Drawbacks and Benefits of Hygienic Behavior in Honey Bees (Apis Mellifera L) a Review

Abstruse

Aseptic beliefs in honey bees, Apis mellifera, has been studied for over 80 years with the aim of understanding mechanisms of pathogen and parasite resistance and colony health. This review emphasizes the underlying behavioral mechanisms of aseptic beliefs in honey bees and when known, in other social insects. We explore the relationship between dearest bee hygienic behavior toward diseased brood and Varroa-parasitized brood (Varroa-sensitive hygiene, VSH); the timing of hygienic removal of diseased, Varroa-infested, and virus-infected brood relative to risk of manual that can impact colony fettle; and the methods, utility, and odorants associated with unlike assays used to select colonies for resistance to diseases and Varroa. We likewise provide avenues for future research that would benefit honey bee wellness and survivorship.

Introduction

Hygienic behavior is an important form of social immunity (Cremer et al. 2007) for a number of social insect species. The term hygienic behavior was coined by Rothenbuhler (1964) to depict the procedure of detection and elimination of diseased brood by adult dear bees (Apis mellifera). The term "Varroa-sensitive hygiene" (VSH) was coined more than recently (Harris 2007) to describe the detection and removal of brood infested with the parasitic mite Varroa destructor by honey bees (Harbo and Harris 2005). The behavioral sequence of uncapping and removing the brood, every bit showtime described (Rothenbuhler 1964), is the aforementioned whether the brood is diseased, mite-infested, or dead, but this motor design may be triggered by the detection of dissimilar odorants associated with the health condition of the brood. In dearest bee colonies, elimination of brood consists of adult bees removing and/or cannibalizing the aberrant brood from individual cells, either intact or in pieces, and discarding remains outside the hive; in Reticulitermes termites, information technology consists of cannibalization (Davis et al. 2018) and in Lasius ants of subversive disinfection past dismembering the infected pupa and so disinfecting with venom (Pull et al. 2018). Aseptic behavior helps maintain the health of densely populated insect societies by limiting horizontal transmission of pathogens and population growth of parasites. Workers that destructively eliminate already infected or infested individuals protect the colony, or superorganism, in a similar way to immune cells that protect an organism from pathogen spread throughout the trunk (Cremer and Sixt 2009).

In recent years, research on hygienic behavior in honey bees has increased with the aim of understanding and restoring colony health. The early research on this behavior was in relation to beloved bee resistance to American foulbrood (caused by Paenibacillus larvae) and to chalkbrood (caused by Ascosphaera apis) diseases (Spivak and Gilliam 1998a, b). Focus shifted to the relationship between hygienic behavior and resistance to the parasitic mite, Varroa in the 1990s (Leclercq et al. 2018a; Mondet et al. 2020). This review emphasizes the underlying behavioral mechanisms of hygienic behavior in honey bees and when known, in other social insects. The goals of this review are to (ane) explore the human relationship between beloved bee hygienic behavior toward diseased breed and Varroa-parasitized breed and (2) provide avenues for future research that would benefit honey bee health and survivorship.

Timing of hygienic removal of diseased breed

In the 1930s, the most serious disease of dear bees was American foulbrood. Beekeepers and researchers (Park 1937) noted that some colonies did not succumb to this disease and they considered these colonies to be resistant. They observed that "the bees sometimes remove and dispose of larvae very soon afterwards they die, thus eliminating the show." Following these observations, it was determined that kickoff instar larvae derived either from resistant or from susceptible colonies were equally susceptible to American foulbrood, but larvae inoculated more than 2 days and 5 h later hatching from the egg did not become infected (Woodrow 1942). It was subsequently observed that the adult bees from resistant colonies removed the majority of the diseased brood from the cells whereas bees from susceptible colonies did not, and concluded that colony resistance depended on behavioral removal of diseased brood past adult bees, rather than physiological resistance of the brood (Woodrow and Holst 1942). These findings were later confirmed past Rothenbuler and others (Spivak and Gilliam 1998a).

The experiments by Woodrow and Holst as well revealed that the timing of adult bees' removal of the infected brood was central to understanding the apparent resistance (Woodrow and Holst 1942). After suspending known quantities of P. larvae spores in the food surrounding private get-go instar larvae, they noted that the resistant colonies started eliminating the infected larvae on the sixth day after inoculation (the day the cell containing a 5th instar is capped with wax) and had removed all of infected brood by day xi. They nerveless intact brood that was removed from the hive past the bees and found the brood had merely the not-infectious rod form of P. larvae, indicating the bees were removing the brood from the nest while the non-infectious rods were multiplying within them. In dissimilarity, bees in a susceptible colony did not begin removing infected brood until 24-hour interval ix after inoculation, and not all of the diseased brood was removed from the cells; some was uncapped merely afterwards recapped with wax. The bacterium reached the highly infectious spore phase in the remaining brood of the susceptible colonies, and bees from susceptible colonies were sometimes removing the breed while bacteria were infectious, potentially spreading the illness. Woodrow and Holst concluded that "…resistance to American foulbrood in the honey bee colony consists in its ability to detect and remove diseased breed earlier the causative organism… reaches the infectious spore phase in the diseased larvae." Observations of hygienic activity against brood infected with Mellisococcus plutonius prompted J. I. Hambleton to study that "American foulbrood resistant strains are highly susceptible to European foulbrood" (Root 1966). The apparent susceptibility may have been because the bees were actively treatment younger honey bee larvae which take infectious M. plutonius just non-infectious P. larvae; this possibility requires further study.

The timely detection and removal of brood was demonstrated after bees were challenged with a dissimilar pathogen, the chalkbrood mucus (Invernizzi et al. 2011). The most hygienic colonies, those that uncapped pin-killed brood (run into section on "Assays" below), besides tended to uncap cells and cannibalize the chalkbrood-infected brood before the brood was consumed by fungal mycelia and became infectious "mummies." Colonies with numerous intact chalkbrood mummies on the bottom lath of the colony indicated that bees were not hygienic because the infected brood was removed afterward it reached the spore stage, increasing the risk of horizontal manual.

The timely elimination of infected brood is important for other social insects, such as colonies of the invasive garden ant, Lasius neglectus (Tragust et al. 2013; Pull et al. 2018), and the subterranean termite, Reticulitermes flavipes (Davis et al. 2018). These social insect colonies nest in the soil where they may get exposed to the soil-borne fungal entomopathogens such as Metarhizium. Adult ants in the genus Lasius groom infectious conidiospores of Metarhizium from the brood into infrabuccal pouches and disinfect the fungal pellets in their pouches with their antimicrobial venom (Tragust et al. 2013). If the fungus is undetected on the cuticle of some ants and germinates into the pupal body, upon detection of the infected pupa, the developed ants unpack it from its cocoon, dismember it, and disinfect the pupal remains with venom (Pull et al. 2018). The detection and subversive disinfection of the infected pupa occurs when the pathogen is in the non-infectious incubation flow, like to how beloved bees detect and remove infected, but not infectious pupae from the nest. The destructive disinfection prevented the pathogen from completing its life cycle, thus preventing intra-colony disease manual (Pull et al. 2018). In R. flavipes termite colonies, Metarhizium conidiospores are groomed from infected individuals, only once the mucus enters the torso, termites cannibalize the infected nestmate (Davis et al. 2018). It was not determined if cannibalism occurred during the non-infectious incubation period; nevertheless, the switch from sanitary prevention (allo-grooming) to elimination (cannibalism) was articulate, suggesting that termites besides are able to notice the stage of infection (Davis et al. 2018).

In sum, the timing of detection and emptying of the diseased brood by adult social insects seems to exist a critical component in preventing pathogen transmission inside these social insect colonies, and thus in colony-level resistance. It would be to the pathogen's advantage for individuals inside the colony to handle diseased brood when infectious considering it would increase the gamble of pathogen transmission, whereas it would be to the colony's advantage if individuals eliminate the brood before it is infectious because it would limit pathogen spread. Whether the timing of the elimination of brood when mite-infested is similarly important is discussed below.

Assays for dearest bee hygienic behavior

Bioassays for hygienic beliefs were recently reviewed in depth (Leclercq et al. 2018a) and thus, only some points are highlighted here. The all-time fashion to determine if a colony of honey bees (or other social insects) can observe and remove diseased brood is to challenge private bees or larvae, or an entire colony, with a known dose of a pathogen and observe the response of adult nestmates to infected individuals. Due to the risks involved in challenging honey bee colonies with potentially lethal and highly infectious pathogens such as P. larvae, researchers began exploring assays that would not involve inoculating larvae with a pathogen. As a proxy for diseased breed, cyanide-killed brood was presented in colonies to facilitate experiments using lines of bees already selected for resistance and susceptibility to American foulbrood (Jones and Rothenbuhler 1964). Later, researchers began screening unselected colonies for hygienic behavior using freeze-killed brood (Spivak and Gilliam 1998b), or pin-killed brood (Newton and Ostasiewski 1986).

How quickly a colony could detect and remove the experimentally killed brood did not e'er represent with the colony's power to remove diseased breed (Gilliam et al. 1983). Thus, after screening colonies using a freeze-killed (or pivot-killed) brood assay, it is important to afterward challenge colonies with a pathogen to decide if they are behaviorally resistant (Spivak and Reuter 2001a). As a recent example, an imperfect correspondence was found between the removal of freeze-killed breed and physiological resistance to chalkbrood in Australian dearest bee colonies (Gerdts et al. 2018). Of 649 colonies tested for aseptic behavior using the freeze-killed brood analysis, 16% were considered highly hygienic (removed 95% of the freeze-killed brood within 24 h), suggesting they should non have signs of disease within the colony, but in fact, 23% of these highly hygienic colonies presented signs of chalkbrood disease. These results provide an instance of how the freeze-killed brood assay does not fully predict behavioral resistance in the test population.

Of note is that colonies that remove less than 95% of the freeze-killed brood inside 24 or 48 h tend to remove petty, if any, pathogen infected brood later on challenge; they tend non to be resistant to American foulbrood or chalkbrood (Yard Spivak, unpublished data). This observation begs the question of why highly hygienic colonies are rare in nature and whether there are associated fitness costs with the trait (Spivak and Gilliam 1993; Mondragon et al. 2005; Bigio et al. 2014; Leclercq et al. 2017). Nosotros speculate that resistance does not depend solely on hygienic beliefs but likely involves a combination of other physiological factors in dear bees, including the immune response (Evans and Spivak 2010), transgenerational allowed priming (Hernandez Lopez et al. 2014), microbiome customs (Raymann and Moran 2018), antimicrobial activity of larval food (Rose and Briggs 1969; Borba and Spivak 2017), presence of propolis in the nest (Borba et al. 2015), and other factors yet to be discovered.

In sum, and as pointed out previously (Leclercq et al. 2018b), assays for aseptic beliefs, like the freeze-killed or pin-killed brood assays, are not necessarily useful predictors of pathogen resistance in a colony or population of colonies. They are useful to screen colonies for the ability of the adult bees to quickly remove dead brood (due east.g., > 95% removal inside 24 h for the freeze-killed brood test) and these colonies can be subsequently challenged to quantify pathogen resistance. In other words, the assays are used to narrow downward the number of colonies to be challenged, to increment the chances of finding resistant colonies.

Hygienic behavior in relation to Varroa

Although some ant and termite colonies accept brood parasites (Korb and Fuchs 2006; Lachaud et al. 2016), studies of their hygienic response are limited; due east.g., the ant Ecatomma tuberculatum detects and removes parasitic wasps (Perez-Lachaud et al. 2015) and other nest intruders (Perez-Lachaud et al. 2019). Thus, this section will concentrate on honey bees' response to Varroa destructor. When V. destructor spread through A. mellifera colonies in Europe and Northward America, researchers looked to this mite's original host species, A. cerana, to determine how it survived without succumbing to the parasite. A number of potential resistance mechanisms were described (Boecking and Spivak 1999), hygienic behavior existence ane of them (Peng et al. 1987a; Peng et al. 1987b; Rath 1999). In Apis cerana, Varroa reproduces only on seasonally produced drone breed and does non reproduce on worker brood. If the mite infests worker brood (or are experimentally introduced onto worker pupae), the pupa dies, due to a toxic salivary gland secretion injected by mite (Zhang and Han 2018) and the bees hygienically remove the dead brood from the nest (Page et al. 2016). The signal or cue from the dying pupa was termed "altruistic suicide" and the removal "social apoptosis"; the combination was hypothesized to increase inclusive fitness benefits to the colony (Page et al. 2016). In A. mellifera, Varroa reproduces successfully on both drone and worker brood, and worker pupae do not dice if infested with the mites, although they could if also infected with high enough virus levels (Martin 2001; de Miranda and Genersch 2010; Dainat et al. 2012).

After Varroa spread through Europe, A. one thousand. carnica colonies in Frg were tested for their power to detect and remove Varroa-infested brood (Boecking and Drescher 1992). The removal of infested breed would be a course of mite resistance because it would increase mite mortality or disrupt mite reproductive success (Leclercq et al. 2018a). In the Boecking and Drescher report (Boecking and Drescher 1992), the colonies were not previously selected for hygienic behavior or mite resistance. After experimentally introducing mites into recently capped brood cells, 29% of the infested brood were removed after 10 days when one mite per cell was introduced and 55% were removed when two mites per cell were introduced, indicating that in fact, some A. mellifera colonies could detect and remove some mite-infested pupae, fifty-fifty though they were naïve hosts to this parasite.

Afterward, it was explored whether colonies selected for hygienic behavior based on the freeze-killed breed assay would be able to detect and remove pupae infested with Varroa (Spivak 1996). Two lines of bees were challenged with Varroa, one bred over several generations for rapid hygienic behavior (colonies that removed > 95% of the freeze-killed brood within 48 h, the Minnesota Hygienic bees) and ane bred for tiresome aseptic behavior (colonies that removed twenty–30% of freeze-killed brood within 48 h). Thus, the test population was more bimodal than continuous in its hygienic response. In 3 of four years, the rapid or highly hygienic colonies removed over sixty% of the experimentally mite-infested brood by the 10th day later one mite per cell was introduced into recently sealed brood. The slow or non-aseptic colonies removed ten–20% of the infested brood in the same years (Figure 1).

A significant negative relationship between the results of the freeze-killed brood assay and mite population growth over one season was found in the UK (Toufailia et al. 2014). The statistical significance was driven past viii of the 42 colonies that removed > 95% of the freeze-killed breed within 48 h and were thus highly hygienic, over again confirming that screening for these highly aseptic colonies based on the freeze-killed brood analysis volition help locate colonies with a relatively college potential of removing mite-infested brood. Colonies that removed less than 95% of the freeze-killed brood showed no significant human relationship between aseptic behavior and mite growth (Toufailia et al. 2014), which was also observed in Mexico (Mondragon et al. 2005).

A large population derived from various sources of colonies in western Canada was selected over 3 generations for hygienic behavior using either the freeze-killed brood test or peptide biomarkers from bees' antennae, with the goal of testing the utility of marker-assisted selection for hygienic behavior (Guarna et al. 2017). 11 of the 13 protein markers were linked to hygienic beliefs (including two linked to VSH, run into department below), and two were linked to grooming beliefs. This remarkable study showed two things: that protein biomarkers tin be used successfully in breeding bees (and possibly other livestock) and that compared to unselected stocks, colonies selected using either the freeze-killed breed assay or peptide biomarkers had increased hygienic behavior, showed no loss of love production, and had increased survival when challenged with either P. larvae or Varroa.

Researchers in Germany take used the pin-killed breed assay in breeding programs to successfully reduce mite loads. Other researchers reported no correlation betwixt the removal of freeze-killed or pin-killed brood and the mite infestation of colonies, reviewed in Locke (2016). Nevertheless, the latter studies used these assays to try to make up one's mind the mechanism of resistance of a population, not to screen and narrow down the number of colonies for subsequent challenge to quantify potential resistance, or to use in convenance programs.

In sum, the freeze-killed and pin-killed brood assays for aseptic behavior are useful screening tools to notice colonies that may remove diseased and mite-infested brood upon subsequent challenge. For Varroa in item, selecting bees based on these assays will yield colonies with lower mite loads relative to unselected colonies (Spivak and Reuter 1998; Spivak and Reuter 2001b; Büchler et al. 2010; Guarna et al. 2016; Guarna et al. 2017) but to date, selection using these assays has non resulted in populations resistant to mites; that is, populations that do not require treatment to survive. Thus, these field assays should not be used equally sole tests or indicators of Varroa resistance, equally other traits contribute to various degrees to this resistance, reviewed in Mondet et al. (2020).

Varroa -sensitive hygiene

Varroa-sensitive hygiene is a specialized term for the hygienic trait in which beloved bees detect and remove brood specifically infested with Varroa. VSH activity is largely the same equally that of the hygienic trait; the bees perform the hygienic behavioral sequence of uncapping and removing brood, but the removal in this case is triggered by the detection of mite-infested breed, rather than diseased or dead brood. Note that the term VSH likewise is often used for lines of bees bred for enhanced expression of the trait. Bees that express high levels of VSH testify clear resistance to Varroa in that they practise non require treatments to survive mite infestations, as has been demonstrated by USDA researchers in Baton Rouge, LA, U.s.. Of annotation, a critical experiment has not been conducted which could clarify the relationship betwixt colonies selected for VSH and those selected for hygienic beliefs based on the freeze-killed or pin-killed brood assay. Information technology would exist informative to challenge colonies that limited VSH with P. larvae or A. apis pathogen to determine if bees that limited VSH but respond to mite-infested brood, or if they also detect and remove diseased breed and thus, are hygienic in full general.

This history of bees with VSH-based mite resistance, and how it has been selected over the years is somewhat convoluted. Harbo and Hoopinger began by searching for colonies that displayed resistance to Varroa with no a priori assumptions near which traits would be involved (Harbo and Hoopingarner 1997). They inoculated 43 colonies with known quantities of Varroa at the starting time of the season and quantified mite loads after ~ 10 weeks. They found iii colonies with fewer mites at the end of the exam than were originally inoculated. Afterward running a number of tests to decide the mechanism for active resistance confronting the mites, they ended that the gene that best explained the apparent resistance was the low reproductive success of the mites on worker brood. They selectively bred a line from several of the highest-performing colonies and gave it the proper name suppression of mite reproduction or SMR. The mechanism for how bees or brood from the SMR colonies could reduce mite reproductive success was unknown. The mites entered worker brood cells to feed and reproduce; yet, the authors reported that the mites died in the cell without reproducing, produced no progeny, produced males only, or produced progeny also late to mature (Harbo and Harris 1999).

SMR colonies removed > 95% of the freeze-killed brood inside 48 h, which indicated that the bees were expressing a high level of hygienic beliefs (Ibrahim and Spivak 2006). These results were surprising because the SMR line was selectively bred for reduced mite reproduction, not for hygienic beliefs (Harbo and Harris 1999). It was hypothesized that the SMR bees could be detecting and removing pupae on which the mites were reproducing, leaving pupae with mites that did not reproduce successfully. This hypothesis was tested in two ways. In one test, recently capped brood combs with known percentages of mite infestation were introduced into colonies with and without the SMR trait (Harbo and Harris 2005). Later on 8 days, the SMR colonies had significantly lower mite infestation (2%) compared to the controls (ix%). Of the mites that remained, the SMR colonies had a lower proportion of reproductive mites, 20% vs. 71%, suggesting the SMR bees were targeting pupae with reproductive mites. In a 2d examination, mites were experimentally introduced onto private pupae of two types of colonies: SMR bees and Minnesota Aseptic bees that had been selected using the freeze-killed breed assay (Ibrahim and Spivak 2006). The SMR colonies removed significantly more mite-infested pupae than colonies from the hygienic line. Together, these findings indicated that bees bred for SMR express hygienic behavior and that adult bees may selectively remove pupae infested with reproductive mites. In addition, hygienic activity may disrupt the reproduction of mites on targeted pupae (Kirrane et al. 2011), and some of these mites may re-invade other open brood cells and after be counted as non-reproductive. In 2007, Harris renamed the line from SMR to VSH to reverberate that the main mechanism that leads to not-reproductive mites (and thus mite resistance) patently is hygienic behavior rather than the ability of the breed to somehow reduce mite reproductive success.

A farther finding was that the reproductive success (fertility and number of viable female offspring) of Varroa on pupae not hygienically removed by bees was significantly lower in VSH colonies than in Minnesota Hygienic colonies (Ibrahim and Spivak 2006). This suggests an additional result of VSH pupae that reduced mite reproductive success, indicating that hygienic behavior alone was not completely responsible for the mite resistance in this line. Recent studies also propose a brood outcome that suppresses mite reproduction (Wagoner et al. 2018; Wagoner et al. 2019). Such an effect originating from breed could be a valuable trait to support mite resistance. However, a brood-based effect was non increased reliably in an endeavour to select and brood for it (Villa et al. 2016).

The methods used for selecting Varroa-resistant bees past the USDA researchers in Baton Rouge has varied through time. Progress originally came by quantifying the relative population growth of the mites over a short period, typically ~ 10 weeks (Harbo and Hoopingarner 1997). Colonies later were selected based on the frequency of non-reproductive mites in them, after this factor was determined to be the main determinant of resistance (Harris and Harbo 2000). The frequency of non-reproductive mites has been the nigh extensively used benchmark for pick and continues to be used today. After the function of hygiene was discovered, some choice involved introducing combs containing known percentages of mite-infested brood and quantifying the decrease in infestation after 1 calendar week (Villa et al. 2009). This method requires more replication to be accurate when colonies being tested have depression mite resistance (Villa et al. 2017). Feel with these iii methods suggests that highly mite-resistant colonies (i.e., those that require no treatment against Varroa) generally have mite population growth of ≤ 1.0 per reproductive cycle (Harbo and Harris 2009) and ≥ threescore% of mites that are non-reproductive, and remove ≥ lxxx% of mite-infested brood afterward 1 week (Danka et al. 2016).

Measuring mite population growth, the frequency of non-reproductive mites or the removal of mite-infested breed is technically difficult and tiresome, and these issues accept limited bee breeders' pick for the VSH trait. To appointment, there is no simple field analysis that will yield the high Varroa resistance of the bees selected with these technical methods. Choice based on the freeze-killed breed analysis will non exist sufficient (Danka et al. 2013) (and discussed before). Some resistant populations, particularly the "survivor" stocks that thrive without treatment indicate that aseptic behavior, however assayed, may not be the main mechanism for all populations, e.g., African populations in Africa and the neotropics, plus populations in Sweden, France, and the Arnot Forest in New York (Locke 2016; Mondet et al. 2020). Populations of highly resistant bees, including survivor populations (Locke 2016) and Russian bees (Rinderer et al. 2001), display non-reproduction of mites or low mite population growth, but the lack of, or tiresome, mite increment may exist due to a combination of inter-related factors that range from life-history traits (e.thousand., high swarming frequency) to distinct behavioral traits (VSH or grooming).

Timing of removal of Varroa-infested and virus-infected breed

Information technology is non known if the timing of detection and removal of Varroa-infested brood is every bit disquisitional of a component in preventing parasite transmission as information technology is for pathogen manual during removal of diseased brood. This issue has not been studied. The timing of hygiene may non depend on the presence of the mite per se just on the virus levels in the pupae, such as deformed wing virus (DWV), which are induced to replicate and vectored past the mites equally the mite feeds. The bees' removal of mite-infested brood tends to increase 72 h after the larvae is capped with wax (Spivak 1996; Harris 2007), which is when the larva initiates metamorphosis into a pupa and when the mite feeds and begins reproducing in the cell (Donzé and Guerin 1994; Martin 1995; Donzé and Guerin 1997). The removal process can continue for the duration of pupal development (Vandame et al. 2002). Aseptic handling of the virus-infested brood could either increment or decrease transmission of the pathogen. The risk of increasing manual would depend on the type and level of the virus infection, which could depend on the stage of bee pupal development, and the relative infectivity and virulence of the virus to the bees. This area requires testing because these factors are only beginning to exist understood in honey bees (Brutscher et al. 2016; Grozinger and Flenniken 2019).

A few studies have shown a link between aseptic beliefs and reduction in virus-infested brood. Aseptic colonies, determined based on the pin-killed brood analysis, tended to remove worker pupae infected with DWV (Schöning et al. 2012). Highly hygienic colonies, determined based on the freeze-killed brood analysis, also had significantly lower levels of DWV in addition to lower mite population growth over the flavour (Toufailia et al. 2014). Brood infected with DWV produced chemic compounds that when experimentally applied to brood elicited hygienic beliefs (Wagoner et al. 2019). The correspondence between mite infestation, virus load, and stimulus intensity has not been explored relative to the timing of hygienic detection and removal by honey bees. Understanding the relationship amidst these factors volition not exist easy, nor necessarily robust from ane population of bees to the next, but is worthy of study.

Mechanisms of detection of diseased and Varroa-infested breed by adult bees

To study the mechanisms underlying how adult dearest bees discover diseased breed earlier the pathogen reaches the infectious spore stage, it was hypothesized that hygiene was mediated by olfactory stimuli emitted from diseased breed (Spivak et al. 2003). Information technology was not known if the odorant was passively or actively emitted, i.e., whether it was a cue or signal (Maynard Smith and Harper 2003; Leonhardt et al. 2016). A number of neuroethological methods were employed to test the olfactory hypothesis, using chalkbrood every bit the test pathogen, and the line of dearest bees selectively bred for hygienic behavior based on the colony response to a freeze-killed brood analysis (Arathi et al. 2000; Masterman et al. 2000; Masterman et al. 2001; Gramacho and Spivak 2003; Spivak et al. 2003; Arathi et al. 2006; Swanson et al. 2009). Based on the results of these experiments, it was concluded that bees from hygienic colonies were able to discover and discriminate betwixt odors of diseased and salubrious brood at a lower stimulus level compared to bees from non-hygienic colonies. Not-hygienic bees would, and do, observe and remove diseased breed, but only when the pathogen is infectious and the stimulus level is very high (Figure two), increasing the risk of pathogen transmission.

Similarly, observations by USDA scientists revealed different reactions to Varroa infestation from bees with VSH-based hygiene versus from bees that were not selected for hygiene. Unselected bees tended to detect and remove dead or highly diseased breed just non alive, mite-infested brood on the same comb. Exposing the same brood comb to VSH bees, however, resulted in hygiene confronting mite-infested brood that the unselected bees ignored (Figure 3). This example illustrates how hygienic responses to mite-infested brood and illness-infected brood both vary depending on the olfactory sensitivity of the adult bees.

A complementary approach to quantifying olfactory sensitivity of adults is to identify odorants emitted by the brood when expressionless, diseased, or parasitized. There take been several studies that attempted to identify the compounds emitted by mite-parasitized brood that elicit hygienic removal of the brood (Nazzi et al. 2004; Schöning et al. 2012; Mondet et al. 2016; Wagoner et al. 2019). To appointment, results indicate there may be multiple compounds associated with Varroa-infested or disease-infected brood, which may vary equally a office of the genetic origin of the bees (Wagoner et al. 2018) or of the experimental methods used past different researchers (reviewed in Mondet et al. (2020)).

The capability of A. mellifera to answer to live, mildly injured brood is seen when pupae are uncapped because of infestation by wax moth (Galleria or Achroia spp.) larvae. This action suggests that a behavioral defense which predated Varroa is now existence used as a primary tool of social immunity against the mite (Villegas and Villa 2006; Martin et al. 2019). The action also is notable considering it evidently represents a response only to stimuli produced by the pupa. Such stimuli (rather than stimuli from the wax moth larva) are suggested considering the uncapping occurs for pupae within a narrow age range (typically those with white, pinkish, or purple optics). These pupae are the same age as those targeted by hygiene against Varroa, suggesting that hygiene is closely related to pupal development. Stimuli initiated past a response of mildly injured or "disturbed" brood may be quantitatively and qualitatively different from stimuli produced from dead or severely injured or diseased brood. These latter stimuli may be associated with broader aseptic responses rather than more narrowly targeted hygiene such as VSH.

It is known that social insects tin can notice sick brood while non infectious, but it is not known if the intensity of the stimulus (cue or betoken) is low when detected and eliminated, and and so increases in intensity equally it reaches the infectious stage. The correspondence between affliction load and stimulus intensity has been studied in ants. In Lasius, changes were plant in the cuticular hydrocarbon profiles of ants infected with the fungal pathogen Metarhizium (Pull et al. 2018). Infected ant pupae had higher relative abundances of four cuticular hydrocarbons compared to uninfected control pupae, and infected pupae that were unpacked by adults had higher relative abundances of those four plus an additional four cuticular hydrocarbons compared to control pupae, suggesting that these compounds may increment in affluence over the course of infection. The compounds on the surface of the ants were long-chained cuticular hydrocarbons (carbon chain length C33–35) with depression volatility and were distinct chemically from the compounds that induce undertaking, or the removal of corpses in ants (Wilson et al. 1958). 2 of the four cuticular hydrocarbons that were increased on infected pupae had higher abundances on virus-infected honeybees (Baracchi et al. 2012) and were similar to the compounds establish by Wagoner et al. (2018, 2019) on infected beloved bee pupae that were detected and removed past aseptic bees. It was speculated that these compounds may be "conserved sickness cues" in social insects, selected over evolutionary time to enhance inclusive fitness of the diseased private and to enhance direct fitness of the colony (Pull et al. 2018).

An untested hypothesis about the part of breed odorants that nosotros propose is that adult dear bees may have a chemic recognition template of "healthy brood" and thus are able detect numerous compounds coming from any "abnormal" brood, whether expressionless, diseased, or parasitized. Specific odorants, however, may initiate responses that can be differentiated into hygienic response to pathogens or mites. This "healthy brood" template would exist analogous to how the immune organisation detects self vs foreign using blueprint recognition receptors (Medzhitov and Janeway 2002; Kawasaki and Kawai 2019) or how social insects recognize nestmates from non-nestmates using cuticular hydrocarbons (Perez-Lachaud et al. 2015; Leonhardt et al. 2016). The stimulus from good for you brood would likely exist a alloy of chemical compounds that vary with the age of the brood (Le Conte et al. 1990; Le Conte and Hefetz 2008; Mondet et al. 2020). Adult bees from hygienic colonies, while inspecting larvae and wax-capped breed with their antennae, would be able to discover and discriminate salubrious from any abnormal brood because of different brood odorants. The specific chemical nature of the odorants of the abnormal brood may be less important to the bees compared to its relative irregularity from the healthy breed template.

Recapping

Colonies that are apparently resistant to Varroa brandish loftier frequencies of cell recapping; that is, the wax capping over a pupa is opened, so recapped with wax (Boecking and Spivak 1999; Aumeier et al. 2000; Harris et al. 2012; Oddie et al. 2018; Martin et al. 2019). Recapping by the bees is axiomatic when the prison cell capping is experimentally removed and inspected from underneath; if information technology has been recapped, there is a round area with no silk lining. It was postulated that uncapping and recapping of breed cells would disrupt mite reproduction in various ways (Leclercq et al. 2018a). Uncapping and recapping has been noted since early studies on resistance to American foulbrood (Woodrow and Holst 1942) and thus, this behavior is non specific to mite-infested breed. Recapping has been observed in relation to the removal of freeze-killed brood (Spivak and Gilliam 1993) and the process of uncapping and recapping was interpreted every bit inefficient task partitioning among bees of different hygienic tendencies (Arathi et al. 2006). Bees that uncapped the breed were not the same as those that removed it: the uncappers had higher olfactory sensitivity compared to the removers (Gramacho and Spivak, 2003). These information propose that some bees may be detecting the stimuli from the dead (diseased or mite-infested) breed and chew a pigsty in the jail cell capping. Other bees with lower olfactory sensitivity may epitomize the cell, not detecting the problem within. At the other extreme, excessive uncapping is seen in some colonies where the brood appears to exist healthy; this situation may bespeak dysfunction between the components of hygiene (Figure 4).

The uncapping-recapping behavioral sequence requires further report, particularly in relation to mite infestation, where its function and utility equally an indicator of hygienic behavior or mite resistance is still unclear (van Alphen and Fernhout 2019; Oddie et al. 2019). Information technology is likely that the corporeality of recapping reflects the interplay betwixt brood stimulus intensity and adult bee olfactory sensitivity of the test colonies, and may involve differences of olfactory sensitivities among patrilines within colonies.

Conclusions

1
The freeze-killed and pivot-killed breed assays for aseptic behavior are useful screening tools to find colonies that may remove diseased and mite-infested breed upon subsequent challenge with a specific pathogen or Varroa; nevertheless, these field assays should not be used equally sole tests or indicators of pathogen or Varroa resistance. Selection using these assays for aseptic beliefs has not resulted in populations resistant to mites; that is, populations that do non require treatment to survive.
2
It would be helpful to clarify terms, for example, when Varroa-sensitive hygiene (VSH) is being referred to equally a trait vs a bred line of bees. Referring to VSH equally distinct trait, dissimilar from hygienic beliefs (sometimes abbreviated HYG) is more disruptive than helpful as they involve the same behavioral sequence of detecting, uncapping, and removing. The deviation is in specificity: VSH refers to hygienic behavior directed to mite-infested brood. Hygienic beliefs is a more general term for removal of dead, diseased (including virus-infected), and mite-infested brood. However, the critical test of challenging colonies bred for VSH with a pathogen to decide the specificity of the response has not been conducted.
3
Enquiry is required on the timing of hygienic removal of Varroa-infested and virus-infected brood relative to risk of further virus transmission. More work is needed on the potential correspondence between brood stimulus intensity and level of pathogen infectivity in relation to hygienic detection and removal of the infected brood. It increases colony fitness when individuals eliminate the brood before information technology is infectious by limiting pathogen manual; it may decrease colony fettle to handle diseased breed when infectious, depending on the infectivity of the pathogen and the health status of the colony.

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Acknowledgments

M. Spivak acknowledges previous funding from the National Science Foundation for studies on hygienic behavior (NSF IBN 9307026, 9722416, and 031991).

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Affiliations

Department of Entomology, University of Minnesota, 1980 Folwell Ave., St. Paul, MN, 55018, USA

Marla Spivak
Beloved Bee Breeding, Genetics, and Physiology Laboratory, USDA-ARS, 1157 Ben Hur Rd., Baton Rouge, LA, 70820, USA

Robert G. Danka

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One thousand. Spivak conceived of ideas for the manuscript; R. Danka contributed additional ideas; both authors wrote the manuscript.

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Correspondence to Marla Spivak.

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The authors declare that they take no conflict of interest.

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Perspectives sur le comportement hygiénique d' Apis mellifera et d'autres insectes sociaux.

immunité sociale / Varroa Sensitive Hygiène / odeurs chimiques / fourmis / termites.

Perspektiven für das Hygieneverhalten bei Apis mellifera und anderen sozialen Insekten.

Soziale Immunität / varroa-sensitive Hygiene / chemische Duftstoffe / Ameisen / Termiten.

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Spivak, M., Danka, R.G. Perspectives on hygienic beliefs in Apis mellifera and other social insects. Apidologie 52, i–16 (2021). https://doi.org/10.1007/s13592-020-00784-z

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Received: 26 February 2020
Revised: xiv May 2020
Accustomed: 05 June 2020
Published: 19 November 2020
Result Date: February 2021
DOI : https://doi.org/x.1007/s13592-020-00784-z

Keywords

social immunity
Varroa-sensitive hygiene
chemic odorants
ants
termites

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