Over the past few decades, as a beekeeper/biologist I’ve had the opportunity to watch evolution in action. I’ve observed the catastrophic effects upon colony health due to the introduction of new parasites, periodic pathogen epidemics, and the more subtle effects of changing land use practices and climate change. I’ve also witnessed the evolution of both recreational beekeeping and the bee industry, as we’ve been forced to change our management practices and income streams due to the aforementioned biological and environmental factors, plus changes in markets and the impacts of regulatory decisions.

My point is that things change, each change altering the realized niche of both bees and beekeepers. Neither Nature nor the Market are the least bit sentimental. Those who don’t adapt to change die.

The adaptive process may make headlines, or it may go largely unnoticed. But one thing’s for sure—the more that we understand the changes in the parameters of the bee and beekeeper niches, the better we can successfully engage in the adaptive process.

We Are Two Adaptive Species

Both Apis mellifera, and those Homo sapiens categorized as “beekeepers” have proven to be incredibly adaptive species (ecologists would say that we exhibit a high degree of plasticity). At times, each of our populations face limiting factors that weed out the least fit. And the higher the failure rate of individual colonies or beekeeping operations, the stronger the selective pressure to adapt.

So what sort of failure rate is “normal” for bees under optimal natural conditions (the fundamental niche)? Let’s do the math! Given: an established and stable local population of bees under optimal conditions. In the spring each colony will produce at least one swarm. At that point, the colony population will have temporarily at least doubled. But such a rate of reproductive increase is obviously unsustainable, since by definition a “stable” population ends with the same number of colonies each year. So simple arithmetic tells us that in nature, on average, at least half of all colonies will succumb each season, even under the best of conditions.

Although half the colonies will fail on average, it is not the average colony that fails. The key point is that it is the least fit that tend to fail, and a greater proportion of the most fit survive. This considerable amount of selective pressure is what drives adaptation and evolution in each natural population of bees.

It’s the same with beekeepers. The failure rate for beginning beekeepers is often even higher than the above. Commercial operations also fail; despite record high prices for honey and pollination services, our recent elevated colony mortality rate is eliminating the profit margin for some operators, who, sadly, will go out of business. But, again, the hard fact is that it is the less fit (or less adaptable) operations that are failing—I speak with plenty of operators who aren’t experiencing egregiously high winter losses, and whose businesses are firmly in the black. It is these operations that are successfully adapting to their realized niche.

Honey Bees Are Designed For Rapid Adaptation

As I study the honey bee reproductive strategy, one principle jumps out:

Everything about the honey bee reproductive process is designed for rapid adaptation to changes in its realized niche, and for the recovery of the bee population from decimation events [¹].

Apis mellifera has the highest known rate of genetic recombination of any animal. And those “experimental” recombinations are then filtered for success through the haploid drones, who have only one set of chromosomes, meaning that only the best novel combinations of genes (alleles) have any chance of being passed to the next generation.

The genetic combinations of the fittest drones then predominate in the matings that occur in drone congregation areas, thus ensuring that each virgin queen has the best chance of loading up with the best genetics that the overall bee population in that area has to offer. And she further ensures the maximum diversity of her offspring by mating with multiple drones. Add to this the incredible epigenetic plasticity of the honey bee [²], and we have an organism able to quickly adapt to whatever Nature throws at it!

I observe something similar with beekeepers. Those who are consistently trying new things and adapting to the changing biological and business environments are those who tend to be the most successful in the long run.

The Human-Facilitated Realized Niche Of The Bee

OK, so in nature, half the colonies fail each year. But provided facilitation by human beekeepers, that rate can drop to around 10% for well-managed operations. However, in recent years, U.S. beekeepers have been reporting distressingly high rates of colony failure. Clearly, something in the realized niche of our honey bees has changed in the last decade (one or more limiting factors). In order to attempt to figure out exactly which factors are responsible, let’s first determine what the primary limiting factors were for honey bee populations prior to humans. Perhaps then we can better understand how our actions (and the Earth’s burgeoning human population) are affecting honey bee survival. And maybe then we can take steps to make life easier for our beloved bees (and improve the bottom line of those of us who make our living at keeping ‘em).

The Natural Limiting Factors Of The Honey Bee Population

Limiting Factor: The Weather

The weather would be an obvious limiting factor—colonies are stressed by extreme cold, unfavorable flight weather during the spring or summer, or by lack of forage and water during droughts. Such intermittent weather events may sporadically cull the bee population, but would only affect long-term adaptation if they occurred regularly. So let’s focus upon which factors limited bee populations in favorable years, during which they have the intrinsic ability to increase exponentially.

Limiting Factor: Predation

Honey bees are herbivores. The populations of many herbivores are controlled by predators (Fig. 1). If the population of the prey species becomes dense, predator species ramp up their numbers to take advantage of the food source. The result is typically an oscillating predator/prey population dynamic (this is one of the bases for integrated pest management in agriculture).

Figure 1. Foraging bees face plenty of predators, such as wasps, assassin bugs, birds, spiders, and dragonflies. One of “my” bees (above) became a meal for a robber fly.

Although predators of foraging bees may take a bite out of the population of older bees in the hive, they do not appear to be a primary limiting factor of the overall bee population. An exception to this rule might be the Asian Hornet (Vespa velutina) (now introduced in Europe), which can decimate small colonies of bees by picking off returning foragers [³].

A more serious form of predation is direct invasion of the hive. A healthy colony can generally repel or otherwise deal with small invaders such as ants, wasps, and Small Hive Beetles. More problematic are those large mammalian predators willing to ignore the bees’ defensive stinging, such as bears, skunks, honey badgers, and humans. The bees’ main defense against such predators is to nest in inaccessible fortifications. And that leads us to…

Limiting Factor: Competition For Nest Cavities

Bees are pretty picky about the nest cavities that they choose, strongly preferring elevated tree cavities having small, defendable entrances [⁴] (Fig. 2). In treeless areas, the lack of suitable nest sites could well have been a limiting factor for the honey bee population. But this is unlikely to have been the primary limiting factor anywhere that patches of ancient forest were within range.

Figure 2. This hollow black oak provides a protected nest cavity impenetrable by our local black bears.

Although a lack of suitable cavities may not the main limiting factor of the bee population, it does bring to mind another fascinating aspect of bee behavior. Please allow me to digress for a bit. Not all beekeepers are aware that intra- and inter-species parasitism is common among bees, wasps, and ants. For example, queens of a number of bumblebee species parasititically invade and take over other bumblebee colonies. And the Cape Bee (Apis mellifera capensis) is famous for its ability to parasitically take over colonies of the Savannah Bee (Apis mellifera scutellata) [⁵]. This sort of deplorable behavior appears to be ingrained in the bee genome– bees covet the fruits of their neighbors’ hard work.

Part of the Africanized honey bees’ ability to rapidly expand its range in the Americas was likely its ability to invade and usurp the established nests of European bees [⁶]. Lately, Dr. Wyatt Mangum has been reporting on his observations of similar behavior by ostensibly non-Africanized bees in Virginia [⁷].

Such takeovers give the usurping swarm a profound advantage. Rather than needing to establish a nest and provision it with stores from scratch, it can simply take over an established colony, essentially hijacking its combs, stores, and entire workforce. Although Mangum, so far as I know, is the first to report such behavior for European honey bees, his observation may answer a question that has been bugging me for years: why do European bees send out what appear to be doomed swarms in late summer?

Bees typically swarm in spring, for the obvious reason that that timing allows the swarm colony to establish and provision a nest in time for winter. But in actuality, there are two peaks of swarming during a season (Fig. 3). I’d long noticed this, and wondered why in the heck a colony would bother to swarm in the late summer—natural selection should have eliminated such suicidal behavior. It just didn’t make sense!

Figure 3. Seasonal timing of swarm emergence dates in New York, showing the main late-spring peak, followed by a lesser peak around the first of September. Why the heck would colonies swarm in late September? After Seeley [[i]].

[i] I transcribed and plotted the data from Fig. 1 in Seeley, TD, et al (1989) Bait hives for honey bees. Cornell Coop Ext Inf. Bull. No. 187. http://ecommons.cornell.edu/bitstream/1813/2653/2/Bait%20Hives%20for%20Honey%20Bees.pdf

I assumed that the data was for New York and from the following paper, but I was unable to obtain a copy:

Fell, R. D., et al (1977) The seasonal cycle of swarming in honeybees. J. Apic. Res. 16:170-173.

But Mangum’s observations reminded me that I’ve also seen in past years late-summer swarms landing on hives, and also seen balled queens in hives in late summer. Perhaps I simply never put it all together! Could it be that this is an innate, but previously unrecognized, behavior in European bees?

It is certainly biologically plausible that under certain circumstances European colonies behave like their Africanized brethren (they are, after all, the same species), and send out older queens who have already successfully built up a colony (and perhaps even a second swarm colony), but still have enough vigor left to do an invasive usurpation of a nearby nest. If the colony were already superseding that queen, then it would be an inexpensive gamble to send her out, accompanied by a hit team of experienced workers, to try to take over an unsuspecting colony, its stores, and its workforce shortly before winter.

Pardon my digression—let’s return to our search for the main limiting factor of the natural bee population.

Limiting Factor: Carrying Capacity Of The Habitat

The maximum population density for the realized niche of a population is set by the carrying capacity of that particular environment, typically limited by resources such as food. However, the honey bee is a special case; similar to the bear, the colony can gorge when food is plentiful, and store “fat” (honey and beebread) as reserves for lean times (as during overwintering).

There are indeed areas in which colonies can barely put on enough honey during the main flow in order to make it through the winter. But by definition, such areas would not meet a primary requirement of the fundamental (optimum) niche of the honey bee, so we can disregard such areas from this discussion. What we are interested in is the limiting factor of the bee population in areas that normally produce a good honey flow.

Limiting Factor: The Timing Of The Bloom

Honey bees are defined by their ability to store food reserves—honey and beebread—to see them through lean times. But there are times other than the main honey flow during which the availability of nectar, and especially pollen, are of critical importance to the ability of colonies not only to survive, but also to reproduce. Colonies must build up and produce a swarm early enough in the season that both parent and swarm colony have fighting chances to store enough honey to make it through the following winter [⁹]. Such buildup requires the initiation of broodrearing in the middle of winter, which is in turn dependent upon having stored a large supply of beebread during the fall pollen flow [¹⁰].

What we must keep in mind is that a colony of bees is only effective at putting away a honey surplus if it has grown a large enough population to efficiently forage upon and store the available nectar. Timing is everything. Too large a population at the wrong time of the year would be counterproductive, since those hungry mouths would consume more honey than they were able to store. A locally-adapted population of bees times its buildup to coincide with the main flow, and then quickly shrinks back to survival mode.

Many of us tend to base our idea of typical bee behavior upon that of commercially-selected Italian stock. Such stock, originally adapted to Mediterranean climates, and bred for continuous broodrearing and high honey production, can hardly be expected to be representative of wild type bees adapted to cold-winter areas (I am not dissing Italian-type bees—they are well adapted to build up early for almond pollination).

Bees adapted to colder winters, such as the Carniolans or Russians, are far more responsive to the environment, especially to the availability of pollen. As soon as plants start producing pollen in spring, bees of these races explode into action —working even in cool and wet weather, and madly brood up.

The reason for their frenzy is that they must build up their population early enough to produce a swarm in time for it to have a decent chance at establishing a nest and putting away adequate winter honey stores during the brief main honeyflow (typically May through June; in temperate climates, colonies may only gain weight for a few weeks a year). I’ve previously graphed the bee colony’s amazing ability to quickly build up [¹¹]. An absolute requisite for such a rapid rate of growth is a monster supply of pollen in the early spring.

After the main flow comes the summer dearth. When pollen is unavailable, wild-type bees sit tight in survival mode [¹²], cooling their heels and conserving their energy. I’ve seen Russian bees cease broodrearing in August in the arid California foothills, appearing as though they were queenless. In the adjacent yards, my Italian stock just keep on rearing brood, and required supplemental feeding of protein in order to keep them in decent shape for going into winter..

So I suspect that the limiting factor for bees in a natural realized niche is not the amount of food available during a brief period of food abundance (the main honey flow), but rather the quality and quantity of forage available during spring and late summer/fall.

Practical application: the realized niche of the honey bee is likely largely defined not by the amount of nectar available during the main honey flow, but rather by the quantity and quality of pollen available prior to and after that period. A successful colony requires a dependable abundance of quality pollen and nectar for early spring buildup; and then adequate late-season pollen to ensure its ability to produce a cluster of protein-rich “winter bees” and to store beebread for midwinter broodrearing.

Nevertheless, prior to man, biologically productive areas typically supported a diversity of native vegetation that produced exactly such an extended season-long buffet of nutrition. Thus, I doubt that during favorable years, a lack of available spring or fall food resources was the limiting factor of the bee population prior to man.

Limiting Factor: Competition For Those Food Resources

Competition for food resources, either against other species or one’s own species, is a common limiting factor of the realized niche. So what sort of competition do bees face?

Anywhere that there are flowering plants, there are pollinators that have coevolved with them. Most are insects (although in some areas, birds, bats, or other mammals may be important). Does competition with other pollinators limit the honey bee population?

Let’s think about it. Since one can place a hive of bees into most any favorable habitat and still make honey despite the presence of established populations of native pollinators, I suspect that competition with other species is not normally the limiting factor of the honey bee population. On the other hand, as any beekeeper quickly recognizes, honey bee colonies certainly compete with one another!

Beekeepers tend to focus upon the amount of nectar available during the main honey flow, and understand that one can overload an area with managed hives. But how about the density of a natural population of bees—does the amount of nectar available during the main flow limit that population?

Again, let’s check easily-verifiable observations. In areas with well-established populations of feral bees (Australia, Hawaii, formerly in the U.S), one can bring in additional managed colonies, yet still produce a substantial honey crop during the main flow—clearly, nectar is produced in excess of what an established natural population of bees can harvest. It follows then that at a “normal” population density of unmanaged colonies, competition for nectar during the main flow was not the limiting factor for colony survival.

On the other hand, competition for pollen during spring or fall could well be a limiting factor. And along with that competition comes…

Limiting Factor: Intercolony Parasitism

Competition between colonies does not occur only for nest sites or at the flower; it can also happen directly at the hive. All’s fair in love, war, and in Nature. If you can save yourself effort by stealing the fruits of another’s labor, so be it. The term for this is kleptoparasitism (kleptoparasite: a bird, insect, or other animal that habitually robs animals of other species of food).

What we call “robbing” is a form of kleptoparasitism, and during early spring or the summer dearth, the robbing pressure between colonies can brutal. There would be a clear competitive advantage to those colonies that successfully robbed honey from others; conversely, there would be an advantage to those colonies best able to defend their hard-won stores.

Robbing behavior may also be more insidious than the overt invasion of a weak colony by a strong colony. Dr. Wyatt Mangum detailed the sneaky “progressive robbing” of one colony by another [¹³]. Such robbing would constitute an insidious drain upon the victim colony. In areas of high colony population density, I suspect that robbing pressure–at times other than during major honey flows–is a limiting factor in colony density.

And this very robbing behavior brings us to our last suspect factor– that famous Horseman of the Apocolypse, Pestilence.

Limiting Factor: Pathogen Transmission

As most beekeepers soon find out, honey bees are host to a number of parasites and pathogens. To a biologist, a pathogen is a parasite (such as a virus, fungus, or bacterium) that can cause disease. These parasites can cause the bees to suffer from either endemic or epidemic infections. A well-adapted parasite typically does not, under normal circumstances, cause serious disease, but rather smolders in the bee population of each individual colony as an endemic infection; sacbrood virus or Nosema apis follow this model. These well-adapted parasites are typically vertically transmitted, that is, from parent to offspring, or in the case of bees, from mother colony to daughter colony. They can generally be found in a colony, but so long as the colony is not stressed, there are no symptoms of disease.

Other parasites tend to go epidemic, sometimes in recurring cycles; chalkbrood, Chronic Bee Paralysis Virus, American Foulbrood, and European foulbrood fall into this category. Individual colonies are able to “clear” themselves of these parasites; the parasites maintain a presence in the local bee population, but may not be found in every colony. Epidemic parasites are largely dependent upon horizontal transmission from colony to colony, and unlike the well-adapted endemic parasites, actually benefit by the weakening or death of an infected colony. As such, they would be considered to be density dependent infectious diseases. As the density of the host (honey bee colonies) in the environment increases, the opportunities for transmission of the parasite from colony to colony directly increases [¹⁴]. The pathogen causing the disease can only persist if the host density exceeds a certain threshold (if bee colonies were scattered beyond flight distance, there would be slim possibility for an infectious pathogen to transmit from one colony to another).

Conversely, not being regularly exposed to a pathogen removes the selective pressure for the bees to maintain genetic (or epigenetic) resistance. Thus, in nature, epidemics of certain pathogens ebb and flow, often decimating a host population one year, at which point the host density is decreased to the extent that the pathogen nearly disappears, struggling to maintain a foothold in the few remaining, and most resistant, hosts. As the host population then recovers over the years, an epidemic may then recur (higher host densities favor virulent mutations of the pathogen). This is a common cyclic pattern in insect species with large populations, and bees are no exception [¹⁵].

Practical application: After a plague it may take years for a particular pathogen to again recover its hold in the bee population. And it may take a special combination of environmental circumstances, and perhaps coinfection with other parasites, in order for it to do so.

For most species of wildlife, natural populations tend to reach some sort of dynamic equilibrium, with pestilence being the ultimate limiting factor if all other conditions are optimal. Anderson [¹⁶] explains:

It is likely that interplay between the pathogenicity of viral, bacterial, [or] protozoan infections and the nutritional state of the host contributes importantly to the density-dependent regulation of natural populations, with the parasites greatly amplifying the effects of low levels of nutrition.

Such pestilence typically occurs in the form of epidemics, during which the pathogen(s) efficiently spread through a stressed and overcrowded population, the key word being overcrowded. Too many colonies of bees in an area is a recipe for disaster—a ticking time bomb just waiting for the right combination of environmental circumstances and the presence of a virulent pathogen (or combination thereof).

A Special Case: The Viruses

But it’s a bit more complicated when reservoir hosts are involved. That is, when a pathogen is not limited to honey bees as its sole host. And this is the case with the “bee” viruses, most or all of which appear to actually be generic insect viruses that bees pick up when they visit flowers. So it is likely that the density of the bee population is not limited merely by diseases specific to honey bees, but also by the entire pool of viruses that infect pollinating insects [¹⁷] (Fig. 4).

Breaking news: As I type these words, a collaboration of researchers associated with the USDA ARS labs is about to release a stunning paper [¹⁸], in which they detail how a plant virus is now infecting both honey bees and varroa, and appears to be associated with collapsing colonies. Their findings suggest that varroa may be a key player in the cross-kingdom jump of this virus. The complexity of the bee, mite, plant, and virus web of infection continues to astound us!

Figure 4. These Russian bees near the hive entrance are in the process of cooking a too-bold bald-faced hornet to death [[i]]. Hornets and yellowjackets eat bees, and are thus exposed to bee pathogens. Exposure also goes the other way as the wasps contaminate nectar with virus particles when they visit flowers, or, as in this case, if the dying wasp exudes any body fluids.

[i] Ugajin A, et al. (2012) Detection of neural activity in the brains of Japanese honeybee workers during the formation of a “hot defensive bee ball”. PLoS ONE 7(3): e32902.

Historically (meaning prior to varroa), these viruses were sporadically present in bee colonies, but generally as inapparent (free of noticeable symptoms) infections [²⁰]. It was only under certain circumstances that they went epidemic and caused noticeable morbidity or mortality of colonies:

Taken together, these data indicate that bee virus infections occur persistently in bee populations despite the lack of clinical signs, suggesting that colony disease outbreaks might result from environmental factors that lead to activation of viral replication in bees [²¹].

In any case, in some years in some localities, such “perfect storms” of environmental factors, virulent mutations of one or more pollinator viruses, and coinfections with other parasites have historically led to serious colony collapse events [²²]. This is not a new thing!

Conclusion

My original question was what were the primary limiting factors in the realized niches of the honey bee prior to human influence? I hope that I have adequately covered these factors, since I feel that our understanding of them is critical for us to be better beekeepers, and to make good management decisions.

As always, I prefer to let the reader draw his/her own conclusions, but to me it appears that that the primary limiting factors in colony survival in favorable areas were most likely the density-dependent competition for pollen during spring and fall, coupled with the associated transmission of certain pathogens.

The above factors have long been associated with epidemics in the bee population. It appears to me that our bees today are in the midst of an ongoing and complex multi-pathogen epidemic largely precipitated by the actions of mankind. In the next installment of this article I will explore how this situation came about, examining how changes in world trade, agriculture, the environment, and in beekeeping practices have affected the realized niche of the bee, its parasites and pathogens, and the business models of beekeepers. My hope is that by fully understanding how we inadvertently helped to create the problem, that perhaps we can better take steps to help our poor bees deal with the problem, and for ourselves to stay in business in the process.

Footnotes and Citations

¹ “Decimation events” being plagues, droughts, wildfires, extreme weather events, etc.

² http://www.nature.com/news/job-swapping-makes-its-mark-on-honeybee-dna-1.11418#/b1

³ Tan, K, et al (2007) Bee-hawking by the wasp, Vespa velutina, on the honeybees Apis cerana and A. mellifera. Naturwissenschaften 94(6): 469-472. Open access.

⁴ Seeley TD and RA Morse (1978) Nest site selection by the honey bee, Apis mellifera. Insectes Sociaux 25: 323–337.

⁵ Martin, S, et al (2002) Usurpation of African Apis mellifera scutellata colonies by parasitic Apis mellifera capensis workers. Apidologie 33: 215-232.

Danka, RG, RL Hellmich, TE Rinderer (1992) Nest usurpation, supersedure and
colony failure contribute to Africanization of commercially managed European honey
bees in Venezuela. Journal of Apicultural Research 31 (3/4): 119-123.

⁶ Schneider, SS, et al (2004) Seasonal nest usurpation of European colonies by African swarms in Arizona, USA. Insectes Sociaux 51(4):359-364.

⁷ Mangum, W (2010) The usurpation (takeover) of established colonies by summer swarms in Virginia. ABJ 150(12): 1139-1144.

Mangum, W (2012) Colony takeovers (usurpations) by summer swarms: they chose poorly. ABJ 153(1): 73-75.

Mangum, W (2013) Summer swarms with queen balling. ABJ 153(2): 163-165.

⁸ I transcribed and plotted the data from Fig. 1 in Seeley, TD, et al (1989) Bait hives for honey bees. Cornell Coop Ext Inf. Bull. No. 187. http://ecommons.cornell.edu/bitstream/1813/2653/2/Bait%20Hives%20for%20Honey%20Bees.pdf

I assumed that the data was for New York and from the following paper, but I was unable to obtain a copy:

Fell, R. D., et al (1977) The seasonal cycle of swarming in honeybees. J. Apic. Res. 16:170-173.

⁹ Otis, GW and JM Wearing-Wilde (1992) Net reproductive rate of unmanaged honeybee colonies, (Apis mellifera L.). Ins. Soc. 39:157-165.

¹⁰ Seeley, TD and PK Visscher (1985) Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecological Entomology 10: 81-88.

¹¹ https://scientificbeekeeping.com/sick-bees-part-17-nosema-the-smoldering-epidemic/

¹² This physiological change to diutinus bees occurs when newly-emerged workers sense queen pheromone, but no young brood pheromone, which tells them that the colony is in survival mode. This typically occurs in fall, but can also occur during summer dearth. See https://scientificbeekeeping.com/an-adaptable-workforce/

¹³ Mangum, W (2012) Robbing: Part 2: Progressive robbing. ABJ 152(8): 761-764.

¹⁴ Hudson PJ, et al (2001) The Ecology of Wildlife Diseases. Oxford University Press, Oxford.

¹⁵ https://scientificbeekeeping.com/sick-bees-part-9-pathogens-and-plagues/

¹⁶ Anderson, RM and RM May (1979) Population biology of infectious diseases: Part I. Nature 280(2): 361-367.

¹⁷ Singh R, et al (2010) RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS ONE 5(12):e14357.

¹⁸ Lian JL, Cornman RS, Evans JD, Pettis JS, Zhao Y, Murphy C, Peng WJ, Wu J, Hamilton M, Boncristiani HF, Jr., Zhou L, Hammond J, Chen YP. 2014. Systemic spread and propagation of a plant-pathogenic virus in European honeybees, Apis mellifera. mBio 5(1):e00898-13. doi:10.1128/mBio.00898-13. Open access.

¹⁹ Ugajin A, et al. (2012) Detection of neural activity in the brains of Japanese honeybee workers during the formation of a “hot defensive bee ball”. PLoS ONE 7(3): e32902.

²⁰ Hornitzky, M (1987) Prevalence of virus infections of honeybees in eastern Australia. Journal of Apicultural Research 26(3) : 181-185.

Anderson, DL and AJ Gibbs (1988) Inapparent virus infections and their interactions in pupae of the honey bee (Apis mellifera Linnaeus) in Australia. J. Gen. Virol. 69: 1617-1625.

Mouret, C, et al (2013) Prevalence of 12 infectious agents in field colonies of 18 apiaries in western France. Revue Méd. Vét. 164(12): 577-582. http://www.revmedvet.com/2013/RMV164_577_582.pdf

²¹ Tentcheva, D, et al (2004) Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl. Environ. Microbiol 70(12): 7185-7191. http://aem.asm.org/content/70/12/7185.full

²² Underwood, R and D vanEngelsdorp (2007) Colony collapse disorder: have we seen this before? Bee Culture 135(7): 13-18. http://ento.psu.edu/pollinators/publications/underwood