1. Introduction 

In contrast to human medicine, one of the most prominent features of veterinary medicine is that a veterinarian has to deal with a large variety of species. Whereas dogs, cats and horses are common patients in a veterinary practice, the honeybee (Apis mellifera L.) is only rarely in contact with veterinarians as a patient. Official veterinarians and diagnostic laboratories are responsible for the analysis of honey samples and for animal disease control in case of, e.g., American foulbrood, but the general disease prevention and control are done by the beekeepers. The majority of the establishments for veterinary education in Europe accredited by ESEVT (European System of Evaluation of Veterinary Training) offer elective or no training in honeybee veterinary medicine. Only in 24 of 68 surveyed schools honeybee veterinary medicine is part of the curriculum as a separate subject ^[1]. This is a very limited consideration in the curriculum and veterinary practice for a food-producing animal with such a tremendous importance for global agriculture ^[2].

However, in recent years, the honeybee has aroused increasing interest among veterinarians. While only 9 veterinarians held a specialization about honeybees in Germany in 2014 ^[3], five years later, there were 17 bee veterinarians or nearly twice as many experts in this field ^[4]. Honeybee diseases are on the rise ^[5] and at the same time, a decline of honeybee colonies and beekeepers in Europe can be seen ^[6]. More and more, veterinarians publish specialist literature to deal with honeybee diseases ^[7][8]. At the supranational level, the European Parliament in 2008 called for the Commission "to incorporate into its veterinary policy, research into, and actions to tackle bee disease" ^[9], and in April 2011, a European Union Reference Laboratory for Bee Health was designated to coordinate diagnostic methods, disease monitoring and expert training ^[10][11].

In honeybee colonies, a large number of individuals together form a superorganism. Both this unit as well as the individual bee have to be investigated carefully. General principles of herd health management and hygiene concepts are well-known to veterinarians and thus, can be applied to the honeybee. Nevertheless, dealing with diseases in honeybees is different from the normal approach in veterinary medicine. Usual examination techniques, known from mammals, are not applicable to insect species, although the general approach and procedures are similar. Food control is not possible as the feed is provided by the environment and not by the beekeeper or the veterinarian ^[7]. The honeybee is a food-producing animal and assuring the quality of honey is an additional objective for veterinarians and beekeepers.

A variety of biotic and abiotic factors have an impact on honeybee colonies. Belsky et al. presented a broad overview of these stressors: habitat and climate changes, weather, the density of apiaries and food resources, as well as transportation of colonies, are external aspects influencing the honeybee ^[12]. Equally, the bees depend on intrinsic factors such as genetics and queen longevity ^[13]. The intensive agriculture with monocultures decreases the plant diversity and thus, the food supply for the honeybees. Between mass flowering of, e.g., rapeseed (Brassica napus) and sunflower (Helianthus annuus), pollen harvest severely declines ^[12] and limits adequate nutrition. Such an insufficient protein diet weakens the bees in defending against pathogens ^[14]. Various bacteria, microsporidia, viruses and pests cause bee diseases, among which viruses have become more relevant during recent years ^[5].

2. Virus Diseases in Honeybees and Contributing Factors

Viruses, mostly positive single-strand RNA viruses, are the largest class of honeybee infecting pathogens ^[13]. Over 20 bee viruses have been identified to date, including the Acute bee paralysis virus (ABPV), Kashmir bee virus (KBV), Israeli acute paralysis virus (IAPV), forming the ABPV-KBV-IAPV complex, Black queen cell virus (BQCV), Chronic bee paralysis virus (CBPV), Deformed wing virus (DWV) and Sac brood virus (SBV). Detailed reviews about the most important ones can be found in the literature ^{[15][16][17][18]}. Information on symptoms and transmission routes of ABPV-KBV-IAPV, CBPV and DWV, which is relevant to the veterinary diagnostic approach, will be presented in this review. Table 1 provides a summary of taxonomy, symptoms, affected castes and main transmission routes.

Table 1. Overview of selected honeybee viruses (taxonomy, symptoms, affected casts of bees and transmission routes), modified after Vidal-Naquet ^[19].

Legend: RNA = Ribonucleic acid, w = worker, d = drone, q = queen, c = direct contact, o = oral–fecal, vec = vector-borne, ver = vertical, v = venereal, to = transovarial.

3. Veterinary Diagnostic Approach

As mentioned above, honeybee health is often influenced by many different factors ^[7]. Without clinical findings, the appearance of a pathogen in a colony does not constitute a disease. For that reason, the terms overt and covert infections were introduced by de Miranda and Genersch to describe honeybee virus diseases ^[20]. The descriptive terms overt and covert are widely used in insect virology. Overt infections are characterized by obvious clinical findings related to the virus infection and a high virus production rate. Acute and chronic forms are differentiated. In covert infections, low titers of virus particles are present in the absence of clinical symptoms. Vertical transmission allows virus persistence over several generations and competent virus particles can turn into overt infections due to various influencing factors. Persistent infections with low-level virus production can be distinguished from latent infections without virus production ^[20].

From the veterinary perspective, a holistic diagnostic work-up of medical issues in honeybee colonies is important, because the environment, the colony, the pathogens and every bee are each just a link in the chain leading to occurrences of infections ^[7]. Figure 1 shows a detailed plan for diagnostics and management in general. Starting from the environmental observations, followed by an examination of the hive, the colony and the bees, samples are taken, and relevant laboratory diagnostics carried out and further illnesses investigated. The resulting problem list leads to a prognosis and a management plan. The main goal is the healthy colony formed by fit individuals.

Figure 1. Diagnostic approach in bee diseases, © Julia Dittes.

4. Conclusions

A holistic approach to bee disease diagnosis is important to establish a correct and comprehensive diagnosis and save colonies. Disease outbreaks in honeybees are often tied to more complex interactions than in other species. Especially, the biological form of life in a superorganism has to be considered during the entire course of examination and management. Furthermore, the diagnostic techniques and possible ways of treatment are more limited than in the "normal" veterinary patient. There are no vaccinations and less veterinary medical products available for honeybees. The lifetime of an individual bee and the dependence on the season have to be considered.

A detailed and careful investigation is the base of diagnosis, and treatment decisions are to be made focusing on the colony as a whole rather than the individual animal. Depending on the colony location, the number of colonies in an apiary and beekeeping strategies as well as further influencing factors, diagnostics and the management plan have to be adapted to the individual requirements.

Veterinarians can be a valuable asset to the beekeeper because of their ability to prevent, diagnose and treat diseases in various species and in populations. In the future, veterinarians should recognize the important role and also the opportunities they can have within the honeybee sector. Taking the chance offered, the veterinarians may be part of education of beekeepers, part of sanitary audits and part of bee health overall in the veterinary practice, in addition to their official function in Veterinary Authorities.