The role of penguins in the Recycling of Trace Metals in Antarctica and their Ecological Impact

Abstract

The Antarctic continent and the surrounding Southern Ocean play a fundamental role in regulating climate, ocean circulation and global ecosystems. Understanding how biogeochemical cycles drive primary production and the Southern Ocean ecosystem is crucial for elucidating the ecological functioning of this region. In this context, biological recycling is considered a key mechanism for the retention and supply of Trace Metals in surface waters. Through this process, marine organisms contribute to the nutrient pool that supports phytoplankton community's growth, limited in many areas due to the depletion of iron. Despite the attention focused on krill and whales, whose excretion products are recognised as the main iron recycling mechanism in the Antarctic ecosystem, the role of penguins, one of the most emblematic organisms of the region, in the biogeochemical cycles of the Southern Ocean has not been addressed. The central axis of this Doctoral Thesis is the study of guano from two Antarctic penguin species, involving a multidisciplinary approach encompassing both the chemical characterisation in terms of dissolved Trace Metals and particulate biogeochemical components, together with the assessment of its effects on organisms of the coastal ecosystem based on ecotoxicological assays. The results derived from a literature review on metal contents in different body tissues, feathers and penguin guano, with our guano samples analysis indicated that guano is the main reservoir of Trace Metals considered essential (Chapter 3). Guano conteins concentration of Cu (2.0 ± 1.4) x 102, Fe (4.1 ± 2.9) x 102, Mn (30 ± 34) and Zn (210 ± 90) (g g-1 dry weight), that are of the same order of magnitude as those reported for whale faeces: Cu (2.9 ± 2.4) x 102, Fe (1.5 ± 1.4) x 102, Mn (28 ± 17) and Zn (6.2 ± 4.3) x 102 (g g-1 dry weight). This allowed to provide evidence for the potential role of penguins in the recycling of Trace Metals. The challenge of characterising the coastal waters around the penguin colonies, which are dangerous and difficult to access, required the development of a novel water sampling system operated from drone (Chapter 4). This automated water autosampler (AWA) system onboard a drone, was effective for the determination of dissolved elements in coastal aquatic environments, particurarly in harsh or inaccessible areas, like those sorrounding penguin colonies. Through the chemical characterisation of penguin guano (Chapter 5), it was estimated that with an average guano concentration of 3 mg Fe g-1, Chinstrap penguin populations can recycle 521 tonnes iron yr-1 in the Southern Ocean waters. Furthermore, the potential contribution of guano to carbon export was considered in relation to the presence of microplastics. The highest concentration found in guano was the smallest fraction (25 50 m), suggesting that it may alter guano sinking pathways, thereby affecting carbon export. Finally, due to the presence of potentially toxic Trace Metals in guano, exposure experiments were carried out to assess the possible impact on Antarctic biota (Chapter 6). A wide panel of ecotoxicological responses was investigated after the exposure of marine organisms belonging to distinct levels of the Antarctic food chain to different concentrations of guano. The results indicated that guano boosted phytoplankton growth, which allowed an estimation of 0.47 ± 0.22 g C m-2 yr-1, as annual net primary productivity driven by the input of iron recycled by Chinstrap penguin populations in Antarctic waters. On the other hand, slight bioaccumulation in tissues of some Trace Metals (e.g. Cd, Cu, Zn and As) and a decrease in antioxidant enzyme activities (e.g. EROD, GST and GR) upon exposure to guano were observed in the Antarctic clams. Lastly, a clear avoidance response was observed in amphipods, indicating that guano could shape the structure of amphipod communities, before reaching toxic levels.