Schiff & Sheppard, 1995;Delaney, Meixner, Schiff, & Sheppard, 2009).Lack of genetic diversity may be responsible for colony losses as the genetic similarity among colonies in wide areas increases the chances of successful disease transmission.

Other Factors Associated with Honey Bee Decline
In addition to the above mentioned drivers, there are other drivers like parasites, predators and competition from invasive non-native species of animals and plants in specific location.Ravoet et al. (2013) reported that the presence of the parasite Crithidia mellificae (Phylum-Euglenozoa and Class-Kinetoplastea) has effects on winter colony mortality.Sometimes, the environmental stresses may also be responsible for the decline of honey bees.
The exotic plants and land-use negatively affect specialized plant-pollinator interactions (Grass, Berens, Peter, & Farwig, 2013).Invasive alien species of plants and insects, may have effects on native honey bees worldwide (Stout & Morales, 2009).There is a need to determine the impacts of invasive animals, plants, parasites and pathogens on native honey bees.

Conclusion and Future Directions
The recent declines of honey bees can result in loss of pollination services leading to ecological and economic impacts.Due to the recent loss in these important pollinators, there is a need of some mitigation strategies for their loss and associated risks.The use of pesticides has a pronounced effects on bee health and colony populations.Additional factors like viruses, parasites, pathogens and lack of genetic diversity have remarkable effects on declining recent honey bee populations.These diverse threats to honey bees might interact and produce synergistic effects.
To reduce the ecological damage and loss, an understanding of the commercial and pollination needs of each country is needed to enable for pollination services which helps to maintain a sustainable level and reduce the risk of crop loss.Farmers can also practice agricultural techniques which can provide non-toxic methods of weed and pest control thus preventing the honey bees from harmful effects of pesticides and chemicals.Also, continued research in identifying the disease resistant ecotypes of honey bee is essential.

Figure 2 .
Figure 2. Percentage of colony winter losses in 2009/2010 in several countries (Cited from Van der Zee et al., 2012)

Table 1 .
Crops dependent on bee pollination

Table 2 .
Percent change (negative) in value of production of select crop sectors due to global pollinator loss