For several years in many countries around the world, we have been facing growing concern about the loss of bee colonies. This study explores the factors contributing to hive depopulation and the complex mechanisms of honey bees social immunity in response to various environmental and pathogenic stresses.

In recent years, articles related to the loss of bee colonies and the depopulation of hives around the world have been appearing frequently in the scientific literature. Indeed, it has been shown that these losses are due to various factors such as pathogens (parasites, fungi, bacteria and viruses), malnutrition, alteration or loss of ecosystems and the use of agrochemicals. These factors do not appear individually, but act together (Figure 1), negatively affecting the defense mechanisms of the bee immune system.

Figure 1. Impact of various stressors on honey bee health. Modified from El-Seedi et al. (2022).

Bees, Apis mellifera, possess an immune system that allows them to cope with different external agents through mechanisms similar to those of other insects, either through humoral and cellular responses, physical barriers, pathogen recognition receptors, etc. In fact, they utilize similar mechanisms as those found in Drosophila flies or Anopheles mosquitoes. But compared with these, they only possess about one third of the genes related to the immune system. So how do bees make up for this lack of genetic implementation of immune functions? The answer is: Thanks to social immunity.

Social immunity is described as a set of cooperative defense behaviors among members of a social group in order to prevent, control or eliminate infectious and parasitic organisms. Thus, the group’s cooperative defense strategy decreases the pressure on the immune system of individual bees.

Social immunity behaviors are based on the ability of each individual to communicate and respond to the conditions of the surrounding environment and, consequently, to make individual decisions that affect the colony as a superorganism. In various/several scientific publications (Hamilton et al., 2008; Westra et al., 2015), researchers differentiate between constitutive mechanisms and inducible mechanisms. Constitutive mechanisms are associated with the immunity of individual bees, whereas inducible mechanisms are activated upon exposure to a pathogen to reduce dispersal within and between colonies (Figure 2). The mechanisms developed by bees are detailed below:

• Polyandry: The female mates with different drones during her nuptial flight in order to increase the genetic diversity of the colony. The more mating partners, the greater the genetic diversity of the offspring. It has been observed that colonies with high diversity are more efficient in the search for resources, have a healthier microbiome and are overall more productive and efficient. They have also been found to be more resistant to different diseases and parasites.

• Division of labor: The organization of tasks in the beehive with worker bees fulfilling different roles offers a great advantage in minimizing the spread of pathogens and parasites in colonies. This division of tasks depends on the age of the worker bees. When they are a few days old, they are responsible for cell cleaning, afterwards for the care and feeding of the brood and queen, followed by hive maintenance and building, until they finally move outside into the field to collect nectar, pollen, water and propolis. In this system, the foraging bees, which are more exposed to pathogens and parasites, reduce their contact with younger bees which are closer to the brood area. It should be noted that the transition between tasks is sometimes flexible and can vary if necessary.
• Antimicrobial compounds: Insects produce antimicrobial compounds in order to protect themselves against different microorganisms. In social insects these molecules serve multiple functions and, in some cases, have evolved as a defense against pathogens and parasites at the colony level. An example of this are the peptides found in bee venom which are present as well in the cuticle of bees. The venom has antimicrobial properties, which could play an important role in limiting / controlling / inhibiting the spread of various diseases. The presence of antimicrobial peptides in larval food has also been demonstrated, which could reduce the levels of infection in the colony.

Figure 2. Mechanisms of social immunity in honeybees (Simone-Finstrom, 2017).

• Propolis collection: Bees collect propolis from the resins of certain plants. These resins are mixed by the bees with wax and used to create a sanitizing envelope around the brood nest, acting as an antimicrobial barrier. In the colony, propolis serves several functions such as waterproofing, sealing cracks, mummifying animals that enter and die inside the hive and preventing or minimizing the development of pathogenic bacteria and fungi. Different studies show that the presence of certain types of propolis in the hive can promote the expression of genes related to the bee immune system (Simone et al., 2009; Simone-Finstrom & Spivak, 2010, Larsen et al., 2019).

• Grooming: bees have the ability to remove external parasites with the help of their mandibles or legs. There are two types of grooming: individual, which is more frequent, and social grooming, which involves the collaboration of several individuals. Colonies in which this behavior is more frequently expressed are more resistant to Varroa destructor mite infestations. This behavior, which is influenced by genetic factors, has been associated with the Neurexin gene in several research studies (Hamiduzzaman et al., 2017; Tsuruda et al, 2014).

• Hygienic behavior: The ability of worker bees to detect and eliminate diseased or parasitized larvae or pupae (Figure 3). Moreover, this behavior is a defense mechanism against fungal diseases such as chalkbrood (Ascosphaera apis), American foulbrood (Paenibacillus larvae) and varroa. It is a mechanism that depends on the activation of several genes and is therefore more complex than grooming.

• Social fever: This mechanism involves increasing the temperature of the brood nest in order to control the growth of the fungus that causes chalkbrood (Ascosphaera apis). This behavior has a high energetic cost for each individual, but reduces the incidence of this pathogen.

• Flight: the appearance of a disease can lead the colony to initiate behaviors to eliminate it. However, sometimes the strategy is to leave the nest behind and start a new colony in a different, disease-free location. This behavior is common in Africanized bees and some Asian bees. But also occurs in A. mellifera under when high levels of pathogens or parasites are present in the colony.

Figure 3. Hygienic behavior in honeybees.

a) worker brood cells. b) top of a worker cell. c) emerging worker bee. d) opening / uncapping cells. e) and f) capping cells again, a darker area on the operculum is observed. g) removal of diseased or parasitized brood (Oddie et al., 2018).

Other behaviors such as decreased contact between bees are also cited in the literature.(Rueppell et al., 2010; Larsen et al., 2019). It has been observed that there are individuals that demonstrate an altruistic behaviour when they get sick, moving away from the hive to die outside, thus avoiding the spread of the disease. Brood cannibalism occurs when stressful situations cause brood mortality (e.g. malnutrition or extreme temperatures). Nurse bees cannibalize the dead brood in order to prevent the increase of pathogen levels and avoid certain diseases, such as mycosis.

As a defense strategy, social immunity significantly reduces the pressure on the individual immune system, thereby decreasing the number of genes needed for defense against various pathogens. It is exciting to observe how these amazing creatures act. Not only on an individual level, but as a superorganism in which the colony behaves as an individual.

Bibliography:

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