The rare marine protistDinophysis acuminata

How do the gametes mate?

P. Gentien, E. Nézan, P. Lazure, M. Lunven & H. Xie*

* LED, South China Sea Institute of Oceanology

This is not biomassIt is a species and it’s rare

The key to a species is « FITNESS »

Picture by E. Nézan

• It is the major toxic species in Atlantic Europe and is still largely a « mystery »

• Nutrition by phagotrophy (Yih et al., 2006)

• A Lot of pending questions :– How can we predict an event ?– What are the major control factors of

population dynamics of this RARE species?

Two valves Dinophysis

Two Scrippsiella cells

PHAGOTROPHY

All pictures by E. Nézan

Rarity• Rarity applies to two groups of species (K.J.Gaston,

terrestrial sp.)• Abundant at times but very localized• Ubiquitous but sparse everywhere

• D. acuminata is ubiquitous (LSU rDNA, (Guillou et al., 2002) but never dominates the assemblage despite a reasonable max. growth rate of 0.6 day-1 (Reguera et al., 2003) – specific nutritive source?

• Rare species face specific challenges summarized underthe term Allee effect. One of the main challenge issexual recombination (find a mate !)

DO THEY?

WHEN ?

Every species needs sexEvery species needs sex(included phytoplankters)

• While in a finite asexual population elimination of all individuals free of harmful mutations is irreversible (Muller’s ratchet, 1964), such individuals may reappear in a sexual population due to recombination.

• Multiplicative selection provides an exponential decrease of individual’s fitness with an increase of mutation number in the genome.

Do Do DinophysisDinophysis recombine ?recombine ?

Phases of sexual combination

Live samples from the Bay of Biscay

Collected over the last ten years

2 flagellae

(McLachlan, 1993).

PLANOZYGOTE

When When do do theythey needneedrecombinationrecombination ??

• After a certain number of asexual divisions FIXED• in all species, darwinian fitness decreases exponentially with replication• like in diatoms, there is an upper and a lower cell size• some divisions are depauperating, i.e. daughter cells are smaller• when cells reach the smaller size, they have to mate to regain the upper size.

Dinophysis size varies from 60 to 25 µm (Reguera, 2001)After an undefined number of divisions, mating is needed ( @ 1 year ?)

• When environmental conditions are unfavourable• in diatoms, silica deprivation induces gametogenesis VARIABLE• by analogy, plants produce flowers when stressed• this is likely to happen for protists when one of the resources of the niche has been

exhausted or is not supplied in sufficient quantity

OBSERVATIONS Month I II III IV V VI VII VIII IX X XI XIIObs. n.s. n.s. n.s. G.- P. G. G.- P. G. n.o. P. n.o. G. P.

Observations made on live samples from the Bay of Biscay

G. stands for Gamete fusion & Gamete attachment

P. For Planozygote

n.s. : not sampled & n.o. : sampled but not observed

There may not be a overwintering phase

They sexually recombine at any time

HOW CAN THIS HAPPEN ?HOW CAN THIS HAPPEN ?

Gametes need to get closeGametes need to get close enoughenough,,

when neededwhen needed

Concentrations presented are sampled in the standard way

Nearest N

C ( c/ml) NND (µm)0,1 27000

1 1200010 5700

100 26001000 1200

eighbour Distance<d>= 0.55 * C-1/3 (Rothschild, 1992)

with C : mean density of cells

Random walk model

CHARACTERISTIC MATING TIME

(if all cells became gametes and matingefficiency of 100% (Wyatt & Jenkinson, 1997))

At 102- 103 cells/ml the characteristic

time is of the order of months (rem.)

WHAT ABOUT CONCENTRATIONS LESS THAN l.d. ?

Ed Malkiel’s holographic movie(Johns Hopkins Univ.)

Dinophysis track

WHAT STRATEGIES TO DECREASE WHAT STRATEGIES TO DECREASE SEPARATION LENGTH ?SEPARATION LENGTH ?

• Clonal (asexual) reproduction to increase the encounter ratebalance between the mutation rate and the success of gamete encounter

• Concentration by active behaviourapplicable only to swimmers

Swarmers vs. Swimmers ??

Do they concentrate effectively ?

Density

0

5

10

15

20

25

30

35

40

45

25 25.5 26 26.5 27 27.5

Depth(m)

Dinophysis(cell.l-1)

2 50

6 10

11 8

15 20

21 4200

41 30

21 m -50

-40

-30

-20

-10

0

-200

300

800

1300

1800

2300

2800

3300

-50

-40

-30

-20

-10

0

24.4

24.8

25.2

25.6

26

26.4

26.8

27.2

14/07 16/07 18/07 20/07 22/07 24/07

DENSITY

DINOPHYSIS

12/07

DINOPHYSIS - Station 309 - 12 / 24 Juillet 1996

0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90

Fluorescence Leg TH072

-100

-80

-60

-40

-20

0

Dep

th (m

)

(km)Scan fish transect

These thin layers of phytoplankton are not rare

But they don’t necessarlycontain Dinophysis

AUV track under the fluorescence layer with a 1200 kHz ADCP looking upwards

BAY OF SEINE (English Channel)SouthWest winds

-1.2 -0.8 -0.4 0.049.2

49.4

49.6

49.8

23

25

27

29

31

33

35

-1.2 -0.8 -0.4 0.049.2

49.4

49.6

49.8

20

1000

5000

15000

30000

45000

SALINITY Maximum Cell Density (l-1)

Max. Observed (48000 c. l-1)Iso σ/ z

English Channel

SeineRiver

English Channel

Wind

LOIRE PLUME (Southern Brittany)SouthWest Winds

-4.5 -4.0 -3.5 -3.0 -2.5 -2.0

47.0

47.5

48.0

32.0

33.0

34.0

34.3

34.6

35.0

35.4

-4.5 -4.0 -3.5 -3.0 -2.5 -2.0

47.0

47.5

48.0

200

1000

1800

2600

Iso σ/ z

SALINITY Maximum Cell Density (l-1)Max. Observed (2800 c. l-1)

Atlantic OceanBay of BiscayWind

LOIRE PLUME (Southern Brittany)

-4.5 -4.0 -3.5 -3.0 -2.5 -2.0

47.0

47.5

48.0

32

33

34

34.3

34.6

35

35.4

250

750

2000

4000

-4.5 -4.0 -3.5 -3.0 -2.5 -2.0

47

47.5

48

Loire River

Atlantic Ocean

Bay of Biscay

North East Winds (following NorthWest winds)

Iso σ/ z

SALINITY Maximum Cell Density (l-1)

Max. Observed (4800 c. l-1)

(In a <40 cm layer)

Wind

12.07 Surface

19.07 Surface

19.07

Mid-depth

12.07

Mid-depth

WindWind

Dinophysis patch

Residual Currents

@ tidal period

Eddy induced by wind regimechanges

Geometrictrapping of the eddy ?

• One could hypothetize improved mate location by pheromones However, it would be too costlyfor organisms smaller than 250 µm unless a 2D-diffusion (Dusenbury & Snell, 1995).

• Patchy distributions are associated with highshear areas (pycnocline) which effectively limitthe diffusion to 2D- diffusion.

• Furthermore, the diffusion of the population islimited by small scale eddies at the appropriatescale ( 10 days, 10 n.m.) which act as incubators

• The link with river plumes needs furtherinvestigations. The plume creates :

» stratification» quasi-inertial eddies at the interface» chemical attractants ?

Dinophysis• Confined in the vertical

– Biological drivers unknown(tropism ? , specific nutrition ? , both ? )

- Relative contribution of growth vs. Aggregation ?

• Present in temporary retentive structures– Small scale eddies (10 – 15 n.m.)– Limitation of the population dispersal

There is a need for predictive tools

What can be done with such a limited knowledge ?

Mainly Dinophysis acuminata

Most of the problems can be solved by appropriate mitigation :- early harvest and preservation of live animals with preservation of organoleptic quality

- depuration of low levels of toxins.

METHODS

A mix of numerical method and fuzzy logic

3D finite difference free surface modelSigma coordinates (30 layers)The horizontal grid resolution is 5km×5km (1.7x1.7). Boundary condition supplied by 2D Atlantic ocean modelForcing : Tides, Meteorological Forecast, Rivers outflow

Dinophysis data (coastal network)

Time window for appearance of Dinophysis eventsSystems’ Rules

800 km

In press J. Mar. Sys (next issue)

Some results

The residual current vector at surface and 12m depth on May, 11th 1998

BV

BV

12.0 mThese eddies are typically confined in the pycnocline.

They have been observedin different areas including the Baltic Sea

Their mechanisms of formation are not clearlyunderstood yet.

The existence of theseeddies has been validated

But their location isvariable

The residual current vector (tidally filtered) at surface and 12m depth on May, 11th 1998

BV

BV

April, 4th

BV

BV

March, 28th

A TYPICAL SEQUENCE

The beginning of the Dinophysis season is the date at which that the concentration of Dinophysis is larger than 100 cell.l-1 for a minimum duration of two weeks in at least half of the stations in one bay.

100

5100

10100

15100

20100

25100

0 4 8 12 16 20 24 28 32 36 40 44 48 52

week number

conc

entra

tion(

cell/

L)

The weekly distribution of Dinophysis for 14 years from 1989 to 2003 in Baie de Vilaine

as measured by the French monitoring network (REPHY)

Dinophysis time window

1- The central temperature of eddy should exceed 11 °C.

The relation between temperature and growth rate is not known but the 11 °C limit is drawnfrom temperature time series and corresponds roughly to the opening of the Dinophysis time window.

2- The eddy must last more than 24 h.

If an eddy is stable only for few hours, it would probably have no population build-up by tropism (diurnal scale) or by sheer growth.

3- The eddy must then, be advected to the bay of interest.

Based on the examination of few years, three rules were fixed :

PREDICTION OF THE BEGINNING OF THE SEASON

Year Seas. beginning

Eddy onset

Eddy position Lag time

Predictive type

1989 126 92 2.69W,47.27N 34 False pos.

110 2.69W,47.27N 16 Positive

1990 97 83 2.69W,47.22N 14 Positive

1991 124 119 2.69W,47.22N 5 Positive

1992 123 98 2.69W,47.22N 25 Positive

1993 156 121 2.69W,47.22N 35 False pos.

145-155 2.69W,47.27N 1 Positive

1994 134 121-127 2.69W,47.27N 7 Positive

1995 154 125-128 2.69W,47.27N 26 False pos.

141-150 2.69W,47.22N 4 Positive

1996 97 89-92 2.75W,47.22N 5 Positive

1997 102 94 2.81W,47.17N 8 Positive

1998 136 100 2.69W,47.22N 36 False pos.

115-121 2.69W,47.22N 15 False pos.

130-134 2.69W,47.27N 2 Positive

1999 69 61-67 2.69W,47.27N 2 Positive

2000 85 67-73 2.69W,47.27N 12 Positive

• There is no false negative :

i.e. all the events are preceded by the establishment of an eddy

• The position of the eddy isremarkably stable

topographically trapped ?

Position for a monitoring buoy

• All the false positive cases are followed by a true positive case

Improvement in the advection criteria needed

CONCLUSIONS• Planozygotes observed all the year round

No need to invoke cyst beds

• Efficient gathering strategy (Unknown tropism factors)

• Prediction of the season’s beginning is feasible(downscaling of the 3D-model)

• Dispersal and advection of incubating structures are the key mechanisms (better understanding of physics)

• Link with river plumes and wind regimes• Biological control (growth – grazing ??)