Cristian R. Kleemann1,2; Thaís C.S. Rodrigues3,4*+; Winnie Brum1; Rodrigo Hoff1; Pedro L.M. Barreto2; Mariana L.C. Martins3; Hilda I.C. Perez3; Kliszilla P. Avila3; Sthéfani E. Siqueira3; Adria C. Moreira3; Kellen K.G. Lopes3; Claudia L. Souza3; Maria Clara C. Rodrigues3; Isadora S.C. Dias3; Karen L.F. Marinho3; Cristiane K.M. Kolesnikovas5; Miriam Marmontel3
Abstract
River dolphins are important indicators of the aquatic ecosystem’s quality, and because human health is also dependent on good water quality, their health is indirectly linked to public health. All species of river dolphins in the world are currently classified as Endangered or Critically Endangered due to the multiple pressures they face. As they are sensitive to environmental changes, threats related to global warming, habitat degradation, and pollution are of increasing concern to their conservation. Such environmental changes may induce alterations in the bacterial and phytoplankton population resulting in eutrophication, low oxygen concentrations, and at times, presence of harmful toxins.1
From September to November 2023, an unprecedented Amazonian River dolphin unusual mortality event (UME) took place in the Brazilian Amazon. The UME resulted in the deaths of more than 150 Amazon River dolphins (Inia geoffrensis) and tucuxis (Sotalia fluviatilis) in Lake Tefé. An extensive multidisciplinary response was set up aiming to better understand the causes of this UME. As part of multiple ongoing studies, the dolphins’ carcasses were collected, and comprehensive necropsies and sampling were performed. Samples of liver and/or kidney from three tucuxis and four Amazon River dolphins were frozen at −80°C and submitted for detection of the aquatic toxins palytoxin (PITX) and PITX-like toxins, using a liquid chromatography–tandem mass spectrometry method.4 PITX was detected in the liver samples from two female tucuxis, an adult (<10 µg/kg) and a calf (18,7 µg/kg).
PITXs are among the most toxic non-peptide substances known, showing remarkable biological activity even at very low concentrations. Such toxins have been associated with a variety of marine organisms (e.g., corals, bacteria, alga, dinoflagellates) and are distributed worldwide. In mammals, PITX can be lethal and induces hemorrhagic lesions on cardiovascular, kidney, gastrointestinal, and respiratory systems.5 In humans, PITX-like are suggested to be among the toxins causing Haff disease, a syndrome of myalgia and rhabdomyolysis that occurs after consumption of cooked seafood.6 In Brazil, the first reported outbreak of the disease occurred in 2008, in the Brazilian Amazon, due to consumption of local fish species.7 Since 2020, an increase of Haff’s disease cases has been reported all over the country, but mostly in warmer regions such as the coastal region of the Northeast and around the Amazon River Basin.8
PITXs have never been reported in liver samples from a dolphin previously, and this novel report may be of great significance for river dolphin conservation in the Amazon. Further analyses are being developed using high-resolution mass spectrometry to confirm the findings and search for additional PITX analogues. The knowledge of PITX toxicity in mammals naturally intoxicated is still lacking, and further investigation is needed to better understand the clinical relevance of PITX in the tucuxis’ liver samples, if any. We plan to expand the detection of PITX to more samples and animals related to the UME, in addition to comparing such findings with the dolphin’s histopathology lesions and other diagnostic test results, aiming to understand the correlation of our findings to the UME.
Acknowledgements
The authors thank all institutions and their volunteers that collaborated in the emergency response of the UME: Aiuká Consultoria em Soluções Ambientais, Aqua Viridi, Aquasis, Corpo de Bombeiros de Tefé, Conselho Regional de Medicina Veterinária do Amazonas, European Association for Aquatic Mammals, Exército Brasileiro, Friends of Nuremberg Zoo Association, Fundação Mamíferos Aquáticos, Fundación Mundo Marino, GRAD (Grupo de Resgate de Animais em Desastres), Greenpeace, IBAMA (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis), INPA (Instituto Nacional de Pesquisas da Amazônia), Instituto Aqualie, Instituto Baleia Jubarte, Instituto Oswaldo Cruz (IOC/Fiocruz), International Fund for Animal Welfare, IPAAM (Instituto de Proteção Ambiental do Amazonas), LAPCOM-USP, Loro Parque Fundación, Marinha do Brasil, National Marine Mammal Foundation, Nuremberg Zoo, Oceanogràfic València, Planète Sauvage, Polícia Militar do Amazonas, Prefeitura de Tefé, R3 Animal, Rancho Texas, Sea Shepherd Brasil, Sea Shepherd France, SeaWorld and Busch Gardens Conservation Fund, SEMMAC (Secretaria Municipal de Meio Ambiente e Conservação de Tefé), Universidad de Las Palmas de Gran Canaria, WWF Alemanha, WWF Brasil, YAQU PACHA, and Zoomarine Portugal.
*Presenting author
+Student presenter
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