Disruption of Fish Reproduction in Hypoxic Coastal Waters: Potential - PowerPoint PPT Presentation

Disruption of Fish Reproduction in Hypoxic Coastal Waters: Potential Impacts on Coastal Fisheries Worldwide Peter Thomas University of Texas at Austin

Hypoxia Hypoxia – when dissolved oxygen ≤ 2.0mg/l, (~ 30% of normal oxygen levels), too low to support most marine life. Anoxia – occurs when the bacteria use up the rest of the oxygen, suffocating even themselves.

How coastal hypoxic zones form 1.Stratification of water column ● oxygen in water column used by marine organisms, ● bottom layer cannot be re-oxygenated ● seasonal increase in oxygen consumption with temp., biomass increase Surface water Fresh water: plankton lighter Warmer water: lighter No mixing Sea water: heavier O 2 O 2 Bottom water Colder water: heavier

How coastal hypoxic zones form 2. Increased nutrient load- eutrophication Nitrogen, phosphorous ● plankton production increases from ● dead plankton and waste products fall into bottom layer fertilizers, ● bacteria digest dead organisms, waste – consuming etc. remaining O 2 Surface water Fresh water: lighter plankton No mixing Sea water: O 2 heavier O 2 Bottom water O 2 O 2 Bacteria O 2 O 2 consume O 2

Global distribution of hypoxic systems associated with anthropogenic nutrient inputs Diaz and Rosenberg, 2008. Science 321 ● hypoxic regions have tripled in past 30yrs- Major Global Change ● over 400 coastal hypoxic regions worldwide, covering 250,000 km 2 ● Major concern Long term ecological impacts unknown

Assessment of long term effects of increased coastal hypoxia on marine ecosystems and fishery resources • Necessary for the development of effective management strategies • Requires knowledge of longterm biological effects of exposure to sublethal hypoxic conditions in marine organisms • However, information lacking on hypoxia effects on physiological processes that affect fisheries stocks such as reproduction

Control of the Reproduction in Fish Primary regulators Stressors Environmental Photoperiod stimuli Pollution females Temperature Disease + ve -ve Water chemistry Capture (pH) social Hypoxia? Brain Gonadotropin releasing hormone (GnRH) Sensitive stages: pituitary ● sex differentiation E 2 ER Liver GtH Gonadal function Gonadotropin ● Puberty Function ● egg and sperm production and Population gonadal growth Size vitellogenin ● egg and sperm maturation, Egg Production reproductive success fecundity

Laboratory studies: Effects of chronic hypoxia on egg production and endocrine function 10.0 7.5 2.0 GnRH I mRNA level GtH GtH (ng/ml) Estrogen GnRH E 2 (ng/mL) 7.5 1.5 5.0 * 5.0 1.0 * 2.5 2.5 0.5 * *** GnRH 0.0 0.0 Control 1.7 ppm Control 2.7ppm 1.7ppm 0.0 Control 2.7 ppm 1.7 ppm E 2 ER Liver GtH Gonadal 75 function Relative ER1 α mRNA Estrogen Function Model predicts receptor 50 decreased population size * vitellogenin * 25 Egg Production 0 fecundity Control 2.7ppm 1.7ppm 10.0 1500 200000 Vitell. ( µ g/ml) Egg production Ovary growth Vitellogenin 7.5 150000 * Fecundity (eggs/fish) 1000 GSI * * 5.0 * 100000 * 500 2.5 50000 * 0 0 0.0 control 2.7ppm 1.7ppm Control 2.7ppm 1.7ppm Control 2.7 ppm 1.7 ppm

Question: Does environmental hypoxia exposure disrupt reproduction in Atlantic croaker? Estuarine Hypoxia: High rainfall in 2003 resulted in extensive and persistent hypoxia throughout East Bay, Florida 4 hypoxic sites 87 o 10 ‘ 87 o 00 ‘ 30 o 30 ‘ 6 6 N * 4 4 6 * Escambia Bay W E 2 2 4 H1 0 0 2 S DO HIF-1 DO HIF-1 East Bay 0 6 2 normoxic DO HIF-1 H2 4 sites H3 2 6 * H4 0 4 6 DO HIF-1 2 4 TR Pensacola Bay 0 2 6 DO HIF-1 0 * 4 DO HIF-1 N2 2 N1 0 Santa Rosa Sound DO HIF-1 SC MS AL GA 30 o 20 ‘ LA FL Gulf of Mexico Study area 5 km Thomas et al., Proceedings of the Royal Society, London B. 2007

Hypoxia in Estuaries: Hypoxia exposure causes reproductive dysfunction in females hypoxic normoxic E 2 ER GtH Ovary Function normoxic 10 Function Ovary size GSI vitellogenin 5 hypoxic * Oocyte Production * * * * fecundity 0 H1 H2 H3 H4 TR N2 N1 normoxic * 300 Vitellogenic eggs/fish) fecundity * compared to Bridge normoxic normoxic normoxic Fecundity (1000 2000 2000 * compared to Bridge * compared to Bridge Vitellogenin ( µ g/m) Vitellogenin ( µ g/m) vitellogenin hypoxic hypoxic 200 1500 1500 hypoxic hypoxic 1000 1000 100 * 500 500 * * * * * * * * * * * * * 0 0 0 P12 P13 P14 PB5 Trans Bridge PensaBay P12 P12 P13 P13 P14 P14 PB5 PB5 Trans Trans Bridge Bridge PensaBay PensaBay H1 H2 H3 H4 TR N2 N1 H1 H2 H3 H4 TR N2 N 1 1.3ppm 1.3ppm 1.4ppm 1.4ppm 1.9ppm 1.9ppm 3.0ppm 3.0ppm 1.2-4.8ppm 1.2-4.8ppm 4.9ppm 4.9ppm 4.6ppm 4.6ppm egg production and endocrine function impaired at hypoxic sites Similar to endocrine impairment seen in laboratory studies

Hypoxia in Estuaries: Hypoxia exposure also causes reproductive dysfunction in males Spermatogenesis impaired 5 5 4 4 Testis size GSI GSI 3 3 2 2 * * hypoxic c normoxic * * 1 1 * * * * 0 0 P12 P12 P13 P13 P14 P14 PB5 PB5 Trans Trans Bridge PenBay Bridge PenBay H1 H2 H3 H4 TR N2 N1 normoxic 2 relative sperm production * compared to Bridge normoxic plasma 11-KT (ng/ml) Plasma 11-KT Sperm hypoxic production 1 * * * * hypoxia 0 P12 P13 P14 PB5 Trans Bridge PensaBay H1 H2 H3 H4 TR N2 N1 Site P 13 P 14 P B5 Bridge P 12 Pensa Bay Trans H1 H2 H3 H4 TR N2 N1 1 st evidence for reproductive /endocrine impairment in fish exposed to environmental hypoxia

Question: Does large scale hypoxia cause similar reproductive impairment in fish in the Gulf of Mexico hypoxic zone covering 1000s of square miles - much greater potential impact on fisheries

Hypoxia in the northern Gulf of Mexico 2 nd largest coastal hypoxic zone in the world Mississippi-Atchafalaya Drainage Basin • “ top 10 ” river flow- stratification • drains 41% of continental US • Nitrogen loading tripled since 1950s eutrophication Dissolved oxygen ≤ 2.0 mg Mapping since mid 1989 1989 1994 1994 1980 ’ s: increased from 5,000 km2 - 16,000 km2 1990 1990 1995 1995 1993 1993 1997 1997 Dissolved oxygen ≤ 2.0 mg

Hypoxic region on Louisiana continental shelf- 2006-2008 Hypoxic from late spring until mid September CTL normoxic F C In fall 2007 : 3 control sites and 6 hypoxic sites along two transects 120km apart were sampled

Fall 2007 Croaker gonads undeveloped at hypoxic sites Normoxic Normoxic sites sites Testis Ovary hypoxic hypoxic zone sites zone sites

Fall 2007 Gonadal growth impaired at hypoxic sites in both females and males Testicular growth Ovarian growth ** ** 8 4 Normoxic Ovarian development Normoxic Testicular development 6 3 hypoxic zone sites zone sites hypoxic until 2 wks before (GSI) (GSI) 4 2 2 1 0 0 CTL-1CTL-2CTL-3 C-5 C-6 C-7 F-3 F-4 F-5 CTL-1CTL-2CTL-3 C-5 C-6 C-7 F-3 F-4 F-5 Sampling Sites Sampling Sites Thomas & Rahman, Proceedings of the Royal Society, London B. 2011

2007,2008 Reproductive impairment in males at hypoxic sites C transect Normoxic site F transect normoxic 75 Ralative sperm pro. (%) * Sperm production a 50 Hypoxic zone sites ac ac 25 bc bc b b b b 0 CTL1CTL2CTL3 C-5 C-6 C-7 F-3 F-4 F-5 Sampling Sites CTL CTL CTL C C C F F F DO (mg/L) 4.1 5.2 4.8 5.5 4.3 4.5 6.1 5.9 6.2 Normoxic 2 weeks before hypoxic Spermatogenesis and sperm production decreased at hypoxic zone sites

Reproductive impairment in females at hypoxic sites 2007 hypoxic zone sites Normoxic site C transect F transect Normoxic 50 Fecundity (10 3 eggs/fish) Large eggs> 350 μ m 40 30 fecundity 20 10 Hypoxic zone sites 2 weeks before hypoxic 0 CTL1 CTL2 CTL3 C5 C6 C7 F3 F4 F5 Very few mature eggs (low fecundity) at hypoxic zone sites

Fall 2007 Endocrine function decreased at hypoxic sites GnRH GnRH mRNA 3 GnRH mRNA levels Liver *** * Nested ANOVA E 2 ER GtH a-c Fisher's PLSD test Ovary Function 2 Function a a ac ab 1 ab ab vitellogenin ab ab bc Oocyte Production 0 CTL1CTL2CTL3 C5 C6 C7 F3 F4 F5 fecundity ER mRNA 3 3 Relative ER α mRNA levels Plasma VTG levels (mg/mL) *** P <0.001, Nested ANOVA; vitellogenin a-c Fisher's PLSD test *** * 2 a 2 a a ac ac ac bc 1 1 b b b b bc b b b b b b 0 0 CTL-1 CTL-2 CTL-3 C5 C6 C7 F3 F4 F5 Sampling Sites CTL-1 CTL-2 CTL-3 C-5 C-6 C-7 F-3 F-4 F-5 DO (mg/L) 4.1 5.2 4.8 5.5 4.3 4.5 6.1 5.9 6.2 2 weeks before hypoxic Reproductive impairment due to endocrine disruption at hypoxic sites

2006, 2007 Evidence for Ovarian Masculinization Some ovaries from hypoxic zone sites contain spermatogenic cells: Suggests masculinization under hypoxic conditions

Percent ovaries masculinized Field Studies 75 Year 2007 Intersex fish (%) Year 2006 Lab. experiments Lab. experiments 50 27.6% 27.6% 25.0% 25.0% 24% 25 14% 0 Control Control Hypoxia Hypoxia Recovery Recovery Suggests masculinization caused by hypoxia exposure