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Disruption of Fish Reproduction in Hypoxic Coastal Waters: Potential Impacts on Coastal
Fisheries Worldwide
Peter ThomasUniversity 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.
Fresh water: lighter
Sea water: heavier
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
O2
Warmer water: lighter
Colder water: heavier
No mixing
Surface water
Bottom waterO2
plankton
How coastal hypoxic zones form
Fresh water: lighter
Sea water: heavier
2. Increased nutrient load- eutrophication ● plankton production increases● dead plankton and waste products fall into bottom layer ● bacteria digest dead organisms, waste – consuming
remaining O2
O2
No mixing
Surface water
Bottom waterO2
Nitrogen, phosphorous from fertilizers, etc.
Bacteria consume O2
O2
O2
O2
O2
How coastal hypoxic zones form
plankton
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 km2
● 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
Gonadal Function
Egg Production
GtH
vitellogenin
ER Liver function
E2
Brain
pituitary
Gonadotropin releasing hormone (GnRH)
Gonadotropin
PollutionDiseaseCapture
PhotoperiodTemperatureWater chemistry (pH) social
Environmental stimuli
Primary regulators Stressors
+ ve -ve
Control of the Reproduction in Fish
females
Sensitive stages:
● sex differentiation
● Puberty
● egg and sperm production and gonadal growth
● egg and sperm maturation, reproductive success
fecundity
Population Size
Hypoxia?
Gonadal Function
Egg Production
GtH
vitellogenin
ER Liver function
E2
control 2.7ppm 1.7ppm0
500
1000
1500
**
Vite
ll. ( µ
g/m
l) Vitellogenin
Control 2.7 ppm 1.7 ppm0.0
2.5
5.0
7.5
**E 2
(ng/
mL) Estrogen
Control 2.7 ppm 1.7 ppm0.0
2.5
5.0
7.5
10.0
* *GSI
Ovary growth
Laboratory studies: Effects of chronic hypoxia on egg production and endocrine function
Control 2.7ppm 1.7ppm0.0
2.5
5.0
7.5
10.0
*
GtH
(ng/
ml) GtH
Control 1.7 ppm0.0
0.5
1.0
1.5
2.0
***GnR
H I
mR
NA
leve
l
GnRH
GnRH
fecundity
Model predicts decreased population size
Control 2.7ppm 1.7ppm0
25
50
75
* *
Estrogen receptor
Rel
ativ
eER
1α
mR
NA
Control 2.7ppm 1.7ppm0
50000
100000
150000
200000
**
Egg production
Fecu
ndity
(egg
s/fis
h)
Estuarine Hypoxia: High rainfall in 2003 resulted in extensive and persistent hypoxia throughout East Bay, Florida
LA
Study areaFL
AL
SC
MS GA
5 km
30o20‘
87o00‘87o10‘
Pensacola Bay
Gulf of Mexico
Escambia Bay
Santa Rosa Sound
East Bay
N
S
W E
30o30‘
H4
N2N1
H3
H2
H1
DO HIF-10246
DO HIF-10246
DO HIF-10246
*
DO HIF-10246
*DO HIF-1
0246 *
DO HIF-10246
DO HIF-10246
*
TR
2 normoxic sites
4 hypoxic sites
Thomas et al., Proceedings of the Royal Society, London B. 2007
Question: Does environmental hypoxia exposure disrupt reproduction in Atlantic croaker?
P12 P13 P14 PB5 Trans Bridge PensaBay0
500
1000
1500
2000
1.3ppm 1.4ppm 1.9ppm 3.0ppm 1.2-4.8ppm 4.9ppm 4.6ppm
* compared to Bridge
* * * * *
Vite
lloge
nin
(µ g
/m)
hypoxic
normoxic
P12 P13 P14 PB5 Trans Bridge PensaBay0
500
1000
1500
2000
1.3ppm 1.4ppm 1.9ppm 3.0ppm 1.2-4.8ppm 4.9ppm 4.6ppm
* compared to Bridge
* * * * *
Vite
lloge
nin
(µ g
/m)
hypoxic
normoxichypoxic
normoxic
P12 P13 P14 PB5 Trans Bridge PensaBay0
100
200
300* compared to Bridge
* * **
*
Fecu
ndity
(100
0Vi
tello
geni
c eg
gs/fi
sh)
hypoxic
normoxic
vitellogeninfecundity
Similar to endocrine impairment seen in laboratory studies
H1 H2 H3 H4 TR N2 N 1 H1 H2 H3 H4 TR N2 N1
H1 H2 H3 H4 TR N2 N10
5
10
** * **
GSI
Hypoxia in Estuaries: Hypoxia exposure causes reproductive dysfunction in females
Ovary size
hypoxic normoxic
hypoxic
normoxicOvary Function
Oocyte Production
GtH
vitellogenin
E2 ERFunction
fecundity
egg production and endocrine function impaired at hypoxic sites
P12 P13 P14 PB5 Trans Bridge PensaBay0
1
2* compared to Bridge
* ** *
Site
plas
ma
11-K
T (n
g/m
l)
hypoxic
normoxic
P 12 P 13
P 14
P B5
Tran
s
Brid
ge
Pens
aBa
y
hypoxia
normoxic
rela
tive
sper
m p
rodu
ctio
n
Plasma 11-KTSperm production
H1 H2 H3 H4 TR N2 N1
P12 P13 P14 PB5 Trans Bridge PenBay0
1
2
3
4
5
* * **
GSI
P12 P13 P14 PB5 Trans Bridge PenBay0
1
2
3
4
5
* * **
GSI
H1 H2 H3 H4 TR N2 N1
Hypoxia in Estuaries: Hypoxia exposure also causes reproductive dysfunction in males
hypoxicc normoxic
Spermatogenesis impairedTestis size
H1 H2 H3 H4 TR N2 N1
1st 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
Mississippi-Atchafalaya Drainage Basin• “top 10”river flow- stratification
• drains 41% of continental US
• Nitrogen loading tripled since 1950s
eutrophication
Hypoxia in the northern Gulf of Mexico
1989
1990
1993
1994
1995
1997
1989
1990
1993
1994
1995
1997
Mapping since mid 1980’s:increased from 5,000 km2 - 16,000 km2
Dissolved oxygen ≤ 2.0 mg
2nd largest coastal hypoxic zone in the world
Dissolved oxygen ≤ 2.0 mg
CTL
normoxic
Hypoxic from late spring until mid September
Hypoxic region on Louisiana continental shelf- 2006-2008
CF
In fall 2007 : 3 control sites and 6 hypoxic sites along two transects 120km apart were sampled
hypoxic zone sites
Normoxic sites
TestisOvary
hypoxic zone sites
Normoxic sites
Fall 2007 Croaker gonads undeveloped at hypoxic sites
Gonadal growth impaired at hypoxic sites in both females and males
CTL-1CTL-2CTL-3 C-5 C-6 C-7 F-3 F-4 F-50
2
4
6
8
Normoxic
hypoxic until 2 wks before
Sampling Sites
Ova
rian
dev
elop
men
t(G
SI)
Ovarian growth Testicular growth
CTL-1CTL-2CTL-3 C-5 C-6 C-7 F-3 F-4 F-50
1
2
3
4 Normoxic
hypoxic zone sites
Sampling Sites
Test
icul
ar d
evel
opm
ent
(GSI
)
** **
Fall 2007
Thomas & Rahman, Proceedings of the Royal Society, London B. 2011
zone sites
Normoxic site C transect F transect
2007,2008 Reproductive impairment in males at hypoxic sites
CTL1CTL2CTL3 C-5 C-6 C-7 F-3 F-4 F-50
25
50
75
acac
bc
a
b bb bbc
*
DO (mg/L) 4.1 5.2 4.8 5.5 4.3 4.5 6.1 5.9 6.2Sampling Sites
Normoxic 2 weeks before hypoxic
Ralat
ive sp
erm
pro
. (%
)
CTL CTL CTL C C C F F F
Spermatogenesis and sperm production decreased at hypoxic zone sites
Sperm production
Hypoxic zone sites
normoxic
Reproductive impairment in females at hypoxic sites
Normoxic site C transect F transect
2007hypoxic zone sites
Very few mature eggs (low fecundity) at hypoxic zone sitesCTL1CTL2CTL3 C5 C6 C7 F3 F4 F5
0
10
20
30
40
50Normoxic
2 weeks before hypoxicFecu
ndity
(103 e
ggs/
fish)
Large eggs> 350 μm
fecundity
Hypoxic zone sites
CTL1CTL2CTL3 C5 C6 C7 F3 F4 F50
1
2
3
***
aac
a
abbcab ab ab ab
*Nested ANOVAa-cFisher's PLSD test
GnR
H m
RN
A le
vels
CTL
-1
CTL
-2
CTL
-3 C5
C6
C7 F3 F4 F5
0
1
2
3
ac aa
b b bbc
b b
******P<0.001, Nested ANOVA;
a-cFisher's PLSD test
Rel
ativ
e ER
α m
RN
A le
vels
Ovary Function
Oocyte Production
GtH
vitellogenin
E2
Fall 2007 Endocrine function decreased at hypoxic sitesGnRH
CTL-1CTL-2CTL-3 C-5 C-6 C-7 F-3 F-4 F-50
1
2
3
aac ac
bb
bc
bb b
*
DO (mg/L) 4.1 5.2 4.8 5.5 4.3 4.5 6.1 5.9 6.2Sampling Sites
2 weeks before hypoxic
Plas
ma
VTG
leve
ls (m
g/m
L)
GnRH mRNA
ER Liver
Function
ER mRNAvitellogenin
fecundity
Reproductive impairment due to endocrine disruption at hypoxic sites
Some ovaries from hypoxic zone sites contain spermatogenic cells:
Suggests masculinization under hypoxic conditions
2006, 2007 Evidence for Ovarian Masculinization
Percent ovaries masculinized
Suggests masculinization caused by hypoxia exposure
0
25
50
75
14%24%
Year
200
6
Year
200
7
Inte
rsex
fish
(%)
Field Studies
Con
trol
Hyp
oxia
Rec
over
y
25.0% 27.6%
Lab. experiments
Con
trol
Hyp
oxia
Rec
over
y
25.0% 27.6%
Lab. experiments
How does hypoxia cause the croaker ovary to produce sperm?
Ovary Function
Egg Production
GtH
vitellogenin
Estrogen ERLiver Function
fecundity
Egg production
Androgens (testosterone)
Enzyme: aromataseSperm production
sperm
HYPOTHESIS: HYPOXIA
CTL
-1
CTL
-2
CTL
-3
C-5
C-6
C-7 F-3
F-4
F-50
1
2
3
***
ac ac
a
bc
b b
bc
bbOva
rian
AR
OM
mR
NA
leve
ls hypoxic zone
normoxic
Aromatase mRNA levels in females
Aromatase, decreased expression at hypoxic sites- could be related to masculinization
2007 field studiesLab study-ovaries
Control Hypoxia0
1
2
3
*Aro
mat
ase
mR
NA
leve
lsControl Hypoxia
0
10
20
30
40
50
Aro
mat
ase
activ
ity(p
mol
/mg
prot
ein/
h)
*
Arom. mRNA
Arom. activity
N1 N2 N30
25
50
75
100
-----------------------
52% males
Prop
ortio
n of
mal
e (%
)
N1N2
N3
C5C6
C7
F3F4
F5
A D BC
M
L J EH
IGF
K
A
B
CE
F
GH
IJ
K
L
M
NO P
Q R
29°00?
Gulf of Mexico
LA MS
89°00?90°00?91°00?92°00?
Hypoxic zone
89°00?90°00?91°00?92°00?
D
N
A B C D E F G H I J K L M0
25
50
75
100
-----------------------------------------------------------
N1N2
N3
C5C6
C7
F3F4
F5
A D BC
M
L J EH
IGF
K
A
B
CE
F
GH
IJ
K
L
M
NO P
Q R
29°00?
Gulf of Mexico
LA MS
89°00?90°00?91°00?92°00?
Hypoxic zone
A B C D E F G H I J K L M N O P Q R0
25
50
75
100
50% males
-------------------------
------------------------------------------------
89°00?90°00?91°00?92°00?
D
N
Our samples Louisiana fisheries NOAA SEAMAP
Consistent male bias in sex ratio in fish from hypoxic zone
Sex ratio of Atlantic croaker
58% males 63% males61% males
east west
Conclusions: hypoxia field studies in northern Gulf of Mexico
• Egg and sperm production, endocrine function greatly impaired in both male and female croaker at hypoxic sites 120km apart, ~ 3-4000km2
• Evidence for intersex -masculinization of female gonads; male skewed sex ratio
• Results support hypothesis: hypoxia in the northern Gulf of Mexico significantly decreases egg and sperm production in croaker
Funded by NOAA NGOMEX research program
Potential Long-term Effects of Hypoxia-induced Decline in Reproductive Output on Fish Population Size.
Determining long term effects difficult
- Population affected by multiple factors that vary together and have interactive effects
-Separation of hypoxia effects from other factors is difficult. e.g fishing by catch
Population Modeling is a valuable approach
Modeling allows for systematic evaluation of multiple factors in a controlled world
Year of Simulation
0 20 40 60 80 100
Tota
l Abu
ndan
ce (m
illion
s)
0.0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
1.8Baseline10 % Louisiana25 % Louisiana50% Louisiana
Rose et al. (2009) JEMBE
Modeling Results 1- Predicted Decline in Louisiana Population Size if 25-50% Croaker Exposed to Hypoxia
Average age 2+ abundance for model years 61-100 ranged from 81-83% of baseline abundance (17-19% reduction)
Modeling 2- A Second Model also Predicts a Decline in Croaker Population Size—Dr. Kenneth Rose
- Less dramatic decline than predicted in other simulation
Does Increased Hypoxia in Coastal Regions Threaten Fishery Stocks over the Long-term ?
-Most extensive study conducted on a coastal fish species, croaker, predicts long-term population decline.
-Hypoxia-induced reproductive impairment has been observed in other aquatic species. But information lacking on reproductive effects on coastal marine species.
- Difficult to detect hypoxia effects on size of fish populations from current stock assessments. Relevant data lacking. Clear evidence for a few fisheries.
Conclusion: Critical to examine commercially important marine fish in other coastal hypoxic regions worldwide for evidence of reproductive impairment in order to predict the long-term population effects