Global change and cyanobacterial blooms in French freshwater

Jul 17, 2003 - Blue-green algae. Photosynthetic prokaryotes. Long evolutionary history .... non colony forming. • Gas vesicles. • no heterocysts. • no akinetes.
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The impact of global environmental problems on continental and coastal marine waters ------------------------------------Water related environmental risk of global importance

Global change and cyanobacterial blooms in French freshwater ecosystems Jacquet S, Dufour P, Latour D, Briand JF, Bernard C, Humbert JF

NEAR conference, Geneva, 17 July 2003

What are Cyanobacteria ? Blue-green algae Photosynthetic prokaryotes Long evolutionary history (3.5 Gy) High tolerance to stress (pollution, UV…) Bloom forming species : proliferation phases Toxic forms Ecological implications

Cyanobacterial blooms result from competitive situations between phytoplanktonic species

Environmental factors favoring these situations : ! Nutrient pollution (54 % of eutrophic lakes in Europe) !

Stability and “high” temperature of the water column (blooms occur principally in summer)

Why cyanobacteria are often the winner in competitive situations ? - Control of their buoyancy - Heterocysts , akinetes - Photo-heterotrophic - High reserve capacities - Accessory pigments (ex: phycoerythrin) - Multicellular organization (filaments, colonies) - Poor food quality - Synthesis of toxins

nutrient/light uptake & resistance

defense against predation

… and the winner is:

Impacts of cyanobacteria ! Ecological impact : - Perturbations of the ecosystem functioning - Shade - toxin accumulation and transfer thru the trophic chains - Anoxia at the end of the bloom ! Sanitary impacts : - Mortality and morbidity in aquatic and terrestrial invertebrates and vertebrates Example: In Switzerland, more than 100 cattle deaths were attributed during the last two decades to cyanotoxin poisoning

- Human contamination

Human poisoning by cyanotoxins ! Short term effects - Gastrointestinal and/or hepatic illnesses - Death of kidney dialysis patients in Brazil ! Chronic term effects - Hepatic carcinoma

Principal routes of exposure ! Oral exposure through drinking water, ! Oral and dermal exposure trough recreational water use ! Oral exposure through consumption of toxic products and/or algal health food tablets ! Haemo-dialysis

What is global change ? Eutrophisation / re-oligotrophisation (restoration) (phosphorus) Increase of temperature (warmer winter and springs) Urbanization of catchment's area (more inhabitants and constructions around the lakes) New types of pollution (agriculture, industry & domestic sources)

4 case-studies in France # Planktothrix rubescens in Lake Bourget # Planktothrix agardhii in Lake Viry # Microcystis aeruginosa in Grangent reservoir # Cylindrospermopsis raciborskii in the Francs-Pécheurs pond

The case of Planktothrix rubescens Decrease of P from 120 µg/l to 30 µg/l in the last 20 years In the largest natural French lake: Lake Bourget BUT problems with the toxic cyanobacterium P. rubescens since 1996-97

Lake Bourget

The case of Planktothrix rubescens in Lake Bourget 0m

50 m July 99

April 00

July 00

April 01

MCYS-RR (µg/l) 6

10 m 15 m

5 4

20 m

WHO drinking water guideline conc. of 1µg/l

3 2 1

03

-a oû t-9 31 9 -a oû t-9 9 13 -s ep t-9 9 29 -s ep t-9 9 14 -o ct -9 9 03 -n ov -9 9 16 -n ov -9 9 29 -n ov -9 9 07 -d éc -9 9 22 -d éc -9 05 9 -ja nv -0 18 0 -ja nv -0 31 0 -ja nv -0 0 15 -fé vr -0 0

0

July 01

April 02

How to explain P. rubescens bloom since 6 years ?

P +++

24 °C

P +++

P +++

PP+

7 °C

Eutrophic conditions

P +++ Meso-trophic conditions

P. rubescens is - low light, low temperature, low nutrient adapted - photo-heterotrophic - filamentous and toxic and hence little grazed - probably little affected by parasitism (viruses) - able to regulate its buoyancy - enhanced by P pulses, …

A possible scenario Climatic influence = Warmer winter & spring

Advance of spring bloom & zooplankton development = Advance in population decline & advance of clear water phase

Human pressure = Reduction of P

Advance of P-depleted Surface waters = Sinking of population & the P-depleted zone

Very competitive species for the new environmental conditions: low nutrient, low light of metalimnion

Planktothrix rubescens Low grazing, low viral attack, stable water column

The case of Microcystis aeruginosa Grangent reservoir

The case of Microcystis aeruginosa water 0,5 m

Sediment 0-2cm

100

1500 1000

50 500 0

Sediment colonies.mL-1

Water colonies.L-1

2000

0 1/4

1/5

1/6

1/7

= recruitment from benthic colonies Cause: O2 reduction = growth stimulation and back of floatability

The case of Microcystis aeruginosa Benthic colonies

12

1200

8

800

4

400

0

0 1/2

1/3

1/4

1/5

1/6

1/7

Colonies.ml-1

Temperature (°C)

Temperature at 40m

1/8

Cause : Temperature elevation of hypolimnion (>8°C) = metabolic activity, bloom and surface accumulation

The case of Microcystis aeruginosa 2000 No bloom

400

8

8°C 4

200

0

0 1/4

1/5

1/6

1/7

1/8

M. aeruginosa

800

600

12

8°C

8

8°C

400

4 200

0

0 1/4

1/5

1/6

1/7

1/8

In this context, increasing temperature (global warming) will increase the problem of this eutrophicated ecosystem ?

Temperature (°C)

8°C

temperature 12

Colonies.L-1

Colonies.L-1

600

M. aeruginosa

Temperature (°C)

temperature

800

2001 Bloom

The case of Planktothrix agardhii • Filamentous, uniseriate • Maximum length : 300 µm • no mucilage • non colony forming • Gas vesicles • no heterocysts • no akinetes • European northern area : Scandinavia,Estonia, Germany, The Netherlands, France…), also Japan, Korea and Minnesota (United States) • The more southern countries : Spain and Florida (US)

The case of Planktothrix agardhii

Viry-Châtillon, 25 km south of Paris, France Surface : 978 000 m2 Depth : 5.3 m max 2.8 m mean Main activity : fishing, sailing, water-skiing

The case of Planktothrix agardhii

4,5E+06

90

4,0E+06

80

3,5E+06

70

3,0E+06

60

2,5E+06

50

2,0E+06

40

1,5E+06

30

1,0E+06

20

5,0E+05

10

0,0E+00

0

6,0

5,0

MCYST-LR eq. (µg / L)

100

4,0

3,0

2,0

1,0

0,0 20 /0 1/ 99 24 /0 2/ 99 25 /0 3/ 99 20 /0 4/ 99 18 /0 5/ 99 22 /0 6/ 99 20 /0 7/ 99 18 /0 8/ 99 23 /0 9/ 99 14 /1 0/ 99 16 /1 1/ 99 16 /1 2/ 99 03 /0 2/ 00

5,0E+06

conc. chl.(µg/L), Secchi disk (cm)

trichomes nb / L

Viry-Châtillon recreational area

H2O (PP2A)

Cells (HPLC-DAD)

20

/0 1 24 /99 /0 2 25 /99 /0 3 20 /99 /0 4 18 /99 /0 5 22 /99 /0 6 20 /99 /0 7 18 /99 /0 8 23 /99 /0 9 14 /99 /1 0 16 /99 /1 1 16 /99 /1 2 03 /99 /0 2/ 00

Cells (PP2A)

P. agardhii

L. redekei (x10)

chl. a

Secchi disk

2.3 ± 1.9 µg/L MCYST-LR eq. (cells) • perenial bloom of P. agardhii • only one associated microalgae : max. : 5.2 µg/L MCYST-LR eq. (cells) Limnothrix redekei (Cyanobacteria)

The case of Planktothrix agardhii

$ eutrophication $ perennial bloom $ Highest P. agardhii biomass not correlated with highest MCYSTs concentrations $ High MCYSTs concentrations $ Contamination of the food web ? $ Public health threats

The case of Cylindrospermopsis raciborskii

C. raciborskii = filamentous

cyanobacteria with heterocyst & akinetes producing hepatotoxins (cylindrospermopsin) & neurotoxins (PSP) Important sanitary problems in Australia and south America

The case of Cylindrospermopsis raciborskii ! Present on all continents ! initially described as a typical tropical & sub-tropical species ! For the last 50 years, colonization of latitudes further north : - Central Asia in the 1950’s - Greece in the 40’s - Hungria in the 60’s - Volga in the 60’s - Austria in the 90’s - France - Germany

The case of Cylindrospermopsis raciborskii

Questions : ! What is the origin of invading strains in France ? ! Why this tropical strain occurs under temperate latitudes by now ? The 3 working hypotheses : ! Clone selection of C. raciborskii, adapted to temperate climate, while colonization of the species towards north ! High temperature tolerance of C. raciborskii for growth in very different conditions ! Global warming increases the probability of encountering good conditions for C. raciborskii growth

The case of Cylindrospermopsis raciborskii

RBRE2 RBRE1 CBRE1 CBRE2 CMEX CBRE3

16S ITS1 rpoC1 nifH

99

AF118 AF115

99

CAUS60 CAUS99 CAUS59

South and central America

0.01

99

CFRAN1 CFRAN2 AF117

Australia + Africa

CAL66

CFRAN3 CHON

Europe

The case of Cylindrospermopsis raciborskii

The case of Cylindrospermopsis raciborskii 0.5

0.9

0.4

0.8 0.7

0.3

µ (d-1)

µ (d-1)

0.6

0.2 0.1

0.5 0.4

0.0

0.3

-0.1

0.2 0.1

-0.2 10

15

20

25

30

35

Temperatures (°C)

40

45

0 0

50

100

150

200

250

300

350

400

450

Light Intensity (µEm-2s-1)

! No selection of C. raciborskii clones adapted to temperate climate ! Tolerance to a wide range of light and temperature with optima corresponding to typical tropical conditions (30°C). Global warming could favor the dispersion

500

Conclusions & “take home messages” Developments of freshwater toxic cyanobacteria have a negative impact on biodiversity, ecosystem functioning and potentially animal and human health. These proliferations can occur everywhere and health risks for terrestrial vertebrates are still largely ignored almost everywhere. Note also that the toxicity of many cyanobacteria is due to unknown toxins to date. SO: - More awareness & surveys are required with efficient monitoring tools ; - Take care about eutrophication but also of re-oligotrophisation processes (no real rule), species-dependent situations ; - Have in mind that global change (typically warmer winters and springs) is likely to favor these proliferations ; - We know almost nothing about toxin accumulation and transfer thru the food web : a very important research perspective.