Abstract:

This review examines current issues surrounding global Anthophila (bee) populations. It explores the dangers of commercially managed hives to replace wild pollinators. Apis mellifera (European honeybee) and Bombus terrestris (buff-tailed bumblebee) are the preferred species for commercial use (crop pollination), hobbyist apiaries and bee produced goods. These uses have devastated biodiversity. This review evaluates the causes of wild pollinator decline and disease and parasite transmission inter and intraspecifcally between species. Studies referenced emphasise the disturbing effects that follow the introduction of commercial hives, for example, the extinction of certain species. This review also highlights the need for further research into the ability of solitary bee species to act as pathogen reservoirs. It discusses solutions for wild pollinator decline, which includes reducing usage and transportation of commercial hives and ensuring more rigorous parasite and infection screening of colonies. This should prevent new habitats being overwhelmed by invasive diseases and parasites.

Introduction:

Anthophila (bees) are facing numerous problems contributing to large population declines. Several anthropogenic factors have been linked to decline, including habitat fragmentation, climate change, agricultural intensification, increased use of pesticides/acaricides, inadequate nutrition and the introduction of invasive species/pests (Goulson, Nicholls, 2022). There is a prominent focus placed on the plight of the Apis mellifera (European honeybee) alongside Bombus terrestris (commonly known as a buff-tailed bumblebee). Globally, these are the most common for commercial honey and hobbyist beekeeping, crop pollination, and are present in most terrestrial ecosystems (Khalifa et al., 2021). These types of bees are easily artificially managed and cultivated, making them a quick fix solution to global pollinator declines. Commercial hives are used globally to replace the loss of native pollinators (including insect species) (Carvalheiro et al., 2013). Hence, these hives become “Massively Introduced Managed Species” (MIMS). Solitary bees have an equally important role in pollination as A. mellifera, and collectively make up a greater proportion of the world’s bee species (Peters et al., 2017). A large percentage of alternative pollinators receive much less research focus than MIMS. The increased use of commercial MIMS and bee products has created a rapid and disturbing spread of diseases and pests. Consequentially, commercial MIMS increase the stress on wild colonies and can lead to pathogen spill over. This is when transmission occurs via a “reservoir population” as opposed to within the “host population” (Alger et al., 2019). For example, transmission from A. mellifera to a solitary bee species back to A. mellifera. These inter and intraspecific transmission of diseases that will be discussed include, Varroa mites and Deformed Wing Virus (DWV), Chronic Bee Paralysis Virus (CBPV), Nosemi thomsoni, Crithidai Bombi, Apicystis Bombi, and Chaetodactylus krombeini.

Honeybees:

Honeybees are eusocial insects that communicate through pheromones and physical movements. They live in colonies with a strict hierarchical structure. Worker bees perform all tasks except laying brood and mating with the queen (Flanders, 1960). In the hive there is constant contact with other bees allowing easy vectoral transmission of diseases and pests (Gould, 1974). When bees forage for pollen and water it allows diseases to spread to neighbouring hives. For solitary bees, transmission would be harder due to fewer interactions with different bees and species. This review will look at the transmission of A.mellifera diseases and parasites to wild populations of bee species.

Chronic Bee Paralysis Virus (CBPV):

A. mellifera intraspecifically spread CBPV between wild and managed colonies. The virus is transmitted orally through bee faeces remaining at the bottom of the hive or through brushing against the furry legs of other bees, then being ingested (Bailey, 1965). Within five days of infection, bees become symptomatic and die shortly afterwards. This virus mainly affects adult bees but can be contracted in the early developmental brood stages. Bailey et al (1968) showed that young bees tend to have a much lower viral load and therefore, are less likely to die due to CBPV infection. This experiment was performed by the identical team as in 1963 and was a second attempt, as initially the virus was too dilute to prove conclusive results (Bailey et al., 1963). This study rectified the mistakes, increasing accuracy. CBPV symptoms include issues with memory, motor control, behaviour, body orientation, and sensory processing. The irreversible damage leads to colonies being unable to perform daily tasks which can be a factor leading to colony collapse (Budge et al., 2020).

As the virus is highly contagious it is easily spread from commercial hives to wild colonies. Budge et al (2020) showed artificially managed colonies had twice the prevalence of disease within their hives. CBPV was recorded once in 2007 in one English county, yet by 2017 it was documented in “39 of the 47 English counties” and “6 of the 8 Welsh counties” (Budge et al., 2020). This emphasises the dangers of MIMS and artificially managed hives being used commercially. Porrini et al. (2016) showed CBPV to be one of the most prevalent diseases in Italian beehives that, combined with the toxic effects of pesticides, created colony collapses. However, this research had low generalisability to hives outside of Europe. Although no one single factor contributed to the colony collapse, CBPV “significantly influenced mortality” (Porrini et al., 2016). This highlights CBPV is spread by these MIMS and its consequences for wild populations. Hence, it is important to prevent the virus being spread further through transporting commercial hives and should be rigorously screened for.

Varroa:

A highly common honeybee pest is the mite Varroa destructor, which is being rapidly spread to other populations. This ectoparasite has two haplotypes, the Korean and Japanese. The more common Korean haplotype exists in Europe, Asia, Africa, the Americas, and the middle East (Le conte et al., 2010). Although there are five known types of mites, only V. destructor has spread from Apis cerena to A. mellifera. The mites feed on the fat body cells of adult and developing bees (Ramsey et al., 2019). This highly infectious mite also carries DWV. The virus can be transmitted through its vector, V. destructor, and orally through infected faeces. It causes wing deformities and pupal deaths preventing hives from functioning. Both field and laboratory experiments showed mite infestations combined with DWV made the bees more susceptible to negative effects from the 5 insecticides used. The study used methodological triangulation thereby, increasing ecological validity. Miranda and Genersch (2009) showed that without the presence of V.destructor, DWV infection does not result in any apparent negative impacts. Yet with mites present and DWV infection there is a 90-95% chance the colony will die within 2 years. Zhu et al. (2022) proved that mite intensity grew as the season progressed and with increased interaction between bees, showing it is highly dangerous for eusocial hives. This study proves that proximity affects transmission rates. Transmission of viruses occurs from artificially cultivated and managed honeybee hives (which are treated with oxalic acid as a parasite resistance) into wild bumblebee populations. These have no help against the parasite and thus is more fatal.

DWV was first detected in commercial hives of B. terrestris (Genersch et al., 2006). Both bees and pollen collected from flowering plants in the U.S reported detection of RNA viruses (including DWV) even in the pollen of uninfected bees. Interspecific transmission is thus possible, but pollen may also harbour viruses (Singh et al., 2010). The study was limited, as how the pollen sources were infected was indeterminable. Furst and Brown (2014) showed that across 26 sites in the UK, 11% of bumblebee hives had contracted the virus and a third of those had the virus replicating. The virus is probably much more prevalent as some fatalities weren’t reported in the study’s results, which was a limiting factor. B. terrestris hives contain fewer worker bees than A. mellifera. This combined with the DWV may cause a large reduction in the typical lifespan, from 21 days to around 6 days. Hence, colonies may be unable to gather enough food and water meaning they starve to death. As DWV has no cure, much stricter regulations need to be placed on commercial hives who are the main vector of the virus.

Nosema thomsoni:

Another common A. mellifera transmission is Nosema thomsoni which is spreading into populations of solitary bees. It is now recognized as a “highly reduced lineage of fungi” (Adl, et al., 2005). These symbionts infect the midgut of bees, injecting cellular matter into the host cell whereby phagocytosis, consumes the host cell’s contents. After laying down a spore wall, it ruptures the cell and unleashes spores (Gisder et al., 2011). These spores are highly infectious and transmitted through faeces to infect other cells in the bee’s digestive tract. The spores contaminate pollen and floral reserves through the faeces of foraging bees. This fungus is dangerous due to the bees’ large foraging distances, so the pathogen load of the fungus is dispersed to novel habitats and hosts (Grupe and Quandt, 2020). The transmission of this fungus has been recorded between A. mellifera and Andrena vaga with critical consequences. The fungus causes lethargy, mortality, reduced homing ability, shorter foraging flights, and inefficient foraging behaviour. This is more dangerous for solitary bees who rely entirely on their own efforts for survival as opposed to a hive of eusocial honeybees who can rely on other workers. Ravoet et al. (2014) in Belgium found a microsporidium in A. vaga that very closely resembled N. thomsoni indicating transmission from the surrounding commercial hives. This study also showed that solitary bee species act as reservoirs for Apis pathogens. The microsporidium was likely N. thomsoni yet there was a 0.2% chance this could be a different pathogen. This problem of N. thomsoni is accentuated through the use and dispersal of commercial hives and their products e.g., pollen. (Periera et al., 2019).

Bumblebees:

Another bee species commonly used in commercial hives is B. terrestris. Although Apis are incredibly important pollinators, there are plant species which require different forms of pollination. The most famous example is tomato species which require buzz pollination to release their pollen (Rosi-Denadai et al., 2018). They are excellent pollinators for soft fruits as they can forage in colder weather which is valuable for commercial farming. However, importing these MIMS has created a swarm of problems for the wild colonies in surrounding habitats (Geslin et al., 2017). This section of the review will discuss the problems associated with the use of commercial colonies of Bombus.

Crithidai bombi:

One parasite passed intraspecifically from commercially used bumblebees is Crithidai bombi. C. bombi is a trypanosome parasite which infects the digestive tract of bees and invades the epithelium (Pham and Schneider, 2008). They are transmitted via ingestion of contaminated faeces and passed as cyst matter. Brown et al. (2003) found that B. terrestris had a 50% increase in mortality as although C. bombi is usually benign, when in starvation conditions has detrimental effects on their immune systems. This was supported by prior work of Schmid-Hempel (1998). The introduction of commercial hives is often followed by starvation conditions in wild populations. This is especially problematic as it means that the few pollen resources available will be highly competitive, thus increasing the rate of transmission. The problem of rapid transmission has only been accelerated by the transportation of MIMS. Graystock et al (2013) looked at the parasitic rates of commercial B. terrestris and showed that 25% of the commercial hives contained infections of Crithidai spp (there are two species) alongside other parasites (e.g. Nosema bombi). Out of these colonies 77% had at least one parasite infection. This study was important as it proved that bees being sold as “parasite free” still had high levels of infection and suggested solutions to combat this. These commercially cultivated hives create pathogen spill-over into wild colonies. Otterstatter and Thomson (2008) proved that the parasitic infections of wild Bombus species and even wild A. mellifera colonies increased the closer the foraging sites were to the location of the commercial hives. These unregulated MIMS have caused drastic population declines in wild colonies and need much more rigorous screening of parasitic infection alongside preventing overlap with “wild congeners” (Otterstatter and Thompson, 2008).

Apicystis bombi:

Another problem from MIMS that infects the Bombus spp is Apicystis bombi. This protozoan, parasitic alveolate is transmitted through oocysts in the faeces of bees (Lipa and Triggiani, 1996). Once orally ingested the oocysts migrate to the intestine where they become sporozoites and eventually end up in the fat body cells where they reproduce. A. bombi is highly pathogenic causing increased worker mortality and sucrose sensitivity. Graystock et al (2015) showed that fifteen days after artificial infection of A. bombi, 22% of bees had died. This research proved the alveolate had both lethal and sublethal effects on B. terrestris hives. Moreover, Rutrecht and Brown (2008) proved that after infection of A. bombi, queen bees had a significantly lower survival rate after the hibernation period. As only the queen bee can lay brood to regrow the hive, it can devastate the hive. However, this experiment had low ecological validity by using a laboratory setting which may have increased stress, thus increasing the parasite’s pathogenicity. The parasite is believed to have been rapidly spread from Europe through commercially cultivated hives of Bombus lucorum (white-tailed bumble bees) and B. terrestris transported into Chile and laterally to the rest of South America. Commercial B. lucorum and B. terrestris hives were introduced into Chile in 1997 to pollinate crops (Plischuk, Lange, 2009). This section discusses the interspecies transmission from commercial B. lucorum to wild colonies of A. mellifera. Since their introduction many species of bees have had population declines including the disappearance of the native Bombus dahlbomii (giant bumble bee) (Morales et al., 2013).

Due to the MIMS escaping from Chilean greenhouses there has been pathogen spill-over into many other species of bees including local A. mellifera in Patagonia. This neogregarine was previously considered as a low prevalence parasite for Bombus spp. Morales et al. (2013) suggested that only 1-8% of B. terrestris and B. lucorum in Europe will be infected with this deadly parasite. However, in Patagonia the parasite has thrived, infecting almost half of the B. locurum. Plischuk et al (2011) showed that infections of A. bombi in A. mellifera increased from 7.6% in 2009 to 13.6% in 2010. This alarming increase shows that preventative measures are required to stop the interspecies spread of the deadly parasite and further highlights the dangers of transporting commercial hives.

Solitary bees:

There is a gap in the literature as to whether these pathogens can be transmitted to and from solitary bees. Solitary bees such as Osmia cornifrons have been used commercially to increase pollination rate for Brassicaceae and Rosaceae plants. After the introduction of O. cornifrons alongside another species of Asian mason bee, LeCroy et al. (2020) showed a serious decline in the population numbers of six other native mason bee species. However, a limitation was the study did not exclude climatic change as a variable for population decline. This may be down to two reasons. Firstly, O. cornifrons has been linked to the parasite Chaetodactylus krombeini which is transmitted hive to hive by adult O. cornifronswhen walking past nest entrances and through emergency holes (Park et al., 2009). These dangerous mites when introduced into novel environments with no natural predators and favourable conditions can proliferate. These pollen mites have both mobile and immobile phases increasing the ability for transmission. Secondly, not only do these MIMS introduce new sources of diseases and parasites, but they also increase the competition for local resources making the surrounding solitary bees more food stressed (Ravoet et al., 2014). Thus, making them more susceptible to further diseases and side effects from pesticides/insecticides. However, there is very little research on the effects of using solitary bees commercially and the impacts commercial hives have on solitary bees.

One potential reason for the gap in literature is the bias towards significant results. Also, it may be that honey and bumble bees are only able to transmit diseases easily to each other due to being somewhat closely phylogenetically related. Hence, solitary bees which are “further away” in relatedness, may be less at risk. However, this topic needs more thorough research as there are examples where they can act as reservoirs for honey and bumble bee pathogens (Ngor et al., 2020). A second reason may be that when solitary bees contract these pathogens they will die quickly and so are less likely to infect other solitary bees. They have less contact with other bees, unlike eusocial hives, thus speeding up transmission to other bees and resources. Also, with a large hive it is more noticeable when many bees start dying; however, with a solitary bee it is hard to decipher whether their death would differ from the natural life cycle unless closely monitored.

Agricultural background:

Since the industrialization of farming, we have been adding more stressors to our pollinators including insecticides, pesticides, fertilizers, removing hedgerows and growing primarily monocultures causing habitat fragmentation. Monoculture planting critically harms the biodiversity of surrounding areas causing catastrophic effects. Sadly, it is economically more profitable and creates a higher yield of crop. Yet this exploitation of the environment, causes serious concerns about food security and the availability and volume of native pollinators. The combination of intensive farming and global warming has created an “insect apocalypse” with insect pollinator numbers declining by 49%. Jackson (2019) concluded in the East of England that “25 species of bee are threatened, 17 species are regionally extinct, and 31 species were put under conservation concern”. Since this report, the figures have worsened, and this trend of bee decline is seen globally and on a greater scale. Millard et al. (2021) also showed that increased agricultural intensity in urban environments caused a 43% reduction in bee species richness and 62% reduction in abundance. Zhu et al. (2022) also proved parasites increase susceptibility to the dangers of insecticides (e.g., neonicotinoids which damage neotropic activity in bees). Hence, for rural environments this caused a 75% reduction in abundance of pollinators. The combination of intensive farming and commercial hives has created cascading problems.

Summary:

All research clearly states that transporting artificially managed hives to be used commercially is highly problematic. Not only does it introduce new diseases, viruses and parasites, but also can increase virulence and the strength of a parasite’s effects by being placed into new environments with no natural predators. This makes it harder for wild pollinators to fight off diseases for which they have no prior resistance, unlike managed hives that benefit from chemical treatments. It also means the wild colonies of pollinators have increased environmental pressures for feeding with their limited resources being exploited. This again increases the effects of pathogens on bees. Commercial hives may be saving crops through their expediency, but it comes at the cost of wild pollinators and will lead to devastating effects on the environment. We need to consider the long-term negative effects opposed to the short-term solutions which only further accentuates the problem.

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