- Animals: bees
- Animal Production: general animal production
Honey bees, as social insects, rely on collective behavioral defenses that produce a colony level immune phenotype, or social immunity, which in turn impacts the immune response of individuals. One behavioral defense is the collection and deposition of antimicrobial plant resins, or propolis, in the nest. We tested the effect of a naturally constructed propolis envelope within standard beekeeping equipment on the pathogen and parasite load of large field colonies, and on immune system activity, virus and storage protein levels of individual bees over the course of a year. The main effect of the propolis envelope was a decreased and more uniform baseline expression of immune genes in bees during summer and fall months each year, compared to the immune activity in bees with no propolis envelope in the colony. The most important function of the propolis envelope may be to modulate costly immune system activity. As no differences were found in levels of bacteria, pathogens and parasites between the treatment groups, the propolis envelope may act directly on the immune system, reducing bees’ need to activate the physiologically costly production of humoral immune responses. Colonies with a natural propolis envelope had increased colony strength and vitellogenin levels after surviving the winter in one of the two years of the study, despite the fact that the biological activity of the propolis diminished over the winter. A natural propolis envelope acts as an important antimicrobial layer enshrouding the colony, benefiting individual immunity and ultimately colony health.
Social insect colonies may be considered superorganisms, a group of related individuals living in a nest, whose collective behaviors produce a colony-level phenotype, which in turn influences the behaviors of individuals in the nest (Seeley, 1989). Highly social insects’ immune defenses function in a similar collective way: at the individual level, an immune response is initiated via cellular or humoral immune pathways (Evans et al., 2006). At the colony-level, some individuals perform behaviors that defend and protect the colony against pathogens and parasites (Simone et al., 2009). These behavioral defenses in a honey bee colony include hygienic behavior and grooming (Wilson-Rich et al., 2008), antimicrobial secretions (e.g. the spread of venom on bee’s cuticle; Baracchi et al., 2011), and the collection of antimicrobial compounds (e.g. resins) from the environment (Simone et al., 2009). Combined with the division of labor among individuals (Naug and Smith, 2007; Stroeymeyt et al., 2014), these behavioral defenses produce a colony-level immune phenotype, or social immunity (Cremer et al., 2007), which in turn impacts the immune response of individuals (Otti et al., 2014).
Behavioral, or social, immunity benefits overall colony health and may have less physiological cost to individuals compared to the cost of maintaining a diverse immune system (Evans and Pettis, 2005; Schmid-Hempel, 2005). In honey bees, social immunity plays an important role in reducing parasite establishment and spread within colonies (Arathi et al., 2000; Evans and Spivak, 2010; Simone-Finstrom and Spivak, 2012).
The collection of antimicrobial resins from the environment by honey bees (Simone et al., 2009) and its deposition into the nest architecture is a fundamental component of their social immunity. Resin is a plant exudate secreted prophylactically to protect young leaf buds from pathogen infection and herbivore attack. It is composed primarily of antimicrobial compounds (e.g. monoterpenes and flavonoids) that play a major defensive role in the survival of the plant (Langenheim, 2003). Honey bees collect plant resins and deposit the resins in the nest as a form of cement, called propolis. When honey bees nest in tree cavities, they use propolis to coat the entire inner surface of the nest cavity, constructing a propolis envelope (Seeley and Morse, 1976). However honey bees do not construct a natural propolis envelope within standard beekeeping equipment because the inner walls of the wooden boxes are smooth and do not elicit propolis deposition behavior. Instead, bees deposit propolis only in dispersed cracks and crevices and not as a continuous envelope (Simone-Finstrom and Spivak, 2010).
Simone et al. (2009) first tested the benefits of a propolis envelope to the bees’ immune system by experimentally coating the inside of boxes with a propolis extract solution (ethanolic solution of propolis) to simulate a propolis envelope surrounding small colonies of honey bees. After just seven days exposure to the propolis enriched nest environment, bees’ immune-related gene transcription was significantly lower compared to bees in boxes not enriched with the propolis-extract. The bacterial load (eubacterial 16S gene expression, which measures internal and external bacteria carried by bees) was also significantly lower in bees in propolis-enriched colonies. These results suggested that the propolis reduced the level of immune-elicitors in the nest, so that the bees were able to expend less energy on costly immune system activation (Simone et al., 2009).
Other benefits of propolis to honey bee health have been documented. Numerous in vitro studies have demonstrated the inhibitory activity of propolis, and specific compounds within propolis, against the growth of the honey bee bacterial pathogen Paenibacillus larvae and Ascosphaera apis (Antúnez et al., 2008; Bastos et al., 2008; Bilikova et al., 2013; Lindenfelser, 1968; Wilson et al., 2013; Wilson et al., 2015). It is not known if honey bees actually consume propolis, but Johnson et al. (2012) demonstrated that when bees were experimentally fed propolis in sucrose syrup the transcription of three cytochrome 450s, involved in pesticide detoxification, was induced (Johnson et al., 2006; Mao et al., 2011). The placement of natural propolis in the nest cavity has been positively correlated with brood viability, worker lifespan, honey production, hygienic behavior and pollen stores (Nicodemo et al., 2013; Nicodemo et al., 2014).
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Here, we tested the effect of a naturally constructed propolis-envelope within standard beekeeping equipment on the strength, pathogen and parasite load of large field colonies, and immune system activity, virus and storage protein level of individual bees over the course of a year. Our aim was to examine the relative immune and health benefits of the natural propolis envelope from the scale of the individual bee to the level of the entire colony. At the individual level, we hypothesized that the presence of a propolis envelope enshrouding the nest area would result in a decrease in eubacterial load (based on findings from Simone et al., 2009) and possibly virus load. Additionally, we predicted that in response to the lower level of immune elicitors (pathogens and other microbes) within the nest, the immune-related gene expression in bees from colonies with a propolis envelope would be lower compared to bees in colonies without the propolis envelope (Simone et al., 2009). At the colony level we hypothesized that colonies with a propolis envelope would have greater colony strength (more bees and brood; e.g. Nicodemo et al., 2013; Nicodemo et al., 2014) and would have increased winter survivorship. Our findings revealed significant reduction in the baseline activity of a number of immune gene transcripts in individual bees, but no effects on other measured microbes, pathogens or parasites. Colonies with the natural propolis envelope had increased colony strength after the surviving winter in one of the two years of the study. This is the first study to investigate the seasonal benefits of propolis to honey bees, and demonstrates how the collection and deposition of resins into the nest architecture produces a colony-level immune phenotype that impacts individual immunity, and ultimately colony health.