Discussion
Our behavioural test with young male blackcaps captured on migration showed that birds preferred anthocyanin- or fat-enriched food alternatives depending on their physiological condition. The results supported a scenario in which feeding decisions helped birds to cope with the oxidative challenges they face as they recover from and prepare to the intense aerobic exercise during endurance flight. In this scenario, haemosporidian parasites had an impact on host physiology by exacerbating oxidative challenges, which influenced on individual food preferences supporting the idea that increasing the intake of dietary antioxidants may be a self-medication mechanism to cope with elevated risk of oxidative stress due to infection (Mancio-Silva et al. 2017; Zuzarte-Luís and Mota 2018). This interpretation was supported by our observation of infected birds having lower total antioxidant capacity, and individuals with higher levels of oxidative damage to lipids having more preference for anthocyanin-enriched food.
Co-infected blackcaps preferred anthocyanin-enriched food. Consumption of antioxidants such as anthocyanins could be a means of self-medicating if it reduced oxidative damage caused by the parasite or by activation of the immune system during the infection (Beaulieu and Schaefer 2013; de Roode et al. 2013; Muriel 2020). This effect of parasitism was only significant in multiple infections, which could increase parasite virulence or the cost of the host’s immune response (Pigeault et al. 2018; Garcia-Longoria et al. 2022). In this context, the consumption of antioxidants could be detrimental to the energy intake essential for migration performance (Beaulieu and Schaefer 2014), or it could compromise the active search of alternative essential nutrients, such as polyunsaturated fatty acids that may enhance physiological performance during migration (Weber 2009).
We found a correlation between infection and the oxidative balance, since infected birds showed lower values of plasma antioxidant capacity. Antioxidant depletion associated with immune activation (Costantini and Møller 2009) or production of free radicals as a result of parasite exploitation (Percário et al. 2012) may induce an increase in ROS in infected birds (Delhaye et al. 2016). Similar results of infections have been found in other stressful situations such as during reproduction (Badás et al. 2015), or in poor habitat (Messina et al. 2022). However, we did not detect any correlation between infection status and other biomarkers of oxidative status. These correlations could have been concealed by a hormetic response, which is supported by a positive correlation between tGSH and RBC-MDA. Faced with predictable oxidative stress, migrating birds could up-regulate antioxidant defences before suffering too much oxidative damage (Costantini 2010; McWilliams et al. 2021), thus buffering the relationships between oxidative parameters and the sources of stress.
We did not find any relationship between parasitemia and biomarkers of oxidative stress, although other studies have found it in other species such as great tits Parus major (Isaksson et al. 2013; Delhaye et al. 2016). However, blackcaps showed very low parasitemia in our study. This result indicates that blackcaps during autumn migration have mostly chronic infections with few parasites in the bloodstream, yet such low-intensity infections may have an impact on oxidative status during migration, which could contribute to the mortality cost of haemosporidian infections observed in other migratory bird species (Asghar et al. 2015).
We found a positive correlation between relative body mass and preference for fat-enriched food, which we attribute to the fact that body mass of migrating blackcaps captured on stopover is most dependent on the time they have spent at the stopover site, as birds gain body mass from arrival to departure (Langslow 1976; Arizaga et al. 2010). Thus, leaner birds may prefer anthocyanin-enriched food if dietary antioxidants help them cope with oxidative damage associated to the aerobic effort of the preceding flight stage (Costantini 2008; Eikenaar et al. 2020). Conversely, fatter birds closer to departure may focus on putting on fats to fuel the next flight stage, thereby preferring fat-enriched food. Preference for olive oil could be further increased close to departure if birds benefit from acquiring so-called ”natural doping” polyunsaturated fatty acids present in olive oil as these may increase metabolic efficiency during endurance flight (Weber 2009). Our interpretation of the relationship between body mass and food preferences observed in blackcaps is supported by the fact that blackcaps lose weight on arrival at stopover sites (Langslow 1976), which may be indicative of a period of tissue repair during which birds do not put on any fat. Furthermore, birds with less oxidative damage in plasma (as measured by MDA) selected fats rather than anthocyanins, supporting the idea that individuals with a good oxidative status could focus on rebuilding fat stores or prioritise the intake of alternative essential nutrients that may give them a physiological advantage during endurance flight (Weber 2009; Costantini 2010; Beaulieu and Schaefer 2014).
Understanding the intricate relationships between body condition, oxidative status and dietary preferences during migration has long been at the centre of research on the physiological performance of migrating birds (Weber 2009). Our results support the idea that haemosporidian infections influence on these relationships by exacerbating the oxidative challenges faced by birds during this critical life cycle stage, thereby providing a physiological mechanism to explain the negative impact of chronic avian malaria infections on survival observed in migrating birds (Asghar et al. 2015), and emphasising the importance of accounting for parasite infections in studies of animal performance (Chrétien et al. 2023).
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