Biogeochemical and Physical Controls of

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Biogeochemical and Physical Controls of Estuarine
Phytoplankton Community Structure
James L. Pinckney Estuarine Ecology Lab Marine
Science Program and Department of Biological
Sciences University of South Carolina Columbia, SC
Presented at a Seminar in the Department of
Marine Sciences, University of Georgia, Athens,
GA, 06 March 2006
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This work would not have been possible without
the assistance of Dr. Erla Örnólfsdóttir Beth
Lumsden Alyce Lee Alicia Salazar Daniel
Marshalonis Elizabeth Mitchell And Funding
from EPA, NSF, Sea Grant, and Texas Institute
of Oceanography
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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What regulates phytoplankton biomass and
community composition in estuarine and coastal
ecosystems?

• The answer to this question is essential for
  assessing the effects of
• eutrophication and anthropogenic modifications on
  ecosystem structure, function, and health
• Research on this topic will supply process-based
  insights into
• planktonic and benthic trophodynamics and
  biogeochemical cycling

Neuse River Estuary, North Carolina 1993
1998 UNC Institute of Marine Sciences, Morehead
City, NC Galveston Bay, Texas 1998 2004 Texas
AM University, College Station, TX
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Galveston Bay is the second largest estuary in
the Gulf of Mexico with an open-water area of
1,550 km2 (600 mi2)
Galveston Bay, Texas
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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• Galveston Bay
• Large, urbanized estuary
• One of the busiest
• seaports in the US
• Shallow, well-mixed
• Mostly diurnal tides
• Narrow tidal range (40 cm)
• Nutrient inputs from
• many point (pipes) and
• non-point (ag runoff) sources

Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Surface Area 1,554 km2 Mean Depth 2.4 m Houston
Ship Channel 14 m deep 600 m wide Sediments mud,
sandy mud, oyster reefs
Houston Ship Channel
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Comparison of Galveston Bay with 74 Other
Estuaries In the continental US Data Source
NOAAs Estuarine Eutrophication Survey (Bricker
et al. 1997)
Charleston Harbor
Winyah Bay
Average Depth (m)
Estuary Surface Area (km2)
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Sampling Stations in Galveston Bay
Instituted in May 1998
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Salinity and River Discharge
Tropical Storm Allison 1 m rain over 5 days
Trinity River Discharge (x 106 m3 d-1)
Salinity (psu)
Distance (km)
1999
2000
2001
2002
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Total Dissolved Inorganic Nitrogen
Concentrations (nitrate nitrite ammonium)
Trinity River Discharge (x 106 m3 d-1)
Distance (km)
Total N (µmol l-1)
1999
2000
2001
2002
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Dissolved Inorganic Phosphorus Concentrations
Trinity River Discharge (x 106 m3 d-1)
Distance (km)
Total P (µmol l-1)
1999
2000
2001
2002
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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NP Ratios for Galveston Bay (1999-2002)
Phosphate (µmol P L-1)
N Limited
P Limited
DIN (µmol N L-1)
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Phytoplankton Biomass (Chlorophyll a)
Distance (km)
Total N (µmol l-1)
Trinity River Discharge (x 106 m3 d-1)
Distance (km)
Chl a (µg l-1)
1999
2000
2001
2002
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Early Phytoplankton Research
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Some Chemotaxonomic Phytoplankton Photosynthetic
Pigments
Chlorophyll a Chlorophyll b Alloxanthin Fucoxanth
in Peridinin Zeaxanthin
All Phytoplankton Chlorophytes Cryptophytes Diato
ms Dinoflagellates Cyanobacteria
Chlorophyll a molecule
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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25 diagnostic photopigments can be used to
quantify the relative abundances of 18 different
algal groups
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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ChemTax CHEMical TAXonomy

• A matrix factorization algorithm (macro runs in
  Matlab)
• Convert chemotaxonomic pigment concentrations
  into
• measures of relative abundance of different algal
  groups
• Abundance expressed in common units of µg Chl a
  liter-1

Total Chlorophyll a
Cyanos
Cryptos
diatoms

• Artificial Neural Network approach with Jim
  Morris at USC

Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Chl a (µg l-1)
Spatio-temporal Abundance of Phytoplankton
Groups in Galveston Bay
Chl a (µg l-1)
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Phytoplankton Community Dynamics in Galveston Bay
Cyano
Crypto
Chloro
K. brevis
Dino
Diato
Relative biomass in units of Chl a ?g L-1
Distance from mouth of Galveston Bay (km)
1999
2000
2001
From Örnólfsdóttir et al. 2004a
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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In situ bioassay incubation corral
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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13 Bioassays over an annual cycle showed no
evidence of P-limitation
Phytoplankton in Galveston Bay are primarily
nitrogen-limited
From Örnólfsdóttir et al. 2004b
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Red Tides in the Gulf of Mexico
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Texas Red Tide Karenia brevis, Gymnodinium
breve, Ptychodiscus breve
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Bay Water
Frontal Zone
Karenia brevis Bloom
Karenia brevis Bloom Water Sample
Red Tide Bloom in Galveston Bay 18 September 2000
Bay Water
Karenia brevis Bloom
Estimated Economic Impact 18 million
Frontal Zone
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Gyroxanthin is a diagnostic photopigment for
Karenia sp.
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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HPLC Photopigment Chromatograms
305 cells/ml
453 cells/ml
31,000 cells/ml
1,375 cells/ml
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Comparison of Gyroxanthin Concentrations in
Karenia brevis Blooms in Florida and Texas
Gyroxanthin (?g/liter)
Abundance (cells/ml)
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Texas Red Tide

• Gyroxanthin is a reliable biomarker pigment for
  Karenia brevis
• HPLC methods allow for rapid assessments of K.
  brevis abundance at low concentrations (lt 5 cells
  ml-1)
• K. brevis in Texas waters seems to have a higher
  concentration of gyroxanthin per cell than
  Florida blooms (why?)
• The red tide bloom in Galveston Bay was likely
  due to advection of coastal water containing high
  concentrations of K. brevis into the bay

Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Galveston Bay Pink Oysters
A major negative impact on the oyster industry

• Historical Observations
• Usually occur in the fall (October January)
• Number of pink oysters varies from year to year
• Seem abundant in the region between Smith Point
  and Eagle Point
• Seem to follow large rainfall events
• Have been a problem for at least 14 years
• Usually not a problem after January
• Color more intense after freezing and thawing
• 1999 Few to no pink oysters
• 2000 Lots of pink oysters (December to January)
• 2001 Pink oysters common in some areas
  (November to December)

Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Cryptophytes Cryptomonads

• Photosynthetic nanoplanktonic (6 - 20 µm)
  flagellates
• Common in marine, estuarine, and freshwater
  habitats
• Have unique biomarker photopigments
• Alloxanthin and Monadoxanthin
• Phycobilins (red/pink color, water soluble)

Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Cryptophytes and Pink Oysters Phycoerythrin Colors
Oyster Liquor
Cryptophyte cultures
Cells on Filters
Pink Oyster
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Cryptophyte Biomass
1999
2000
2001
2002
Cryptophytes also bloom when N concentrations are
high
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Calculations
Oyster filtration rate 5 ml water/minute 300
ml per hour 7.2 liters per day Cryptophyte
Biomass 5 µg Chl a liter-1 Daily Oyster
Consumption of Cryptophytes 5 7.2 36 µg Chl
a per day
In 1 day, an oyster in Galveston Bay would
consume this amount of cryptophyte biomass
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
35
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Pink Oysters in Galveston Bay

• The occurrence of pink oysters is correlated with
  cryptophyte abundance
• Phycoerythrin is responsible for the red
  coloration
• Cryptophyte blooms occur in the fall
• The intensity of blooms is controlled by nutrient
  inputs
• Some evidence that cryptophyte blooms are
  terminated by dinoflagellate grazing

Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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How can we use phytoplankton photopigment data as
an indicator of estuarine structure, function,
and ecosystem health?
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
38
Phytoplankton Community Dynamics in Galveston Bay
Cyano
Crypto
Chloro
K. brevis
Dino
Diato
Relative biomass in units of Chl a ?g L-1
Distance from mouth of Galveston Bay (km)
1999
2000
2001
From Örnólfsdóttir et al. 2004
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Species vs. Functional Groups
The functional group component of diversity is a
greater determinant of ecosystem processes than
the species component of diversity (Tilman et
al. 1997, Science 2771300-1302) Other studies
suggesting that the functional characteristics of
species are more important than the number of
species for ecosystem processes.. Bolam et al.
2002 (Ecol. Monogr. 72599-615) Emmerson
Rafaelli 2000 (Oikos 91191-203) Grime 1997
(Science 2771260-1261) Hector et al. 1999
(Science 2861123-1127) Hooper Vitousek 1997
(Science 2771302-1305) Symstad et al. 1998
(Oikos 81389-397) Wardle 1999 (Oikos
87403-407)
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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• Assume that an increase in functional diversity
  promotes ecosystem stability, homeostasis, and
  resilience to perturbations
• Change in group diversity over time may indicate
  ecosystem health

More Stable
Group Diversity
Less Stable
Time
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Phytoplankton functional group diversity measures
over time may be a useful metric for comparing
the ecosystem states for different estuaries
Estuary A
Group Diversity
Estuary B
Estuary C
Time
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Non-Parametric Measures of Diversity
Provide a quantitative measure based on the
number of individuals and the number of different
species

• Shannon-Wiener Function
• H ranges from 0 (low diversity) to 5 (high
  diversity)

Confidence Limits can be calculated using
bootstrapping techniques
The Shannon-Wiener index is most sensitive to
changes in the abundances of rare species in the
community sample

• Group Diversity can be easily calculated using
  ChemTax-derived
• phytoplankton group abundances expressed in units
  of Chl a

Thus, Functional Group Diversity is an
integrative measure of both the abundances of
individuals within a group as well as the number
of groups in the sample
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Phytoplankton Functional Group Diversity and
Biomass in Galveston Bay (March 1999 to February
2002) Calculated using the Shannon-Wiener Function
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Back to the Neuse River Estuary
The slope of the regression line is significantly
different from 0 (p 0.011) Is Phytoplankton
Functional Group Diversity slowly increasing in
the Neuse?
Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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The Phytoplankton Functional Group Diversity Index

• Average values of FGD are similar for both
  estuaries
• FGD in both estuaries exhibits cyclic
  oscillations
• FGD appears more variable in the Neuse River
  than Galveston Bay
• May be related to hydrodynamics or biogeochemical
  cycling in a river-dominated estuary vs. a
  shallow coastal plain estuary
• FGD is not simply a function of total
  phytoplankton biomass
• FGD can be used to compare phytoplankton
  community dynamics in different estuarine
  ecosystems
• May be a useful metric for determining the major
  factors that regulate phytoplankton biomass and
  community composition in estuarine and coastal
  ecosystems

Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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Summary

• Phytoplankton in Galveston Bay are
  nitrogen-limited
• The primary source of N for blooms is from
  riverine inputs
• Phytoplankton community composition is dynamic
  on weekly scales
• Shifts in community structure can produce
  nuisance algal blooms
• Phytoplankton functional group diversity indices
  provide a useful metric for quantifying
  ecosystem-scale community dynamics
• FGD also allows for a non-parametric
  cross-system comparison of important ecosystem
  properties
• FGD is a useful tool for generating testable
  hypotheses concerning ecosystem responses to
  perturbations and assessing ecosystem health

Estuarine Ecology Lab
University of South Carolina
Marine Science Program
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http//biol.sc.edu/jpinckney jpinckney_at_biol.sc.ed
u
Estuarine Ecology Lab
University of South Carolina
Marine Science Program