Seasonal and Inter-annual Changes in
Dinoflagellates Community Composition
in Near-shore Alabama Waters
Lucie Novoveská1, William L. Smith2, Carol P. Dorsey2
and Hugh L. MacIntyre3
1Dauphin
Island Sea Lab and University of South Alabama, USA
Department of Public Health, USA
3Dalhousie University, Canada
2Alabama
Why Dinoflagellates?
 Dinoflagellates are causing Harmful Algal Blooms (HABs)
 HABs may impact the entire ecosystem (toxin production, oxygen depletion, etc.)
 75-80% of toxic phytoplankton species are dinoflagellates (Cembella 2003)
~2000 living dinoflagellate species, 1700 are marine (Taylor et al. 2008)
Prorocentrum minimum bloomed in winter and spring in 2003, 2005,
2007, 2009 and 2011 in coastal Alabama.
Picture courtesy of ADPH
Karlodinium veneficum bloomed in summer 2007.
Fish tested positive for karlotoxin (KmTx2) (Dr. Place University of
Maryland, Center for Environmental Science).
Goal
Our goal is to describe the temporal variability in
dinoflagellate community composition in nearshore Alabama waters and to relate it to
environmental changes.
Sample Collection
Alabama Department of Public Health collected samples at 4 sites
bi-weekly over a 10-year period (1999-2008).
For each sample, dinoflagellate composition was described and
temperature and salinity were measured at the time of collection.
Data hurdles...
Missing data
Changes in names: synonyms Gonyaulax monilata to Alexandrium monilatum
Changes in counting personnel: Karenia spp. to Karenia mikimotoi
High degree of merging:
Prorocentrum minimum var. triangulatum
Prorocentrum minimum var. minimum
Prorocentrum minimum var. mariae-lebouiae
From Jacob Larsen
114 taxonomic groups in 37 genera (22 ecosystem disruptive species)
Akashiwo sanguinea
Ceratium trichoceros
Heterocapsa rotundata
Podolampas spp
Proto. depressum
Alexandrium monilatum
Ceratium tripos
Heterocapsa spp.
Podolampas palmipes
Proto. divergens
Alexandrium spp.
Cochlodinium spp.
Heterocapsa triquetra
Polykrikos kofoidii
Proto. grande
Amphidiniopsis kofoidii
Dinophysis acuminata
Karenia brevis
Polykrikos schwartzii
Proto. leonis
Amphidiniopsis spp
Dinophysis acuta
Karenia mikimotoi
Polykrikos spp.
Proto. oblongum
Amphidinium carterae
Dinophysis caudata
Karenia papilionaceae
Pronoctiluca acuta
Proto. pallidum
Amphidinium klebsii
Dinophysis spp.
Karenia spp.
Pronoctiluca pelagica
Proto. pellucidum
Amphidinium spp.
Diplopsalis lenticula
Karlodinium venficum
Prorocentrum compressum Proto. pentagonum
Balechina coerulea
Diplopsalis spp.
Katodinium glaucum
P. concavum
Proto. punctulatum
Brachidinium capitatum
Goniodoma polyedricum Katodinium spp.
P. conicum
Proto. quinquecorne
Ceratium carriense
Gonyaulax diegensis
Krypto. foliaceum
P. emarginatum
Protoperidinium spp.
Ceratium furca
Gonyaulax digitale
Kryptoperidinium spp.
P. gracile
Proto. steidingerae
Ceratium fusus
Gonyaulax minima
Lingulodinium polyedrum P. lima
Ceratium hircus
Gonyaulax polygramma Lingulodinium spp.
P. mexicanum
Pyrophacus horologium
Ceratium horridum
Gonyaulax spp.
Noctiluca scintillans
P. micans
Pyrophacus spp.
Ceratium incisum
Gonyaulax spinifera
Oxyphysis oxytoxoides
P. minimum
Pyrophacus steinii
Ceratium kofoidii
Gymnodinium spp.
Oxyphysis spp.
P. rostratum
Scripsiella spp.
Ceratium lineatum
Gymn. splendens
Oxytoxum scolopax
P. scutellum
Scripsiella trochoidea
Ceratium macroceros
Gyrodinium estuariale
Paleophalacroma spp.
Prorocentrum spp.
Ceratium massiliense
Gyrodinium simplex
Phalacroma biceps
P. triestinum
Spatulodinium
pseudonoctiluca
Ceratium pentagonum
Gyrodinium spp.
Phalacroma rotundatum
Protoperidinium claudicans
Ceratium spp.
Gyrodinium spirale
Pheopolykrikos hartmannii Proto. conicum
Ceratium symmetricum
Heterocapsa niei
Pheopolykrikos spp.
Proto. crassipes
Pyrodinium bahamense
Takayama pulchella
Torodinium teredo
Unidentified Dinoflagellate
Karenia brevis
35,000
Number of cells per liter
Monthly
Average
30,000
25,000
20,000
15,000
10,000
5,000
0
1
2
3
4
5
6
7
8
9
10 11 12
Alexandrium monilatum
Monthly
Average
Number of cells per liter
4,000
3,000
2,000
1,000
0
1
2
3
4
5
6
7
8
9
10 11 12
Average Dinoflagellate Composition per Month
Multi-dimensional Scaling Analysis (MDS) of Dinoflagellate Composition
02
01
winter
12
fall
11
03
spring
04
10
summer
05
07
09
08
Strong seasonal cycle
Bray- Curtis Similarity: Stress 0.05 (Primer E)
06
Annual
Average
Number of cells per liter
25,000
Karenia brevis
20,000
15,000
10,000
5,000
0
10,000
Alexandrium monilatum
Number of cells per liter
Annual
Average
8,000
6,000
4,000
2,000
0
Average Dinoflagellate Composition per Year
Multi-dimensional Scaling Analysis (MDS) of Dinoflagellate Composition
P. micans
(10%)
1999
2007
2005
2008
K. brevis
(37%)
K. brevis
(35%)
K. brevis
(31%)
H. triquetra
(8%)
2004
2001
2000
A. monilatum
(18%)
2003
P. scutellum
(13%)
2006
P. minimum
(14%)
P. micans
(12%)
2002
Shifts between the years
Bray- Curtis Similarity: Stress 0.09 (Primer E)
Primer E: SIMPER analysis
Dinoflagellate Community Composition vs. Environmental Data
Temperature and Salinity combined explained 32% of monthly variation among
dinoflagellate community (p=0.01) but it did not significantly explain interannual variation (Primer E: BIOENV analysis)
Acquired Data: River Discharge (Daily Values)
AL
Perd
ido
Bay
USGS stations (red) in nearshore Alabama waters
Acquired Data: Climate Indices (Monthly Values)
 Multivariate El Niño/Southern Oscillation (ENSO)
 North Atlantic Oscillation (NAO)
 East Pacific/ North Pacific Pattern (EP/NP)
NAO
 Pacific/ North American Pattern (PNA)
 Madden Julian Oscillation (MJO)
2.5
ENSO
+
ENSO
NAO
-
1.5
-1.5
-1.5
-2.5
-2.5
2008
2008
2007
2007
2006
2006
2005
2005
2004
2004
2003
2003
2002
2002
2001
2001
-0.5
-0.5
2000
2000
0.5
1999
1999
Normalized
Normalizedanomalies
anomalies
 Tropical Northern Atlantic Index (TNA)
Phytoplankton and Climate Indices
ENSO:
Moore, S.K. et al., 2010. The relative influences of El Nino Southern Oscillation
and Pacific Decadal Oscillation on paralytic shellfish toxin accumulation in Pacific
Northwest shellfish. L&O 55(6): 2262-2274.
Ochoa, J.L., 2003. ENSO phenomenon and toxic red tides in Mexico.
Geofisica Internacional, 42(3): 505-515.
NAO:
Edwards, M. et al., 2006. Regional climate change and harmful algal blooms in
the northeast Atlantic. L&O 51(2): 820-829.
Belgrano, A et al., 1999. North Atlantic Oscillation primary productivity and toxic
phytoplankton in the Gullmar Fjord, Sweden (1985-1996). Proc. R. Soc. 266(1418):
425-430.
MJO:
Isoguchi, O. and Kawamura, H., 2006. MJO-related summer cooling and
phytoplankton blooms in the South China Sea in recent years. Geo. Res. L. 33(16).
Which environmental variables are driving the dinoflagellate
composition?
Environmental variables:
Climate indices daily values were interpolated from monthly values.
Discharge, temperature and 6 climate indices data were averaged per 2-week
interval: 2 weeks prior collections, 2-4 weeks prior collection and 4-6 weeks prior
collections.
Dinoflagellate composition:
Biweekly data for 4 sites
more than 80% similar
average across the sites
Which environmental variables are driving the dinoflagellate
composition?
(PRIMER E: BIOENV analysis)
Average per year and month:
ENSO (Rho = 0.20, p = 0.01, n = 120)
Average per year:
ENSO, NAO, PNA (Rho = 0.66, p = 0.01, n = 10), ENSO alone (Rho = 0.41)
Discharge (m3 s-1)
1500
1200
900
600
300
0
-1.2 -0.8 -0.4
0
0.4
ENSO (MEI)
0.8
1.2
Big portion of inter-annual variation in dinoflagellate
composition was explained by climate indices.
Ideally, we would have more data…
Grazing
Competition
Nutrients
Viral lysis
Dinos
Light
Conclusions
 Analysis of water samples collected from AL coastal waters
over 10 years showed strong seasonal cycle. Significant portion
of monthly variation in dinoflagellate composition was
explained by temperature and salinity.
 There was a relationship between inter-annual dinoflagellate
composition variability and El Nino Southern Oscillation.
Acknowledgement
We thank personnel at the Baldwin County Health
Department and Alabama Department of Environmental
Management (ADEM), particularly Camilla English and
Suzie Farr, for sample collection.
We also thank Lei Hu for help with database work.
Average Dinoflagellate Composition per Site
Beach
Samples
There is a difference in dinoflagellate composition going from
East to West.
Average Density of Dinoflagellates per Year
Pattern is driven by Prorocentrum minimum bloom in 2003, 2004, 2005 and 2007.