P.W., Seeley, T.D., and Reeve, H.K. (1998). Parasites, pathogens, and polyandry in honey bees. The American Naturalist 151 (4): 392–396.68 Simone, M., Evans, J.D., and Spivak, M. (2009). Resin collection and social immunity in honey bees. Evolution 63 (11): 3106–3022.
69 Spivak, M. and Downey, D.L. (1998). Field assays for hygienic behavior in honey bees (Hymenoptera: Apidae). Apiculture and Social Insects 91 (1): 64–70.
70 Tarpy, D.R. and Seeley, T.D. (2006). Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93: 195–199.
71 vanEngelsdorp, D., Evans, J.D., Saegerman, C. et al. (2009). Colony collapse disorder: a descriptive study. PLoS One 4 (8): e6481. https://doi.org/10.1371/journal.pone.0006481.
72 Winston, M.L. (1980). Swarming, afterswarming, and reproductive rate of unmanaged honey bee colonies (Apis mellifera). Insectes Sociaux 27 (4): 391–398.
73 Zheng, H., Steele, M.I., Leonard, S.P. et al. (2018). Honey bees as models for gut microbiota research. Lab Animal 47: 317–325.
2 The Superorganism and Herd Health for the Honey Bee
Robin W. Radcliffe
Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA
* Illustrations by Anna Connington
Introduction
The honey bee colony is a magnificent product of evolution. Collective decision‐making of thousands of individual bees, each with roles that change as they age, work seamlessly together to create a highly integrated system (the colony) that functions as a single organism (the superorganism). In this chapter we will explore the marvelous world of the honey bee with a focus on how the organization and structure of the colony allows honey bee societies to function as a single coordinated living entity. The superorganism must build new comb, make replacement bees, collect food, water, and hive materials all while protecting their home from pests and pathogens, and survive to reproduce by casting a swarm and sending off drones. Deviations in any one of these collective pathways can lead to disorders, disease, or colony failure.
We will follow the honey bee as it allocates tasks in sophisticated communication networks that help prevent the spread of pathogens, make and use organic compounds to fight disease, collect plant resins to make propolis, and manipulate the hive environment to prevent and even treat infections in the colony. In an extraordinary example of social behavior, we will also learn how honey bees can treat themselves and prevent disease by working as their own “doctors”! These novel methods of disease control and mitigation are just now becoming well understood. The marvels of resin and pollen collection and the myriad bioactive elements in these compounds, collected from nature itself, offers wonderful insights into the ways that honey bees protect themselves from harm. The health benefits of propolis to human health have been known since the days of the ancient Greeks, Romans, and Egyptians; the word itself comes from the Greek “pro” to defend and “opolis” the city, or in this case the beehive or wild nest. Here we will explore the value of propolis to the bees themselves, a topic deserving of more in‐depth research. Honey bees can also control fundamental environmental conditions that are protective against disease, including the remarkable ability to regulate the “body temperature” of the superorganism. Used against large invaders such as a bumble bee that attempts to enter the colony, honey bees use heat to “bake” the invader in a ball of heater bees, while small invaders such as some bacteria and fungi that infect the brood are killed by small elevations in temperature (enough to kill the pathogen, but not the developing brood). Scientists call the latter a “social fever”, and it is another example of how the colony can ward off infections through cooperative action.
Finally, the health and fitness of honey bees as a superorganism can be examined and evaluated in much the same way as a herd of livestock – herd health for honey bees offers a big picture “lens” through which serial monitoring of population level determinants of health are made. An understanding of how honey bees coordinate important hive processes (including collection of pollen, nectar and tree resins, coordination of bee caste populations, maintenance of biosecurity, and ensuring a healthy living environment) combined with the collection of relevant data will provide one of the most important tools for the bee doctor to help decipher health at the level of the colony working in concert with the beekeeper.
Part 1: The Superorganism and Swarm Intelligence
At the peak of summer activity, an estimated 30 000–50 000 bees live in close proximity within the confines of the typical beehive, or a bee tree if a wild colony. The value of social living must exceed the disadvantages of being closely packed together since parasites and pathogens can exploit the high density of individuals and their network of interactions, predisposing the colony to disease outbreaks. Conditions inside the colony can likewise favor pathogen spread as the bees maintain strict control of the hive environment (brood nest T = 34–36 °C; outer winter cluster T > 10°C; RH = 60–80%) (Avitabile 1978; Li et al. 2016). This combination of a stable temperature and humidity is essential to support key hive processes including brood development and rearing, yet these conditions also set up a perfect storm for infectious and parasitic disease to thrive. How then do bees work together to prevent infection and maintain colony health within the framework of this environment of potential harmful organisms? Before we delve into the wonderful colony‐level adaptations that support health in the hive environment, we will begin by reviewing the structure of the superorganism.
The idea of the “superorganism” is more than a century old, having first been contemplated by the entomologist William Morten Wheeler (Wheeler 1911). Wheeler believed an ant colony is a system that possesses fundamentally the same properties of an individual organism – namely the complex system (the ant colony in Wheeler's studies) obtains and assimilates substances from the environment, produces offspring, and protects both the system and offspring from disruptions of the environment. Future researchers, including famed ecologists Edward O. Wilson and Bert Hölldobler, refined the definition of a superorganism (also known as eusocial insect societies) by outlining a fundamental couplet: division of labor whereby a small segment of a society produce offspring while the vast majority forgo reproduction to work for the hive – together with the overlap of generations (Wilson 1971; Hölldobler and Wilson 2009). The offspring of the reproductive queen must remain in the nest to help raise the next generation; it was the reproductive division of labor combined with the sibling care for younger siblings in the same nest that marked the rise of eusociality.
Honey bees represent the pinnacle of social evolution by taking this division of labor to the extreme with a single queen monopolizing the egg‐laying role (a healthy queen can lay upward of 2000 eggs per day) while 50 000 or more worker bees toil in the hive. The workers still possess ovaries, but rarely lay eggs, and those that are laid are unfertilized and will only produce males. Worker bees cannot function as individual organisms – their only survival is linked inextricably to a promiscuous queen by way of a tightly choreographed system of communication among closely related sisters. The role of the male is simply as a conveyor of genes offering a mechanism to induce diversity (a maiden queen will mate with up to 20 drones) – such diversity is an essential ingredient for Darwin's recipe of natural selection. In their book, The Superorganism, the authors equate the male of these female‐dominated societies as simply “sperm‐guided missiles.” While essential to the reproduction of the
