Thermal sensitivity of fish
reproduction and proposed
temperature standards
Preliminary Information
Colorado Parks and Wildlife
Mindi May
March 19, 2015
Temperature
Existing Quality
31.14
Warmwater
Winter Acute
Values
Update
Temperature
Database
UILT/
Acclimation
Calculation
Shoulder Season
Implementation
Sector-Based
Variance
Feasibility
Study
SECTION 1
Shoulder Seasons for Cold
Water streams
WQCD Stepped Proposal
CS-II, proposed steps
CS-II, Current
30
30
chronic
chronic
25
20
20
Degrees C
25
15
10
acute
15
10
Dec
Nov
Oct
Sep
Aug
Jul
Jun
May
Apr
Mar
Dec
Nov
Oct
Sep
Aug
Jul
Jun
May
Apr
Mar
Feb
0
Feb
0
Jan
5
5
Jan
Degees C
acute
WQCD Narrative Proposal
CS-II, Current
30
CS-II, Proposed Narrative
30
chronic
chronic
25
20
20
acute
Degrees C
25
15
15
10
Dec
Nov
Oct
Sep
Aug
Jul
Jun
May
Apr
Mar
Feb
Dec
Nov
Oct
Sep
Aug
Jul
Jun
May
0
Apr
0
Mar
5
Feb
5
Jan
10
Jan
Degees C
acute
General Concerns
Proposed narrative or stepped numeric standards
would relax required temperature standards during
critical spawning and incubation periods
• Spring spawners
• Cutthroat trout (CS-I)
• Rainbow trout (CS-II)
• Fall spawners
• Brook trout (CS-I)
• Brown trout (CS-II)
• Mountain whitefish (CS-II)
How is WQCD’s proposal
different than winter shoulder
season excursion?
All excursions address 303(d) listing decision
• DON’T list due to abnormally low flows
• DON’T list due to abnormally high air temperatures
• DON’T list due to abnormally warm spring or abnormally
warm fall (shoulder season excursion).
NO assumption that high temperatures due to these conditions
are protective of aquatic life.
Ovary and Sperm Development
• High water temperature during spawning inhibited
ovulation and decreased % survival to hatch
(Taranger and Hansen 1993, Jobling et al 1995)
• Thermal stress reduces oocytes ability to form egg
yolk (King and Pankhurst 2003)
Fertilization
• When fertilization occurs at elevated temperatures
larval survival is reduced (Van Der Kraak and Pankhusrt
1997)
• (Alavi and Cosson 2005) Increase in temperature…
• Increased initial velocity
• Decreased the percentage of motile spermatozoa
• Significantly decreased the total duration of forward
movement between 14-21 oC
Embryo Development
• At 15 oC or more, rainbow trout embryo quality
was poor (Billard 1985)
• The period of optimum egg viability is shortened
by elevated temperatures (Van Der Kraak and
Pankhurst 1997)
What triggers spawning?
• Photoperiod
• Temperature
For Salmonids
• Photoperiod is most important
• temperature secondary
(Van Der Kraak and Pankhurst 1996, Bye 1984)
Salmonidae - Rainbow Trout
Spawning in Colorado River (Nehring 1988)
April 20-May 10
• Viable levels of ovulation, egg production, and survival to
eyed stage occurs 9-15oC (9-12 oC is optimal) (Pankhurst et
al 1996).
Standard for CS-II during rainbow trout spawning
Spawning Numeric steps Narrative Current
Months
(proposed)
(proposed) standard
Narrative 18.3 oC
April
15.2 oC
May
18.3 oC
18.3 oC
18.3 oC
Salmonidae - Rainbow Trout
Incubation in Colorado River (Nehring 1988)
April 20-June 15
Optimal incubation temperature 7-15 oC (Humpesch 1985)
19oC is detrimental (Humpesch 1985)
Standard for CS-II during rainbow trout incubation
Incubation Numeric steps
Narrative
Current
Months
(proposed)
(proposed) standard
April
15.2 oC
Narrative
18.3 oC
May
18.3 oC
18.3 oC
18.3 oC
June
18.3 oC
18.3 oC
18.3 oC
Salmonidae - Brown Trout
Incubation in Colorado River (Nehring 1988)
November 1 – March 30
• Optimal incubation 8-10 oC (Ojanguren and Brana 2003,
Lahnsteiner 2012)
Standard for CS-II during brown trout incubation
Incubation Numeric steps Narrative Current
Months
(proposed)
(proposed) standard
November 12.1 oC
Narrative 9.0 oC
December 9.0 oC
9.0 oC
9.0 oC
January
9.0 oC
9.0 oC
9.0 oC
February 9.0 oC
9.0 oC
9.0 oC
March
12.1 oC
Narrative 9.0 oC
SECTION 2
Warm Water Streams
WQCD Stepped Proposal
WS-I, Proposed
WS-I, Current
35
30
chronic
35
acute
30
20
15
20
15
10
10
5
5
0
acute
25
Degrees C
Degees C
25
chronic
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
WQCD Narrative Proposal
WS-I, Current
35
30
WS-I, Proposed Narrative
chronic
35
acute
30
acute
25
Degrees C
Degees C
25
chronic
20
15
20
15
10
10
5
5
0
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Concerns
Does not provide adequately long or cold enough
winter for successful spawning of thermally
sensitive warm-water species.
Current standard may not provide adequate
protection for incubating eggs of spring spawners
What triggers spawning?
• Photoperiod
• Temperature
In general…
• Centrarchids- Photoperiod and temperature equally
important (Kaya and Hasler 1972)
• Cyprinids - mixed
• Golden shiners - Long photoperiods and warm
temperatures are required to induces spawning (de
Valming 1975).
Cyprinidae
Lake chub (Ahsan 1966)
• low temperatures (5–12 °C) are essential for normal gonadal
proliferation and formation of the primary spermatocytes.
Goldfish (Gillet et al 1978)
• High temperatures (20 and 30 oC) in spring blocked oogenesis
Carp (Davies et al 1986)
• Unseasonal elevation in temperature resulted in failure to ovulate
Golden Shiner (De Vlaming 1975).
• Cold temperatures trigger egg and sperm development
Moronidae – Striped Bass
Females constantly exposed to warm water (18 °C), with or
without a natural photoperiod cycle (Clark et al 2005)
• diminished levels of hormones that trigger yolk
formation
• Reduction in egg size
• premature degeneration of ovaries
Percidae – Yellow Perch
yellow perch
•Growth phase of the
ovaries is during
winter
•Optimum gonad
maturation occurred
at 6oC or lower for
185 days
Jones et al 1977
via Hokanson 1977
Percidae – Yellow Perch
•Optimum gonad maturation occurred at 6oC or lower
for 183 days (Krieger et al 1983)
•A winter minimum of 10 oC is near the upper limit,
for a minimum of 145 days (Krieger et al 1983)
Standard for WL during yellow
Months
Numeric steps
(proposed)
November
26.3 oC
December
21.9 oC
January
17.6 oC
February
13.2 oC
March
17.6 oC
April
26.3 oC
perch gondad development
Narrative
Current
(proposed)
Standard
26.3
26.3 oC
Narrative
26.3 oC
Narrative
13.2 oC
13.2oC
13.2 oC
Narrative
13.2 oC
Narrative
26.3 oC
Percidae – Yellow Perch
• Spawn and incubate in spring
• Egg and sperm viability during spawning is highest at 6 to 9 oC
• Highest percentage of hatch occurred at 9-15 oC (Hokanson
1977).
Standard for WL during yellow
incubation
Months
Numeric steps
(proposed)
April
26.3 oC
May
26.3 oC
June
26.3 oC
perch spawning and
Narrative
(proposed)
Narrative
26.3 oC
26.3 oC
Current
standard
26.3 oC
26.3 oC
26.3 oC
Percidae – Walleye
• Also require an extended cool period below 10 oC
throughout the winter
• Conclusions supported by field data (Miller 1967).
• Walleye failed to reproduce in isothermal
reservoir 10-12.5 oC throughout winter
walleye
Percidae – Walleye
(Smith and Koenst 1975) Walleye
reproduction was most successful when…
•fertilization occurred at 6-12 oC
•incubation 9-15 oC (48 – 54 oF)
Fertilization &
incubation
temperature
%
Abnormal
Fry
6
1
8.9
3.8
12
3.3
15
1.0
18.1
15.0
20.9
18.0
Percidae – Walleye
• Spawn and incubate in spring
• Optimum fertilization temperature 6 to 9 oC (Smith and Koenst 1975)
• Highest percentage of hatch occurred at 9-15 oC (Smith and Koenst
1975)
• Upper lethal temperatures for embryos is 19 oC (Smith and Koenst
1975)
Standard for WL during walleye spawning and incubation
Months
Numeric steps
Narrative
Current
(proposed)
(proposed)
standard
April
26.3 oC
Narrative
26.3 oC
May
26.3 oC
26.3 oC
26.3 oC
June
26.3 oC
26.3 oC
26.3 oC
Catastomidae- White Sucker
• Incubation thermal tolerance
studied by McCormick et al 1977
% normal
Incubation
temperature oC hatch
6.2
0.5
9.0
61.3
11.7
63.2
15.2
79.5
17.2
63.9
20.8
50.5
24.1
0
Catastomidae- White Sucker
• Spring spawners – late May – early June (Woodling 1985)
• Upper incubation temperature about 21 oC
• Current WS-II temperature during white sucker spawning
27.5 oC
Standard for WS-II during white sucker spawning and incubation
Months
Numeric steps
Narrative
Current
(proposed)
(proposed)
standard
May
27.5 oC
27.5 oC
27.5 oC
June
27.5 oC
27.5 oC
27.5 oC
11/26/2014
11/19/2014
11/12/2014
11/5/2014
10/29/2014
10/22/2014
10/15/2014
10/8/2014
10/1/2014
9/24/2014
9/17/2014
9/10/2014
9/3/2014
8/27/2014
77
8/20/2014
8/13/2014
8/6/2014
7/30/2014
7/23/2014
7/16/2014
7/9/2014
7/2/2014
6/25/2014
6/18/2014
6/11/2014
6/4/2014
5/28/2014
5/21/2014
5/14/2014
5/7/2014
Daily Mean Temperatue (˚F)
West Plum Creek Thermograph
WS-I MWAT
72
67
62
57
52
47
42
37
32
SECTION 3
Path Forward &
References
Potential path forward
• Continue to revise and update the temperature
standards to protect fisheries and aquatic life.
• Explore heat removal treatment options –
Feasibility study being explored by WQCD.
• Address compliance issues with variances?
• Potential for sector-based variance?
References
Alavi, S. M. H., & Cosson, J. (2005). Sperm motility in fishes. I. Effects of temperature and pH: a review. Cell biology
international, 29(2), 101-110.
Billard, R. (1983). Environmental factors in salmonid culture and the control of reproduction. In International Symposium on Salmonid
Reproduction, Bellevue, Washington (USA), 31 Oct-2 Nov 1983. Washington Sea Grant Program. Univ. of Washington.
Bye, V. J. (1984). The role of environmental factors in the timing of reproductive cycles. Fish reproduction: strategies and tactics,
187-205.
Clark, R. W., Henderson-Arzapalo, A., & Sullivan, C. V. (2005). Disparate effects of constant and annually-cycling daylength and water
temperature on reproductive maturation of striped bass (Morone saxatilis). Aquaculture, 249(1), 497-513.
Davies, P. R., Hanyu, I., Furukawa, K., & Nomura, M. (1986). Effect of temperature and photoperiod on sexual maturation and
spawning of the common carp: III. Induction of spawning by manipulating photoperiod and temperature. Aquaculture, 52(2), 137144.
de Vlaming, V. L. (1975). Effects of photoperiod and temperature on gonadal activity in the cyprinid teleost, Notemigonus
crysoleucas. Biological Bulletin, 402-415.
de Vlaming, V. L., & Paquette, G. (1977). Photoperiod and temperature effects on gonadal regression in the golden shiner,
Notemigonus crysoleucas. Copeia, 793-797.
Gillet, C., Breton, B., & Billard, R. (1978). Seasonal effects of exposure to temperature and photoperiod regimes on gonad growth and
plasma gonadotropin in goldfish (Carassius auratus). In Annales de Biologie Animale Biochimie Biophysique (Vol. 18, No. 4, pp.
1045-1049). EDP Sciences.
Humpesch, U. H. (1985). Inter-and intra-specific variation in hatching success and embryonic development of five species of salmonids
and Thymallus thymallus. Archiv für Hydrobiologie, 104(1), 129-144.
Jobling, M., Johnsen, H. K., Pettersen, G. W., & Henderson, R. J. (1995). Effect of temperature on reproductive development in
Arctic charr, Salvelinus alpinus (L.). Journal of Thermal Biology, 20(1), 157-165.
Kaya, C. M., & Hasler, A. D. (1972). Photoperiod and temperature effects on the gonads of green sunfish, Lepomis cyanellus
(Rafinesque), during the quiescent, winter phase of its annual sexual cycle. Transactions of the American Fisheries
Society, 101(2), 270-275.
References
King, H. R., & Pankhurst, N. W. (2003). Ovarian growth and plasma sex steroid and vitellogenin profiles during vitellogenesis in
Tasmanian female Atlantic salmon (Salmo salar). Aquaculture, 219(1), 797-813.
King, H. R., Pankhurst, N. W., & Watts, M. (2007). Reproductive sensitivity to elevated water temperatures in female Atlantic salmon
is heightened at certain stages of vitellogenesis. Journal of Fish Biology, 70(1), 190-205.
Krieger, D. A., Terrell, J. W., & Nelson, P. C. (1984). Habitat suitability information: Yellow perch. Western Energy and Land Use
Team, Division of Biological Services, Research and Development, Fish and Wildlife Service, US Department of the Interior.
Lahnsteiner, F. (2012). Thermotolerance of brown trout, Salmo trutta, gametes and embryos to increased water
temperatures. Journal of Applied Ichthyology,28(5), 745-751.
McCormick, J. H., Jones, B. R., & Hokanson, K. E. (1977). White sucker (Catostomus commersoni) embryo development, and early
growth and survival at different temperatures. Journal of the Fisheries Board of Canada, 34(7), 1019-1025.
Nehring, B. (1988). Fish Flow Investigation and Wild Trout Introductions. Colorado Division of Wildlife. Federal Aid Project F-15-R
Ojanguren, A. F., & Braña, F. (2003). Thermal dependence of embryonic growth and development in brown trout. Journal of Fish
Biology, 62(3), 580-590.
Pankhurst, N. W., Purser, G. J., Van Der Kraak, G., Thomas, P. M., & Forteath, G. N. R. (1996). Effect of holding temperature on
ovulation, egg fertility, plasma levels of reproductive hormones and in vitro ovarian steroidogenesis in the rainbow trout
Oncorhynchus mykiss. Aquaculture,146(3), 277-290.
Pankhurst, N. W., Purser, G. J., Van Der Kraak, G., Thomas, P. M., & Forteath, G. N. R. (1996). Effect of holding temperature on
ovulation, egg fertility, plasma levels of reproductive hormones and in vitro ovarian steroidogenesis in the rainbow trout
Oncorhynchus mykiss. Aquaculture,146(3), 277-290.
Taranger, G. L., & Hansen, T. (1993). Ovulation and egg survival following exposure of Atlantic salmon, Salmo salar L., broodstock to
different water temperatures. Aquaculture Research, 24(2), 151-156.
Van Der Kraak, G., & Parnkhurst, N. (1997). Temperature effects on the reproductive performance of fish. Global warming:
implications for freshwater and marine fish, 61, 159.
Vladiĉ, T., & Jätrvi, T. (1997). Sperm motility and fertilization time span in Atlantic salmon and brown trout—the effect of water
temperature. Journal of Fish Biology, 50(5), 1088-1093.