Molecular Pathogens 2024, Vol.15, No.3, 129-141 http://microbescipublisher.com/index.php/mp 133 temperatures may facilitate the spread of invasive species and parasites that negatively impact bee health (Pirk et al., 2016). The combined effects of these changes can lead to reduced foraging efficiency and increased mortality rates among honeybees. 4.3 Pollution and contaminants Pollution and environmental contaminants, including pesticides and other agrochemicals, have been widely documented to affect honeybee health adversely. Bees are exposed to a variety of chemicals through their foraging activities, which can impair their immune systems and make them more susceptible to diseases and parasites (O’Neal et al., 2018; García-Valcárcel et al., 2019). The interaction between pesticides and pathogens is particularly concerning, as exposure to certain chemicals can increase the toxicity of others and reduce bees' resistance to infections (Centrella et al., 2019). Moreover, pollutants can accumulate in bee habitats, leading to chronic exposure and long-term health effects (Lin et al., 2023). 4.4 Changes in floral resources Changes in floral resources, driven by both natural and anthropogenic factors, significantly impact honeybee populations. The decline in the abundance and diversity of flowers due to habitat loss, agricultural practices, and invasive species reduces the availability of essential nutrients for bees (Jones et al., 2021). Seasonal variations in floral resource availability can create periods of food scarcity, particularly during critical times of the year when bee populations are at their peak (Requier et al., 2015). Enhancing floral diversity and availability through agri-environmental schemes and sustainable farming practices can help mitigate these effects and support bee health and productivity (Samuelson et al., 2020). In conclusion, environmental changes, including habitat loss, climate change, pollution, and alterations in floral resources, play a critical role in the decline of honeybee populations. Addressing these challenges requires a multifaceted approach that includes habitat restoration, sustainable agricultural practices, and effective management of pollutants and pests. By understanding and mitigating these environmental stressors, we can help ensure the survival and health of honeybee populations, which are vital for ecosystem services and agricultural productivity. 5 Combined Effects of Multiple Stressors 5.1 Interactions between pathogens and pesticides The interaction between pathogens and pesticides has been shown to significantly impact honeybee health. For instance, studies have demonstrated that the combination of the microsporidian parasite Nosema and neonicotinoid pesticides like Thiamethoxam and Imidacloprid can lead to increased mortality and reduced immunocompetence in honeybees (Grassl et al., 2018; Alaux et al., 2020). These synergistic effects are particularly concerning as they can exacerbate the decline in bee populations. Additionally, the combination of Nosema ceranae and the insecticide fipronil has been found to have a synergistic effect on honeybee survival, especially when stressors are applied at the emergence of honeybees (Aufauvre et al., 2012). This highlights the importance of considering the sequence and timing of exposure to multiple stressors. 5.2 Combined impact of environmental changes and pathogens Environmental changes, such as habitat loss and climate change, combined with pathogen exposure, can further stress honeybee populations. The Bumble-BEEHAVE model, which simulates the impact of multiple stressors on bumblebee populations, has shown that environmental changes can interact with pathogens to affect bee numbers and population dynamics (Becher et al., 2018). This model underscores the complexity of these interactions and the need for a holistic approach to understanding and mitigating the impacts of environmental changes on bee health. Furthermore, the absence of certain pathogens, such as Varroa destructor, in specific regions like Australia, provides unique insights into how environmental factors alone can influence viral landscapes and colony losses (Roberts et al., 2017).
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