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Hypoxia: Problems and Scientific Challenges

Explore the increasing trend of anthropogenic nutrient input into coastal waters, leading to a rise in hypoxia levels globally. Learn about the severe consequences such as mass fish mortality, changes in species composition, and impacts on fish reproduction. Discover the scientific evidence indicating hypoxia as an endocrine disruptor and teratogen, affecting fish development and sex balance. Dive into the research on hypoxia-induced reproductive impairments and potential long-term effects on various species, from fish to mammals, and question the future of aquatic populations.

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Hypoxia: Problems and Scientific Challenges

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  1. Hypoxia: Problems and Scientific Challenges Prof. Rudolf Wu School of Biological Sciences The University of Hong Kong (rudolfwu@hku.hk)

  2. Hypoxia: An Old Problem with New Insights

  3. Hypoxia: Trend During the last few decades, anthropogenic input of nutrients into our coastal environment has increased ca. three folds, and is expected to double or triple if no action is taken

  4. Decrease in dissolved oxygen recorded over large coastal areas worldwide (including USA, China, Norway, UK, Sweden, Germany, Denmark, the Black Sea, Adriatic Seas) in the last 30-80 years Hypoxia: Trend Diaz & Rosenberg, 1995; Rabalais, 2001

  5. Total area>245,000 km2

  6. Number of Dead Zones doubled every 10 years since the 1960s Diaz & Rosenberg, 2008

  7. Mass mortality of fish and benthos Changes in species composition Changes in trophic relationships Decrease in biodiversity and species richness Decrease in fisheries production Hypoxia Has Caused Major Changes in Structure and Functions of Ecosystems Phil, 1994; Wu, 2002; Gray et al., 2002 Wu, 2002; Gray et al., 2002

  8. Generalized Changes in Structure and Functions of Ecosystems Normoxia Hypoxia Deposit feeders Meiofauna, Nanoplankton Pelagic fish Short life cycle Suspended feeders Diversity, Species richness Demersal fish Larger body size Predator Wu, 2002

  9. New Scientific Evidencefurther show that…..

  10. Hypoxia is an endocrine disruptor Common carp (Cyprinus carpio)

  11. Male Estradiol Testosterone (ng/ml) ** *** ** p<0.01; *** p<0.001 Wu et al, 2003

  12. Female (ng/ml) *** * *p<0.05; *** p<0.001 Wu et al, 2003

  13. Hypoxia impairs fish reproduction • Gonadal development • Gametogenesis • Spawning • Fecundity • Fertility • Gamete quality • Offspring survival • Reproductive behavior Common carp (Wu et al. 2003) Zebrafish (Shang et al. 2006) Atlantic croaker (Thomas et al. 2006,2007) Gulf killifish (Landry et al. 2007)

  14. Sperm Motility * µmS-1 * * Curvilinear velocity Straight Line velocity Actual Path velocity *p < 0.05 Wu et al, 2003

  15. Reproductive Impairment *** % *** *** *** Fertilization Hatching Larval Survival Egg to Larvae *** p < 0.001 Wu et al, 2003

  16. A smaller gonad and reduced hormone production due to reduced energy intake and reduced growth? Hypoxia affects synthesis and metabolism of sex hormones? Hypoxia affects GnRH and gonadotropins? Follow-up questions: What caused the observed endocrine disruption?

  17. In vitro evidence • In vitro studies using H295R human adrenocortical carcinoma cell line and primary cell culture of medaka gonads

  18. Cholesterol CYP11A Pregnenolone 3β-HSD Progesterone CYP21 11-Deoxy-corticosterone CYP11B1 Corticosterone CYP11B2 Aldosterone CYP17 17α-OH- Pregnenolone 3β-HSD CYP17 17α-OH- Progesterone CYP21 11-Deoxycortisol CYP11B1 Cortisol CYP17 DHEA 3β-HSD CYP17 Androstene-dione 17β-HSD Testosterone CYP19 17β-Estradiol Zonareticularis Zona fasciculata Zona glomerulosa StAR

  19. Hypoxia is a teratogen Zebrafish (Danio rerio)

  20. Hypoxia delays development 24hpf 48hpf Control Hypoxia (0.5mg/l) Shang & Wu, 2004

  21. Hypoxia caused spine and cardiac malformations ** 5.8 mg/L ** * 0.8 mg/L * p < 0.05; **p < 0.01 Malformation (%) Time (hour) Shang & Wu, 2004

  22. Control Hypoxia Under hypoxia, apoptosis concentrates in the head but not the tail Shang & Wu, 2004

  23. Gonads differentiate into ovaries Sex differentiation begins Sex differentiation/ reversal completed Final maturation of the gonads Spawning Male 3-HSD (-) CYP11A (-) CYP19A (+) CYP19B (+) T/E2 (NC) Male 3-HSD (-) CYP11A (-) CYP19A (-) CYP19B (NC) T/E2 (NC) 3-HSD (-) CYP11A (-) CYP19A (ND) CYP19B (-) 3-HSD (-) CYP11A (-) CYP19A (-) CYP19B (-) Female 3-HSD (+) CYP11A (-) CYP19A (+) CYP19B (+) T/E2 (+) Female 3-HSD (-) CYP11A (-) CYP19A (+) CYP19B (NC) T/E2 (+) (A) 10 dpf (B) 40 dpf (C) 60 dpf (D) 120 dpf 10-12dpf 23-25 dpf 42dpf 60 dpf 120 dpf Larval Juvenile Adult 3 dpf 30 dpf 90 dpf Shang et al, 2006

  24. Hypoxia tips sex balance & favors a male biased population ♀ ♀ ♀ ♂ ♂ ♂ ♂ ♂ ♂ ♂ *** Hypoxia *** p < 0.001 Shang, Yu & Wu, 2006

  25. Where the girls are? Will this affect reproductive success of the natural population?

  26. Is the observed male biased phenotypic or geneotypic?Will the same happens to species with XY chromosomes?

  27. Phenotypic & gonadal Sex in genotypic females (O. latipes) are altered by hypoxia Cheung, 2006; Wu, 2009

  28. Salamanders (Ambystoma sp.): delayed development and hatching, less developed and deformed embryos Australian frog (Crinia georgiana): delayed embryonic development, increased malformation Male albino rats: reduced numbers of sertoli cells and Leydig cells in testis Male Wistar rats: lower levels of LH and testosterone Will the same occur in higher vertebrates? Seymonr et al., 2000; Shevantaeva & Kosyuga, 2006; Farias et al., 2007

  29. Will the same occur in invertebrates? Methyl farnesoate? Ecdysteroid? ***p<0.005 Wu & Orr, 2005

  30. Is the situation getting better or getting worse?

  31. Growth of treatment facilities is unlikely to catch up with growth of population and industry, especially in developing counties Contributions from atmospheric fallout and non-point source are significant Trans-boundary issues are difficult to resolve The situation is likely to get worse because…..

  32. Global Warming Increase Temperature Increase freshwater input Increase nutrient flux Increase metabolic rate Increase stratification Nutrient enrichment Enhanced productivity Hypoxia Sediment

  33. Risk Assessment • Ecological consequence Very serious • Area affected Very large • Socioeconomic loss Very big • No. people affected Very large • Probability of occurrence Very high • Trend Getting worse The new scientific evidence presented here calls for an urgent re-assessment of this old problem

  34. Will the same happen in humans? Patients suffering from sleeping apnea have lower sex drive and testosterone level (Saaresranta & Polo, 2003) Sex ratio in human depends on level of sex hormones of father and mother during conception, and high testosterone level during conception favors subsequent birth of sons (James, 2004)

  35. Summary of effects of hypoxia on The HPG axis in female zebrafish (+) E2 FSH (+) (+) CYP19A sGnRH (-) FSH-R LH (-) HMGR Pituitary Blood (+) (+)? Ovary (+) Brain Progestin ? ER CYP19A GnRH FSH E2

  36. Collaborate with fisheries authorities and undertake a scientific global review, focusing on : Trend analysis (spatial and level in the last 50 years) Changes in structure and trophodynamics of marine communities (plankton, benthos, fish) Identification of sensitive groups (bioindicators) Proposed Work

  37. Collaborate with fisheries authorities and undertake a scientific global review, focusing on : Reproductive status and reproductive impairment of fish in hypoxic areas vs normoxic areas Endocrine disruption, malformation, sex ratio Deciphering effects of hypoxia from those caused by other anthropogenic activities (chemicals) prevailing simultaneously in the marine environment?? Identifying information gaps and further studies Proposed Work

  38. zebrafish *** *** % of each stage in testis *** common carp *** common carp Hypoxia Normoxia *** No. of cysts/lobule ** p < 0.01; ***p < 0.001 Diameter (m)/Lobule *** ** Normoxia Hypoxia Hypoxia affects spermatogenesis Wu et al., 2003; Shang et al., 2006

  39. zebrafish *** Atlantic croaker % of each stage in oocyte *** *** *** Ovarian cell stage % of oocytes Hypoxia Normoxia ***p < 0.001 Hypoxia affects Oogenesis Shang et al., 2006; Thomas et al., 2007 Landry et al., 2007

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