Prymnesium parvum Documented in 1920s and 1930s in Europe Prymnesium - - PDF document

5/25/2010 1

Prymnesium parvum in Inland Waters

1

Bryan W. Brooks1, James P. Grover2, Daniel L. Roelke3

1Baylor University, 2University of Texas Arlington, 3Texas A&M University

Bryan_Brooks@Baylor.edu; Tel: 254-710-6553

ORSANCO, 4 May, Cincinnati

Prymnesium parvum

• Documented in 1920s and

1930s in Europe

• Flagellated
• Mixotrophic
• “feeding swarms”

Photo: John LaClaire, University of Texas at Austin

2

• Euryhaline
• Eurythermal
• Encysts
• Produces exotoxins

– prymnesin ‐1, ‐2; others? – See Manning & La Claire (2010) for prymnesin review

Photo: Christina Esplund, Edna Graneli

Lake Granbury L k Lake Possum Kingdom 3 Lake Whitney Lake Waco

States where golden algae identified

• Originally a marine, coastal

species

• Moved inland to Texas

– Low salinities

Prymnesium parvum Blooms

4

– Invasive species – 1st identified in Pecos River 1985 – Now identified in at least 5 river basins, 33 water bodies – 2 hatcheries affected

Prymnesium parvum Blooms

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Prymnesium parvum Blooms

6

5/25/2010 2

Ceriodaphnia dubia

Lab Field ‐cosms

Towards a Predictive Understanding of P. parvum

7

Societal Value Variability Statistical Power

‐ + ‐ + ‐ +

Cell Density Does Not Always Correlate with Ambient Toxicity

Toxicity believed to result following exposure to prymnesium‐1, ‐2 and potentially others

8

Igarashi et al 1999

Cell Density Does Not Always Correlate with Ambient Toxicity

Lack of analytical standards preclude in‐depth understanding of exposure, toxicology to aquatic and terrestrial

• rganisms, including mammals.

1 M it d f t i d d Toxicity believed to result following exposure to prymnesium‐1, ‐2 and potentially others

9

• 1. Magnitude of toxins produced as a

function of ecophysiology/stress?

• 2. Fate of various toxins under a

range of environmental conditions: photolysis, biotransformation?

• 3. Accumulation and higher trophic

level effects (maitotoxin)?

Igarashi et al 1999

Previous Literature on P. parvum “Toxicity”

‐ Reviewed 96 published studies of aquatic toxicity attributed to

• P. parvum

‐ 23 3% vertebrates 21 1% zooplankton 20% erythrocytes

10

‐ 23.3% vertebrates, 21.1% zooplankton, 20% erythrocytes, 18.9% phytoplankton, 9.5% misc in vitro, 7.4% bacteria ‐ Only 50.5% specifically reported salinity of the assay (10 studies reported % of “seawater,” but not seawater salinity) ‐ 14.7% studied salinities less than 4 psu; 11.6% of these studies were recently reported from our project team

Brooks et al 2010

Optimum Conditions for Growth: ‐ temperature = 27oC ‐ salinity = 22 psu

Cell Density Does Not Always Correlate with Ambient Toxicity

11

Non‐optimum growth conditions = ↑ toxicity per cell (toxin production) Lower temperatures and low salinities = a recipe for Texas fish kills?

Baker et al 2007

Abiotic Influences on Ambient Toxicity

12

Granéli and Salomon 2010

5/25/2010 3

Nutrient Limitation and P parvum

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Nutrient Limitation and P. parvum

TAMU, UTA, BU

+ P. parvum ‐ BSE +

Comparative Toxicity during a Limnocorral Study

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‐ ‐ 28 day study in Spring 2006 ‐ 23 factorial design (3 reps) 1 m x 2 m limnocorals

Roelke et al 2007

TAMU, UTA, BU

melas Survival dilution)

10 12 14 16

Nutrient Treatment Main Effects

*

15

Mean Pimephales prom NOEC (percent

2 4 6 8

No Nutrients Nutrients Less Toxic More Toxic Roelke et al 2007

TAMU, UTA, BU

na Fecundity male-1)

25 30 35

Nutrient Treatment Main Effects

*

16

No Nutrients Nutrients Less Toxic More Toxic Roelke et al 2007

Mean Daphnia magn (neonates fem

5 10 15 20

Roelke et al 2007

Nutrient Limitation Increases Toxicity

17

Valenti et al 2010 Johansson and Granéli 1999

Comparative Aquatic Toxicity of P. parvum

18

Brooks et al 2010

5/25/2010 4

Hydrology Salinity and P parvum

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Hydrology, Salinity and P. parvum

TAMU Dataflow

On‐board, flow through system with geo‐referenced data collection

Heterogeneity of bloom: High‐resolution mapping

20

Hydraulic flushing terminates a toxic bloom in Lake Granbury, Brazos River, Texas

21

‐ Bloom initiation prior to Feb. 2007 ‐ Development, peak and decline Feb. through April ‐ Abrupt termination between April and May

Roelke et al 2010

Lake Granbury

120 River flow (106 m3 d-1)

Chlorophyll-a (µg liter-1)

Following prolonged period of drought

22

period of drought Chlorophyll a patches on the scale of 1 km

Roelke et al 2010

Lake Granbury

120 River flow (106 m3 d-1)

Chlorophyll-a (µg liter-1)

Following period of high inflows

23

inflows Chlorophyll a patches on the scale of 6 km

Roelke et al 2010

24

Roelke et al 2010

5/25/2010 5

Cell Density Does Not Always Correlate with Ambient Toxicity

25

Non‐optimal growth conditions = ↑ toxicity

Baker et al 2007

Salinity, Temperature and P. parvum Growth

26

Baker et al 2010

A Decade of Blooms in Lakes Possum Kingdom, Granbury, Whi h B

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Whitney on the Brazos River, Texas

Roelke et al. accepted. J. Plank Res

Bloom Dynamics

Timing of blooms

• wintertime phenomena
• environmental conditions far removed from the

ti diti f th

28

• ptimum conditions for growth
• concurrent in each reservoir

Magnitude of blooms

• higher population densities before Spring 2007
• Lake Granbury highest densities

Roelke et al. accepted. J. Plank Res

Bloom Dynamics

Hydrology Thresholds Identified

(7‐day accumulated inflow)

• ~10 x106 m3 Lake Possum Kingdom (0.01 d‐1)

20 106

3 L k G

b (0 12 d 1)

29

• ~20 x106 m3 Lake Granbury

(0.12 d‐1)

• ~40 x106 m3 Lake Whitney

(0.10 d‐1)

Bloom termination

• high inflows not a requirement

Roelke et al. accepted. J. Plank Res

Bloom Dynamics

Salinity Thresholds Identified

• ~1.5 psu for Lake Possum Kingdom
• 0.5 psu for Lakes Granbury and Whitney

30

Relationship non‐monotonic

linear function (41%) power function (40%) exponential function (35%)

Roelke et al. accepted. J. Plank Res

5/25/2010 6

pH and P parvum

31

pH and P. parvum

Locations of fish kills attributed to P. parvum

32

Southard, Fries, Barkoh. 2010.

Brazos River Watershed

33

Lower pH Generally, higher pH

120 River flow 106 m3 d-1

Highest ambient toxicity coincident with highest pH

34

Valenti et al 2010a, Roelke et al 2010

Ambient toxicity to fish/daphnia is influenced by pH

35

Valenti et al 2010a

Why is toxicity to fish and daphnia influenced by pH?

[ F/2 Nutrient ] NO CELLS FHM LC50 value

(% media)

6.5 7.5 8.5

20 40 60 80 100

36

‐ similar to previous studies with fish and pH at higher salinities ‐ but with lower pH hemolysis reported to increase

Valenti et al 2010a

6.5 7.5 8.5

pH

5 10 15 [ F/8 Nutrient ] NO CELLS FHM LC50 value

(% media)

6.5 7.5 8.5

pH

5/25/2010 7

Why is toxicity to fish and daphnia influenced by pH?

37

‐ other toxins?

Valenti et al 2010a,b

Sunlight and P parvum

38

Sunlight and P. parvum

BU, TAMU, UTA

Study 1. Natural sunlight influences on aquatic toxicity

• f cell free P. parvum cultures (8 hrs)

‐ Three treatment levels

39

Full Sun ~50% Sun No Sun

James et al, Accepted. J. Plank Res urvivorship (%)

70 80 90 100 Full Sunlight Partial Sunlight

Survivorship (%)

60 70 80 90 100 No Sunlight Lab Dark Control

Toxicity to fish ameliorated by full and partial sunlight

40 Prymnesium parvum Cell-Free Filtrate (%)

10 20 30 40 50 60 70 80 90 100

Pimephales promelas Su

10 20 30 40 50 60 a t a Su g t No Sunlight Lab Dark Control

Exposure Time (hrs)

1 2 3 4 5 6 7 8 9 10

Pimephales promelas S

10 20 30 40 50 60

LT50 = 2.3 hrs

James et al, Accepted. J. Plank Res

BU, TAMU, UTA

Study 2. Natural sunlight influences on aquatic toxicity

• f cell free P. parvum cultures (0.5, 1, 2, 4, 8 hrs)

‐ Two treatment levels, varied exposure durations

41

Full Sun No Sun

James et al, Accepted. J. Plank Res

BU, TAMU, UTA

Recall some aquatic chemistry and toxicology principles…

42

1/LC50 C0/Ct Time Time t1/2

5/25/2010 8

BU, TAMU, UTA promelas LC50 (% sample) 40 60 80 100 es promelas LT50 (hrs ) 15 20 25 30

ales promelas LC50

0.4 0.6 0.8 1.0

y = -0.9061x + 0.8359 R² = 0.8941

Toxicity to fish ameliorated by full and partial sunlight

43

Natural Sunlight Exposure Duration (hrs) Pimephales p 20 40 Pimephale 5 10 0 0.5 1 2

• Initial derivation of an aggregate photolysis half-life (t1/2) for P. parvum toxins?
• Based on the conditions of natural sunlight exposure in this study (mean PAR =

1762 µE), an aggregate t1/2 of 0.37 hrs is predicted for P. parvum toxins.

• Actual t1/2 would be compound specific and would be longer based on light

penetration with depth.

Time (hrs)

0.0 0.2 0.4 0.6 0.8 1.0

1/ Pimepha

0.0 0.2

James et al, Accepted. J. Plank Res

Salinity, Temperature

Developing a predictive understanding of P. parvum dynamics in inland waters

44

0.000611(I - 222) - 0.00000573(I - 222)2 +

Grover et al (2010) Baker et al (2009)

Salinity, Temperature, Light

Maximum growth rate

Baker et al., 2009 Grover et al., 2010

During bloom initiation

• P. parvum not

stressed During bloom

45

g development and peak P. parvum stressed! During bloom decline

• P. parvum not

stressed

Roelke et al 2010

2006-07 P. parvum blooms in Lake Granbury

sity Initiation: resource competition Development: resource competition, allelopathy, grazing inhibition Decline: pathogens? Termination: flushing, cessation of toxicity

46

Fall Winter Spring Summer

• P. parvum

population dens competition, immigration? Summer Fall Winter Spring Summer Summer

Roelke et al. accepted. J. Plank Res

Small population with active, motile cells Large population with active, motile cells Toxic, mixotrophic population Population growth Prey available Prey not available

47 Bloom Development

Toxic Phase Encystment Germination Immigration

Hypothesized role of toxicity and life history stages of P. parvum in the development

• f toxic blooms. Increasing size and darkness of arrows indicates stronger support
• f the hypothesized transition by observations to date.

Where We Stand

Developing predictive models that include f

48

numerous factors (competitors, predators, nutrients, light, salinity, temperature , allelopathy, flushing, exchange with coves, etc) Grover et al 2010

5/25/2010 9

Research Needs

Bloom initiation / termination, exposure, toxicology and risk

• competition and roles of toxin‐resistant grazers and virus
• allelopathy and mixotrophy
• comparative sensitivities of sport fish

49

• toxins elucidation, behavior/fate, transport, MOAs

Management Implications

• Several agents have been tested (ammonia, barley straw extract, copper herbicides)
• Other factors are being explored (flushing, cyanobacterial allelopathy, site specific pH)

Acknowledgements

50

Numerous students, staff, colleagues in Texas, Canada and Europe

References

JamesSV, Valenti TW, Prosser KP, GroverJP, Roelke DL, Brooks BW. Accepted. Sunlight amelioration of Prymnesium parvum toxicity to fish. J. Plank. Res. JamesSV*, Valenti, TW*, Roelke DL, GroverJP, Brooks BW. Accepted. Probabilistic ecological assessment of microcystin‐LR: Application in a case study of allelopathy to Prymnesium parvum. J. Plankt. Res. Schwierzke‐Wade L*, Roelke DL, Valenti TW*, Brooks BW, Grover JP. Accepted. Prymnesium parvum bloom termination: Roles of hydraulic dilution, without flushing, and grazing. J. Plank. Res. Roelke DL, Grover JP, Brooks BW, Glass J, Buzan D, Southard GM, Fries L, Gable GM, Schwierzke‐Wade L, Byrd M, Nelson J. Accepted. A decade of fish‐killing Prymnesium parvum blooms in Texas: Roles of inflow and salinity. J. Plank. Res. Grover JP, Crane KW*, Baker JW, Brooks BW, Roelke DL. 2010, In press. Spatial variation of harmful algae and their toxins in flowing‐water habitats: a theoretical exploration. J. Plank. Res. Manning SR, La Claire JW. 2010. Prymnesins: toxic metabolites of the golden alga, Prymnesium parvum Carter (Haptophyta). Marine Drugs 8:678‐704. Valenti Jr TW*, James SV*, Lahousse M*, Schug KA, Roelke DL, Grover JP, Brooks BW. 2010. Influence of pH on amine toxicology and implications for harmful algal bloom ecology. Toxicon 55: 1038‐1043. Valenti Jr TW*, James SV*, Lahousse M*, Schug KA, Roelke DL, Grover JP, Brooks BW. 2010. A mechanistic explanation for pH‐dependent ambient aquatic toxicity of Prymnesium parvum Carter. Toxicon 55: 990‐998. Roelke DL, Gable GM, Valenti TW*, Grover JP, Brooks BW, Pinckney JL. 2010. Hydraulic flushing as a Prymnesium parvum bloom‐terminating mechanism in a subtropical lake. Harmful Algae 9: 323‐332. Schug KA, Skingel TS*, Spencer SE*, Serrano C*, Le CQ*, Schug CA*, Valenti Jr. TW*, Brooks BW, Mydlarz LD, and JP Grover. 2010, In press. Hemolysis, fish mortality and LC‐ESI‐MS of cultured crude and fractionated golden alga (Prymnesium parvum). Journal of American Water Resources Association 46:33‐44. Brooks BW, James SV*, Valenti Jr. TW*, Urena‐Boeck F*, Serrano C*, Berninger JP*, Schwierzke L*, Mydlarz LD, Grover JP, & DL Roelke. 2010. Comparative toxicity of Prymnesium parvum in inland waters. Journal of American Water Resources Association 46: 45‐62. Schwierzke L* Roelke DL Brooks BW Grover JP Valenti Jr TW* Lahousse M* Miller CJ* & JL Pinckney 2010 Prymnesium parvum population dynamics during bloom development: a role assessment of

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Schwierzke L , Roelke DL, Brooks BW, Grover JP, Valenti, Jr TW , Lahousse M , Miller CJ , & JL Pinckney. 2010. Prymnesium parvum population dynamics during bloom development: a role assessment of grazers and virus. Journal of American Water Resources Association 46: 63‐75. Roelke DL, Schwierzke L*, Brooks BW, Grover JP, Errera RM, Valenti Jr. TW*, & JL Pinckney. 2010. Factors influencing Prymnesium parvum population dynamics during bloom initiation: Results from in‐lake mesocosm experiments. Journal of American Water Resources Association 46: 76‐91. Grover JP, Baker JW, Roelke DL, & BW Brooks. 2010. Mathematical models of population dynamics of Prymnesium parvum in inland waters. Journal of American Water Resources Association 46: 92‐107. Graneli E, Salomon P. 2010. Factors influencing allelopathy and toxicity in Prymnesium parvum. Journal of American Water Resources Association 46: 108‐120. Baker JW*, Grover JP, Nair R*, Valenti Jr TW*, Brooks BW, & DL Roelke. 2009. Dynamics at the edge of the niche: an experimental study of the harmful alga Prymnesium parvum. Limnology and Oceanography 54: 1679‐1687. Errera RM*, Roelke DL, Kiesling R, Brooks BW, Grover JP, Ureña‐Boeck F*, Baker JW*, Schwierzke L* & JL Pinckney. 2008. The effect of nitrogen and phosphorus availability, barley straw extract, and immigration on Prymnesium parvum community dominance and toxicity: Results from in‐lake microcosm experiments, Texas, USA. Aquatic Microbial Ecology 52: 33‐44. Grover JP, Baker JW*, Ureña‐Boeck F*, Brooks BW, Errera RM*, Roelke DL, & RL Kiesling. 2007. Laboratory tests of ammonium and barley straw extract as agents to suppress abundance and toxicity to fish

• f the harmful alga Prymnesium parvum. Water Research 41: 2503‐2512.

Baker JW*, Grover JP, Brooks BW, Ureña‐Boeck F*, Roelke DL, Errera RM* & RL Kiesling. 2007. Growth and toxicity of Prymnesium parvum (“golden algae”) as a function of salinity, light and temperature. Journal of Phycology 43: 219–227. Roelke DL, Errera RM*, Kiesling RL, Brooks BW, Grover JP, Ureña‐Boeck F*, Baker JW* & JL Pinckney. 2007. Effects of nutrient enrichment on Prymnesium parvum population dynamics and toxicity: results from field experiments, Lake Possum Kingdom, USA. Aquatic Microbial Ecology 46: 125–140. Igarashi T, Satake M, Yasumoto T. 1999. Structural and partial stereochemical assignments from prymnesin‐1 and prymnesin‐2: potent hemolytic and ichthyotoxic glycosides isolated from the red tide alga Prymnesium parvum. J. Am. Chem. Soc. 121: 8499–8511. Johansson N, Graneli E. 1999. Influence of different nutrient conditions on cell density, chemical composition and toxicity of Prymnesium parvum (Haptophyta) in semi‐continuous cultures. J. Exp. Mar. Biol.

• Ecol. 239, 243–258.

In Review: Skingel TR, Spencer SE, Le CQ, Serrano CA, Mydlarz LD, Scarbrough BJ, Schug KA, Brooks BW, Grover JP. In review. Hemolytic toxicity and nutritional status of Prymnesium parvum during population growth