Oceanographic forcing of phytoplankton dynamics in the ...€¦ · nutrients. Thus, both in the DCM...

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

1

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

2

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


4

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


6

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.


8

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


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


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


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).


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


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.,


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).


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


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).


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).


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


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).


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).


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;


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).


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


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).


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).


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


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


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


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)


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).


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).


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,


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).


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


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.


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.


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


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).


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.


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


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).


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)


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


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.


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,


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.


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.


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


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


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.


53

(b)

Figure 3.4. Cont’d.


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.


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).


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.


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.


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.


59

(b)

Figure 3.7. Cont’d.


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


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.


62

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


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).


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


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.


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.


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).


68

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).


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


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


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


72

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


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


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


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.


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)


76

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


78

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


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.


4.3.1 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


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.


82

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).


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.


84

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


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


86

Figure 4.2. Relative frequency of phytoplankton biomass (as chl a) at the surface and

DCM within Leeuwin Current/offshore waters.


87

Figure 4.3. Linear regression of particulate organic carbon (POC) versus chlorophyll a,

for surface and deep chlorophyll maximum (DCM) samples.


88

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


89

Figure 4.4. Relative frequency of phytoplankton biomass (as phytoplankton carbon) at

the surface and DCM within Leeuwin Current/offshore waters.


90

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;


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.


92

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


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.


94

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


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


96

Figure 4.7. Comparison of areal and volumetric primary production rates under

contrasting conditions of a) photoinhibition (), and b) light attenuation coefficient (Kd).


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


98

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).


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)


100

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.


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.


102

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.


104

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


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


106

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


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.


108

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


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.


110

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


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


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,


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.


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


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


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.


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;


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).


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


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.


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).


122

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


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


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


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


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.


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


128

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


129

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).


130

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.


131

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)


132

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.


133

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 –


134

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).


135

Figure 5.5. The geographic location of the four main chemotaxonomic clusters (see

Fig. 5.4) identified in surface (< 2 m) waters.


136

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).


137

Figure 5.7. The geographic location of the three main chemotaxonomic clusters (see

Fig. 5.6) identified at the DCM.


138

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


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).


140

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)


141

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)


142

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


143

*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.


144

Figure 5.9. Total cell count (from light microscopy) vs. chl a concentration (from

HPLC analyses) for surface and deep chlorophyll maximum (DCM) samples.


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).


146

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


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.


148

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


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


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


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,


152

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


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


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


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


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.


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.


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


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.


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


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.


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


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


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


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).


166

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.


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.


168

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).


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.


170

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.


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


172

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 - - - - - - - -


174

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.


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


176

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).


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


178

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.


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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


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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).


182

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).


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.


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.


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).


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.


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


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


190

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.


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


192

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.


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


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.


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


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


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


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


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


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


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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Oceanographic forcing of phytoplankton dynamics in the ...€¦ · nutrients. Thus, both in the DCM...

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