Skip to main content Skip to main navigation menu Skip to site footer
Short communication
Austral J. Vet. Sci.
Vol 56, 47-54 (2024)
DOI: 10.4206/ajvs.561.06

Identification of potentially harmful bacterial genera of veterinary relevance in the Llanquihue urban wetlands

1 Laboratorio Institucional Patagonia, Universidad San Sebastián, Puerto Montt, Chile.
2 Facultad de Ciencias de la Naturaleza, Escuela de Medicina Veterinaria, Universidad San Sebastián, Puerto Montt, Chile.
Keywords: Mandatory reportable diseases Wetlands DNA sequencing bioinformatics

Submitted: 2023-08-09

Accepted: 2023-10-20

Published: 2024-01-25

*Corresponding author:
daniel.medina@uss.cl

How to Cite

Rocha, J. D., Opitz, C., Cárdenas, V. ., Mella, C., & Medina, D. (2024). Identification of potentially harmful bacterial genera of veterinary relevance in the Llanquihue urban wetlands. Austral Journal of Veterinary Sciences, 56(1), 47–54. https://doi.org/10.4206/ajvs.561.06

License

Copyright (c) 2024 Jose Dellis Rocha, Catherine Opitz, Vicente Cárdenas, Cristal Mella, Daniel Medina

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Abstract

Water bodies constitute natural, social, and ecological heritage under constant threat from the footprint of human action. They are the habitats of many species and play a key role in sustaining biodiversity in different ecosystems. However, anthropogenic activity can result in eutrophication of water bodies, favoring the excessive growth of microorganisms, which can be a risk factor for animal, human, and environmental health. The Agricultural and Livestock Service [Servicio Agrícola y Ganadero, (SAG)] of Chile developed a list of Mandatory Reportable Diseases (MRD) to report suspected contagious diseases of veterinary relevance. In this sense, the detection of microorganisms in water bodies for the characterization of their sanitary status is important for the development of monitoring strategies and the prevention of possible diseases. This study aimed to determine the presence of potentially harmful bacteria in Llanquihue urban wetlands. Here, we used metagenomic sequencing of amplicons to characterize the composition of microorganisms in three urban wetlands in the city of Llanquihue, which could be a risk factor for animal health. Our main finding was the detection of genera that may be associated with MRD, in addition to other microbial genera that have pathogenic potential. On the other hand, we also report the presence of cyanobacteria genera that can be involved in toxin production in water bodies as another potential source of risk. This is the first study to use massive sequencing techniques to analyze the sanitary status of urban wetlands in the city of Llanquihue.

 

Downloads

Download data is not yet available.

References

  1. Agrawal, M. K., Ghosh, S. K., Divya, B., Juergen, W., Marcel, E., & Bagchi, S. N. (2006). Occurrence of Microcystin-Containing Toxic Water Blooms in Central India. Journal of Microbiology and Biotechnology, 16(2), 212–218. https://www.koreascience.or.kr/article/JAKO200617033429134.page
  2. Akinnawo, S. O. (2023). Eutrophication: Causes, consequences, physical, chemical and biological techniques for mitigation strategies. Environmental Challenges, 12, 100733. https://doi.org/10.1016/j.envc.2023.100733
  3. Almanza, V., Parra, O., Bicudo, C. E. De M., Baeza, C., Beltran, J., Figueroa, R., & Urrutia, R. (2016). Occurrence of toxic blooms of Microcystis aeruginosa in a central Chilean (36° Lat. S) urban lake. Revista Chilena de Historia Natural , 89, 1–12. https://doi.org/10.1186/s40693-016-0057-7
  4. Amorim, C. A., & Moura, A. do N. (2021). Ecological impacts of freshwater algal blooms on water quality, plankton biodiversity, structure, and ecosystem functioning. Science of the Total Environment, 758, 143605. https://doi.org/10.1016/j.scitotenv.2020.143605
  5. Banerjee, S., & van der Heijden, M. G. A. (2023). Soil microbiomes and one health. Nature Reviews Microbiology, 21(1), 6–20. https://doi.org/10.1038/s41579-022-00779-w
  6. Bass, D., Christison, K. W., Stentiford, G. D., Cook, L. S. J., & Hartikainen, H. (2023). Environmental DNA/RNA for pathogen and parasite detection, surveillance, and ecology. Trends in Parasitology, 39(4), 285–304. https://doi.org/10.1016/j.pt.2022.12.010
  7. Behrendt, L., Larkum, A. W. D., Trampe, E., Norman, A., Sørensen, S. J., & Kühl, M. (2011). Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella. The ISME Journal, 6(6), 1222–1237. https://doi.org/10.1038/ismej.2011.181
  8. Bhagowati, B., & Ahamad, K. U. (2019). A review on lake eutrophication dynamics and recent developments in lake modeling. Ecohydrology & Hydrobiology, 19(1), 155–166. https://doi.org/10.1016/j.ecohyd.2018.03.002
  9. Bierque, E., Thibeaux, R., Girault, D., Soupé-Gilbert, M.-E., & Goarant, C. (2020). A systematic review of Leptospira in water and soil environments. PloS One, 15(1), e0227055. https://doi.org/10.1371/journal.pone.0227055
  10. Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics , 30(15), 2114–2120. https://doi.org/10.1093/bioinformatics/btu170
  11. Booth, Szmidt-Middleton, King, & Westbrook. (2018). RStudio: integrated development for R. Nature.
  12. Briand, J.-F., Jacquet, S., Bernard, C., & Humbert, J.-F. (2003). Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water ecosystems. Veterinary Research, 34(4), 361–377. https://doi.org/10.1051/vetres:2003019
  13. Briand, J.-F., Jacquet, S., Flinois, C., Avois-Jacquet, C., Maisonnette, C., Leberre, B., & Humbert, J.-F. (2005). Variations in the microcystin production of Planktothrix rubescens (cyanobacteria) assessed from a four-year survey of Lac du Bourget (France) and from laboratory experiments. Microbial Ecology, 50(3), 418–428. https://doi.org/10.1007/s00248-005-0186-z
  14. Bunesova, V., Vlkova, E., Rada, V., Killer, J., & Musilova, S. (2014). Bifidobacteria from the gastrointestinal tract of animals: differences and similarities. Beneficial Microbes, 5(4), 377–388. https://doi.org/10.3920/BM2013.0081
  15. Byndloss, M. X., & Tsolis, R. M. (2016). Brucella spp. Virulence Factors and Immunity. Annual Review of Animal Biosciences, 4, 111–127. https://doi.org/10.1146/annurev-animal-021815-111326
  16. Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581–583. https://doi.org/10.1038/nmeth.3869
  17. Carmichael, W. W. (1996). Toxic Microcystis and the environment. In: Watanabe, M. F. & Fujiki, H., (Eds.), Toxic Microcystis, CRC Press, Boca Raton, pp. 1–11.
  18. Carvalho, L., Miller nee Ferguson, C. A., Scott, E. M., Codd, G. A., Davies, P. S., & Tyler, A. N. (2011). Cyanobacterial blooms: statistical models describing risk factors for national-scale lake assessment and lake management. Science of the Total Environment, 409(24), 5353–5358. https://doi.org/10.1016/j.scitotenv.2011.09.030
  19. Céspedes Z, M. (2005). Leptospirosis: Enfermedad Zoonótica Emergente. Revista Peruana de Medicina Experimental y Salud Publica, 22(4), 290–307. http://www.scielo.org.pe/scielo.php?pid=S1726-46342005000400008&script=sci_arttext
  20. Chislock, M. F., Doster, E., & Zitomer, R. A. (2013). Eutrophication: causes, consequences, and controls in aquatic ecosystems. Nature Education Knowledge. https://www.wilsonlab.com/wp-content/uploads/2021/05/2013_NE_Chislock_et_al.pdf
  21. Chorus, I., & Welker, M. (2021). Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management (2nd ed.). CRC Press, London. https://doi.org/10.1201/9781003081449
  22. Codd, G. A., Lindsay, J., Young, F. M., Morrison, L. F., & Metcalf, J. S. (2005). Harmful cyanobacteria: from mass mortalities to management measures. In: Huisman, J., Matthijs, H. C. P., & Visser, P. M. (Eds.), Harmful cyanobacteria. Springer Dordrecht, pp. 1–23. https://doi.org/10.1007/1-4020-3022-3
  23. Codd, G., Bell, S., Kaya, K., Ward, C., Beattie, K., & Metcalf, J. (1999). Cyanobacterial toxins, exposure routes and human health. European Journal of Phycology, 34(4), 405–415. https://doi.org/10.1080/09670269910001736462
  24. Decreto 389 Exento [Ministerio de Agricultura] Enfermedades De Declaración Obligatoria Para La Aplicación De Medidas Sanitarias Y Deroga Decretos Que Indica. 14-NOV-2014. https://bcn.cl/2rlwg
  25. Dittmann, E., Fewer, D. P., & Neilan, B. A. (2013). Cyanobacterial toxins: biosynthetic routes and evolutionary roots. FEMS Microbiology Reviews, 37(1), 23–43. https://doi.org/10.1111/j.1574-6976.2012.12000.x
  26. Dreher, T. W., Collart, L. P., Mueller, R. S., Halsey, K. H., Bildfell, R. J., Schreder, P., Sobhakumari, A., & Ferry, R. (2019). Anabaena/Dolichospermum as the source of lethal microcystin levels responsible for a large cattle toxicosis event. Toxicon: X, 1, 100003. https://doi.org/10.1016/j.toxcx.2018.100003
  27. Evangelista, K. V., & Coburn, J. (2010). Leptospira as an emerging pathogen: a review of its biology, pathogenesis and host immune responses. Future Microbiology, 5(9), 1413–1425. https://doi.org/10.2217/fmb.10.102
  28. Faine, S. (1994). Leptospira and leptospirosis. CRC Press Inc.
  29. Farschtschi, S., Riedmaier-Sprenzel, I., Phomvisith, O., Gotoh, T., & Pfaffl, M. W. (2022). The successful use of -omic technologies to achieve the “One Health” concept in meat producing animals. Meat Science, 193, 108949. https://doi.org/10.1016/j.meatsci.2022.108949
  30. Garvey, M. (2020). Mycobacterium Avium Paratuberculosis: A Disease Burden on the Dairy Industry. Animals, 10(10), 1773. https://doi.org/10.3390/ani10101773
  31. Ginestet, C. (2011). ggplot2: Elegant Graphics for Data Analysis. Journal of the Royal Statistical Society. Series A , 174(1), 245–246. https://ideas.repec.org/a/bla/jorssa/v174y2011i1p245-246.html
  32. Gkelis, S., Lanaras, T., & Sivonen, K. (2006). The presence of microcystins and other cyanobacterial bioactive peptides in aquatic fauna collected from Greek freshwaters. Aquatic Toxicology , 78(1), 32–41. https://doi.org/10.1016/j.aquatox.2006.02.001
  33. Gruszecka-Kosowska, A., Ampatzoglou, A., & Aguilera, M. (2022). Integration of Omics Approaches Enhances the Impact of Scientific Research in Environmental Applications. International Journal of Environmental Research and Public Health, 19(14). https://doi.org/10.3390/ijerph19148758
  34. Hilborn, E. D., & Beasley, V. R. (2015). One health and cyanobacteria in freshwater systems: animal illnesses and deaths are sentinel events for human health risks. Toxins, 7(4), 1374–1395. https://doi.org/10.3390/toxins7041374
  35. Holdeman, L. V., & Moore, W. E. C. (1974). New genus, Coprococcus, twelve new species, and emended descriptions of four previously described species of bacteria from human feces. International Journal of Systematic Bacteriology, 24(2), 260–277. https://doi.org/10.1099/00207713-24-2-260
  36. Huang, J., Ghaly, M., Hobson, P., & Chow, C. W. K. (2022). Innovative method of utilising hydrogen peroxide for source water management of cyanobacteria. Environmental Science and Pollution Research International, 29(15), 22651–22660. https://doi.org/10.1007/s11356-021-17511-5
  37. Ibelings, B. W., Fastner, J., Bormans, M., & Visser, P. M. (2016). Cyanobacterial blooms. Ecology, prevention, mitigation and control: Editorial to a CYANOCOST Special Issue. Aquatic Ecology, 50(3), 327–331. https://doi.org/10.1007/s10452-016-9595-y
  38. Irshath, A. A., Rajan, A. P., Vimal, S., Prabhakaran, V.-S., & Ganesan, R. (2023). Bacterial Pathogenesis in Various Fish Diseases: Recent Advances and Specific Challenges in Vaccine Development. Vaccines, 11(2). https://doi.org/10.3390/vaccines11020470
  39. Jančula, D., & Maršálek, B. (2011). Critical review of actually available chemical compounds for prevention and management of cyanobacterial blooms. Chemosphere, 85(9), 1415–1422. https://doi.org/10.1016/j.chemosphere.2011.08.036
  40. Jisha, K. C., & Puthur, J. T. (2021). Ecological importance of wetland systems. In: Sharma, S., & Singh, P. (Eds.). Wetlands Conservation, pp. 40–54. Wiley. https://doi.org/10.1002/9781119692621.ch3
  41. Khan, M. N., & Mohammad, F. (2014). Eutrophication: challenges and solutions. In: Ansari, A., Gill, S. (Eds.), Eutrophication: Causes, Consequences and Control, pp. 1-15. https://doi.org/10.1007/978-94-007-7814-6_1
  42. La Reau, A. J., & Suen, G. (2018). The Ruminococci: key symbionts of the gut ecosystem. Journal of Microbiology , 56(3), 199–208. https://doi.org/10.1007/s12275-018-8024-4
  43. Lahti, L., Shetty, S., Blake, T., & Salojarvi, J. (2017). Tools for microbiome analysis in R. http://microbiome.github.com/microbiome
  44. Lapointe, B. E., Herren, L. W., Debortoli, D. D., & Vogel, M. A. (2015). Evidence of sewage-driven eutrophication and harmful algal blooms in Florida’s Indian River Lagoon. Harmful Algae, 43, 82–102. https://doi.org/10.1016/j.hal.2015.01.004
  45. Loch, T. P., & Faisal, M. (2015). Emerging flavobacterial infections in fish: A review. Journal of Advertising Research, 6(3), 283–300. https://doi.org/10.1016/j.jare.2014.10.009
  46. Markensten, H., Moore, K., & Persson, I. (2010). Simulated lake phytoplankton composition shifts toward cyanobacteria dominance in a future warmer climate. Ecological Applications, 20(3), 752–767. https://doi.org/10.1890/08-2109.1
  47. Martinez, A. (2018). Enfermedades infecciosas que afectan la producción de smolts en Chile Laboratorio Antares S.A. Salmonexpert. Consultado el 4 de mayo del 2023 de https://www.salmonexpert.cl/enfermedades-infecciosas/1236500
  48. McMurdie, P. J., & Holmes, S. (2013). phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS One, 8(4), e61217. https://doi.org/10.1371/journal.pone.0061217
  49. Mitchell, M., Nguyen, S. V., Macori, G., Bolton, D., McMullan, G., Drudy, D., & Fanning, S. (2022). Clostridioides difficile as a Potential Pathogen of Importance to One Health: A Review. Foodborne Pathogens and Disease, 19(12), 806–816. https://doi.org/10.1089/fpd.2022.0037
  50. Moore, C. E., Juan, J., Lin, Y., Gaskill, C. L., & Puschner, B. (2016). Comparison of Protein Phosphatase Inhibition Assay with LC-MS/MS for Diagnosis of Microcystin Toxicosis in Veterinary Cases. Marine Drugs, 14(3). https://doi.org/10.3390/md14030054
  51. Nematollahi, A., Decostere, A., Pasmans, F., & Haesebrouck, F. (2003). Flavobacterium psychrophilum infections in salmonid fish. Journal of Fish Diseases, 26(10), 563–574. https://doi.org/10.1046/j.1365-2761.2003.00488.x
  52. Nimptsch, J., Woelfl, S., Osorio, S., Valenzuela, J., Moreira, C., Ramos, V., Castelo-Branco, R., Leão, P. N., & Vasconcelos, V. (2016). First record of toxins associated with cyanobacterial blooms in oligotrophic North Patagonian lakes of Chile-a genomic approach. International Review of Hydrobiology, 101(1-2), 57–68. https://doi.org/10.1002/iroh.201401780
  53. Oberhaus, L., Gélinas, M., Pinel-Alloul, B., Ghadouani, A., & Humbert, J.-F. (2007). Grazing of two toxic Planktothrix species by Daphnia pulicaria: potential for bloom control and transfer of microcystins. Journal of Plankton Research, 29(10), 827–838. https://doi.org/10.1093/plankt/fbm062
  54. Olea-Popelka, F., Muwonge, A., Perera, A., Dean, A. S., Mumford, E., Erlacher-Vindel, E., Forcella, S., Silk, B. J., Ditiu, L., El Idrissi, A., Raviglione, M., Cosivi, O., LoBue, P., & Fujiwara, P. I. (2017). Zoonotic tuberculosis in human beings caused by Mycobacterium bovis—a call for action. The Lancet Infectious Diseases, 17(1), e21–e25. https://doi.org/10.1016/S1473-3099(16)30139-6
  55. Oliveira, M. M. E., Lopes, A. P., Pinto, T. N., da Costa, G. L., Goes-Neto, A., & Hauser-Davis, R. A. (2023). A Novel One Health Approach concerning Yeast Present in the Oral Microbiome of the Endangered Rio Skate (Rioraja agassizii) from Southeastern Brazil. Microorganisms, 11(8), 1969. https://doi.org/10.3390/microorganisms11081969
  56. Olsen, S. C., & Palmer, M. V. (2014). Advancement of knowledge of Brucella over the past 50 years. Veterinary Pathology, 51(6), 1076–1089. https://doi.org/10.1177/0300985814540545
  57. Paerl, H. W., Gardner, W. S., McCarthy, M. J., Peierls, B. L., & Wilhelm, S. W. (2014). Algal blooms: Noteworthy nitrogen. Science, 346(6206), 175. https://doi.org/10.1126/science.346.6206.175-a
  58. Paerl, H. W., & Huisman, J. (2008). Blooms like it hot. Science, 320(5872), 57–58. https://doi.org/10.1126/science.1155398
  59. Paerl, H. W., & Huisman, J. (2009). Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports, 1(1), 27–37. https://doi.org/10.1111/j.1758-2229.2008.00004.x
  60. Papadimitriou, T., Kagalou, I., Bacopoulos, V., & Leonardos, I. D. (2010). Accumulation of microcystins in water and fish tissues: an estimation of risks associated with microcystins in most of the Greek Lakes. Environmental Toxicology, 25(4), 418–427. https://doi.org/10.1002/tox.20513
  61. Parlapani, F. F., Boziaris, I. S., & Mireles DeWitt, C. A. (2023). Pathogens and their sources in freshwater fish, sea finfish, shellfish, and algae. In: Knowles, M. E., Anelich, L. E., Boobis, A. R., & Popping, B. (Eds.), Present Knowledge in Food Safety, pp. 471–492. Academic Press. https://doi.org/10.1016/B978-0-12-819470-6.00056-1
  62. Parulekar, N. N., Kolekar, P., Jenkins, A., Kleiven, S., Utkilen, H., Johansen, A., Sawant, S., Kulkarni-Kale, U., Kale, M., & Sæbø, M. (2017). Characterization of bacterial community associated with phytoplankton bloom in a eutrophic lake in South Norway using 16S rRNA gene amplicon sequence analysis. PloS One, 12(3), e0173408. https://doi.org/10.1371/journal.pone.0173408
  63. Peng, L., Liu, Y., Chen, W., Liu, L., Kent, M., & Song, L. (2010). Health risks associated with consumption of microcystin-contaminated fish and shellfish in three Chinese lakes: significance for freshwater aquacultures. Ecotoxicology and Environmental Safety, 73(7), 1804–1811. https://doi.org/10.1016/j.ecoenv.2010.07.043
  64. Pitois, S., Jackson, M. H., & Wood, B. J. (2001). Sources of the eutrophication problems associated with toxic algae: an overview. Journal of Environmental Health, 64(5), 25–32. https://www.ncbi.nlm.nih.gov/pubmed/11764678 PMID: 11764678
  65. Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41(Database issue), D590–D596. https://doi.org/10.1093/nar/gks1219
  66. Rankin, K. A., Alroy, K. A., Kudela, R. M., Oates, S. C., Murray, M. J., & Miller, M. A. (2013). Treatment of cyanobacterial (microcystin) toxicosis using oral cholestyramine: case report of a dog from Montana. Toxins, 5(6), 1051–1063. https://doi.org/10.3390/toxins5061051
  67. R Core Team. (2013). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. http://www.R-project.org/
  68. Roset, J., Aguayo, S., & Muñoz, M. J. (2001). Cyanobacteria and toxins detection. A review. Revista de Toxicologia 18(2), 65-71 https://digital.csic.es/handle/10261/294473
  69. Servicio Agrícola y Ganadero (2019). SAG: Lista de enfermedades de denuncia obligatoria https://www.sag.gob.cl/sites/default/files/enfermedades_denuncia_obligatoria_sag_9-10-2019.pdf
  70. Shetty, S. A., Hugenholtz, F., Lahti, L., Smidt, H., & de Vos, W. M. (2017). Intestinal microbiome landscaping: insight in community assemblage and implications for microbial modulation strategies. FEMS microbiology reviews, 41(2), 182-199. https://doi.org/10.1093/femsre/fuw045
  71. Tett, A., Pasolli, E., Masetti, G., Ercolini, D., & Segata, N. (2021). Prevotella diversity, niches and interactions with the human host. Nature Reviews Microbiology, 19(9), 585–599. https://doi.org/10.1038/s41579-021-00559-y
  72. Tigistu-Sahle, F., Mekuria, Z. H., Satoskar, A. R., Sales, G. F. C., Gebreyes, W. A., & Oliveira, C. J. B. (2023). Challenges and opportunities of molecular epidemiology: using omics to address complex One Health issues in tropical settings. Frontiers in Tropical Diseases, 4. https://doi.org/10.3389/fitd.2023.1151336
  73. Trinh, P., Zaneveld, J. R., Safranek, S., & Rabinowitz, P. M. (2018). One Health Relationships Between Human, Animal, and Environmental Microbiomes: A Mini-Review. Frontiers in Public Health, 6, 235. https://doi.org/10.3389/fpubh.2018.00235
  74. van der Merwe, D., Sebbag, L., Nietfeld, J. C., Aubel, M. T., Foss, A., & Carney, E. (2012). Investigation of a Microcystis aeruginosa cyanobacterial freshwater harmful algal bloom associated with acute microcystin toxicosis in a dog. Journal of Veterinary Diagnostic Investigation, 24(4), 679–687. https://doi.org/10.1177/1040638712445768
  75. Walters, S. P., Thebo, A. L., & Boehm, A. B. (2011). Impact of urbanization and agriculture on the occurrence of bacterial pathogens and stx genes in coastal waterbodies of central California. Water Research, 45(4), 1752–1762. https://doi.org/10.1016/j.watres.2010.11.032
  76. Wang, Z., Akbar, S., Sun, Y., Gu, L., Zhang, L., Lyu, K., Huang, Y., & Yang, Z. (2021). Cyanobacterial dominance and succession: Factors, mechanisms, predictions, and managements. Journal of Environmental Management, 297, 113281. https://doi.org/10.1016/j.jenvman.2021.113281
  77. Wilhelm, S. W., Bullerjahn, G. S., & McKay, R. M. L. (2020). The Complicated and Confusing Ecology of Microcystis Blooms. mBio, 11(3). https://doi.org/10.1128/mBio.00529-20
  78. Wood, R. (2016). Acute animal and human poisonings from cyanotoxin exposure - A review of the literature. Environment International, 91, 276–282. https://doi.org/10.1016/j.envint.2016.02.026
  79. Xie, L., Xie, P., Guo, L., Li, L., Miyabara, Y., & Park, H.-D. (2005). Organ distribution and bioaccumulation of microcystins in freshwater fish at different trophic levels from the eutrophic Lake Chaohu, China. Environmental Toxicology, 20(3), 293–300. https://doi.org/10.1002/tox.20120
  80. Zamyadi, A., Choo, F., Newcombe, G., Stuetz, R., & Henderson, R. K. (2016). A review of monitoring technologies for real-time management of cyanobacteria: Recent advances and future direction. Trends in Analytical Chemistry: TrAC, 85(A), 83–96. https://doi.org/10.1016/j.trac.2016.06.023
  81. Zedler, J. B., & Kercher, S. (2005). WETLAND RESOURCES: Status, trends, ecosystem services, and restorability. Annual Review of Environment and Resources, 30(1), 39–74. https://doi.org/10.1146/annurev.energy.30.050504.144248
  82. Zhang, D., Xie, P., Liu, Y., Chen, J., & Liang, G. (2007). Bioaccumulation of the hepatotoxic microcystins in various organs of a freshwater snail from a subtropical Chinese lake, Taihu Lake, with dense toxic Microcystis blooms. Environmental Toxicology and Chemistry, 26(1), 171–176. https://doi.org/10.1897/06-222r.1
  83. Zhang, D., Xie, P., Liu, Y., & Qiu, T. (2009). Transfer, distribution and bioaccumulation of microcystins in the aquatic food web in Lake Taihu, China, with potential risks to human health. Science of the Total Environment, 407(7), 2191–2199. https://doi.org/10.1016/j.scitotenv.2008.12.039
  84. Zinia, N. J., & Kroeze, C. (2015). Future trends in urbanization and coastal water pollution in the Bay of Bengal: the lived experience. Environment, Development and Sustainability, 17, 531–546. https://doi.org/10.1007/s10668-014-9558-1
  85. Zinsstag, J., Crump, L., Schelling, E., Hattendorf, J., Maidane, Y. O., Ali, K. O., Muhummed, A., Umer, A. A., Aliyi, F., Nooh, F., Abdikadir, M. I., Ali, S. M., Hartinger, S., Mäusezahl, D., de White, M. B. G., Cordon-Rosales, C., Castillo, D. A., McCracken, J., Abakar, F., … Cissé, G. (2018). Climate change and One Health. FEMS Microbiology Letters, 365(11). https://doi.org/10.1093/femsle/fny085

Make a Submission

Make a Submission

Journal Metrics (2023) & Ranking

Impact Factor
→
0.5 (2024)
5 years Impact Factor
→
0.8
JCR Quartile
→
Q4
JIF Rank
→
134/170 (Veterinary Sciences)
SJR (2024)
→
0.244
SNIP (2024)
→
0.35

 

 

SCImago Journal & Country Rank

Indexed in

Publisher


This journal is published by the Facultad de Ciencias Veterinarias, Universidad Austral de Chile

Keywords