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 2Alabama Department of Public Health, USA 3Dalhousie University, Canada 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 near- shore 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 Pyrodinium bahamense 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. Spatulodinium pseudonoctiluca Ceratium massiliense Gyrodinium simplex Phalacroma biceps P. triestinum Takayama pulchella Ceratium pentagonum Gyrodinium spp. Phalacroma rotundatum Protoperidinium claudicans Torodinium teredo Ceratium spp. Gyrodinium spirale Pheopolykrikos hartmannii Proto. conicum Unidentified Dinoflagellate Ceratium symmetricum Heterocapsa niei Pheopolykrikos spp. Proto. crassipes Karenia brevis 35,000 Monthly Average 30,000 25,000 20,000 15,000 10,000 5,000 Number of cellsNumber per liter 0 1 2 3 4 5 6 7 8 9 10 11 12

Monthly Alexandrium monilatum Average 4,000

3,000

2,000

1,000 Number of cellsNumber per liter 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 03

11 fall spring 04

10 summer 05 07 06

09 08

Strong seasonal cycle Bray- Curtis Similarity: Stress 0.05 (Primer E) Karenia brevis 25,000

Annual 20,000 Average 15,000

10,000

5,000 Number Number of cells per liter 0

10,000

Annual Alexandrium monilatum Average 8,000

6,000

4,000

2,000 Number Number of cells per liter

0 Average Dinoflagellate Composition per Year

Multi-dimensional Scaling Analysis (MDS) of Dinoflagellate Composition

2007 1999 P. micans (10%) 2005 K. brevis 2008 (37%)

K. brevis H. triquetra (35%) K. brevis (8%) (31%) 2004 2006 P. minimum (14%) 2001 A. monilatum 2003 (18%) P. micans 2000 P. scutellum (12%) (13%) 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 inter- annual variation (Primer E: BIOENV analysis)

Acquired Data: River Discharge (Daily Values)

AL

Perd USGS stations (red) in near- ido shore Alabama waters Bay Acquired Data: Climate Indices (Monthly Values)

 Multivariate El Niño/Southern Oscillation (ENSO)  North Atlantic Oscillation (NAO)  East Pacific/ North Pacific Pattern (EP/NP)  Pacific/ North American Pattern (PNA) NAO  Madden Julian Oscillation (MJO)  Tropical Northern Atlantic Index (TNA)

2.5 + - ENSO NAOENSO 1.5

0.5

-0.5 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 -1.5 Normalized anomalies Normalized anomalies

-2.5 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?

Average per year and month: (PRIMER E: BIOENV analysis) 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)

1500 ) ) -1 1200 s 3 900

600

300 Discharge (m Discharge 0 -1.2 -0.8 -0.4 0 0.4 0.8 1.2 ENSO (MEI) Big portion of inter-annual variation in dinoflagellate composition was explained by climate indices.

Ideally, we would have more data…

Grazing

Competition Viral lysis

Nutrients 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.