Diseases infecting Honey bees

Honeybees, vital pollinators essential for ecosystem health, are vulnerable to various bacterial, fungal, and viral diseases that pose a threat to honeybee colonies. As many as 60% and 90% of plant species depend upon pollinators to reproduce (Kremen et al. 2007). Since many agricultural crops depend on pollinators, bees play a vital role in the ecology, economy, and food production across all countries (Garcia-Anaya et al. 2016; Hamadache et al. 2017). Apart from pollination services honey bees also provide honey, beeswax, royal jelly, propolis and bee venom (Tej et al. 2017, Greenleaf and Kremen, 2006, Bosch and Kemp, 2002). Similar to other living organisms, honeybees and their products are susceptible to harmful diseases, pests, and pesticides. Successful beekeeping requires regular and timely monitoring of any factors that harm bee colonies. Honeybee diseases have been recognized as one of the primary biotic factors hindering successful beekeeping practices. Bee diseases cause considerable loss for beekeepers resulting in absconding of colonies, reduction in honey and beeswax production. Perez-Sato et al. (2009) stated that the major constraint faced by the beekeepers all over the world is pests and diseases. It is evident that therefore, both beginning and advanced beekeepers should learn to recognize and control bee diseases. Diseases of honey bees are generally classified into brood diseases and adult diseases. Brood diseases are caused by bacteria (American foul brood and European foul brood); virus (sac brood disease) and fungi (chalk brood and stone brood diseases). Adult diseases are mainly caused by protozoa (nosema disease) (Abrol, 1997).

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Introduction

Introduction

Bacterial diseases

An earliest report of bacterial disease was given by Aristotle (384-322 B.C.) in his Book IX of History of Animals. Although several diseases have been observed in honey bee brood, American Foul Brood (AFB) and European Foul Brood (EFB) are considered a global threat to honey bees (Smith et al., 2014; Goulson et al., 2015) [54,31] . The name ''foulbrood" was given to the honey bee disease characterized by a foul odour emitted from brood infected with these pathogens (Schirach, 1769) [52] . Cheshire and Cheyne (1885) [20] further described the symptoms of the disease in the late 19th century and recognized that the cause of the disease was Bacillus alvei. However, White in 1912 described that there are actually two honey bee brood diseases, namely American foulbrood caused by the spore-forming bacterium Paenibacillus larvae (Genersch et al., 2005) [29] and European foulbrood caused by the bacterium Melissococcus plutonius (Bailey, 1956) [8] . American Foul Brood is predominantly found in tropical and subtropical regions. It was first documented by White in 1907 and subsequently recognized as a serious disease affecting various regions across the globe (Bailey and Ball, 1991) [7] .

Consequently, beekeepers and extension specialists must be familiar with the symptoms of this disease and understand how to manage it if necessary. AFB disease is caused by Paenibacillus larvae, which is a gram-positive, sporeforming, facultative anaerobic bacterium (Ash et al., 1994) [6] . It was originally described as Bacillus larvae, and It causes substantial economic losses to beekeepers. The spores of P. larvae are extremely infectious, but colonies differ in their resistance to AFB outbreaks. Honeybee workers are effective for the early identification of AFB (Lindstrom et al., 2005) [41] .

Symptomatology and control

In the early phase of American Foulbrood (AFB) infection, symptoms include isolated capped cells with no brood emergence, visible on the comb. The affected cells typically show dark, sunken, or perforated cappings with punctures made by the investigating adult bees, unlike healthy brood cells which are slightly protruding and fully closed. Infected larvae are brown in color (White, 1907) [60] , and an accompanying foul smell is produced, which is why this disease is also known as "Stinking disease." In advanced cases, the brood displays the pepper box symptom an irregular, patchy brood pattern on the comb resembling a pepperbox, caused by the disease killing and digesting larvae in their cells (Shimanuki, 1997) [53] . The highly resilient endospores represent the sole infectious form of this organism. These spores are infectious exclusively to larvae; adult bees do not become infected upon ingestion of P. larvae spores (Hitchcock et al., 1979; Wilson, 1971) [36, 64] . Larvae exhibit the highest susceptibility to infection during the initial larval stages, specifically 12-36 hours postegg hatching. Within this timeframe, oral consumption of approximately ten spores or fewer through contaminated larval food is sufficient to trigger a lethal infection (Bamrick and Rothenbuhler, 1961; Woodrow and Holst, 1942) [12,65] . To control the disease, oxytetracycline hydrochloride (OTC) or sulfathiazole help prevent multiplication of the agent, though they do not kill the spores. Consequently, multiplication can resume soon after treatment, necessitating repeated treatments at progressively shorter intervals. However, prolonged use of antibiotics poses several issues: (i) antibiotics do not target infectious spores and only alleviate clinical symptoms, thereby concealing the disease without curing AFB; (ii) chemical residues may remain in honey, affecting its quality and safety for human consumption (Lodesani and Costa, 2005; Martel et al., 2006) [42,43] ; (iii) administration of antibiotics to larvae and adult bees may impact the vitality of the brood as well as the longevity of the bees (Peng et al., 1992); and (iv) resistance to OTC and sulfathiazole in P. larvae has become prevalent (Evans, 2003; Piccini and Zunino, 2001; Negash, 2022) [25,50,67] , making new alternatives increasingly necessary (Alippi et al., 2005; Peng et al., 1996; Williams et al., 1998) [48,63] .

European foulbrood disease (EFB)

European foulbrood (EFB) is a bacterial infection that affects honey bee larvae before they reach the capped stage. The disease is characterized by the presence of dead and dying larvae, which may exhibit curled upward postures and can appear brown or yellow, as well as melted, desiccated, or rubbery. European foulbrood has long been reported from the United Kingdom (Cheshire and Cheyne, 1885) [20] and later from the United States of America (White, 1907) [60] in A. mellifera. Subsequently, the disease was documented worldwide, causing serious problems resulting in economic losses to beekeepers. The disease has been observed in many countries including North and South America, Europe, Japan, Australia, India, China, and South Africa (Matheson, 1993) [45] . Wilkins and colleagues reported in 2007 that EFB is the most widespread bacterial brood disease in Great Britain. Incidence of the disease has steadily increased in Switzerland since the late 1990s (Roetschi et al., 2008) [51] .

Symptomatology and control

The causative agent, Melissococcus plutonius, is consumed by honey bee larvae, where it competes for nourishment within the larvae. If the bacterium outcompetes the larva, the larva dies before the cell is sealed. Conversely, if the larvae have adequate food resources, they may develop into healthy adults. G. F. White is credited with first identifying the bacterium responsible for European foulbrood in 1908, initially naming it Bacillus Y, which he later renamed Bacillus pluton (Bailey, 1983) [9] . A patchy brood pattern arises when some larvae die in their cells due to disease, while others survive and become capped, resulting in a spotty or "shotgun" appearance of the capped brood. To manage bacterial diseases, beekeepers utilize a range of antibiotics, including tetracycline, chloramphenicol, sulphonamides, and glycosides. These antibiotics have been associated with residue problems in honey, thereby reducing its quality in the global market. Oxytetracycline hydrochloride (OTC) is an antibiotic acting as a bacteriostatic agent that inhibits the growth of M. plutonius and is used in many countries (Thompson and Brown, 2001) [56] . Since the 1950s, American beekeepers have applied OTC to prevent both European foulbrood (EFB) and American foulbrood (AFB). Although resistance to OTC in Paenibacillus larvae has been documented (Miyagi et al., 2000) [46] , no resistance to OTC has been reported in M. plutonius; research in the UK confirmed susceptibility of this bacterium to OTC (Waite et al., 2003). In Australia, where OTC is also applied against EFB, M. plutonius isolates remain sensitive (Hornitzky and Smith, 1999) [37] . In Great Britain, EFB-infected colonies are treated with OTC or the shook swarm method, whereby bees are transferred to new comb foundation and infected combs discarded; severely infected colonies may be destroyed (Wilkins et al., 2007) [62] . Combining the shook swarm method with OTC reduces the recurrence of clinical symptoms at the colony level (Waite et al., 2003) [58] . Requeening may further assist disease control by interrupting the brood cycle and introducing a more prolific queen (Shimanuki, 1997) [53] .

Fungal disease

Chalkbrood and stonebrood are two fungal diseases that affect honey bee brood. Chalkbrood, caused by Ascosphaera apis, is a prevalent and widespread disease that can significantly decrease the number of emerging worker bees, thereby impacting overall colony productivity. Although the fungus rarely causes the death of infected colonies, it weakens them, resulting in lower honey yields and increased vulnerability to other pests and diseases affecting bees. Engles et al. (2004) [24] also reported that during winter months, fungal diseases weakened honeybee colonies, which led to the development of European foulbrood.

Infected young larvae typically do not exhibit visible signs of illness but die upon being sealed in their cells as pupae. Worker bees often uncap the cells containing deceased larvae, making the mummified brood distinctly visible. Sometimes, they remove the mummified larvae and place them on the hive floor or at the hive entrance. According to Bailey (1967) [10] , honey bee larvae are particularly vulnerable to chalkbrood. A wide array of fungicides has been evaluated for their effectiveness in managing chalkbrood (Heath, 1982; Davis and Ward, 2003) [34,22] . Hornitzky (1999) [37] identified certain chemicals that appeared effective in inhibiting fungal growth, whether in culture or within bee colonies. Unfortunately, none of the tested compounds provided sufficient control to combat the disease. Stonebrood disease, caused by Aspergillus spp., is rarely observed, and consequently, its impact on colony health is not well understood (Jensen et al., 2013) [38] .

Viral disease

Ray stated that viruses are possibly the hidden enemies of honey bees, because, unlike other pathogens, viral infections often occur without distinct clinical disease symptoms (Chen et al., 2006; Martin et al., 2012) [19,44] . Viral particles disseminate among honey bees primarily via two transmission routes: vertical and horizontal (Beaurepaire et al., 2020; De Miranda et al., 2012). In the vertical transmission pathway, viruses propagate from the queen (trans-ovarial), drones (trans-spermal), or during mating (venereal) to the offspring. In contrast, horizontal transmission occurs among colony members of the same generation (Chagas et al., 2019; De Miranda et al., 2012) [16,23] and between different castes, either orally or via direct contact. More than 20 viruses have been recognized to infect honey bees globally, primarily from the Dicistroviridae and Iflaviridae families, including Acute Bee Paralysis Virus (ABPV), Black Queen Cell Virus (BQCV), Kashmir Bee Virus (KBV), Sacbrood Virus (SBV), Chronic Bee Paralysis Virus (CBPV), Slow Bee Paralysis Virus (SBPV), Israeli Acute Paralysis Virus (IAPV), and Deformed Wing Virus (DWV). Among these, IAPV and DWV are particularly significant threats to honey bee health (Amjad Ullah et al., 2021) [57] . The first documented virus among these diseases was Sacbrood Virus (SBV), which remains one of the most widespread viruses affecting honey bees worldwide (Choe et al., 2012) [21] . Sacbrood disease in Apis mellifera was first observed in the USA by White in 1917. SBV is a picornalike virus classified within the Iflaviridae family, genus Iflavirus (Ghosh et al., 1999) [30] . Recent studies indicate that SBV has a broader host range than previously thought, with evidence of interspecies transmission, especially among wild pollinator species (Wei et al., 2022) [59] . The Thai Sacbrood Virus (TSBV), a variant of SBV, was first discovered infecting Apis cerana in Thailand in 1976 and is known to exclusively infect this species. Since its discovery, TSBV has become a major challenge to beekeeping in many Asian countries, causing outbreaks with colony losses exceeding 95% in regions such as Myanmar, Nepal, China, Korea, and India (Yoo et al., 2012) [66] . Infected larvae change color from pearly white to pale yellow and subsequently die, desiccating into dark brown, gondola-shaped scales (Bailey, 1969) [9] . Although SBV can also infect adult bees, they typically show no clear signs of illness (Anderson, 1989) [4] , but may experience reduced lifespan. Sacbrood is most commonly observed in the spring when colonies grow rapidly and many susceptible larvae and young adults are present. Currently, no chemical treatment effectively prevents or controls sacbrood disease. Colonies frequently recover on their own without beekeeper intervention, especially if the infection is established in the region, largely due to the hygienic behavior of the bees.

Protozoan disease Nosema disease

Nosematosis, caused by microsporidia from the genus Nosema, is recognized as one of the well-documented opportunistic infections affecting honey bees (Broadrup et al., 2019) [15] . To date, three distinct microsporidian species linked to honey bee infections have been identified within the genus Nosema. These infections are collectively referred to as nosematosis, regardless of whether they are caused by Nosema apis (Fries, 1993) [27] , Nosema ceranae (Fries et al., 1993) [27] , or Nosema neumanni (Chemurot et al., 2017) [18] . The first two species have spread globally and are responsible for observable symptoms such as diarrhea and a decline in bee populations within the hive (Higes et al., 2006; Klee et al., 2007) [35,39] . In contrast, N. neumanni has been recently identified in Ugandan bees, with its effects on host bees yet to be fully documented. Nosema disease is typically considered one of the most harmful diseases affecting adult bees, impacting workers, queens, and drones alike. Severely affected worker bees lose their ability to fly and may be observed crawling near the hive entrance or trembling atop the frames. Such bees exhibit signs of accelerated aging: their lifespan is significantly shortened, and their hypopharyngeal glands deteriorate, leading to a rapid decline in colony strength. Unfortunately, there is currently no reliable field diagnostic symptom that allows identification of diseased workers without killing them, nor can infected queens be easily recognized by beekeepers (FAO, 2006). However, in cases of severe infection, it may be possible to distinguish healthy from diseased bees by the swollen and shiny appearance of the abdomen in infected workers. The most effective management strategy for Nosema focuses on maintaining colony strength and minimizing stressors. Adequate ventilation and protection against cold and humidity are crucial for colonies and apiaries. Moreover, providing bees with regular opportunities to forage facilitates defecation, which helps reduce the spread of spores within the colony.

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