Zebra Mussel: Shifting Environmental Thresholds Living on the Thermal Edge Robert F

Zebra Mussel: Shifting Environmental Thresholds Living on the Thermal Edge Robert F. McMahon Professor Emeritus Department of Biology The University of Texas at Arlington Center for Biological The University of Texas WRP and GASRP Combined Fall Meeting Macrofouling Research at Arlington September 17-19 2014, Houston, Texas

Zebra Mussels in Lake Texoma, TX/OK 2011 Outline

• Thermal Aspects of the Present Distribution of Zebra Mussels in North America and Europe • Zebra Mussel Thermal Adaptation in Southwestern Water Bodies • Zebra Mussel Population Dynamics in a Warm Texas Water Body • Zebra Mussel Starvation at Elevated Summer Water Temperatures • Hydrological and Thermal Characteristics of Texas Water Bodies Relative to Zebra Mussel Invasion Resistance • Conclusions Zebra and Quagga Mussels in North America

• Originally endemic to Europe • Introduced to North America in ~ 1984-1985 • Zebra mussels found in Lake Erie in 1986 • Rapidly spread throughout major eastern US drainage systems • Zebra Mussels: Great Lakes, Mississippi River and eastern tributaries, lower Missouri River, Arkansas River, isolated water bodies • Quagga Mussels: Great Lakes, upper Mississippi and lower Ohio Rivers, lower Colorado River, reservoirs in Colorado, Arizona, southern California • Rapid dispersal through navigable waterways on commercial vessels and through canals and water conduits between water bodies • Dispersed more slowly to isolated water bodies (i.e., overland transport) • Zebra Mussels recently found in San Justo Reservoir Central California (2008), in Texas, Lake Texoma, (2009), Lake Ray Roberts (2012) and Lake Belton (2013), and Lake Bridgeport (2014) Thermal Aspects of the Present Distribution of Zebra Mussels in North America and Europe

Open GIS Webmapping Service

Zebra/Quagga Mussel Temperature Limits for Invasion

Predicted Zebra Mussel Distribution Based on Average Maximal and minimal Monthly Surface Water Temperatures

• Generally agreed long-term incipient upper thermal limit of zebra mussels was 30°C and 28°C for quagga mussels based on European and Northeastern US studies • Generally agreed temperature for initiation of spawning was 16-18°C • These temperature limits were used predict potential zebra mussel distribution in North America based on maximum summer surface water temperatures – similar for quagga mussels • Recent successful establishment of zebra mussels in warm waters of Texas and quagga mussels in the warm waters of the Lower Colorado, southern California and Arizona requires a re-examination of these assumptions European Distribution of Dreissenid Mussels Relative to Peak Summer Temperature

Endemic Invasion Range Range 1°C Mean Maximum Air Temperature Isotherms (1961-1990) Source: Spatial Climate Analysis Service, Oregon State University

Windfield City Lake Lake Oologah

35°C 33°C Lake Texoma Lake Bridgeport Lake Ray Roberts 32°C Lake Belton 34°C Confirmed western quagga mussel populations 35°C Confirmed zebra mussel populations Zebra Mussel Thermal Adaptation in Southwestern Water Bodies

Todd Robinson of TPWD with zebra mussel infested rock from Lake Texoma. From State Impact: Energy and Environment reporting for Texas 03/19/2014 ComparisonComparison of Median ofSurvival Median Times Survivial Between Times ZebraBetween Mussels from WinfieldWinfield City City Lake Lake (KS) KS and and Hedges Hedges Lake Lake NY (NY)

900 Shell Length = 15 mm 800 Acclimation Temp. = 20øC 700 WCL Incipient Upper Thermal Limit = 31.7°C

600 WCL Ea rly WCL La te 500 HL 2 0 0 6 400 HL 2 0 0 7 300

200

Median Survival Time (h)

100

Near 100% Su rvival o ver 672 h Su 672 o rvival ver 100% Near

Near 100% Su rvival o ver 672 h Su 672 o rvival ver 100% Near 0 h Su 672 o rvival ver 100% Near 28 29 30 31 32 33 34 Treatment Temperature (øC) Morse 2009 2011 and 2012 qPCR Results

1e+10 Spring 2011 1e+09 1e+08 1e+07 1000000 100000 10000 1000 100 10 1 1e+10 F a ll 2 0 1 1 1e+09 1e+08 1e+07 1000000 100000 10000 1000 100 10 1 NSa o t mple d NSa o t mple d NSa o t mple d NSa o t mple d 1e+10 Spring 2012 1e+09 LTX: Lake Texom a LLV: Lake Lavon 1e+08 LA: Lake Arr ow head LTA: Lake Taw akoni 1e+07 LB: Lake Bri dgepor t LF: Lake For k 1000000 EM L: Eagl e M ount ai n LakeLBS: Lake Bob Sandl i n 100000 LLE: Lake Lew i svi l l e LO P: Lake O ' t he Pi nes 10000 LRR: Lake Ray Rober t s LWP: Lake Wri ght Patman 1000 100 LRH: Lake Ray Hubbar d CL: Caddo Lake 10 1 1e+10 Fall 2012 1e+09 1e+08

Number of DNA Fragment1e+07 Copies/Sample 1000000 100000 10000 1000 100 10 1 LTX LA LB EML LLE LRR LRH LLV LTA LF LBS LOP LWP CL Wa te r Body 2013 qPCR Results for 23 Texas Water Bodies

1e+11 Results of 2013 Spring-Early Summer and Fall qPCR 1e+10 Testing of Plankton Samples for Zebra Mussels 1e+09 in 23 Texas Water Bodies

1e+08

1e+07 Spring-Early Summer Sampling

1000000 Fall Sampling

100000

10000

1000

100

Number of DNA Fragment Copies of DNA Number 1

0.1

Fork

Worth

Lavon

A thens

C onroe

Texoma

Joe P ool Joe

P alesti ne

A rl i ngton

Granbury

Tawakoni

eisvilLewi l e

Grapevine

Livingston

B ri dgeport

B endbrook

R ay RR ay oberts CC reek edar

R ay RH ay ubbard

Mari ne MariC ne reek

E agle EMountain agle

P ossum K iP ngdom ossum

Water Body Name CR hambers i chland Texas Water Bodies with Known or Suspected Zebra Mussel Infestations

2009 2010 2011 2012 2013

Water Body

qPCR Larvae Juveniles Adults qPCR Larvae Juveniles Adults qPCR Larvae Juveniles Adults qPCR Larvae Juveniles Adults qPCR Larvae Juveniles Adults

Texoma                 Ray Roberts         Belton  Lavon     Ray Hubbard   Arrowhead  Bridgeport     Eagle Mountain   Lewisville     Caddo Lake  Bob Sandlin  Worth  Grapevine  Fork  Tawakoni  Joe Pool  Granbury  Livingston  Arlington Benbrook Athens Palestine Marine Creek Possum Kingdom Richland Chambers Cedar Creek Conroe Livingston

Not Infested Unlikely Suspect Probable Infested Legend Present State of Zebra Infested Mussel Invasion of Probable Texas Water Bodies Suspect Unlikely Texoma Arrowhead

Not Infested Ray Roberts Bridgeport Lewisville Lavon Bob Sandlin Grapevine Fork Possum Eagle Mountain Ray Hubbard Marine Creek Tawakonil Caddo Kingdom Worth Benbrook Joe Pool Arlington Granbury

Athens Palestine Cedar Creek Richland Chambers

Belton

Conroe Livingsto n Zebra Mussel Population Dynamics in a Warm Texas Water Body (Lake Texoma)

Lake Texoma • Hobo data loggers recorded surface water temperatures continuously at one hour intervals

Settlement Monitor • Daily mean surface water temperatures computed from hourly data

Data Logger

Brick Weight August Mean Daily Water Temperature (°C)

Gran b u ry Mean AugustWater Surface P o ssum Kin g d o m Bo b Sa n d lin C a d d o O' the Pin e s P a le stin e A rrow h e a d

T e xoma In fe ste d in TexasWater Bodies A the n s y d o B r e t a W s a x e T F o rk T a w a k o n i C o n roe Wrig h tPa tman L a v o n Ra yHu b b a rd

S U n r e t s e w h t u o S t i m i L r e p p U

L e w isville S U m r t s e w h t u o S l a n i g r a M

In fe ste d e p o r u E t i m i L l a m r e h T

R a yRo b e rts S U n r e t s a e h t r o N & A rlin g ton B rid g e p o rt In fe ste d (L o w L e v e l) Grap e v in e Ea g le Mo u n tain

Joe Po o l Temperature Ma rin e Cree k Wo rth Ce d a rCree k L iv in g ston Ric h lan d Ch a mbe rs

rainage Basins n i s a B e g a n i a Dr

s o z a r B

- y t i n i r T

s s e r y C

s e h c e N

e n i b a S

r u h p u S

d e R

o t n i c a J n a S

k r o F t s a E - y t i n i r T

k r o F m l E - y t i n i r T

- y t i n i r T

m e t S n i a M

k r o F t s e W Zebra Mussel Distribution in Lake Texoma (TK/OK) D ai l y M ean W at er T em per at ur e ( º C )

5/1/11 Lake

7/1/11

9/1/11 Texoma 11/1/11

1/1/12 C º 0 3 3/1/12

5/1/12 DailyMean Water Temperature

7/1/12

r a e Y d n a h t n o M 9/1/12

11/1/12

1/1/13 3/1/13

5/1/13

7/1/13

9/1/13 11/1/13

1/1/14 3/1/14 5/1/14

7/1/14

9/1/14 Zebra Mussel Size Distributions in Lake Texoma

2011 2012 2013 A M J J A S 0 N D J F M A M J J A S O N D J F M A M J J A S O N D 35

2 0 1 2 - S

5% of Sample 2 0 1 1 - S

30 2 0 1 2 - S

2 0 1 2 - S

25 2 0 1 1 - S

2 0 1 2 - S

2012 - S

2 0 1 1 -S 2 0 1 2 - S

2012 - S

2012 - F

2 0 1 2 - S 20 2011 - S

201 15 2 0 1 1 - S

Shell Length (mm)

201 10

2 0 1 2 - F

5 2 0 1 1 - S

2 0 1 2 - F

2 0 1 2 -S 2 0 1 2 - S S

2 0 1 2 -S -

0 2 0 1 2 - F 2012- F 2 0 1 2 - F

201

100 200 300 400 500 600 700 800 900 1000 1100 Days Since 01/01/2011 Zebra Mussel Growth Rate & Life Spans in Lake Texoma

2011 2012 2013 2014 AM J J A S 0 N D J F M A MJ J A S O N D J F MAM J J A S O ND J FM AM J J A S ON D 30

Mean ShMean ell L eng th (mm)

6 S-2012 G enerat i on

3 S-2013 G enerat i on S-2011 F-2012 G enerat i on G enerat i on S-2014 0 G enerat i on

100 200 300 400 500 600 700 800 900 1000 1100 1200 1300 1400 Days Since 01/01/2011 Dreissenid Growth Rates – US and Europe

50 Lake Texoma, TX (ZM) Boulder Basin Lake M ead (QM ) Lower M ississippi, Baton Rouge, LA (ZM ) 40 Great Yarmouth, England (ZM ) Walthamstow, England (ZM ) Szczecin Lagoon, Poland (ZM ) 30 M asurian Lakes, Poland (ZM )

Mean Shell Length (mm) Length Shell Mean 10

0 0 1 2 3 4 5 Y ear s of Life Zebra Mussel Veliger Size Distributions in Lake Texoma

2011 2012 2013 A M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D

400 10% of Sam pl e Spr i ng Spaw ni ng 350 Fal l Spaw ni ng

300

250 Pedivel i ger Settl ement Size

200

150

L arval ShLarval ell Length (æm)

100

n= 145

12 n= 2

n= 168

n= 56

n= 105

n= n= 108

n= 123

50 n= 59

n= 110

n= 135

n= 107

n= 129

n= 106 n= 101

n= 110

No No vel i ger s pr esent

n= 205

0 100 200 300 400 500 600 700 800 900 1000 1100 Days Since 01/01/2011 Zebra Mussel Settlement in Lake Texoma

70000

60000

-2 50000

40000

30000

20000

Settled Juveniles m

10000

No Settlement Occurred Settlement No 0 Spri ng 2011 Fall 2011 Spri ng 2012 Fall 2012 Spri ng 2013 Fall 2013 Spri ng 2014 Sampling Period Zebra Mussel Starvation at Elevated Summer Water Temperatures

7 Lake Texoma Temperature and Dissolved O with Depth (07/27/2011) 30 2 6 29 Temp: NTM WD Intake Temp: Dam Intake 28 DO: NTNWD Intake 5

DO: Dam Intake -1)

27 Data Provi ded by Texas Dept. of Parks and Wi l dli fe 4

(mg l (mg

26 2

25 3

24 2

23 O Dissolved

22 1

Ambient Water Temperature (ºC) Temperature Water Ambient 21 0 20 0 2 4 6 8 10 12 14 16 18 20 22 24 26 Depth (m ) 30 120 Zebra Mussel Dry Tissue A100% A 100 A90% 25 Weight Variation in 30 mm 20 80 C67% Winfield City Lake, KS A100% BC 57% A89% B50% 15 60 B47% 25 mm BC 60% C66% ● Estimated DTW from 40 B100% B51% B54% 10 A86% regression equations for CD 63% D65% 20 mm C56% CD 58%

20 5 Mean Daily Temp. (øC)

Dry Tissue Weight (mg) specific sized mussels

0 0 ● J u n . J u l. Au g . Se p t. Oc t. SL = 5, 10, 15, 20, 25, and 30 Date of Collection mm

30 ● DTW declined at water 14 B100% B temperatures >25°C

12 A85% 25 15 mm C69% ● Most pronounced in larger 10 C66% C64% C64% 20 mussels 8 15 6 ● Suggests starvation above B100% 4 A82% A77% A76% A78% 10 C62% 25°C 10 mm 2 A75% A97% A89% A100% A99% B57% 5

Mean Daily Temp. (øC)

Dry Tissue Weight (mg) ● Most pronounced in larger 0 5 mm 0 individuals J u n . J u l. Au g . Se p t. Oc t. Date of Collection McMahon, Leung and Morse Comparison of Mussel DTW of Lake Oologah and Winfield City Lake

110 100 Lake Oologah (06/29/07)

100 90 Winfield City Lake, KS (06/29/08) Winfield City Lake (06/29/07)

Log10 DTW (g) = -5.3829 + 2.9842 x Log SL (mm) 10 90 80

80 70 Lake Oologah, OK (06/29/07) Log10 DTW (g) = -5.1202 + 2.4739 x Log SL (mm) 10 70 60 60 50 50 40

Dry Tissue Dry Weight (mg) 40 32.3%

30 Estimated Tissue Dry Weight (mg) 30

20 35.4%

20 39.7% 10

10 46.0% 56.6% 0 80.5% 0 0 5 10 15 20 25 30 5 10 15 20 25 30 Shell Length (mm) Shell Length (mm) Dry Tissue Weight for Standard Sized Individuals Annual Dry Tissue Weight Variation 80. 0 A Las Vegas Boat Harbor 60. 0 SL = 25 mm • In all examined standard sized mussels a 40. 0 tendency to loss DTW occurred when water 20. 0 temperatures rose above 25°C 0. 0 B • More pronounced in larger individuals 25. 0 SL = 20 mm 20. 0 • Indicative of summer starvation 15. 0 • Maintenance energy demands > energy 10. 0 5. 0 assimilation 0. 0 • Negative scope for growth 8. 0 C SL = 15 mm • Larger individuals gain tissue mass when 6. 0 water temperatures are <18°C 4. 0 Maintenance energy demands < energy 2. 0 • 0. 0 assimilation D 4. 0 • Positive scope for growth SL = 10 mm 3. 0 • Not spawning 2. 0 • Reduced maintenance energy due to low 1. 0 Dry Tissue Weight (mg) water temperatures 0. 0 40 2. 0 E Dreissena polymorporpha Dreissena bugensis SL = 5 mm 5°C Acclimated 5°C Acclimated 1. 5 35 15°C Acclimated 20°C Acclimated 1. 0 30 25°C Acclimated 0. 5 25 0. 0 F 30 G ravi d G onads 20 25øC O 25 15 20 18øC 15 10 T e mp. (ø C) 10 5

0 7/1/09 8/1/09 9/1/09 1/1/10 2/1/10 3/1/10 4/1/10 5/1/10 6/1/10 7/1/10 8/1/10 9/1/10 10/1/09 11/1/09 12/1/09 10/1/10 11/1/10 5 10 15 20 25 30 35 40 45 Temperature (°C) Hydrological and Thermal Characteristics of Texas Water Bodies Relative to Resistance to Zebra Mussel Invasion

Adult Zebra Mussels on Settlement Monitor in Lake Ray Roberts, August 4, 2014 Texas Water Body Hydrological Characteristics Relative to Mussel Invasion 35 28 Drianage Basins 21 Walnut (KS) 14

In fe d ste

In fe d ste Max. D epth Max. (m) D epth 7 Arkansas (OK)

In fe d ste (L o wL e v e l) 0 C y r e s s 10 8 R e d 6 S a b i n e 4

A vg. D epth A (m) vg. D epth

In fe d ste 2 In fe d ste S u p h u r

In fe d ste (L o wL e v e l) 0 Trinit y-East Fork 0.5 0.4 Trinity-West Fork 0.3 Trinit y-Elm Fork 0.2

0.1 In fe d ste

In fe d ste

Max. Max. / A vg. D epth

In fe d ste (L o wL e v e l) 0.0

F o rk

L a v o n

C a d d o

T e xoma

T a w a k o n i L e w isville

i gB rid e p o rt

rwhA rrow e a d

Bo bSa n d lin

O' thePin eO' s

R a y Ro R b a e y rts

R a y Hu Ra b b y a rd

Oo log a h(OK)

Wrig h t Pa h tman t Wrig

Ea gMo le u n tain

Win fie ld City (KS ) City ld fie Win W a t e r B o d y Texas Water Body Thermal Characteristics Relative to Mussel Invasion

32 31 30 Drianage Basins 29 Walnut (KS) 28

27 In fe d ste

In fe d ste Arkansas (OK) 26 In fe d ste (L o wL e v e l)

Mean Aug. Temp.(ºC) 25 C y r e s s 150 130 R e d 110 S a b i n e 90

D a y s > 2 5 º C

In fe d ste 70 In fe d ste S u p h u r

In fe d ste (L o wL e v e l) 50 Trinit y-East Fork 6 00 5 00 Trinity-West Fork 4 00 3 00 Trinit y-Elm Fork 2 00

In fe d ste

In fe d ste (L o wL e v e l)

Sum1 00ºC Days >25ºC 0

F o rk

L a v o n

C a d d o

T e xoma

T a w a k o n i L e w isville

i gB rid e p o rt

rwhA rrow e a d

Bo bSa n d lin

O' thePin eO' s

R a y Ro R b a e y rts

R a y Hu Ra b b y a rd

Oo log a h(OK)

Wrig h t Pa h tman t Wrig

Ea gMo le u n tain

Win fie ld City (KS ) City ld fie Win W a t e r B o d y Correlation of Texas Water Body Hydrological and Thermal Characteristics

160 150 r = 0.4582, p =0.0994 140 Lake Bridgeport 130 120 Lake Ray Roberts Days > 25ºC Lake Texoma 110 Maximum Depth (m) 1 00 5 10 15 20 25 30 35 150 r = 0.4493, p =0.1070 140 Lake Bridgeport 130 120 Lake Ray Roberts Lake Texoma Days110 >25 ºC Mean Depth (m) 1 00 0 1 2 3 4 5 6 7 8 9 10 150 r = 0.0229, p =0.9381 Lake 140 Bridgeport 130 Lake Ray 120 Roberts Lake

D a y s > 2 5 º C 110 Texoma Maximum / Mean Depth 1 00

0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55 0.60 Lake Ray Roberts Lake Ray Roberts Plankton Sample 06/14/2014

Lake Ray Roberts • Maximum depth = 32.3 m

13.53 km 13.53 • Average depth = 8.39 m • Mean August Temperature = 29.9°C • Number of days >25°C = 121 • Sum °days >25°C = 399.5 Lake Lewisville • Maximum depth = 14.33 m • Average depth = 6.32 m • Mean August Temperature = 30.4°C • Number of days >25°C = 137 • Sum °days >25°C = 473.178 Lake Lewisville Lake Lewisville may be thermally resistant to zebra mussel invasion Conclusions

• Zebra mussels appear to have evolved increased thermal resistance in warm southwestern water bodies • Increased thermal tolerance (31°C) • Continue to spawn up to 30°C (>25°C upper limit in European and Northeastern US) • Veliger larvae tolerate temperatures up to 30°C (<25°C in Europe and Northeastern US)

• Impacts of elevated water temperatures on zebra mussel biology and ecology • Increased growth rates and shorter life spans in Texas water bodies • Elevated summer water temperatures (>25°C) lead to starvation and loss of tissue mass • Nutrient removal – reduction in phyto-bacterioplankton food availability • Most prominent in adult mussels • May result in life spans being reduced to 1-1.5 years • May eventually lead to population density reduction or extirpation

• Some southwestern water bodies may be thermally resistant to zebra mussel invasion • Surface water temperatures tend to increase with decreased water body depth • Increases the number of days when water temperature is >25°C • Increases the number of °days >25°C experienced by mussels during summer months • Increased heat stress in shallow water bodies may lead to mussel starvation and extirpation • Highest at-risk water bodies may be characterized by: • Elevated maximum and mean depths • Reduced surface water temperatures (<31°C) during summer months • May be a potential parameter for zebra mussel invasion risk assessment for southwestern water bodies • May be the basis for lack of successful zebra mussel invasion of Lake Lewisville even though it is receiving mussel larvae from the highly mussel infested Lake Ray Roberts 13.5 km upstream Acknowledgements

Funding US Fish and Wildlife Service (USFWS) Texas Parks and Wildlife Department (TPWD)

Collaborators David K. Britton (USFWS) Earl Chilton (TPWD) Brian VanZee (TPWD) Mark Ernst (Tarrant Regional Water District)

Technical and Field Assistance M. Colette McMahon (UT Arlington) Heather Arterburn (UT Arlington) Maj Angarano (Volunteer) Tim Mattingly (Tarrant Regional Water District) The many marina owners who allowed mussel veliger larvae sampling to be conducted and settlement monitors deployed at their facilities Thanks For Your Attention