Our study underscores distinct patterns of metal bioaccumulation and oxidative stress responses in waterbirds inhabiting organic and conventional rice crops, which are associated with variations in trace metal concentrations. As anticipated, Pb and Cu levels were notably higher in the feathers of birds from conventional farms, while Cd and Zn concentrations tended to be elevated in waterbirds from organic farms, as detailed in Table 1. Notably, all trace metal concentrations detected in the feathers remained below documented thresholds known to cause acute biochemical effects in waterbirds (Lucia et al. 2012a; Mansouri and Majnoni 2014; Kanwal et al. 2020). We observed significant variations between conventional and organic crop systems in LPO, NPSH, PC, SOD, and CAT, as highlighted in Table 1. Among these parameters, CAT activity exhibited a direct relationship with variations in feather Pb concentration. These results suggest an early indication of waterbird contamination by Pb, resulting in detectable metabolic responses.
It's worth noting that the association of trace metals and biomarkers with the rice systems was comparatively weaker in the direct ordination, and we only detected one significant interaction between trace metals and biomarkers. This suggests that other factors within the studied agrosystems may play a more significant role in waterbird metabolism than trace metal exposure alone (Khare et al. 2019). Indeed, oxidative stress biomarkers, such as LPO, NPSH, and PC, showed higher activity levels in the organic farm, while SOD and CAT activity was elevated in the conventional farm. These biomarkers can interact with various other biological and inorganic compounds, influencing their activity (Martinez-Haro et al. 2011; Kanwal et al. 2020), which may contribute to the lower detection of NPSH and PC in our study. Additionally, interactions with other biomarkers like metallothioneins and non-enzymatic antioxidants (e.g., Vitamin E) can influence the formation of TBARS (LPO) (Mateo et al. 2003; Martinez-Haro et al. 2011; Lucia et al. 2012b). The interplay between trace metals, like Fe-Cd, can also impact SOD activity (Kamiński et al. 2009). These biochemical processes vary due to multiple factors beyond trace metal exposure, posing a challenge to establishing direct associations. Nevertheless, they indicate an initial contact with contaminants and a potential risk to animal health (van der Oost et al. 2003). Pesticide use, a major disparity between organic and conventional farming practices, can also induce oxidative stress through various mechanisms, including interference with reduction-oxidation reactions, cellular metabolism, inactivation of antioxidant enzymes, and alterations in transcription and translation processes, indirectly elevating reduction-oxidation reactions (Lushchak 2011; Chowdhury and Saikia 2020).
Despite not observing a clear general trend in the trace metal profile separating the two farming systems, our study did reveal a connection between lead concentration and the oxidative stress activity of waterbirds across the compared rice crop systems. The birds in the conventional farm exhibited higher levels of Pb and Cu, while those in the organic farm had greater concentrations of Cd and Zn. It's important to note that livestock diets, fertilizers, and lead projectiles are sources of Cd, Zn, and Cu (Nicholson et al. 2003), while fuels and lead ammunition are known sources of Pb contamination in waterbirds (Peakall and Burger 2003; Freudenberger et al. 2013). Glyphosate, a commonly used herbicide, can also form chemical bonds with lead, facilitating its transport into the bloodstream and organs (Si et al. 2013)(Si et al. 2013), potentially contributing to lead exposure. Notably, both farms share the same soil class, employ mechanized practices, and have no reported incidents of illegal hunting.
It is important to acknowledge that various factors that influence oxidative stress activity in birds, but were not controlled in our study, could have impacted the results. These factors include circadian rhythm, environmental temperature, the presence of parasitic infections (Lushchak 2011; Kaminski et al. 2014), nutritional status, and access to an antioxidant-rich diet (Koivula and Eeva 2010). In our analyses, we controlled for these factors by treating species as a random factor in the GLMM and by collecting only adult, healthy individuals. However, there are factors beyond our control, such as collecting waterbirds in different years at the organic and conventional farms, and a lack of farm replication. Nevertheless, the selected farms are representative of their respective modes of cultivation in southern Brazil, and the two calendar years under consideration exhibited similar climate and productivity. Moreover, the surface waters used in these regions do not naturally contain significant concentrations or variations in trace metals that could explain the observed differences (González et al. 2019). Additionally, waterbirds, due to their mobility, may not be strictly tied to specific feeding spots. A prior study conducted in the same areas, using fish (Astyanax lacustris) as a model species, found comparable and stronger effects and relationships (Bergmann et al. 2020).
In conclusion, our study reveals that organic and conventional irrigated rice crops in South Brazil differ in several factors, including trace metal exposure, leading to measurable variations in oxidative stress responses among waterbirds. These findings underscore the importance of monitoring agricultural production practices for potential environmental and wildlife impacts.