**1. Introduction**

Bees, including honey bees, bumble bees, and solitary bees, are a prominent and economically important group of pollinators worldwide. In fact, 35% of the global food crop production depends on these pollinators [1], and in Europe, the production of 84% of crop species is, to some extent, dependent on animal pollination [2]. Bees also fulfill an important role in the pollination of wild plants. Thus, habitat fragmentation seems to have a negative effect on pollination and plant reproduction [3]. However, there is still a debate on how to approach the pollen limitation in plant dynamics [4,5]. Furthermore, honey bees provide additional economic inputs in temperate areas where honey production is a fundamental source of income to professional beekeepers.

The honey bee colony is a complex system in which thousands of individuals work together to ensure its sustainability. Multiple factors play an important role in colony viability, such as climate, environment, nutrition, and pathogens, and consequently, in colony pollination and production capabilities. Thus, any deterioration of honey bee colonies has

**Citation:** Alonso-Prados, E.; González-Porto, A.-V.; Bernal, J.L.; Bernal, J.; Martín-Hernández, R.; Higes, M. A Case Report of Chronic Stress in Honey Bee Colonies Induced by Pathogens and Acaricide Residues. *Pathogens* **2021**, *10*, 955. https:// doi.org/10.3390/pathogens10080955

Academic Editor: Giovanni Cilia

Received: 10 June 2021 Accepted: 26 July 2021 Published: 29 July 2021

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a direct negative environmental impact and, in the case of honey bees, economic consequences in countries where there is a large proportion of professional beekeepers as in Mediterranean areas [6].

Many factors have been related to the decline in honey bee colonies over the past decades (revised in [7]). On one hand, the global spread of pathogens related to colony losses entails changes to the ecological and evolutionary dynamics of both pathogens and hosts, often leading to the selection of the most virulent variant of the pathogen and reducing the heterogeneity of the host. A range of treatments exist to combat pathogens and diseases during the last decades. Thus, chemicals that keep *Varroa* mite populations under control may accumulate in different hive matrices, chronically exposing honey bees to the residues of chemicals. Due to foraging activities, honey bees may also be exposed to a wider range of potentially toxic compounds (naturally produced or not), which may also accumulate inside the hive. The action of pathogens and xenobiotics or the combination of both provokes physiological changes, immunosuppression, and gut microbiota disruption on honey bees, which may finally produce the collapse of colonies. These changes may be also influenced by the nutrition quality of the collected pollen, which depends on the seasonal climatological conditions [8–10]. Overall, the impact of pathogens on this decline (mainly parasites and related viruses) may be particularly important [11–13], probably in conjunction with the accumulation of pesticide residues in hive matrices. Thus, the combined effect of two or more such stressors could drive the mortality of individuals, eventually leading to colony collapse [14–16].

Accordingly, we present here a screening study of a professional Spanish apiary that reported a problematic health situation. To investigate the factors that had possibly provoked this situation, we performed a comprehensive evaluation of multiple drivers, including pathogens and pesticides, also analyzing the foraging flora, in an attempt to determine whether new factors should be examined in future monitoring programs.

Severe *Nosema ceranae* infection, in conjunction with the accumulation of acaricides used to control *Varroa* mite infestations in honey bee hives, represents a real threat to colonies, indicating that appropriate preventative strategies should be adopted in honey bee health programs.
