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TRANSCRIPT
Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
Christine Elizabeth Hanson B. Sc. (Hons.)
This thesis is presented for the degree of Doctor of Philosophy
of The University of Western Australia
School of Water Research October 2004
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Summary
This work was the first large-scale biological oceanographic study to be undertaken in
the coastal eastern Indian Ocean adjacent to Western Australia, and covered both
northwest (Exmouth Peninsula to the Abrolhos Islands) and southwest (Cape
Naturaliste to Cape Leeuwin) regions. The study area was dominated by the Leeuwin
Current (LC), an anomalous eastern boundary current that transports tropical water
poleward and prevents deep nutrients from reaching the surface by creating large-scale
downwelling. Indeed, LC and offshore waters were consistently associated with low
nitrate concentrations and low phytoplankton biomass and production
(< 200 mg C m-2 d-1). However, the physical forcing of the LC was offset, during the
summer months, by upwelling associated with wind-driven inshore countercurrents
(Ningaloo and Capes Currents), which provided a mechanism to access high nutrient
concentrations normally confined to the base of the LC. Production rates in these
countercurrents were significantly higher than expected (~ 700 – 1300 mg C m-2 d-1)
along this otherwise oligotrophic coast. Furthermore, phytoplankton biomass within the
Leeuwin Current was largely confined to the base of the LC’s mixed layer, forming a
deep chlorophyll maximum (DCM). Between 10 and 40 % of total water column
production was attributable to the DCM. Coupling between nutrients at depth and the
DCM indicate that the balance between light and nutrient availability is critical in
controlling primary productivity in the LC. Variation in the depth (and therefore
production) of the DCM was also related to changing oceanographic conditions along
the length of the study area, including variation in the strength of the LC and the
presence of offshore eddies. Phytoplankton community composition was quite distinct
between LC/offshore and shelf/countercurrent regions. Smaller sized phytoplankton
(including cyanobacteria and prochlorophytes) dominated the Leeuwin Current waters,
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and were primarily dependent on regenerated forms of nitrogen at both the surface and
DCM. In upwelling regions, larger phytoplankton (including diatoms) were more
abundant, although production was still heavily reliant on regenerated forms of
nutrients. Thus, both in the DCM and upwelling countercurrents, nitrogen recycling via
heterotrophy appears to play a critical role in sustaining primary productivity. Limited
seasonal investigations off the Capes region of southwestern Australia showed that the
winter production scenario can be very different than summer conditions, with strong
Leeuwin Current flow that meanders onto the continental shelf and entrains seasonally
nutrient-enriched shelf waters. However, production in the LC was still low ( 450
mg C m-2 d-1) due to light limitation resulting from both increased light attenuation and
reduced surface irradiance characteristic of the winter months. This investigation
provides fundamental knowledge on physical-biological coupling off Western Australia,
with implications for fisheries management in view of seasonal and inter-annual
variability in the strength of both the Leeuwin Current and inshore countercurrents.
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To my parents
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Table of Contents
Statement of content and candidate contribution .................................................... ix Acknowledgments ...................................................................................................... x
CHAPTER 1 INTRODUCTION
1.1 Motivation ......................................................................................................... 1 1.2 Structure of the Thesis ...................................................................................... 3
CHAPTER 2 LITERATURE REVIEW
2.1 Marine Pelagic Ecosystem Dynamics ............................................................... 5 2.2 Primary Production in Subtropical Oceanic Waters ......................................... 9
2.2.1 Importance of picoautotrophs ................................................................. 12 2.2.2 Deep chlorophyll maxima and the carbon:chlorophyll a ratio ................ 13 2.2.3 Role of micronutrients in phytoplankton dynamics ................................ 15
2.3 Coastal Upwelling and Primary Production.................................................... 17 2.4 Oceanography of the Coastal Eastern Indian Ocean ....................................... 18
2.4.1 Physical features ..................................................................................... 18 2.4.2 Nutrient dynamics ................................................................................... 23 2.4.3 Pelagic ecology ....................................................................................... 27
2.5 Summary of Previous Investigations .............................................................. 32 2.5.1 Phytoplankton biomass ........................................................................... 32 2.5.2 Primary production ................................................................................. 33
2.6 Concluding Remarks ....................................................................................... 35 3.1 Summary ......................................................................................................... 37
CHAPTER 3 SPORADIC UPWELLING ON A DOWNWELLING COAST: PHYTOPLANKTON RESPONSES TO
SPATIALLY VARIABLE NUTRIENT DYNAMICS OFF THE GASCOYNE REGION OF WESTERN
AUSTRALIA
3.2 Introduction ..................................................................................................... 38 3.3 Materials and Methods .................................................................................... 41
3.3.1 Oceanographic sampling and laboratory analyses .................................. 42 3.3.2 Data processing and production calculations .......................................... 44
3.4 Results ............................................................................................................. 47 3.4.1 Physical water types ................................................................................ 47 3.4.2 Phytoplankton biomass and nutrients ..................................................... 50 3.4.3 Production stations .................................................................................. 57
3.5 Discussion ....................................................................................................... 69 3.5.1 Biomass and production rates in context ................................................ 69 3.5.2 Regional patterns in coupled physical-biological processes ................... 71 3.5.3 Implications of biomass and productivity patterns for community ecology 74
3.6 Concluding Remarks ....................................................................................... 75
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CHAPTER 4 DEEP CHLOROPHYLL MAXIMUM DYNAMICS IN LEEUWIN CURRENT AND OFFSHORE
WATERS OF WESTERN AUSTRALIA
4.1 Summary ......................................................................................................... 77 4.2 Introduction ..................................................................................................... 77 4.3 Materials and Methods .................................................................................... 80
4.3.1 Study region ............................................................................................ 80 4.3.2 Field sampling, experimentation and laboratory analyses ...................... 80 4.3.3 Data analysis and sensitivity estimates (Kd, *) ..................................... 83
4.4 Results ............................................................................................................. 85 4.4.1 Phytoplankton biomass ........................................................................... 85 4.4.2 Phytoplankton production ....................................................................... 88 4.4.3 Effects of * and Kd estimates on production calculations ..................... 95 4.4.4 Physical and chemical influences on the DCM ....................................... 97
4.5 Discussion ..................................................................................................... 104 4.5.1 Photosynthetic characteristics and significance of deep chlorophyll
maxima .................................................................................................. 104 4.5.2 Controls on vertical distribution of phytoplankton biomass and
productivity ........................................................................................... 108 4.5.3 Deep chlorophyll maxima and the Leeuwin Current ............................ 110
4.6 Concluding Remarks ..................................................................................... 113 CHAPTER 5 PHYTOPLANKTON COMMUNITY STRUCTURE AND NITROGEN NUTRITION IN THE COASTAL
EASTERN INDIAN OCEAN
5.1 Summary ....................................................................................................... 115 5.2 Introduction ................................................................................................... 115 5.3 Materials and Methods .................................................................................. 117
5.3.1 Sample collection, processing and calculations .................................... 119 5.3.1.1 15N uptake ......................................................................................... 120 5.3.1.2 Taxonomic analyses – chemical........................................................ 122 5.3.1.3 Taxonomic analyses – microscopic .................................................. 124
5.4 Results ........................................................................................................... 124 5.4.1 Nitrogen uptake ..................................................................................... 124 5.4.2 Species composition and abundance ..................................................... 131 5.4.3 Nitrate uptake as a function of species composition ............................. 142 5.4.4 Stable isotope signatures ....................................................................... 145
5.5 Discussion ..................................................................................................... 148 5.5.1 Nitrogen nutrition .................................................................................. 148 5.5.2 Phytoplankton community composition ............................................... 153 5.5.3 Ecological interpretations from stable isotopes .................................... 155
5.6 Concluding Remarks ..................................................................................... 156
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CHAPTER 6 SEASONAL PRODUCTION REGIMES OFF SOUTHWESTERN AUSTRALIA: INFLUENCE OF THE
CAPES AND LEEUWIN CURRENTS ON PHYTOPLANKTON DYNAMICS
6.1 Summary ....................................................................................................... 157 6.2 Introduction ................................................................................................... 158 6.3 Materials and Methods .................................................................................. 160
6.3.1 Hamelin Bay transect ............................................................................ 160 6.3.2 Cape Naturaliste transect ...................................................................... 164
6.4 Results ........................................................................................................... 165 6.4.1 Sea surface temperature (SST) and meteorological conditions ............ 165 6.4.2 Vertical structure: temperature, salinity, nutrients and phytoplankton
biomass ................................................................................................. 171 6.4.3 Photosynthetic parameters and depth-integrated primary production .. 177 6.4.4 Phytoplankton species composition ...................................................... 182 6.4.5 Stable isotopic ratios of particulate matter ............................................ 185
6.5 Discussion ..................................................................................................... 187 6.5.1 Summer upwelling and shelf break dynamics: biological significance 188 6.5.2 Winter nutrient and productivity dynamics .......................................... 191
6.6 Concluding Remarks ..................................................................................... 192 CHAPTER 7 GENERAL DISCUSSION, CONCLUSIONS AND FUTURE WORK
7.1 Discussion and Conclusions ......................................................................... 195 7.2 Recommendations for Future Work .............................................................. 200
REFERENCES ................................................................................................................. 203
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Statement of Content and Candidate Contribution
I hereby declare that all material presented in this thesis is original except where due
acknowledgment is given, and has not been accepted for the award of any other degree
or diploma. The body of this thesis (Chapters 3 to 6) is presented as a series of self-
contained papers intended for journal publication, and some repetition of the literature
review, study site details and methodology has therefore been necessary. Chapter 3 has
been accepted for publication under the joint authorship of Professor Charitha
Pattiaratchi and Dr Anya Waite, which reflects their review and discussions of a
supervisory nature. Chapters 4 to 6 will also have joint authorship when submitted for
publication, including Dr Stéphane Pesant (Chapter 4) and Dr Peter Thompson (Chapter
5), to acknowledge the reviews and discussions with my supervisors and colleagues that
are part of the research process. As the author of all material within this thesis, I am
completely responsible for all data analyses, figures and written text contained herein.
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Acknowledgments
Sincere thanks to my supervisors, Professor Chari Pattiaratchi and Dr Anya Waite, for
their guidance over the duration of this project, and for their assistance with all aspects
of my work. This PhD has been an incredibly valuable learning experience, and I
appreciate all the opportunities that they provided me with.
I also thank Dr Stéphane Pesant for help in the field and laboratory, with data
analyses and interpretations, for his excellent editorial assistance, and for being such a
good colleague and friend.
For the RV Franklin study, I thank the Captain, crew and scientific support staff
for the successful execution of voyage FR10/00, and the shipboard scientific party (Dr
Tony Koslow, Betsy Nahas, Prof Chari Pattiaratchi, Dr Will Schroeder, Dr Peter
Thompson, Dr Anya Waite, Mun Woo) for their assistance and constructive discussions.
I would like to further acknowledge Mun Woo for her excellent analyses of the physical
data and for assisting with my interpretations and graphical presentations; and Peter
Thompson for use of the nitrogen uptake data in this thesis. Brian Griffiths (CSIRO
Marine Research) is thanked both for the loan of the photosynthetron equipment and for
the detailed training provided on its use. Dr David Griffin (CSIRO Marine Research)
supplied real-time satellite imagery, and the staff at CMR Data Centre (particularly
Terry Byrne, Gary Critchley and Bob Beattie) provided extensive assistance with the
CTD and hydrology datasets. Bridget Alexander and Jamie McLaughlin are thanked for
pre- and post-cruise technical support, Ian Jameson (CSIRO Marine Research) for
phytoplankton taxonomic analysis and Dr Lesley Clementson (CSIRO Marine
Research) for HPLC analyses. Financial assistance for the Franklin study was provided
by a UWA Research Grant and a UWA Vice Chancellor’s Discretionary Grant.
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For the Capes Current study, I gratefully acknowledge the assistance of Bridget
Alexander, Joanne O’Callaghan, Chari Pattiaratchi and Stéphane Pesant in the field and
laboratory; Graham Pateman and the crew of the FV Cape Leeuwin for field operations;
Roger Head and Bill Foster for assistance with modifications to the F-probe; the
Australian Bureau of Meteorology for wind data; Alan Pearce (CSIRO Marine
Research) and the Western Australian Satellite Technology and Applications
Consortium (WASTAC) for SST imagery; and Chari Pattiaratchi for use of data
obtained on RV Southern Surveyor voyage SS09/03. This work was financially
supported by an Australian Research Council Small Grant.
Ocean colour imagery for both studies was obtained from the SeaWiFS Project,
as distributed by the Goddard Earth Sciences Data and Information Services
Center/Distributed Active Archive Center at the Goddard Space Flight Center,
Greenbelt, MD 20771.
Funding for my degree was provided by an International Postgraduate Research
Scholarship, a University Postgraduate Award and an ad hoc scholarship from the CWR
Coastal Oceanography group. I feel very privileged to have received these awards,
which allowed me to fulfill a long-held dream of moving to Australia and gave me the
opportunity to work in such an interesting oceanographic region. I also thank the
University of Western Australia, the Australian Marine Sciences Association and my
supervisors for financial support to present my work at both national and international
conferences.
Thanks to all my postgraduate colleagues at CWR for their friendship and
assistance over the past few years, and especially to Dr Matthew Simpson for
continuing to be such a great office-mate even from the other side of the country.
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A very special thanks to Team Canada – the Hansons, the Kuehleins and the
McLaughlins – for all their support and patience during what I think they have
perceived as my never-ending scholastic career…! I also thank Dr Lou Hobson for
guidance from afar, particularly during the early stages of my degree.
And finally, my enduring gratitude and appreciation to my partner, Jamie
McLaughlin, without whom none of this would matter. It is only Jamie who truly
knows all the effort that has gone into the completion of this project, and I could not
have done it without the daily support and encouragement he provided.
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CHAPTER 1
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Introduction
1.1 Motivation
Primary production is often greatly enhanced along the eastern boundaries of the major
ocean basins, where eastern boundary currents (EBCs) flow towards the equator in both
the northern and southern hemispheres (Wooster and Reid, 1963). Under the influence
of shore-parallel wind, combined with the Coriolis force, surface waters in these
relatively weak currents are deflected offshore and replaced by upwelling of cold,
nutrient-rich water from depth. Fluxes of ‘new’ nitrogen (as nitrate) into the euphotic
zone stimulate high rates of primary production (Barber and Smith, 1981; Mann and
Lazier, 1996). Proliferation of relatively large (> 5 m diameter) phytoplankton species
supports the development of a herbivorous food web (Cushing, 1989; Legendre and
Rassoulzadegan, 1995), with a short trophic pathway resulting in the significant finfish
stocks common to EBCs (Cushing, 1971).
There is, however, one eastern boundary region that does not conform to these
patterns. The anomalous poleward-flowing Leeuwin Current (LC) dominates the
eastern Indian Ocean adjacent to the coast of Western Australia (WA). This current
restricts the eastern arm of the Indian Ocean gyre to offshore regions and generates
large-scale downwelling as it travels along the continental shelf break (Pearce, 1991;
Smith et al., 1991). The LC transports warm, low salinity tropical waters southwards,
and due to low nutrient levels (Johannes et al., 1994) is considered to support only a
limited amount of phytoplankton biomass and productivity, leading to oligotrophic
conditions (Pearce, 1991).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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Against the backdrop of this general downwelling framework, a system of
equatorward coastal countercurrents is driven along the inner continental shelf by
upwelling-favourable southerly winds that prevail during the austral summer
(December to March). Part of that system, the Capes Current (CC) extends along the
southwest coast of WA (Pearce and Pattiaratchi, 1999) while the Ningaloo Current
(NC) extends along the northwest coast (Taylor and Pearce, 1999). The combination of
these wind-forced shelf currents and localized Ekman-driven upwelling (Gersbach et
al., 1999; Woo et al., 2004) seasonally restricts the inshore extent of the LC (Pearce and
Pattiaratchi, 1999; Taylor and Pearce, 1999).
The dominance of the Leeuwin Current within this region has had strong
impacts on marine biota, resulting in a southward extension of tropical species ranges
(Morgan and Wells, 1991) and some of the highest latitude coral reefs in the world
(Hatcher, 1991). Interannual variations in the strength of the LC, related to the El
Niño/Southern Oscillation cycle, show empirical relationships with recruitment patterns
of invertebrates and finfish (Lenanton et al., 1991; Caputi et al., 1996), however the
mechanisms behind these relationships have yet to be elucidated (Caputi et al., 1996;
Caputi et al., 2001). For example, modelling efforts suggest that recruitment success of
the western rock lobster (Panulirus cygnus) is not a function of physical transport
mechanisms but rather related to non-advective fluctuations in the LC, such as
temperature or rates of primary production (Griffin et al., 2001).
The primary objective of this study is therefore to provide a first assessment of
the physical and chemical oceanographic controls on phytoplankton dynamics in the
coastal eastern Indian Ocean. We specifically tested the general hypothesis that the
Leeuwin Current inhibits phytoplankton productivity in WA coastal waters by a)
providing a nutrient-poor (oligotrophic) environment, and b) suppressing upwelling-
Chapter 1 – Introduction
3
driven production. This was accomplished through intensive field investigations of
nutrient and primary production regimes within the LC and inshore countercurrents,
which included measurements of phytoplankton biomass, rates of primary production,
nitrogen nutrition and phytoplankton community structure. The findings provide
fundamental knowledge on physical-biological coupling off Western Australia, with
implications for fisheries management in view of seasonal and inter-annual variability
in the strength of both the Leeuwin Current and inshore countercurrents.
1.2 Structure of the Thesis
Following this introduction, Chapter 2 presents a Literature Review which provides an
overview of marine pelagic ecosystem dynamics and features unique to primary
production within subtropical oceanic waters, examines the impact of coastal upwelling
on primary production, gives detailed background on the physical, chemical and
biological oceanography of the eastern Indian Ocean, and includes a summary of
previous investigations on phytoplankton dynamics in the study region. The core
results sections of this thesis (Chapters 3 to 6) are presented as a series of stand-alone
manuscripts, intended for journal publication in slightly modified form. Some
repetition of background, study site details and methodology has been required for
completeness, although the Introduction for each chapter also expands upon the
Literature Review. These chapters each address different features of phytoplankton
dynamics in the coastal eastern Indian Ocean, but are united by the common theme of
physical and chemical forcing of primary productivity and pelagic ecosystem structure.
In Chapter 3, we explore regional spatial dynamics by examining links between
large-scale surface circulation/water types, nutrient distributions, phytoplankton
biomass and primary productivity. In Chapter 4, we consider processes in the vertical
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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and examine the structure and significance of deep chlorophyll maxima in Leeuwin
Current and offshore waters. Chapter 5 follows on from the patterns and dynamics
identified in Chapters 3 and 4, and investigates differences in nitrogen nutrition and
species composition between regions/water types and also between the surface and the
deep chlorophyll maximum. Chapter 6 investigates temporal patterns in productivity by
comparing summer conditions of localized upwelling with winter conditions impacted
by storm activity and seasonally strengthened Leeuwin Current flow. General
conclusions and recommendations for future research directions are presented in
Chapter 7.
CHAPTER 2
5
Literature review
2.1 Marine Pelagic Ecosystem Dynamics
Conventional models of the marine pelagic ecosystem suggest that there are two main,
and relatively separate, trophic pathways. Typical of nutrient-rich conditions such as
the temperate-latitude spring bloom, or active coastal upwelling, the herbivorous
(‘traditional’) food web is based in large (> 5 m) phytoplankton which support a
relatively short food chain that leads directly from phytoplankton to copepods to fish
(Fig. 2.1; Cushing, 1989). In contrast, stratified nutrient-depleted waters are
characterised by the microbial food web/loop, where bacteria and picophytoplankton
(0.2 – 2 m; Sieburth et al., 1978) can exploit the low nutrient environment, and are
consumed in turn by protozoa, ciliates and microzooplankton (Fig. 2.1; Azam et al.,
1983, Cushing, 1989). The combination of smaller cell/organism size and a greater
number of trophic levels within the microbial web results in a lower amount of
secondary production compared to the herbivorous food chain (Lalli and Parsons,
1997).
Legendre and Rassoulzadegan (1995), however, have challenged both the
simplicity and exclusivity of these two models, and have proposed that the pelagic
ecosystem is instead based on a continuum of trophic pathways. This continuum
includes both the herbivorous food web (Fig. 2.2a) and microbial loop (Fig. 2.2d), but
these are considered as two extreme and transient cases at either end of the spectrum
(Legendre and Rassoulzadegan, 1995). Linking these two ecological states are the
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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Figure 2.1. Schematic of trophic levels within the microbial loop and traditional
(herbivorous) food chain (from Cushing, 1989).
Chapter 2 – Literature Review
7
Figure 2.2. Schematic of the four trophic pathways within the pelagic ecosystem,
where solid arrows represent nitrogenous nutrient fluxes, open arrows indicate DOC
flux, and line thickness is proportional to flux rates with dashed lines indicating weak or
no flux (from Legendre and Rassoulzadegan, 1995). See text for further detail.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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multivorous web (Fig. 2.2b) and microbial web (Fig. 2.2c), both considered relatively
stable with time.
The functional distinction between microbial ‘loop’ and microbial ‘web’ was
defined by Rassoulzadegan (1993), where microbial loop describes the almost closed
system of heterotrophic bacteria and their zooflagellate grazers, while the microbial
food web includes these components plus small (< 5 m) phytoplankton (Fig. 2.2c,d).
In the closed loop system, which is most common in dissolved organic nitrogen (DON)
limited systems (Legendre and Rassoulzadegan, 1995), bacterial growth is tightly
coupled to dissolved organic material (DOM) release from zooflagellate grazers (Azam
et al., 1993; Hagstrom et al., 1988) and little carbon export occurs. In a higher DON
environment, ammonium fluxes from heterotrophic bacteria and protozoan activity
support an active picoplankton component (Legendre and Rassoulzadegan, 1995),
contributing to export of biogenic carbon (Mousseau et al., 2001).
Within the multivorous food web, it is recognized that both the herbivorous and
microbial web pathways play important roles, with significant coupling between these
two trophic modes (Legendre and Rassoulzadegan, 1995). Actively grazing
herbivorous copepods contribute both to the ammonium pool (via excretion) and the
dissolved organic carbon (DOC) and DON pools through, for example, sloppy feeding
(Roy et al., 1989) and fecal pellet degradation (Jumars et al., 1989). Fluxes of ‘new’
(nitrate) nitrogen, which support the production of large phytoplankton within these
systems, are therefore channelled into the microbial web to support bacterial and
picoplanktonic production (Legendre and Rassoulzadegan, 1995).
As suggested by Cushing (1989), the herbivorous food web is characteristic of
dynamic, high-nutrient systems such as upwelling regions and the temperate spring
bloom. These conditions, which are inherently transient, have led Legendre and
Chapter 2 – Literature Review
9
Rassoulzadegan (1995) to classify the strictly herbivorous pathway as unstable.
Similarly, the microbial loop is based in a transitory condition within oligotrophic
waters where bacterial production completely dominates over autotrophic production,
and bacterial populations rapidly increase under very little grazer control (Legendre and
Rassoulzadegan, 1995). This microbial loop has been observed in the oligotrophic
systems of the subtropical Sargasso Sea (Fuhrman et al., 1989) and the central North
Pacific Gyre (Cho and Azam, 1990). The more stable scenario of pico- and
nanoplankton production closely linked with ammonium remineralization by
heterotrophic bacteria, has been observed in regions such as the Antarctic ice edge
(Legendre et al., 1992) and the Subtropical Front off New Zealand during winter
(Bradford-Grieve et al., 1999). The multivorous food web has been demonstrated in
‘high nutrient, low chlorophyll’ (HNLC) regions of the Southern Ocean and subarctic
Pacific Ocean (as reviewed in Legendre and Rassoulzadegan, 1995), and in the
nearshore waters of the Gulf of St Lawrence (Mousseau et al., 2001). Legendre and
Rassoulzadegan (1995) have hypothesized that the trophic complexity associated with
the multivorous and microbial food webs contributes to their stability over time.
2.2 Primary Production in Subtropical Oceanic Waters
Unlike polar and temperate regions, which experience significant seasonality in physical
conditions such as light, temperature, wind field and nutrient fluxes (Lalli and Parsons,
1997), subtropical oceanic regions are typified by greater physical stability associated
with the diminishing seasonality at lower latitudes (Blackburn, 1981). A persistently
warmed surface layer and strong permanent thermocline contribute to vertical stability
of the water column, which is characteristic of open ocean waters within the large
subtropical gyres of the Atlantic, Pacific and Indian Oceans (Blackburn 1981). These
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
10
conditions can lead to a distinct ecological separation of phytoplankton communities
within the euphotic zone, where nutrient-limited surface populations exploit a tightly
coupled regenerative microbial web system (Banse, 1992; Legendre and
Rassoulzadegan, 1995), while populations near the nitracline take advantage of higher
vertical nutrient fluxes but must cope with severe light limitation (Venrick, 1982;
Cullen, 1982). Typically, a deep chlorophyll maximum (DCM) layer forms just above
the nutricline, often as a combination of both higher phytoplankton biomass within the
strata and decreased carbon:chlorophyll a (C:chl a) ratio as a physiological adaptation to
lower light levels (Cullen, 1982; Geider, 1987).
The most intensive studies of biogeochemical processes in subtropical oceanic
regions have been conducted in the Atlantic Sargasso Sea and in the North Pacific
Subtropical Gyre, as part of the U.S. Joint Global Ocean Flux Study (JGOFS; Siegel et
al., 2001). Results from the Bermuda Atlantic Time-Series Study (BATS; Michaels and
Knap, 1996) and the Hawaii Ocean Time-Series (HOT; Karl and Lukas, 1996),
collected since 1988 and still on-going, have challenged some of the assumptions about
ecological stability within the subtropical gyres. In particular, significant seasonal and
interannual variability in phytoplankton biomass, production and community structure
have been found both off Hawaii (Karl et al., 2001) and Bermuda, where primary
productivity in this theoretically stable system exhibited dynamic fluctuations between
100 and 1500 mg C m-2 d-1 over nine years of study (Fig. 2.3; Steinberg et al., 2001).
Seasonal changes in surface heat flux and wind stress are responsible for much of the
upper ocean physical variability off Bermuda, and enhanced vertical mixing during
winter generates vertical nutrient fluxes that support a short spring bloom period from
January to March (Steinberg et al., 2001). Summer brings thermal stratification and
nutrient depletion within the upper euphotic zone (Lipschultz, 2001), with a deep
Chapter 2 – Literature Review
11
Figure 2.3. Depth-integrated (0 – 140 m) primary productivity results from the
Bermuda Atlantic Time-Series Study (BATS), with stars indicating associated
measurements of physical mixing deeper than 150 m (adapted from Steinberg et al.,
2001).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
12
chlorophyll maximum layer between 60 and 120 m (Steinberg et al., 2001). In both the
Bermuda and Hawaii subtropical regions, picoplankton (especially the prokaryotic
components) are important and often dominant components of the pelagic ecosystem
(Karl et al., 2001; Steinberg et al., 2001).
2.2.1 Importance of picoautotrophs
While generally associated with relatively low (< 400 mg C m-2 d-1) carbon fixation
rates (Longhurst et al., 1995; Maranon et al., 2000), the subtropical gyres account for
> 60 % of the world ocean and > 30 % of total marine primary production (Longhurst et
al., 1995). However, as mentioned above, an intensive time-series study off Bermuda
demonstrated that subtropical regions can be more productive than originally thought
(Steinberg et al., 2001). The primary contributors to pelagic production in these warm,
low nutrient waters are the picoplankton, small (< 2 m) autotrophic cells (Li et al.,
1983) that are often prokaryotic. The unicellular cyanobacteria Synechococcus, first
recognized in 1979 (Waterbury et al., 1979), is a widely occurring species that can be a
major contributor to nitrogen fixation in the oligotrophic Pacific Ocean (Montoya et al.,
2004). The extremely small (0.5 – 0.7 m) Prochlorococcus is a more recent discovery
(Chisholm et al., 1988) whose phylogenetic origins are currently being debated
(Partensky et al., 1999). These prochlorophytes, which can tolerate a wide range of
irradiance and are found throughout the euphotic zone (as reviewed in Partensky et al.,
1999), also possess unique divinyl derivatives of chlorophyll (Goericke and Repeta,
1992) that allow for their ready identification using pigment methods (Jeffrey and Vesk,
1997). The ecological importance of the eukaryotic component within the picoplankton
(Simon et al., 1994) has also been recently recognized (Worden et al., 2004). While
numerically less abundant than the picoprokaryotes, Worden et al. (2004) found that in
Chapter 2 – Literature Review
13
Pacific Ocean coastal waters the eukaryotic fraction (which included the prasinophyte
Ostreococcus as identified through molecular techniques) accounted for up to 76% of
net carbon production.
2.2.2 Deep chlorophyll maxima and the carbon:chlorophyll a ratio
As mentioned previously, a deep chlorophyll maximum (DCM) layer is a typical feature
of subtropical oceanic regions. The optimal vertical position for photosynthesis is
generally determined by a combination of irradiance and nutrients (Falkowski and
Woodhead, 1992), and can result in active accumulation of phytoplankton at distinct
water depths (Cullen, 1982). There are, however, a number of other scenarios that may
be involved in DCM formation, as reviewed in Cullen (1982). These include passive
accumulation of cells at a pycnocline, or behavioural aggregation of motile cells
(especially dinoflagellates) as a defense against grazing (Cullen, 1982). In addition, the
amount of chlorophyll per unit biomass can be highly variable (Geider, 1987; Li et al.,
1992; Geider et al., 1997), increasing with a decrease in ambient irradiance in a process
termed photoacclimation (Geider, 1987). Accordingly, deep chlorophyll maxima may
not necessarily correspond to an increase in biomass, but rather signify a physiological
adaptation of cellular carbon:chlorophyll a (C:chl a).
Phytoplankton carbon has traditionally been determined by linear regression of
particulate organic carbon (POC; collected by filtering a known volume of seawater
through a precombusted GF/F filter) on chl a (Eppley et al., 1977; Townsend and
Thomas, 2002). As POC from a bulk seawater sample can be composed of not only
phytoplankton, but also bacteria, microzooplankton and detritus, the regression intercept
is taken as that portion of POC not associated with live phytoplankton (Eppley et al.,
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
14
1977). However, Banse (1977) has noted that this method can potentially overestimate
C:chl a () and underestimate the detrital carbon component.
Another common method of phytoplankton carbon determination involves the
conversion of microscopic cell counts to carbon content based on cell biovolumes
(Strathmann, 1967; Montagnes et al., 1994; Hillebrand et al., 1999). While time-
consuming, this can alleviate the errors associated with the inclusion of the non-
phytoplankton component typical of the filtration method. However, this technique can
underestimate the picoplanktonic fraction, unless epi-fluoresence microscopy is
employed (Schluter et al., 2000; Havskum et al., 2004). In recent years, phytoplankton
carbon has also been derived from a relationship with cellular DNA content, as
determined using nuclear staining methods with flow cytometry (Veldhuis et al., 1997;
Veldhuis and Kraay, 2004).
The C:chl a ratio is a sensitive physiological parameter that varies as a function
of temperature, irradiance levels and nutrient availability (Yoder, 1979; Terry et al.,
1983; Osborne and Geider, 1986; Geider, 1987). At constant temperature and non-
limiting nutrient concentrations, increases linearly with irradiance; conversely, at
constant irradiance, decreases exponentially with increasing temperature (Geider,
1987) and declines as a function of nutrient limitation (Osborne and Geider, 1986;
Geider et al., 1997). Within the euphotic zone, these factors are often correlated with
depth and therefore of particular importance when examining the dynamics of stratified
phytoplankton populations. The generally lower C:chl a ratio of DCM phytoplankton
(as a result of photoacclimation; Geider, 1987) precludes the use of a single value of
in studies of subtropical oceanic regions (e.g. Everitt et al., 1990; Spitz et al., 2001;
Veldhuis and Kraay, 2004).
Chapter 2 – Literature Review
15
A novel combination of methods, including size fractionation, flow cytometry,
DNA analysis and HPLC pigment techniques, has also allowed accurate estimation of
for different phytoplankton population types within the subtropical waters of the
Atlantic Ocean, specifically prochlorophytes versus the eukayotic phytoplankton
community (Veldhuis and Kraay, 2004). Prochlorococcus showed a 30-fold increase in
chl a between the surface and DCM, resulting in a value of that ranged from a high of
450 mg C mg chl a-1 at the surface to 15 mg C mg chl a-1 at 150 m depth. In contrast,
the eukaryotic component exhibited a much lower 3–7 fold increase in chl a with depth,
and a surface that ranged from 30 – 80 mg C mg chl a-1 (Velhuis and Kraay, 2004).
However, both the prochlorophyte and eukaryotic components had similar values of
below the mixed layer depth and within the DCM. The lower eukaryotic variability
was linked to co-variation of pigment concentration and cell size associated with a
community shift from the surface to the DCM, while with the prokaryotes a single
species with uniform cell size (Prochlorococcus) exhibited a high degree of
photoacclimation associated with successful coverage of the entire euphotic zone
(Veldhuis and Kraay, 2004).
2.2.3 Role of micronutrients in phytoplankton dynamics
While macronutrients such as nitrate, phosphate and silicate are often considered as
principal regulars of primary productivity, recent advances in analytical chemistry
(Salbu and Steinnes, 1995) have allowed further investigation into the role of
micronutrients (present at concentrations < 0.1 M) in phytoplankton dynamics. Most
studied within the marine system are the trace metals (Fe, Co, Cu, Zn, Mn, Ni and Cd),
which have biological roles as enzymatic cofactors and structural protein elements
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
16
(Donat and Bruland, 1995). These metals, generally sourced from soil and rocks, have
limited solubility and are rapidly removed within the coastal zone by phytoplankton
uptake. The open ocean is therefore often depleted in trace metals, with aeolian dust
one of the only sources for Fe and Mn in this region (as reviewed in Morel and Price,
2003).
Small and large phytoplankton have different tolerances for trace metal
limitation, as evidenced by the specific impact of Fe limitation on diatoms within the
subtropical Pacific (Price et al., 1994). Diatoms flourish under high nitrate conditions,
and require Fe to facilitate the reduction (via nitrate reductase) of NO3- to NH4
+ for
assimilation within the cell (Eppley and Rogers, 1970; Price et al., 1994). In contrast,
picoplankton (< 2 m) can acquire micronutrients more effectively by virtue of their
small size, and are adapted to utilize the low ambient concentrations of NH4+
characteristic of subtropical regions (Morel and Price, 2003). Species such as
Prochlorococcus are also under strong grazing control by microzooplankton in
oligotrophic waters, which limits their biomass response to experimental Fe additions
(Cavender-Bares et al., 1999). Large-size (> 10 m) phytoplankton (primarily pennate
diatoms) can exhibit 60-fold increase in biomass (as chl a) to Fe enrichment, as
compared to a 7-fold increase for the small size fraction (Cavender-Bares et al., 1999).
There has also been speculation that N2 fixation by cyanobacteria is likely Fe limited
(Falkowski et al., 1998), although recent measurements from the Caribbean Sea and
North Atlantic indicate that the Fe requirements of N-fixing Trichodesmium are less
than previously estimated (Kustka et al., 2003).
Chapter 2 – Literature Review
17
2.3 Coastal Upwelling and Primary Production
As autotrophic producers, phytoplankton form the primary link between the physical
environment and higher levels of the pelagic food chain. These microscopic organisms
convert inorganic materials (carbon dioxide, water, nutrients, trace elements) into
organic matter using energy provided by the sun. Photosynthetic production can
therefore be under strong ‘bottom-up’ control (Hunter and Price, 1992), where resource
availability (e.g. light, nutrients) can either limit or enhance rates of carbon fixation and
the accumulation of autotrophic biomass. Phytoplankton community structure, and the
trophic pathways associated with the pelagic food web, is also closely tied to nutrient
supply, with nitrogen as the most commonly limiting macronutrient in the marine
environment (Carpenter and Capone, 1983).
Coastal upwelling regimes, where deep nitrate concentrations are transported
into the euphotic zone, are of global importance for both primary and secondary
productivity (Cushing, 1971; Mann and Lazier, 1996). Upwelling events can result in
rapid changes in both the light and nutrient environment, often requiring physiological
adaptation of the phytoplankton community (Kudela et al., 1997). A ‘shift-up’ period,
during which previously nutrient-depleted cells must manufacture the necessary
metabolic compounds (e.g. nitrate reductase) to utilize high nitrate concentrations
(Eppley and Rogers, 1970), can result in an apparent time-lag response of
phytoplankton to upwelling (MacIsaac et al., 1985; Dugdale and Wilkerson, 1989).
In these high nutrient environments, where dissolved nitrate can reach 20 –
30 M (Dickson and Wheeler, 1995; Kudela et al., 1997), new production (sensu
Dugdale and Goering, 1967) and the traditional (short) food chain can predominate
(Cushing, 1989). However, upwelling regions can be extremely dynamic, with
upwelling pulses interspersed with periods of stratification (Mann and Lazier, 1996).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
18
During these ‘relaxation’ periods, when the supply of nitrate decreases, regenerated
production based on nitrogen recycled within surface waters (i.e. ammonium and urea)
can be considerable (Codispoti, 1983; Bode and Varela, 1994). Under these conditions,
a much more diversified and heterotrophic food web may develop. Typified by pico-
and nano-phytoplankton, heterotrophic microflagellates, ciliates and microzooplankton,
this microbial food web (Azam et al., 1983; Cushing, 1989; Legendre and
Rassoulzadegan, 1995) is now acknowledged as an important component of coastal
upwelling ecosystems (Probyn, 1987; Probyn et al., 1990; Bode and Varela, 1994; Bode
et al., 2004).
Major upwelling regions (Fig. 2.1) are generally associated with eastern boundary
currents (Wooster and Reid, 1963), which are located along the western coasts of
continents in both the northern and southern hemispheres. However, oceanographic
conditions off the west coast of Australia are unique, being associated with a
combination of large-scale downwelling interspersed with small-scale seasonal coastal
upwelling. In the following section, we examine in detail the distinctive oceanography
of this region.
2.4 Oceanography of the Coastal Eastern Indian Ocean
2.4.1 Physical features
The eastern Indian Ocean adjacent to the coast of Western Australia (WA) is dominated
by the Leeuwin Current (LC), a poleward-flowing eastern boundary current generally
located along the continental shelf-break and upper slope (Cresswell and Golding,
1980). The LC is driven by an alongshore geopotential gradient (Thompson, 1984;
Thompson, 1987), itself a product of the unique connection between the Indian and
Pacific oceans north of Australia (Fig. 2.2) and the low density of the tropical source
Chapter 2 – Literature Review
19
Figure 2.1. Major upwelling regions in the world ocean are generally located along the
west coast of continents, where the prevailing winds (indicated by arrows) blow towards
the equator (from Mann and Lazier, 1996).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
20
Figure 2.2. Schematic of the major surface currents in the eastern Indian Ocean and the
connection between the Indian and Pacific oceans through the Indonesian archipelago
(adapted from Godfrey, 2001).
Chapter 2 – Literature Review
21
waters. The steric height gradient is sufficiently large to overcome the opposing
equatorward wind stress, allowing the LC to progress southwards (Cresswell, 1991). A
consequence of this anomalous flow is a general downwelling regime (as evidenced by
onshore surface transport) along the coast of Western Australia (Pearce, 1991). This is
in sharp contrast to eastern boundary currents of the Atlantic and Pacific Oceans, which
have equatorward surface flow, offshore Ekman transport and large-scale upwelling of
cold, nutrient-rich water (Wooster and Reid, 1963).
The Leeuwin Current is present year-round, however flow is maximal in autumn
and winter (April to August) when the equatorward wind stress is weakest (Godfrey and
Ridgway, 1985). Commencing as a broad (400 km) and shallow (50 m) flow off the
North West Shelf, this warm, low-salinity current narrows to 100 km and deepens to
300 m as it progresses southwards (Smith et al., 1991). Attaining speeds of up to
0.5 ms-1 along the west coast, it rounds Cape Leeuwin and proceeds eastwards where it
may travel at up to 1.5 ms-1 (Cresswell, 1991). LC strength and volume are also linked
to the El Niño/Southern Oscillation (ENSO) cycle. The interannual ENSO signals are
transmitted along across the Indonesian Throughflow and along the WA coastline as
coastally trapped waves (Meyers, 1996; Wijffels and Meyers, 2003). High coastal sea
levels correspond to stronger LC flow during La Niña years, and contrast with low sea
levels and weaker flow during El Niño years (Pearce and Phillips, 1988; Feng et al.,
2003, 2004).
The presence of the LC restricts the equatorward-flowing eastern arm of the
Indian Ocean gyre, the West Australian Current, to offshore regions (Andrews, 1977;
Pearce, 1991). However, as the LC flows southwards its volume is augmented by
eastward geostrophic inflow (Fig. 2.3) from these offshore waters (Hamon, 1965;
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
22
Figure 2.3. Illustration of the geostrophic inflow of Indian Ocean waters that augment
the Leeuwin Current’s volume as it travels southwards along the continental shelf break
(adapted from Godfrey and Ridgway, 1985 and Pearce and Phillips, 1988).
Chapter 2 – Literature Review
23
equatorward return flow (the Leeuwin Undercurrent) at a depth of between 300 and
600 m (Thompson, 1984; Smith et al., 1991).
Inshore of the Leeuwin Current, a seasonally dominated inner-shelf current
system follows the mean wind patterns. In the southwest of Western Australia this is
represented by the Capes Current (CC; Fig. 2.4a), a northward current present during
the summer months (December to March; Pearce and Pattiaratchi, 1999); its counterpart
along the northwest coast is the Ningaloo Current (NC; Taylor and Pearce, 1999).
Associated with an offshore movement of the LC (Gersbach et al., 1999; Pearce and
Pattiaratchi, 1999), the Capes Current is predominantly generated by localized Ekman-
driven upwelling (Gersbach et al., 1999), with source waters from the mid to lower
depth of the outer continental shelf (Fig. 2.4b). Modeling simulations revealed that
transient upwelling associated with the CC occurs numerous times during the summer
season (dependent on wind forcing), and is generally confined to the inner shelf by the
position of the Leeuwin Current (Gersbach et al., 1999).
2.4.2 Nutrient dynamics
Surface waters of the eastern Indian Ocean are considered strongly oligotrophic, with
nitrate and phosphate concentrations typically below 0.2 M (Rochford, 1980). The
warm Leeuwin Current has similarly low nutrient levels in the upper mixed layer (Fig.
2.5), with the nutricline present between 100 and 200 m depth (Pearce et al., 1992). For
comparison, total combined inorganic nitrogen (nitrate, nitrite, ammonium)
concentrations in temperate surface waters are typically between 8 – 15 M, with
corresponding phosphate levels of 0.5 – 1.0 M (Spencer, 1975).
There are few measures of nutrient dynamics in continental shelf waters off
Western Australia. The inner shelf region has been studied most frequently in the
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
24
(a)
(b)
Figure 2.4. Schematic of the northward-flowing Capes Current, (a) present along the
coast of southwestern Australia during the summer months, and (b) predominantly
generated through Ekman-driven upwelling (from Gersbach et al., 1999).
Chapter 2 – Literature Review
25
Figure 2.5. Nitrate and phosphate concentrations (M) across a section of the Leeuwin
Current (stations C2 to C5) at 29.12S during August/September 1987 (adapted from
Pearce et al., 1992).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
26
vicinity of Perth (WA’s state capital; Fig. 2.3), and is characterized by winter peaks of
nitrate and silicate followed by a summer phosphate maximum (Johannes et al., 1994).
Annual ranges of nitrate in northern Perth coastal waters are from 0.5 M (summer) to
1.6 M (winter), while summer phosphate concentrations (~ 1.0 M) are generally
twice what is found in winter. These concentrations are notably higher than at an open
shelf sampling station with strong Leeuwin Current influence, where nitrate ranged
from 0.3 to 0.5 M and phosphate averaged 0.1 M, with no clear seasonal pattern
(Johannes et al., 1994).
Additional studies on the continental shelf, south of the Abrolhos Islands
(Pearce et al., 1992) and off Cape Leeuwin (Pearce and Pattiaratchi, 1999), indicate the
same or lower nutrient concentrations as found near Perth. Whilst higher than open
ocean values, these coastal nutrient levels are in the lower range reported for similar
temperate regions. The absence of significant terrestrial runoff, combined with a
nutrient-poor eastern boundary current and lack of large-scale upwelling, have been
cited as the predominant factors impacting the nutrient status of Western Australian
marine waters (Rochford, 1980).
However, seasonal upwelling associated with the inshore countercurrents may
also play an important role in nutrient dynamics along the west coast of Australia. The
impact of the Capes Current on nitrate and phosphate concentrations has been examined
by Gersbach et al. (1999). Nutrient sections from a field study in summer 1994
revealed that upwelled water has its source at the base of the Leeuwin Current mixed
layer, close to the nutricline. Capes Current surface water was shown to have slightly
elevated nutrients (0.4 M NO3-) as compared to the bulk of the Leeuwin Current
(0.2 M NO3-; Gersbach et al., 1999). This study therefore provided a first estimate of
the impact of the Capes Current on nutrient dynamics. However, given the seasonal and
Chapter 2 – Literature Review
27
inter-annual variability both in upwelling strength and the position and strength of the
Leeuwin Current (Pearce and Pattiaratchi, 1999), further investigations are warranted.
2.4.3 Pelagic ecology
2.4.3.1 Secondary production
The Leeuwin Current has an important influence on the ecology of Western Australian
coastal waters, although research efforts have primarily been devoted to understanding
the LC’s effect on commercial fisheries, with a focus on magnitude, structure, and
fluctuations in annual recruitment (Pearce and Phillips, 1988; Lenanton et al., 1991;
Caputi et al., 1996). There is a direct link between the strength of the Leeuwin Current
(as determined by sea level height and influenced by ENSO; Feng et al., 2003, 2004)
and the recruitment of various fish and invertebrate species common to WA coastal
waters. This relationship is positive for western rock lobster (Panulirus cygnus) and
whitebait (Hyperlophus vittatus) populations, but negative for saucer scallop (Amusium
balloti) and pilchard (Sardinops sagax neopilchardus) populations (Caputi et al., 1996).
Recent modelling studies of Leeuwin Current influence on rock lobster recruitment
have indicated that the mechanisms behind the relationship between LC flow and
recruitment strength are not directly related to advective features of the LC (Caputi et
al., 2001), indicating that variations in levels of primary production may be a major
factor (Griffin et al., 2001).
Finfish resources off WA, while composed of similar planktivorous species as
found in the upwelling eastern boundary regions (e.g. pilchard, herring, anchovy), are
notably lower in quantity. Annual harvests within the Humboldt system off South
America (1-13 million tonnes) and the Benguela system off South Africa (1-4 million
tonnes) far out-weigh the Leeuwin Current system (< 0.001 million tonnes; Lenanton et
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
28
al., 1991). Yet WA is home to the most valuable single-species fishery in Australia, the
western rock lobster (Panulirus cygnus), worth ~ $300 – 350 million in 2002/2003
(Penn et al., 2003). Hatched during late spring or summer on the outer edge of the
Western Australian continental shelf, P. cygnus undergoes an extensive period as a leaf-
like phyllosoma larvae (9 to 11 months), much of which is spent in the offshore waters
of the south-eastern Indian Ocean (Gray, 1992). Late-stage phyllosoma are transported
back towards the coast by the subsurface eastward geostrophic flow (Phillips, 1981),
and undergo the critical metamorphic moult into the nektonic (and non-feeding)
puerulus stage that actively swims across the continental shelf to the adult habitat in the
coastal reef system (Gray, 1992).
The continental shelf break off Western Australia, often associated with the core
or frontal edge of the Leeuwin Current, has been identified as a region of relatively high
plankton and micronekton biomass compared to offshore Indian Ocean waters (Phillips
and Pearce, 1997). McWilliam and Phillips (1997) suggest that it is these food
resources, and not environmental cues related to temperature and salinity gradients
associated with the LC (Phillips and McWilliam, 1986), that determine the timing and
success of the metamorphic moult and final recruitment to the adult population. Mixing
and shear associated with flow at the shelf break (Pearce and Griffiths, 1991; Cresswell,
1996; Meuleners et al., 2003) may lead to nutrient enrichment and enhanced
phytoplankton and zooplankton production in this region (McWilliam and Phillips,
1997).
This is just one example of a potentially important link between physical
processes and biological production in the coastal waters of Western Australia.
However, as we address in the next section, there has been extremely limited research
into the key relationships between physical oceanography, nutrient dynamics and
Chapter 2 – Literature Review
29
primary productivity in continental shelf and Leeuwin Current waters. Until these
dynamics are understood, furthering of hypotheses related to higher trophic levels will
be limited.
2.4.3.2 Primary production Marine waters can be classified according to the amount of primary production they
support (Nixon, 1995), although there is often high variability both within and between
regions. Coastal upwelling areas, with injections of new nutrients from depth, range
from mesotrophic to hypertrophic (500 – 3000 mg C m-2 d-1; Brown et al., 1991;
Pilskaln et al., 1996). At the opposite end of the production spectrum are relatively
stable, nutrient-depleted oligotrophic waters, typical of the subtropical gyres, with
production levels generally 400 mg C m-2 d-1 (Longhurst et al., 1995; Maranon et al.,
2000).
Along the coast of Western Australia, low nutrient conditions are thought to
support only oligotrophic levels of water column productivity. Data sourced from the
International Indian Ocean Expedition (IIOE; 1959 – 1965) indicates average
production rates of 100 – 250 mg C m-2 d-1 off WA (Fig. 2.6; Koblentz-Mishke et al.,
1970; FAO, 1981). However, these measurements were undertaken in open ocean
waters along 110E (Jitts, 1969), approximately 400 km offshore and well outside
Leeuwin Current and coastal countercurrent waters.
A recent review of phytoplankton biomass (as estimated via chlorophyll a) in
WA coastal waters found sparse coverage of in situ data over the majority of the
continental shelf, with little information available on vertical structuring as most
samples were either surface-only or integrated over the water column (Pearce et al.,
2000). Satellite imagery of ocean colour from Coastal Zone Colour Scanner (CZCS)
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
30
Figure 2.6. Average rates of phytoplankton production (mg C m-2 d-1) in oceanic and
coastal waters off South America, southern Africa and Australia (from FAO, 1981).
Chapter 2 – Literature Review
31
data provided more broad-scale coverage, but was limited to assessment of near-surface
phytoplankton distributions. Within the constraints of the in situ and satellite data,
Leeuwin Current and offshore waters were characterized as very low chlorophyll
environments (< 0.25 mg m-3), with elevated concentrations found along the continental
shelf (< 1.0 mg m-3; Pearce et al., 2000; Pattiaratchi et al., in press). High chlorophyll
a values (~ 2 – 5 mg m-3) were considered representative only of shelf waters or
estuaries subjected to anthropogenic nutrient inputs (Pearce et al., 2000).
Due to the limited nature of previous investigations, the response of
phytoplankton to the unique Leeuwin Current-dominated system off Western Australia
has yet to be elucidated on a regional scale. The impact of seasonal upwelling,
associated with the Capes and possibly Ningaloo Currents, on phytoplankton
productivity is also unknown. Estimates of phytoplankton biomass and productivity in
WA coastal waters therefore form an important component of this thesis, although it is
essential to remember that these parameters are not interchangeable, as they convey
different information about the phytoplankton community. Profiles of biomass show
where cells are situated (or where chlorophyll:carbon is highest; Cullen, 1982), but give
little information about their viability or adaptation to their physical environment. In
contrast, photosynthetic rates indicate whether the phytoplankton are actively growing,
are limited by some parameter (e.g. light or nutrients) or are quiescent cells advected
from elsewhere. Biomass profiles would underestimate production if, for example, the
phytoplankton population was being actively grazed down (Welschmeyer and Lorenzen,
1985).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
32
2.5 Summary of Previous Investigations
The thesis examines oceanographic forcing of phytoplankton dynamics in Western
Australian coastal waters from North West Cape to Cape Leeuwin, with the offshore
extent generally limited to the 1000 m isobath (21.5S to 34.5S and 112.0E to
115.5E). Here, we specifically consider past studies of phytoplankton biomass levels
and productivity within this region, excluding estuarine waters.
2.5.1 Phytoplankton biomass
The International Indian Ocean Expedition (IIOE) was one of the first large-scale
surveys of the eastern Indian Ocean, and the phytoplankton biomass results are
summarized in Humphrey (1966) and Krey and Babenerd (1976). While these studies
contain useful information on vertical structuring (up to six depths sampled per station)
and seasonal trends, they have poor spatial resolution in coastal waters. Recent studies
have been more localized in nature, and are concentrated in Geographe Bay (Waite and
Alexander, 2000), the Peel-Harvey region (Black et al., 1981) and Perth coastal waters
(Lord and Hillman, 1995; Department of Environmental Protection, 1996). Additional
shelf-scale surveys off Perth are detailed in Department of Environmental Protection
(1996) and Helleren and Pearce (2000).
Little chlorophyll data exists in the region between Perth coastal waters and
North West Cape. Some previously unpublished data from the Abrolhos Islands is
tabulated in Helleren and Pearce (2000), while two small-scale studies within Shark Bay
are detailed in Kimmerer et al. (1985) and Peterson and Black (1991). Further north,
the tropical waters of the North West Shelf are considered an area of high biological
production (Hallegraeff and Jeffrey, 1984), and a few studies have examined
autotrophic biomass in this region (Hallegraeff and Jeffrey, 1984; Tranter and Leech,
Chapter 2 – Literature Review
33
1987; Furnas and Mitchell, 1999). Physical nutrient transport mechanisms (e.g. tidal
mixing, tropical cyclones, localized upwelling) that may account for this elevated
productivity have been examined by Holloway et al. (1985).
Analysis of archived CZCS data by Pattiaratchi et al. (in press) provides the first
large-scale, seasonal overview of surface chlorophyll distributions from Shark Bay to
Cape Leeuwin. The data were constrained by a lack of sea-truth data for calibration, but
clearly shows entrainment of higher chlorophyll shelf water into the Leeuwin Current.
2.5.2 Primary production
An extensive oceanographic database (MarLIN) is maintained by the CSIRO Division
of Marine Research, with cruise reports dating back to the 1950’s. Over 30 cruises have
been conducted (fully or partially) within the study boundaries of North West Cape to
Cape Leeuwin. Of these, only a few have included primary production in their
sampling protocol (Table 2.1) and all were limited to oceanic waters offshore of the
Leeuwin Current. Some recent studies have measured phytoplankton productivity in the
Perth and Geographe Bay regions (Thompson et al., 1999; Waite and Alexander, 2000),
but focused only on shallow coastal waters (Table 2.1).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
34
Table 2.1. Summary of previous measurements of primary production (14C uptake) off
the west coast of Australia.
Cruise/Study Location Comments
Diamantina (IIOE)
Cruises 2/59 to
3/62
Eastern Indian Ocean
Good vertical and horizontal coverage
in offshore waters (stations along
110E), but coastal areas not sampled
Kabanova, 1968 Indian Ocean Summary of all IIOE primary
production data (1951-1965), coastal
region from NW Cape to Cape
Leeuwin poorly sampled
Thompson et al.,
1999; Waite and
Alexander, 2000
Perth Coastal Waters,
Geographe Bay
Limited to nearshore regions
Chapter 2 – Literature Review
35
2.6 Concluding Remarks
Within the unique oceanographic setting of the coastal eastern Indian Ocean, our current
knowledge of phytoplankton dynamics is clearly limited. The majority of regional
spatial information on phytoplankton biomass distributions has been derived from
satellite imagery, which reveals relatively high biomass on the continental shelf and low
biomass in Leeuwin Current and offshore waters (Fig. 2.7; Pattiaratchi et al., in press).
These surface ocean colour distributions have been taken to infer high phytoplankton
productivity in coastal waters and low productivity within the Leeuwin Current (Pearce
et al., 2000). However, without any actual measurements of photosynthetic rates and
with little information on subsurface biomass distributions, it is not possible to evaluate
proposed linkages between physical oceanographic processes, nutrient dynamics and
biological productivity within this region. This thesis addresses this gap in knowledge
by undertaking the first large-scale biological oceanographic study along the west coast
of Australia, with a focus on assessing the physical and chemical controls on
phytoplankton productivity and community composition along both the northwest
(North West Cape to the Abrolhos Islands) and southwest (Cape Naturaliste to Cape
Leeuwin) coasts of Western Australia.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
36
Figure 2.7. Ocean colour (SeaWiFS) image from 5 April 2002, illustrating relatively
high chlorophyll concentrations on the continental shelf and low concentrations in
Leeuwin Current and offshore waters. The two large eddies between 29S and 32S
show the entrainment of shelf waters into the Leeuwin Current.
CHAPTER 3
37
Sporadic upwelling on a downwelling coast: phytoplankton responses to
spatially variable nutrient dynamics off the Gascoyne region of
Western Australia *
3.1 Summary
This chapter explores regional spatial oceanographic dynamics along the northwest
coast of Australia by examining links between surface water types, physical dynamics,
nutrient distributions, phytoplankton biomass and species composition, and rates of
primary production. We found Leeuwin Current (LC) and offshore waters to be
associated with low phytoplankton biomass (21.4 6.9 s.d. mg chl a m-2) and low
primary production (110 – 530 mg C m-2 d-1); surface (< 50 m) waters were nitrate-
depleted (generally < 0.1 M), with a strong nutricline present at the base of the mixed
layer. However, upwelling associated with the Ningaloo Current sourced water from
this nutricline, and in conjunction with mixing generated by seaward offshoots, resulted
in nitrate levels of up to 2 – 6 M within the euphotic zone. Biomass in these Ningaloo
Current waters (35.9 11.6 mg chl a m-2) was significantly higher than in LC/offshore
regions, with primary production in the range of 840 – 1310 mg C m-2 d-1. Capes
Current water was also highly productive (990 mg C m-2 d-1), and with low silicate
levels and a high proportion of centric diatoms, was typical of an aging upwelled water
mass. Thus the dominance of the oligotrophic Leeuwin Current along the Gascoyne
region can be offset by these equatorward countercurrents, although we hypothesize that
*Published as: Hanson, C.E., Pattiaratchi, C.B. and Waite, A.M. Sporadic upwelling on a downwelling coast: phytoplankton responses to spatially variable nutrient dynamics off the Gascoyne region of Western Australia. Continental Shelf Research, in press.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
38
the biological impact of any upwelling on the inner shelf will be a function of: (a) the
depth of the LC’s mixed layer; (b) the strength and duration of upwelling-favourable
winds (i.e. the intensity of upwelling); and, (c) geographical location, primarily with
respect to the width of the continental shelf and resultant proximity of upwelling flows
to deep nutrient pools.
3.2 Introduction
Eastern boundary currents are present in all of the major ocean basins, and generally
consist of an equatorward surface flow accompanied by large-scale upwelling, high
rates of primary production and abundant fisheries (Wooster and Reid, 1963; Mann and
Lazier, 1996). Off the coast of Western Australia (WA), the unusual poleward-flowing
Leeuwin Current (LC) restricts the eastern arm of the Indian Ocean gyre to offshore
regions, generating large-scale downwelling as it travels along the continental shelf
break (Pearce, 1991; Smith et al., 1991). The LC is known to reduce coastal nutrient
levels (Pearce et al., 1992; Johannes et al., 1994), influence marine species distributions
(Morgan and Wells, 1991) and limit productivity at higher trophic levels (Lenanton et
al., 1991; Caputi et al., 1996). As opposed to the dominance of pelagic finfish stocks in
other eastern boundary regions, the major fishery off WA is the benthic rock lobster,
with its life cycle and recruitment strongly tied to the dynamics of the LC (Phillips et
al., 1991).
Inshore of the Leeuwin Current, a system of equatorward coastal countercurrents
is driven by upwelling-favourable southerly winds which prevail during the austral
summer (December to March). Part of that system, the Capes Current (CC) extends
along the southwest coast of WA (Pearce and Pattiaratchi, 1999) while the Ningaloo
Current (NC) extends along the northwest coast (Taylor and Pearce, 1999). The
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
39
combination of these wind-forced shelf currents and localized Ekman-driven upwelling
(Gersbach et al., 1999; Woo et al., 2004) seasonally restricts the inshore extent of the
LC (Pearce and Pattiaratchi, 1999; Taylor and Pearce, 1999).
The Gascoyne continental shelf extends from North West Cape (21.3S) to
Shark Bay (26.5S), Western Australia (Fig. 3.1), and encompasses the northern portion
of LC waters. Control of phytoplankton production in coastal regions such as the
Gascoyne is often closely tied to ambient nutrient levels, which in turn are strongly
influenced by the local oceanography (Denman and Gargett, 1995; Mann and Lazier,
1996). In such a physically dynamic area, both vertical mixing (induced through wind
mixing and upwelling processes) and advective transport (via the Leeuwin, Ningaloo
and Capes Currents) may influence phytoplankton distributions and primary production.
Vertical mixing not only impacts nutrient concentrations within the euphotic zone, but
also controls photosynthetic responses through exposure to different light gradients
(Demers et al., 1986; Delgadillo-Hinojosa et al., 1997). Lateral transport can disperse
phytoplankton from productive frontal regions (Daly et al., 2001), export significant
amounts of phytoplankton carbon from the continental shelf to offshore waters (Yoder
and Ishimaru, 1989), and generate phytoplankton patchiness (Martin, 2003).
Along the west coast of WA, the nutrient-poor LC is thought to support only a
limited amount of phytoplankton biomass and productivity, leading to oligotrophic
conditions (Pearce, 1991). However, both phytoplankton biomass and primary
production data in the Gascoyne region are sparse. Historical chlorophyll a estimates,
sourced from the International Indian Ocean Expedition (IIOE; 1959 – 1965), give an
annual range of 5 to 20 mg chl a m-2 (recalculated from Humphrey, 1966 as per
Humphrey, 1978) in an irregularly sampled 5 latitude/longitude grid off the Gascoyne
coast. Limited primary productivity data (also sourced from the IIOE) indicates levels
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
40
Figure 3.1. Eleven cross-shore transects undertaken along the Gascoyne continental
shelf, Western Australia in November 2000; CTD casts and water sampling were
completed at all stations, while 14C uptake experiments were performed at production
stations only (marked by filled circles and station numbers).
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
41
of 100 – 250 mg C m-2 d-1 (Koblentz-Mishke et al., 1970; FAO, 1981), although these
measurements were restricted to 110E (Jitts, 1969), approximately 400 km offshore
and well outside Leeuwin Current and coastal countercurrent waters. To date, a lack of
research effort along the Gascoyne continental shelf has limited regional estimates of
phytoplankton biomass and productivity. The importance of such measurements are
highlighted by recent studies of Leeuwin Current influence on rock lobster recruitment,
which note that the mechanisms behind the relationship between LC flow and
recruitment strength are unclear (Caputi et al., 2001), and that variations in levels of
primary production may be a major factor (Griffin et al., 2001).
The aim of this chapter is therefore to identify how the Leeuwin, Ningaloo and
Capes Currents influence phytoplankton dynamics (biomass levels and distribution,
rates of primary production, species composition) along the Gascoyne shelf. The
dominance of the LC in the region has led to the paradigm that conditions remain
oligotrophic along this coast through suppression of upwelling-driven production. We
investigated this theory using field data from the northern portion of the LC and
associated coastal countercurrents.
3.3 Materials and Methods
An oceanographic cruise was undertaken off Western Australia from 13 to 27
November 2000 (early austral summer) aboard the Australian National Facility RV
Franklin (voyage FR10/00), incorporating eleven onshore/offshore transects (A to J)
and a total of 118 stations (Fig. 3.1). The study region was located between North West
Cape and the Abrolhos Islands (ca. 21S to 30 S; Fig. 3.1), and encompassed the
Gascoyne continental shelf (0 – 200 m), shelf break (200 – 300 m) and offshore (300 –
4000 m) waters.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
42
3.3.1 Oceanographic sampling and laboratory analyses
Water samples were obtained using 24 General Oceanics 5 L Niskin bottles mounted on
a rosette equipped with Seabird Conductivity-Temperature-Depth (CTD) profiler,
dissolved oxygen sensor, fluorometer and Li-Cor LI-192SA underwater quantum
sensor. Between three and thirteen discrete depths were sampled at each station
(dependent on bottom depth) including surface (roughly 2 m), and above, below and
within the fluorescence maximum (as determined by the downcast fluorometer trace).
Dissolved inorganic nutrients (nitrate + nitrite, phosphate and silicate) were analyzed
for all depths (996 samples) using a shipboard Autoanalyzer. Detection limits were 0.1
M for nitrate + nitrite (hereafter nitrate), 0.01 M for phosphate and 0.1 M for
silicate (Cowley, 1999). Over 500 two-litre water samples for chlorophyll (chl) a and
pheopigments were filtered onto Whatman GF/F filters, stored at 20C and returned to
the laboratory for analysis. Pigments were extracted in 90 % acetone with grinding, and
measured using a Turner Designs Fluorometer (detection limit of 0.01 mg chl a m-3)
following the acidification technique of Parsons et al. (1989).
At 18 ‘production stations’ (chosen to give good coverage of the sampling
region without a priori knowledge of the locations of the different water masses),
primary productivity versus irradiance (P vs. I) experiments were performed using the
small-volume (7 mL) 14C incorporation technique (Lewis and Smith, 1983), with
modifications and photosynthetron equipment as per Mackey et al. (1995, 1997a). Due
to the opportunistic nature of the biological sampling program, water from some
stations was collected at night and held in the dark at ambient seawater temperature
until processing at dawn the following morning. Each water sample (a total of 64 for
the cruise) was inoculated with 14C to a final concentration of 1.0 Ci per 1.0 mL
seawater, and triplicate aliquots from each sampling depth were incubated for ca. 2 to 3
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
43
hours at six main light levels (plus dark), achieved using different combinations of
neutral density and spectrally-resolving blue filters. However within each light level the
triplicates were exposed to slightly different irradiance levels by using variable
thicknesses of filter. This resulted in up to 18 different light levels (plus dark) per
experiment. Total initial activity was determined using two 100 L aliquots from each
depth, with duplicate 7mL time zeros also completed (Mackey et al., 1995). For the
first six experiments, irradiance levels within the photosynthetron (maximum of 400
E m-2 s-1) were too low to reach the maximum photosynthetic rate for shallow-water
(< 50 m) samples (hereafter referred to as UNSAT experiments). From the seventh
production station onwards, additional incubations of the surface and next-deepest
sample were conducted in natural sunlight (hereafter referred to as SAT experiments) at
two light levels (100% and 30% of incident irradiance). Incubations were completed by
adding 0.25 mL of 6M HCl, and placing the samples in an orbital shaker at 180 revs per
minute for 2 hours (Mackey et al., 1995). All samples were counted on-board the ship
using a LKB Rackbeta liquid scintillation counter.
Phytoplankton taxonomy was also assessed at production stations, with 100 mL
seawater samples collected from surface waters (~ 2 m) and preserved with acid Lugol’s
solution (Parsons et al., 1989). The entire sample was sedimented and enumerated
using an inverted microscope (Utermöhl, 1958), with identification to species level
where possible. For data analysis purposes, the following standard groupings are used:
flagellates (< 20 m), pennate diatoms, centric diatoms, dinoflagellates,
coccolithophores, and ‘other’ (consisting of chrysophytes, prasinophytes,
prymnesiophytes, silicoflagellates, cryptophytes and filamentous cyanobacteria). Note
that coccolithophore abundance may have been underestimated due to the use of an
acidic preservative (Sournia, 1978).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
44
3.3.2 Data processing and production calculations
The upper limit of the nitracline was defined as the depth where the nitrate
concentration equalled 0.2 M, as linearly interpolated between water sampling depths.
In these extremely oligotrophic waters, this value was considered more representative of
the nitracline than the criteria of 1.0 M commonly used for other regions (e.g. Cullen
and Eppley, 1981; Maranon and Holligan, 1999).
In situ fluorescence was calibrated with extracted chl a data using linear
regression, and used as a proxy for phytoplankton biomass. Where data permitted
(minimum of 5 data points), a separate regression was performed for each station;
otherwise, stations were calibrated using pooled data for that transect (r2 = 0.76-0.92).
The deep chlorophyll maximum (DCM) was taken as the depth of maximum subsurface
chl a concentration. Contour plots of both nutrient and chl a data were generated in
Matlab using linear interpolation.
Non-linear curve fitting of P vs. I data was performed in SigmaPlot to estimate
photosynthetic parameters according to the equation of Platt et al. (1980):
P = Ps(1-e-I/Ps)e-I/Ps (3.1)
where P = photosynthetic rate (mg C m-3 h-1), Ps = maximum, potential light-saturated
photosynthetic rate under conditions of no photoinhibition (mg C m-3 h-1), = initial
slope (mg C mg chl a-1 h-1[mol m-2 s-1]-1), = photoinhibition parameter
(mg C mg chl a-1 h-1 [mol m-2 s-1]-1) and I = irradiance (mol m-2 s-1). Ps is calculated
as:
m
sP
P(3.2)
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
45
where Pm = maximum photosynthetic rate (mg C m-3 h-1). If no photoinhibition is
observed (i.e. = 0), Equation 3.1 collapses to:
P = Pm(1-e-I/Pm) (3.3)
Computations of daily rates of primary production were performed as in Mackey et al.
(1995) and Walsby (1997). Chlorophyll-normalized photosynthetic parameters (Pm* or
Ps*, * and *) were linearly interpolated between sample depths. Calibrated
fluorescence was used to scale these parameters at 2 m depth intervals, and production
(P) was calculated using Equation 3.1. Daily rates were computed using both actual
irradiance data (recorded in air at five minute intervals by a deck-board Li-Cor LI-
192SB Quantum Sensor) and theoretical sine curves of irradiance (based on latitude and
date). Irradiance in air was corrected for water reflectance to obtain irradiance below
surface by incorporating solar elevation, effective zenith angle and surface wind
roughening (from five minute wind averages; Walsby, 1997).
The vertical light profile was obtained using attenuation coefficients (Kd)
calculated from field data through a linear regression of the natural log of PAR
(photosynthetically available radiation) vs. depth, according to the relation:
ln Ed(0) = -Kdz + ln Ed(z), where Ed(0) and Ed(z) are the values of downwelling PAR at
the surface and at z m, respectively (Kirk, 1994). A smoothed irradiance profile was
then used to determine the depth of the euphotic zone. Attenuation coefficients used for
production calculations were those measured at each station, although if the data did not
exist the mean value of Kd for the study area was used.
The double integral of photosynthesis through depth and time (mg C m-2 d-1)
was computed using trapezoidal integration (Walsby, 1997). These calculations provide
only an estimate of daily gross production, as no attempt was made to correct for carbon
losses via respiration. All depth integrations (for primary production, chl a and
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
46
nutrients) were to the 0.1% light level, or sea bottom if shallower. As sampling was
undertaken with standard uncoated hydrowire and General Oceanics Niskin bottles that
had not been fitted with silicone tubing and o-rings, we must assume that photosynthetic
rates were potentially underestimated due to contamination effects (Marra and
Heinemann, 1987; Williams and Robertson, 1989). Using similar methodologies as the
present study, Mackey et al. (1995) found that depth-integrated productivity was
underestimated by up to 50%. It is reasonable to consider that a similar effect may have
occurred with our results, although of course while the absolute production values may
have been underestimated, any identified differences in productivity between regions
should remain valid.
In the case of UNSAT experiments, Pm was taken as the maximum
photosynthetic rate achieved in the photosynthetron (at ~ 400 E m-2 s-1), providing a
conservative estimate of this parameter. These UNSAT experiments were consequently
without a measure of the photoinhibition parameter (). In the case of SAT
experiments, surface samples did not display photoinhibition, as is common for
phytoplankton adapted to high light conditions (e.g. Kana and Glibert, 1987; Maranon
and Holligan, 1999; Basterretxea and Aristegui, 2000; Moran and Estrada, 2001).
Samples associated with the DCM did exhibit photoinhibition, but because light levels
at these depths were below the inhibition threshold, this was of little importance when
calculating in situ production. Thus, for UNSAT experiments we have assumed that
= 0. The implications of that assumption are addressed in Chapter 4.
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
47
3.4 Results
3.4.1 Physical water types
To facilitate the interpretation of geographical patterns, CTD and production stations
were grouped into water types based on temperature-salinity (TS) characteristics,
Acoustic Doppler Current Profiler (ADCP) data and sea-surface temperature (SST)
images (Woo et al., 2004). Stations from the Leeuwin Current, offshore waters and
three shelf water types were classified as follows (Fig. 3.2): (1) Leeuwin
Current/offshore waters (LC); (2) Ningaloo Current water (NC); (3) Shark Bay outflow
(SB); and, (4) Capes Current water (CC). The 18 production stations sampled each of
these four water types (Fig. 3.3).
Leeuwin Current (LC) and offshore waters were characterised (Fig. 3.3a) by
warmer and less saline water to the north of the study area (Stn 52), and a general
cooling and increase in salinity towards the south (Stn 132). The Leeuwin Current is
driven by an alongshore pressure gradient which results in entrainment of offshore
waters into the LC through geostrophic inflow (Smith et al., 1991; Woo et al., 2004).
Meuleners et al. (2003) estimated that, within the study region, up to 40 % of the total
flow of the LC could be derived from geostrophic inflow of offshore waters,
representing Indian Ocean central water that is colder and more saline than LC source
waters. However, on each transect, LC and offshore waters were characterised by
warmer and less saline waters when compared to the shelf waters, which allowed
identification of the water types. For example, along Transect D the inshore station (Stn
42, T = 22.67C, S = 35.02) was cooler and more saline than the offshore station (Stn
52, T = 23.77C, S = 34.75). Similarly, along Transects H and J, the inshore stations
(Stn 90, T = 21.57C, S = 35.20 and Stn 120, T = 21.29C, S = 35.52) were cooler and
more saline than the offshore stations (Stn 101, T = 22.60C, S = 35.05 and Stn 131,
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
48
Figure 3.2. The generalized surface circulation patterns encountered during the field
study, including a detailed view of flow dynamics along Cape Range Pensinsula
(adapted from Woo et al., 2004); numbers as per text description in Results and
Discussion.
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
49
Figure 3.3. Mean temperature-salinity (TS) values (calculated for the top 40 m of the
water column) for production stations (a) within Leeuwin Current and offshore waters,
and (b) within Ningaloo Current, Shark Bay outflow and Capes Current waters. TS
values are indicated by the respective station numbers, except for stations 65, 101 and
112, which are indicated by black dots due to their close proximity.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
50
T = 21.80C, S = 35.18). Thus, it was possible to identify each of the four distinct
water types found within the study area through their TS characteristics (similar to Woo
et al., 2004).
The Ningaloo Current (NC) water type (Fig. 3.3b) represents all of the shelf
stations on Transects A to E (Fig. 3.1), and is characterised by warmer and less saline
water compared to other shelf water types. Woo et al. (2004) attributed the NC water
type as resulting from re-circulation of LC water northward (Fig. 3.2), augmented by
wind-driven upwelling of cooler, more saline water. The Shark Bay (SB) water type
(Fig. 3.3b) was present in the vicinity of Shark Bay, a semi-enclosed coastal embayment
characterised by higher salinity due to high evaporation and minimal terrestrial runoff.
The shelf stations on Transects F to I consisted of higher salinity water derived through
the mixing of the high salinity outflow from Shark Bay with the shelf waters. The
Capes Current (CC) water type (Fig. 3.3b) was found in the shelf waters on Transect J.
The cooler, higher salinity (S = 35.52) water present on this transect was considered to
originate from upwelling and advection into the study area through the northward
flowing Capes Current (Woo et al., 2004).
3.4.2 Phytoplankton biomass and nutrients
A common feature throughout much of the study area was higher chl a concentration at
depth, either near the seabed or as distinct peaks within the water column. The deep
chlorophyll maximum (DCM) was generally deeper offshore compared to onshore (as
the onshore stations were limited by water depth), with highest chl a concentrations
found near the seabed in shelf waters (Fig. 3.4b). Concurrent measurements of nitrate
showed low concentrations (< 0.5 M) in both the inner shelf region and in surface
(< 50 m) waters across each transect (Fig. 3.4a), with some exceptions in the northern
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
51
portion of the study area. At North West Cape (Fig. 3.4a, Transect A), nitrate reached
2.5 M in surface (< 50 m) waters, and > 5.0 M towards the base of the euphotic zone
(~ 100 m), with a maximum of 6.4 M at 70 m. In the nearshore region along Cape
Range Peninsula (Fig. 3.4a, Transect C) and at the shelf break south of Point Cloates
(Fig. 3.4a, Transect D), nitrate measured up to 1.5 M in surface waters (< 60 m).
The persistence of the DCM in the alongshore direction was observed in both
shelf (50 m isobath; Fig. 3.5a) and offshore (1000 m isobath; Fig. 3.5b) regions.
Ningaloo Current waters (Transects A to E; Fig. 3.5a) were associated with relatively
shallow chlorophyll maxima, with a distinct surface chlorophyll signature also evident
in offshore waters at Transects B and C (Fig. 3.5b) due to an offshoot of the Ningaloo
Current (Fig. 3.2). Maximum chl a for the study region was located along the inshore
edge (55 to 75 m isobath) of Transect F, where a near-bed plume of hypersaline Shark
Bay outflow contained up to 2.4 mg chl a m-3 (Fig. 3.5a). Excluding this unusual
feature, Gascoyne shelf waters were generally characterized by a maximum
concentration of 1.0 mg chl a m-3. DCMs were quite distinct in offshore (300 – 1000 m
isobath) waters south of Point Cloates, where near surface (< 50 m) biomass was
extremely low (< 0.1 mg chl a m-3; Fig. 3.4b, Transects D, H and J). Individual vertical
profiles of chl a illustrate the variability of the biomass profile within both inshore (0 –
200 m) and shelf break/offshore (250 – 1000 m) regions (Fig. 3.6).
Depth-integrated chl a ranged from 4.4 mg chl a m-2 (inshore station on
Transect F; Fig. 3.1) to 59.3 mg chl a m-2 (mid-shelf station on Transect A; Fig. 3.1),
with a mean of 25.4 11.6 s.d. (n = 110). Peak concentrations for the study area
(~ 45 – 60 mg m-2) were located along Cape Range Peninsula (Fig. 3.7a). South of
Point Cloates, maximum chl a (up to 45 mg m-2) was generally found along, or inshore
of, the 200 m shelf break (Fig. 3.7a). Mean depth-integrated chl a was found to
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
52
(a)
Figure 3.4. Cross-shelf contours of (a) nitrate (M) and (b) chl a (mg m-3) for five
transects representative of the different water types and conditions within the study
region. Black dots in (a) indicate water sampling depths, and triangles in (b) indicate
station locations. Note that the scaling on the x-axis for Transect C is twice that of the
other plots.
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
53
(b)
Figure 3.4. Cont’d.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
54
Figure 3.5. Alongshore chl a contours from north (left) to south (right) through the
study area for the (a) 50 m isobath, and (b) 1000 m isobath. Station locations are
indicated by triangle markers and transect letters.
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
55
be significantly higher in NC waters than LC/offshore and SB regions (Kruskal-Wallis
ANOVA by ranks and posthoc comparison, p < 0.05; Table 3.1).
Depth-integrated nitrate exhibited a very large range (< 0.1 to 225 mmol NO3-
m-2) and distinctive spatial patterns (Fig. 3.7b). Maximum concentrations (175 – 225
mmol m-2) were located off North West Cape, with isolated patches of > 100 mmol m-2
found just south of Point Cloates and at the 1000 m isobath off Shark Bay (Fig. 3.7b).
South of Point Cloates, the shelf was generally nitrate-depleted, with the exception of a
patch of nitrate south of Shark Bay (Fig. 3.7b; note co-occurence with chl a patch in
Fig. 3.7a). Ningaloo Current waters had significantly higher depth-integrated nitrate
than SB outflow (Kruskal-Wallis and posthoc comparison, p < 0.01; Table 3.1), but
were not found to be significantly different than LC waters. In the LC/offshore region,
the majority of this nitrate was sequestered at the base of the euphotic zone, with the
nitracline 70 m in depth (Fig. 3.8a,b). In contrast, high concentrations of nitrate were
found within the upper euphotic zone of NC waters, with the nitracline often 50 m in
depth (Fig. 3.8d,e). Phosphate displayed the same general trends as nitrate, and is not
shown.
For silicate, the Capes Current water type was found to have a significantly
lower mean concentration (1.6 M) within the euphotic zone than all other shelf
( 200 m isobath) water types (2.7 – 2.8 M; Kruskal-Wallis H (3,325), p < 0.001,
multiple comparisons CC < NC, LC, SB at p < 0.001; Fig. 3.9). A significant difference
was also found between inner shelf LC and NC silicate levels (LC < NC, multiple
comparisons, p < 0.05; Fig. 3.9).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
56
Figure 3.6. Vertical chl a profiles (mg chl a m-3) for (a)-(d) continental shelf (0 - 200 m
isobath) and (e)-(h) shelf break and offshore (250 – 1000 m) regions for four
representative transects.
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
57
3.4.3 Production stations
Areal production over the entire region was variable, ranging from 110 to 1310
mg C m-2 d-1 (Table 3.2) with a mean s.d. of 560 420 mg C m-2 d-1 (n = 18). The
values presented are for theoretical ‘cloudless’ irradiance based on latitude and date
(Kirk, 1994; Walsby, 1997), which allowed a spatial comparison regardless of cloud
conditions. Integrated productivity calculated from actual (cloud-affected) irradiance
measured on deck ranged from 90 to 1120 mg C m-2 d-1 with a mean s.d. of 480 370
mg C m-2 d-1, which is ~ 14 % lower than that calculated from theoretical irradiance.
Depth-integrated primary production was found to vary geographically, primarily
according to water type (Fig. 3.10). The most productive waters were found: (1) in a
coherent grouping along Cape Range Peninsula and just south of Point Cloates (NC
water; 840 – 1310 mg C m-2 d-1), and (2) in a single highly productive (990
mg C m-2 d-1) inner shelf station at the southernmost extent of the study area (CC water;
Fig. 3.10 and Table 3.2). The majority of Leeuwin Current/offshore waters had
productivity 200 mg C m-2 d-1 (range 110 – 530 mg C m-2 d-1; Fig. 3.10 and Table
3.2). The production station with 530 mg C m-2 d-1 was the only measurement of
primary production in the LC’s core (Stn 112, at the 250 m isobath on Transect I); all
other LC/offshore stations were 1000 m depth. Shark Bay outflow was characterized
by integrated productivity between 550 and 560 mg C m-2 d-1 (Fig. 3.10). Grouped
together, shelf/countercurrent waters (NC, SB, CC) were significantly more productive
(Mann-Whitney test, p < 0.001) than Leeuwin Current/offshore regions.
Ocean colour satellite imagery (Fig. 3.11; valid for ‘Case 1’ waters deeper than
30 m) obtained on 21 November 2000 (close to the mid-point of the sampling program
and coincident with Transects E and F) allowed an evaluation of whether regions of
high primary productivity were also regions of high surface phytoplankton biomass.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
58
(a)
Figure 3.7. Contours of (a) depth-integrated chl a (mg m-2), and (b) depth-integrated
nitrate (mmol m-2) through the study region, with an offshore limit of 1000 m.
Integrations were to the 0.1 % light level or seabed; stations are indicated by black dots.
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
59
(b)
Figure 3.7. Cont’d.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
60
Table 3.1. Mean ( s.d.) depth-integrated chl a (mg m-2; n1) and nitrate (mM m-2; n2)
within each of the four water types (LC: Leeuwin Current; NC: Ningaloo Current;
SB: Shark Bay outflow; CC: Capes Current). Kruskal-Wallis (K-W) ANOVA by ranks
and nonparametric posthoc multiple comparisons (Siegel and Castellan, 1988) were
used to assess the statistical significance of differences between water types (note: CC
not included in analysis due to small sample size).
Water type LC
n1 = 52 n2 = 53
NC n1 = 28 n2 = 27
SB n1 = 14 n2 = 17
CC n1 = 4 n2 = 4
K-W Multiple comparisons
(p 0.05)
Chl a 21.4 (6.9) 35.9 (11.6) 24.0 (10.8) 13.6 (3.9) p < 0.001 NC>LC=SB
NO3- 33.2 (40.1) 41.9 (35.9) 13.0 (18.4) 0.9 (0.2) p < 0.01 NC=LC>SB
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
61
Figure 3.8. Vertical profiles of primary production (mg C m-3 d-1), chl a (mg m-3),
nitrate (M) and density (t) and for stations representative of (a)-(c) Leeuwin
Current/offshore, (d)-(f) Ningaloo Current, (g)-(h) Shark Bay outflow, and (i) Capes
Current water types. Note that the production axis for Leeuwin Current/offshore
stations is twice the scale of the other water types.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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Leeuwin Current/offshore waters featured the lowest surface chl a concentrations, while
the more productive shelf waters were associated with higher chl a. However, the
highly productive Cape Range Peninsula area (Transects B and C) was poorly indicated
by surface ocean colour. Imagery from one week later (28 November 2000; Fig. 3.11
inset) showed both a large chlorophyll plume off the Peninsula, and relatively higher
chl a levels along the northern Gascoyne shelf.
Vertical profiles of primary production, chl a, nitrate and density indicate
variation both between, and within, water types (Fig. 3.8). Leeuwin Current/offshore
waters were characterised by well-defined deep chlorophyll maxima located near the
nitracline (Fig. 3.8a-c). These DCMs were often (~ 60 % of stations) associated with
deep peaks in productivity, although maximum production rates were generally found in
near-surface waters. Station 112 (from the shelf break on Transect I; Fig. 3.1) had the
shallowest nitracline (69 m) of all LC/offshore production stations (Fig. 3.8c).
The water column was fairly well-mixed at NC production stations, and chlorophyll
profiles had less distinct subsurface peaks than in LC/offshore regions (Fig. 3.8e,f).
Station 15 (on Transect A off North West Cape) was an exception, with a shallow
pycnocline and marked DCM above the seabed. In NC waters along Cape Range
Peninsula, elevated nitrate levels were often found throughout the water column (Fig.
3.8d,e), although inshore waters south of Point Cloates were generally nitrate depleted
(Fig. 8f). NC production rates peaked in surface (< 20 m) waters (Fig. 3.8e,f), with the
exception of Stn 15 (Fig. 3.8d).
In the shallow SB outflow, chl a was maximal just above the seabed (Fig.
3.8g,h). In the northern SB production station (Stn 90; Fig. 3.8g), productivity peaked
at depth (coincident with nitrate concentrations), while at the southern station (Stn 106;
Fig. 3.8h) production was fairly uniform through the nitrate-depleted water column. In
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
63
Figure 3.9. Mean ( 95 % C.I.) silicate concentration (M) within the euphotic zone
(to 0.1 % light level or seabed) for shelf ( 200 m isobath) waters associated with the
Ningaloo Current (NC; n = 109), Leeuwin Current (LC; n = 94), Shark Bay outflow
(SB; n = 101) and Capes Current (CC; n = 21).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
64
Table 3.2. Depth-integrated biomass and primary production for stations within each of
the four water types: Ningaloo Current (NC), Leeuwin Current/offshore (LC), Shark
Bay outflow (SB), and Capes Current (CC). Integration depth represents 0.1 % light
level or seabed.
Water type
Stn
Max depth (m)
Integration depth (m)
Biomass (mg chl a m-2)
Primary prod’n (mg C m-2 d-1)
NC 15 48 48 17.5 1090 NC 28 250 104 46.1 1310 NC 33 72 72 42.8 1050 NC 40 990 104 37.1 840 NC 42 56 56 23.6 900 NC 62 96 96 35.7 1050
LC 52 2050 104 15.0 190 LC 55 1000 104 17.4 140 LC 65 1000 104 23.8 110 LC 101 1000 104 16.1 200 LC 112 260 104 38.6 530 LC 116 1000 90 14.6 175 LC 119 4020 104 9.1 120 LC 131 1000 104 19.6 170 LC 132 3100 104 13.9 170
SB 90 32 32 10.9 550 SB 106 54 54 13.9 560
CC 120 40 40 13.3 990
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
65
Figure 3.10. Schematic of the geographical groupings of production stations as derived
from TS relationships, ADCP and SST data (Woo et al., 2004), with bars indicating
depth-integrated primary production (mg C m-2 d-1); see Table 3.2 for specific values.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
66
Figure 3.11. Ocean colour imagery (SeaWiFS) from 21 November 2000, overlaid with
transects and the location of production stations (open circles). Inset: Partial SeaWiFS
image from 28 November 2000, showing high chlorophyll a levels on the northern
Gascoyne shelf and in a plume off Cape Range Peninsula.
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
67
the well-mixed CC waters, chl a and nitrate (maximum of 0.1 M) peaks were found
just above the seabed, while production gradually decreased with depth (Fig. 3.8i).
Production stations within all water types were dominated by flagellates
(contributing 47 – 64 % to total counts, or 28 – 95 × 106 cells m-3), with the exception of
Capes Current waters, where the principal taxa (54 %) were centric diatoms (Fig. 3.12).
In all cases, diatoms (centric + pennate) were numerically dominant over
dinoflagellates, although in Leeuwin Current and Shark Bay waters, pennate diatoms
were more numerous than centric species (Fig. 3.12). Relatively high percentages of
coccolithophores were noted in CC and SB surface waters (16 and 13 %, respectively).
The highest mean cell counts (1480 105 cells m-3) were found in Ningaloo Current
waters (Fig. 3.12).
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Figure 3.12. Mean cell counts ( 105 cells m-3; in parentheses) and percent abundance
(pie charts) of phytoplankton taxa in surface (~ 2 m) waters of production stations
within each of the four main water types (NC: Ningaloo Current waters; LC: Leeuwin
Current/offshore waters; SB: Shark Bay outflow; CC: Capes Current waters).
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
69
3.5 Discussion
In this early summer field study, the Gascoyne continental shelf was found to be a
region of dynamic physical oceanographic processes, a detailed description of which is
presented in Woo et al. (2004) and summarized in Figure 3.2. The key features include:
(1) the southward-flowing Leeuwin Current (LC), generally centred along the shelf
break (~ 200 m isobath) and associated with downwelling south of Point Cloates;
(2) the Ningaloo Current (NC), (a) sourced from re-circulated LC waters south of
Point Cloates, and (b) augmented by upwelling (with a contribution from colder
water below the LC) and mixing with LC waters via coastal offshoots along Cape
Range Peninsula;
(3) hypersaline Shark Bay (SB) outflow, which mixed with LC water and formed a
distinctive water mass that flowed poleward from Shark Bay; and,
(4) the northern extension of the Capes Current (CC), encountered on the inner shelf
at the southern limit of the study region (Fig. 3.2).
The following discussion investigates how the processes summarized above directly
affect phytoplankton biomass distributions, rates of primary production and species
composition. First, we compare our biomass estimates and production rates with
historical values and those from other regions, and second we elucidate regional
patterns in the coupling of physical and biological processes along the Gascoyne shelf.
We then consider the implications of our findings for higher trophic levels.
3.5.1 Biomass and production rates in context
This study provides a much more detailed spatial examination of phytoplankton
biomass and primary production than has previously been undertaken along the
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
70
Gascoyne continental shelf, and updates historical estimates for the region. The
majority of Leeuwin Current and offshore stations had productivity levels below 200
mg C m-2 d-1, similar to waters of the Coral Sea (Furnas and Mitchell, 1996), the eastern
Mediterranean (Ignatiades et al., 2002) and the North Pacific gyre (Hayward et al.,
1983); this eastern boundary current was therefore strongly oligotrophic (defined as
< 270 mg C m-2 d-1; Nixon, 1995). Average LC/offshore phytoplankton biomass (~ 21
mg chl a m-2) was also characteristic of low productivity oceanic waters of the Indian,
Pacific and Atlantic Oceans (~ 20 – 28 mg chl a m-2; Humphrey and Kerr, 1969;
Dandonneau and Lemasson, 1987; Maranon et al., 2000). Historical values for the
Gascoyne region (~ 5 – 20 mg chl a m-2 and 100 – 250 mg C m-2 d-1; Humphrey, 1966
and Koblentz-Mishke et al., 1970) are mainly indicative of offshore waters due to
inadequate coverage of the continental shelf region, and are thus comparable to the
majority of our LC/offshore measurements.
Primary production rates in coastal countercurrent waters (Ningaloo and Capes
Currents) ranged from 840 – 1310 mg C m-2 d-1. Such levels of production are
regionally significant for the Gascoyne region, although are at the lower end of
estimates found in other upwelling-influenced zones off California (500 to 2600
mg C m-2 d-1; Pilskaln et al., 1996), NW Spain (400 to 3700 mg C m-2 d-1; Tilstone et
al., 1999), and southern Africa (1000 to 3500 mg C m-2 d-1; Brown and Field, 1986,
Estrada and Marrase, 1987, Brown et al., 1991). Phytoplankton biomass in such
upwelling regions can reach ca. 120 to 180 mg chl a m-2 (Brown and Field, 1986;
Basterretxea and Aristegui, 2000). In comparison, the maximum depth-integrated chl a
in our study was about half this amount (59 mg chl a m-2), and associated with the
upwelling-influenced Ningaloo Current water off North West Cape. Thus, although the
equatorward summer countercurrents can offset the regional dominance of the Leeuwin
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
71
Current along the Gascoyne coast (with production levels up to five times greater than
historical estimates for the area), their productivity is considerably less than upwelling
regimes along other eastern ocean boundaries.
3.5.2 Regional patterns in coupled physical-biological processes
The Leeuwin Current is a well-documented feature of the west coast of WA (Pearce,
1991; Woo et al., 2004), and nitrate and phosphate concentrations in the mixed layer of
the LC are known to be < 0.2 M (Pearce et al., 1992), similar to offshore surface
waters of the Indian Ocean (Rochford, 1980). The nutricline at the base of the LC can
be between 70 and 200 m deep (Pearce et al., 1992; Pearce, 1997), and the prevalence
of downwelling along the coast of WA is thought to prevent deep nutrient
concentrations from reaching surface waters (Pearce, 1991).
However, in the early summer of 2000, both localized upwelling and mixing
associated with seaward offshoots along Cape Range Peninsula resulted in high nitrate
concentrations in the euphotic zone. These nutrients were most likely sourced from the
nutricline at the base of the Leeuwin Current, given the close proximity of NC and LC
waters along the peninsula (Woo et al., 2004). This region has both the narrowest shelf
(6 – 17 km) and steepest shelf break found in any part of the study area, and this
bathymetry is critical in bringing the opposing flows in close contact with each other
and enhancing mixing (Woo et al., 2004). Maximum nitrate levels within the euphotic
zone reached approximately 2 – 6 M along Cape Range Peninsula, and appeared to be
advected southwards by the Leeuwin Current along the shelf break past Point Cloates,
This input of ‘new’ nitrogen was linked with substantial carbon uptake rates (840 to
1310 mg C m-2 d-1) and high phytoplankton cell counts. But overall nutrient enrichment
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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levels, and consequent primary productivity, are likely capped in this region by the
presence of the Leeuwin Current.
The depth of the LC’s nutrient-depleted mixed layer governs nutrient
concentrations within upwelled water, as suggested by Gersbach et al. (1999) in relation
to Capes Current upwelling off southwestern WA. In that case, upwelled water from
the base of the LC contained 0.4 M nitrate (Gersbach et al., 1999). This is an order of
magnitude less than our observations off northwestern WA, and indicates the potential
variability of the upwelling response associated with these equatorward countercurrents.
The strength and position of the Leeuwin Current, and the depth of its mixed layer,
varies both spatially (Smith et al., 1991) and temporally (Godfrey and Ridgway, 1985;
Pearce and Phillips, 1988) along the west coast of WA. Interannually, flow is weakened
during ENSO (El Niño/Southern Oscillation) years, when the north-south geopotential
anomaly (the driving force for the Leeuwin Current) is reduced (Pearce and Phillips,
1988; Pattiaratchi and Buchan, 1991; Feng et al., 2003). Conditions of weakened flow
may result in shoaling of the LC’s nutricline, allowing wind induced upwelling to
access higher nutrient concentrations, and also lessen the force opposing the northward
flowing countercurrents. The biological impact of any upwelling in this region is thus
expected to be a function of: (a) conditions within the Leeuwin Current, (b) the strength
and duration of upwelling-favourable winds (i.e. the intensity of upwelling), and (c)
geographical location, primarily with respect to the width of the continental shelf and
resultant proximity of upwelling flows to deep nutrient pools.
In contrast to the active upwelling and mixing processes identified at North West
Cape, the northward-flowing Capes Current water type (located on the inner shelf at the
southern extent of the study area) was postulated to consist of previously upwelled
water advected from beyond the study region (Woo et al., 2004). The low nitrate/high
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
73
productivity signature associated with this flow is consistent with an aging upwelled
water mass (Dugdale et al., 1990). This case is also supported by our observations of
low silicate levels and a high proportion of centric diatoms within Capes Current
surface waters (Kudela et al., 1997; Tilstone et al., 2000). Carbon uptake rates in
upwelling zones are known to peak a number of days after nitrate enrichment occurs
(Kudela et al., 1997), given the physiological time lag between nitrate uptake and
utilization by phytoplankton (Collos and Slawyk, 1980). Intracellular storage of nitrate
can occur in marine microalgae and may, under some conditions, provide a buffer
during low-nitrate conditions (Bode et al., 1997). However, of much greater importance
during the later stages of upwelling events is the shift from ‘new’ to ‘regenerated’ forms
of nitrogen (Dugdale and Goering, 1967), as seen in the upwelling regions off Spain
(Bode and Varela, 1994) and California (Kudela et al., 1997). Accordingly,
measurement of ammonium and/or urea concentrations in the study area would provide
an important connection between nutrient dynamics and production, both in the Capes
Current and in the nitrate-depleted inner shelf waters south of Point Cloates.
In addition to dynamics associated with localized upwelling, processes at the
shelf break were also found to be of biological importance. South of Point Cloates, the
200 m isobath essentially formed the boundary between high biomass (15.0 – 45.0
mg chl a m-2) continental shelf waters and lower biomass (7.5 – 22.5 mg chl a m-2)
offshore waters, similar to the observations of Pattiaratchi et al. (2004). A band of
relatively high depth-integrated nitrate was located along much of the shelf break
(reflective of a shoaling of the nitracline evident in the cross-shelf nitrate contours), and
provided some evidence for potential alleviation of oligotrophic conditions within the
Leeuwin Current. While the bulk of the LC/offshore production stations were located
along the 1000 m isobath, one station was situated at the shelf break (Stn 112 on
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
74
Transect I), where the LC’s core flow (maximum velocity) occurred (Woo et al., 2004).
Relatively high biomass (38.6 mg chl a m-2) and primary production (530 mg C m-2 d-1)
at this station provides an indication of the impact of shelf break processes on
phytoplankton dynamics. Current shear between LC and shelf waters has been
observed (Pearce and Griffiths, 1991) and modelled (Meuleners et al., 2003) along this
boundary, and Leeuwin Current meanders can entrain significant amounts of shelf water
(Pattiaratchi et al., 2004). Thus, the shelf break can be an area of active mixing, and we
infer that this may promote nutrient fluxes into the euphotic zone and fuel localized
production and biomass peaks.
3.5.3 Implications of biomass and productivity patterns for community ecology
This study has highlighted Ningaloo Current waters as a ‘hotspot’ for primary
production off Western Australia; the same may be true of Capes Current waters,
although limited data in the southern region does not allow us to draw this conclusion
without further investigation. The uniqueness of the Ningaloo area has been known for
some time, as it is the site of the only substantial coral reef system found on the west
coast of a continent (Taylor and Pearce, 1999) and attracts a number of megafauna
(including whale sharks and manta rays; Taylor, 1994). Dense schools of zooplankton
are seasonally common in this region, and Wilson et al. (2002b) proposed that
upwelling near North West Cape might drive the production of large euphausiid
populations off Ningaloo reef.
The high primary productivity and phytoplankton biomass we measured at Point
Cloates and along the Cape Range Peninsula are a potential link between coastal
upwelling and secondary productivity, with nutrient inputs via upwelling generally
supporting a shorter food chain than found in oligotrophic waters (Cushing, 1989). The
Chapter 3 – Phytoplankton responses to spatially variable nutrient dynamics off Western Australia
75
relatively high proportion of centric diatoms at NC production stations provides
additional support for the existence of an active herbivorous food web in the region
(Legendre and Rassoulzadegan, 1995).
However, flagellates were numerically dominant in Ningaloo Current waters,
although their relative contribution to total biomass would likely be fairly low given
their small size (similar to observations in the Iberian upwelling system; Joint et al.,
2001). Yet this may indicate the presence of a more diverse multivorous web, where
both the herbivorous and microbial web pathways play important roles (Legendre and
Rassoulzadegan, 1995). Interestingly, a recent laboratory study by Ianora et al. (2004),
challenges the importance of diatom production for higher trophic levels, as copepods
fed on an exclusive diet of Skeletonema costatum showed suppressed reproductive
output that was attributed to aldehyde toxicity. However, multiple field studies indicate
that copepods can be quite selective with their food intake, and that a diverse diet
(especially common with multivorous food webs) may help negate toxic impacts of
certain diatom species (Irigoien et al., 2002). Studies that examine size-fractionated
primary production, in conjunction with the seasonality of nutrient enrichment and
secondary productivity, would be the next step in elucidating the ecological processes
and trophic pathways of this region.
3.6 Concluding Remarks
In this chapter, we investigated early summer primary production regimes, linked with
mesoscale physical processes and nutrient dynamics, along a broad stretch of the
Western Australian coastline. While large-scale upwelling is incompatible with the
poleward flowing Leeuwin Current, localized seasonal upwelling associated with inner
shelf countercurrents has been demonstrated for both the Ningaloo (Woo et al., 2004)
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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and Capes Currents (Gersbach et al., 1999). We found that primary production
associated with these equatorward flows was of regional significance, and we
hypothesize that nutrient enrichment associated with these currents may be a function of
geographical location, intensity of the upwelling flow, and depth of the Leeuwin
Current’s nutricline. Mixing and/or current shear along the 200 m shelf break, which
separated high biomass continental shelf waters from low biomass offshore waters, was
also considered an important process leading to peaks in productivity along on this
otherwise oligotrophic coast.
CHAPTER 4
77
Deep chlorophyll maximum dynamics in Leeuwin Current and offshore
waters of Western Australia
4.1 Summary
This chapter undertakes a detailed examination of the vertical phytoplankton biomass
and productivity structure in Leeuwin Current (LC) and offshore waters along the
Gascoyne region of Western Australia, where a deep chlorophyll maximum (DCM)
layer is a ubiquitous feature. Through particulate organic carbon (POC) analyses, we
found that this DCM was a true biomass maxima, with phytoplankton POC up to five
times higher in the DCM than surface waters. Generally located between 60 and 100 m
depth in this region, the DCM layer accounted for 10 to 40 % of total water column
production and was closely associated with both the nitracline and pycnocline. Light
limitation at depth played a critical role in DCM productivity, with photosynthesis in
this layer particularly sensitive to modifications in the light attenuation coefficient (Kd).
Deep chlorophyll maximum depth (and therefore production) was also related to
changing oceanographic conditions in both the alongshore and cross-shore directions,
which included variation in the strength of the Leeuwin Current.
4.2 Introduction
In stratified waters, phytoplankton productivity is generally limited by nutrients in the
upper euphotic zone (Dugdale and Goering, 1967), while light limitation plays a
primary role towards the base of the euphotic zone (Behrenfeld and Falkowski, 1997),
where irradiance falls to 0.1% of surface levels. Primary production can also be limited
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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directly below the sea surface by photoinhibition (Kirk, 1994), although phytoplankton
may exhibit physiological responses at high light and low nutrient levels (such as an
increase in the carotenoid:chl a ratio through a reduction in cellular chl a content) to
protect against photo-damage (Staehr et al., 2002). Light intensity impacts not only the
photoadaptive state of phytoplankton, but also the depth of the upper light-saturated
section of the euphotic zone (Behrenfeld and Falkowski, 1997).
The extent of photosynthesis can therefore be a complex trade-off between
irradiance and nutrient conditions, both of which vary in the vertical. As a result,
phytoplankton often accumulate at distinct water depths which do not necessarily
correspond to a maximum in either irradiance or nutrient concentration (Cullen, 1982).
Such accumulation may occur right at the surface or may take the form of a deep
chlorophyll maximum (DCM). In a comparison of various waterbodies, Jeffrey and
Hallegraeff (1990) illustrate the shoaling of DCM depth from 90 – 130 m in the open
ocean to 15 – 30 m in coastal regions.
There are a number of processes that may be involved in DCM formation, as
reviewed in Cullen (1982). These include passive accumulation of cells at a pycnocline,
or behavioural aggregation of motile cells (especially dinoflagellates) as a defense
against grazing. However, as pointed out in Cullen (1982), deep chlorophyll maxima
may not necessarily correspond to an increase in biomass, but rather signify a
physiological adaptation of the cellular carbon:chlorophyll a (C:chl a) ratio.
Accordingly, in the field, we sometimes see a decrease of C:chl a with decreasing
ambient irradiance (i.e. with increasing depth) resulting from photoacclimation to low
light levels, as found near the base of the euphotic zone (Geider, 1987).
Photoacclimation is also manifested through the photosynthetic response, where light-
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
79
limited cells (such as from DCM depths) exhibit significant photoinhibition when
incubated under high light (as reviewed in Zonneveld, 1998)
The amount of total water column production attributable to the DCM can vary
both spatially and temporally. In the North Sea, the DCM accounted for a mean of
~ 40% of total areal production, although at some stations was as high as 75%
(Richardson et al., 1998). In the sub-Antarctic region south of Australia, the
spring/summer DCM is relatively shallow (< 60 m) with high chlorophyll (up to 1.5
mg m-3) and contributes 30-50% of total production, while in early winter the DCM is
deep ( 100 m) with lower chlorophyll (~ 0.5 mg m-3) and a lower contribution ( 20%)
to water column production (Parslow et al., 2001). The most persistent DCMs have
been observed in the subtropical ocean gyres, where they are present throughout the
year (Mann and Lazier, 1996) and are predominantly controlled by the slow upward
diffusion of nutrients from depth (Cullen, 1982). However, in the oligotrophic
Atlantic, Maranon et al. (2000) found that the DCM formed primarily as a result of
lower C:chl a at depth and therefore made a minor contribution to total biomass and
production.
The importance of these subsurface chlorophyll layers can therefore vary from
case to case. In Chapter 3, we documented a ubiquitous deep chlorophyll maximum on
the continental shelf of Western Australia (0-200 m water depth) and offshore (200-
4000 m water depth), where the Leeuwin Current (LC), a poleward flowing eastern
boundary current, transports tropical low salinity, low nutrient waters along the coast of
Western Australia (Pearce, 1991). The DCM was most pronounced in Leeuwin Current
and offshore regions, where a low chl a (< 0.15 mg m-3) surface layer overlaid
chlorophyll peaks of up to 0.90 mg m-3. These were located between 60 and 100 m
depth (Chap. 3), which is well beyond the detection limit of ocean colour satellite
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
80
imagery (SeaWiFs optical depth is a maximum of 40-60 m in LC/offshore waters; P.
Fearns, pers. comm.). It is therefore important to address whether these DCMs make a
significant contribution to total water column production in the LC. In the present
chapter, we determine if DCMs in the LC are ‘true’ biomass maxima, and we assess the
relative contribution of DCMs and their overlaying waters to the total primary
production in the LC. We also discuss variations in the depth of the DCM in relation to
changing oceanographic conditions along the path of the Leeuwin Current.
4.3 Materials and Methods
4.3.1 Study region
The field study was undertaken in November 2000 aboard RV Franklin voyage
FR10/00, during which we sampled the coastal eastern Indian Ocean along the
Gascoyne region of Western Australia, from ~ 21S to 30S and offshore to 111E (Fig.
4.1). A total of 118 oceanographic stations were occupied along 11 onshore/offshore
transects (Chap. 3, Fig. 3.1) through continental shelf (0-200 m), shelf break (200-300
m) and offshore (300-1000 m) waters. However, this chapter primarily examines 51
stations located within Leeuwin Current and offshore waters (Transects D to J from
approximately the shelf break westwards; Fig. 4.1), and only briefly touches on the
upwelling-influenced Leeuwin Current/Ningaloo Current waters along North West Cape
(Chap. 3, Fig. 3.2).
4.3.2 Field sampling, experimentation and laboratory analyses
Water samples were obtained using General Oceanics 5 L Niskin bottles mounted on a
rosette equipped with Seabird CTD, in situ fluorescence sensor and Li-Cor LI-192SA
underwater quantum sensor. In addition to standard oceanographic depths (which
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
81
Figure 4.1. Location of sampling stations in Leeuwin Current and offshore waters of
the coastal eastern Indian Ocean, with the path of maximum Leeuwin Current surface
velocity indicated by arrows. CTD casts and water sampling (nutrients, chl a) were
conducted at all stations, while production stations also included 14C uptake experiments
and particulate organic carbon and nitrogen (POC/PN) measurements.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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included ≤ 25 m intervals within the euphotic zone), Niskin sampling targeted the DCM
by sampling above, within and below the fluorescence maximum (as determined by the
downcast fluorometer trace).
All samples were analyzed for dissolved inorganic nutrients (nitrate + nitrite,
phosphate and silicate) using a shipboard Autoanalyzer. Detection limits were 0.1 M
for nitrate + nitrite (hereafter nitrate), 0.01 M for phosphate and 0.1 M for silicate
(Cowley, 1999). For phytoplankton pigments (chlorophyll a and pheopigments), 2L
water samples were filtered onto Whatman GF/F filters, stored at -20C and returned to
the laboratory for analysis. Pigments were extracted in 90% acetone with grinding, and
measured using a Turner Designs fluorometer (detection limit of 0.01 mg chl a m-3),
following the acidification technique of Parsons et al. (1989).
Nine ‘production stations’ were occupied in LC/offshore waters, where primary
productivity versus irradiance (P vs. I) experiments were performed on samples from
2 - 6 depths. We used a photosynthetron and the small-volume 14C incorporation
technique (Lewis and Smith, 1983) with modifications as per Mackey et al. (1995,
1997a). Each water sample was inoculated with 14C to a final concentration of 1.0 Ci
per 1.0 mL seawater, and triplicate aliquots from each sampling depth were incubated
for ca. 2 to 3 hours at six main light levels (plus dark), achieved using different
combinations of neutral density and spectrally-resolving blue filters. Also at these
stations, particulate organic carbon (POC) and particulate nitrogen (PN) were
determined for the surface and DCM. 4L were filtered on pre-combusted Whatman
GF/F filters and stored at -20C until analysis by mass spectrometer, following the
preparation techniques of Knap et al. (1996).
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
83
4.3.3 Data analysis and sensitivity estimates (Kd, *)
In situ fluorescence was calibrated with extracted chl a data using linear regression.
Where data permitted (minimum of 5 data points), a separate regression was performed
for each station; otherwise, stations were calibrated using pooled data for that transect
(r2 = 0.76-0.92). Deep chlorophyll maximum (DCM) depth was taken as the depth of
maximum subsurface chl a, while the upper limit of the DCM was defined using a
minimum gradient criterion of 0.02 mg chl a m-3 (m-1) over a 2 m depth interval.
Pycnoclines were identified by a density (t) gradient criterion (calculated as [t *
1000]/z) of 20, a value used by Tranter and Leech (1987) on the Australian
Northwest Shelf to indicate a strong density gradient. This criterion is equivalent to
0.01 t units m-1.
Computation of daily rates of primary production were performed as in Mackey
et al. (1995) and Walsby (1997). Chlorophyll-normalized photosynthetic parameters
(Pm* or Ps
*, * and *) were linearly interpolated between sample depths. Calibrated
fluorescence was used to scale these parameters at 2 m depth intervals, and production
(P) was calculated using the equation of Platt et al. (1980): P = Ps (1-e-I/Ps) e-I/Ps,
where I is in situ irradiance. The latter parameter was computed using theoretical
‘cloudless’ irradiance based on latitude and date (Kirk, 1994; Walsby, 1997), corrected
for water reflectance by incorporating solar elevation, effective zenith angle and surface
wind roughening (from five-minute wind averages, as per Walsby, 1997), and finally,
corrected for light attenuation with depth using Kd, the light attenuation coefficient
(Kirk, 1994).
In Chapter 3, where we also examined total water column production, we
identified some potential limitations of our production calculations, and in the present
chapter we are interested in evaluating how these impact on our productivity estimates.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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Firstly, a number of P vs. I experiments did not reach photosynthetic saturation due to
low maximum irradiance levels within the photosynthetron (400 E m-2 s-1). These
experiments were consequently without a measure of the photoinhibition parameter
(*), so that in Chapter 3 we used a value of = 0.00 mg C mg chl a-1 h-1
[mol m-2 s-1]-1 to calculate light-saturated primary production. In an extensive review
of various field studies, Platt et al. (1980) found that * ranged between extremes of
0.00 and 0.01 mg C mg chl a-1 h-1 [mol m-2 s-1]-1; we have therefore calculated
production in the present chapter using both of these scenarios.
Secondly, for the majority (~ 70 %) of production stations within the study
region, we used a regional average value of Kd for calculations, as light profiles were
only obtained at a limited number of CTD stations. This mean value of Kd (0.066 m-1;
n = 27) may have underestimated light attenuation for the nine production stations
within Leeuwin Current and offshore waters, as limited light profiles in this region
(n = 6) indicate that Kd can be as low as 0.050 m-1. Therefore, as we primarily focus on
LC/offshore waters in the present chapter, we have calculated production using both of
these Kd values (0.050 m-1 and 0.066 m-1) for comparison.
For all production estimates, the double integral of photosynthesis through depth
and time (mg C m-2 d-1) was computed using trapezoidal integration (Walsby, 1997).
These calculations provide only an estimate of daily gross production, as no attempt was
made to correct for carbon losses via respiration. All depth integrations (for primary
production and chl a) were to the 0.1% light level of 104 m, chosen as the standard
estimate of euphotic depth over the 1.0% light level because a large proportion of the
DCM was found to be at or below 1.0% irradiance.
As sampling was undertaken with standard uncoated hydrowire and General
Oceanics Niskin bottles that had not been fitted with silicone tubing and o-rings, we
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
85
must assume that photosynthetic rates were potentially underestimated due to
contamination effects (Marra and Heinemann, 1987; Williams and Robertson, 1989).
Using similar methodologies as the present study, Mackey et al. (1995) found that Pm*
and depth-integrated productivity was underestimated by up to 50%. It is reasonable to
consider that a similar effect may have occurred with our results.
4.4 Results
4.4.1 Phytoplankton biomass
Extracted chlorophyll a ranged from 0.01 – 0.23 mg m-3 at the surface and 0.28 –
0.83 mg m-3 at the DCM of Leeuwin Current/offshore stations. Concentrations of
0.10 mg m-3 were most common at the surface (80% frequency), while levels of 0.4 –
0.5 mg m-3 were most common at the DCM (35% frequency; Fig. 4.2).
Phytoplankton biomass was also estimated in units of carbon. Particulate
organic carbon (POC) collected on a GF/F filter can be composed of not only
phytoplankton, but also bacteria, microzooplankton and detritus. To determine the
fraction attributable to autotrophs, a linear regression of POC on chl a was performed,
with the intercept taken as that portion of POC not associated with live phytoplankton
(Eppley et al., 1977). Note that, due to the small sample sizes involved, this
relationship was determined using POC data from all 18 production stations within the
study region (see Chap. 3), which included those from outside LC/offshore waters.
Separate regressions for surface and DCM samples yielded (Fig. 4.3):
Surface: y = 67.5x + 43.6, r2 = 0.47, p < 0.005
DCM: y = 65.1x + 23.6, r2 = 0.32, p < 0.05
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Figure 4.2. Relative frequency of phytoplankton biomass (as chl a) at the surface and
DCM within Leeuwin Current/offshore waters.
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
87
Figure 4.3. Linear regression of particulate organic carbon (POC) versus chlorophyll a,
for surface and deep chlorophyll maximum (DCM) samples.
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The intercepts were subtracted from total POC to yield phytoplankton POC, which was
found to be significantly higher (t-test, p < 0.01) at the DCM than surface. This
transformation resulted in four surface samples from LC/offshore waters with negative
values (-6.9 to -10.3 mg m-3), which we considered as zero when investigating data
distributions (Fig. 4.4). Within LC/offshore waters, phytoplankton POC ranged from
0.0 – 10.1 mg m-3 at the surface and 6.4 – 54.4 mg m-3 at the DCM. Concentrations of
10 mg m-3 were measured in 90% of surface samples, while at the DCM
concentrations of 10 – 40 mg m-3 accounted for 80% of samples (Fig. 4.4).
The regression coefficients for POC and chl a (67.5 and 65.1) provided a measure
of phytoplankton-specific C:chl a (Townsend and Thomas, 2002), and were not
significantly different between surface and DCM datasets (t-test, p < 0.001). This
permitted calculation of the weighted regression coefficient underlying the two slopes
(Zar, 1996), which equalled 65.4 and was used as the common C:chl a ratio for this
study.
4.4.2 Phytoplankton production
To examine the significance of DCM production, we divided the water column into an
upper (surface) layer and a lower (DCM) layer. The surface layer was defined from 0 m
to the top of the DCM (identified using the minimum gradient criterion of
0.02 mg chl a m-1), and the DCM layer was from the top of the DCM to the base of the
euphotic zone (104 m). To evaluate the frequency distribution of photosynthetic rates
in each layer, we examined values of volumetric production from 20 m intervals
through the water column. These reveal that, despite higher biomass in the DCM,
productivity was significantly lower (mean s.d., 0.96 0.7 mg C m-3 d-1) than in the
surface layer (3.12 1.46 mg C m-3 d-1; Mann-Whitney U, p < 0.01). Approximately
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
89
Figure 4.4. Relative frequency of phytoplankton biomass (as phytoplankton carbon) at
the surface and DCM within Leeuwin Current/offshore waters.
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90% of samples from the DCM were characterized by production 2.0 mg C m-3 d-1
(Fig. 4.5a), with the exception of Stn 112 (up to 7.02 mg C m-3 d-1) and Stn 131 (up to
2.39 mg C m-3 d-1).
As a percentage, the DCM layer most commonly accounted for 20 – 30 % of total
water column production (mg C m-2 d-1; Fig. 4.5b) in the LC/offshore region. The least
productive DCM (Stn 119) accounted for only 6 % of production, while the most
productive (Stn 131) accounted for 37 %. This parameter had a significant (p < 0.05)
negative linear relationship with DCM depth (Table 4.1). As a regional comparison,
and to further examine the relationship between DCM depth and productivity, we have
included Ningaloo Current data (Chap. 3) and plot DCM production (as percentage of
total) against DCM depth for both the Leeuwin Current/offshore and Ningaloo Current
regions (Fig. 4.6). This gave a strongly significant negative exponential relationship
(r2 = 0.71, p < 0.001; Fig. 4.6), with the relatively shallow Ningaloo Current DCMs
(approximately 15 – 40 m depth) accounting for up to 80 % of total water column
production (Fig. 4.6). The model infers that any proportion of the DCM layer located
below 88 m depth will not contribute to overall water column production
The maximum light-saturated rate of photosynthesis (Pm*) ranged from 0.21 to
11.75 mg C mg chl a-1 h-1 (Table 4.2), and was significantly higher at the surface (mean
SE, 7.66 0.75) than the DCM (1.80 0.23; Mann-Whitney U, p < 0.001). The
initial (light limited) slope of the P vs. I curve (*) showed much lower variability
(0.005 to 0.071 mg C mg chl a-1 h-1 [mol m-2 s-1]-1), and was not significantly different
between surface and DCM depths (Mann-Whitney U, p = 0.79). The photoinhibition
parameter (negative slope of the P vs. I curve at high irradiance; *) was only > 0 at the
DCM of 3 stations (Stns 52, 55, 65; Table 4.2), with an overall range of 0.003 – 0.0095
mg C mg chl a-1 h-1 [mol m-2 s-1]-1. The half-saturation coefficient for irradiance (Ik;
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
91
Figure 4.5. Relative frequency distributions of primary production (calculated using
= 0.00 mg C mg chl a-1 h-1 [mol m-2 s-1]-1 and Kd = 0.066 m-1) showing: (a) the
spread of values from 20 m intervals in the surface and DCM layers; and (b) the
contribution of the surface and DCM layers to total areal phytoplankton production.
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Table 4.1. Coefficients of determination (r2) and associated levels of statistical
significance (p-value) for the linear relationship between percentage of total water
column production within the DCM and the depths of the nitracline, DCM and top of
DCM.
Slope r2 p Top of DCM (m) -0.76 0.37 0.08
DCM (m) -0.95 0.59 0.02 Nitracline (m) -1.85 0.47 0.06
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
93
Figure 4.6. Percentage of total water column production (mg C m-2 d-1) contained
within the DCM layer, plotted as a function of DCM depth for both Leeuwin
Current/offshore and Ningaloo Current regions. A negative exponential model provided
the best fit to the data.
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Table 4.2. Total water column biomass (mg C m-2; converted from chl a using C:chl a
of 65.4), primary production (PP; mg C m-2 d-1) and photosynthetic parameters from all
sampling depths: Pm* (mg C mg chl a-1 h-1); * (mg C mg chl a-1 h-1 [mol m-2 s-1]-1);
* (mg C mg chl a-1 h-1 [mol m-2 s-1]-1); Ik (mol m-2 s-1). Parameters from surface and
DCM sampling depths are highlighted in bold.
Stn Depth (m) Pm* * * Ik Biomass PP
52 2 7.52 0.050 - 149 980 190 45 2.09 0.026 0.0004 80 75 0.98 0.024 0.0015 41 100 1.61 0.041 0.0046 39 125 0.72 0.027 0.0004 26
55 3 5.66 0.039 - 146 1140 140 60 1.71 0.016 0.0005 109 90 2.30 0.048 0.0095 48 125 0.21 0.005 0.0003 38
65 2 4.07 0.024 - 169 1555 110 70 0.60 0.014 0.0017 44 90 0.53 0.016 0.0006 34 125 0.41 0.039 0.0003 11
101 2 9.33 0.030 - 307 1055 200 60 2.28 0.025 - 90 80 2.42 0.044 - 55 100 1.90 0.056 0.0080 34
112 2 8.79 0.059 - 149 2525 530 70 2.05 0.036 - 57 100 1.88 0.045 0.0033 42
116 2 11.75 0.037 - 320 650 175 65 3.32 0.028 - 117 95 2.16 0.051 - 42 125 1.03 0.060 0.0041 17
119 2 8.55 0.050 - 170 595 120 74 1.68 0.050 - 94 100 1.40 0.029 - 48 150 1.08 0.035 0.0030 31
131 5 6.92 0.032 - 220 1280 170 75 2.30 0.37 - 63 80 2.59 0.047 - 55 125 1.76 0.071 0.0076 25
132 5 6.34 0.029 - 216 910 170 55 1.18 0.012 - 102 75 1.04 0.011 - 99 120 1.11 0.021 - 53
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
95
calculated as Pm*/) was significantly higher at the surface (205 22 mol m-2 s-1) than
the DCM (54 6 mol m-2 s-1; Mann-Whitney U, p < 0.001). An unusually high value
of Ik was measured at the DCM of Stn 132 (99 mol m-2 s-1; Table 4.2), which sampled
the edge of an anti-cyclonic (downwelling) eddy. Based on the calculated subsurface
irradiance profile (Section 4.3.3), the average irradiance just below the surface (2 m
depth; I2m) over the daylight period (05:30 – 18:30) was ~ 1250 mol m-2 s-1. To
evaluate the ambient light levels to which phytoplankton were adapted and further
assess the potential impact of photoinhibition in the surface layer, we also calculated the
parameter Ik/I2m, which for surface samples ranged from 12 – 26 %, with a mean ( s.d.)
of 16.4 5.4 %.
4.4.3 Effects of * and Kd estimates on production calculations
For Leeuwin Current/offshore waters, we have examined the sensitivity of both
volumetric and total water column (areal) production to the photoinhibition parameter
() and the light attenuation coefficient (Kd; Fig. 4.7). There are three outcomes
associated with these calculations (Fig. 4.7): 1) data points on the 1:1 line indicate that
production calculations are not sensitive to our modifications of these parameters; 2)
data points above the 1:1 line indicate that calculations on the x-axis ( = 0.01
mg C mg chl a-1 h-1 [mol m-2 s-1]-1 or Kd = 0.050 m-1) set a lower limit on production
estimates; and 3) data points below the 1:1 line indicate that calculations on the x-axis
set an upper limit on production estimates. From this, we find that production rates at
the DCM were not influenced by manipulations (Fig. 4.7a), while production rates at
the surface were not affected by Kd manipulations (Fig. 4.7b). However, total areal
production was reduced when calculated under the * = 0.01 condition, primarily as a
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Figure 4.7. Comparison of areal and volumetric primary production rates under
contrasting conditions of a) photoinhibition (), and b) light attenuation coefficient (Kd).
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
97
result of decreased productivity in the surface layer (Figs. 4.7a, 4.8). In contrast, areal
production was increased when calculated at lowered light attenuation (0.050 m-1) due
to an increase of productivity in the DCM layer (Fig. 4.7b). These potential errors
therefore provide a lower (* = 0.01) and upper (Kd = 0.050) limit for productivity
estimates in LC/offshore waters, as compared to our original calculations using
* = 0.00 mg C mg chl a-1 h-1 [mol m-2 s-1]-1 and Kd = 0.050 m-1 (Table 4.3).
4.4.4 Physical and chemical influences on the DCM
Multiple pycnoclines were found in most density profiles between the surface and
200 m water depth. To identify any correlation between the DCM and these density
gradients, the depth of the pycnocline located closest to the DCM (either above or
below) was compared to the DCM depth (Fig. 4.9). The majority of deep chlorophyll
maxima were located within 20 m of a strong density gradient. A similar relationship
was identified between DCM depth and the nitracline (Fig. 4.9).
With the strong connection between DCM depth and productivity identified in Section
4.4.2, we are interested in investigating mechanisms within Leeuwin Current/offshore
waters that may impact on DCM depth. As identified by Woo et al. (2004), the LC
exhibited three distinct regimes within the study area. In the northern section (Transects
D to F; Fig. 4.1), the current flowed relatively strong (surface velocity of 0.38 – 0.50 m
s-1) and narrow. In the central section of the study area, along the broad shelf off Shark
Bay (Transects G and H), the current was wide and relatively slow (0.26 – 0.28 m s-1).
In the southern section (Transects I and J), with a narrow and steep shelf break, the
current exhibited maximum velocity (0.64 – 0.68 m s-1) and was also influenced by
geostrophic inflow from the Indian Ocean, particularly entrainment of Indian Ocean
Central Water (Woo et al., 2004). In Figure 4.10, Transects E to J are
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Figure 4.8. Vertical profiles of primary production from three representative stations.
Solid lines show primary production calculated using * = 0.00 mg C mg chl a-1 h-1
[mol m-2 s-1]-1 (no photoinhibition); dashed lines show primary production calculated
using * = 0.01 mg C mg chl a-1 h-1 [mol m-2 s-1]-1 (high photoinhibition).
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
99
Table 4.3. Total water column production (to 0.1% light level; 104 m) calculated using
different values of (mg C mg chl a-1 h-1 [mol m-2 s-1]-1) and Kd (m-1).
Primary production (mg C m-2 d-1)
Stn = 0.00,
Kd = 0.066 = 0.01,
Kd = 0.066 = 0.00,
Kd = 0.050 52 190 100 260 55 140 80 235 65 110 60 170 101 200 130 320 112 530 370 825 116 175* 120 355 119 120 80 180 131 170 130 335 132 170 80 220
200 125 130 95 320 200
* Kd = 0.078 (the only LC production station with an in situ light measurement)
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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Figure 4.9. Depth of the DCM vs. depth of the nitracline and pycnocline for Leeuwin
Current/offshore waters; dotted lines indicate 20 m from a 1:1 relationship.
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
101
Figure 4.10. Cross-shelf chl a distribution from north (Transect D) to south (Transect
J) through the study area, overlaid with the nitracline (solid line) and a mean estimate of
euphotic zone depth (0.1 % light; dotted line). Triangles indicate sampling stations;
filled triangles and station numbers (S) indicate production stations.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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vertically aligned according to the location of maximum LC surface velocity (as per
ADCP analyses by Woo et al., 2004 and illustrated in Fig. 4.1) to identify whether
current velocity and the location of core flow influences chl a distributions. The mean
euphotic zone depth (104 m; 0.1 % light level) is also indicated (Fig. 4.10).
Along many transects (E, G, I and J), the DCM/nitracline layer was physically
depressed (with a somewhat U-shaped profile) near the Leeuwin Current’s core flow
(Fig. 4.10), and was found at or near the base of the euphotic zone (e.g. Transects E, F,
J; Fig. 4.10). In the central region of the study area (Transects G, H and I) the DCM
and nitracline were generally shallower and found between 60 and 80 m (2.0 – 0.5%
light; Fig. 4.10). Distinct features were noted along Transect J, where the nitracline
depression under the LC was bordered on the offshore edge by an extremely deep (~
180 m) nitracline/chlorophyll layer, and at Transect E, where an unusually shallow
nitracline (50 m; ~ 4.0 % light) was located in the centre of the transect (Fig. 4.10).
Relationships between water column structure, nitracline depth and the DCM
were further examined with vertical profiles of density (t), nitrate and chl a at
individual stations through the core of the LC (Fig. 4.11). DCM depth (defined as the
depth of maximum subsurface chl a concentration; Section 4.3.3) for these seven
stations ranged between 84 and 110 m (Fig. 4.11). For the three northernmost transects
(D to F), peak chl a was located at ~100 m; in the central section (Transects G and H),
the DCM was shallower and found at ~ 85 m depth; whilst at the two southernmost
transects (I and J), the DCM was located at 95 and 110 m, respectively (Fig. 4.11). For
the northern region (Transects D to H), the bulk of the DCM was situated above the
main pycnocline, which was generally 120 m depth. In some cases (Transects D, F,
H), the upper limit of the DCM was bordered by a shallow pycnocline between ~ 40 and
60 m; in others (Transects E and G), the water column was well-mixed to ~ 100 m with
103
Figure 4.11. Vertical profiles of density (t), chl a and nitrate along the core of the Leeuwin Current, from north (Transect D) to south (Transect J).
Open circles indicate the location of pycnoclines, as defined using the density gradient criterion of Tranter and Leech (1987); see text.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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a more diffuse DCM structure and higher chl a concentrations in surface waters (Fig.
4.11). The southernmost transects (I and J) showed distinct structure, with the
chlorophyll maximum situated within a broad pycnocline region between ~ 60 and
140 m (Fig. 4.11).
4.5 Discussion
One of the primary factors controlling the productivity, and hence the ecological
importance, of deep chlorophyll maximum (DCM) layers is light limitation (Estrada,
1985; Richardson et al., 2000; Parslow et al., 2001). In a stratified euphotic zone, with
a nutrient-rich but light limited bottom layer overlaid by a nutrient-depleted surface
layer, chlorophyll and production maxima are often found associated with the nutricline
boundary (Cullen, 1982; Eppley et al., 1988), and thus modifications in the depth of this
boundary can impact ambient light conditions at the DCM. Off Western Australia
(WA), we found a ubiquitous DCM that was closely associated with the nitracline and
pycnocline, and contributed to between 10 and 40 % of total water column production
within Leeuwin Current and offshore waters. In this discussion, we investigate
mechanisms that impact the formation of this DCM, and examine controls on
productivity in this layer, with a focus on the photosynthetic response to light and
oceanographic influences on DCM depth.
4.5.1 Photosynthetic characteristics and significance of deep chlorophyll maxima
Physiological adaptation of phytoplankton to light and nutrients can alter the C:chl a
ratio and produce chlorophyll distributions that are not reflective of phytoplankton
abundance or biomass (Cullen, 1982). To address this issue, we used two independent
measurements of phytoplankton biomass in this study, i.e. extracted chlorophyll a and
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
105
particulate organic carbon (POC). The determination of phytoplankton C:chl a is not
necessarily a straightforward calculation, as the commonly used regression technique
(Eppley et al., 1977) can potentially overestimate C:chl a and underestimate the detrital
carbon component (Banse, 1977). Alternative methods include the conversion of
microscopic cell counts to carbon content based on biovolume (Strathmann, 1967), and
the estimation of phytoplankton carbon as a function of cellular DNA content,
determined using nuclear staining methods on a flow cytometer (Veldhuis et al., 1997;
Veldhuis and Kraay, 2004). Additionally, C:chl a can vary between phytoplankton
community types, which is of particular significance when picoplankton (specifically
Prochlorococcus) form a large component of the autotrophic ecosystem (Velhuis and
Kraay, 2004). It can therefore be advantageous to calculate C:chl a for different size
fractions, where possible.
The available dataset necessitated use of the regression technique of Eppley et
al. (1977). We found that surface waters and deep chlorophyll maxima had almost
identical C:chl a (67.5 and 65.1, respectively), with phytoplankton POC up to five times
higher at the DCM compared to the surface. We have therefore classified these deep
chlorophyll maxima as ‘true’ biomass maxima within Leeuwin Current and offshore
waters, although would recommend a more detailed examination of phytoplankton
community-specific C:chl a (following the techniques of Veldhuis and Kraay, 2004) for
future studies of biomass distributions and C turnover rates in these oligotrophic waters.
However, despite the apparently higher biomass in the DCM, we do not
necessarily expect higher primary production in this layer. As detailed in the
Introduction, the extent of photosynthesis in the DCM depends on a trade-off between
the availability of light and nutrients. Variation in the rate of maximum (light-saturated)
chlorophyll-normalized photosynthesis (Pm*; also known as the assimilation index) is
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recognized to be a function of environmental conditions such as temperature and
nutrient concentrations (Lalli and Parsons, 1997) and is an indication of overall
photosynthetic capacity. Additionally, phytoplankton communities living towards the
base of the euphotic zone show photoadaptation to ambient light conditions via a
significantly lower Pm*, in comparison to surface waters (Mackey et al., 1995; Maranon
and Holligan, 1999). This lower Pm* at depth was quite apparent within Leeuwin
Current/offshore waters, where at the chlorophyll maximum Pm* ranged between 0.60
and 2.59 mg C mg chl a-1 h-1 compared with 4.07 to 11.75 mg C mg chl a-1 h-1 at the
surface, thus impacting the total amount of production within the DCM and surface
layer, respectively. Lorenzo et al. (2004) have recently recommended a focus on the
accurate spatial and temporal characterisation of Pm* and the application of simple light-
saturated photosynthetic models (as utilized for this study) within oligotrophic regions.
They note that, in stratified oceanic waters with a permanent DCM, spectral
photosynthetic parameters (such as m, the maximum quantum yield of carbon fixation)
and characterisation of the spectral light field can be disregarded without significant
impact on production estimates (Lorenzo et al., 2004).
The initial slope of the P vs. I curve () is a function of physiological conditions
within the cell and an indicator of photosynthetic efficiency at lower light levels. Lalli
and Parsons (1997) give a general range for in subtropical waters of 0.005 – 0.01 mg
C mg chl a-1 h-1 [mol m-2 s-1]-1. Within LC/offshore waters, relatively high values at
both the surface (0.024 – 0.059 mg C mg chl a-1 h-1 [mol m-2 s-1]-1) and DCM (0.011 –
0.051 mg C mg chl a-1 h-1 [mol m-2 s-1]-1) may indicate the predominance of
picoplankton. These small (< 1.0 m) phytoplankton generally have an elevated value
of (0.02 – 0.06 mg C mg chl a-1 h-1 [mol m-2 s-1]-1; Lalli and Parsons, 1997) due to
their small size and efficient light utilization (Platt et al., 1983). The adaptation of the
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
107
deep phytoplankton population to ambient light conditions was also indicated by the
relatively low light saturation parameters (Ik; 39 – 55 mol m-2 s-1) for the majority of
the DCM.
The percentage of water column production within the DCM layer in Leeuwin
Current/offshore waters ranged between approximately 10 and 40 %, and had a
significant negative correlation with DCM depth. Shallow chlorophyll maxima were
most productive, implying a strong relationship between productivity and irradiance.
Accurate estimate of light attenuation (Kd) can therefore have an important impact on
production calculations, especially within the DCM layer, where light limitation of
phytoplankton growth is a well-known phenomenon (Estrada, 1985; Eppley et al.,
1988). We found that a reduction in Kd from 0.066 m-1 to 0.050 m-1 could, in some
cases, almost double the total amount of water column production, with much of this
increased productivity effected in the DCM layer as a function of the increased euphotic
zone depth from 70 m to 92 m. Given the uncertainty associated with our original Kd
estimate (0.066 m-1) in LC/offshore waters, we should therefore consider 10 – 40 % of
total water column production to be a conservative estimate for the contribution of the
DCM in this region.
Variation in DCM depth in both the cross-shore and alongshore directions points
to a regionally varying contribution of the chlorophyll maxima to total water column
production within Leeuwin Current/offshore waters. With a view towards
understanding what controls this regional difference in DCM depth, and therefore
predicting areas of shallow and productive deep chlorophyll maxima, in the next two
sections we examine relationships between physical/chemical dynamics, chlorophyll
profiles and primary productivity.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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4.5.2 Controls on vertical distribution of phytoplankton biomass and productivity
Cullen (1982) defines a number of scenarios that result in DCM formation in different
environments. In temporally and spatially stable tropical waters, the chlorophyll
maximum is closely associated with the nitracline and primary production peaks at, or
slightly above, the DCM. This ‘typical tropical structure’ (TTS; Herbland and
Voituriez, 1979) is essentially a two-layer system, where a nutrient-depleted surface
layer overlies a light-limited deeper layer and production is a function of the slow
vertical diffusion of nitrate (Dugdale and Goering, 1967). Although generally defined
as a tropical feature, this scenario is also relevant for stable water columns at higher
latitudes (Cullen, 1982). In more dynamic environments, such as temperate latitudes
where mixing and nutrient inputs vary seasonally, the production peak can be near the
surface and quite separate from the nitracline and chlorophyll peak at depth (Cullen,
1982). Such conditions occur following the spring bloom, where nitrate depletion in
surface waters is followed by a shift to regenerated production.
We envisage some combination of the above factors as being important for
chlorophyll and production profiles in Leeuwin Current and offshore waters. In many
respects, conditions in the oligotrophic eastern Indian Ocean can be characterized as
TTS, because chlorophyll peaks and subsurface productivity maxima were strongly
associated with the deep nitracline. However, highest photosynthetic rates were almost
invariably located at or just below the surface, where nitrate was below detection limits
and chlorophyll was at a minimum. This is similar to observations in the oligotrophic
western Mediterranean, where Estrada (1985) proposed that surface production was
based on regenerated nitrogen while phytoplankton growth at the DCM was largely a
function of nitrate diffusion from depth (i.e. new production; Dugdale and Goering,
1967). Whether such a scenario holds true for Leeuwin Current/offshore waters will be
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
109
explicitly tested in Chapter 5, through the measurement of 15NO3- and 15NH4
+ uptake at
the surface and DCM.
However, we must also be cautious with our interpretations of the absolute
magnitude of primary production in the surface layer, as we had no estimate of *, the
photoinhibition factor, for near-surface samples. In a well-mixed surface layer,
photosynthetic parameters (especially Pm* and *; Kirk, 1994) will reflect adaptations to
the average conditions encountered by phytoplankton during their vertical excursion in
that layer. Although we do not have a measure of vertical mixing for this study,
inspection of the vertical density profiles and calculation of pycnocline depths revealed
that surface waters could be well-mixed down to 40 – 100 m. The light saturation
parameter (Ik) is a fair indication of the irradiance level for which phytoplankton is
adapted (Sakshaug et al., 1997). For samples from the surface layer, Ik/I2m ranged from
12 – 26 %, indicating that phytoplankton were adapted to these light intensities. For a
Kd of 0.066 m-1, this corresponds to a depth of ~ 20 – 30 m. In such a case, it would not
be surprising to find some amount of photoinhibition in near-surface samples, such that
our original vertical profiles of photosynthesis (based on = 0.00 mg C mg chl a-1 h-1
[mol m-2 s-1]-1) may have been somewhat overestimated in the upper euphotic zone.
The lack of chlorophyll accumulation in surface waters despite apparently
maximal productivity rates could be explained by concurrently high grazing rates by
microzooplankton, which are prevalent members of the oligotrophic food web and play
an important part in nutrient recycling (Azam et al., 1983; Cushing, 1989). Close
coupling between phytoplankton growth rates and microzooplankton grazing rates is
common (Strom, 2002). Preliminary results from microzooplankton grazing
experiments in Leeuwin Current surface waters off Perth (32S) indicate that between
60 and 100% of primary production can be grazed over a 24 h period (H. Paterson, pers.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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comm.). An active microbial food web (which encompasses bacteria, small
phytoplankton, protozoa, ciliates and microzooplankton) could also explain the notable
surface productivity despite the absence of measurable nitrate. In such a system,
ammonium and urea are the predominant nitrogen forms (Eppley and Peterson, 1979;
Cushing, 1989), with a close relationship between excretion by heterotrophs and uptake
by autotrophs.
Another important loss term for phytoplankton is cell lysis, which has recently
been shown to represent 50% of gross phytoplankton growth in the oligotrophic surface
waters of the Mediterranean (Agusti et al., 1998). Cell death and lysis can occur as a
result of virus or bacterial attack (Suttle et al., 1990), nutrient stress and exposure to
high irradiance (Laws, 1983). This process leads to the direct release of nutrients to the
microbial loop, resulting in relatively high respiration rates in surface waters due to
enhanced microbial activity (Agusti et al., 1998). Interestingly, lysis accounts for a
much lower (only 7%) proportion of cell loss at the DCM (Agusti et al., 1998). The
extent to which this process, and microzooplankton grazing, regulate phytoplankton
biomass profiles in the oligotrophic waters of the Leeuwin Current is unknown, and
would be possible lines of further investigation.
4.5.3 Deep chlorophyll maxima and the Leeuwin Current
Similar to other systems (Eppley et al., 1988; Basterretxea et al., 2002), the critical
balance between light and nutrients is a key factor driving the productivity of the
LC/offshore region. We have shown that there is a close association between the DCM
and nitracline, and also that DCM productivity is a function of ambient irradiance levels
(i.e. depth). Variation in water column structure, such as the presence of density
gradients and the depth of the mixed layer, is known to impact DCM depth (Hobson and
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
111
Lorenzen, 1972; Cullen, 1982), and we therefore hypothesized that physical
oceanographic processes within the study area might play an important part in the depth
(and thus productivity) of the deep chlorophyll maximum.
One of the main features identified by Woo et al. (2004) was a variation in
Leeuwin Current velocity and depth with latitude, such that three regimes were
identified within the study area. The LC flowed strong and deep in the north, widened
and shallowed in the central section off Shark Bay, and rapidly narrowed and
accelerated south of Shark Bay (Woo et al., 2004). Much of this north/south variability
in Leeuwin Current flow was a function of bathymetry, specifically both the width and
slope of the continental shelf, and the increase in geostrophic inflow of Indian Ocean
waters at the southern extent of the study area (Woo et al., 2004). In general, we found
that DCM depth within the core of the LC was correlated with these regimes, with a
shallower DCM (~ 85 m) in the central section off Shark Bay, and a deeper DCM (~ 95
– 110 m) in both the northern and southern portions of the study area.
Other, more localized, oceanographic conditions also had an impact on DCM
depth. For example, the edge of Transect J was influenced by an anti-clockwise
(downwelling) eddy, which transported cooler, more saline water Indian Ocean Central
Water (Woo et al., 2004) and depressed the chlorophyll/nitracline layer to ~ 180 m.
Additionally, the presence of a pycnocline can also be an important control on biomass
distributions (Cullen, 1982). However, rather than solely acting as a physical barrier to
sinking cells, the associated light and/or nutrient environment at the pycnocline may
result in a physiologically mediated slowing of sinking rates. Waite et al. (1992) have
shown that diatom cells from chlorophyll maximum depths have higher internal nitrate
pools and lower sinking rates than those from surface waters. The proximity of DCMs
to strong density gradients within Leeuwin Current/offshore waters indicates that
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
112
physiological adjustment of sinking rates to exploit the nitracline could be an important
feature of local DCM dynamics. The phytoplankton species composition of the DCM,
and the relative abundance of diatoms, are addressed in Chapter 5.
The postulated coupling between Leeuwin Current strength and DCM depth has
significance when considering seasonal or interannual variation in Leeuwin Current
dynamics. On a seasonal basis, the LC flows less strongly during the summer months
of November to March, due to increased opposing wind stress (Godfrey and Ridgway,
1985). Interannually, flow is weakened during ENSO (El Niño/Southern Oscillation)
years, when the north-south geopotential anomaly (the driving force for the Leeuwin
Current) is reduced (Pearce and Phillips, 1988; Pattiaratchi and Buchan, 1991; Feng et
al., 2003). Under both these conditions, we would expect shoaling of the nitracline and
associated DCM, allowing phytoplankton at the nitracline access to higher light levels.
This could lead to periods of increased production, as well as a shift in the balance of
physical versus biological controls on nitracline depth. The opposite scenario would
occur during autumn/winter conditions (April to September) and La Niña years, when
the LC flows strong and deep and further confines nitrate concentrations to depth.
Finally, this hypothesis provides a mechanistic link between Leeuwin Current
DCM dynamics and the dynamics of countercurrents such as the Ningaloo Current
(Chap. 3). It is clear that DCM depth is the primary determinant of DCM productivity,
not only in the LC but also in the Ningaloo Current, which is sourced (physically) from
both upwelled and recirculated Leeuwin Current water (Woo et al., 2004; Chap. 3).
This places the upwelling regimes as special cases of extreme DCM shallowing, and
emphasizes both the physical and ecological connectivity between the two currents.
These hypotheses point towards a serious need to examine both seasonal and
interannual DCM dynamics within the Leeuwin and Ningaloo Currents. In recent years,
Chapter 4 – Deep chlorophyll maximum dynamics in Leeuwin Current and offshore waters
113
empirical relationships between the strength of LC flow and recruitment to coastal
fisheries have been established (Caputi et al., 1996). Using sea level height measured
off southwestern Australia as a proxy for Leeuwin Current strength, significant links
have been found with recruitment of both benthic invertebrates (e.g. scallops, Amusium
balloti; western rock lobster, Panulirus cygnus) and pelagic finfish (e.g. pilchards,
Sardinops sagax neopilchardus; whitebait, Hyperlophus vittatus; Lenanton et al., 1991;
Caputi et al., 1996). The influence of the current is primarily on the larval phase of
these species, however for some the effect is positive (rock lobster, whitebait) while for
others the effect is negative (scallops, pilchards; Caputi et al., 1996). The mechanisms
by which the Leeuwin Current impacts the larval success of these organisms can only be
determined by a detailed examination of the links between physical oceanographic
processes, phytoplankton dynamics and food web structure on both temporal and spatial
scales.
4.6 Concluding Remarks
In this chapter, we determined that the deep chlorophyll maximum (DCM) feature
within Leeuwin Current/offshore waters was also a maximum of phytoplankton
biomass, and conservatively estimated that the DCM contributed to between 10 and
40 % of total water column production (mg C m-2 d-1). Close coupling between the
nitracline/pycnocline and phytoplankton biomass indicated that the critical balance
between light and nutrients was a key factor driving DCM structure. Productivity of
this layer was negatively correlated with depth, implying a strong relationship with
ambient irradiance. Oceanographic processes within the study area impacted the DCM
layer, as variation in the strength of the Leeuwin Current was correlated with the depth
of the DCM/nitracline layer, thus impacting light conditions at the DCM. We
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
114
hypothesize that productivity in the DCM layer may be affected by the strength and
volume of the Leeuwin Current, which is known to fluctuate both seasonally and with
the El Niño/Southern Oscillation cycle.
CHAPTER 5
115
Phytoplankton community structure and nitrogen nutrition in Leeuwin
Current and coastal waters off the Gascoyne region of Western Australia
5.1 Summary
This chapter follows on from the phytoplankton productivity patterns and nutrient
dynamics identified in Chapters 3 and 4, and examines nitrogen nutrition and species
composition within the different water types and also at the surface and the deep
chlorophyll maximum. The results provide the first estimate of nitrogen uptake rates
within a broad section of the coastal eastern Indian Ocean, and demonstrate the
importance of ammonium-based production throughout the study area. Interestingly,
pelagic ecosystem structure was quite distinct between LC/offshore and
shelf/countercurrent regions. Smaller sized phytoplankton (including cyanobacteria and
prochlorophytes) dominated Leeuwin Current/offshore waters, and were primarily
dependent on regenerated forms of nitrogen at both the surface and DCM. In upwelling
regions, where larger phytoplankton (including diatoms) were more abundant,
production was still heavily reliant on regenerated forms of nutrients. Thus, both in the
DCM and upwelling countercurrents, nitrogen recycling via heterotrophy appears to
play a critical role in sustaining primary productivity.
5.2 Introduction
In the coastal eastern Indian Ocean adjacent to the west coast of Australia, oligotrophic
conditions generally predominate due to the influence of the Leeuwin Current (LC), a
poleward-flowing eastern boundary current typified by large-scale downwelling (Smith
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
116
et al., 1991; Woo et al., 2004), nitrate-depleted surface waters, a prominent deep
chlorophyll maximum (DCM) and low primary production (< 200 mg C m-2 d-1;
Chap. 3). However, wind-driven shelf countercurrents (Ningaloo and Capes Currents)
flow inshore of the LC during the austral summer (November to March), and can
enhance nitrate concentrations on the continental shelf through localized upwelling that
sources waters from the nutricline at the base of the Leeuwin Current. Phytoplankton
productivity in these countercurrents ranges between 850 and 1300 mg C m-2 d-1 during
the summer upwelling season (Chap. 3).
The chemical form and availability of dissolved inorganic nitrogen has a major
impact on pelagic food web dynamics (Legendre and Rassoulzadegan, 1995). Nitrate
(NO3-) is sourced from the deep ocean, and enters the euphotic zone through both
advective (e.g. upwelling) and diffusive fluxes. In contrast, ammonium (NH4+) is
generally supplied from biological recycling processes (e.g. cell degradation,
zooplankton excretion) occurring within surface waters (as reviewed in Zehr and Ward,
2002). The proportion of total primary production based on ‘new’ (NO3-) versus
regenerated (NH4+) nitrogen is calculated with the f-ratio of Eppley and Peterson
(1979):
-
34
-3
NONH
NO
where represents nitrogen uptake as measured using the 15N incubation technique
(Dugdale and Goering, 1967).
In more nitrate-dominated environments such as upwelling zones, the f-ratio is
usually high (> 0.5) and the herbivorous food web (based in large phytoplankton and
their zooplankton grazers) can predominate. In contrast, oligotrophic regions generally
have a very low f-ratio (< 0.2) and are more commonly characterised by the microbial
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
117
food web (based in pico- and nanophytoplankton and their protozoan grazers; Azam et
al., 1983, Cushing, 1989; Legendre and Rassoulzadegan, 1995). However, these food
webs are not necessarily mutually exclusive, and in the multivorous food web (defined
by Legendre and Rassoulzadegan, 1995) both herbivorous and microbial web pathways
play important and complementary roles. The multivorous web has been found across a
range of ecosystems, from the generally oligotrophic Aegean Sea (Siokou-Frangou et
al., 2002) to the Chilean upwelling system (Vargas and Gonzalez, 2004).
A large-scale oceanographic study off Western Australia allowed us to compare
nitrogenous nutrition and phytoplankton community composition of the oligotrophic
Leeuwin Current versus the highly productive countercurrents of the Gascoyne region.
We specifically tested the hypothesis that regenerated production and the microbial food
web would predominate in LC surface waters, while nitrate-driven new production
would be of greater importance at the Leeuwin Current DCM and within the upwelling-
influenced countercurrents. This was investigated though isotopic nitrogen uptake
experiments (15NO3-, 15NH4
+) and analysis of phytoplankton species composition and
abundance using both chemotaxonomic (via High Performance Liquid
Chromatography; HPLC) and microscopic methods.
5.3 Materials and Methods
All sampling and experimentation was undertaken during a two-week (13 – 27
November 2000) cruise on the RV Franklin (voyage FR10/00), from North West Cape
to the Abrolhos Islands (~ 21S to 30S), Western Australia (WA; Fig. 5.1). Eleven
cross-shore transects covered continental shelf (30 – 200 m), shelf break (200 – 300 m)
and offshore (300 – 4000 m) waters, and sampled the four main water types (Chap. 3;
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
118
Figure 5.1. Sampling stations along 11 cross-shelf transects undertaken adjacent to the
Gascoyne region of Western Australia. CTD casts and water sampling (nutrients, chl a)
were conducted at all stations, while specialized sampling at production stations
included 14C uptake, 15N uptake, particulate organic carbon and nitrogen (POC/PN), and
phytoplankton species composition (using both chemotaxonomic and microscopic
methods).
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
119
Woo et al., 2004) within the region: Leeuwin Current/offshore waters (LC); Ningaloo
Current (NC); Shark Bay outflow (SB); and Capes Current (CC).
5.3.1 Sample collection, processing and calculations
Water samples were collected using 5 L Niskin bottles mounted on a 24-bottle rosette,
equipped with a Seabird conductivity-temperature-depth (CTD) profiler, fluorometer,
dissolved O2 sensor and Li-Cor LI-192SA underwater quantum sensor. In addition to
standard oceanographic depths, sampling also targeted the deep chlorophyll maximum
(DCM), as identified by the downcast fluorescence trace. Dissolved inorganic nutrient
concentrations (nitrate + nitrite, phosphate, silicate) were measured on all samples using
a shipboard Alpkem Autoanalyser. Detection limits were 0.1 M for nitrate + nitrite
(hereafter nitrate), 0.01 M for phosphate and 0.1 M for silicate (Cowley, 1999). For
calibration of the in situ fluorometer, 2 L water samples from all sampling depths 150
m were filtered through Whatman GF/F filters, frozen at -20C and returned to the
laboratory for chlorophyll a (chl a) and pheopigment analysis. Pigments were extracted
in 90% acetone with grinding, and measured using a Turner Designs fluorometer
(detection limit of 0.01 mg chl a m-3) following the acidification technique of (Parsons
et al., 1989). In situ fluorescence was calibrated by using either a separate linear
regression for each station (minimum of 5 data points) or pooled data for each transect
(r2 = 0.76 – 0.92; Chap. 3).
At selected ‘production’ stations (Fig. 5.1), additional water samples were
collected from the surface (~ 2 m) and DCM for particulate organic carbon
(POC)/particulate nitrogen (PN) analysis, 14C photosynthesis vs. irradiance (PI)
experiments, 15N uptake experiments and determination of phytoplankton species
composition (detailed below). For POC/PN, 4 L was filtered through pre-combusted
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
120
Whatman GF/F filters and stored at -20C until analysis by mass spectrometer (for total
C, total N, 13C, 15N), following the preparation techniques of Knap et al. (1996)
which include the removal of inorganic carbon. The PI experiments followed the small-
volume, short-incubation-time technique of Lewis and Smith (1983), with full protocols
and modifications detailed in Chapter 3.
5.3.1.1 15N uptake Nitrogen uptake experiments consisted of separate nitrate (99% K15NO3
-) and
ammonium (99% 15NH4Cl) additions, at both trace (Dugdale and Goering, 1967) and
saturating levels (perturbation experiments). Due to existing analytical protocols in the
shipboard hydrochemistry laboratory, ambient NO3- concentrations could not be
obtained prior to the experiments, and ambient NH4+ concentrations were not measured.
As oligotrophic conditions were known to predominate in the study area, with NO3-
often below analytical detection limits in surface waters (Pearce, 1997), we used
0.05 M for trace experiments (as recommended by Knap et al., 1996). Inoculations for
perturbation experiments were 5.0 M.
Duplicate samples were incubated in acid-washed 500 mL glass Schott bottles
within a deck-board incubator. Temperature regulation was provided by continuous
surface seawater flow, and light attenuation for the DCM samples (1% of surface
irradiance for all stations) was achieved using neutral density screens. To avoid
substrate exhaustion, and match concurrent short-incubation-time 14C experiments, trace
incubations were ~ 1 h and conducted during daylight hours. Perturbation experiments
were incubated for a 24 h light-dark cycle. To assess any time-dependence of uptake in
the perturbation experiments, subsamples were taken every 6 h over the 24 h period at 5
production stations.
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
121
Experiments were terminated by filtration onto precombusted GF/F filters,
which were frozen at -20C until determination of total PN (g) and 15N atom %
enrichment by mass spectrometry. Absolute nitrogen uptake rates (; nmol N L-1 h-1)
were calculated following (Knap et al., 1996):
tN
PNN
enr15
txs15
where 15Nxs = excess 15N (measured 15N – 15N natural abundance of 0.3663 at %);
PNt = post-incubation particulate N (nmol L-1);
t = incubation time; and,
15Nenr = 15N enrichment in dissolved fraction.
15Nenr is a function of both ambient and labelled N concentrations, and was calculated
as: n15
1415
15
NNN
N100
where 15N = labelled N concentration (nM);
14N = unlabelled N concentration (nM); and,
15Nn = 15N natural abundance.
For a number of samples, 14N could not be estimated as ambient NO3- was below
analytical detection. Uptake rates for these samples were calculated assuming a
constant ½ of the detection limit (or 0.05 M 14NO3-) for 14N, which was more
conservative than using the lower limit of detection (e.g. Metzler et al., 1997).
Nitrogen-specific uptake rates (V; h-1) were calculated as:
tN
N
enr15
xs15
and are a measure of nitrogen uptake per unit of particulate N (Dugdale and Wilkerson,
1986).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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The f-ratio (Eppley and Peterson, 1979) is generally computed as:
-
34
-3
NONH
NO
However, with no measurement of ambient NH4+ concentrations, NH4
+ could not be
directly calculated for trace experiments. To provide an estimate of new production for
these samples, we used a modified f-ratio based on 15Nxs (which is directly proportional
to ):
-
3xs15
4xs15
-3xs
15
NONNHN
NON
This modified f-ratio allowed back-calculation of NH4+ as:
f
f-1NO-3
For perturbation experiments (5.0 M additions), ambient nitrate (14N) had a
minimal impact on the calculation of uptake rates (see Results section 5.4.1.2). Both
NO3- and NH4
+ were calculated following Knap et al. (1996), with the exception that
14N was not included in the estimate of 15Nenr. For these experiments, both standard
(Eppley and Peterson, 1979) and modified f-ratios were calculated.
5.3.1.2 Taxonomic analyses – chemical For analysis of taxonomically significant chlorophylls and carotenoids, 4 L water
samples were filtered through GF/F filters and stored under liquid nitrogen until
processing. Pigments were extracted in acetone (Parsons et al., 1989) and quantified
using HPLC following the ternary gradient method of Wright et al. (1991) as detailed in
Mackey et al. (1995). Note that the divinyl (DV) chlorophylls (a and b) could not be
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
123
separated with this technique, and thus reported concentrations of chl a and chl b
represent chl a + DV chl a and chl b + DV chl b, respectively.
The relative contribution of nine phytoplankton groups to the total chl a
concentration of each sample was assessed using the CHEMTAX (CHEMical
TAXonomy) matrix factorization program (Mackey et al., 1996). It must be clarified
that these groups do not strictly match standard taxonomic classes, as pigment content
can overlap between certain taxa and some species may be dominated by the pigment
signatures of their endosymbionts (e.g. cyanobacterial symbionts within both diatoms
and dinoflagellates; Jeffrey and Vesk, 1997).
In the absence of pigment ratios for phytoplankton specific to the coastal eastern
Indian Ocean, we have used ratios representative of ‘equatorial species’ as given in
Mackey et al. (1996). Prochlorophytes were included in the analysis, as CHEMTAX
can distinguish this group even in the absence of separate DV chl a and b concentrations
by using the zeaxanthin:chl b ratio characteristic of this group (Mackey et al., 1996).
However, since myxoxanthophyll (found in filamentous cyanobacteria; Carpenter et al.,
1993) was not included in the suite of pigments measured, there was no way to
distinguish between Trichodesmium-type and Synechococcus-type cyanobacteria. As
Trichodesmium sp. filaments were relatively rare (see Results), we used the
Synechococcus sp. zeaxanthin:chl a ratio for CHEMTAX calculations. Also note that
euglenophytes were excluded from the CHEMTAX analysis, as they were not observed
in cell counts.
The results of the CHEMTAX analysis are matrices that give the relative and
absolute abundances of each phytoplankton group as a proportion of the total chl a
within each sample. As pigment ratios are known to vary with depth, surface (n = 18)
and DCM (n = 19) samples were analysed separately. It is also recommended that
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
124
samples from different oceanographic regions be analysed as separate groups, however
this further sub-grouping was not possible due to the small sample sizes involved (the
minimum recommended sample size for CHEMTAX analysis is ~ 20; Mackey et al.,
1996).
5.3.1.3 Taxonomic analyses – microscopic Water samples (~ 100 mL) for microscopic analysis were preserved with acid Lugol’s
solution (Parsons et al., 1989) and returned to the laboratory. The entire volume was
sedimented and enumerated using an inverted microscope (Utermohl, 1958) at 400
magnification, with identification to species level where possible. The minimum cell
size enumerated was 5 m. For comparison with HPLC analyses, data from each
station was also grouped into the following eight taxonomic categories: diatoms,
cyanobacteria (filamentous), chrysophytes, haptophytes (coccolithophores and
prymnesiophytes), cryptophytes, dinoflagellates, prasinophytes and flagellates
(< 20 m, unidentified). Data were also grouped according to depth (surface vs. DCM)
and water type (LC/offshore vs. shelf/countercurrent), with mean cell count and
percentage abundance calculated for the major phytoplankton groups. Note that
coccolithophore abundance may have been underestimated due to the use of an acidic
preservative (Sournia, 1978).
5.4 Results
5.4.1 Nitrogen uptake
5.4.1.1 Trace-level (0.05 M) additions Trace additions (0.05 M) ranged between ~ 5 and 50 % enrichment, depending on
ambient nitrate levels (and assuming a minimum concentration of 0.05 M for samples
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
125
below the analytical detection limit). Absolute nitrate uptake rates for all stations and
depths ranged between 0.5 and 7.1 nmol L-1 h-1. In Ningaloo Current/Capes Current
(NC/CC) waters, NO3- uptake was not significantly different (Mann-Whitney U-test) at
the surface (3.0 2.1 nmol L-1 h-1; mean SD) compared to the DCM (2.7 2.3 nmol
L-1 h-1; Fig. 5.2a). However, in Leeuwin Current/offshore (LC) waters, rates were
significantly lower at the surface (1.2 0.7 nmol L-1 h-1) than the DCM (3.9 2.5
nmol L-1 h-1; Mann-Whitney U test, p = 0.05). PN-specific nitrate uptake rates (Fig.
5.2b) ranged between 0.001 and 0.016 h-1 and showed no significant differences
between surface and DCM (Mann-Whitney U test, p = 0.63 for NC/CC and p = 0.22 for
LC/offshore).
The modified f-ratio ranged between 0.06 and 0.28 at the surface, and 0.03 to
0.32 at the DCM for all stations. Mean values showed a remarkable constancy across
sampling depth and water type (Fig. 5.2c): within NC/CC waters, the ratio averaged
0.17 0.07 and 0.16 0.06 at the surface and DCM, respectively; and within LC
waters, averaged 0.14 0.05 at the surface and 0.14 0.09 at the DCM (Fig. 5.2c).
This indicates that, for the trace-level experiments, ammonium accounted for
approximately 85% of the total nitrogen (NO3- + NH4
+) uptake at both the surface and
DCM.
The mean C:N ratio of particulate matter was similar to the Redfield ratio of
6.6:1 (Redfield, 1958) for both LC/offshore and shelf/countercurrent waters (Table 5.1).
We examined the ability for the measured carbon (from P vs. I experiments; Chaps. 3
and 4) and nitrogen (NO3- + NH4
+) uptake to account for the mean C:N ratio of
particulate matter by calculating the C:N uptake ratio. Despite some high variability in
C and N uptake (Table 5.1), it was evident that the combination of NO3- and NH4
+
uptake could account for the carbon uptake observed in the same water samples. The
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
126
Figure 5.2. Results from trace-level (0.5 M enrichment) N-uptake experiments for
surface and DCM samples within the Ningaloo and Capes Currents (NC, CC), and
Leeuwin Current/offshore waters (LC); (a) absolute nitrate uptake rates (nmol L-1 h-1),
(b) PN-specific nitrate uptake (h-1) and (c) the modified f-ratio (see text). Values are
mean SD.
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
127
single exception was in NC/CC/SB surface waters, where C:N uptake (13.5 7.2; mean
SD) was somewhat higher than C:N biomass (7.2 1.0).
A limited number of samples from these experiments were true trace-level
nitrate additions, from DCM depths where 14NO3- ranged between 0.3 and 0.8 M and
resulting 15NO3- enrichments were 14 %. Measurements of NO3
- for this subset of
samples ranged from 1.7 to 6.4 nmol L-1 h-1 for the Ningaloo Current and 1.5 to 7.1
nmol L-1 h-1 for Leeuwin Current/offshore waters, with corresponding modified f-ratios
of 0.19 – 0.24 and 0.03 – 0.32, respectively (Table 5.2).
5.4.1.2 Perturbation experiments (5.0 M additions)
Calculation of 15Nenr for the perturbation experiments (5.0 M additions) using only 15N
(instead of 14N + 15N) resulted in mean uptake rates that were reduced by 1.7 3.6 % as
calculated for NO3-. This difference was considered minimal, and thus allowed for
confidence in the calculation of NH4+ and VNH4
+ for these experiments in the absence
of ambient NH4+ measurements. These NH4
+ values were then used to verify the
accuracy of both the modified f-ratio and back-calculations of NH4+ used in the
interpretation of trace-level data. Comparison of the modified f-ratio (based on 15Nxs)
with the actual f-ratio (based on NO3- and NH4
+) for perturbation experiments gave a
near 1:1 linear correlation (y = 0.96x + 0.0, r2 = 0.91, p < 0.001), indicating that the
modified f-ratio could provide a good estimate of new production. A strong linear
correlation was also found between NH4+ back-calculated from the modified f-ratio
and NH4+ calculated following Knap et al. (1996): y = 0.85x + 0.81, r2 = 0.90,
p < 0.001. The back-calculated values of NH4+ were therefore approximately 15 %
lower than the ‘true’ values, providing a reasonable but somewhat conservative estimate
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Table 5.1. Mean ( SD) rates of carbon (nmol L-1 h-1) and nitrogen (trace-level
incubations; nmol L-1 h-1) uptake and the corresponding molar C:N ratio for uptake and,
measured separately, particulate matter (biomass). All DCM uptake rates were
measured at 1.0 % of surface irradiance.
Water type Depth C uptake
NO3-+NH4
+ uptake
C:N uptake
C:N biomass
LC/offshore Surface 33.2 (12.1)
11.1 (7.5)
4.4 (3.3)
6.6 (1.0)
DCM 21.9 (5.2)
18.6 (13.0)
2.0 (1.7)
6.8 (1.2)
NC, CC, SB Surface 129.9 (39.6)
11.7 (5.1)
13.5 (7.2)
7.2 (1.0)
DCM 34.6 (11.9)
14.4 (10.3)
3.2 (2.1)
7.4 (0.8)
Table 5.2. Absolute (NO3
-) and PN-specific (VNO3-) uptake rates, ambient nitrate
concentrations (NO3-; M) and the modified f-ratio (see text) for samples where 15NO3
-
enrichment was 14 %. These samples were all from the deep chlorophyll maximum
(DCM) in both Ningaloo Current (NC) and Leeuwin Current/offshore (LC) waters.
Water type Stn Depth (m) NO3
- (M)
Enrich (%)
NO3-
(nM h-1) VNO3
- (h-1) f-ratio
NC 15 46 0.3 14 6.4 0.010 0.19 28 64 0.6 7 1.7 0.002 - 42 55 0.4 11 4.3 0.004 0.24
LC 55 90 0.8 6 3.8 0.005 0.03 101 79 0.8 6 6.3 0.010 0.32 112 69 0.5 9 1.5 0.003 0.07 116 94 0.5 9 7.1 0.016 0.19 131 80 0.4 11 3.8 0.006 0.16
‘-‘ no data
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
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of this parameter.
Perturbation experiments are generally considered a physiological measure of
the ability of cells to take up saturating concentrations of a given nutrient. Results for
these experiments contrasted with trace experiments in that for the majority of cases,
measurements of absolute uptake, PN-specific uptake and the modified f-ratio were
significantly higher (Mann Whitney U, p < 0.05) for surface waters than the DCM (Fig.
5.3). The single exception was absolute NH4+ uptake in LC/offshore waters, which was
similar at the surface and DCM (3.63 1.5 and 2.59 0.9 nmol L-1 h-1, respectively;
p = 0.12). Mean f-ratios ranged between 0.08 and 0.26, confirming the importance of
ammonium for phytoplankton production throughout the study area (Fig. 5.3e).
The time series experiments were used to evaluate whether labelled substrate
became exhausted or was diluted (as may occur with NH4+ remineralization; Glibert et
al., 1982) during the 24 h incubation, and whether uptake rates exhibited a diel pattern.
Nitrate and ammonium uptake as a function of incubation time (in 6 h intervals) was
assessed for the surface and DCM using linear regression; no significant relationship
was found (p >> 0.05). There was also no significant difference according to time of
day (measurements grouped as ‘night’ from 19:00 to 05:30 and ‘day’ from 05:30 to
19:00; Mann-Whitney U test, p >> 0.05).
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Figure 5.3. Results from perturbation (5.0 M enrichment) N-uptake experiments for
surface and DCM samples within the Ningaloo and Capes Currents (NC, CC), and
Leeuwin Current/offshore waters (LC); (a,b) absolute (nM h-1) and PN-specific (h-1)
nitrate uptake, (c,d) absolute (nM h-1) and PN-specific (h-1) ammonium uptake (d) the
modified f-ratio (see text). Values are mean SD.
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
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5.4.2 Species composition and abundance
Phytoplankton taxonomic composition and abundance was assessed by two distinct
methods: chemotaxonomy via HPLC analysis of pigments, and cell counts via light
microscopy.
5.4.2.1 Chemotaxonomic analyses The CHEMTAX program provides a quantitative assessment of phytoplankton group
abundance based on HPLC analyses, and is quite robust to random errors in both
pigment ratios and input data (Mackey et al., 1996). However, the calculations are most
accurate when initial pigment ratios are known for the region under study. Using a set
of pigment ratios representative of ‘equatorial species’ (Mackey et al., 1997b), we
found excellent agreement (< 5 % deviation) between these initial ratios and the
pigment ratios from our field data for the majority of phytoplankton groups. In fact, for
6 of 9 groups, the initial pigment ratios underwent no modification during the
CHEMTAX iteration procedure (Table 5.3), indicating an excellent match to the ‘true’
ratios found in the field samples. Exceptions to this were the haptophytes, chrysophytes
and cyanobacteria, where modifications of up to 300 % were made to fit the observed
field ratios (Table 5.3). The maximum recommended variation for these ratios during
the iteration procedure is 500 % (Mackey et al., 1996).
Phytoplankton group abundances, as the relative contribution to total chl a in
each sample, were obtained for 18 surface and 19 DCM samples. This data was then
evaluated with complete-linkage hierarchical cluster analysis (STATISTICA), using the
Bray-Curtis similarity coefficient, to identify groups of stations with similar
phytoplankton assemblages. At the surface, three main clusters containing samples with
70% similarity were identified (Clusters 1s, 2s, 3s), with a fourth ‘cluster’ (4s)
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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Table 5.3. Initial pigment ratios for the nine principal phytoplankton groups, and the
final ratios as calculated by CHEMTAX for surface and DCM samples (bold numbers
indicate values modified by > 5% from the initial ratios).
Perid 19but Fuco 19hex Pras Viol Diad Allo Zeax Chl b Chl a
(a) Initial pigment ratios Pras 0 0 0 0 0.14 0.03 0 0 0 0.41 0.43 Dino 0.46 0 0 0 0 0 0.10 0 0 0 0.43 Crypto 0 0 0 0 0 0 0 0.19 0 0 0.81 Hapto 0 0 0 0.61 0 0 0.04 0 0 0 0.36 Chryso 0 0.15 0.40 0 0 0 0.04 0 0 0 0.41 Chloro 0 0 0 0 0 0.04 0 0 0.01 0.20 0.75 Prochl 0 0 0 0 0 0 0 0 0.13 0.45 0.42 Cyano 0 0 0 0 0 0 0 0 0.26 0 0.74 Diat 0 0 0.40 0 0 0 0.07 0 0 0 0.53 (b) Final pigment ratios – surface samples Praso 0 0 0 0 0.14 0.03 0 0 0 0.41 0.43 Dino 0.46 0 0 0 0 0 0.10 0 0 0 0.43 Crypto 0 0 0 0 0 0 0 0.19 0 0 0.81 Hapto 0 0 0 0.32 0 0 0.14 0 0 0 0.53 Chryso 0 0.24 0.19 0 0 0 0.04 0 0 0 0.52 Chloro 0 0 0 0 0 0.04 0 0 0.01 0.20 0.75 Prochl 0 0 0 0 0 0 0 0 0.13 0.45 0.42 Cyano 0 0 0 0 0 0 0 0 0.54 0 0.46 Diat 0 0 0.40 0 0 0 0.07 0 0 0 0.53 (c) Final pigment ratios – DCM samples Praso 0 0 0 0 0.14 0.03 0 0 0 0.41 0.43 Dino 0.46 0 0 0 0 0 0.10 0 0 0 0.43 Crypto 0 0 0 0 0 0 0 0.19 0 0 0.81 Hapto 0 0 0 0.56 0 0 0.04 0 0 0 0.40 Chryso 0 0.44 0.07 0 0 0 0.01 0 0 0 0.49 Chloro 0 0 0 0 0 0.04 0 0 0.01 0.20 0.75 Prochl 0 0 0 0 0 0 0 0 0.13 0.45 0.42 Cyano 0 0 0 0 0 0 0 0 0.27 0 0.73 Diat 0 0 0.40 0 0 0 0.07 0 0 0 0.53 Pigment abbreviations: Perid, peridinin; 19but, 19’-butanoyloxyfucoxanthin; Fuco, fucoxanthin; 19hex, 19’-hexanoyloxyfucoxanthin; Pras, prasinoxanthin; Viol, violaxanthin; Diad, diadinoxanthin; Allo, alloxanthin; Zeax, zeaxanthin; Chl b, chlorophyll b; Chl a, chlorophyll a. Note that neoxanthin and lutein were not detected in any samples and thus not included in the Praso and Chloro pigment ratios. Phytoplankton group abbreviations: Praso, prasinophytes; Dino, dinoflagellates; Crypto, cryptophytes; Hapto, haptophytes; Chryso, chrysophytes; Chloro, chlorophytes; Prochl, prochlorophytes; Cyano, cyanobacteria; Diat, diatoms.
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
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containing a single station (Fig. 5.4a). Most distinctive was Cluster 1s, which contained
over half of the surface samples, and was dominated by cyanobacteria (mean SD of
65.2 7.0 %) and haptophytes (32.0 6.1%), with small amounts (0.1 – 1.7 %) of
prochlorophytes, chlorophytes, cryptophytes and diatoms (Fig. 5.4b). This cluster
included all of the Leeuwin Current/offshore stations, plus the northern-most Ningaloo
Current station (Stn 15; Fig. 5.5). Cluster 2s (NC stations 40 and 42) was also
dominated by cyanobacteria (40.3 9.4 %) and haptophytes (23.1 1.8 %), but
additionally had large contributions from chlorophytes (16.7 15.2 %), chrysophytes
(9.3 2.6 %) and prochlorophytes (6.0 8.5 %). Cluster 3s, composed of a mix of NC,
CC and SB stations (Figs. 5.4b and 5.5), was the only surface cluster with prasinophytes
(1.4 3.0 %), although the principal groups were haptophytes (35.3 9.2 %),
cyanobacteria (20.1 5.5 %), chrysophytes (18.1 1.4%), prochlorophytes (9.4 2.8
%) and diatoms (6.7 5.3 %). Station 90 (Shark Bay outflow; 4s) showed distinctive
characteristics that separated it at the 50% similarity level from Cluster 3s (Fig. 5.4a).
In addition to a large contribution from haptophytes (57.3%), this station had the highest
diatom (19.6 %) and lowest cyanobacteria (13.4 %) abundance of all surface samples.
The DCM stations also clustered into three main groups (1d, 2d, 3d) at
approximately the 70 % similarity level (Fig. 5.6a). Cluster 1d included all the LC
stations (Fig. 5.7), which were dominated by prochlorophytes (32.3 7.5 %),
cyanobacteria (22.6 6.1 %), haptophytes (21.1 3.4 %) and chrysophytes (20.1
3.9 %), with minor contributions (0.3 – 2.0 %) from chlorophytes, cryptophytes,
prasinophytes and diatoms. Cluster 2d incorporated the four southern-most NC stations
(Fig. 5.7), which had a high concentration of cyanobacteria (38.5 11.6 %), moderate
amounts of haptophytes (16.4 3.4 %) and prochlorophytes (12.4 5.3 %), and fairly
equal proportions of chrysophytes, cryptophytes, diatoms and prasinophytes (5.8 –
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Figure 5.4. (a) Cluster analysis (using Bray-Curtis similarity coefficient) of
CHEMTAX results for surface samples, which identified 4 main clusters at the 70%
similarity level; (b) the mean relative contribution of the different phytoplankton groups
in each cluster, and associated water type (LC, Leeuwin Current/offshore; NC, Ningaloo
Current; CC, Capes Current; SB, Shark Bay outflow).
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
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Figure 5.5. The geographic location of the four main chemotaxonomic clusters (see
Fig. 5.4) identified in surface (< 2 m) waters.
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Figure 5.6. (a) Cluster analysis (using Bray-Curtis similarity coefficient) of
CHEMTAX results for DCM samples, which identified 3 main clusters at the ~ 70%
similarity level; (b) the mean relative contribution of the different phytoplankton groups
in each cluster, and associated water type (LC, Leeuwin Current/offshore; NC, Ningaloo
Current; CC, Capes Current; SB, Shark Bay outflow).
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
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Figure 5.7. The geographic location of the three main chemotaxonomic clusters (see
Fig. 5.6) identified at the DCM.
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9.6 %; Fig. 5.6b). Cluster 3d, containing SB, CC and northern NC stations (Fig. 5.7),
was dominated by haptophytes (25.4 7.5 %) and diatoms (22.2 7.7 %), with lower
amounts of chrysophytes (13.3 5.3 %), cryptophytes (11.6 2.4 %), cyanobacteria
(11.2 6.6 %), prochlorophytes (9.2 3.5 %) and prasinophytes (6.7 3.8 %). This
cluster also included a small amount of dinoflagellates (0.4 0.8 %), the only notable
occurrence of this group in the HPLC data.
5.4.2.2 Microscopic analyses Both the surface and DCM of Leeuwin Current/offshore and shelf/countercurrent
stations were numerically dominated by small (5 – 20 m), unidentified flagellates
(Table 5.4; note that cells < 5 m could not be enumerated). Mean flagellate
abundance, as calculated for shelf/countercurrent (NC, CC, SB) and Leeuwin
Current/offshore (LC) waters, ranged from 44 to 63 % of the total cell counts (Table
5.4).
The second-most abundant group was the diatoms, which accounted for 24 to
40 % of mean cell counts (Table 5.4). Approximately 76 species were recorded, with
centric diatoms accounting for the majority (74 %) of these. However, although the
pennate diatoms exhibited lower species diversity, they were generally numerically
dominant over centric species. The exception to this was in NC/CC/SB surface waters,
where centrics were most abundant (Table 5.4). The principal diatom species were
remarkably consistent both between surface and DCM within a water type, and also
between different water types. Nitzschia closterium, Pseudonitzschia
pseudodelicatissima and unidentified small (< 40 m) pennates were most commonly
encountered. For the centrics, Chaetoceros sp., Skeletonema sp., Bacteriastrum
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
139
furcatum and Leptocylindrus danicus were widespread, with C. pseudocurvisetus
dominating NC/CC/SB surface waters (Table 5.4).
The dinoflagellate taxa were primarily composed of heterotrophic species such
as unidentified gymnodinioids, Heterocapsa cf. niei, Oxytoxum cf. gracile, Katodinium
rotundata, Amphidinium sp. and Protoperidinium sp. (Table 5.4). Leeuwin Current
surface waters had the highest mean proportion of dinoflagellates (8.3 % of total cell
counts), with the lowest amount found in NC/CC/SB surface waters (3.7 %). The deep
chlorophyll maximum of both regions was composed of ~ 6 % dinoflagellate cells
(Table 5.4).
The Haptophyceae (a.k.a. Prymnesiophyceae) were numerically dominated by
one species, Emiliania huxleyi, which accounted for ~ 80 to 90 % of the cell count
within this class (Table 5.2). Other recorded coccolithophore species included
Anoplosolenia brasilienis (all regions except the LC DCM), Discosphaera tubifer (all
regions except NC/CC/SB surface waters) and Calciopappus sp. (LC waters only).
Pheocystis sp. exhibited fairly low abundance, with highest mean concentration
(40 cells L-1) recorded in NC/CC/SB surface waters (Table 5.4).
Unidentified cryptophytes accounted for up to 3.4 % of total cell counts, and
were least abundant in NC/CC/SB surface waters (2.0 %; Table 5.4). Chrysophytes
were most commonly represented by the silicoflagellate Octactis octonaria, which was
present in all regions except the LC DCM (Table 5.4). Other minor ( 0.1 %
abundance) groups included prasinophytes (Pyramimonas sp. and/or Pachysphaera sp.)
and filamentous cyanobacteria (Trichodesmium/Oscillatoria sp.; Table 5.4).
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Table 5.4. Mean (cells L-1) and percentage abundance (in parentheses) of major
phytoplankton groups and principal species at the surface and deep chlorophyll
maximum (DCM) in shelf/countercurrent waters (Ningaloo Current, Capes Current,
Shark Bay outflow; NC, CC, SB) and Leeuwin Current/offshore waters (LC).
NC, CC, SB – Surface Mean (%) LC – Surface Mean (%) Total 109545 (100) Total 57761 (100) Unidentified flagellates (< 20m) 67210 (61.4) Unidentified flagellates (< 20m) 25512 (44.2) CHROMOPHYTA CHROMOPHYTA Bacillariophyceae Bacillariophyceae
Bacillariales (pennate) 13605 (12.4) Bacillariales (pennate) 18015 (31.2) Pseudonitzschia pseudodelicatissima 6198 Nitzschia closterium 11241 Nitzschia closterium 3578 Pseudonitzschia pseudodelicatissima 3342 Pseudonitzschia pungens 1577 Unidentified small pennates (<40m) 1574 Unidentified small pennates (<40m) 812 Navicula/Nitzschia sp. (40-100m) 638 Navicula/Nitzschia sp. (40-100m) 339 Nitzschia sp. (small) 274 Thalassiothrix sp. 224 Thalassionema nitzschoides 268 Others 877 Others 677
Biddulphiales (centric) 18608 (17.0) Biddulphiales (centric) 4527 (7.8) Chaetoceros pseudocurvisetus 3052 Chaetoceros sp. (large) 932 Chaetoceros sp. (large) 2833 Skeletonema sp. 809 Leptocylindrus danicus 1894 Bacteriastrum furcatum 632 Skeletonema sp. 1398 Guinardia striata 472 Chaetoceros sp. (small) 1101 Chaetoceros cf. tenuissimus 219 Bacteriastrum furcatum 1092 Leptocylindrus danicus 211 Others 7238 Others 1251
Dinophyceae 4148 (3.7) Dinophyceae 4800 (8.3) Unidentified gymnodinioid (small) 1816 Unidentified gymnodinioid (small) 1898 Heterocapsa cf. niei 1053 Heterocapsa cf. niei 1190 Unidentified gymnodinioid (medium) 287 Unidentified gymnodinioid (medium) 472 Scripsiella trochoidea 166 Oxytoxum cf. gracile (short) 239 Katodinium rotundata 163 Alexandrium cf. minutum 206 Alexandrium cf. minutum 94 Alexandrium/Scripsiella sp. 88 Oxytoxum cf. gracile (short) 90 Gyrodinium sp. 77 Amphidinium sp. 45 Protoperidinium sp. 63 Others 434 Others 567
Haptophyceae/Prymnesiophyceae 3529 (3.2) Haptophyceae/Prymnesiophyceae 2830 (4.9) Emiliania huxleyi 3181 Emiliania huxleyi 2332 Unidentified prymnesiophyte 217 Discosphaera tubifer 106 Unidentified coccolithophore 69 Unidentified coccolithophore 96 Phaeocystis sp. 40 Unidentified prymnesiophyte 74 Others 22 Others 222
Cryptophyceae 2175 (2.0) Cryptophyceae 1970 (3.4) Unidentified cryptophyte (small) 2090 Unidentified cryptophyte (small) 1846 Unidentified cryptophyte (large) 85 Unidentified cryptophyte (large) 124
Chrysophyceae 125 (0.1) Chrysophyceae 33 (0.1) Octactis octonaria 115 Octactis octonaria 22 Apedinella sp. 10 Apedinella sp. 11
CHLOROPHYTA CHLOROPHYTA Prasinophyceae 127 (0.1) Prasinophyceae
Pyramimonas sp. 92 Pachysphaera sp. 62 (0.1) Pachysphaera sp. 35
CYANOPHYTA CYANOPHYTA Trichodesmium/Oscillatoria sp. 19 (<0.1) Trichodesmium/Oscillatoria sp. 13 (<0.1)
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
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Table 5.4. Cont’d.
NC, CC, SB – DCM Mean (%) LC – DCM Mean (%) Total 63217 (100) Total 66275 (100) Unidentified flagellates (< 20m) 37856 (59.9) Unidentified flagellates (< 20m) 41962 (63.3) CHROMOPHYTA CHROMOPHYTA Bacillariophyceae Bacillariophyceae
Bacillariales (pennate) 10322 (16.3) Bacillariales (pennate) 9703 (14.6) Nitzschia closterium 3846 Nitzschia closterium 5085 Pseudonitzschia pseudodelicatissima 3011 Pseudonitzschia pseudodelicatissima 2674 Unidentified small pennates (<40m) 1300 Unidentified small pennates (<40m) 697 Pseudonitzschia pungens 546 Navicula/Nitzschia sp. (40-100m) 448 Navicula/Nitzschia sp. (40-100m) 532 Thalassionema nitzschoides 172 Thalassionema nitzschoides 334 Navicula sp. (<70m) 96 Others 753 Others 530
Biddulphiales (centric) 6578 (10.4) Biddulphiales (centric) 6089 (9.2) Chaetoceros sp. (large) 1844 Chaetoceros sp. (large) 1194 Leptocylindrus danicus 813 Bacteriastrum furcatum 721 Chaetoceros pseudocurvisetus 384 Chaetoceros sp. (small) 704 Chaetoceros affinis 378 Skeletonema sp. 447 Bacteriastrum furcatum 344 Leptocylindrus danicus 351 Skeletonema sp. 340 Chaetoceros pseudocurvisetus 301 Others 2476 Others 2370
Dinophyceae 3742 (5.9) Dinophyceae 4360 (6.6) Unidentified gymnodinioid (small) 1399 Unidentified gymnodinioid (small) 1257 Heterocapsa cf. niei 823 Heterocapsa cf. niei 1194 Unidentified gymnodinioid (medium) 311 Unidentified gymnodinioid (medium) 487 Oxytoxum cf. gracile (short) 204 Oxytoxum cf. gracile (short) 414 Oxytoxum cf. gracile (long) 111 Alexandrium/Scripsiella sp. 176 Alexandrium cf. minutum 90 Gyrodinium sp. 109 Katodinium rotundata 88 Katodinium rotundata 94 Scripsiella trochoidea 73 Oxytoxum cf. gracile (long) 90 Others 645 Others 540
Haptophyceae/Prymnesiophyceae 2460 (3.9) Haptophyceae/Prymnesiophyceae 2337 (3.5) Emiliania huxleyi 2132 Emiliania huxleyi 1889 Halopappus/Michaelsarsia sp. 145 Unidentified prymnesiophyte 181 Unidentified prymnesiophyte 59 Calciopappus sp. 69 Unidentified coccolithophore 32 Syracosphaera sp. 58 Others 93 Others 139
Cryptophyceae 2100 (3.3) Cryptophyceae 1775 (2.7) Unidentified cryptophyte (small) 2001 Unidentified cryptophyte (small) 1675 Unidentified cryptophyte (large) 99 Unidentified cryptophyte (large) 100
Chrysophyceae 1 (<0.1) Chrysophyceae 0 (0) Octactis octonaria 1
CHLOROPHYTA CHLOROPHYTA Prasinophyceae 87 (0.1) Prasinophyceae
Pachysphaera sp. 44 Pyramimonas sp. 37 (0.1) Pyramimonas sp. 42
CYANOPHYTA CYANOPHYTA Trichodesmium/Oscillatoria sp. 71 (0.1) Trichodesmium/Oscillatoria sp. 11 (<0.1)
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5.4.2.3 Comparison – chemotaxonomy vs. microscopy As two separate methods were used to examine phytoplankton species composition, we
undertake here a direct comparison of the main results from each. As generally
indicated above, the relative abundance of major phytoplankton groups was notably
different in HPLC data compared to microscopic data. This is further illustrated by a
detailed comparison of taxonomic abundance for individual stations from the four main
water types (Fig. 5.8). For example, the diatom fraction was of much greater relative
magnitude based cell counts than based on pigment concentration, especially in surface
waters (Fig. 5.8). These differences are not unexpected, as these two methods are quite
distinct from each other: cell counts provide an estimate of numerical abundance, while
HPLC analyses provide an estimate of biomass as pigment concentration (addressed
further in the Discussion). This was demonstrated by the absence of a relationship
between cell count and pigment concentration (Fig. 5.9). These two estimates are also a
measure of different size fractions, as microscopic analyses were restricted to cells > 5
m, and therefore could not estimate the picoplankton fraction (which included
cyanobacteria and prochlorophytes) that formed an important component of the HPLC
data (Figs. 5.4, 5.6, and 5.8).
5.4.3 Nitrate uptake as a function of species composition
Relationships between the absolute biomass of each of the CHEMTAX-derived
phytoplankton groups and nitrate uptake from the trace experiments were examined
using linear regression. The only statistically significant correlations were found in
surface waters, where cryptophytes, haptophytes and prochlorophytes each exhibited
positive relationships that accounted for 48 %, 56 % and 39 % of the observed variance
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
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*unidentified flagellates (5-20 m, cell counts only)
+chlorophytes and prochlorophytes (detected by HPLC only)
Figure 5.8. Comparison of HPLC-derived species composition with microscopic cell
counts for representative stations (in brackets) from each water type (LC, Leeuwin
Current/offshore; NC, Ningaloo Current; SB, Shark Bay outflow; CC, Capes Current).
The HPLC results include all cells > 0.7 m, while the minimum cell size enumerated
using light microscopy was 5 m.
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Figure 5.9. Total cell count (from light microscopy) vs. chl a concentration (from
HPLC analyses) for surface and deep chlorophyll maximum (DCM) samples.
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
145
in NO3-, respectively (Table 5.5).
5.4.4 Stable isotope signatures
The mean stable isotope signatures of particulate matter were significantly different
between shelf/countercurrent waters and Leeuwin Current/offshore waters (MANOVA,
F(2,29) = 8.28, p < 0.01; one outlier > 3 s.d. from the mean was excluded). The primary
contributor to this difference was 15N (Fig. 5.10), which was significantly lower (t-test,
p < 0.01) in LC waters (mean SE of -0.3 0.5 o/oo) compared to NC/CC/SB waters
(1.99 0.4 o/oo). Mean 13C ranged between -24.3 o/oo and -24.9 o/oo (Fig. 5.10).
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Table 5.5. Coefficients of determination (r2) and associated levels of statistical
significance (p-value) for the regression of NO3- (trace-level incubations) on
phytoplankton group biomass (absolute abundance as proportion of total chl a in
mg m-3) for all samples from the surface and deep chlorophyll maximum (DCM).
Phytoplankton group abbreviations as per Table 3.
Surface DCM Group r2 p r2 p Pras - - 0.01 n.s. Dino - - - - Crypto 0.11 n.s. 0.03 n.s. Hapto 0.48 < 0.05 0.04 n.s. Chryso 0.56 < 0.01 0.07 n.s. Chloro 0.07 n.s. 0.10 n.s. Prochl 0.39 < 0.05 0.04 n.s. Cyano 0.00 n.s. 0.02 n.s. Diat 0.13 n.s. 0.00 n.s.
n.s. not significant
‘-‘ no biomass
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
147
Figure 5.10. Mean ( SE) stable isotope ratios (o/oo) for surface (n = 16) and DCM
(n = 16) samples from shelf/countercurrent (NC, SB, CC) and LC/offshore waters.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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5.5 Discussion
This study provides the first estimates of nitrogen nutrition and phytoplankton
community composition in a broad section of the coastal eastern Indian Ocean, adjacent
to the west coast of Australia. We specifically examined the hypothesis that regenerated
production and the microbial loop would predominate within Leeuwin Current (LC) and
offshore surface waters, while nitrate-driven new production would be of greater
importance within the deep chlorophyll maximum (DCM) and the upwelling-influenced
countercurrents. Despite some of the methodological limitations of this dataset, we
have shown that regenerated ammonium-based production plays a key role throughout
the study area, within both surface and DCM waters of the Leeuwin and also the higher
productivity Ningaloo Current, Capes Current and shelf waters. Yet these regions did
separate on the basis of phytoplankton composition (potentially associated with
different trophic pathways, sensu Legendre and Rassoulzadegan, 1995), as identified
through the novel application of chemotaxonomic methods within the study area.
5.5.1 Nitrogen nutrition
5.5.1.1 New vs. regenerated production
The prevalence of ammonium-based production has long been recognized in
oligotrophic and stratified systems (Eppley and Peterson, 1979; Cushing, 1989). More
recently, however, the importance of nutrient recycling in upwelling ecosystems has
also been highlighted (e.g. Kudela et al., 1997; Bode et al., 2004), challenging the
simplified views of the traditional nitrate-based herbivorous food chain in these systems
(Cushing, 1989). For example, in the upwelling region off the coast of Spain, nutrient
regeneration during upwelling pulses can account for up to 50% of primary productivity
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
149
(Bode and Varela, 1994), with heterotrophic microplankton (bacteria, flagellates and
ciliates) as the primary agents of remineralization (Bode et al., 2004).
Mesozooplankton (> 200 m; mostly copepods) contributed less than 15% to
ammonium inputs, and had a minimal grazing impact on phytoplankton populations
(Bode et al., 2004).
This more closely matches the characteristics of a multivorous food web, where
herbivorous and microbial web pathways coexist and significant coupling is exhibited
between these two trophic modes (Legendre and Rassoulzadegan, 1995). Actively
grazing micro- and mezozooplankton can contribute both to the ammonium pool (via
excretion) and the dissolved organic carbon (DOC) and DON pools through, for
example, sloppy feeding (Roy et al., 1989) and fecal pellet degradation (Jumars et al.,
1989). Fluxes of ‘new’ (nitrate) nitrogen, which support the production of large
phytoplankton within these systems, are therefore channelled into the microbial web to
support bacterial and picoplanktonic production (Legendre and Rassoulzadegan, 1995).
In the sporadic upwelling system associated with the Ningaloo Current,
ammonium regeneration and the microbial web obviously play large parts in sustaining
productivity levels that may have initially been generated by advective nitrate fluxes.
While diatoms formed an important component of cell counts in Ningaloo waters, the
dominance of pico- and nano-planktonic groups (as revealed by the chemotaxonomic
HPLC analyses) and the low f-ratio supports this theory. One reason for the potentially
small contribution of the herbivorous food web is that absolute levels of nitrate injection
are capped in this region by the influence of the Leeuwin Current, and in this study were
a maximum of 2 – 6 M within the euphotic zone (Chap. 3). This is notably lower than
in other eastern boundary regions, where coastal upwelling can access nitrate
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
150
concentrations as high as 20 – 30 M (Dickson and Wheeler, 1995; Kudela et al.,
1997).
Yet absolute nitrate uptake rates, while low, showed interesting patterns in
relation to species composition. In surface waters, the primary groups responsible for
nitrate use were the haptophytes and chrysophytes. Prochlorophyte abundance also
showed a relationship with nitrate uptake, but it must be assumed that this group co-
varied with the others, as prochlorophytes are generally thought to rely on regenerated
forms of nitrogen (Partensky et al., 1999). The involvement of haptophytes and
chrysophytes in nitrate uptake, as opposed to diatoms, may provide some explanation
for the predominance of regenerated production even in areas where upwelling was
occurring. These relatively small phytoplankton can be effectively targeted by
microzooplankton (Strom, 2002), leading to rapid recycling of any newly-assimilated
nitrate and an active microbial web (Legendre and Rassoulzadegan, 1995). We
therefore surmise that high production rates in the Ningaloo region (Chap. 3) are
coupled to both nitrate-driven new production and significant amounts of regenerated
production.
5.5.1.2 Measurement of nitrogen uptake in oligotrophic regions
Application of the 15N uptake technique in oligotrophic waters is known to be
problematic given such inherently low nutrient levels (Harrison et al., 1996). While the
methodology to measure nanomolar nitrate and ammonium concentrations exists
(Garside, 1982; Jones, 1991), it has only recently been used in conjunction with tracer
experiments to measure uptake at ambient oligotrophic levels (Rees et al., 1999).
Ideally, 15N inoculations should result in an enrichment of 10% of ambient
concentrations, following the trace-level protocols of Dugdale and Goering (1967). In
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
151
our case, additions of 0.05 M NO3- gave enrichments of between 5 and 50% based on
the assumption that any samples below analytical detection had a concentration of
0.05 M. Results from these trace-level experiments may be more analogous to
theoretical maximum uptake rates than ambient in situ uptake, and thus we are cautious
with our interpretations.
However, in some cases nutrients were high enough that experiments could be
considered true trace-level samples ( 14% enrichment). These samples, all from the
deep chlorophyll maximum, gave an unbiased estimate of ambient NO3-, which ranged
from 1.5 – 7.1 nmol L-1 h-1. For comparison, oceanic levels of NO3- range between
0.26 – 3.73 nmol L-1 h-1 in the North Atlantic and 0.0 – 18.6 nmol L-1 h-1 offshore of the
Benguela upwelling region (Probyn, 1985). These rates contrast with the higher uptake
in the neritic regions on the North Atlantic (1.18 – 42.9 M; Harrison et al., 1996) and
the inshore/shelf waters of the Benguela system (21– 440 nmol L-1 h-1; Probyn, 1985).
Our measurements, even those at > 14% enrichment, were generally within the ranges
reported for oligotrophic and offshore regions, and therefore provide a reasonable first
estimate for the eastern Indian Ocean region.
Interpretation of the trace-level ammonium uptake experiments was additionally
complicated by the lack of ambient NH4+ measurements. It must be assumed that these
experiments, used in our estimates of the modified f-ratio, were perturbed at a level
equal to that experienced by the NO3- incubations. Ammonium generally only
accumulates in the water column when regeneration and uptake are uncoupled, such as
in the oligotrophic North Atlantic where subsurface maxima of 0.016 – 0.059 M NH4+
have been measured (Brzezinski, 1988). However, in such low nutrient waters where
regenerated production dominates (f-ratio 0.02 – 0.28), ambient NH4+ can be ~ 5 – 15
times greater than NO3- (with ranges of 0.044 – 0.081 and 0.004 – 0.017 M,
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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respectively; Rees et al., 1999). If NH4+:NO3
- ratios were similar in our study region,
then inoculations of 0.05 M may have actually had a lesser enhancement effect on
NH4+ than NO3
-.
We therefore recognize the limitations of the N-uptake data presented here.
However, even with the issues identified above, the results allow for the general
assessments that we have made regarding the prevalence of new vs. regenerated
production. While these data must be only considered as indicative and not conclusive,
they still represent a major step forward in our understanding of phytoplankton ecology
within the coastal eastern Indian Ocean.
5.5.1.3 Impact of saturating-level nutrient additions The perturbation (5.0 M N-addition) experiments essentially explored the
physiological impact of a sudden injection of nutrients on N-uptake, such as nitrate
injection via upwelling or ammonium injection via enhanced zooplankton production.
Interpretation of these results was not limited by lack of knowledge of ambient nutrient
levels, as these maximum uptake rates (which follow Michaelis-Menten kinetics) are
independent of ambient substrate concentration (Harrison et al., 1996).
The significantly higher maximum uptake rates at the surface compared to the
DCM illustrate the ability of the surface phytoplankton community to better utilize a
sudden influx of nutrients, due to higher photosynthetic rates at the surface compared to
the DCM layer (Chap. 4). Light limitation at the DCM strongly impacted ambient
photosynthetic rates, and is known to have a similar effect on NO3- and NH4
+
(Probyn et al., 1995; Varela and Harrison, 1999). The half-saturation constants for
irradiance for NO3- and NH4
+ in the field can range between ~ 1.0 % and 10 % of
surface irradiance (Io; Kudela et al., 1997, Varela and Harrison, 1999), and in our study
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
153
DCM incubations were at the lower end (1.0 % Io) of this spectrum. Nutrient
enrichment within the upper euphotic zone would therefore have the greatest impact on
production. This scenario would be most realistic for the Ningaloo Current region,
where seasonal upwelling can transport relatively high nutrient concentrations into
surface waters (Chap. 3).
5.5.2 Phytoplankton community composition
One of the most remarkable findings of this study was the consistency in phytoplankton
community structure within Leeuwin Current and offshore waters, which operated on a
very large spatial scale. The strength of chemotaxonomy is in the quantification of the
picoplanktonic component (Jeffrey et al., 1999), and was this group that formed the
principal biological division between Leeuwin Current/offshore and
shelf/countercurrent waters. These small (< 2 m) autotrophic cells (Li et al., 1983)
can be primary contributors to pelagic production in warm, low nutrient subtropical
waters. Prokayotic members of this group include the unicellular cyanobacteria
Synechococcus (Waterbury et al., 1979), and the extremely small (0.5 – 0.7 m) but
ubiquitous Prochlorococcus (Chisholm et al., 1988), a member of the cyanobacteria
whose exact phylogenetic origins are currently being debated (Partensky et al., 1999).
Prochlorococcus exhibits a high degree of photoacclimation associated with successful
coverage of the entire euphotic zone (Veldhuis and Kraay, 2004), although in WA
coastal waters this group was most common within the deep chlorophyll maximum.
This was the first application of chemotaxonomic methods and the CHEMTAX
program (Mackey et al., 1996) to the coastal eastern Indian Ocean. Without knowledge
of the natural pigment ratios of phytoplankton within this region, we found that the set
of standard ratios for ‘equatorial species’ (Mackey et al., 1996) provided a reasonable
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
154
starting point. The final ratios for the field data (after modification by the CHEMTAX
iteration procedure) were within the known ranges for each of the nine taxonomic
groups assessed, as summarized in Mackey et al. (1997b).
The microscopic data, while restricted to the > 5 m size fraction, offered
additional species-level details that the chemotaxonomic analyses could not provide.
For example, they illustrated the larger proportion of centric diatoms (common to
upwelling zones; Kudela et al., 1997; Tilstone et al., 2000) in countercurrent/shelf
surface waters compared to LC/offshore regions. There is, however, an inherent
difficulty in comparing the chemotaxonomic and microscopic data (Schluter et al.,
2000), as the former provides an estimate of biomass (as chl a) while the latter can only
estimate numerical abundance, which is generally a poor indicator of biomass especially
for small flagellates (Garibotti et al., 2003). To compensate for this, biovolumes can be
calculated for each species based on cell dimensions (Hillebrand et al., 1999) and
converted to carbon using published estimates (e.g. Strathmann, 1967; Montagnes et al.,
1994). Unfortunately, measurements of average cell dimensions for each phytoplankton
species were not undertaken in this study. Additional confounding effects in comparing
these two measures include the known change in pigment content per cell with depth
(Geider, 1987), and, as previously indicated, the different size fractions that these
methods measure (i.e. HPLC > 0.7 m, the retention size of a GF/F filter, and
microscopy > 5 m). These two methods are therefore best used in a complementary
fashion (Havskum et al., 2004) to better elucidate key features of phytoplankton
communities.
Notably, one group that was poorly estimated by HPLC (as compared to
microscopy) was the dinoflagellates, which were almost totally absent in the
CHEMTAX results but accounted for up to 8.3% of numerical cell abundance. Their
Chapter 5 – Phytoplankton community structure and nitrogen nutrition in the coastal eastern Indian Ocean
155
characteristic pigment, peridinin (Jeffrey and Vesk, 1997), was detectable in only one
sample. A few autotrophic species are known to lack peridinin (Millie et al., 1993),
which has led to some uncertainty about the use of this chemotaxonomic marker
(Garibotti et al., 2003). However, we can most likely conclude that the majority of
dinoflagellates in the study area were heterotrophic species. Approximately half of all
dinoflagellate species are obligate heterotrophs (Gaines and Elabrachter, 1987), and
such species (e.g. Gymnodinium sp., Oxytoxum sp., Protoperidinium sp., Katodinium
sp., Amphidinium sp.) were common in the cell counts, similar to the findings of
Hallegraeff and Jeffrey (1984) in northern Australian waters. The prevalence of these
heterotrophs may have been related to the overall abundance of picoautotrophs, a
known food source for dinoflagellates (Gaines and Elabrachter, 1987; Kuipers and
Witte, 2000).
5.5.3 Ecological interpretations from stable isotopes
The isotopic nitrogen signature (15N) of particulate matter is known to vary as a
function of the N substrate utilized by phytoplankton. Values corresponding to N2-
fixation are close to 0 o/oo, matching atmospheric nitrogen (Minagawa and Wada, 1986).
Nitrate and ammonium usage typically result in higher values of 2-5 o/oo and 6.5-9.0 o/oo,
respectively (summarized in Waser et al., 2000). However, in extremely N-depleted
environments the NH4+ signature can be as low as 0 o/oo, with no discrimination between
14N and 15N as the phytoplankton utilize all available nitrogen (Waser et al., 1999).
In the countercurrent/shelf regions, 15N averaged 1.99 o/oo and was significantly
higher than in Leeuwin Current/offshore waters (-0.33 o/oo), indicating that these two
regions have distinct nitrogen sources. The higher ambient nitrate concentrations in the
Ningaloo region are likely reflected in the 15N of ~ 2 o/oo, while lack of isotopic
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
156
discrimination in LC/offshore waters may describe the signature of ~ 0 o/oo. However,
this also provides qualitative evidence for the occurrence of nitrogen fixation. In the
subtropical Pacific Ocean, coccoid cyanobacteria have recently been demonstrated to
fix significant amounts of N2 (Zehr et al., 2001; Montoya et al., 2004), and these
picoplankton were the major component of the phytoplankton community at the surface
of the Leeuwin Current and offshore eastern Indian Ocean waters. If significant in this
region, N2 fixation would increase the relative proportion of new production in this
system (Dugdale and Goering, 1967), with important implications for trophic pathways
in these subtropical oceanic waters.
5.6 Concluding Remarks
In this chapter, we tested the hypothesis that regenerated production and the microbial
food web predominates in LC surface waters, while nitrate-driven new production is of
greater importance at the Leeuwin Current DCM and within the upwelling-influenced
countercurrents. We found that, within all regions of the study area, regenerated
production plays the primary role and generally accounts for > 80% of total (NO3- +
NH4+) nitrogen uptake. High productivity within the upwelling regions, while likely
stimulated by nitrate fluxes from depth, is strongly dependent on rapid recycling
processes and the smaller phytoplankton species characteristic of the microbial food
web. Distinct phytoplankton communities within the different water types were
identified through the use of chemotaxonomic methods, which proved to be an
important tool to study pelagic ecosystem structure in WA coastal waters.
CHAPTER 6
157
Seasonal production regimes off southwestern Australia: preliminary
observations on the influence of the Capes and Leeuwin Currents on
phytoplankton dynamics
6.1 Summary
This chapter complements the spatial studies of previous chapters by examining
temporal dynamics in primary production off southwestern Australia. Here, we
compare the summer upwelling regime of the Capes Current with early winter
conditions, which are characterized by strengthened nearshore Leeuwin Current (LC)
flow. Upwelling in this region sourced nitrate levels of 1 M from the nutricline at
the base of the LC’s mixed layer (similar to Ningaloo Current dynamics; Chap. 3), with
total water column production reaching a maximum of 945 mg C m-2 d-1 in the Capes
Current. Stable isotope signatures of particulate matter indicated that productivity off
southwestern Australia was heavily reliant on nitrate as a nitrogen source, with mean
15N ranging from ~ 4 – 5 o/oo under both upwelling and non-upwelling (winter)
conditions. Unexpectedly, significant nutrient enrichment within the Leeuwin Current
occurred during the winter, a result of the meandering LC flooding the inner shelf north
of the study area and entraining relatively high-nutrient shelf waters in its southwards
flow. However, winter production under these nutrient-replete conditions was still low
due to light limitation, both as a result of reduced surface irradiance characteristic of the
winter months, and also higher light attenuation within the water column as compared to
the summer months.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
158
6.2 Introduction
Coastal upwelling is a biologically important process along many coastlines, generally
resulting in the vertical transport of cool, nutrient-rich water into the euphotic zone.
Equatorward-flowing eastern boundary currents, in particular, have a large upwelling
component and are typified by high rates of primary and secondary water column
production (Wooster and Reid, 1963; Mann and Lazier, 1996). However, Australia’s
eastern boundary current, the Leeuwin Current (LC), is atypical in that it transports
tropical water poleward and is characterized by large-scale downwelling (Pearce, 1991).
This oligotrophic current dominates much of the coast of Western Australia (WA), and
is known to have strong physical controls on the lifecycles of many fish and invertebrate
species (Lenanton et al., 1991; Caputi et al., 1996). Water column production within
the LC can be quite low (< 200 mg C m-2 d-1; Chap. 3), with phytoplankton restricted to
deep chlorophyll maximum (DCM) layers near the nitracline (Chap. 4).
Inshore of the Leeuwin Current, the presence of equatorward-flowing upwelling
summer countercurrents has been well established in recent years (Gersbach et al.,
1999; Pearce and Pattiaratchi, 1999; Taylor and Pearce, 1999; Woo et al., 2004).
Implications of this seasonal upwelling for phytoplankton dynamics in WA coastal
waters are only just beginning to be investigated (Chap. 3). Nutrient levels in upwelled
water are capped by the presence of the Leeuwin Current (Gersbach et al., 1999), and in
the Ningaloo Current (NC) region off northwestern WA, reach only a maximum of 2 – 6
M NO3- within the euphotic zone (Chap. 3). Whilst low compared to other eastern
boundary regions (where NO3- can be as high as 20 – 30 M; Dickson and Wheeler,
1995; Kudela et al., 1997), this nutrient enrichment can result in primary production
rates of up to 1300 mg C m-2 d-1 in the Ningaloo Current region (Chap. 3). An
important mechanism that also contributes to production dynamics in the NC is a
Chapter 6 – Seasonal production regimes off southwestern Australia
159
shallower DCM layer, associated both with upwelling and the depth-limited shelf waters
(Chaps. 3 and 4).
Off southwestern WA, the Capes Current (CC) flows inshore of the LC during
summer months (Pearce and Pattiaratchi, 1999), and a detailed field and numerical
study showed that a minimum southerly wind speed of 7.3 m s-1 was required to
overcome the alongshore geopotential gradient and induce upwelling (Gersbach, 1999).
The shape of the continental shelf is quite distinctive in the Capes region, with an inner
shelf break at 50 m followed by an outer shelf break at 200 m, creating a terrace-like
structure (Pearce and Pattiaratchi, 1999). This bathymetry strongly influences the local
oceanography, and during the summer months the Capes Current is located on the upper
shelf and bounded offshore by the Leeuwin Current on the lower shelf, with upwelling
occurring over the inner shelf break (Gersbach et al., 1999). During the winter months,
the Leeuwin Current strengthens and in the absence of the Capes Current moves closer
inshore, flooding both upper and lower terraces (Pearce and Pattiaratchi, 1999).
The Capes Current may be an important feature for WA coastal fisheries, as the
current provides a cool-water conduit for the transport of larval and adult species of
commercial interest (Pearce and Pattiaratchi, 1999). Satellite ocean colour imagery
(SeaWiFS) also indicates this upwelling region is associated with phytoplankton
blooms, and thus the current may be important for pelagic ecology in this region both
for its advective and biological features. However, since the Capes Current is only
active during the summer months, there is also a need to understand the seasonal shift
between upwelling and non-upwelling regimes and the subsequent impact on biological
production. Within this chapter, we detail a temporal series of field studies within the
Capes region, which allowed us to assess the influence of seasonal upwelling on
primary production, and to contrast the dynamics of these summer conditions with the
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
160
winter scenario of strengthened near-shore Leeuwin Current flow. We hypothesized
that production rates would be significantly enhanced by nutrient fluxes associated with
localized summer upwelling off southwestern Australia, and would contrast strongly
with nutrient-limited winter conditions dominated by the Leeuwin Current.
6.3 Materials and Methods
Field investigations in the Capes region of Western Australia (Fig. 6.1) were undertaken
as single-day transects during December 2001, March 2002 and May 2002 at Hamelin
Bay (HB) and during November 2003 at Cape Naturaliste (CN).
6.3.1 Hamelin Bay transect
The HB study comprised three single-day field trips (11 Dec 01, 7 Mar 02 and 19 May
02), which will be referred to as HB100, HB200 and HB300, respectively. A 27.5 km
transect (from the 20 m to 140 m isobath; Fig. 6.1) was sampled using the commercial
fishing vessel Cape Leeuwin. Up to 13 CTD stations were conducted, of which
approximately half were concurrent water sampling (‘biological’) stations (Fig. 6.1b).
The CTD package consisted of an F-probe (a fine-scale CTD sampler developed at the
Centre for Water Research), Sea Tech fluorometer and Li-Cor 192-SA quantum sensor.
Maximum sampling depth for the CTD was ~ 100 m on HB100, but limited to ~ 55 m
on HB200 and HB300 due to failure of the CTD cable. Water samples were collected
in 5 L Niskin bottles, except for surface samples, which were obtained using a flow-
through pump.
For chlorophyll (chl) a and pheopigments (collected on HB200 and HB300 only),
2 to 4 L of water was filtered through Whatman GF/F filters and frozen at -20C for 2 to
Chapter 6 – Seasonal production regimes off southwestern Australia
161
Figure 6.1. a) The southwestern region of Western Australia and location of sampling
transects at Cape Naturaliste (CN) and Hamelin Bay (HB), and b) detail of CTD stations
along each transect. Biological stations are indicated by closed circles and were
sampled for chlorophyll a, POC/PN, nutrients, and primary production. Nutrients were
also sampled at all CN stations.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
162
5 days. Pigments were extracted in 90% acetone with grinding, following the
fluorometric acidification technique of Parsons et al. (1989). In situ fluorescence was
calibrated with chl a using a linear regression of pooled data for each transect. Water
samples for phytoplankton species composition (250 mL) were collected from the
surface (< 2 m) in amber glass bottles, preserved with acid Lugol’s solution (Parsons et
al., 1989) and returned to the laboratory. A 50 mL aliquot was sedimented and
enumerated using an inverted microscope (Utermohl, 1958) at 630 magnification, with
algal groups identified using Tomas (1997) as a taxonomic reference. Crossed-diameter
transects were used for counting (Sournia, 1978), with monads and flagellates 10 m
counted in a subsample of 30 field-of-view, and all other groups ( 10 m) counted in a
subsample of 200 field-of-view.
Samples for particulate organic carbon (POC) and particulate nitrogen (PN)
were collected on precombusted GF/F filters and frozen until analysis by mass
spectrophotometer (Knap et al., 1996), which gave stable isotope ratios (13C and 15N).
Filtered nutrient samples were frozen (2 to 4 weeks) until analysis for nitrate (+ nitrite),
ammonium, phosphate and silicate using an autoanalyser (Marine and Freshwater
Research Laboratory, Murdoch University).
Note that sampling during HB100 was hindered by strong winds and equipment
failure, with only 6 stations completed and measurements/analyses limited to
temperature, in situ fluorescence and nutrients.
For primary productivity (14C uptake) experiments during HB200 and HB300,
500 mL water samples from 6 stations were collected in cleaned and acid-washed
polycarbonate containers, kept dark and cool and transported back to the laboratory at
the end of the day. The samples were held overnight within approximately one degree
of in situ temperatures and on a 12:12 L:D cycle at 50 moles of photons m-2 s-1
Chapter 6 – Seasonal production regimes off southwestern Australia
163
(Thompson, 1998), and processed the following day. While not ideal, this was our only
option given the remoteness of the field site and lack of facilities aboard the chartered
vessel for the handling of unsealed radioisotope. Thompson (1998) used a similar
protocol and found no significant difference in photosynthetic parameters for samples
processed in late afternoon on the day of collection versus those held overnight. The
productivity experiments followed the small-volume, short-incubation time 14C
incorporation technique (Lewis and Smith, 1983), with modifications and equipment as
per Mackey et al. (1995, 1997a). Each water sample was inoculated with 14C to a final
concentration of 1.0 Ci per 1.0 mL seawater, and triplicate aliquots from each
sampling depth were incubated for ca. 1 to 2 hours at six main light levels (plus dark),
achieved using different combinations of neutral density and spectrally-resolving blue
filters. Photosynthetic parameters (Pm or Ps, and ) were fit using non-linear least
squares regression to the equation of Platt et al. (1980): P = Ps(1-e-I/Ps)e-I/Ps, where I =
irradiance.
Calculation of daily depth-integrated production rates (mg C m-2 d-1) followed
Walsby (1997), where daily insolation is computed based on latitude and date, and
subsurface irradiance derived using measured attenuation coefficients (Kd; although for
a limited number of stations where Kd was not available, the value for the next-nearest
station was used). Chlorophyll-normalized photosynthetic parameters (Pm* or Ps
*, *
and *) were linearly interpolated between sample depths, and calibrated fluorescence
was used to scale the parameters at 1 m depth intervals (Mackey et al., 1995).
Trapezoidal integration was then used to calculate the double integral of photosynthesis
through depth (to 0.1% light level) and time (24 h).
As sampling was undertaken with standard uncoated hydrowire and General
Oceanics Niskin bottles that had not been fitted with silicone tubing and o-rings, we
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
164
must assume that photosynthetic rates were potentially underestimated due to
contamination effects (Marra and Heinemann, 1987; Williams and Robertson, 1989).
Using similar methodologies as the present study, Mackey et al. (1995) found that Pm*
and depth-integrated productivity were underestimated by up to 50%. It is reasonable to
consider that a similar effect may have occurred with our results, although of course
while the absolute production values may have been underestimated, any spatial or
temporal differences in productivity should remain valid.
Satellite imagery of sea surface temperature (SST) was derived from the
Advanced Very High Resolution Radiometer (AVHRR) on the NOAA-16 satellite,
acquired via WASTAC (Western Australian Satellite Technology and Applications
Consortium) and processed using the McMillin and Crosby (1984) algorithm. Ocean
colour was obtained from the Sea-viewing Wide-Field-of-View (SeaWiFS) satellite via
the NASA Goddard Flight Centre public web database. Hourly wind data for Cape
Leeuwin and Cape Naturaliste were obtained from the Australian Bureau of
Meteorology.
6.3.2 Cape Naturaliste transect
The transect at Cape Naturaliste was undertaken on 3 November 2003 as part of
research cruise SS 09/2003 aboard the Australian National Facility RV Southern
Surveyor. Eight CTD stations (Stns 135 – 142; Fig. 6.1b) were sampled along 33.5 S,
between the 30 m and 200 m isobaths. Sampling was undertaken with a 24 bottle
rosette equipped with General Oceanics 10 L Niskin bottles, a Seabird SBE 911 plus
CTD, and in situ fluorometer (for uncalibrated fluorescence). Dissolved inorganic
nutrients (nitrate + nitrite, phosphate and silicate) were analyzed at all water sampling
Chapter 6 – Seasonal production regimes off southwestern Australia
165
depths using a shipboard Autoanalyzer. Detection limits were 0.01 M for nitrate +
nitrite (hereafter nitrate) and phosphate.
6.4 Results
6.4.1 Sea surface temperature (SST) and meteorological conditions
As observed in the satellite imagery (Fig. 6.2), HB100 and HB200 were typified by a
strong Capes Current signal off Hamelin Bay, with cool water present at the inshore
portion of HB100 (Fig. 6.2a), and a cold upwelling core just off-centre of transect
HB200 (Fig. 6.2b). Southerly, upwelling-favourable, winds predominated for at least
10 days prior to each of these sampling dates (Fig. 6.3a,b), with significant wave heights
from 1 – 2 m prior to HB100 and 1 – 3 m prior to HB200 (Fig. 6.4a,b). Conditions
prior to the Cape Naturaliste (CN) sampling in early November 2003 were also
dominated by southerly winds of up to 8 m s-1 (Fig. 6.5).
In contrast, winds were predominantly northerly prior to HB300 (May 02), with
a large wind event ( 20 m s-1) 8 days prior to the field trip (Figs. 6.3c). Significant
wave height reached almost 7 m after this event, and ~ 7.5 m two days prior to sampling
HB300 (Fig. 6.4c). The Leeuwin Current flowed strongly along the coast and flooded
much of the inner shelf both north of the study area and between Capes Naturaliste and
Leeuwin (Fig. 6.6), although at the Hamelin Bay transect the LC core was narrowed and
centred more offshore, with cooler water present at the coast (Fig. 6.2c).
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Figure 6.2. Sea surface temperature (SST) brightness images (cool to warm from blue
to red, black line indicates 200 m contour) from AVHRR Band 4, and digital SST
transects (open circles indicate concurrent CTD sampling stations), for a) 11 December
01 (HB100), b) 6 March 02 (one day prior to HB200 due to cloud-contamination of the
7 March 02 image) and c) 19 May 02 (HB300). Images/data provided by WASTAC.
Chapter 6 – Seasonal production regimes off southwestern Australia
167
Figure 6.3. Hourly wind vectors recorded at Cape Leeuwin for ten days prior to, and
four days after, sampling in a) Dec 01 (HB100), b) Mar 02 (HB200) and c) May 02
(HB300). Positive speeds indicate upwelling-favourable southerly winds, blowing
towards the north.
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Figure 6.4. Significant wave height recorded at Cape Naturaliste for ten days prior to,
and four days after, sampling in a) Dec 01 (HB100), b) Mar 02 (HB200) and c) May 02
(HB300).
Chapter 6 – Seasonal production regimes off southwestern Australia
169
Figure 6.5. Hourly wind vectors recorded at Cape Naturaliste prior to, and following,
sampling of the CN transect on 3 November 2003. Positive speeds indicate upwelling-
favourable southerly winds, blowing towards the north.
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Figure 6.6. Sea surface temperature image from 19 May 2002, showing the relatively
warm Leeuwin Current flooding much of the continental shelf inshore of the 200 m
shelf break. Image courtesy of the Department of Land Administration (DOLA)
Western Australia.
Chapter 6 – Seasonal production regimes off southwestern Australia
171
6.4.2 Vertical structure: temperature, salinity, nutrients and phytoplankton biomass
The limited in situ data for HB100 indicated cool (17.6-17.7 C), well-mixed water on
the inner shelf, bounded by a frontal region of increasing horizontal temperature (to a
maximum of 18.7 C) just offshore of the 50 m shelf break (Fig. 6.7a). The frontal
region showed some evidence of the downwelling influence of the Leeuwin Current,
although exact differentiation of water masses was not possible due to failure of the
salinity sensor on HB100. Fairly uniform nitrate concentrations (0.2 – 0.5 M) were
present in the upper 80 m of the water column, with a peak of 0.9 M at 100 m at the
most offshore station (113; Fig. 6.7a). A similar pattern was observed with ammonium
concentrations, silicate was generally < 2 M except at the 50 m shelf break, and
phosphate ranged between 0.13 and 0.16 M (Table 6.1). Peak fluorescence was noted
both within and offshore of the frontal region, between 40 and 100 m depth (Fig. 6.7b).
During HB200, a cold upwelling core was visible in the SST data (Fig. 6.2b),
and in situ was bounded by the 19.7C isotherms at stations 206 and 208 (Fig. 6.8b).
Clear differentiation between the Capes Current and Leeuwin Current is seen in the
temperature-salinity (TS) plot for the upper 55 m of the water column (Fig. 6.9a), with
the CC as a cooler water type that increased in salinity and temperature towards the
inner shelf. Based on the temperature and nitrate signals, the upwelling core appeared
to be sourced from at least 75 m depth on the outside of the shelf break (Fig. 6.8b).
The relatively high nitrate (0.7 – 0.9 M) subsurface upwelling region was
bounded to the east by vertically well-mixed shelf waters containing 0.4 – 0.6 M
nitrate, and to the west by the nitrate-depleted upper layer of the Leeuwin Current (Fig.
6.8b). Ammonium was generally low ( 0.4 M) across the transect, with the exception
of surface waters at the innermost station (0.9 M) and just offshore of the upwelling
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Figure 6.7. HB100 – 11 Dec 01: a) Temperature contours overlaid with discrete nitrate
concentrations from Niskin sampling depths, and b) uncalibrated in situ fluorescence
(extracted chl a data not available).
173
Table 6.1. Concentration (M) of ammonium (NH4+), phosphate (PO4
3-) and silicate (SiO3-) in water samples from the three
sampling trips (left to right: HB100, HB200 and HB300). Values of < 0.2 M are below instrumental detection limits, and
‘-’ indicates no data available.
Stn
Depth (m)
NH4+
(M) PO4
3- (M)
SiO3-
(M)
Stn Depth (m)
NH4+
(M)PO4
3- (M)
SiO3-
(M)
Stn Depth (m)
NH4+
(M)PO4
3- (M)
SiO3-
(M) 102 0 0.5 0.13 1.0 202 0 0.9 0.23 1.7 302 0 0.5 0.23 2.6
- - - - - - - - 25 0.6 0.26 2.5 40 0.4 0.13 1.1 40 0.4 0.19 2.1 40 0.4 0.23 2.8
104 - - - - 204 0 0.3 0.16 2.5 304 0 0.2 0.19 2.8 - - - - 20 0.3 0.23 2.0 30 0.4 0.23 2.7 - - - - 40 0.2 0.23 1.9 - - - -
106 0 0.6 0.16 3.5 206 0 0.2 0.19 2.2 306 0 0.4 0.19 2.5 - - - - 20 0.4 0.19 1.2 25 0.3 0.19 2.3 45 0.6 0.16 3.6 40 0.3 0.19 2.2 45 0.3 0.23 2.7
108 - - - - 208 0 < 0.2 0.19 2.2 308 0 0.3 0.19 2.6 - - - - 25 0.2 0.16 3.4 25 0.4 0.23 2.6 - - - - 50 0.3 0.19 2.0 55 0.4 0.26 2.8
110 0 0.5 0.13 1.4 210 0 0.6 0.16 1.7 310 0 0.4 0.19 3.3 - - - - 25 < 0.2 0.19 2.3 30 < 0.2 0.26 2.7 80 0.8 0.16 1.4 75 0.3 0.19 2.5 50 0.3 0.23 2.9
113 0 0.8 0.16 1.9 212 0 0.3 0.16 1.5 313 0 0.4 0.26 2.7 20 0.4 0.16 1.5 25 0.2 0.13 1.7 30 0.6 0.26 2.7 60 0.4 0.16 1.9 50 0.4 0.16 2.1 50 0.2 0.19 3.6 100 1.6 0.16 2.2 - - - - - - - -
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Figure 6.8. HB200 – 7 Mar 02: a) Depth-integrated primary production
(mg C m-2 d-1); b) temperature contours overlaid with discrete nitrate concentrations
from Niskin sampling depths (values of < 0.1 M were below instrumental detection
limits); and c) chl a derived from calibrated in situ fluorescence. Station locations (Stns
201 – 212) are indicated with inverted triangles.
Chapter 6 – Seasonal production regimes off southwestern Australia
175
zone (0.6 M; Table 6.1). Phosphate ranged between 0.13 and 0.23 M, while silicate
was generally > 2 M (although there were a few patches ranging from 0.12 to
0.19 M; Table 6.1). Maximum chl a ( 0.60 mg m-3) was found in a broad band that
shoaled from approximately 50 m at station 213 to the surface at station 202, with a
peak of 0.65 mg m-3 just inshore of the upwelling zone between 20 and 40 m depth (Fig.
6.8c).
Conditions at Cape Naturaliste in summer 2003 were very similar to those found
off Hamelin Bay during summer 2002 (HB200), with a cold upwelling core found at the
50 m shelf break along the CN transect (Fig. 6.10a). The surface expression of the
upwelling was located near Stn 138, which was bounded by the 17.2C isotherms, with
warmer water both inshore (17.4C) and offshore (17.4 – 17.8C). This shelf break
water was sourced from the base of the Leeuwin Current, which was located at the most
offshore station (Fig. 6.10a).
Concurrent with the temperature pattern, an elevated nitrate signal was also
noted in surface (< 2 m) waters, with 0.08 M at the upwelling core, compared to 0.03
and 0.05 M inshore and offshore, respectively (Fig. 6.10a). The magnitude of nutrient
enrichment was most evident in the subsurface, where upwelled waters along the slope
between the 200 m and 50 m isobaths were typified by nitrate concentrations between
~ 1.0 and 1.6 M. A region of maximum in situ fluorescence was also located at the 50
m shelf break (Fig. 6.10b).
Physical water column structure during the winter conditions of HB300 (May
2002) was markedly different than that observed during the summer upwelling months.
An offshore to onshore gradient of decreasing temperature and increasing salinity is
evident in the HB300 TS diagram (Fig. 6.9b), with inner shelf waters forming a mixed
TS signature. The frontal region between LC and inshore waters was centred on the
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Figure 6.9. Temperature-salinity (TS) plots for the upper 55 m of the water column, for
a) HB200 and b) HB300 sampling dates (salinity data not available for HB100).
Chapter 6 – Seasonal production regimes off southwestern Australia
177
50 m shelf break, and was the area of lowest surface nitrate concentrations (0.7 – 0.9
M; Fig. 6.11b). Both inshore and offshore surface waters had relatively elevated
nitrate levels (1.3 and 2.1 M, respectively), in addition to high concentrations (up to
3.1 M) throughout much of the mid-water column (20 – 40 m; Fig. 6.11b).
Ammonium was generally 0.4 M, phosphate ranged between 0.19 and 0.26 M, and
silicate concentrations were 2.3 M (Table 6.1).
Minimum chl a concentrations were generally found on the inner shelf ( 50 m
isobath) and in surface waters across the transect (Fig. 6.11c). A subsurface chl a
maximum, between ~ 15 and 50 m depth, was located from the shelf break to the most
offshore station, with peak concentrations (0.7 mg m-3) in the frontal region between
stations 308 and 310 (Fig. 6.11c). The pheopigment:chl a ratio was significantly higher
during HB300 than HB200 (Mann-Whitney U test, p < 0.001; Table 6.2).
6.4.3 Photosynthetic parameters and depth-integrated primary production
During HB200, depth-integrated primary production was highest in the upwelling zone
(945 mg C m-2 d-1), decreasing to approximately 600 mg C m-2 d-1 at the inshore and
offshore edges of the transect (Fig. 6.8a). Photosynthetic parameters (Pm, ) followed a
similar spatial trend in surface waters, and showed a notable decrease with increasing
depth in the water column (Fig. 6.12a-c). Photoinhibition was only measurable on one
water sample (stn 206 at 40 m, = 0.0009). Light attenuation was found to increase
from inshore to offshore, with a mean value of 0.070 m-1 (Table 6.3). The maximum
surface irradiance based on latitude and date was ~ 1800 E m-2 s-1, with a total of
12.75 h of daylight (05:45 – 18:30 h).
During HB300, depth-integrated primary production was at a minimum on the
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Figure 6.10. CN – 3 Nov 03: a) temperature contours overlaid with discrete nitrate
concentrations from Niskin sampling depths, and b) uncalibrated in situ fluorescence.
Station locations (135 – 142) are indicated with inverted triangles.
Chapter 6 – Seasonal production regimes off southwestern Australia
179
Figure 6.11. HB300 – 19 May 02: a) Depth-integrated primary production
(mg C m-2 d-1); b) temperature contours overlaid with discrete nitrate concentrations
from Niskin sampling depths; and c) chl a derived from calibrated in situ fluorescence.
Station locations (Stns 301 – 313) are indicated with inverted triangles.
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Table 6.2. Comparison of light attenuation (Kd; m
-1), pheopigment:chl a ratio (pheo:chl
a), depth-integrated primary production (PP; mg C m-2 d-1), maximum photosynthetic
rate (Pm; mg C m-3 h-1), light absorption coefficient (; mg C m-3 h-1(E m-2 s-1)-1) and
photoinhibition coefficient (; mg C m-3 h-1(E m-2 s-1)-1) between HB200 and HB300.
Values are mean s.d., with statistical significance (p-value) assessed using the Mann-
Whitney U test (‘n.s.’ = not significant).
Parameter HB200 HB300 df p Kd 0.070 0.017 0.120 0.040 14 < 0.05
Pheo:chl a 0.56 0.14 0.80 0.16 32 < 0.001 PP 695 140 310 105 10 < 0.01 Pm 1.32 0.94 1.18 0.76 29 n.s. 0.021 0.012 0.017 0.011 29 n.s. 0.0001 0.0002 0.0020 0.0015 29 < 0.001
Table 6.3. Light attenuation (Kd) and euphotic zone depth (Zeu) for HB200 and HB300;
bold values are mean s.d.
Stn Max depth (m) Kd (m-1) Zeu (1.0 %) Zeu (0.1%)
204 45 0.053 column column 206 50 0.044 column column 207 55 0.083 column column 208 65 0.082 56 column 209 70 0.080 58 column 210 100 0.080 58 86
0.070 0.017 301 20 0.187 column column 302 45 0.174 26 40 303 45 0.134 34 column 304 45 0.127 36 column 305 50 0.075 column column 306 50 0.057 column column 310 100 0.118 39 58 311 130 0.091 51 76 312 140 0.114 40 61 313 140 0.122 38 57
0.120 0.040
Chapter 6 – Seasonal production regimes off southwestern Australia
181
Figure 6.12. Photosynthetic characteristics (Pm, shaded bars; , black dots) for water
samples from HB200 (left panels; a-c) and HB300 (right panels; d-f), as a function of
distance from shore and depth in the water column. Pm = maximum photosynthetic rate,
(mg C m-3 h-1), and = initial slope (mg C m-3 h-1)/(E m-2 s-1).
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inner shelf (150 mg C m-2 d-1), increased up to 450 mg C m-2 d-1 in the frontal region
and dropped to 310 – 350 mg C m-2 d-1 in offshore waters (Fig. 6.11a). Mean
production during HB300 was significantly lower than during HB200 (Mann-Whitney
U test, p < 0.01; Table 6.2). Photosynthetic parameters (Pm, ) in surface waters
followed a similar spatial pattern as the depth-integrated values, and similar to HB200
decreased notably with depth (Fig. 6.12d-f). Photoinhibition was present in all HB300
samples, a significant difference (p < 0.001, Table 6.2) compared to HB200. However,
note that there was no significant difference in values of Pm and between HB200 and
HB300 (p >> 0.05; Table 6.2). The mean light attenuation across the transect was 0.120
m-1 (Table 6.3), significantly higher than in HB200 (Table 6.2). The maximum surface
irradiance based on latitude and date was ~ 1200 E m-2 s-1, with a total of 10.00 h of
daylight (07:00 – 17:00 h).
6.4.4 Phytoplankton species composition
Small monads and flagellates dominated the phytoplankton cell counts in both
upwelling (HB200; Fig. 6.13a) and non-upwelling (HB300; Fig. 6.14a) conditions, with
a distinct peak in cell numbers at the 50 m shelf break during winter (Fig. 6.14a).
During HB200, diatoms (mainly small pennates, e.g. Pseudonitzschia spp.) and
dinoflagellates peaked in abundance near the upwelling core (at Stn 206; Fig. 6.13b).
In contrast, during the winter conditions of HB300 diatoms were distributed fairly
evenly across the transect, while dinoflagellate numbers peaked both at the shelf break
and at the offshore station (Fig. 6.14b).
Chapter 6 – Seasonal production regimes off southwestern Australia
183
Figure 6.13. Abundance (cells L-1) of major phytoplankton taxonomic groups in
surface (< 2 m) waters during Mar 02 (HB200), as a function of distance from shore.
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184
Figure 6.14. Abundance (cells L-1) of major phytoplankton taxonomic groups in
surface (< 2 m) waters during May 02 (HB300), as a function of distance from shore.
Chapter 6 – Seasonal production regimes off southwestern Australia
185
6.4.5 Stable isotopic ratios of particulate matter
The mean ( SE) isotopic ratios for particulate matter collected during HB200 were
-24.87 ( 0.06) o/oo 13C and 4.06 ( 0.27) o/oo
15N (Fig. 6.15). These were significantly
lower than the values of 13C (-24.53 0.12) and 15N (5.01 0.23; mean SE)
obtained during HB300 (MANOVA, F(2,18) = 4.93, p = 0.02; Fig. 6.15).
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
186
Figure 6.15. Mean ( SE) stable isotopic ratios (o/oo) for samples from upwelling
(HB200, Mar 02; filled symbol, n = 10) and non-upwelling (HB300, May 02; open
symbol, n = 11) conditions off Hamelin Bay, Western Australia.
Chapter 6 – Seasonal production regimes off southwestern Australia
187
6.5 Discussion
Two distinct seasonal scenarios characterize oceanographic conditions in the coastal
waters of southwestern Australia. During the fall and winter months, when equatorward
wind stress is weakest (Godfrey and Ridgway, 1985), the Leeuwin Current (LC) flows
strongly southwards and can flood much of the continental shelf (Pearce and Griffiths,
1991; Pattiaratchi et al., in press). During summer months, southerly winds weaken the
LC’s flow and generate localized upwelling along the inner continental shelf, forming
the source water of the Capes Current (Gersbach et al., 1999). In a series of field
experiments, we examined the hypothesis that production rates would be significantly
enhanced by nutrient fluxes associated with this localized summer upwelling, and
contrast strongly with nutrient- and production-limited winter conditions dominated by
the Leeuwin Current. We found that seasonal upwelling can indeed source significant
amounts of nutrients from the base of the Leeuwin Current, leading to maximum
production rates of 945 mg C m-2 d-1. Interestingly, however, we established that winter
conditions of strengthened Leeuwin Current flow can also lead to high nutrient levels
within the Capes region, which we argue were associated with entrainment of
seasonally nutrient-enriched shelf water north of the study area. However, reduced light
attenuation and lowered surface irradiance in the winter months limits primary
production under these nutrient-replete conditions. These preliminary observations of
the seasonal phytoplankton dynamics associated with the Capes and Leeuwin Currents
off southwestern Australia provides a basis to further hypotheses about pelagic ecology
within the region.
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6.5.1 Summer upwelling and shelf break dynamics: biological significance
Coastal upwelling regimes are important mechanisms for enhancing phytoplankton
productivity, as they transport ‘new’ nutrients from deeper waters into the euphotic zone
(Mann and Lazier, 1996). Upwelling can also impact on the light climate experienced
by phytoplankton, by advecting cells to shallower water and therefore higher light levels
(Brown and Field, 1986), and by the retention of those cells in the surface layer during
the stratification (relaxation) period which typically follows an upwelling event
(Cushing, 1989; Mann and Lazier, 1996). During upwelling conditions off Hamelin
Bay, the offshore deep chlorophyll maximum (DCM) shoaled towards the upwelling
zone (Fig. 6.8), a feature also seen with Ningaloo Current upwelling (Chaps. 3 and 4).
When coupled with nutrient inputs form upwelling, this physical shift in DCM depth
has an important impact on production rates in this region (Chap. 4). Maximum
production within the Capes Current (945 mg C m-2 d-1) was of a similar magnitude to
that measured in the Ningaloo Current (800 – 1300 mg C m-2 d-1; Chap. 3), providing
further evidence that these coastal countercurrents are important seasonal contributors to
production along the coast of Western Australia.
In a previous study of seasonal upwelling associated with the Capes Current,
Gersbach et al. (1999) found that upwelled water contained only slightly elevated
nutrients (0.4 M NO3-) as compared to the bulk of the Leeuwin Current (0.2 M NO3
-).
In contrast, we have found that it is possible for CC upwelling to transport relatively
high nitrate concentrations ( 1.0 M) into the upper euphotic zone ( 50 m). These
levels were notably greater than those at the equivalent depth within the Leeuwin
Current (< 0.1 M). Comparable to mechanisms associated with Ningaloo Current
upwelling (Chap. 3), this high nutrient water was sourced from the nutricline at the base
of the LC’s mixed layer. The amount of nutrient enrichment associated with the Capes
Chapter 6 – Seasonal production regimes off southwestern Australia
189
Current is likely a function of both the depth of the LC’s thermocline/nutricline, and the
strength of the wind-driven upwelling, both of which may vary during the course of the
summer season (Gersbach, 1999; Gersbach et al., 1999) and from year to year
(Cresswell, 1991).
The Capes Current (CC) is generally restricted to the inner shelf ( 50 m
isobath), with a width of approximately 20 km (Gersbach et al., 1999; Pearce and
Pattiaratchi, 1999; this study). The inner (50 m) shelf break is therefore a significant
area from a physical standpoint, being the location of the upwelling core and/or
temperature front between LC and inshore waters. Off Western Australia, the shelf
break typically forms a shear-influenced boundary between different water masses
(Peace and Griffiths, 1991; Pattiaratchi et al., 2004) and is associated with elevated
nutrient, chl a and plankton concentrations (Phillips and Pearce, 1997; Chap. 3). These
enhanced food resources have been suggested to influence the timing and success of
rock lobster (Panulirus cygnus) metamorphic moults and final recruitment to the adult
population (McWilliam and Phillips, 1997).
Similarly, we found that the inner shelf break was an important region for
phytoplankton dynamics, with peak chl a concentrations, highest numbers of large-size
(> 10 m) phytoplankton, and maximum production rates located at or near the shelf
break. As discussed in Lu et al. (2003), adult euphausiid populations also form
aggregations at shelf-break upwelling centres to take advantage of higher food resources
(a function of phytoplankton productivity and biomass accumulation). Cross-shore
separation of juvenile and adult euphausiid populations, where the former are retained
within offshore-flowing surface waters while the latter position themselves deeper in the
water column and stay within the main upwelling zone, is also a common physical
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
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dynamic associated with shelf break upwelling regions (Lu et al., 2003) and may reduce
the incidence of cannibalism by adults on larval euphausiids (Brinton, 1976).
An important contrast between the two seasonal upwelling regimes off WA (the
Ningaloo and Capes Current systems) was seen in the stable isotope ratios of particulate
matter. This was most notable with the 15N signature, which is known to vary
according to the nitrogen substrate utilized by phytoplankton (Wada, 1980; Altabet and
McCarthy, 1985). Isotopic fractionation (preferential uptake of 14N relative to 15N)
results in 15N-depleted particulate nitrogen, and recent estimates indicate that the
signature of nitrate uptake in the ocean ranges between 2 – 5 o/oo (Waser et al., 2000).
In Ningaloo Current and shelf waters off northwestern WA, 15N averaged ~ 2 o/oo and
was significantly higher than the 15N signature of Leeuwin Current/offshore waters
(~ 0 o/oo; Chap. 5), providing evidence for a more nitrate-driven system in Ningaloo
waters compared to the LC. The even higher (~ 4 – 5 o/oo) 15N signature seen in the
present study off southwestern Australia indicates a very strong reliance on nitrate-
driven production, interestingly during both upwelling and non-upwelling conditions.
In fact, the winter scenario with strengthened inshore Leeuwin Current flow was
characterized by higher nitrate concentrations (~ 2 – 3 M) and significantly higher
15N than the upwelling-driven Capes Current regime. Food web structure is closely
linked to nutrient inputs: ammonium-driven systems are generally associated with
picoplankton and the microbial food web, while high nitrate contributions lead to the
multivorous and herbivorous food webs typical of upwelling zones (Legendre and
Rassoulzadegan, 1995). While we theorize, based on the available data, that the
multivorous or herbivorous pathways may be dominant in this region, further seasonal
studies which specifically examine size-fractionated primary production will assist in
answering this question.
Chapter 6 – Seasonal production regimes off southwestern Australia
191
6.5.2 Winter nutrient and productivity dynamics
While the Leeuwin Current generally follows the 200 m shelf break, it is also a
frequently meandering flow (Pearce and Griffiths, 1991) that can impinge on, or
completely flood, the continental shelf and thereby entrain inshore waters (Pattiaratchi
et al., in press). These shelf waters often contain relatively high phytoplankton biomass
compared to surface waters of the Leeuwin Current (Pattiaratchi et al., in press; Chap.
3), and can also be enriched in dissolved nutrients. Annual winter nitrate maxima on
the continental shelf have been documented off Perth (Pearce et al., 1985; Johannes et
al., 1994) and in the Capes region (Pearce and Pattiaratchi, 1999), with maximum
concentrations reaching approximately 2.0 to 3.0 M NO3-. The source of this winter
nutrient peak has yet to be conclusively identified, but is likely a function of increased
surface runoff during May to September (when the southwestern region of Australia
receives 80 % of its annual rainfall; Bureau of Meteorology, 1966) and frequent winter
storms. This storm activity generates significant wind and wave mixing, which in the
shallow coastal zone can suspend nutrient-rich sediments and may contribute to
remineralization of beach wrack (benthic algae and seagrass; Hansen, 1984).
We therefore postulate that the high nitrate concentrations measured off Hamelin
Bay during the winter (May) of 2002 were advected into the region by the Leeuwin
Current. This generally nutrient-poor current was seen to flood the continental shelf
north of the study area, mixing with shelf waters that were likely nutrient-enriched
compared to the Leeuwin Current. Additionally, storm activity (indicated by wind
speeds 20 m s-1 and significant wave height 7 m) in the period just prior to sampling
may have contributed to the high nutrient signature, as discussed above.
However, despite these nutrient-replete conditions, total water column
production in winter (May) was significantly lower than during summer upwelling
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conditions (March). Nutrients are, of course, only one factor that determines the
amount of production within the water column (Mann and Lazier, 1996; Tilstone et al.,
2000). Light plays a key role in these dynamics, both in terms of the absolute amount
of irradiance received at the water’s surface and in the attenuation of light with depth
(Kirk, 1994; Cloern, 1999). Winter measurements of increased nutrients were also
associated with significantly higher light attenuation and high amounts of
pheopigments, which are chlorophyll degradation products resulting from cell
senescence and death (Jeffrey, 1997; Lourda et al., 2002). These conditions, indicating
high amounts of detritus and associated turbidity within the water column, were coupled
with a shorter day length and the reduced maximum surface irradiance characteristic of
the winter season. Significantly higher photoinhibition (), as measured by a reduction
of photosynthetic rates at high irradiance (Platt et al., 1980), also indicated cells were
photoadapted to lower light conditions (as reviewed in Han et al., 2000). Thus, water
column production off southwestern WA can be under strong light limitation during
winter, serving to further highlight the importance of seasonal upwelling events for
productivity in this region. Upwelling occurs during summer months characterized by
maximum incident irradiance and low light attenuation, when nutrient fluxes can have
the greatest impact on primary production.
6.6 Concluding Remarks
In a temporal series of field investigations off southwestern Australia, we found that
seasonal upwelling associated with the Capes Current can source significant amounts of
nutrients from the base of the Leeuwin Current. Phytoplankton production within this
summer upwelling current can reach 945 mg C m-2 d-1, and is of similar magnitude to
that measured in the Ningaloo Current upwelling regime off northwestern Australia
Chapter 6 – Seasonal production regimes off southwestern Australia
193
(Chap. 3). Interestingly, winter conditions of strengthened Leeuwin Current flow can
also be responsible for high nutrient levels within the Capes region. However, reduced
light attenuation and lowered surface irradiance in winter can limit levels of production
under these nutrient-replete conditions. While this work provides only single snap-shots
of a very dynamic system, by illuminating key mechanisms through which the Capes
and Leeuwin Currents impact primary production it represents an important first step in
elucidating physical-biological coupling within this region.
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
194
CHAPTER 7
195
General discussion, conclusions and future work
7.1 Discussion and Conclusions
This thesis has comprised a holistic study of the physical, chemical and biological
oceanographic linkages within a broad region of the coastal eastern Indian Ocean. For
the first time, we have measured rates of primary production and nitrogen uptake,
phytoplankton community structure via chemotaxonomy, and the large-scale subsurface
distribution of phytoplankton biomass in continental shelf and Leeuwin Current (LC)
waters off Western Australia (WA). The many facets of this study were united by
examining the general hypothesis that the Leeuwin Current inhibits phytoplankton
productivity in WA coastal waters by a) providing a nutrient-poor (oligotrophic)
environment, and b) suppressing upwelling-driven production.
The original view of phytoplankton within the LC, primarily obtained via ocean
colour satellite imagery (Pattiaratchi et al., in press), was one of extremely low biomass
( 0.1 mg chl a m-3). From our in situ measurements, we have found that significant
vertical nutrient and biomass gradients exist within the current, with phytoplankton
forming a deep chlorophyll maximum (DCM) associated with the nitracline at the base
of the LC’s mixed layer (Chaps. 3 and 4). These DCMs can have concentrations of up
to 0.9 mg chl a m-3, and are ‘true’ maxima of phytoplankton carbon biomass (Chap. 4).
While total water column productivity is indeed fairly low within Leeuwin Current and
offshore waters (generally 200 mg C m-2 d-1; Chap. 3), an important proportion of this
production (up to 40%) was associated with the DCM (Chap. 4). One of the major
implications of this ubiquitous DCM is that it is generally found well beyond the range
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
196
of ocean colour satellites, which have a maximum optical depth of 40 – 60 m in
Leeuwin Current waters (P. Fearns, pers. comm.). Satellite data will therefore have to
be carefully combined with in situ measurements of vertical structure to develop
functional biomass and primary production algorithms for this region (Sathyendranath
and Platt, 1993).
It is interesting to speculate on the potential importance of these phytoplankton
layers for general pelagic ecology within the Leeuwin Current, as we know that the
larval forms of many fish and invertebrate species are entrained within the LC’s
southward flow (Pearce et al., 1992; Gaughan and Fletcher, 1997), and may therefore
target these layers as a food source. Mid- to late-stage rock lobster (Panulirus cygnus)
phyllosoma larvae, returning to the coast of WA after spending their first year in
offshore waters, are generally found between 50 and 120 m depth within the Leeuwin
Current (Rimmer and Phillips, 1979; Griffin et al., 2001). It is at this depth, which also
corresponds to the general location of the DCM, that they are transported towards the
coast via the onshore geostrophic flow (Phillips, 1981). Variation in the amount of
productivity within the DCM, which we have shown is strongly correlated with ambient
light levels (i.e. depth; Chap. 4), may impact on the survival rates of these, and other,
larval forms.
As identified in Chapter 5, regenerated production and the microbial food web
dominate within the Leeuwin Current’s DCM. The microbial web has traditionally
been considered a ‘sink’ for biogenic carbon, where most of the autotrophic production
generated by pico- and nanoplankton is oxidized within the microbial loop, and
therefore not available for export to higher trophic levels or as sinking particulate matter
to the deep ocean (Ducklow et al., 1986; Smith et al., 1986; Michaels and Silver, 1988).
However, other authors have argued that microbial food webs are in fact a ‘link’ to
Chapter 7 – General discussion, conclusions and future work
197
mesozooplankton communities through protozoan and microzooplankton grazing
(Vezina and Platt, 1988; Fortier et al., 1994). This provides for an interesting and
testable hypothesis on the extent of coupling between picoplanktonic production and
higher trophic levels within LC waters.
While the Leeuwin Current is present along the coast of Western Australia
throughout the year, coastal dynamics in the summer months are influenced by wind-
driven countercurrents (the Ningaloo and Capes Currents) that flow northwards along
the continental shelf, pushing the Leeuwin Current more offshore (Pearce and
Pattiaratchi, 1999; Taylor and Pearce, 1999). We have found that these countercurrents,
associated with seasonal upwelling (Gersbach et al., 1999; Woo et al., 2004; Chap. 6),
can be five times more productive than LC/offshore waters, with total water column
production between approximately 700 and 1300 mg C m-2 d-1 (Chaps. 3 and 6). The
Leeuwin Current therefore does not fully suppress upwelling-driven production in this
region, but it can place a limit on nutrient levels that are transported into the euphotic
zone. Maximum nitrate concentrations were ~ 2 – 6 M in the Ningaloo Current (NC)
upwelling off northwestern Australia (Chap. 3), and ~ 1 – 1.5 M in the Capes Current
(CC) upwelling off southwestern Australia (Chap. 6). These nutrients, sourced from the
nutricline at the base of the LC’s mixed layer, are notably lower than in upwelling
regions associated with equatorward eastern boundary currents (e.g. up to 20 – 30 M
NO3- in the eastern Pacific; Dickson and Wheeler, 1995; Kudela et al., 1997).
However, they still result in production rates that are significantly higher than expected
for this otherwise oligotrophic coast, and undoubtedly play an important role in food
web dynamics off Western Australia. For example, it is not likely a coincidence that the
highly productive Ningaloo Current is located next to a major coral reef system
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
198
(Ningaloo Reef) that is also known for substantial zooplankton biomass (Wilson et al.,
2002b, 2003).
As we hypothesized in Chapter 3, the biological impact of any upwelling in this
region is expected to be a function of: (a) conditions within the Leeuwin Current, (b) the
strength and duration of upwelling-favourable winds (i.e. the intensity of upwelling),
and (c) geographical location, primarily with respect to the width of the continental
shelf and resultant proximity of upwelling flows to deep nutrient pools. The strength
and position of the Leeuwin Current, and the depth of its mixed layer, varies both
spatially (Smith et al., 1991) and temporally (Godfrey and Ridgway, 1985; Pearce and
Phillips, 1988) along the west coast of WA. Interannually, flow is weakened during
ENSO (El Niño/Southern Oscillation) years, when the north-south geopotential anomaly
(the driving force for the Leeuwin Current) is reduced (Pearce and Phillips, 1988;
Pattiaratchi and Buchan, 1991; Feng et al., 2003). We theorize that conditions of
weakened flow may result in shoaling of the LC’s nutricline, allowing wind induced
upwelling to access higher nutrient concentrations, and also lessen the force opposing
the northward flowing countercurrents.
Intensity of coastal upwelling is closely linked to the ambient wind field (Barber
and Smith, 1981), which means that both upwelling and any associated nutrient fluxes
are episodic in nature (Nelson and Hutchings, 1983; Carr, 1998). This variability, in
addition to the strong seasonality of the wind-driven countercurrents, has likely resulted
in a number of adaptations of both pelagic and benthic organisms to this physical
forcing. Taylor and Pearce (1999) have suggested that coral spawning within the
Ningaloo region is timed to coincide with the presence of the Ningaloo Current, thus
minimizing dispersal of larvae from the reef zone by the southward-flowing Leeuwin
Current. The large phytoplankton biomass and high productivity we measured off
Chapter 7 – General discussion, conclusions and future work
199
Ningaloo may provide a seasonally predictable input of food resources to the micro- and
mesozooplankton populations (Wilson et al., 2002b, 2003) within the region, which in
turn are regularly exploited by the large filter feeders (e.g. manta rays and whale sharks)
that are seasonal visitors to this region (Taylor, 1994). The extent of such bottom-up
control of trophic structure (Hunter and Price, 1992) provides an additional testable
hypothesis related to the ecology of the area.
Intriguingly, we found that regenerated, ammonium-driven production played a
primary role throughout the region, accounting for over 80% of total nitrogen uptake
even in the upwelling-influenced Ningaloo Current (Chap. 5). Nitrogen recycling via
the microbial food web can complement the short nitrate-based herbivorous food chain
within upwelling zones (Codispoti, 1983; Probyn et al., 1990; Bode et al., 2004), and in
the NC region plays a large part in sustaining productivity levels that may have initially
been generated by advective nitrate fluxes (Chaps. 3 and 5). Phytoplankton species
composition in Ningaloo Current and continental shelf waters, while featuring a higher
diatom fraction than in Leeuwin Current/offshore regions, was dominated by pico- and
nano-planktonic groups including chrysophytes and haptophytes (Chap. 5). These
relatively small phytoplankton can be effectively targeted by microzooplankton (Strom,
2002), leading to efficient remineralization of newly incorporated nitrate (Bode et al.,
2004). The predominance of regenerated production indicates that measurement of
ammonium should become a priority for oceanographic research in this region. These
results will hopefully help provide the impetus for the Australian Marine National
Facility to incorporate such measurements into their shipboard hydrochemical protocols.
Phytoplankton community composition within the LC/offshore region showed
only 40 – 55 % similarity to Ningaloo Current and shelf waters, displaying high
proportions of picoplankton such as cyanobacteria in surface waters and
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
200
prochlorophytes at the DCM (Chap. 5). These groups were only identified through the
use of chemotaxonomic methods (based on HPLC analysis of pigments; Mackey et al.,
1996; Jeffrey, 1997), which proved to be an important tool for assessing pelagic
ecosystem structure in this region of the coastal eastern Indian Ocean.
Through analysis of 15N signatures, the LC/offshore region was also found to
have a distinct nitrogen source compared to NC/shelf waters (Chap. 5). Particulate
matter in the more nitrate-influenced countercurrent and shelf waters was characterized
by a mean 15N of ~ 2 o/oo, while the 15N of the LC/offshore region averaged ~ 0 o/oo
and was indicative of either lack of isotopic discrimination due to extremely nutrient-
depleted waters (Waser et al., 1999) or nitrogen fixation by the large proportion of
coccoid cyanobacteria (Zehr et al., 2001; Montoya et al., 2004). These 15N signatures
contrast even more strongly with the southwestern region of WA, where 15N associated
with Capes Current upwelling was ~ 4 o/oo (Chap. 6), potentially indicating a higher
reliance on nitrate-driven production (Waser et al., 2000) within this region.
Our limited seasonal investigations off the Capes region of southwestern
Australia showed that the winter production scenario can be very different than summer
conditions, with strong Leeuwin Current flow that meanders onto the continental shelf
(Pattiaratchi et al., in press) and entrains nutrient-enriched waters (Chap. 6). In this
case, the Leeuwin Current was nutrient-replete, but total water column production was
under strong light limitation, a result of both high subsurface light attenuation and
reduced surface irradiance characteristic of the winter months (Chap. 6).
7.2 Recommendations for Future Work
The results of this thesis have highlighted a number of avenues that future research
directions could explore. One of the most important would be to undertake temporal
Chapter 7 – General discussion, conclusions and future work
201
investigations into the variability of primary production associated both with the
countercurrents and the Leeuwin Current. We know that there is significant variation in
these oceanographic features, both between seasons and inter-annually (Pearce and
Phillips, 1988; Pearce and Griffiths, 1991; Pearce and Pattiaratchi, 1999), and
understanding how this impacts on rates of primary production will be critical for the
effective management of higher trophic levels (Griffin et al., 2001). Given the
dominance of picoplankton within much of the study region, the determination of
C:chl a ratios for separate phytoplankton community types (potentially combining size
fractionation, flow cytometry, DNA analysis and HPLC pigment techniques following
Veldhuis and Kraay, 2004) will also be important in defining food web types and
trophic pathways (sensu Legendre and Rassoulzadegan, 1995).
While we have examined dynamics related to two of the most important
dissolved nitrogen species for phytoplankton nutrition (nitrate and ammonium), both
urea and di-nitrogen gas (N2) can make significant contributions to regenerated and new
production, respectively (Dugdale and Goering, 1967; Varela and Harrison, 1999).
Certainly, the large amounts of picoplanktonic cyanobacteria, both within Leeuwin
Current and countercurrent waters, may use N2 as a nitrogen source (Zehr et al., 2001;
Montoya et al., 2004) especially under conditions of nitrogen limitation. Also,
exclusion of urea uptake from calculation of the f-ratio can result in an overestimation
of new production by up to 50 % (Metzler et al., 1997; Varela and Harrison, 1999). We
would therefore recommend a more complete investigation of nitrogen nutrition in both
continental shelf and Leeuwin Current waters.
This thesis has also alluded to potentially important linkages between primary
and secondary production, both at the microscale (i.e. nitrate remineralization by
microzooplankton; Chap. 5) and the macroscale (i.e. high rates of primary production
CE Hanson (2004) Oceanographic forcing of phytoplankton dynamics in the coastal eastern Indian Ocean
202
associated with the Ningaloo Current may support the large euphausiid populations
common to the Ningaloo region; Chap. 3). These hypotheses provide a good starting
point for further ecological investigations within this region.
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