Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study · The coral reef ‘paradox’ has been the subject of much study, and various mechanisms have been proposed to explain how

Oceanic Inputs to CoralReefs: Ningaloo Reef

Case Study

Rebecca Gianotti

This dissertation is submitted as partial fulfilment of therequirements for the Degree of Bachelor of Engineering

(Environmental)

Department of Environmental EngineeringUniversity of Western Australia

4 November 2003

Final Year Project

i

In all things of nature there is something of the marvelous.

Aristotle (384 BC - 322 BC), Parts of Animals

The beginning of knowledge is the discovery of something we do not understand.

Frank Herbert (1920 - 1986)

Whenever you are asked if you can do a job, tell 'em, 'Certainly I can!' Then get busy and find

out how to do it.

Theodore Roosevelt (1858 - 1919)

ii

A C K N O WL E D G E M E N T S

I received an enormous amount of support throughout this project, for which I am greatlyindebted:

Thankyou firstly to the Australian Institute of Marine Science and the Department ofConservation and Land Management (W.A.) who provided the funding necessary toundertake the fieldwork. Thanks also go to the Institute for Earth Sciences at HebrewUniversity, Israel, who funded a large portion of the laboratory analysis.

Of the individuals who provided support, my greatest thanks go to my supervisor Dr AnyaWaite, whose organisation of the field and lab work and general direction and guidanceensured this project was completed, while her enthusiasm for the project and unfailing goodspirits made it an enjoyable experience despite periodic events of insanity.

Thanks go to Dr Jonathan Erez (Institute for Earth Sciences, Hebrew University, Israel) forhis help with the project direction and motivation, suggestions for fieldwork and laboratoryanalysis of the samples.

Thankyou to Dr Mark Meekan (AIMS) for his help in project collaboration, funding forfieldwork and fieldwork direction. The fieldwork in this project was conducted under thesupervision of Mark and with the assistance of Samantha Duggan (employee of AIMS) andIan Henderson (engineer on board the Cape Ferguson). Ian conducted the deployment of theCTD probe and Niskin bottles, and Sam assisted me greatly with dealing with the sampledwater and providing a much-needed buddy during the field trip. Thanks also to the rest of theguys on board – Brett Brownlow, Justin McCallum, Cary McLean and Dan Ryan, for theirfriendship and help during the field trip.

At the Centre for Water Research, thankyou to: Georgina Sturrock for her help withorganising fieldwork equipment and for the laboratory analysis of the oceanic nutrients;Christine Hanson and Mun Woo (PhD students) for help with the chlorophyll analysis andwith identifying oceanographic processes and the local currents; and Dr Anas Ghadouani, forhis help with the section on isotope signatures and offering advice on short notice. Thankyouto my fellow thesis students, especially Andrew Crawford, Karina Congdon and MayaWhiteley, for their assistance and motivation.

Thankyou to Bob Black, Jane Prince and Glenn Shiell (Department of Zoology, UWA) forhelp with the identification of reef organisms, and to John Beesley (Animal Science,Department of Agriculture, UWA) for freeze-drying all the samples.

Thankyou to Corey Whisson, Shirley Slack-Smith, Dr Jane Fromont and Loisette Marsh,from the Department of Aquatic Zoology at the WA Museum, for their help in identifying thereef specimens.

Finally, I am forever grateful to Gajan Sivandran, for his help in the project, continualsupport, belief in me, and most of all his unfailing love and enthusiasm.

iii

A B S TR A C T

The coral reef ‘paradox’ has been the subject of much study, and various mechanisms havebeen proposed to explain how coral reefs maintain high levels of gross productivity.Regardless of which mechanism is dominant, coral reefs need to filter large volumes ofoceanic water to obtain the steady input of nutrients they require. The objectives of this studywere to: 1) investigate the oceanographic environment around a coral reef and 2) attempt tounderstand the isotopic composition of key organisms within the reef, with a view tocontributing to analysis of the reef’s nutrient sources. Fieldwork was conducted on a sectionof reef located within Ningaloo Marine Park, Western Australia, during May 2003, whichincluded both oceanographic and reef sampling. Physical, chemical and biologicalcharacteristics of temperature, salinity, dissolved oxygen, dissolved inorganic nitrogen andphosphorous, chlorophyll a concentration and _13C and _15N stable isotope values weremeasured from water samples. A total of 26 reef specimens were collected for _13C and _15Nstable isotope analysis.

The results indicate that the oceanographic environment around Ningaloo Reef is highlycomplex, characterised by several concurrent processes. Upward tilting of isotherms andisohalines towards the shoreline suggest upwelling was present in the area, probably due tothe interaction between the Leeuwin and Ningaloo currents. As a result of offshore processes,a deep chlorophyll maximum was observed offshore and an area of increased productivitywas observed in front of the reef. There was a gradient of increasing temperature, dissolvedinorganic nitrogen and chlorophyll a concentration from north to south, possibly indicatingthe presence of a recirculation pattern near Point Cloates influencing the front of the reef. Thewater found in the channel between reef sections was identified as coming from deep watersoffshore, possibly emanating from an internal wave at the North West Shelf. The reef wasfound to be influencing the local waters through an export of material, to both the lagoon andocean, and by filtering nutrients from the incoming oceanic water. Export was indicated byhigher levels of dissolved inorganic nutrients and filtering by a decrease in nutrients in frontof the reef.

The reef organisms displayed stable isotope ratios indicative of their trophic position andfeeding habits, comparable with values in the literature. These ratios are suggestive of theoffshore environment and indicate the importance of the ocean water as a nutrient source forthe reef. It is likely that nutrients for the reef are gathered over a large range of oceanic water.

This study represents an attempt to relate local oceanography with open sea sources ofnutrients for coral reefs. Further work on identifying the circulation patterns of sources ofnutrients and more extensive parameter sampling will lead to greater insight in this field ofstudy.

iv

G L O S S A R Y

_13C Stable isotope signature for fractionated carbon – 13C/12C_15N Stable isotope signature for fractionated nitrogen – 15N/14N‰ per mil, units for stable isotope ratiosahermatypic corals Corals without a symbiotic relationship with zooxanthellaealgal ridge Ridge of hard encrusting algae on front of reef facing wavesatoll A ringlike coral island and reef that nearly or entirely

encloses a lagoonautotroph An organism capable of synthesising its own food from

inorganic substances, using light or chemical energyback reef Part of the reef flat, on the lagoon side of the reefbarrier reef Type of coral reef, separated from landmass by wide lagoon

too deep for coral growthbiogenic Produced by living organisms or biological processeschannel Pass between reef sections linking lagoon to open oceanfringing reef Type of coral reef, close to landmass with narrow lagoonfront reef Part of the reef flat, on the ocean side of the reefhermatypic corals Corals in a symbiotic relationship with zooxanthellaeheterotroph An organism that cannot synthesise its own food and is

dependent on complex organic substances for nutritionisohalines Contours of identical salinity value in the water columnisotherms Contours of identical temperature value in the water columnlagoon Area of water enclosed by either reef or landmassoligotrophic Lacking in plant nutrients and containing large amounts of

dissolved oxygenparticulate organic aggregates/matter Non-dissolved organic material, can form large aggregatespelagic Relating to the open ocean or ocean water columnphotic zone The layer of the ocean water that is penetrated by sufficient

sunlight for photosynthesisprimary production Creation of organic material through photosynthesis, fixation

of particles from the atmosphere to produce nutrientspsu Practical salinity units – measurement of water salinityreef flat Main body of coral reef, between algal ridge and lagoonrespiration Process of obtaining energy by consuming oxygen and

releasing carbon dioxide and water, reverse of productionsecondary production Production of organic material through consumption of

primary producers, grazing on photosynthesising organismsstanding stock/crop Amount of biomass present at any one timesymbionts Organisms existing in a symbiotic relationshipthermocline Layer in the water column over which temperature changes

rapidly between surface mixed layer and bottom watersturnover rate Ratio of production to respiration, measure of how quickly

nutrients are used and cycled through a systemupwelling Process of deep offshore waters being brought closer to the

surface onshore due to Ekman transportzooxanthellae Type of photosynthesising algae, a species of dinoflagellate,

living within a coral in a symbiotic relationship

v

TA B L E O F C O N T E N T S

ACKNOWLEDGEMENTS ..................................................................................................... II

ABSTRACT ............................................................................................................................ III

GLOSSARY............................................................................................................................ IV

TABLE OF CONTENTS ..........................................................................................................V

LIST OF FIGURES ...............................................................................................................VII

LIST OF TABLES ............................................................................................................... VIII

1 INTRODUCTION..............................................................................................................1

2 BACKGROUND ................................................................................................................4

2.1 CORAL REEF ECOLOGY ..........................................................................................42.1.1 Structure of coral reefs .........................................................................................42.1.2 Types of reefs and their formation.........................................................................52.1.3 Zonation of a coral reef system .............................................................................72.1.4 Reef distribution and limiting factors ....................................................................8

2.2 CHARACTERISTICS OF MARINE SYSTEMS INFLUENCING CORAL REEFDEVELOPMENT..................................................................................................................10

2.2.1 Important components of oceanic waters.............................................................102.2.2 Controlling factors on production .......................................................................12

3 LITERATURE REVIEW ................................................................................................14

3.1 CORAL REEF PARADOX AND ASSOCIATED STUDIES......................................143.1.1 Internal compensation mechanisms.....................................................................153.1.2 Inputs FROM open ocean water..........................................................................243.1.3 Summary of nutrient sources...............................................................................27

3.2 MOTIVATION FOR STUDY.....................................................................................283.3 NINGALOO REEF ....................................................................................................28

3.3.1 Previous studies on Ningaloo Reef......................................................................303.3.2 Physical characteristics of Western Australian coastline.....................................35

3.4 MEASURING NUTRIENT FLUXES AND SOURCES .............................................403.4.1 Methods used to measure nutrient fluxes and sources .........................................403.4.2 Use of stable isotope signatures ..........................................................................42

4 METHODOLOGY...........................................................................................................49

4.1 STUDY SITE .............................................................................................................494.2 FIELDWORK ............................................................................................................50

4.2.1 Water sampling...................................................................................................514.2.2 Reef organism sampling......................................................................................564.2.3 Transport of samples...........................................................................................564.2.4 Sources of error in sampling ...............................................................................57

4.3 LABORATORY ANALYSIS OF SAMPLES.............................................................574.3.1 Analysis of POC, PON and isotope signatures ....................................................574.3.2 Analysis of chlorophyll a concentration ..............................................................584.3.3 Analysis of nutrient concentrations .....................................................................614.3.4 Reef organism analysis for isotope signatures .....................................................62

5 RESULTS.........................................................................................................................63

vi

5.1 CTD DATA ................................................................................................................635.1.1 Offshore stations.................................................................................................635.1.2 Channel station comparison ...............................................................................73

5.2 WATER SAMPLING DATA......................................................................................765.3 STABLE ISOTOPE RATIO SAMPLING...................................................................83

5.3.1 Water samples ....................................................................................................835.3.2 Reef Specimens ...................................................................................................85

6 DISCUSSION...................................................................................................................87

6.1 LOCAL OCEANOGRAPHIC ENVIRONMENT .......................................................876.1.1 Upwelling ...........................................................................................................876.1.2 North to south gradients......................................................................................906.1.3 Effect of reef on surrounding water.....................................................................916.1.4 Channel pass ......................................................................................................93

6.2 NUTRIENT SOURCES FOR THE REEF ..................................................................95

7 CONCLUSIONS ..............................................................................................................99

8 RECOMMENDATIONS ...............................................................................................100

9 REFERENCES...............................................................................................................103

10 APPENDICES ................................................................................................................ I

10.1 DESCRIPTION OF SAMPLE POSITION, DEPTH, FILTRATION, ANALYSIS PERFORMED AND

CTD DROP FOR EACH STATION SITE ............................................................................................ I10.2 POSITION IN LATITUDE AND LONGITUDE OF EACH WATER AND REEF ORGANISM

SAMPLING SITE………………………………………………………………………………………...VI10.3 IDENTIFICATION OF REEF ORGANISM SAMPLES ............................................................. VII

vii

L I S T O F F I G U R E S

Figure 1: Different types of reefs in order of formation: fringing, barrier and atoll (Mann2000) ...................................................................................................................................6

Figure 2: Zones of a coral reef (Mann 2000) ................................................................................8Figure 3: Location of Ningaloo Reef Marine Park (Storrie and Morrison 1998) .........................30Figure 4: Wind circulation patterns around Ningaloo Reef (Hearn et al. 1986)...........................31Figure 5: Passage of Leeuwin Current down west coast of Australia, with other local currents

also shown (Woo and Pattiaratchi 2003).............................................................................37Figure 6: Ningaloo Current off northwest Australia (Hanson 2003)............................................39Figure 7: Recirculation pattern south of Point Cloates, as proposed by Taylor and Pearce

(1999) ................................................................................................................................40Figure 8: Sampling sites on chosen reef section - water and reef sampling (map taken from

Royal Australian Navy 1985) .............................................................................................50Figure 9: Deployment of the Niskin bottle .................................................................................52Figure 10: Deployment of the CTD probe ..................................................................................53Figure 11: Transfer of sample water from Niskin bottle to 20 L storage container ......................54Figure 12: Filtering sample water onto Whatman GF/F filters ....................................................55Figure 13: Temperature contours along the northern transect, shown in cross-section ................65Figure 14: Temperature contours along the middle transect, shown in cross-section...................65Figure 15: Temperature contours along the southern transect, shown in cross-section ................66Figure 16: Salinity contours along the northern transect, shown in cross-section ........................68Figure 17: Salinity contours along the middle transect, shown in cross-section ..........................68Figure 18: Salinity contours along the southern transect, shown in cross-section........................69Figure 19: Dissolved oxygen concentration contours on the northern transect, shown in cross-

section................................................................................................................................71Figure 20: Dissolved oxygen concentration contours on the middle transect, shown in cross-

section................................................................................................................................71Figure 21: Dissolved oxygen concentration contours on the southern transect, shown in cross-

section................................................................................................................................72Figure 22: Comparison of temperature profiles for channel and selected offshore stations..........73Figure 23: Comparison of salinity profiles for channel and selected offshore stations.................74Figure 24: Temperature versus salinity for channel pass and majority of offshore stations..........75Figure 25: Comparison of dissolved oxygen concentration profiles for channel and selected

offshore stations .................................................................................................................75Figure 26: Comparison of DIN concentration profiles for offshore and lagoon stations ..............77Figure 27: Comparison of DIP concentration profiles for offshore and lagoon stations...............79Figure 28: Comparison of DIN and DIP concentrations with Redfield ratio for ocean waters .....81Figure 29: Comparison of chlorophyll a profiles for offshore and lagoon stations ......................82Figure 30: Regions used for presentation of summary stable isotope ratios from water

sampling ............................................................................................................................83Figure 31: _13C and _15N stable isotope ratios, for reef specimens and various water sampling

locations.............................................................................................................................86Figure 32: Speculative representation of oceanographic environment around sampled section

of Ningaloo Reef................................................................................................................94

viii

L I S T O F TA B L E S

Table 1: Summary of temperature data for the three transects and the channel ...........................64Table 2: Summary of the salinity values for the transects and the channel ..................................67Table 3: Summary of the dissolved oxygen concentrations from the transects and channel.........70Table 4: Summary of the DIN concentrations for the transects and lagoon stations ....................77Table 5: Summary of the DIP concentrations for the transect and lagoon stations ......................79Table 6: Summary of the chlorophyll a concentrations for the transect and lagoon stations ........81Table 7: Summary of _13C values for the transect and lagoon stations........................................84Table 8: Summary of the _15N values for the transect and lagoon stations ..................................84Table 9: Summary of the _13C ratios analysed from the reef organism specimens.......................85Table 10: Summary of the _15N ratios analysed from the reef organism specimens ....................85

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study Introduction

1

1 I N T R O D U C T I O N

Coral reefs are very important marine ecosystems for recreational purposes, commercial uses,

aesthetic beauty and abundance and diversity of life forms. More generally they are important

as natural systems that contribute to global processes such as climate regulation and

greenhouse mitigation. Coral reefs should therefore be carefully managed and attempts made

to better understand their functions.

It was noted early on in reef studies that coral reefs have very high rates of gross primary

production, at one reef approximately 24 gC/m2/day (Odum and Odum 1955), which is

especially high when compared with the relatively low rates found in the oceanic water

passing over them (about 0.2 gC/m2/day, Sargent and Austin 1949). This finding led to

considerable discussion of the apparent ‘coral reef paradox’ – how do coral reefs sustain such

high production when they are not fed high concentrations of nutrients?

Proposed explanations for this phenomenon include various internal recycling mechanisms

(e.g. Pomeroy 1970, Muscatine and D’Elia 1978, Sorokin 1990), inputs from sediments and

caves (Froelich 1983), nitrogen fixation (e.g. Wiebe et al. 1975) and efficient filtering of large

volumes of oceanic water (e.g. Erez 1990). These internal mechanisms are thought to account

for the observed high rates of gross productivity, and it is likely that all of them are important

for a coral reef’s growth.

It has also been found that the turnover rate (the ratio of production to respiration rates) for

the whole reef system at several study sites averages approximately 1, although it varies

between reef systems and between parts of an individual system; meaning that coral reefs

cycle nutrients rapidly within the system, but don't accumulate biomass very quickly (Kinsey

1983). Therefore any net productivity (production minus respiration, which is low) is thought

to be able to be maintained by the continual input of low concentrations of nutrients from the

open ocean. Additionally, any inefficiency in recycling mechanisms or losses from the system

appears to be compensated for by these oceanic inputs.

These findings highlight the necessity of understanding the local oceanography of coral reef

systems and how the oceanic water is supplying the reef system with nutrients. What remains

to be quantified is the link between the local oceanographic environment and the nutrient

sources for coral reefs. This is especially important in areas where the adjacent ocean to a reef

is used commercially, for example for oil exploration, fishing or high volumes of tourists,


2

because these activities could impact on the reef’s oceanic sources of nutrients, send pollution

towards the reef or alter the flow patterns near the reef system.

The objectives of this study were to investigate the oceanographic environment around a coral

reef and attempt to understand the isotopic composition of key organisms within the reef, with

a view to contributing to analysis of the reef’s nutrient sources. The study used a sample site

within Ningaloo Reef as the basis for fieldwork to investigate these questions.

Ningaloo Reef is located offshore of northwest Australia and is positioned relatively far south

for a coral reef, primarily due to the presence of the Leeuwin Current. It is an important reef,

as its presence in the junction between tropical and temperate waters makes it rare, if not

unique in the southern hemisphere (Storrie and Morrison 1998). It is also the largest fringing

coral reef in Australia and important for tourist and fishing opportunities. In addition, there

are potential impacts from oil production activities in the North West Shelf area, as well as

more localised effects from local commercial and development activities, leading to the

necessity for preservation and appropriate management strategies (D'Adamo and Simpson

2001).

The sampling regime undertaken in this study included both oceanographic and reef

sampling. CTD data was gathered to measure the temperature, salinity and dissolved oxygen

values of the ocean water and attempt to characterise the local hydrodynamic processes.

Water samples were taken for analysis of dissolved inorganic nitrogen (as nitrate and nitrite)

and phosphorous (as phosphate), particulate organic carbon and nitrogen, chlorophyll a

concentration and stable isotope ratios of _13C and _15N. These measurements can help

describe the waters flowing onto the reef and suggest areas of relatively high and low

productivity. It was also hoped that analysing this data could provide evidence of how the reef

filters nutrients from the oceanic waters. Water samples were also taken from behind the reef

in the lagoon waters to identify how nutrients are exported from the reef system.

Specimens were taken from the reef to attempt to understand (using the abovementioned

isotopes) the isotopic composition of key organisms within the reef by comparing the isotope

ratios of the reef specimens with those observed in the ocean waters.

In summary this study provides a first attempt to describe how Ningaloo Reef is receiving

nutrients from oceanic waters and contributes to understanding about the reef’s nutrient

sources. This will become particularly important as tourist operations, land-based

developments and oil exploration in the North West Shelf area become more advanced, and


3

further work of this kind can help identify the potential for these commercial developments to

impact on the reef.

This dissertation is divided into chapters. Chapter 2 provides an introductory background to

the nature of coral reefs and influences on their production, for the benefit of readers not

familiar with these ecosystems. Chapter 3 presents a critical discussion of research undertaken

in the field of nutrient sources to coral reefs and outlines the motivation for and objectives of

this study. Also contained in Chapter 3 is an introduction to the study area of Ningaloo Reef,

the local oceanographic context and an overview of the work that has been conducted thus far

on the reef. Finally, Chapter 3 presents a discussion of the methods used in this study,

focussing on the use of stable isotope values. The study site and methodology used for

fieldwork are described in detail in Chapter 4, with the results from the fieldwork presented in

Chapter 5. Implications of these results are discussed in Chapter 6, and then conclusions and

recommendations for further work in this area are presented in Chapters 7 and 8 respectively.

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study Background

4

2 B A C K G R O U N D

This chapter provides an introductory background to the nature of coral reefs and influences

on their production. This includes the structure, formation and zoning of coral reefs,

limitations on their production and a brief overview of the important characteristics of marine

systems with respect to coral reefs.

2.1 CORAL REEF ECOLOGY

Coral reefs dominate the shallow inshore waters of a large portion of the tropics and are often

used to define the limits of the tropical marine environment. In the Indian Ocean coral reefs

are found in East Africa, the Red Sea and throughout the Indo-Pacific area as far east as

Hawaii (Achituv and Dubinsky 1990). They are globally significant ecosystems, in that about

half the calcium that enters the world’s oceans each year is taken up and bound into coral

reefs as calcium carbonate (Nybakken 2001). Since each bound calcium atom requires the

incorporation of a molecule of carbon dioxide, reefs also remove about 700 billion kilograms

of carbon from the atmosphere every year, and are therefore very important to the continuing

health of the marine environment and the planet (Nybakken 2001). Coral reefs have existed

on the earth for hundreds of millions of years. Despite their long history and ability to create

the most massive structures built by living organisms, the thin layer of living coral tissue

seems particularly sensitive to a number of natural and man-made disturbances (Nybakken

2001), necessitating adequate monitoring and management to ensure their continued health

and existence.

2.1.1 STRUCTURE OF CORAL REEFS

Coral reefs are biogenic marine ecosystems, meaning that they are produced by living

organisms and biological processes in situ (Achituv and Dubinsky 1990). The reef bases are

essentially massive deposits of calcium carbonate, produced primarily by corals with lesser

additions from calcareous algae and other organisms that secrete calcium carbonate

(Nybakken 2001). Although corals are found throughout the oceans of the world, in polar and

temperate seas as well as the tropics, it is only in the tropics that reefs achieve their greatest

development and diversity. This is because there are two different types of corals, hermatypic

and ahermatypic (Nybakken 2001). Hermatypic corals are those that produce reefs,

ahermatypic do not. While ahermatypic corals are found worldwide, the most important

hermatypic corals are found in warm, transparent and well-illuminated oligotrophic waters,

like those in the tropical regions of the Indo-Pacific and Atlantic Oceans (Achituv and

Dubinsky 1990). The distinguishing characteristic between the two is that most hermatypic


5

corals have a symbiotic relationship with microscopic photosynthesising algae called

zooxanthellae, which live in their tissues, while ahermatypic corals do not.

It has been suggested that the morphology of reefs is explained by the action of wind, waves

and currents (Fairbridge 1950), and the importance of hydrologic-bathymetric-biological

balances (Maxwell 1968, in Achituv and Dubinsky 1990). More recent work has stressed that

the morphology and depth of the pre-Holocene reef surface, nature of the Holocene sea-level

curve and net rate of reef accretion are also important factors in shaping contemporary reefs

(Hopley 1983).

The calcified structures formed by corals are only the base of a coral reef ecosystem. There

are numerous other organisms important for coral reef systems, including seaweeds,

invertebrates such as sea urchins, sea cucumbers, various molluscs, sponges, free-swimming

phytoplankton and zooplankton and worms, as well as vertebrates including numerous species

of reef fish, eels and larger predators such as sharks. The coral reef ecosystem incorporates

many and complex relationships between these components.

2.1.2 TYPES OF REEFS AND THEIR FORMATION

Coral reefs are generally classified into three categories, according to Charles Darwin’s

theory: atolls, fringing reefs and barrier reefs (Achituv and Dubinsky 1990). Atolls are usually

easily noticeable because they rise out of deep water far from large landmasses and are

horseshoe or ring-shaped reefs, each surrounding a sub-circular lagoon (Nybakken 2001).

Both barrier and fringing reefs occur adjacent to a landmass, where a barrier reef is separated

from the land by a greater distance and deeper lagoon than the fringing reef (Nybakken 2001).

Fringing reefs closely follow shorelines, leaving only a narrow and shallow lagoon between

reef and land (Achituv and Dubinsky 1990). These types of reefs are common in the Red Sea,

along the shores of East Africa and around the Indo-Pacific islands. In addition to these three

classifications, studies using aerial photography and geological drilling for seismic profiling

have resulted in a number of schemes that subdivide the three original reef types into

numerous sub-types, based on morphological criteria and developmental or genetic

considerations (Achituv and Dubinsky 1990). These additional classifications are not widely

used and therefore not discussed here. The three main types of reefs are shown in Figure 1, in

order of formation according to Darwin’s theory.


6

Figure 1: Different types of reefs in order of formation: fringing, barrier and atoll (Mann 2000)

The most common explanation for the formation of atolls was first espoused by Charles

Darwin, and is called the subsidence or compensation theory (Nybakken 2001). According to

this theory, atolls are created when fringing reefs begin to grow on the shores of newly

formed volcanic islands that have pushed to the surface from deep water. These islands often

subside, and if the subsidence is not too rapid, the reef growth can keep pace with the

subsidence, such that a barrier reef will then form, finally leaving an atoll as the island

subsides below sea level (Nybakken 2001).

Darwin’s theory was recently verified by drilling through atolls to find volcanic rock under

layers of limestone (Ladd et al 1953, as in Achituv and Dubinsky 1990), and further

strengthened by the discovery of guyots: flat-topped submerged mountains with remains of

corals at their surface (Nybakken 2001).

Darwin’s theory links all three types of reefs in a sequence but does not explain the

appearance of all fringing and barrier reef types. Where fringing and barrier reefs occur

around continental margins and non-volcanic islands, the subsidence theory does not seem to

apply. Reefs may also be much younger than atolls, which are often very old structures. In

these other cases, reefs appear to grow simply because there are suitable environmental

conditions and substrate on which to begin growth (Nybakken 2001).


7

2.1.3 ZONATION OF A CORAL REEF SYSTEM

Coral reefs are complex ecosystems, with different physical locations able to provide habitat

for a wide variety of species. On a local scale, zonation within a reef is determined primarily

by the interaction of current direction and intensity and the underwater light field (Done

1983).

Lagoons between the shore and the reef are protected from strong oceanic swells, and contain

sandy bottoms that provide a good location for the growth of seagrass meadows and hard

corals (Storrie and Morrison 1998). Offshore from the lagoon is a reef flat or ‘back reef’, a

usually shallow area that is washed by a strong surge of water flowing from the surf that

breaks on the reef’s outer edge (Storrie and Morrison 1998). The continuous flow of water

brings nutrients and oxygen to corals on the reef flat, which can take advantage of the shallow

water and thus proximity to abundant sunlight (Storrie and Morrison 1998).

The most rapidly calcifying zone of the reef is the algal ridge, which is a strong bulwark

formed of encrusting coralline algae that resists wave destruction, situated at the foremost part

of the reef (Nybakken 2001). The algal ridge is subject to the highest wave energies

experienced by the reef (Achituv and Dubinsky 1990). The outer edge of the reef drops off to

a rocky bottom, about 10 to 25 m deep. This drop is often steep and has been weathered by

constant swells that have hit the reef edge over a long period of time. Marine life is extremely

diverse and prolific in this region (Storrie and Morrison 1998). Beyond the drop off, the

bottom slopes gently offshore towards deep water.

Passages or breaks in the reef flat form channels between the open ocean and the lagoon, and

can occur every few kilometres along a coral reef (Storrie and Morrison 1998). These

channels serve to allow the passage of water from ocean to lagoon and vice versa (Hearn et

al. 1986). The exchange of water through these channels due to tidal and swell action

provides a good habitat for an array of marine life (Storrie and Morrison 1998).

The zones of a coral reef are illustrated in Figure 2.


8

Figure 2: Zones of a coral reef (Mann 2000)

These differing areas of substrate, exposure to wave and current action and growth of

different kinds of algae or seagrass mean that coral reefs are able to support a huge diversity

of organisms within a relatively small geographical area (Nybakken 2001). Because these

different factors vary in their extent or presence on reefs, gradients in water motion, light

penetration and biological interactions (competition, grazing and predation) lead to zonal

patterns within reefs (Nybakken 2001).

2.1.4 REEF DISTRIBUTION AND LIMITING FACTORS

The primary producers of the reef, including seaweeds, phytoplankton and the zooxanthellae

themselves, are subject to controls on their production due to characteristics of the ocean

environment.

Five major physical factors limit coral reef development: temperature, light, salinity,

sedimentation and emergence into air (Nybakken 2001). In, addition, there are physical

characteristics of oceanic systems that influence coral reef development, including waves,

tidal action and wind stress.

Temperature

Nearly all coral reefs are found only within the 20 oC surface isotherm, and no reefs develop

where the annual mean minimum temperature is below 18 oC; optimal reef development

occurs in waters where the mean annual temperatures are about 23 – 25 oC (Nybakken 2001).

It is generally thought that these boundaries on reef growth are determined by subtle

temperature effects on feeding or on reproduction patterns (Achituv and Dubinsky 1990).


9

Light

Coral reefs do not develop in water that is deeper than about 50 – 70 m, and most reefs grow

in depths of 25 m or less, which is why reefs are restricted to the margins of continents or

islands (Nybakken 2001). This depth restriction is due to the hermatypic corals’ need for

light, which is crucial for photosynthesis by the zooxanthellae in the coral tissue.

Salinity

Restriction by salinity is due to the fact that hermatypic corals are true marine organisms and

therefore are intolerant of salinities significantly different from that of normal sea water

(approximately 32 – 35 psu) (Nybakken 2001). Because of this dependence on saline waters,

corals are absent from coastlines that have significant inflows of freshwater from river

discharges, for example on the east coast of South America (Nybakken 2001).

Sedimentation

Sedimentation adversely affects corals because it clogs their feeding structures. Although

many corals have a limited ability to remove sediment by trapping it in mucus and carrying it

off by ciliary action, too much sediment overwhelms this cleaning mechanism and smothers

the corals (Nybakken 2001). Also, although the bathymetric distribution of reefs is

determined by light, their actual depth limit depends on water transparency (Achituv and

Dubinsky 1990). Turbidity reduces water clarity and therefore restricts the amount of light

reaching photosynthesising organisms, decreasing coral reef growth (Nybakken 2001).

Adverse effects of sedimentation, for example, are the reason that coral reefs are absent near

the outlets of all dry riverbeds along the Sinai Peninsula (Achituv and Dubinsky 1990).

Emergence into air

The final limitation to coral reef development is emergence into air. While the production of

mucus can keep corals hydrated for a short time, most corals are killed by prolonged exposure

to air (more than a couple of hours at a time). This therefore restricts the vertical growth of

corals to the level of low tides (Nybakken 2001).

Waves

Coral reef development is generally greater in areas of moderate wave action, which provides

a constant source of fresh, oxygenated seawater, plankton and nutrients to the reef,


10

simultaneously preventing sediment from accruing on the reef (Nybakken 2001). It is

suggested that for reefs exposed to ocean swells or large waves, the main transport of water

into lagoons is by waves over-topping the outer ridge of the reef and subsequently flowing

over the reef (Andrews and Pickard 1983). The coral reef structure is usually resistant to

damage by wave action and can adapt its structure to a degree under different intensities of

wave action (Nybakken 2001).

Tidal action

Tides result in several important processes with regard to coral reefs. Firstly, they can

potentially expose the living base of the reef to the air and direct sunlight during low tides,

which can severely damage the reef. Secondly, they generate swift currents around and over

reefs, which are important for bringing fresh supplies of oceanic nutrients and plankton to the

reef and advecting waste products away from the reef (Nybakken 2001). Finally, tidal

currents are highly important for causing exchange of water between the lagoon and oceanic

waters.

Wind stress

For reefs that are less exposed to wave action, local wind stress and tides together are

important for causing flow of water over reefs, essential for delivering nutrients to the back

reef areas and lagoonal waters (Andrews and Pickard 1983). Additionally, wind stress is

important for water circulation within deep lagoons and passages between reefs, and for

creating swell waves (Andrews and Pickard 1983).

2.2 CHARACTERISTICS OF MARINE SYSTEMS INFLUENCING CORALREEF DEVELOPMENT

2.2.1 IMPORTANT COMPONENTS OF OCEANIC WATERS

The characteristics of ocean waters are very important for influencing reef development,

because they bring fresh nutrients to the reefs and carry away waste. The most important

components of oceanic waters, in terms of primary production, are the smaller organisms –

phytoplankton and bacteria, which are briefly discussed here.

Phytoplankton

Phytoplankton are the primary photosynthesising organisms in open oceans, and therefore

form the base of the food web. The phytoplankton found in the surface layers of both

temperate and tropical seas are dominated by organisms in the nanoplankton and


11

picoplankton size fraction, in not only numbers of individuals but also the amount of

photosynthesis (Nybakken 2001). Pomeroy (1970) studied the cycling of minerals through

various systems, including oceanic waters and coral reefs. It was found that the most

important photosynthetic organisms in these waters, both numerically and photosynthetically,

are usually nanoplankton (Pomeroy 1970), which Odum and Odum (1955) have suggested

could be responsible for providing coral reefs with nutrients.

The small size classes of phytoplankton are not only abundant, but also show less seasonal

variation in biomass than the larger phytoplankton, particularly in warmer seas (Nybakken

2001). This steady state situation can be attributed to the characteristic stable hydrographic

regimes in the open ocean, which lead to steady low concentrations of nutrients. Low nutrient

concentrations favour smaller photosynthetic organisms, which have a proportionately greater

surface area to absorb the nutrients but a lower relative need (Nybakken 2001).

Bacteria

It is known that perhaps one quarter of the carbon fixed by photosynthesis in the ocean is lost

to the water as dissolved organic matter “leaked” from cells, which may be due to

microorganisms, primarily bacteria, directly taking up the dissolved organic matter

(Nybakken 2001). Such direct uptake may account for up to 50% of the total oceanic primary

productivity, and bacteria may not only take up dissolved matter but also attack both living

and dead particulate matter, thus freeing more dissolved matter to the water column

(Nybakken 2001). These findings suggest that bacteria are abundant in the water column, and

new techniques of counting have confirmed large numbers of free-living bacterioplankton,

with larger bacteria associated with planktonic particulate matter (Nybakken 2001).

Because bacteria are partly responsible for the regeneration of nutrients in the photic zone,

they permit the continued productivity of phytoplankton even in the absence of an influx of

nutrient-rich water, which is particularly important in the highly stratified waters of the

tropics and subtropics (Nybakken 2001). In addition to this, photosynthetic bacteria have been

shown as ubiquitous in seawater, responsible for a significant fraction of the photosynthetic

activity, especially in oligotrophic waters (Nybakken 2001).

Other plankton

The ecological interactions of the larger phytoplankton, primarily diatoms and dinoflagellates,

and the larger zooplankton, primarily copepods, still dominate coastal, upwelling and polar


12

seas (Nybakken 2001). As on land, primary production (from photosynthesising organisms

such as phytoplankton) is transferred into the food chain of the pelagic community through

the grazing activity of herbivores, including many protistan and invertebrate planktonic

species, but dominated by the larger herbivores – various species of copepods. The copepods

have been found in field studies to be responsible for the regulation of the larger

phytoplankton populations, and can graze on phytoplankton cells rapidly (Nybakken 2001). It

is possible for the standing crop of phytoplankton to decline due to grazing, while the rate of

primary production increases or remains steady, in which case the major portion of the carbon

fixed in photosynthesis appears not in the standing crop of phytoplankton, but in the standing

crop of zooplankton (Nybakken 2001).

Grazing, and hence the break up of phytoplankton cells during passage through the copepod

gut, releases the nutrients fixed by phytoplankton, which are then excreted back into the

water, keeping the nutrients constantly regenerated in the upper layers and allowing for

continued productivity (Nybakken 2001). In the tropics, there are no real pulses in either

phytoplankton or copepod cycles, but a steady but inconspicuous consumption by copepods

of the small phytoplankton crop (Nybakken 2001).

2.2.2 CONTROLLING FACTORS ON PRODUCTION

Primary production in the ocean is influenced by a number of factors, the most important of

which are light, nutrient supply and turbulence or water dynamics (Nybakken 2001). These

factors combine to determine the amount of primary production present in the oceanic waters

that reaches coral reefs.

Light

Photosynthesis is only possible when the light reaching an autotrophic cell is above a certain

intensity, limiting phytoplankton to the uppermost layers of the ocean, and limiting the depth

to which primary production can occur (Nybakken 2001). Therefore inputs of primary

producers to coral reefs are more likely to come from the surface waters.

Nutrient supply

The major inorganic nutrients required by phytoplankton for growth and reproduction are

nitrogen (as nitrate NO3-, nitrite NO2

-, or ammonium NH4+) and phosphorous (as phosphate

PO43-) (Nybakken 2001). Diatoms and silicoflagellates also require silicate (SiO2) in

significant amounts. Other inorganic and organic nutrients may be required in smaller


13

amounts. Nitrogen and phosphorous are usually treated as the limiting factors for

phytoplankton productivity under most conditions, because they are in short supply in most

oceanic waters, however it has also been suggested that low concentrations of trace elements

and vitamins in ocean water could contribute to the low standing-crop of phytoplankton

characteristic of the oceanic waters supplying coral reefs (Crossland 1983).

Water dynamics

Vertical mixing of the water column brings nutrients to the surface, but it also carries

phytoplankton cells into deeper waters. As long as vertical mixing is confined only to the

upper illuminated zone, the phytoplankton cells can be carried downward only a short

distance and will remain where there is sufficient light for photosynthesis. When mixing

includes the lower water mass however, it is possible for the plant cells to be carried well

below the compensation depth (where the rate of photosynthesis equals the rate of

respiration), therefore decreasing productivity (Nybakken 2001). Therefore the greatest

amount of primary productivity usually occurs at the intersection of the photic zone and the

reach of the deep water nutrients.

Characteristics of tropical seas

Light is optimal for phytoplankton production in tropical areas, because the upper waters are

well lit throughout the year. At the same time, the continual input of energy from the sun

maintains the surface layers of water at temperatures much higher than those of deeper

waters, which creates a density difference leading to stratification (Nybakken 2001). This

thermal stratification prevents mixing and the upward transport of nutrients, inhibiting high

production in tropical oceanic waters. Production is therefore low but constant throughout the

year (Nybakken 2001). This provides a continuous pulse of water with a low concentration of

productivity to coral reefs.

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study Literature Review

14

3 L I T E R AT U R E R E V I E W

This chapter presents a critical discussion of the research undertaken in the field of nutrient

sources to coral reefs and outlines the motivation for and objectives of this study. Also

contained in this chapter is an introduction to the study area of Ningaloo Reef, the local

oceanographic context and an overview of the work that has been conducted thus far on the

reef. Finally, this chapter presents a discussion of the methods used in this study, focussing on

the use of stable isotope ratios.

3.1 CORAL REEF PARADOX AND ASSOCIATED STUDIES

Coral reefs have traditionally been regarded as a paradox with regard to their productivity.

This belief arose from early studies on reef systems, primarily Sargent and Austin (1949 and

1954) and Odum and Odum (1955).

Sargent and Austin (1949 and 1954, as in Odum and Odum 1955) suggested that coral reefs

must subsist on their own primary production, because their studies indicated that the primary

production values of water in both the open sea and lagoon side of a reef were too small to be

of significance in comparison to the production of the whole reef. However, Sargent and

Austin’s work (1949 and 1954) did not prove that ocean water passing over the reef was not

quantitatively an important source of nutrition, only that production in the water while

passing over the reef was small relative to the attached community below (Odum and Odum

1955). Their work served to generate interest in nutrient sources for coral reefs.

Odum and Odum (1955), in their seminal work on the productivity of Eniwetok Atoll in the

Pacific Ocean’s Marshall Islands, found that the gross primary production of the reef could be

measured as 24 gC/m2/day, while the productivity of the water flowing onto the reef had been

measured as 0.2 gC/m2/day (Sargent and Austin 1949). Odum and Odum (1955) also noted

that: 1) the efficiency of the primary producers was low (suggesting that the reef was a steady

state community adjusted to low efficiency as a necessary compensation for high total

productivity); 2) total production on the reef was almost equal to the reef’s total respiration

(total production amounted to 26 g/m2/day while total respiration was 24 g/m2/day); and 3)

the reef acted as a highly efficient filter of the water crossing the reef.

Odum and Odum (1955) concluded that the reef was behaving as a steady-state system open

to the oceanic waters, however they were unsure of how the reef obtained sufficient amounts

of nitrogen and phosphorous to sustain its production. The authors also concluded that

whether the reef lives entirely on its on production or not, it is likely that it derives critical


15

nutrients from the strong flow over the reef system. They could not rule out the possibility

that oceanic water provided significant inputs particularly of nanoplankton and dissolved

organic matter (Odum and Odum 1955).

The research by Odum and Odum (1955) therefore provided the stimulus for much of the

research that has been subsequently conducted on nutrient supplies to coral reefs. Odum and

Odum (1955) outlined the problem of how coral reefs manage to sustain such high gross

primary productivity in low nutrient waters, suggesting internal recycling as one mechanism.

Their work also suggested the importance of large inflows of oceanic water for providing

coral reefs with the nutrients they require. Subsequent studies have confirmed the high gross

primary productivity of coral reefs, with an average production rate measured at about 7

gC/m2/day (Smith 1983). Various studies have been undertaken to investigate different

nutrient inputs to coral reefs, including different levels of recycling, inputs from sediments

and nitrogen fixation, and filtering of oceanic water.

The research to date has tended towards two research areas: 1) the use by reefs of a variety of

internal mechanisms, and 2) steady inputs of open oceanic water to coral reefs. These two

areas are discussed further in the following sections.

3.1.1 INTERNAL COMPENSATION MECHANISMS

Studies on coral reefs have measured net exports of nitrogen out of the reef system into the

lagoon (Odum and Odum 1955 and Webb et al. 1975), which would indicate that there needs

to be a concurrent input of nitrogen to the system to maintain a nitrogen balance.

Additionally, many studies have estimated that coral reefs have a net production of organic

material, some of which is suggested to be exported from the reef to the open ocean (Hata et

al. 1998), while other studies have actually measured a net export of organic particles from

coral reefs towards the surrounding ocean (e.g. Johannes 1967, Hata et al. 1998).

Considering these net exports alongside the comparatively low productivity rates of the open

ocean, it appears that coral reefs employ internal coping mechanisms to ensure they obtain the

necessary amounts of energy and nutrients. These mechanisms have been shown to exist on

several scales: the use of symbiotic relationships and thus recycling of material at the cellular

level; the efficient use of material between trophic levels and through multiple food webs; and

transfer of nutrients between separate sections of a reef system. In addition, localised inputs

of nutrients through use of internally produced particulate matter, geothermal endo-upwelling,


16

inputs from cave water and sediments, nitrogen-fixation and efficient cycling of phosphorous

have also been observed.

Recycling between symbionts

Recycling seems to be particularly important within the symbiotic relationship between a

coral and zooxanthellae pair. Photosynthetic rates by zooxanthellae in shallow-water corals

have been measured as high, with the carbon that is translocated from the algae to the coral

being able to meet the daily carbon demand of the coral for respiration and growth (Muscatine

and Kaplan 1994).

The importance of the recycling between symbionts has been reinforced by the work of

D’Elia (1977), who found that although symbiotic corals cannot obtain all the phosphorous

they require by uptake from ocean water, the ability to obtain part of the requirement from the

water column and recycle it efficiently, due to the symbiotic relationship, allowed these corals

to flourish in water with low levels of phosphorous. Additionally, little phosphorous has been

measured as lost from corals containing zooxanthellae (Pomeroy 1970).

Zooxanthellae have also been suggested as the reason that corals can uptake and retain

ammonium (Muscatine and D'Elia 1978). Symbiotic corals seem well adapted to low nitrogen

conditions, by retaining virtually all of the animal excretory ammonium and having the ability

to scavenge ammonium from the surrounding waters (Muscatine and D'Elia 1978).

Zooxanthellae are also very effective scavengers of dissolved nitrogen, often taking up

ambient dissolved inorganic nitrogen at or below concentrations of 1µmol/L (Muscatine and

Kaplan 1994).

Sorokin (1990) also highlighted the important role within symbiotic relationships of recycling

of material between the autotrophic and heterotrophic components, which increases efficiency

of use of localised nutrients.

It would therefore appear that at this level (that is, the cellular level in symbiotic

relationships), recycling allows for efficient use of nutrients, and can largely explain why

hermatypic corals are able to flourish in low nutrient waters. This however does not explain

how coral reef systems can maintain their productivity, given that the corals are only one part

of the whole system.


17

Recycling between trophic levels and food webs

Recycling can occur within the reef system by nutrients being consumed, excreted back to the

water column and then taken up again, or through very tight autotrophic-heterotrophic

relationships, where the nutrients do not necessarily have to be mixed back into the water

column (Atkinson 1987 and Erez 1990).

A recycling mechanism has been observed in pelagic systems where net plankton (greater

than 20 µm in diameter) seem to preferentially take up nitrogen in the form of nitrate (nitrate

is generally viewed as a “new” source of nitrogen, because it needs to be advected into a

system by fresh supplies of water) and nanoplankton and picoplankton (less than 20 µm in

diameter) preferentially take up ammonium and urea (viewed as “recycled” or “regenerated”

forms of nitrogen, because they are produced through the excretion of material by other

organisms) (Probyn et al. 1990). This difference in preferential uptake by different organisms

could suggest that the plankton system efficiently recycles nutrients to compensate for limited

availability in low-nutrient waters (Probyn et al. 1990).

It appears that all benthic communities release high quantities of organic matter to the reef

environment, which constitutes a very important energy pathway for the heterotrophic

processes in the reef system (Arias-Gonzalez et al. 1997). Modelling studies (Arias-Gonzalez

et al. 1997) using existing biological, physical and geomorphological data for fringing and

barrier reefs in French Polynesia, found that benthic heterotrophic activity, particularly the

heterotrophic bacteria pools, represent a significant contributor to reef productivity. This

study also found that the secondary production of both the fringing and barrier reef systems

was mainly based on detritus, with a proportion of the net primary production entering the

coral reef food chain through heterotrophic benthos links rather than direct usage (Arias-

Gonzalez et al. 1997). Microbial cycling in the benthos also comprised a large portion of the

detritus-based food chain (Arias-Gonzalez et al. 1997).

The importance of the detritus pathways in the study by Arias-Gonzalez et al. (1997) was

clear for both the fringing and barrier reefs, and the flow of organic matter in a detrital form

seemed to be an essential process in the total energy flow of the two reefs, with suggestions

that the majority of the net primary productivity was recycled directly to the detrital pool

rather than being consumed by herbivores. This process has also been suggested for coral reef

ecosystems elsewhere (e.g. Sorokin 1990).


18

The results from the modelling work suggested a globally efficient and rapid use of energy

within reef ecosystems, however organic waste was found to be higher in the lower trophic

levels than in the higher levels, due to the low assimilation and eco-trophic efficiencies at the

lower levels (Arias-Gonzalez et al. 1997). Because this lower assimilation and efficiency

induces a low input of matter and energy into the upper trophic levels, the authors suggested

that a very efficient recycling and feedback mechanism must be used to conserve this energy.

This was suggested to occur through two possible mechanisms: a relatively large cycle

produced through detritus and an associated microbial food web, with bacteria energy

conversion and algae transformation on the benthos (as previously discussed); and a relatively

short cycle directly produced through predation, with high internal predation and eco-trophic

efficiency in the middle and top of the food webs (Arias-Gonzalez et al. 1997). This suggests

that top-down and bottom-up controls are of equal importance in coral reef systems (Arias-

Gonzalez et al. 1997).

Therefore these studies indicate that the detrital and microbial food webs as well as efficient

autotrophic-heterotrophic links are very important for maintaining productivity in the reef

system.

Recycling between reef sections

Kinsey (1983) has presented a good review of community (sections of reef systems)

metabolism research on coral reefs, and summarises the work that has been done in many reef

studies looking at community production through photosynthesis, respiration and turnover

rates of these systems. The turnover rate is measured as the rate of gross production (through

photosynthesis) divided by the rate of gross respiration. For these various communities, it was

found that there is considerable variation in turnover rates between communities of a coral

reef (Kinsey 1983), which suggests that different processes are occurring in different sections

of the reef system.

From the few studies that have been conducted on the metabolism of an entire coral reef

system, it has been found that excess production (primary production through photosynthesis

minus respiration) is very close to zero, and turnover rates (ratio of production to respiration)

are equal to 1 for these systems (Kinsey 1983). This suggests that the varying turnover rates

expressed by reef communities as described above are balanced when taken in combination as

part of the whole system (Kinsey 1983). This finding is supported by the work of Kinsey

(1979), who found that the turnover rate is generally higher in high energy zones (at the front


19

of the reef facing the open ocean) and lower in low energy zones (at the back of the reef near

the lagoon). This work suggests that the high energy zones could be acting as organic source

zones, while the low energy zones are acting as organic sink zones, such that the system as a

whole is in balance by the transport of material from high energy to low energy zones (Kinsey

1979).

Kinsey’s (1979 and 1983) suggestions are similar to findings by other researchers. It has been

estimated that for many reef flats, where the water column is usually less than a meter deep,

waters flowing over downstream areas may be significantly depleted in nutrients due to

uptake of nutrients upstream (Froelich 1983). It has also been suggested that in the front reef

areas, high rates of vertical mixing due to turbulence over the front ridge may prevent nutrient

depletion from becoming a problem, however at low concentrations and with slow currents

(particularly observable at the back reef) it is unlikely that uptake of oceanic nutrients could

account for much more than net productivity (Froelich 1983). This reasoning has been based

on the assumption that there would be an observable decrease in dissolved inorganic nitrogen

and phosphorous concentrations downstream if oceanic nutrients were acting as the main

source of new growth, and this observation is lacking. This therefore suggests that there are

inputs of nutrients from within the front reef section, which could be advected towards the

back reef as inputs to that section.

It is also recognised that in areas of high hydrodynamic flux, at the front reef and algal ridge,

nutrients are exported from the system, which could potentially make them nutrient limited

(Rougerie et al. 1992), however these areas are exposed to continual inputs from the open

ocean and are recognised as containing efficient filtering organisms (Erez 1990), therefore

these areas could sustain themselves based on these oceanic inputs. The areas of low

hydrodynamic flux, over the reef flat and back reef, may retain nutrients for longer periods of

time, allowing them to be recycled and reused to sustain the productivity of these systems

(Rougerie et al. 1992). Therefore the hydrodynamics observed throughout the reef system

would allow a transfer of nutrients between sections as suggested before, showing how a reef

system can adjust itself such that each section performs a different function as part of the

whole system.

In studies comparing the limiting nature of nitrogen and phosphorous, it has been found that

nitrogen is the limiting nutrient in an open system (such as the ocean or well-flushed reefs)

because nitrogen is exported faster than phosphorous is depleted; conversely in closed

systems (such as lagoons), production is limited by the exogenous oceanographic delivery of


20

phosphorous, while nitrogen requirements are filled by endogenous and mainly benthic

nitrogen fixation (Notes 2001). This finding could be extended to the different sections of a

reef system, and suggests that the front reef could be nitrogen limited, exporting nitrogen to

the back reef and obtaining new inputs of nitrogen from the continual oceanic flow, while the

back reef obtains nitrogen from imports and fixation and recycles phosphorous tightly to

compensate for low levels of inputs.

It has therefore been shown by several researchers that the reef system as a whole is in

balance, where some reef sections are net sources and other sections are net sinks of nutrients.

Use of particulate matter

It has been suggested that the major source of nutrients to coral reefs is in particulate form,

which is taken up through two major mechanisms: the wave-resistant structure of the reef

acting as a huge filter with a large active surface area for the uptake of nutrients, and the

adaptations of corals that make them well suited for hunting zooplankton, as well as the many

other organisms on the reef that are active and passive filter feeders (Erez 1990). The

importance of the filtering effect of reef organisms has been highlighted elsewhere, where

filtering and sedimentary feeding animals (including sponges, polychaete worms, bivalves

and corals) and filtering zooplankton (such as copepods) scavenge dissolved and particulate

inorganic and organic matter, including bacteria, phytoplankton, suspended organic matter

and other zooplankton (Sorokin 1990).

Initially it was thought that the density of zooplankton in the waters over coral reefs was too

low to support the metabolism of animals in the reef (Odum and Odum 1955, Johannes 1970).

However it was subsequently found that a major source of zooplankton left the reef

substratum at night to feed in the surface waters, returning before dawn, and additionally

there were other zooplankton that stayed too close to the substratum to be collected by net,

but did not go into the substratum where they could be collected (Birkeland 1984). It has also

been observed that resident plankton are more productive in slow-current areas, for example

over the reef flat, than in fast-current areas, for example at the front of the reef (Birkeland

1984). Therefore the major source of zooplankton that the reef animals fed upon was found to

be derived from within the reef system, rather than advected onto the reef. Again this

highlights the importance of internal sources of particulate material for filter feeders.

Other sources of important particulate matter for filter feeders have been identified as coming

from bacterioplankton, algal populations, planktonic protozoa, suspended organic detritus,


21

which is detrital matter colonised by benthic microalgae and periphytonic filamentous algae,

and the aggregates formed by flocculated mucus colonised by bacteria (Sorokin 1990), which

could partly be formed within the reef system.

Johannes (1967) studied the formation of particulate organic aggregates occurring in oceanic

water that crossed the windward coral reef at Eniwetok Atoll, and found that aggregates of

coral mucus are an important food source for the zooplankton in the vicinity of coral reefs

(Johannes 1967). Odum (1971) noted that dissolved organic matter is important for forming

particulate matter aggregates, food sources for many coral reef inhabitants. It has also been

suggested that fish faecal material could be a significant source of organic aggregates in reef

waters, containing a large proportion of mucus and being an important nutritional source for

corals and other sessile invertebrates (Froelich 1983).

Therefore the production of particulate matter within the reef system and its subsequent

uptake via filtering could be a means of recycling nutrients between different parts of the

system, enabling more efficient overall use of nutrients.

Inputs from geothermal endo-upwelling

The process of geothermal endo-upwelling results from the conjunction of a geothermal heat

source and a porous and permeable structure (Rougerie et al. 1992). In this process, interstitial

water within a porous limestone atoll structure in contact with a volcanic basement is

progressively heated. Because of the build-up of heat, the interstitial water loses density and a

slow convective current is established in the permeable material, causing the ascent of

nutrient-rich deep ocean water to the top of an atoll (Rougerie et al. 1992). This water then

flows along the most permeable paths, usually through the algal reef crest at the front of the

reef (Rougerie et al. 1992). In their work on a reef flat at Tikehau Atoll in French Polynesia,

Rougerie et al. (1992) found that the nutrients present could not be accounted for by the

apparent oxygen utilisation, and therefore that there must be a source of new nutrients,

probably from the nutrient-rich Antarctic Intermediate Water entering the reef framework at

depths of 500 – 1000 m and circulating to the living reef by endo-upwelling. These findings

were confirmed by additional work on a barrier reef in Tahiti (Rougerie et al. 1992). This

work indicates that the reef system also gets inputs of nutrients from deep below its

structures.

However, this process is only valid in areas with an abnormally high geothermal flux, a

porous reef framework and a deep water source of dissolved nutrients, and therefore will not


22

be able to explain nutrient sources to all reefs (Rougerie et al. 1992). In addition, this theory

has been criticised on the grounds of: 1) a comparison of the phosphate flux delivered by

endo-upwelling with the flux delivered by horizontal flow of surface seawater indicates that

the total flux delivered by seawater is nearly 4 orders of magnitude greater than the endo-

upwelling flux; and 2) the observed increases in nutrient concentration of the interstitial water

of reefs can be explained by the oxidation of organic matter, and does not need to be

explained by endo-upwelling (Tribble et al. 1994). Therefore endo-upwelling appears to be

important only for the long-term diagenesis of older carbonates within the reef structure

(Tribble et al. 1994), but could still be considered a nutrient source in these cases.

Inputs from reef cave water and sediments

Coral reefs contain many caves and tunnels, thought to account for 50 to 75% of the reef’s

volume (Froelich 1983). These caves contain varying amounts of sediments, holding organic

material that is metabolised by microorganisms and therefore regenerating nutrients (Froelich

1983). The high porosity (20-35%) and high permeability of reef structures mean they can

contain a large and dynamic reservoir of interstitial water for bacterial degradation and

remineralisation of inorganic and organic material (Rougerie et al. 1992). The export of water

from these reef cavities has been measured and studies indicate that cave water contains 13

times the concentration of nitrate, 2 times the concentration of ammonium and 3 times the

concentration of organic nitrogen than the surrounding oceanic waters (Froelich 1983).

Additionally, it was shown that outwelled water from these caves resided in the bottom waters

for 10 to 15 minutes or longer before being advected upwards and mixed through the water

column, providing an opportunity for benthic organisms to take up these nutrients before they

are advected away (Froelich 1983). Therefore the mechanism of nutrient storage within reef

caves allows for nutrients to be reused by the reef community.

Other work that has been conducted on the inputs from benthic sources has determined that

benthic fluxes of nutrients are largely responsible for the nutrient dynamics of the near shore

coastal ecosystems, especially where direct terrestrial inputs do not contribute significantly to

the nutrient budget (Mwashote and Jumba 2002).

Therefore, although they are not frequently the subject of much study, it appears that

sediments within coral reefs could play an important role with regard to nutrient sources for

the reef.


23

Inputs from nitrogen fixation

Work conducted by Webb et al on a section of Eniwetok Atoll close to where Odum and

Odum (1955) conducted their research found a net export of combined nitrogen from the

system of between 0.03 and 0.35 gN/m2/day (depending on the time of day) (Webb et al.

1975). The authors suggested that it was unlikely the net export of combined nitrogen is

indicative of decreasing community biomass, but instead that there must be an input of

nitrogen into the system that was unaccounted for. It was recognised by the authors that

upwelling of deep ocean water could provide this nitrogen input, but that was thought to be

associated with an increase in phosphorous, and no net export of phosphorous was observed

from the system (Webb et al. 1975). This led the authors to conclude that the missing nitrogen

was fixed by benthic mats of blue-green algae, which were found in appropriate quantities at

the reef site (Wiebe et al. 1975).

Other organisms that have been reported to fix atmospheric nitrogen are symbiotic blue-green

algae, living in coral skeletons, and sponges (Yamamuro et al. 1995).

In their companion work on nitrogen fixation, Wiebe et al (1975) summarised the three routes

by which nitrogen fixed by the algae on their study site could enter the reef community:

through grazing by fish and other predators, which in turn re-enters the water column through

faeces, by being broken off by strong turbulence and washed downstream, and through the

release of dissolved nutrients into the water column by the fixing algae themselves (Wiebe et

al. 1975). Thus should nitrogen fixation by these algae prove to be a significant input, it is

likely that they contribute nitrogen to the reef system as a whole.

However it has been observed that phosphorous can be stored in parts of coral reefs, for use at

a later time, therefore not necessitating an export of phosphorous should input levels increase

(Odum and Odum 1955, see also following discussion on phosphate flux). The study by

Webb et al (1975) also did not look at the viability of nanoplankton, bacteria and other

microscopic organisms as sources of nitrogen from ocean waters, having only sampled net

(macroscopic) plankton.

This work on nitrogen fixation, though not providing a convincing argument for the role of

nitrogen fixation in providing all necessary inputs of nitrogen to the system, indicates that

inputs of nitrogen from blue-green algae could be a significant contributor of nutrients to the

coral reef system.


24

Efficient use of phosphorous

Measurements made to quantify the flux of phosphorous over a section of Eniwetok Atoll

showed that there was little to no difference in phosphorous uptake and release over the

length of two transects, including little variation between night and day (Pilson and Betzer

1973). This could be expected over corals containing zooxanthellae, which can uptake and

retain phosphorous for later use, however the majority of the transects sampled contained

algal reefs, leading the authors to conclude that either the benthic algae must absorb and

excrete phosphorous in some form, in a way that does not vary between night and day, or the

uptake of phosphorous by plants during the day must be matched by a similar release by

animals (Pilson and Betzer 1973).

This work suggests that the coral reef community as a whole exists in a steady state with

respect to phosphorous, adjusted to recycle between components of the system as well as

within components such as corals. This work provides further evidence that the levels of

recycling within a coral reef community are complex, and exist on several levels: between

individuals of a symbiotic relationship, between communities of the coral reef system and

between the system and the oceanic water flowing over the reef.

Atkinson (1981) conducted important work on Kaneohe Bay in Hawaii regarding phosphate

metabolism of the reef system. It was found that phosphate uptake rate as a percentage of the

community respiration rate is proportional to the ambient reactive phosphate concentration,

suggesting that at low concentrations of phosphorous the respiration rate could be due to a

proportional increase in the uptake of other nutrients, and conversely at higher concentrations

of phosphorous greater energy throughout the community is directed towards uptake of

phosphate (Atkinson 1981and Atkinson 1987). This could suggest that reef systems act based

on the available concentration of phosphate at any given time, taking up the nutrient at a

greater rate when it is in plentiful supply, to be stored for future use or used to fuel sporadic

growth. This is suggested as particularly important for algae that can retain or fix sufficient

amounts of nitrogen for themselves (Atkinson 1987).

3.1.2 INPUTS FROM OPEN OCEAN WATER

Several studies have found that although coral reefs do not require a large input of nutrients

from the open ocean, they require a continual input from this source to sustain a steady state

and slow accumulation of biomass (through low rates of net productivity). This idea is

expanded upon in this section.


25

From the few studies that have been conducted on the metabolism of an entire coral reef

system, it has been found that excess production (primary production through photosynthesis

minus respiration) is very close to zero, and turnover rates (ratio of production to respiration)

are equal to 1 for these ecosystems (Kinsey 1983), indicating the reef system mostly

consumes what it produces and therefore only needs a little of extra inputs from oceanic

sources to sustain a steady state.

Additionally, although completely efficient nutrient recycling within the reef (evidenced by a

turnover rate of 1) can sustain a steady state, it cannot sustain net growth; furthermore should

recycling not be 100% efficient (as is presumably the case in real ecosystems), a net input of

new nutrients (inorganic forms of nutrients, i.e. not recycled forms as predominate within the

reef system) will be required to sustain a steady state (Froelich 1983). Therefore a coral reef

system will continually require an input of new nutrients, despite maintaining a turnover rate

of 1 and having reasonably efficient internal recycling mechanisms, because no recycling can

be completely efficient.

New nutrients can come from both terrestrial and oceanic sources, and also in the form of

nitrogen-fixation in the case of nitrogen (as discussed previously). The majority of coral reefs

are not located near terrestrial inputs, most likely due to adverse effects from sedimentation

and low salinity levels, therefore the majority of new nutrients will come from oceanic

sources. Oceanic sources of nutrients will be dependent on the concentration of nutrients in

the source water, the rate of flow over the reef, and the ability of primary producers to take up

the nutrients at the given concentration (Froelich 1983). Nutrient concentrations in tropical

waters are usually low, but can be supplemented by continental shelf upwelling (Andrews and

Gentien 1982). The rates of water flow over reefs are generally high, and several species of

reef coral have been found to be able to take up nutrients from the low concentrations (D’Elia

1977). Therefore this suggests that oceanic sources of nutrients have the potential to provide

the required nutrients to coral reefs. Various studies have investigated the provision of

specific nutrients, as discussed below.

It has been found that zooplankton play a very minor role in providing nutritional energy to

corals containing zooxanthellae, however they may play a very significant role in providing

nutrients and sources of trace elements (Johannes et al. 1970). The work of Johannes et al.

(1970) suggests that although corals containing zooxanthellae can provide the majority of

their own energy requirements through photosynthesis, they require nutrition in the form of


26

steady inputs of zooplankton from oceanic water to fulfil the need for specific vitamins and

nutrients.

Atkinson found that the advection of phosphate over a typical reef is large compared to the

phosphate uptake of the reef (Atkinson 1987). It was suggested that this large advection can

support a large benthic biomass, but the low concentration of nutrients probably affects the

specific growth rate of the reef producers. In other words, gross primary production of the reef

can be maintained by recycled phosphate, while net community production is maintained by

the advection and uptake of phosphate over the reef (Atkinson 1981 and 1987). This finding

has been supported by more recent work on Tikehau Atoll (in French Polynesia), which also

found that the horizontal phosphorous flux from surface oceanic water is three orders of

magnitude higher than the estimated outer reef new production, and three times higher than

the lagoon new production (Charpy 2001). Thus it is shown that oceanic inputs of

phosphorous are adequate for maintaining net production.

An important assertion from Pomeroy’s work (1970) was that plankton could virtually

maintain their standing stock on regenerated forms of nitrogen (ammonia, which has been

eaten and then excreted and recycled), using new nitrogen (nitrate brought in by advected

water from the open ocean) for population growth. Therefore nitrogen could be considered a

limiting nutrient for coral reef systems, but it is only limiting in the sense of building greater

populations, not of maintaining the current equilibrium (Pomeroy 1970). Thus as for

phosphorous, continual inputs of nitrogen from oceanic waters appear to be adequate for net

production.

The work of Kinsey (1979 and 1983), when considered with the findings of Odum and Odum

(1955), Pomeroy (1970), Pilson and Betzer (1973) and Atkinson (1981), suggests that coral

reefs do not require inputs of large concentrations of nutrients to maintain their current

biomass; inputs of large concentrations go towards building the biomass of the reef, which

occurs over a long time period. Instead the reefs require a continual input of new nutrients in

low concentrations, which goes towards maintaining their low rates of net productivity and

compensating for net exports of material from the system (Froelich 1983). This need is met

by inputs from the ocean.

Role of upwelling – special input to ocean water

The role of upwelling in providing nutrients to the Great Barrier Reef (located off the eastern

shores of Australia) has been investigated by Andrews and Gentien (1982). Their study found


27

that upwelling intrusions over the continental shelf of the continent tended to be confined to

near the bottom, and phytoplankton development quickly took place inshore of the shelf

break. Surface flows carried silicate-rich lagoon waters offshore and nitrogen-rich shelf break

water onshore. Upwelling intrusions penetrated across the entire zone of the reef, with

nutrients delivered out of the shelf thermocline to the living coral of reefs by localised

upwelling induced by the tides and waves (Andrews and Gentien 1982). The estimated

onshore annual nitrogen input from upwelling was 20 _g/L, a significant amount for tropical

waters, indicating that upwelling was a major source of nutrients for the reef (Andrews and

Gentien 1982). This work is a major contributor to the discussion of oceanic sources of

nutrients to coral reefs, and suggests that offshore processes could be very significant in

supplying coral reefs with their required nutrients.

However, it has also been noted that nutrient-rich upwelling should also produce a bloom of

both planktonic and benthic algae, which would decrease the light available to zooxanthellae,

and increase the amount of algal macrophytes, which outcompete the slower growing coral

structures (Rougerie et al. 1992) and thus upwelling would hinder coral growth. Therefore

further work is required into the precise role of upwelling and any associated plankton

increases.

3.1.3 SUMMARY OF NUTRIENT SOURCES

It therefore appears that the coral reef paradox has been solved, with two major conclusions to

be made from the research conducted into nutrient sources to coral reefs.

Firstly, coral reef systems are organised and adjusted to use, store and recycle whatever inputs

they receive from the surrounding waters (Odum 1971). They appear to recycle nutrients

relatively efficiently, particularly between the symbionts of corals and zooxanthellae. The reef

system appears to be especially proficient at using and storing phosphorous efficiently.

However, while recycling occurs at various levels within a reef system (at cellular level in

symbiotic associations, between primary producers and their consumers and at the community

level between different zones of a reef system), it has been noted that no recycling scheme is

100% efficient, and water advection may carry away nutrients before they are able to be

assimilated (Erez 1990).

Secondly, while recycling and other mechanisms such as nitrogen fixation are important for

the efficient utilisation of nutrients that have been acquired by the reef, coral reef systems

ultimately require a continual input of nutrients from oceanic waters, for both nitrogen and


28

phosphorous sources and in dissolved and particulate form. This is necessary to sustain the

reef’s net productivity and turnover rate, and the reef system acts as an efficient filter of

oceanic water.

As an aside, it is possible that the cycle of nitrogen through a coral reef system is different to

the cycle of phosphorous, indicated by the differing levels of export from the reef of these

nutrients and comparative levels of storage and recycling.

3.2 MOTIVATION FOR STUDY

The previous section highlights the need to understand local ocean dynamics for the

understanding and management of coral reefs, due to these systems’ dependence on oceanic

inputs of nutrients. However, while there has been work on the importance of oceanic

upwelling for supplying nutrients to coral reefs (Andrews and Gentien 1982), there has not

yet been work attempting to quantify the oceanic inputs of nutrients to coral reef systems.

Also, aside from the work on upwelling, there has been little investigation into the role of

local oceanography on the development of coral reefs, a failing that has been identified

previously by others (e.g. Crossland 1983).

Therefore this study has been motivated by this lack of knowledge about the link between

local oceanography and a coral reef’s nutrient sources. The objectives of this study were

twofold: firstly, to investigate the oceanographic environment around a coral reef system, and

secondly to attempt to understand the isotopic composition of key organisms within the reef,

with a view to contributing to analysis of the reef’s nutrient sources. This investigation would

be especially important when considering the management requirements of the reef. To

investigate these questions, a study was conducted on Ningaloo Reef, located offshore of

northwest Australia.

3.3 NINGALOO REEF

Ningaloo Reef runs parallel to the western-most promontory of Western Australia and is

managed by the Western Australian Department of Conservation and Land Management as

part of the Ningaloo Reef Marine Park. It is the largest fringing coral reef in Australia and is

important for tourist and fishing opportunities, leading to the necessity for preservation and

appropriate management strategies (D'Adamo and Simpson 2001).

The reef extends for approximately 260 km, from North West Cape (located at 21o 47’ S) to

south of Amherst Point (located at 32o 34’ S), and lies approximately along longitude 113o


29

30’ E (Hearn et al. 1986 and Storrie and Morrison 1998). The location of the reef within the

Marine Park is shown in Figure 3.

It is a part barrier and part fringing reef system, with reefs ranging from 7 km to less than 200

m offshore (Storrie and Morrison 1998) and reef sections broken every few kilometres by

passes with water depth averaging 6 – 8 m (Ayling and Ayling 1987). The width of the

Ningaloo Reef lagoon ranges from 0.5 to 6 km, with an average width of about 2.5 km and a

mean depth of about 2 m at Australian Height Datum (AHD, Australian measurement for sea

level) (Storrie and Morrison 1998).

Ningaloo Reef is located in the arid region of Western Australia, and the land side of the reef

consists primarily of desert with mean annual rainfall of 270 mm (Hearn and Parker 1988),

influenced by periodic cyclones (Hearn et al. 1986). The northern part of the reef is adjunct to

the Cape Range National Park, which is a large tract of protected arid land, such that there are

few terrestrial impacts from this area on the reef (Hearn et al. 1986). The lagoon is floored

with white calcareous sand, indicating little terrigenous sediment input (Ayling and Ayling

1987). To the south of the reef, developments around Coral Bay have been shown to have

impacts on the reef due to groundwater leaching (Survey of water quality, groundwater,

sediments and benthic habitats at Coral Bay 1995). There are also large numbers of tourists to

the reef each year, with recreational uses of the reef such as snorkelling and fishing (Ayling

and Ayling 1987).

The continental shelf off Western Australia (defined as the region between the coast and the

200 m contour) is very narrow between North West Cape and Point Cloates (see Figure 3),

only about 10 km wide, which brings the shelf-break area closer to the coast than at any other

location in Australia (Hearn et al. 1986).


30

Figure 3: Location of Ningaloo Reef Marine Park (Storrie and Morrison 1998)

3.3.1 PREVIOUS STUDIES ON NINGALOO REEF

The majority of the previous work on Ningaloo Reef has investigated various aspects of the

local physical environment and physical forcing characteristics of the reef. Water flow

through the reef system has been identified as controlled by wind, tidal and wave forcing,

discussed further below (Hearn and Parker 1988).

Wind characteristics

It has been identified that alongshore winds will be dominant (over cross-shore winds) along

the entire length of coast in which Ningaloo Reef is situated (Hearn et al. 1986). This could


31

influence the mixing of the water column around the reef and also the transport of nutrients to

and from the reef.

Wind stress occurs predominately from the south but with easterly and westerly components

during certain seasons (Hearn et al. 1986). The circulation patterns created by the winds at the

reef are influenced by the topography of the reef and lagoon (Hearn et al. 1986). Flow (in the

depth-mean currents) driven by a southerly wind is suggested to consist primarily of an anti-

clockwise gyre with water moving northward into the lagoon and returning southward beyond

the reef (Hearn et al. 1986). This is illustrated in Figure 4. Therefore wind stress is suggested

to be dominant in the lagoon and the resultant pressure gradient will drive the flow in the

open ocean (Hearn et al. 1986). In the surface waters the current is with the wind in both

cases.

Figure 4: Wind circulation patterns around Ningaloo Reef (Hearn et al. 1986)

In addition to the main gyre there is flow through the reef line, theoretically either through the

channels between reef sections or over the reef crest, the relative magnitudes of which could

vary with tidal processes (Hearn et al. 1986). Figure 4 shows the suggested case of flow

entering the lagoon through the reef channels (Hearn et al. 1986). However it is still uncertain

what route the water takes after being expelled through the channels between reef sections

(Hearn et al. 1986).


32

In addition, the southwesterly winds that are so strong along the majority of the west coast of

Australia are likely to be weaker in the northern part of the reef, between North West Cape

and Point Cloates, due to sheltering effects from the Cape Range (Hearn et al. 1986). South of

Point Cloates the southwesterly wind is likely to not be as affected by the land mass, and

therefore a considerable change in wind strength will be observed over a distance of order

100km, which could have important effects on large scale circulation on the continental shelf


It is estimated that wind flushing can move water through the lagoon in a little over a day,

such that wind flushing is significantly quicker than tidal flushing (Hearn et al. 1986).

Tidal characteristics

Tidal data collected at Point Murat and Carnarvon (locations at the north and south ends of

Ningaloo Reef respectively) indicate the local tides are mixed, predominately semi-diurnal,

consisting of two high and two low waters each day but with large inequalities in range and

time (Hearn et al. 1986). The maximum tidal range during spring tides at Ningaloo has been

recorded as approximately 2 m (Hearn et al. 1986).

Tidal currents have been identified as influencing the reef lagoon in two ways: firstly creating

an alongshore tidal wave through the lagoon, and secondly creating cross-reef processes

acting to exchange water between the lagoon and open ocean, with an alongshore wave

propagating in the deep water beyond the reef (Hearn et al. 1986). The second effect is

expected to occur where the lagoon is closed at its ends by headlands, for example at the

section of Ningaloo Reef located between Norwegian Bay and Point Cloates (Hearn et al.

1986). At low tide, water enters the lagoon through the breaks or channels between reef

sections, because the reef crest is dry (Hearn et al. 1986). The tidal range inside the lagoon

may be smaller than in the open ocean because of the elevation difference necessary to drive

water through the reef (Hearn et al. 1986). At higher values of water level tidal currents can

pass over the reef crest as well as through the breaks in the reef, in which case the flow is

strongly influenced by inertial forces (Hearn et al. 1986).


33

The incoming tidal waters can form a frontal region with the water already in the lagoon,

whereby the residual lagoon water increases in depth and narrows in horizontal spread, and

the interface between the two waters moves onshore on the flood tide and offshore on the ebb

tide (Hearn et al. 1986). The time taken for tidal waters to move through the lagoon depends

on the volume of incoming water (due to tidal differences), the volume of water residual in

the lagoon, the tidal period and the amount of mixing between the residual water and the tidal

water (Hearn et al. 1986). Tidal exchange processes have been estimated to flush the lagoon

at Ningaloo Reef in about 2 – 5 days (Hearn et al. 1986).

Wave characteristics

Wave-pumped currents have a major influence on the dynamics of the lagoon. The current

trajectories have been observed to cross the straight reef-line perpendicularly, being deflected

into an alongshore direction at distances of a few hundred metres from the shore (Hearn et al.

1986). Over 50% of this alongshore flow occurs in deep channels within the lagoon, which

run alongshore and then turn offshore to allow water to exit the lagoon through channels

between reef sections (Hearn et al. 1986).

The amount of water that exits the lagoon through these channels and the speed at which it

does so depends on the dimensions of the channel (Hearn et al. 1986). It was estimated that

the flushing time of the lagoons at Ningaloo Reef are less than one day based on wave

pumping (Hearn et al. 1986). This time is relatively short compared to many coral reef

systems, which is likely a result of the shallow nature of the lagoon and its limited width


Lagoon vertical mixing

It is anticipated that the lagoon would always be well mixed, because vertical mixing times

have been estimated as on the order of less than 1 hour (Hearn et al. 1986). The

hydrodynamic effects of temperature and salinity (and therefore density) gradients within the

lagoon and between the lagoon and adjacent ocean are yet to be studied; however it is

suggested that there may be significant lagoonal and cross-shelf stratification in these

parameters in the area (D'Adamo and Simpson 2001). D’Adamo and Simpson (2001) suggest

that density gradients may have an influence on vertical mixing within the lagoon and

exchange of water between the lagoon and ocean, for example by layered exchange through

the channel passes; if lagoon water is significantly more dense than the adjacent ocean water,


34

water could flow out from the lagoon as a submerged current, with less dense ocean water

flowing into the lagoon on the surface.

Effect of local internal waves

Internal waves are gravitational oscillations of the thermocline (region of water indicating a

change in temperature between lighter surface and denser bottom waters), although any

variation of density through the water column will support internal waves (Hearn et al. 1986).

Internal waves lead to maximum vertical displacements in the interior of the water column,

with maximum horizontal velocities near the surface and bottom (Hearn et al. 1986). These

waves have been identified on the North West Shelf, located to the northwest of Ningaloo

Reef, producing vertical displacements of up to 300m in water of depth less than 100m, and

with wavelengths from 300m to 1000m (Holloway 1983 and Baines 1981, in Hearn et al.

1986). It has been found that the amplitude of the internal waves is a maximum in the period

November to April, and that internal waves on the North West Shelf have very large

amplitude in relation to the water depth (Hearn et al. 1986). It has been suggested that such

large amplitudes are sufficient to break the surface and release colder bottom water from

offshore into the Ningaloo Reef tract and lagoon (Hearn et al. 1986).

Temperatures of the lagoon

Seawater temperatures in the Ningaloo Reef lagoon have been found to be highly variable in

time and space, due to the variable amounts of flushing within the lagoon (Simpson and

Masini 1986). On average, lagoon waters have shown a minimum of approximately 17.8 oC in

August and a maximum of 29.8 oC in December (D'Adamo and Simpson 2001). In

comparison to the Dampier Archipelago (further north than the Ningaloo Reef), lagoon

seawater temperatures during autumn and winter were higher (by about 2 oC), which may be

due to the influence of the Leeuwin Current (Simpson and Masini 1986).

During fieldwork undertaken on the reef in May 1985, the data on short-term fluctuations (on

the order of days) indicated that an unusually cool water mass was advected into the lagoon

from the open ocean and mixed with the lagoon waters at certain times (Simpson and Masini

1986). The advection of oceanic water into the lagoon was found to be greater during neap

tides, thought to be because that is when the outer reef is continuously covered by water

(Simpson and Masini 1986). It has been suggested that the advected water originates in

localised upwelling, caused by the arrival of an internal wave of suitable amplitude; the

internal waves in this region have been measured as having appropriate time periods to have


35

caused such observations (Hearn et al. 1986). The temperature anomaly was determined to be

relatively short-lived (approximately 12 hours), and therefore unlikely to be caused by

changes in ocean water due to weather patterns, upwelling caused by local currents or tidal

circulations (which would be recurrent) (Hearn et al. 1986).

Reef-front current

Surface and aerial observations taken of the reef-front current (the current located

immediately to the seaward side of the reef) indicate a northward flow during March and

early April, turning southward during mid-April (Taylor and Pearce 1999). The northward

current can be attributed to a regime of the Leeuwin Current flowing southwards offshore,

with a strong Ningaloo Current flowing northwards inside the Leeuwin due to southerly

winds (Taylor and Pearce 1999). These observations are consistent with the known attributes

of these currents (see Section 3.3.2 for further discussion of these currents).

Nutrient characteristics

Crossland (1983) summarised the findings on dissolved nutrient concentrations in both

tropical and temperate waters. Nitrate levels (representing dissolved inorganic nitrogen) in

tropical waters have been measured as 0.1 – 0.3 _g/L, while phosphate (dissolved inorganic

phosphorous) has been measured as less than 0.3 _g/L. These same parameters have been

measured for temperate waters in concentrations of 2.0 – 5.0 _g/L and 0.5 – 2.0 _g/L

respectively (Crossland 1983). There has been little research undertaken to date to quantify

the nutrient characteristics in the region of Ningaloo Reef. However, data collected in sea

waters near the Houtman Abrolhos Group reef off the coast of Western Australia (further

south than Ninagloo Reef) has shown standing stock dissolved inorganic nitrate levels of 0.79

– 5.17 _mol/L and phosphate levels of 0.16 – 2.92 _mol/L, comparable to temperate waters

(Crossland 1983) but with a wider range of values.

3.3.2 PHYSICAL CHARACTERISTICS OF WESTERN AUSTRALIAN COASTLINE

The interactions between currents along the western coast of Australia have important

implications for the productivity of the region and for Ningaloo Reef.


36

Eastern Boundary Currents

In the Southern Hemisphere, the oceanic gyres rotate in an anti-clockwise direction, causing a

surface southward current off the east coasts and surface northward current off the west coasts

of continents (Wooster and Reid 1963). The equator-bound currents found at the eastern side

of the oceans, off the west coasts, are termed Eastern Boundary Currents (EBC).

Due to the effect of the Coriolis force, these surface currents are pushed offshore (a process

termed Ekman transport), generating large-scale upwelling of cooler, nutrient-rich water from

deep waters onto the continental shelves. This leads to increased productivity off the west

coasts of North and South America and northern and southern Africa. High productivity has

been observed via satellite images, has been correlated with field work, and been well studied

in the Southern Hemisphere off the west coast of Peru-Chile (the Humboldt Current) and

southern Africa (the Benguela Current) (for example, see Pearce 1991).

However, increased productivity has not been noted off the coast of Western Australia in

large amounts. It has been noted that the sea surface temperature isotherms off the coast of

W.A. are deflected towards the coast and southwards throughout the year, instead of

northwards as would be expected, therefore showing the suppression of the EBC in this

region (Pearce 1991). Thus the west coast of Australia represents an anomaly with regard to

the EBC, and studies of the productivity within the coastal region have not been conclusive.

Upwelling has however been found on the northwest coast during the summer months,

causing localised areas of high primary productivity (Holloway et al. 1985, in Hearn et al.

1986).

Leeuwin Current system

The open passage along the islands of Indonesia that connects the Pacific with the Indian

Ocean allows a flow through of water into the Indian Ocean, called the South Equatorial

Current, which breaks into two when it reaches the northwest part of W.A., with a part

turning south to flow down the coast (Pearce 1991). This part is called the Leeuwin Current

and, despite interannual variability, the net movement of water is southwards down the west

coast against the prevailing equatorward (and upwelling-favourable) winds (Pearce 1991).

The Current is strongest during the autumn and winter months, when the southerly winds are

weakest, and weakest during the summer months, when upwelling-favourable winds are

strongest (Smith et al. 1991). The passage of the Leeuwin Current in the vicinity of Ningaloo


37

Reef is shown in Figure 5, with the local counter currents also shown for comparison (to be

discussed below).

Figure 5: Passage of Leeuwin Current down west coast of Australia, with other local currents also shown(Woo and Pattiaratchi 2003)

The Leeuwin Current brings warm, low salinity waters from the tropics as it flows on the

surface down the west coast, from the North West Cape in the north to the Great Australian

Bight in the south. However its temperature and salinity signature appears to change as it

flows down the coast, from 24.85 oC and 34.94 psu near Exmouth, to 21.21 oC and 35.44 psu

south of Shark Bay (during November) (Woo and Pattiaratchi 2003). It contains a thick

surface mixed layer of approximately 50 m (Thompson 1984) and is fairly deep, about 250 m

within 100 km of the continental shelf edge (Smith et al. 1991). The Current has been

identified to flow strongly near North West Cape, where the continental shelf is relatively

narrow, then slows down off the region near Shark Bay where the shelf widens, before

speeding up again further south as the shelf narrows once more (Woo and Pattiaratchi 2003).

The Leeuwin Current has traditionally been believed to be the cause of low productivity in the

waters off the west coast, because the westward wind-driven surface flow that would generate

upwelling (caused by the EBC) is offset by the eastward flow in the surface waters due to the

Leeuwin Current, generating downwelling instead (Pearce and Pattiaratchi 1999). However,

the presence of the Leeuwin Current keeps water conditions suitable for coral growth (with


38

appropriate temperatures and prohibiting non-reef building macrophyte communities), hence

allowing the existence of Ningaloo Reef (Pearce and Walker 1991, from Woo 2003, and

Hatcher 1991).

Ningaloo Current

There are also counter currents found along the coast of W.A., which flow northwards along

the inside of the Leeuwin Current. The Capes Current flows between Cape Leeuwin in the

south and Geraldton in the north. The Ningaloo Current flows in the region off the North

West Cape, along Ningaloo Reef. These counter currents are seasonally variable, and are

most dominant in the summer months when the southerly winds are strongest (Woo and

Pattiaratchi 2003). The Ningaloo Current has been shown as strongest between September

and mid-April (Taylor and Pearce 1999).

The Ningaloo Current is believed to be produced by old Leeuwin Current water, due to its

salinity and temperature signature, and it carries cold, high salinity, highly oxygenated,

nutrient-rich water (Thompson 1984). Thompson (1984) and Smith et al. (1991) confirm the

presence of a poleward surface current (the Leeuwin) and equatorward undercurrent (the

Ningaloo) at sample sites off the North West Cape, with Smith et al. (1991) finding the

undercurrent between approximately 250 and 450 m deep. This confirms the presence of the

Ningaloo Current as deep, old Leeuwin Current water. Measurements taken of the Current

have shown it to contain water with temperature 22.95 oC and salinity 34.94 psu during

November (Woo and Pattiaratchi 2003). The Ningaloo Current is depicted more clearly in

Figure 6.

While flowing predominately northwards inside the Leeuwin Current, the Ningaloo Current

has shown variability due to local bathymetry changes. As the Ningaloo Current flows

northwards and arrives at the promontory of Point Cloates, data has shown the current turned

westwards with the curve of the promontory and flowed out across the shelf break (Woo and

Pattiaratchi 2003). This deviation resulted in cool, high salinity Ningaloo Current water (with

mean temperature 22.71 oC and salinity 35.00 psu) being observed across the length of the

shelf break at this location (Woo and Pattiaratchi 2003). Once the Ningaloo Current reached

the seaward edge of the promontory, part of it turned to continue flowing northwards, and part

rejoined the Leeuwin Current to flow southwards (Woo and Pattiaratchi 2003). This

circulation could affect local productivity patterns. It has been suggested that coastal material

swept away by the Leeuwin Current could be recirculated and return up the coast in the


39

Ningaloo Current, thereby affecting the retention and recycling of nutrients in the Ningaloo

ecosystem (Woo and Pattiaratchi 2003).

Figure 6: Ningaloo Current off northwest Australia (Hanson 2003)

The effects of the Ningaloo Current’s interactions with the Leeuwin Current have not been

well described to date, specifically the impact on phytoplankton of these interactions and any

recirculation patterns (Woo and Pattiaratchi 2003). It is known, however, that the Ningaloo

Current creates a circulatory movement, which retains planktonic biomass and nutrients

within the Ningaloo Reef system, enhancing productivity (Taylor and Pearce 1999). Localised

upwelling behaviour along the coast has also been indicated by upward-sloping isohalines and

isotherms beneath the Ningaloo Current (Woo and Pattiaratchi 2003).

Other characteristics

In addition, satellite imagery has revealed an anti-cyclonic circulation pattern located

immediately south of Point Cloates (Woo and Pattiaratchi 2003). This region has been

speculated as containing some degree of cross-shelf exchange or recirculation of Leeuwin

Current water (Taylor and Pearce 1999 and Woo and Pattiaratchi 2003). The proposed

recirculation pattern would bring Leeuwin Current water that has been advected past the reef

back around in the Ningaloo Current, such that the same water was recirculated past the reef,


40

as shown in Figure 7. This recirculation pattern has not yet been investigated with respect to

its destination or nutrient levels.

Figure 7: Recirculation pattern south of Point Cloates, as proposed by Taylor and Pearce (1999)

Offshore eddies have also been observed in the deep waters off Shark Bay, causing the

Leeuwin Current to deviate seaward or coastward from its path, and introducing cooler, more

saline surface waters with average measurements of 20.94 oC and 35.44 psu from an offshore

source closer towards the shore (Woo and Pattiaratchi 2003).

3.4 MEASURING NUTRIENT FLUXES AND SOURCES

3.4.1 METHODS USED TO MEASURE NUTRIENT FLUXES AND SOURCES

There has been much research conducted into measuring nutrients and hydrodynamics in the

open ocean since the early 1900s, and as such the procedures for collection of samples for

analysis and of physical data are wide ranging and have evolved over time. The use of a CTD

probe (Current, Temperature and Density probe, a device for recording various parameters of

the water column including depth, salinity, temperature, dissolved oxygen concentration,

photosynthetically active radiation and fluorescence) is widely accepted for the measurement

of physical parameters in the marine environment. Measurements of nitrogen and

phosphorous, in both dissolved and particulate forms, as well as particulate carbon are widely

used in productivity studies of the marine environment. Therefore the parameters of ocean


41

water chosen for analysis in this study are standard among the literature and studies relating to

their applicability for various purposes are not presented here.

The Joint Global Ocean Flux Study (JGOFS) is an international and multi-disciplinary study

aiming to better understand the role of the ocean in the global carbon and nutrient cycles

(JGOFS 1994). As part of the study, there has been an attempt to standardise procedures for

sample collection and analysis of parameters, outlined in a protocol reference manual. This

manual is generally used as a reference manual for methodology and is widely accepted.

Procedures outlined in the manual cover shipboard sampling, the use of a CTD (including

calibration and processing of data), sediment and surface-tethered trap methods,

determination of salinity, dissolved oxygen, total inorganic carbon, nitrite, nitrate,

phosphorous, reactive silicate, algal chlorophylls, phaeopigments and carotenoids, particulate

organic carbon and particulate nitrogen, dissolved organic carbon, new production by 15N,

bacterioplankton abundance, primary production by 14C, bacterial production,

microzooplankton biomass and microzooplankton herbivory. Therefore this manual covers all

the tests undertaken in this study and has been used as a reference document for water

sampling methods and laboratory analysis.

In addition, the Commonwealth Scientific and Industrial Research Organisation of Australia

(CSIRO) has a set of manuals for standardised procedures of marine research, and the

hydrochemistry manual has been used widely for laboratory analysis of marine parameters.

This study has not attempted to refine the methods used by marine researchers, but has

followed the accepted procedures as outlined by these two groups.

Water samples were taken in this study for analysis of dissolved inorganic nitrogen in the

form of nitrate and nitrite (NO3- and NO2

-), dissolved inorganic phosphorous in the form of

phosphate (PO43-), chlorophyll a concentration and stable isotope values of δ13C and δ15N of

filterable particulate material. Reef specimens were also taken for analysis of δ13C and δ15N.

A brief justification for the use of these parameters in this study is presented here.

Nitrate/nitrite and phosphate were chosen for analysis because the inorganic forms of

nutrients (the most reduced forms of naturally occurring nitrogen and phosphorous

compounds) are easier for primary producers to assimilate and use, and therefore

measurements of these compounds give some indication as to the potential for a water mass to


42

stimulate primary production. In addition, dissolved inorganic nitrogen has been recognised

as a quantitatively important source of new nitrogen for corals, especially shallow-water

hermatypic corals as present in a coral reef (Heikoop et al. 1998).

Ammonium (NH4+) is the most reduced form of naturally occurring nitrogen and therefore is

taken up by microorganisms such as bacteria, however it is recognised that for phytoplankton

cells, nitrate and nitrogen fixation are the most important parameters with respect to nitrogen

limitation of primary productivity, with ammonia being important for maintaining the cell in a

healthy state and when nitrate levels are too low (Dugdale and Goering 1967). In addition,

ammonia is considered a regenerated form of nitrogen, meaning that it is produced through

excretion by organisms, and therefore is more likely to be in abundance and the preferential

form of nitrogen in a closed recycling system, rather than in the open ocean (Notes 2001).

Ammonium analysis is also more prone to error through human contamination, as it is present

in abundance on human skin. Therefore analysis of ammonium concentrations was not used

in this study.

Because only photosynthesising organisms contain active chlorophyll a, analysis of the

concentration of this pigment is often used in measurements of primary productivity. This

measurement cannot be used as the sole indicator of primary production, and production rates

should be measured in conjunction with another parameter such as rates of oxygen

production, however the concentration of chlorophyll a gives a good indication of the

biomass of primary producers present.

The use of stable isotope analysis is discussed in Section 3.4.2.

3.4.2 USE OF STABLE ISOTOPE SIGNATURES

Carbon and nitrogen occur naturally in several isotopic forms. In addition to their common

forms, 12C and 14N, the stable isotopes 13C and 15N occur at low but significant levels in the

natural environment. 13C occurs at about 1% of the natural level of 12C (Aharon and Chappell

1983), and 15N occurs at about 0.37% of the natural level of 14N (Peterson and Fry 1987). The

ratios of 13C/12C and 15N/14N in natural compounds vary with the chemical pathway by which

the compounds were formed and the conditions under which the reaction occurred, hence

these ratios differ locally among specific pools in the environment (Peterson and Fry 1987).


43

Isotopic ratios indicating the variation in natural abundance are given as relative deviations

from the ratio present in a standard, expressed as parts per thousand (_ ‰) (Aharon and

Chappell 1983):

_ ‰ = 1000 x (ratio sample – ratio standard)/(ratio standard)

The ratio is of the concentration of the minor isotope divided by the concentration of the

major isotope. The standard 15N/14N ratio (_15N) is atmospheric nitrogen (present as N2 gas),

which by definition has a value of 0‰, while the standard 13C/12C ratio (_13C) is carbon

dioxide (CO2) gas, the PDB standard (Preston 1992).

Terms used

The term ‘depleted’ is used to describe the quantity of a minor isotope relative to another

quantity. ‘Depletion’ refers to a substance that contains relatively less of the minor isotope;

this is also referred to as ‘lighter’ in the minor isotope (Owens 1987).

The term ‘enriched’ refers to the opposite of depleted, and is used for a substance that

contains more of the minor isotope relative to another quantity; this is also called ‘heavy’

(Owens 1987).

The alteration of ratios by physical, chemical or biological processes is called isotopic

fractionation (Aharon and Chappell 1983) and is the basis of 13C and 15N source studies

(Peterson and Fry 1987). ‘Fractionation’ refers to the unequal partitioning of isotopes between

the substrate of a reaction and the products formed during the reaction. The ‘isotope effect’ is

the process that gives rise to fractionation, associated with the majority of all biological,

physical and chemical reactions involving isotopes (Owens 1987). Although an isotope effect

may occur, its manifestation – fractionation – may not be observable in all instances (Owens

1987).

Use of stable isotopes in ecological studies

Stable isotope ratios have been widely used in ecological studies to identify the sources of

nutrients contributing to mixtures of particulate organic matter and to examine food web

relationships (McClelland and Montoya 2002). For example, they have been used to identify

the fish source for Western Australian penguins (Lenanton et al. 2003).


44

In the marine environment, the abundance of nitrogen and its isotope ratio is controlled by the

balance of nitrogen input, including from biological fixation, river input and atmospheric

precipitation, and its output, including via denitrification and sedimentation (Minagawa and

Wada 1986). Further distribution of nitrogen isotopes is determined by biological processes

like assimilation, degradation and incorporation into the food chain (Minagawa and Wada

1986). These processes are usually accompanied by the specific isotope discrimination of

nitrogen, making it advantageous to investigate nitrogen isotope compositions in order to

determine the sources and utilisation of nitrogen in marine systems (Minagawa and Wada

1986).

One advantage of using stable isotopes is that they reflect a time-integrated measure of

assimilated nitrogen rather than an instantaneous value, therefore reflecting the average diet

of a consumer or average source of nitrogen for a primary producer (Yamamuro et al. 2003).

It has been identified that _15N measurements are most useful when used in combination with

another isotope, usually _13C, _18O or _34S (Handley and Raven 1992).

Fractionation of isotopes

The carbon stable isotope ratios (_13C) of consumers reflect those of their organic matter

sources with a slight enrichment of about 1 ‰ (Achituv et al. 1997). During the fixation of

inorganic carbon (in the form of CO2) by photosynthetic organisms, carbon isotopes are

fractionated and the organic matter is enriched with the lighter isotope of 12C (Achituv et al.

1997). During the next steps in the food chain, grazing, feeding and predation account for

only small isotope fractionations, therefore allowing the detection of carbon flow through

food chains (Achituv et al. 1997).

The nitrogen isotope ratio (_15N) within an organism reflects their diet with an enrichment of

about 3.4 ± 1.1 ‰ with each trophic level increase (Yamamuro et al. 1995). This fractionation

has been attributed to an excretion of isotopically light nitrogen (14N) (Heikoop et al. 1998).

Typical stable isotope ratios in the marine environment

The low values of _15N found in oligotrophic waters have usually been attributed to nitrogen

fixation by cyanobacteria and blue-green algae, as atmospheric nitrogen has a value of 0 ‰. It

has been measured that nitrogen-fixing organisms have an average _15N value of between


45

–1.7 and +2.0 ‰ (Minagawa and Wada 1986). However it has also been found that

zooplankton and other pelagic heterotrophs produce 15N-depleted ammonium and 15N-

enriched particulate matter that are recycled in and exported from the euphotic zone

respectively, therefore causing the observed low values of _15N (Checkley and Miller 1989).

In areas of the ocean where denitrification occurs (thus nitrate levels are lower), _15N values

have been shown to vary from +10 to +18 ‰, while _15N values of nitrate have been found to

range from +5 to +18 ‰ in areas where denitrification does not occur (and thus nitrate levels

are higher) (Owens 1987).

Generally, values of _15N increase with depth, probably due to the degradation of sinking

particles towards the bottom of the water column (Owens 1987).

Macroalgae and seagrass have been identified as having a _13C value between –9 and – 19 ‰,

with a _15N value ranging from +2 to +9 ‰ (Vizzini et al. 2002 and Fry et al. 1982).

The _15N values for zooxanthellae in Jamaican corals has been measured as ranging from

–2.15 to +3.54 ‰ (Muscatine and Kaplan 1994), and the _13C values of zooxanthellae living

in corals in the Red Sea have been measured as ranging from –10 to –14 ‰ (Achituv et al.

1997).

The _13C value of coral tissue can suggest whether their nutrition is primarily autotrophic or

heterotrophic: autotrophic corals typically have similar tissue _13C values as zooxanthellae,

with values ranging from –10 to –14 ‰, while heterotrophic corals have lower _13C values

since these values are closely reflective of their diet of zooplankton (Heikoop et al. 2000).

Coral samples from the Red Sea show _13C values of between –17 and –19.5 ‰ (Achituv et

al. 1997), indicating they are predominately heterotrophic corals, while the average value of

_13C from a literature review of coral samples was –11.8 ‰ (Heikoop et al. 2000), indicating

a dominance of autotrophy and dependence on zooxanthellae for these corals.

Coral samples (from hermatypic corals) that have been analysed for _15N from the Great

Barrier Reef and New Guinea indicate values of between +1.0 and +5.0 ‰ (Aharon and

Chappell 1983), with similar values measured in Jamaican corals of +0.1 to +4.3 ‰ (Heikoop

et al 1998). Hermatypic corals may not show the typical enrichment in _15N relative to their

diet (of +3 to +5 ‰) that is usually expected (Heikoop et al. 1998). This is because the

enrichment is usually driven by excretion of the lighter isotope, however in hermatypic corals

most of the excretory nitrogen (particularly the lighter isotope) will be recycled by the


46

symbiotic zooxanthellae, so that any loss of nitrogen will generally be as mucus or dissolved

organic nitrogen (Heikoop et al. 1998). Hermatypic corals will show a small enrichment of15N relative to zooxanthellae because they also take up small amounts of zooplankton from

the ocean water to supplement their vitamin intake (Muscatine and Kaplan 1994).

Phytoplankton have been identified as having a _15N value of +2 to +12 ‰ from literature

reviews (Owens 1987) or –2 to +7.8 ‰ (Wada 1980), with a _13C value of about –21 to –23

‰ (Vizzini et al. 2002, Achituv et al. 1997 and Dauby 1989). It has been found that the

uptake of DIN by phytoplankton involves discrimination against the heavier isotope, leading

to a fractionation relative to source, which is why phytoplankton can have a lighter isotope

ratio than DIN (Heikoop et al. 1998).

It is thought that biological nitrogen fixation characterises the nitrogen isotope ratio of

phytoplankton, with isotope fractionation associated with nitrate assimilation lowering the

_15N value from about +10 ‰ to +3 or +5 ‰ in ocean areas rich in nitrate (Minagawa and

Wada 1986). This means that the _15N value for plankton can be used to distinguish

biological nitrogen fixation from other nitrogen sources in oligotrophic seas (Minagawa and

Wada 1986).

For invertebrate consumers (such as zooplankton), _13C values have been found to range from

–11 to –22 ‰, with _15N values of +2.5 to +9 ‰ (Vizzini et al. 2002).

It is technically difficult to separate the phytoplankton from the zooplankton, and thus the

primary producers from the secondary producers, in most net or towed sample collections,

especially in oligotrophic areas (Minagawa and Wada 1986). Therefore some phytoplankton

samples being measured for isotopic ratios may be contaminated with zooplankton, and vice

versa (Minagawa and Wada 1986). Mixed plankton samples, containing both phytoplankton

and zooplankton, have been measured with _15N values between +2.0 and +6.0 ‰, whereas

the value for phytoplankton and primary producers alone is expected to be 2 – 4 ‰ lower than

this (Minagawa and Wada 1986).

Particulate matter samples, taken at Ishigaki and Palau reefs in the western Pacific Ocean,

showed average _13C values ranging from –18 to –22 ‰ and _15N values averaging +7.0 ‰

(Yamamuro et al. 1995). The particulate matter was thought to be predominately comprised

of phytoplankton, with contributions from zooplankton and bacteria. Other suspended

particulate matter samples have shown a range of values, with _15N values ranging from –2 to

+43 ‰ (Owens 1987). Given that suspended particulate matter is likely to include


47

phytoplankton, zooplankton, bacteria and resuspended bottom deposits, a range this wide is

not surprising (Owens 1987).

Fish have the most enriched ratios in the coral reef ecosystem, with _13C values ranging from

–11 to –20 ‰, and _15N values ranging from +6.4 to +16 ‰, depending on the range of their

feeding grounds (Vizzini et al. 2002). Transient fish typically show different ratios to resident

fish, with fish from coral reefs found to have about a +4 to 6 ‰ enrichment of _13C compared

to fish from open ocean waters, thought to be because the reef fish’s diet includes benthic

algae and seagrasses whereas the open ocean fish are predominately carnivores (Fry et al.

1982).

Limitations of stable isotope use

The use of natural variations in minor isotopes as an indicator of the source of the nutrient is

based on three assumptions: materials of different origins or composition have detectably

different isotopic ratios, the isotopic ratio of a particular material is unique, and the isotopic

ratio remains unchanged or the change is known (Owens 1987). The first two assumptions

have been proven as invalid, and not all differences in isotope composition are apparent,

however the natural variations in isotope ratios have been used to help determine the sources

and origins of a variety of materials (Owens 1987).

There are further limitations on the use of stable isotope values in ecological studies, aside

from the previously mentioned difficulty in separating phytoplankton from zooplankton when

analysing particulate matter in marine systems.

One major problem is that the number of different food sources that can be discerned in a

consumer’s diet from its isotope ratio is limited to one more than the number of different

isotopes used, while the number of different potential food sources to a consumer is

frequently far greater than the number of isotopes that can be examined (McClelland and

Montoya 2002).

Other factors that can lead to changes in stable isotope values are decomposition, dietary

content, nutritional and water stress and light availability, in the case of photosynthesising

organisms (McClelland and Montoya 2002 and Muscatine and Kaplan 1994). The effect on

isotope ratios of differing nitrogen availabilities, physiological state of organisms, the source

of nitrogen (nitrate, ammonium or urea) and species composition are not yet well understood,

particularly in oligotrophic waters where ambient nutrient concentrations are low (Waser et


48

al. 1998). Additionally, it has been recognised by several authors that the underlying

physiological and biological processes that lead to fractionation of stable isotopes are not well

understood (e.g. McClelland and Montoya 2002). It has been suggested that simultaneous

uptake of nitrate and ammonium may contribute to isotope fractionation (Waser et al. 1998).

In general however, the measurement of stable isotope ratios is useful in providing an

estimate of the source of nutrients and trophic structure of ecosystems.

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study Methodology

49

4 M E T H O D O L O G Y

This chapter describes the study site used for fieldwork and details of the methodology

utilised for sampling and analysis work.

4.1 STUDY SITE

Fieldwork for this study was undertaken from the 4th to the 12th of May 2003 within the

Ningaloo Marine Park, Western Australia, shown in Figure 3.

A section of reef located between Norwegian Bay and Point Cloates was chosen as the base

for the fieldwork. At the study area (see Figure 8), the reef is approximately 1 km wide and

characterised by reef sections 5 – 10 km in length, with a back-reef lagoon approximately 2 m

in depth and 10 m deep channels between reef sections. In this region the reef-line is straight

and close to both the shelf-break and shore, which is comparatively rare on the continental

shelf (Hearn et al. 1986). The offshore oceanographic environment is complex, characterized

by a possible recirculation pattern near Point Cloates (Taylor and Pearce 1999) as well as the

seasonal fluctuations of the Ningaloo and Leeuwin Currents. Previous hydrographic data

collected in the region indicated the surface 150 m to contain water with temperature 22 – 24oC and salinity 34.8 – 35 psu (Woo and Pattiaratchi 2003). The exact position of each

sampling site is given in Appendix 10.2. A full description of sampling at each of the sites is

contained in the following sections.


50

Figure 8: Sampling sites on chosen reef section - water and reef sampling (map taken from RoyalAustralian Navy 1985)

4.2 FIELDWORK

Sampling was conducted from aboard the RV Cape Ferguson, operated by the Australian

Institute of Marine Science (AIMS). During April and May 2003, the RV Cape Ferguson was

utilised to conduct a research project on whale sharks in the Ningaloo Reef area, overseen by

3rd Reef sampling8/5/03

Channel Pass

NORWEGIANBAY

1st Reef sampling5/5/03

2nd Reef sampling5/5/03

NORTH TRANSECT

LAGOON

MIDDLE TRANSECT

TopMiddleBottom

POINTCLOATES

SOUTH TRANSECT

10km

5km4km

3km

1km2km


51

AIMS and in collaboration with the Commonwealth Scientific and Industrial Research

Organisation (CSIRO), Western Australian Department of Conservation and Land

Management and U.S. research groups including SCRIPPS Institute of Oceanography, NOAA

and HUBBS Seaworld (Hull 2003). Sampling for this study was therefore executed

opportunistically between the whale shark researches.

The Cape Ferguson was equipped with a CTD probe (Conductivity, Temperature and Depth

recording device), two 5 L Niskin bottles, two 10 L Niskin bottles, a hydrographic winch for

deploying the CTD probe and Niskin bottles and a dry laboratory, fitted with a vacuum pump

and associated filtering equipment. This equipment was utilised for the water sampling

component of the fieldwork.

A complete list of each sample taken and the analysis performed is given in Appendix 10.1.

4.2.1 WATER SAMPLING

The primary water sampling was conducted along three evenly spaced transects, radiating

outward from the chosen section of reef. The transects are shown in Figure 8. For exact

positions (based on GPS data) of each site, see Appendix 10.2. The first site on each transect

was located 1 km from the reef section, with the three starting sites located 500 m apart. The

three transects were positioned along lines pointing roughly northwest, west and southwest.

Samples were taken at sites located 1 km, 2 km, 3 km, 4 km, 5 km and 10 km from the reef

section, for a total of 6 sample sites per transect, and 18 in total.

In general samples were taken every 20-30 m through the water column, with the number of

samples per site ranging from two (surface and bottom) to four (surface, bottom and two mid-

depth) depending on water column depth, using 5 L and 10 L Niskin bottles. The depths that

were sampled at each station are given in Appendix 10.1. The deployment of the Niskin

bottles is shown in Figure 9.


52

Figure 9: Deployment of the Niskin bottle

In addition to these offshore samples, three sample sites were chosen within the reef lagoon,

on the shore side of the same reef section. The position of these sites is shown in Figure 8.

These three sites were located approximately 500 m from the reef section, opposite the first

three sampling sites on the other side. Two samples were taken at each of these three sites, at

the surface and at the bottom of the water column.

At each offshore sampling site, the CTD probe was deployed as part of the sampling rosette,

logging data at a regular interval of approximately every 0.5 m of depth, from 1m from the

surface to 1 m from the bottom. This recorded the depth, temperature, salinity and dissolved

oxygen concentration of the water column at each site. The probe is shown in Figure 10. The

measurements taken by the CTD probe were recorded on the ship’s data logger, which were

then saved to a CD and sent to Perth for analysis. The ship’s computer performed all the

necessary conversions from the raw sampled data to that which could be used, and therefore

the physical data did not require any further processing. The physical data recorded by the

CTD probe were recorded on both the cast down and up. Only the recordings from the cast

down were used for analysis. Temperature was measured in degrees Celsius (oC), salinity in

practical salinity units (psu) and dissolved oxygen concentration in milligrams per litre

(mg/L).


53

The CTD probe was also utilised for the measurement of the physical parameters in the

channel pass at the northern end of the reef section used for the offshore sampling (see Figure

8).

Figure 10: Deployment of the CTD probe

Dates and conditions for sampling

The stations closest to the reef on each transect (located 1 km from the reef) were sampled on

the 5th of May 2003. Weather conditions were good on this sampling day. There were low

water levels due to low tides, with a southwest sea breeze in the afternoon when the samples

were taken. The good conditions meant that this sampling was easy to conduct and little water

was spilled and wasted in transferring to storage containers from the Niskin bottles.

The northern transect was completed on the 6th of May 2003. Sea conditions were worse on

this day, with 2 m swells beginning early in the morning. There higher water levels on this

day, with the wind stronger in the morning. The wind abated significantly by early afternoon,

when the majority of the sampling was performed, which made sampling much more easy and

enabled greater efficiency in transferring water to storage containers.

The remaining two transects were completed on the 7th of May 2003. On this day the swell

was only to 1 m, but the wind was stronger with more choppy conditions. This made

sampling more difficult; hence more water was spilled and wasted when transferring from


54

Niskin bottles to storage containers. However the rougher conditions did not affect the

filtering process inside the laboratory.

For the three sample sites on the lagoon side of the reef, water samples were taken by

deploying the Niskin bottles by hand from a rubber dinghy. These were then emptied into

labelled 20 L plastic drinking water containers onboard the dinghy and transported back to the

Cape Ferguson. The same procedure for filtering, as outlined below, was then followed as for

the other water samples.

Filtering Procedure for Water Samples

Niskin bottles were emptied into empty 20 L plastic drinking water containers, each labelled

with the station number and depth. Sample water was then taken from these containers. The

transfer of sample to these containers is shown in Figure 11.

Figure 11: Transfer of sample water from Niskin bottle to 20 L storage container

A 1 L container was rinsed with some of the sample water and then used to transfer sample

from the 20 L containers. Water was transferred from the 1 L container to the vacuum pump

using a 100 mL volumetric cylinder, which was first rinsed with a little of the sample water.

1 L of sample was filtered directly onto Whatman GF/F 25 mm filters, which had been pre-

combusted in an oven at 100 oC for four hours and then in a furnace at 450 oC for three hours

to remove any trace amounts of particulate organic carbon.


55

A further 1 L of the sample water was passed through a 37 _m screen to isolate small

particles, and then filtered as above.

These two sets of filters were frozen for later analysis of the concentration of particulate

organic carbon (POC), particulate organic nitrogen (PON) and stable isotopic values of the

particulate material (_13C and _15N).

An additional 100 mL of sample was filtered onto filter papers for analysis of chlorophyll a

concentrations. This was repeated twice, to test the chlorophyll a concentration in two

replicates. Filtering of the sample water is illustrated in Figure 12.

Figure 12: Filtering sample water onto Whatman GF/F filters

Each filter paper was folded into quarters using tweezers and placed on a small square of

aluminium foil.

Another 10 mL of sample water was taken, unfiltered, and put into a clean (washed with

ethanol) vial for analysis of dissolved inorganic nutrient (nitrate/nitrite and phosphate)

concentrations.

All samples were labelled appropriately. After the details were recorded, the filter papers and

vials were stored in an airtight bag and kept frozen for the remainder of the journey.


56

4.2.2 REEF ORGANISM SAMPLING

Organisms were collected on the 5th and 8th of May 2003 from sections of reef a short

distance to the north of that used for the water sampling transects (see Figure 8). This location

was used because the reef section chosen for the water sampling was within a Sanctuary Zone

of the Ningaloo Marine Park, where it is not permitted to disturb the reef in any way or collect

organisms from the reef. The exact positions of the reef specimen sampling sites are given in

Appendix 10.2.

The reef sampling was done from a small rubber dinghy. Collection of immobile specimens

was achieved by picking up organisms with gloved hands from coral sections of the reef or

from the sea floor. Coral samples were collected by breaking off pieces by hand. Collection of

large reef fish was made by using a hand fishing line, from the back of the Cape Ferguson

vessel. Small reef fish were collected by using a small slingshot made from a toothpick and

rubber band, which speared the fish when fired. A total of 26 specimens were taken from the

near vicinity of the reef for analysis.

Three of the large reef fish specimens were identified to species level onboard, therefore only

a small portion of tissue was kept for analysis, cut from the side of the fish around the fins.

The remainder of the samples were unable to be identified to species level, thus the organisms

were kept whole.

Samples were placed in a bucket filled with seawater on the dinghy, for transport back to the

Cape Ferguson. Once on board the Cape Ferguson, samples were transferred into airtight bags

for storage. These were labelled with the specimen number and placed into the freezer, where

they remained for the rest of the voyage. The details of the sample were recorded in a

notebook.

4.2.3 TRANSPORT OF SAMPLES

Upon arrival back in Exmouth harbour on the 12th of May 2003, the frozen water and reef

samples were transferred to an Esky, which was sealed shut with packing tape. The samples

remained in this condition for transport to the airport at Learmonth (half an hour), flight from

Learmonth to Perth (three and a half hours) and transport back to a freezer in Perth. Therefore

the samples were out of the freezer for a total of approximately six hours. Once back in Perth,

the samples were placed in a freezer and remained there until analysis.


57

4.2.4 SOURCES OF ERROR IN SAMPLING

Possible sources of error associated with the process of sample collection are:

- plastic drinking containers used as storage vessels not being rinsed with the sample water

before being filled;

- sample water sitting in storage vessels for up to 6 hours while waiting to be filtered, which

can degrade chlorophyll a due to increased temperature and light intensity (Environmental

Research Laboratory 2003a);

- not thorough enough rinsing of 1 L containers and 100 mL volumetric cylinders when

transferring water from the drinking containers to the vacuum pump for filtering or to the

nutrient vials;

- contamination on and between filter papers by using the same unrinsed tweezers each

time;

- possible contamination of filter papers or aluminium foil pieces by human hands when

being moved;

- possible compromise of sample integrity due to time outside of freezer when being

transported back to Perth.

4.3 LABORATORY ANALYSIS OF SAMPLES

The filter papers to be analysed for particulate organic carbon (POC), particulate organic

nitrogen (PON) and isotope signatures of _13C and _15N were sent to the Institute of Earth

Sciences, Hebrew University, Israel. The filter papers to be analysed for chlorophyll a

concentrations and the water samples to be analysed for nutrient concentrations were kept at

the Centre for Water Research (CWR) to be analysed in the Environmental Research

Laboratory (ERL). The reef organism samples were also sent to the Institute of Earth Sciences

to be analysed for isotope signatures of _13C and _15N.

4.3.1 ANALYSIS OF POC, PON AND ISOTOPE SIGNATURES

These filter papers were kept folded inside the squares of aluminium foil they were originally

placed in, and remained in the freezer until drying. They were transferred to a single unsealed

airtight bag, which was placed in an FD4 freeze-drier, at the Department of Agriculture,

University of Western Australia, to prepare them for analysis and transport. The filter papers


58

were placed in the freeze-drier on the morning of 3rd of June 2003 and removed on the 5th of

June 2003.

The filters were kept in the same airtight bag, to which was added approximately 50 g of

silica gel desiccant. The bag was then sealed and not reopened until arrival in Israel.

The filters were packed into tin foil containers and combusted at 1125 oC with pure oxygen.

Isotope ratios were measured with a mass spectrometer, which is the only instrumentation

precise enough to allow the small variations in natural abundance to be measured (Preston

1992). Spectrometric error for a single determination is kept around ± 0.05% and

reproducibility between sample replicates better than ± 0.1% (Aharon and Chappell 1983).

The filters were analysed on a Delta Model gas ratio mass spectrometer made by Finnigan

Mat, using an automatic carbon and nitrogen analyser. After separation on a GC column, the

peaks and integrated areas of the masses of 28 and 29 for nitrogen and 44 and 45 for carbon

were determined.

4.3.2 ANALYSIS OF CHLOROPHYLL A CONCENTRATION

The filter papers to be analysed for chlorophyll a concentrations were removed from the

freezer on 9th June 2003. In total there were 122 samples to be analysed – 61 samples with 2

repeats of each sample. In addition to this, 5 blank samples were analysed as controls, after

approximately every 25 samples. Because these samples remained in the freezer for 5 weeks

before analysis, there may have been a loss of chlorophyll – the recommended maximum time

for keeping samples frozen before analysis is 3.5 weeks before a significant loss of

chlorophyll occurs (Environmental Research Laboratory 2003a).

The procedure followed for chlorophyll a analysis is outlined below. The chosen extraction

method was extraction by grinding. The method used 90% acetone as the extraction solvent

because of its relatively low toxicity and its efficiency for most types of algae (Environmental

Research Laboratory 2003b).

On the afternoon of 9th June, 42 of the samples were ground up ready for analysis. These were

placed in the freezer for 22 hours before reading in the fluorometer. The remaining samples

were ground up for analysis on the 16th of June 2003 and frozen for 21 hours before reading

in the fluorometer.

Extraction of photosynthetic pigments by grinding was achieved by the following method:


59

Samples were taken from the freezer and kept in a small esky on the bench. Overhead lights

were turned off, but due to large windows in the room there was still a high level of light

present.

One at a time, the pieces of aluminium foil were removed from the esky and the first filter

paper removed with tweezers. The repeat filter paper was left folded inside the aluminium foil

to be analysed next. The first paper was cut into small pieces using scissors, which had first

been wiped down with ethanol, and placed into a clean grinding tube (rinsed with ethanol).

The filter pieces were pushed to the bottom of the tube and 4 mL of 90% acetone was added.

The grinding tube was placed in a beaker of crushed ice. It was then ground using a tissue

grinder until it formed a slurry. The ice prevented overheating of the sample, which would

have caused degradation of the chlorophyll a (Environmental Research Laboratory 2003b).

The slurry was poured into a 10 mL plastic vial. Using the pipette, another 4 mL of acetone

was used to rinse out the grinding tube, which was then added to the plastic vial. The vial was

then capped, shaken and placed in a rack in another small esky. When the rack was full (after

40 filter papers had been ground) it was placed in the freezer overnight.

The grinding tube and pestle were rinsed with acetone and wiped down with a tissue before

proceeding on to the next filter paper, and this procedure was followed until all samples were

prepared for reading in the fluorometer.

The samples were taken out and shaken the morning after they were placed in the freezer.

The afternoon after the samples were ground up, they were removed from the freezer and

shaken again before being prepared for reading in the fluorometer.

The slurry was filtered using a 50 mL glass manifold and electric pump through a Whatman

GF/F 25 mm filter into a clean plastic tube. This was poured into a clean 10 mL disposable

glass culture tube. A small piece of parafilm “M” laboratory film was placed over the top of

the vial to prevent evaporation.

The samples were allowed to come to ambient temperature before analysis.

Before analysis, the TD700 fluorometer was warmed up and calibrated.

The parafilm was removed from the culture tube and the tube was placed in the fluorometer.


60

The reading was recorded as the Rb (before acid result).

3 drops of 1N HCl were added to the tube. The parafilm was replaced over the top of the tube,

the tube was shaken and left for 60 seconds.

The tube was again placed in the fluorometer and the reading recorded as the Ra (after acid

result).

All acetone waste was placed into a waste bottle. Once the sample analysis was finished, the

glass culture tubes were placed in the hazardous waste container. All other equipment (apart

from the plastic tubes) was washed down with ethanol. The plastic tubes were washed

thoroughly with detergent and deionised water and left on a draining rack to dry.

The chlorophyll a concentrations were calculated using the following formula:

Chlorophyll a ( )

( ) ⎟⎠

⎞⎜⎝

⎛−⎟⎟⎠

⎞⎜⎜⎝

⎛

−=

V

vRR

r

rab1

, (_g/L)

Where r = before-to-after acidification ratio of a pure chlorophyll a solution = 2.2

Rb = fluorescence of a sample prior to acidification

Ra = fluorescence of a sample after acidification

v = volume of the ground-up extract (mL)

V = volume of the original filtered sample (mL)

Possible errors associated with the analysis of chlorophyll a concentration are:

- interference in the measurement of chlorophyll a due to the possible presence of a

substance that fluoresces in the red region of the spectrum;

- underestimation of chlorophyll a due to the possible presence of chlorophylls b and c;

- possible degradation of chlorophyll a concentrations due to the fairly bright light

conditions in the ERL during analysis; and

- possible contamination of filters due to contamination of scissors, tweezers, grinding tube

or manifold filter by another sample.


61

4.3.3 ANALYSIS OF NUTRIENT CONCENTRATIONS

Analysis of the water samples for dissolved inorganic nitrogen in the form of nitrate (DIN)

and dissolved inorganic phosphorous in the form of phosphate (DIP) was undertaken at the

ERL at CWR, using an Alpkem Segmented Flow Nutrient Analyser (otherwise known as an

autoanalyser). The procedure followed was based on the Hydrochemistry Operations Manual

from CSIRO (Cowley 1999). The analysis based on this procedure has an associated error

estimated at ± 5% for both DIN and DIP. The following description of the analysis is taken

from the Operations Manual (CSIRO 2003).

The autoanalyser is used for simultaneous analysis of dissolved inorganic nitrate plus nitrite

and dissolved inorganic phosphorous in seawater samples. The autoanalyser uses the

principles of colourmetric analysis, in a continuous flow system where all manipulations of

samples are automated. Therefore each sample and standard is treated identically, by

precision timing and proportioning of reagent additions.

An automated sampler introduces the sample into the analytical stream at precisely timed

intervals. The sample is then split into individual streams according to the number of nutrients

to be measured and each sample segment is then mixed with the reagents, which are dosed

into the analytical stream by a peristaltic pump.

As the sample moves through the system it mixes with the reagents, and a coloured

compound whose light absorbance is approximately proportional to the nutrient concentration

in the sample is formed. Each channel is calibrated with calibrants of known concentration,

establishing the relationship between absorbance at the selected wavelength and the standard

concentration.

Analysis of orthophosphate is based on the formation of a phosphomolybdenum blue species.

Ascorbic acid is added as a reductant to form a mixture of heteropoly acids (_ and _ forms),

which is a highly coloured blue compound analysed at 880 nm.

Nitrate analysis is based on the quantitative reduction of nitrate to nitrite, and the subsequent

formation of an azo dye. The reduction is achieved by passing the sample through a

copperised Open Tubular Cadmium Reactor (OTCR) incorporated into the reaction manifold.

Imidazole buffer is used to adjust the pH of the samples to 7.8, optimising the reduction to

nitrite and preventing further reduction to hydroxylamine and ammonia. The reduction

efficiency of the OTCR is monitored continuously by passing nitrate and nitrite solutions of


62

the same nominal concentration through the column and calculating the ratio of nitrate peak

height to nitrite peak height.

The effluent from the OTCR undergoes diazotisation with sulphanilamide, and the subsequent

coupling with N-1-napthylethylenediamine Dihydrochloride. The resulting azo dye is

analysed at 540 nm. It constitutes any nitrite originally present in the sample, plus the nitrate

that has been quantitatively reduced to nitrite. Therefore the concentration of nitrogen

measured by the analysis is of the combination of nitrate and nitrite, or NOx.

4.3.4 REEF ORGANISM ANALYSIS FOR ISOTOPE SIGNATURES

The reef organism samples needed to be freeze-dried before they could be analysed for

isotope signatures. The samples were placed in the freezer on the morning of the 3rd of June

2003 and were collected on 18th June 2003. The long drying time was due to the large size

(and hence water content) of some of the samples. After collection, the samples were kept in

the same airtight bags they had been initially placed in.

Identification of the reef specimens (to species level where possible) was undertaken in two

stages: a preliminary identification at the Department of Zoology, University of Western

Australia, then a detailed identification at the Aquatic Zoology Department, Western

Australian Museum. A list of the species identifications is given in Appendix 10.3.

Following the preliminary identification analysis, a small piece was cut from the tissue of

each of the samples. These pieces were placed in small, individual airtight bags with

approximately 10 g of silica gel desiccant, and then all the small bags were sealed inside one

large airtight bag. This was sent to the Institute of Earth Sciences in Israel for analysis.

Analysis of the isotope ratios followed the same procedure as for the POC and PON analyses,

using a gas ratio mass spectrometer.

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study Results

63

5 R E S U L T S

Included in this chapter are summaries of the CTD data (for temperature, salinity and

dissolved oxygen concentration), the water samples (for dissolved inorganic nitrogen

concentration, dissolved inorganic phosphorous concentration, chlorophyll a concentration

and stable isotope ratios of δ13C and δ15N) and the reef specimens (for stable isotope ratios of

δ13C and δ15N). Although samples were sent to the Institute of Earth Sciences, Israel, for

analysis of the concentrations of particulate organic carbon and particulate organic nitrogen

from water samples, the complete data set was not received from the laboratory and therefore

has not been included in these results. Additionally, the stable isotopes ratios for 8 reef

specimens that were sent for analysis were unable to be processed, therefore only the data

from the remaining 18 are presented.

5.1 CTD DATA

5.1.1 OFFSHORE STATIONS

Because data was recorded at approximately every 0.5 m through the water column, it is not

feasible to present the complete data set here. However a summary of this data is tabulated

and presented in the following sections.

The data taken at each station along the transects were also used to create cross-sectional

contours along each transect. This was achieved by inputting the data into MATLAB (a

computer plotting program) and creating a grid that was 10 km long in the horizontal (from

reef to offshore) and 133 m deep in the vertical (the deepest point from the three transects,

used on each transect to allow comparison). The data was then interpolated between each

station and sample point using a linear function, to create a value for every point in the new

grid. This created a series of coloured contours showing the gradient in each parameter from

offshore (10 km from reef) to onshore (1 km from reef) and also over depth (133 m offshore

to 20 m onshore). This provided a very useful way to visually appraise the results. The results

from this series of plotting are also shown in the following section. Overlain on the graphs are

black dotted lines, indicating the distance from the reef of each of the sampling stations.

Although there was CTD data taken at the station 1 km from the reef on the middle transect,

the computerised data was subsequently lost, therefore the presentation of data on the middle

transect begins at the 2 km mark.


64

Temperature

A summary of the temperature data is presented in Table 1. This table gives the minimum,

maximum, mean and standard deviation of temperature values for various locations,

differentiated by water depth and transect. The surface 40 m has been isolated from the rest of

the water column for analysis because graphical representation of the data indicated there was

a distinct surface mixed layer to 40 m depth, over which the temperature varied little between

the three transects. Also presented in Table 1 is a summary of the temperatures from the

channel pass between the reef sections.

Table 1: Summary of temperature data for the three transects and the channel

Temperature (deg C)Location

Minimum Maximum Mean Standard DeviationNorthern transect - surface 40 m 27.01 27.63 27.38 0.14Northern transect - below 40 m 25.12 27.22 26.46 0.56Middle transect - surface 40 m 27.24 27.49 27.35 0.08Middle transect - below 40 m 25.86 27.45 26.84 0.41

Southern transect - surface 40 m 27.10 27.43 27.33 0.09Southern transect - below 40 m 26.91 27.36 27.16 0.16

All transects - surface 40 m 27.01 27.63 27.35 0.11All transects - below 40 m 25.12 27.45 26.82 0.51All transects - total water 25.12 27.63 27.09 0.41

Channel pass 25.72 26.40 25.97 0.30

The data indicates that the surface 40 m of water contains fairly constant temperatures

between the northern, middle and southern transects, ranging from 27.01 oC to 27.63 oC. In

general the surface layer is warmer than the bottom layers. Beneath the surface waters there is

a wide range in temperature values, from 25.12 oC to 27.45 oC, as temperatures decrease

towards the bottom of the water column. The data also shows that the channel water is

qualitatively colder than the majority of the water in the transects.

Figure 13, Figure 14 and Figure 15 show the cross-sectional contours for the northern, middle

and southern transects respectively for the temperature data.


65

Figure 13: Temperature contours along the northern transect, shown in cross-section

Figure 14: Temperature contours along the middle transect, shown in cross-section


66

Figure 15: Temperature contours along the southern transect, shown in cross-section

The northern and middle transects show a marked difference between the surface 40 m of

water and the bottom waters, with a difference of approximately 1 oC over a layer about 5 m

thick at around 40 m depth. The decrease in temperature towards the bottom is most marked

in the northern transect. The northern transect also shows an intrusion of cool water along the

bottom towards the shoreline, with contours of similar temperature reaching from 110 m

depth at 10 km to 70 m depth at 4 km offshore. The bottom depth on the middle transect is not

as deep as the north, but indicates a similar pattern. While the southern transect does not

allow a comparison with the deep waters, it shows similar patterns in the surface waters.

The deepest waters on the southern transect are warmer than on the other two transects, with

very little comparative difference between the surface and deep waters.

The contours of temperature within 5 km of the reef are tilted upwards slightly, which is

consistent across the three transects.

Salinity

A summary of the salinity data is presented in Table 2. As for the temperature data, the

surface 40 m has been isolated from the rest of the water column for analysis because

graphical representation of the data indicated there was a distinct surface mixed layer to 40 m

depth. Also presented in Table 2 is a summary of the salinity values from the channel between

the reef sections.


67

Table 2: Summary of the salinity values for the transects and the channel

Salinity (psu)Location




Channel pass 35.04 35.15 35.11 0.04

The data indicates that the ranges of salinity values across the three transects are fairly

constant, varying between 34.91 psu and 35.1 psu. The data show that the water in the

southern transect does not reach the same high salinity values as the northern and middle

transects, and that the surface waters on the southern transect have about the same salinity as

the bottom waters, but it is hard to discern many trends between the transects from this

presentation of the data. Again, the water in the channel appears to be different to that of the

transects, with the minimum salinity value measured in the channel larger than some of the

maximum values measured in the transects and a higher overall maximum than observed

elsewhere.

Figure 16, Figure 17 and Figure 18 show the salinity contours along the three transects in

cross-section. From these plots it is possible to discern some within-transect and between-

transect trends.


68

Figure 16: Salinity contours along the northern transect, shown in cross-section

Figure 17: Salinity contours along the middle transect, shown in cross-section


69

Figure 18: Salinity contours along the southern transect, shown in cross-section

The three cross-sections show the same general trend, for less saline water to be located at the

surface and more saline water at depth. As for the temperature contours, the surface 40 m of

water contain very similar salinity from the 10 km station towards the 4 km station, varying

very little.

However the pattern is different for the stations closer to the reef. The graphs show a tilting of

contours upwards from deep offshore waters towards the shoreline, similar to the temperature

contours. On each of the transects, there is a localised patch of relatively high salinity located

between 2 km and 3 km from the reef at the bottom of the water column. This is most

pronounced in the northern transect, with the patch containing the same salinity as that from

100 m depth at 10 km, of approximately 35.09 psu.

As with the temperature contours, the northern and middle transects indicate a qualitative

difference between the surface 40-50 m and the rest of the water column. Beneath this 40-50

m, the northern and middle transects show the water getting progressively more saline

towards the sediments. Again, the southern transect does not become as saline as the other

two transects, and the shallower depth does not allow for a similar depth comparison as for

the northern and middle transects.


70

Dissolved Oxygen Concentration

A summary of the dissolved oxygen data is presented in Table 3.

Table 3: Summary of the dissolved oxygen concentrations from the transects and channel

Dissolved Oxygen Concentration (mg/L)Location




Channel pass 6.65 6.99 6.84 0.14

The dissolved oxygen data indicates that there is very little qualitative difference between the

concentrations in the surface 40 m and rest of the water column on each of the transects, with

approximately the same ranges of values measured. It appears that the surface waters of the

southern transect contain lower concentrations of dissolved oxygen compared to the rest of

the transects, and that the channel water contains on average less oxygen than is observed in

the transects.

Figure 19, Figure 20 and Figure 21 show the cross-sectional contours for the concentration of

dissolved oxygen on each transect.


71

Figure 19: Dissolved oxygen concentration contours on the northern transect, shown in cross-section

Figure 20: Dissolved oxygen concentration contours on the middle transect, shown in cross-section


72

Figure 21: Dissolved oxygen concentration contours on the southern transect, shown in cross-section

The contours of the concentration of dissolved oxygen indicate that in general there is a fairly

uniform dissolved oxygen profile, both across the three transects and with depth within each

transect. From the surface to very deep water, with a few exceptions, the concentration of

dissolved oxygen varies by about 0.2 mg/L.

The very deep water in the northern and middle transects shows lower levels of dissolved

oxygen, down to approximately 6.7 mg/L. This occurs in the bottom 15 m in the northern

transect and bottom 5 m in the middle transect.

Within each transect, there are also localised patches of low dissolved oxygen concentration

relative to the rest of the cross-section. In the northern transect, the concentration of dissolved

oxygen reaches a minimum of about 6.7 mg/L at a depth of about 40 m, in a thin layer

between 2 km and 4 km from the reef. In the middle transect, there is a low of approximately

6.6 mg/L between 40 and 50 m, in a wedge between 3 km and 4.5 km from the reef. Also on

this transect, there is a patch of low dissolved oxygen at the surface: a minimum of

approximately 6.3 mg/L, within a patch extending from 3 – 4.5 km between the surface and

10 m depth.

The southern transect shows a large area of decreased dissolved oxygen concentrations

compared with the other two transects. Along the length of the transect within the surface 10

m of water, the levels of dissolved oxygen are between 6 mg/L and 6.7 mg/L, with the


73

minima reached at 10 km and 2 km from the reef, and surrounding waters along the surface at

concentrations qualitatively lower than seen throughout the rest of the transect. The minimum

levels shown in the surface of the southern transect are also qualitatively much lower than are

found anywhere on the northern transect.

5.1.2 CHANNEL STATION COMPARISON

This section contains graphical comparisons of the data recorded in the channel pass with that

recorded in the majority of the offshore stations, for temperature, salinity and dissolved

oxygen concentration. The data are shown as vertical profile distributions for each parameter,

as this method allows for an easy comparison between stations as well as an easy visual

appraisal of the change of the parameters with depth at individual stations. The offshore

stations at 2 km and 4 km on each transect are omitted, to allow for easier visual analysis of

the profiles.

0

20

40

60

80

100

120

140

24.5 25 25.5 26 26.5 27 27.5 28

Temperature (deg C)

Dep

th (

m)

north 1 north 3 north 5 north 10middle 3 middle 5 middle 10 south 1south 3 south 5 south 10 channel

Figure 22: Comparison of temperature profiles for channel and selected offshore stations

Figure 22 confirms that there is a qualitatively large difference between the temperatures

within the channel and the surface 40 m of the offshore stations, with the coolest water at the

offshore stations (27 oC) still warmer than the warmest water from the channel (26.4 oC). The

temperatures measured in the channel are more similar to the water found towards the bottom

of the northern and middle transects at 10 km.

The profiles indicate that the water in the channel is highly stratified over the depth of 9 m,

with the surface 2.5 m of water containing similar temperature, varying temperatures


74

indicated between 2.5 m and 5 m, then similar (lower) temperatures between 5 and 9 m. The

range of temperatures observed in the channel is also larger than seen in the offshore stations

with comparative depths – a range of 0.7 oC in the channel compared with ranges closer to 0.5oC in the surface water of the offshore stations. (The station at 10 km on the northern and

middle transects exhibit wider ranges of values, however these waters are much deeper and

therefore the comparison is not so meaningful.)

0

20

40

60

80

100

120

140

34.85 34.9 34.95 35 35.05 35.1 35.15 35.2

Salinity (psu)

Dep

th (

m)

north 1 north 3 north 5 north 6 middle 3 middle 5

middle 6 south 1 south 3 south 5 south 6 channel

Figure 23: Comparison of salinity profiles for channel and selected offshore stations

Figure 23 confirms that the water in the channel is qualitatively far more saline than the

majority of the water in the offshore stations, having a range of approximately 35.04 – 35.15

psu. Similarly high saline values offshore are only reached towards the bottom of some of the

northern transect stations and the 10km station on the middle transect.

The profile for salinity in the channel shows a similar pattern to temperature, with similar

(relatively low) values observed in the surface 2.5 m, varying values between 2.5 m and 5 m

and similar (relatively higher) salinity values between 5 m and 9 m. Again as for temperature,

the range of salinity values found in the channel is greater than for the majority of the rest of

the stations. The channel has a range of 0.11 psu, while the offshore stations have ranges of

approximately 0.03 psu. (Exceptions are the 3 km and 10 km stations on the northern transect

and the 10km station on the middle transect, which have ranges of between 0.12 and 0.19 psu,

however these stations are much deeper than the channel). The range seen in the channel

seems especially large when considered with the shallow depth found there.


75

The difference between the channel water and the offshore water is highlighted by plotting

temperature versus salinity, as in Figure 24. The figure clearly shows the surface waters of the

channel being comparable to the deep waters from the 10km stations, but the bottom waters

of the channel containing water that is qualitatively more saline.

24.5

25

25.5

26

26.5

27

27.5

28

34.9 34.95 35 35.05 35.1 35.15 35.2

Salinity (psu)

Tem

per

atu

re (

deg

C)

channel north 1 north 3 north 5 north 10 middle 3

middle 5 middle 10 south 1 south 3 south 5 south 10

Figure 24: Temperature versus salinity for channel pass and majority of offshore stations

Figure 25 indicates that the dissolved oxygen profiles are more variable than for temperatureand salinity.

0

20

40

60

80

100

120

140

5.5 6 6.5 7 7.5

Oxygen (mg/L)

Dep

th (

m)

north 1 north 3 north 5 north 10middle 3 middle 5 middle 10 south 1south 3 south 5 south 10 channel

Figure 25: Comparison of dissolved oxygen concentration profiles for channel and selected offshorestations


76

The profiles indicate patterns of dissolved oxygen concentration like those described from the

transect cross-sections, with fairly constant levels around 7.0 mg/L observed throughout the

water column, decreasing towards the sediments, and with lower levels observed in the

surface waters of the southern transect.

In comparison, the channel exhibits a lower concentration of dissolved oxygen in the surface

water, of approximately 6.65 mg/L, and increasing concentrations with depth to a maximum

of nearly 7 mg/L. This relationship with depth is the inverse of what is seen in the offshore

stations. The range of values found in the channel is again much greater than found in the

majority of the offshore stations, with a range of 0.35 mg/L compared with an average range

offshore of approximately 0.1 – 0.15 mg/L (aside from the 3 km station on the northern

transect, 5 km station on the southern transect and the three 10 km stations, which exhibit

larger ranges and lower minimum values).

5.2 WATER SAMPLING DATA

A summary of the water sampling parameters are presented in tables in this section. Figure

26, Figure 27 and Figure 29 show the vertical profiles of DIN, DIP and chlorophyll a

respectively, for the lagoon stations and the majority of the offshore stations (stations at 2 km

and 4 km from the reef are omitted to make it easier to visually analyse the profiles). The

stable isotope ratios are presented in Section 5.3, for discussion and comparison with the

isotope ratios found in the reef specimens.

Nitrate and nitrite concentrations (DIN)

A summary of the DIN concentrations is presented in Table 4. The data are differentiated by

transect, depth in the water column and distance from the reef. The averages from the lagoon

data are also presented. There was very little difference between classifying the ‘surface

waters’ as 1 m or 20 m, and in distinguishing the ‘onshore’ waters as within 3 km, 4 km or 5

km from the reef. The tabulated data is presented using the surface 20 m of water as ‘surface

waters’ and within 3 km of the reef as ‘onshore waters’.


77

Table 4: Summary of the DIN concentrations for the transects and lagoon stations

Nitrate and Nitrite (µµµµg/L)Location

Minimum Maximum Mean Standard DeviationAll stations 55.00 115.00 81.00 16.57

Northern transect 55.00 72.00 66.11 4.79Middle transect 62.00 115.00 79.47 17.46

Southern transect 69.00 115.00 92.39 12.58Surface 20 m 61.00 115.00 77.00 14.88Below 20 m 55.00 115.00 82.33 18.37

Onshore - 3km or less from reef 64.00 104.00 74.73 11.05Offshore - 4km or more from reef 55.00 115.00 83.45 19.54

Lagoon stations 86.00 99.00 96.33 5.13

The data shows that there is an increase in average DIN concentrations from the northern

transect to the southern transect. The data also indicates a greater concentration of DIN in the

bottom waters across the transects than in the surface waters. From the averages in this table,

it is difficult to discern any onshore-offshore patterns. The data also indicates that the lagoon

water contains a higher concentration of DIN than the majority of the transect stations.

The vertical profiles of the data are presented in Figure 26 and more clearly show within-

transect patterns.

0

20

40

60

80

100

120

140

0 20 40 60 80 100 120 140

Nitrate/nitrite (ìg/L)

Dep

th (

m)

north 1 north 3 north 5 north 10middle 1 middle 3 middle 5 middle 10south 1 south 3 south 5 south 10lagoon top lagoon middle lagoon bottom

Figure 26: Comparison of DIN concentration profiles for offshore and lagoon stations

Moving across Figure 26 from left to right, the profiles displayed start with the northern

transect having lowest values, then move through the middle and finally the southern transect

having the highest values of DIN, therefore confirming that there is a gradient in DIN

concentration moving from north to south (as indicated by Table 4).


78

The concentrations of DIN across the northern transect range from 60 to about 70 _g/L, with a

minimum of 55 _g/L at approximately 40 m depth at the station 10 km from the reef. The

middle transect’s stations at 1 km and 3 km show concentrations similar to those on the

northern transect (about 65 – 72 _g/L). However, the outer stations on the middle transect (at

5 km and 10 km) exhibit much higher concentrations (of about 80 – 115 _g/L). The

concentrations observed on the southern transect are generally higher than on the northern and

middle transects, with the exception of the station at 1 km, which displays a concentration of

approximately 70 _g/L. The stations at 3 km, 5 km and 10 km on the southern transect all

contain higher concentrations, ranging from 86 – 105 _g/L (comparable to the outer stations

on the middle transect).

There are also within-transect patterns similar to each transect. The concentration of DIN

increases with depth on the 10 km stations, with maximum values at this station observed at

the sediments (69 _g/L in the north, 115 _g/L in the middle and 97 _g/L in the south). Within

the 1 km – 5 km stations, there is a zone of qualitatively elevated values observed on each

transect (around 70 _g/L on the northern and middle transects and around 100 _g/L on the

southern transect) between the surface and the sediments: on the northern transect this appears

at 2-3 km, on the middle transect at 1-2 km and on the southern transect from 3-5 km from the

reef. On the southern transect, the water between this zone of elevated levels and the reef

exhibits decreased levels of DIN compared to the rest of the values.

In addition, the concentrations found in the lagoon waters are higher than the values observed

at the 1 km stations on the transects, with comparable values to the offshore stations on the

southern transect.

Expressed as molar concentrations, the concentrations of DIN observed in the reef area range

from 3.92 _mol/L to 8.21 _mol/L, with an average concentration of 5.78 _mol/L. The

northern transect has an average of 4.72 _mol/L, the middle transect has an average of 5.67

_mol/L and the southern transect an average of 6.59 _mol/L.

Phosphate concentrations (DIP)

A summary of the DIP data is presented in Table 5. Similar distinctions between surface and

deep waters and between onshore and offshore waters were used as for DIN concentrations.

Also presented are the DIP concentrations from the lagoon stations.


79

The lowest DIP concentration detectable was 5 _g/L, hence values of between 0 and 5 _g/L

are recorded as non-detectable (ND). These values are presented graphically as 0 _g/L.

Table 5: Summary of the DIP concentrations for the transect and lagoon stations

Phosphate (_g/L)Location

Minimum Maximum Mean Standard DeviationAll stations ND 10.00 4.39 3.21

Northern transect ND 10.00 4.17 3.26Middle transect ND 10.00 4.00 3.04

Southern transect ND 8.00 3.94 3.32Surface 20 m ND 8.00 3.13 2.95Below 20 m ND 10.00 5.21 3.05

Onshore - 3km or less from reef ND 8.00 3.35 3.01Offshore - 4km or more from reef ND 10.00 4.66 3.19

Lagoon stations 6.00 10.00 7.67 1.51

The data indicates that there is a wide range of DIP concentrations present throughout the

sampling area, which vary with depth, with distance from the reef and between transects.

There appears to be little qualitative difference in DIP concentrations between the transects.

The data indicates that the deeper waters contain a higher concentration of DIP than the

surface waters and the offshore waters contain a higher concentration than the onshore waters

(although this difference is qualitatively very small). The data also indicates that the lagoon

waters contain higher levels of DIP than the transect waters.

0

20

40

60

80

100

120

140

0 2 4 6 8 10 12Phosphate (ìg/L)

Dep

th (

m)


Figure 27: Comparison of DIP concentration profiles for offshore and lagoon stations


80

The values for DIP exhibit different trends to those for DIN. Firstly the graph confirms that

the range of observed values is fairly constant across the three transects (as indicated in Table

5), with low values ND and high values of 7 – 10 _g/L observed on all three transects.

The stations at 10 km on the three transects show an increase in values with depth, with the

maximum values at these stations reached at the sediments: 10 _g/L on the northern and

middle transects and 6 _g/L on the southern transect. The surface waters at this station are

lower in DIP on the middle and southern transects (recording ND values) but relatively high

in the northern (with 6 _g/L). The values of DIP are generally qualitatively high across the

bottom of the water column, compared to the rest of the water column, between 1 km and 5

km from the reef across all three transects, with values of between 5 and 8 _g/L.

On each transect there is a zone of qualitatively elevated levels of DIP (between 5 and 8

_g/L), located: between 2 km and 5 km from the reef at 20 – 40 m depth on the northern

transect, between 1 km and 5 km from the reef at 25 – 50 m depth on the middle transect, and

between 2 km and 5 km from the reef, from the surface to the sediments on the southern

transect. These areas of higher DIP levels are observed at approximately the same location on

each transect – around the point where the seabed slopes away from the shallower to the

deeper offshore waters – but seem to increase in size from north to south.

As with the DIN concentrations, the DIP profiles indicate that the lagoon waters contain

relatively high concentrations compared to the offshore water, between 6 and 10 _g/L.

Expressed as molar concentrations, the values of DIP observed in the reef area range from 0

_mol/L to 0.32 _mol/L, with an average value of 0.14 _mol/L, similar on each transect.

Comparison of nitrogen to phosphorous concentrations

The ratio of nitrogen to phosphorous as observed in open ocean water is generally assumed to

be close to 16:1 (expressed as _mol/L), called the Redfield ratio (Redfield et al. 1937, in

Johannes 1964). This ratio has been plotted in Figure 28 along with the concentrations of DIN

and DIP observed in the sampling area.


81

[Nitrate/nitrite] vs [Phosphate], comparison with Redfield Ratio of 16:1

0123456789

0 0.1 0.2 0.3 0.4

[Phosphate] (ìmol/L)

[Nit

rate

/nit

rite

] (ì

mo

l/L)

[Nitrate/nitrite] and [Phosphate] at each station Redfield Ratio 16:1

Figure 28: Comparison of DIN and DIP concentrations with Redfield ratio for ocean waters

The figure indicates the ocean waters around Ningaloo Reef contain concentrations

qualitatively very different to the Redfield ratio, with higher levels of DIN compared to DIP

observed in the study area. The ratio of the concentration of DIN to DIP averages 24:1 on the

northern transect, 29:1 in the middle transect and 32:1 on the southern transect.

Chlorophyll a

A summary of the chlorophyll a data is presented in Table 6. There was very little difference

between classifying the ‘surface waters’ as 1 m or 20 m, and in distinguishing the ‘onshore’

waters as within 3 km, 4 km or 5 km from the reef. The tabulated data is presented using the

surface 20 m of water as ‘surface waters’ and within 3 km of the reef as ‘onshore waters’.

Table 6: Summary of the chlorophyll a concentrations for the transect and lagoon stations

Chlorophyll a (_g/L)Location

Minimum Maximum Mean Standard DeviationAll stations 0.03 0.51 0.18 0.08

Northern transect 0.06 0.51 0.19 0.11Middle transect 0.07 0.28 0.19 0.06

Southern transect 0.11 0.30 0.20 0.05Surface 20 m 0.06 0.26 0.18 0.05Below 20 m 0.07 0.51 0.22 0.09

Onshore - 3km or less from reef 0.13 0.29 0.22 0.04Offshore - 4km or more from reef 0.06 0.51 0.18 0.09

Lagoon stations 0.12 0.17 0.15 0.02


82

The data indicates that there is very little qualitative difference between the chlorophyll a

concentrations on the three transects, with a marginally higher mean concentration present in

the southern transect but a higher maximum value observed in the northern transect. The data

also indicates that there is a higher concentration of chlorophyll a in the deeper waters than in

the surface 20 m of the water column. Additionally, on average there is more chlorophyll a in

the onshore waters than the offshore, despite the presence of a higher maximum in the

offshore waters.

0

20

40

60

80

100

120

140

0 0.05 0.1 0.15 0.2 0.25 0.3 0.35

Chlorophyll a (ìg/L)

Dep

th (

m)


Figure 29: Comparison of chlorophyll a profiles for offshore and lagoon stations

Figure 29 indicates that there appears to be a general increase in the levels of chlorophyll a

from north to south. While there are areas within the northern and middle transects that

display levels of chlorophyll a comparable to the southern transect, the average values

observed throughout the water column appear to increase from north to south.

At the 10 km station on each transect, there is a maximum of chlorophyll a reached at about

70 m depth of between 0.22 and 0.301 _g/L. Generally the surface waters on each transect

exhibit lower levels of chlorophyll a, from 0.062 to approximately 0.2 _g/L.

On each transect there is an observable zone of qualitatively high chlorophyll a concentration

(between 0.2 and 0.28 _g/L): on the northern transect this is between 1 km and 4 km from the

reef and from the surface or 20 m to 40 m depth, on the middle transect from 1 km and 4 km


83

from the reef and 20 – 40 m depth, and on the southern transect from 1 km to 3 km from the

reef and 30 – 40 m depth.

The lagoon waters display values of chlorophyll a concentrations between 0.12 and 0.17

_g/L.

5.3 STABLE ISOTOPE RATIO SAMPLING

5.3.1 WATER SAMPLES

The _13C and _15N values in the water samples were shown to be spatially variable, thus the

data has been presented according to different physical regions. These regions are shown in

Figure 30, as a diagrammatic cross-section through a transect. Site A refers to the majority of

the water offshore from the reef. Site B represents the water associated with the observed

zone of elevated DIN values closer to the reef, as described in Section 5.2. Site C is the water

associated with the observed zone of elevated chlorophyll a values found approximately 3 km

from the reef, as described in the previous section. Site D represents the waters found deep

offshore, towards the bottom of the water column at the 10 km stations on the three transects.

Figure 30: Regions used for presentation of summary stable isotope ratios from water sampling

_13C stable isotope values

The data from each of the regions identified above are summarised in Table 7. Also shown in

the table are the _13C values for the lagoon waters, which will be referred to as Site E.

Site DSediments

Surface

Site A Site B

Site CReef

Offshore


84

Table 7: Summary of _13C values for the transect and lagoon stations

_13C (‰)Region Site Description

Minimum Maximum MeanStandardDeviation

Site E Lagoon stations -23.06 -18.00 -19.80 1.99Site D Deep offshore waters -23.95 -21.38 -22.82 0.98Site C Near patch high chlorophyll a -17.84 -13.27 -16.76 1.61Site B Near patch high DIN -25.16 -13.27 -22.26 1.50Site A Rest of transect water -24.53 -18.40 -22.21 1.18

Site E shows similar _13C values to Site D, however the range of values observed in Site E is

larger than in Site D. Site E exhibits _13C values of between –18 and –23 ‰, while Site D

shows _13C values of between –21 and –24 ‰. Site C contains qualitatively very different

_13C values to the rest of the sites, of between –13 and –17 ‰. Site B mostly contains _13C

values of between –20 and –23 ‰, with two samples containing _13C values of –13 and –17

‰. The samples displaying these values also overlapped with Site C on the northern transect.

Site A contains values close to –21 to –22‰.

_15N stable isotope values

The data from each of the regions described above are summarised in Table 8. Also shown in

the table are the _15N values for the lagoon waters, which will be referred to as Site E.

Table 8: Summary of the _15N values for the transect and lagoon stations

_15N (‰)Region

Site DescriptionMinimum Maximum Mean

StandardDeviation

Site E Lagoon stations 3.22 6.13 5.01 1.10Site D Deep offshore waters 3.58 7.66 5.73 1.70Site C Near patch high chlorophyll a 3.17 7.91 5.22 1.85Site B Near patch high DIN 5.50 9.79 7.49 1.28Site A Rest of transect water 1.41 6.29 4.25 1.03

This data shows that Site E and Site D have very similar _15N values, similarly to the _13C

values. The Site E values range from 3 to 6 ‰, while the Site D values range from 3.5 to 7.5

‰. Site C displays similar _13C values, with a slightly higher maximum of 7.9 ‰. Site B

displays qualitatively very different _15N values, with a higher mean (of 7.5 ‰) than the rest

of the sites, and a relatively higher range (5.5 to 9.8 ‰). Site A displays a slightly lower mean

than the rest of the sites (with a mean of 4.2 ‰), and the lowest minimum is observed in Site

A (of 1.4 ‰).


85

5.3.2 REEF SPECIMENS

The stable isotope values of _13C and _15N for the reef organism specimens are presented in

Table 9 and Table 10. To allow for easy visual comparison, the specimens have been grouped

into: reef fishes – small and less mobile fish (5 specimens), piscivores – larger and more

mobile fish (4 specimens), seaweed (4 specimens), sea cucumbers (3 specimens), crayfish (1

specimen) and oyster (1 specimen). Data was not received for the remaining 8 out of the

original 26 specimens.

The species identifications for each of these specimens is presented in Appendix 10.3, along

with the members of the sample groups used for analysis as shown in Tables 9 and 10.

Table 9: Summary of the _13C ratios analysed from the reef organism specimens

Samples _13C (‰) Minimum Maximum Mean Standard Deviation

Piscivores (4 specimens) -19.02 -12.29 -16.65 2.99Reef fish (5 specimens) -13.30 -12.02 -12.68 0.59Seaweed (4 specimens) -21.44 -15.18 -17.32 2.83

Sea cucumbers (3 specimens) -16.73 -8.85 -13.00 3.96Crayfish (1 specimen) N/A N/A -14.37 N/AOyster (1 specimen) N/A N/A -14.88 N/A

Table 10: Summary of the _15N ratios analysed from the reef organism specimens

Samples _15N (‰) Minimum Maximum Mean Standard Deviation

Piscivores (4 specimens) 6.53 9.41 8.43 1.31Reef fish (5 specimens) 5.00 6.79 5.84 0.80Seaweed (4 specimens) 2.30 4.70 3.52 1.09

Sea cucumbers (3 specimens) 3.48 7.68 5.88 2.17Crayfish (1 specimen) N/A N/A 5.96 N/A Oyster (1 specimen) N/A N/A 4.39 N/A

This data is also presented graphically in Figure 31. Shown for comparison purposes in Figure

31 are the average values of these isotope ratios for Site D, Site B and Site A (as described in

Section 5.3.1). For each of the categories in Figure 31, the mean value has been displayed by

a coloured marker, with error bars around the mean indicating one standard error either side.

Standard error was calculated as the standard deviation for a group divided by the square root

of the number of samples in that group. Using standard error gives an indication of the

variation of the values within a group based on the sample size. Also displayed on Figure 30

are coloured lines encircling sample groups into broader groups. The significance of these


86

groupings and a comparison of the reef specimens ratios with the water samples are discussed

in Chapter 6.

Figure 31: _13C and _15N stable isotope ratios, for reef specimens and various water sampling locations

The data indicates that the seaweed have a wide range of _13C values of between –15 and –21

‰, averaging around –17 ‰, with a narrower range of _15N values of between 2 and 4 . The

sea cucumbers display a wide range of both _13C and _15N values: _13C values of between –8

and –16 ‰ and _15N values of between 3 and 7 ‰. The piscivores display a similar range of

values, with _13C values varying from –12 to –19 ‰ and _15N values varying from 6 to 9 ‰.

Compared to these data, the reef fish display a relatively narrow range of isotope values, with

_13C values of –12 to –13 ‰ and _15N values of 5 to 6.5 ‰. The crayfish and oyster display

isotope ratios that fall within the above ranges: _13C values of –14.3 ‰ for the crayfish and

–14.8 ‰ for the oyster, and _15N values of 5.9 and 4.4 for the crayfish and oyster

respectively.

ä13C versus ä15N for reef and water isotope signatures

0123456789

10

-25 -20 -15 -10 -5 0

ä13C

ä15N

Piscivores Reef fish SeaweedSea cucumbers Crayfish OysterDeep offshore Node high chlorophyll Rest of offshore

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study Discussion

87

6 D I S C U S S I O N

6.1 LOCAL OCEANOGRAPHIC ENVIRONMENT

There are some major findings from the water sampling that help to characterise the offshore

environment of Ningaloo Reef. These are: 1) the upwelling occurring from offshore to

onshore in the vicinity of the reef, and associated nodes of high productivity caused by the

upwelling of nutrients from the sediments; 2) the north to south gradients that are apparent in

the sampling area; 3) the effects the reef has on the surrounding waters by filtering nutrients

from the incoming ocean water and exporting material both to the ocean and to the lagoon;

and 4) the anomalous occurrence of the colder, more saline water in the channel pass.

The relatively small standard deviations from the mean of _13C values for each water

sampling location (as described in Section 5.3.1) suggest that these different areas are in fact

distinct in the processes occurring within them.

As an aside, the lower values (around 1.4 and 2 ‰) observed in the surface of the offshore

waters are suggestive of nitrogen fixation, while _15N values of around 3 or 4 ‰ are

consistent with phytoplankton and primary producers in nitrate-rich waters (Minagawa and

Wada 1986) (which these waters appear to be). Therefore the _15N values observed in the

offshore waters are consistent with knowledge of these ratios in open ocean waters.

6.1.1 UPWELLING

The upward tilting of the temperature and salinity contours towards the shore indicates

advection of colder, more saline water from the deep waters offshore towards the shallower

waters closer to the reef, which suggests the presence of upwelling in the near vicinity of the

sample section of Ningaloo Reef. The higher salinity values persist into the waters nearer the

reef, between 1 km and 3 km from the reef; while the cooler temperatures are not observed

closer than 5 km from the reef, this could be due to warming of the upwelled waters due to

solar heating over the relatively shallower water column. This pattern of higher salinity closer

to the reef at about 40 m depth could explain why the averages of salinity values from the

surface waters were approximately equal to the averages from the bottom waters (as indicated

in Table 2).

The salinities observed from the surface to the bottom of the water column in the transect

waters are similar to those seen by Woo and Pattiaratchi (2003), however the temperatures

observed are generally warmer, on the order of 2 – 3 oC. Because Woo and Pattiaratchi’s

(2003) data was collected in November, while this data set was compiled in May, the


88

warming of ocean water over the summer period could explain the difference in temperature

range. The deeper water with a signature that is colder and more saline than the surface waters

is suggestive of an origin in the Ningaloo Current, while the warmer and less saline surface

waters are suggestive of the Leeuwin Current (Woo and Pattiaratchi 2003). Therefore this

data provides strong indication of upwelling near Ningaloo Reef due to the interaction

between these two currents.

Offshore Deep Chlorophyll Maximum

There is a gradient of increasing concentration of DIN and DIP with increasing depth at the

10 km stations on all three transects, indicating the nutrient-rich nature of the deeper waters.

The deep offshore waters (Site D from Section 5.3.1) are shown to be a nutrient-rich area, due

to the congregation in this region of material settling out from the water column. This

environment could support increased productivity. This region displays a range of values

typically associated with both primary productivity (–21 to about –23‰, due to the presence

of the deep area of elevated chlorophyll a concentrations) (Vizzini et al. 2002) and

decomposing and settling material, typical of deeper waters (Owens 1987).

At the 10 km station on all three transects, there is a node of high chlorophyll a

concentrations at a depth of about 70 m, which intersects with the areas of high nutrients

found at the sediments of these stations. These data are consistent with the presence of an

offshore deep chlorophyll maximum. This is an area commonly found in deeper waters,

exhibiting higher levels of chlorophyll a coinciding with the intersection of benthic nutrients

and the extent of the photic zone, providing an opportunistic location for primary production

(Hanson 2003).

Similarly high values to this zone are not observed at the bottom of the stations located 4km

and 5km from the reef, indicating that this zone is not omnipresent but a feature of the deeper

waters. However, it is still possible that the production from this zone could be advected

towards the reef and serve as a source of nutrients.

Zones of Increased Productivity

The contours of DIN concentration show upward tilting towards the reef in the middle and

southern transects, with the most pronounced tilting of contours in the southern transect,

showing that the upwelling process is also bringing nutrient-rich water towards the reef. The


89

area of high DIP located towards the bottom of the water column between 3 km and 10 km

from the reef further confirms the occurrence of this process.

On the northern and middle transects, the zone of high chlorophyll a intersects with the areas

of elevated DIN and DIP, contains _13C values of between –13 and –17 ‰ and exhibits lower

levels of dissolved oxygen. These _13C values (of around –17‰) are typically associated with

both primary producers, such as diatoms (Achituv et al. 1997), and secondary producers,

grazers on primary producers (Vizzini et al. 2002). Therefore the data indicates this is an area

of both primary and secondary and production (with similar stable isotope values to those

observed by Minagawa and Wada (1986) and Yamamuro et al. (1995)) located at the

intersection of upwelling of nutrients and the shallower water column, where the availability

of light for photosynthesis increases.

On the southern transect the zone of high chlorophyll a is further onshore than either of the

high nutrient zones, does not contain the same low levels of dissolved oxygen and the _13C

values are similar to those observed offshore of about –21 ‰. However this does not mean

that the peak of chlorophyll a is not due to the upwelling of nutrients, as a value of –21 ‰

indicates primary productivity in ocean waters (Vizzini et al. 2002). Thus the data could just

suggest that the peak of chlorophyll a on the southern transect is comprised only of primary

producers and not secondary producers or grazing organisms.

The zones of high chlorophyll a concentrations are located approximately at the same position

on each transect, although the zone becomes less pronounced from north to south as the

average levels of chlorophyll a observed throughout the transect increase. On all three

transects, this patch of elevated chlorophyll a concentration occurs at the onshore limits of the

zone of high DIP concentrations and could suggest the peak is a response to upwelling of

nutrients. On the northern and middle transects this zone happens to coincide with the zone of

high DIN concentrations, however on the southern transect the zones of high DIN and DIP

concentrations both lie slightly offshore from the zone of high chlorophyll a. It is unclear

whether this suggests the presence of high chlorophyll a is independent of the location of the

DIN or whether it is still a response to the upwelling nutrients. However, following the trends

from the northern and middle transects, it is likely to be a response to upwelling.

Because the material generated in this area does not appear to be advected in large quantities

towards the reef (indicated by the localised nature of the chlorophyll a peak), it is possible

that the material found in this area has become trapped, as observed by Hata et al. (1998).


90

However, because sampling only occurred once, it is unknown whether this peak of

chlorophyll a is transient. The creation of a time-series of chlorophyll a concentration data in

the onshore waters would clarify this point.

Therefore the data shows that upwelling impacts productivity in the very near vicinity of the

reef. It is possible that this productivity is advected towards the reef and could be a nutrient

source for the reef.

6.1.2 NORTH TO SOUTH GRADIENTS

The data shows a clear gradient of increasing DIN and (generally) chlorophyll a concentration

from north to south. As described in Chapter 5, across the northern transect, the ratio of DIN

to DIP averages 24:1, across the middle transect, this ratio increases to 29:1, and on the

southern transect the average ratio is 32:1, indicating a proportional increase in DIN from

north to south. The observed gradients could possibly be explained by the upwelling process

mentioned above having a north-south direction as well as an offshore to onshore direction,

influenced by the local bathymetry (with the southern transect being relatively shallower than

the other two), bringing nutrients from the northern part of the sampling region to the

southern and thereby enhancing productivity in the southern part.

However, if this process were occurring, a concurrent advection of cooler and more saline

water into the southern region would also be expected (as upwelled water would be cooler

and more saline (Woo and Pattiaratchi 2003)). Instead, the southern transect is observed to

contain warmer water than seen elsewhere and only moderate salinity levels compared to the

other two transects. Also, the surface waters of the southern transect exhibit lower dissolved

oxygen concentrations than elsewhere, however the upwelling from the Ningaloo Current is

associated with higher levels of oxygen. There would also be an expected increase in DIP

associated with the increase in DIN were upwelling occurring in this fashion.

The data collected instead suggests that the prediction made by Taylor and Pearce (1999) is

correct: there is a recirculation of water just south of Point Cloates. This recirculation causes

advection of Leeuwin Current water, which is warmer and generally less saline than the

Ningaloo Current, back up the coast by re-joining the Ningaloo Current. This would make the

southern part of the sampling region warmer by comparison and explain the advection of

water low in dissolved oxygen. However this recirculation does not necessarily explain the

higher DIN levels observed in the southern part.


91

The reef section that was the base for the transect and lagoon sampling in this study ends at

the southern end of Point Cloates, roughly at the same latitude as the 10 km station on the

southern transect. It is possible that lagoon water containing enriched levels of nutrients (see

also the sections below on Effect of Reef and Channel Pass) is exiting through this reef break

to flow back out to the ocean, as many researchers have shown that lagoon water exits to the

ocean through the reef breaks (e.g. Hearn et al. 1986). If this process is occurring, taken in

combination with the possibility of a recirculation pattern, the lagoon water could be advected

back around to the front of the reef section, therefore causing the enhanced nutrient and

productivity levels seen in the southern part of the sampling region. This mechanism would

also explain the slightly heavier _15N signature observed in the southern offshore waters

compared to the northern and middle transects, because of the heavier signature observed in

the lagoon waters from the wide variety of material.

Therefore the north to south gradients observed could be explained by the simultaneous

occurrence of multiple processes – a recirculation of Leeuwin Current water into the Ningaloo

Current and export of lagoon waters into the offshore ocean water.

6.1.3 EFFECT OF REEF ON SURROUNDING WATER

Export to Lagoon

The values of DIN in the lagoon waters are qualitatively higher than any of those found in the

1 km stations on any of the transects, indicating an export of DIN from the reef to the lagoon.

Export of nitrogen from a coral reef to the lagoon has also been observed in other studies (e.g.

Odum and Odum 1955, Webb et al. 1975, Crossland 1983). The values of DIP in the lagoon

are also qualitatively higher than those in the front of the reef. There is a decrease in DIP

concentration in the lagoon waters from north to south, however this is a relatively small

decrease considering the range of values displayed in the offshore stations, and therefore may

not be significant. The chlorophyll a levels observed in the lagoon in this study were mid-

range, indicating that the material being exported to the reef is not necessarily based on

primary producers but could also contain secondary producers, such as zooplankton, and

recycled and excreted material.

The lagoon waters (Site E from Section 5.3.1) have been shown above to contain a variety of

material exported from the reef, which is confirmed by the isotope ratios. These ratios are

suggestive of primary productivity (which would range from –21 to about –23‰ (Wada 1980

and Vizzini et al. 2002)), secondary production (which would range from –11 to about –22‰


92

(Vizzini et al. 2002)) and general particulate matter (which can range from –18 to about

–23‰ (Yamamuro et al. 1995)). It therefore appears that there is an export of a wide variety

of material from the reef to the lagoon.

Export to Ocean

Many studies have estimated that coral reefs have a net production of organic material, some

of which is suggested to be exported from the reef to the open ocean (Hata et al. 1998). Other

studies have actually measured an export of organic particles from a reef to the surrounding

ocean (e.g. Johannes 1967).

The observed behaviour in this study of upwelling leading to increased productivity closer to

the reef does not seem to explain the existence of the area of high DIN observed in the

onshore waters. On the northern transect, the values of DIN observed between 2 km and 3 km

from the reef are higher than seen anywhere else on the transect (including the bottom of the

10 km station), and on the middle and southern transects there is a relative decrease in DIN

between the offshore waters and the area of high DIN closer to shore, indicating that it exists

independently of the upwelling. Additionally, the area of high DIN overlaps with an area of

heavier _15N values (between about 6 and 8 ‰) on each transect, which is not observed

anywhere else between the reef and the 5 km stations. These heavier signatures are usually

indicative of secondary producers (Vizzini et al. 2002), and therefore such a concentration of

these organisms is unlikely to be sourced from the open ocean waters.

It is possible that these high DIN concentrations and _15N values are due to an export of

material from the reef, as has been observed elsewhere (e.g. Erez 1990). It has been suggested

that a localised internal wave, propagating along the interface between two water layers of

different densities, can pull material from a coral reef along with it in an offshore direction

(Koseff 2003). The _15N values associated with the region are indicative of particulate matter,

secondary producers and decomposing material (Owens 1987, Vizzini et al. 2002 and

Yamamuro et al. 1995). This shows that the export of material from the reef to the ocean

could be composed of a variety of material. The data therefore indicates that the reef is also

affecting the onshore waters (as well as the lagoon waters) by export of various materials.


93

Filtering effect of the reef

There is a decrease in DIP levels between 1 km and 3 km from the reef, on all three transects.

Also, between the node of high DIN levels and the reef on the southern transect (at the station

1km from the reef), the DIN levels are decreased, displaying lower values than observed

elsewhere on the transect. These lower DIN and DIP concentrations are not visibly associated

with a chlorophyll a peak, suggesting that these low levels could be due to a filtering effect of

the reef producers on the ocean water. Potentially the observed decrease in nutrients could be

due to offshore plankton taking up the nutrients immediately adjacent to the reef, however the

chlorophyll a peak observed near the bottom of the water column at about 3 km from the reef

is removed from the reef itself, suggesting that the decrease in nutrients closer to the reef is

attributable to the reef producers. Therefore this observation provides evidence that the

nutrients provided by the ocean waters are used by the reef organisms.

6.1.4 CHANNEL PASS

The data obtained from within the channel pass to the north of the transect sampling area

indicates the water located there originates from deep waters offshore. While this water has

similar temperatures to the bottom of the 10 km stations on the northern and middle transects,

it is significantly more saline and contains lower levels of dissolved oxygen, therefore is

unlikely to have originated from the same deep water upwelling as the transect stations. This

finding corroborates with the work of Simpson and Masini (1986), who found advection of an

unusually cool water mass into the lagoon at certain times, including during May (i.e. the

same time of year as this study was undertaken).

It was experientially observed that the bathymetry around the channel was relatively steep

compared with the surrounding area, with the channel being 10 m deep and approximately

500 m wide. This allowed ship traffic into the channel, but the shallow nature of the reef on

either side of the channel required a wide berth. This would suggest the channel has an almost

dredge-like nature, and could explain why water from offshore would be preferentially drawn

into the channel.

Hearn et al. (1986) suggested that the presence of the unusually cold water mass observed in

the lagoon by Simpson and Masini (1986) could be due to upwelling caused by an internal

wave, emanating from the North West Shelf area further offshore. The authors suggested the

upwelled water was advected into the lagoon due to tidal action over the reef flat during high

tide. However, this study suggests otherwise. If the upwelled water were being advected over


94

the reef flat, it would have been observed to some extent on the front side of the reef in the

transect stations, but the water in front of the reef was warmer than the channel water and

consistent with the known patterns of Leeuwin and Ningaloo Currents (Woo and Pattiaratchi

2003). Therefore, while the suggestion of upwelling caused by an internal wave is still

feasible, it is more likely that the water is being advected into the lagoon via the channel pass

between reef sections. The cold lagoon water observed by Simpson and Masini (1986) could

therefore have come from alongshore circulation within the lagoon, with one end of a reef

section acting as an inflow channel and the other end acting as an outflow channel.

Therefore in the case of the lagoon sampled in this study, it is possible that cold water is being

advected into the lagoon through the channel pass at the northern end of the lagoon, is

circulating in an alongshore direction (north to south) and then exiting the lagoon at the

southern end, whereupon it is recirculated with the ocean water as described above. This

circulation would therefore be in the reverse direction to that suggested by Hearn et al. (1986,

see Figure 4).

In summary, the oceanographic environment around the sampled section of Ningaloo Reef is

highly complex. A speculative summary representation of this discussion is shown in Figure

32.

Figure 32: Speculative representation of oceanographic environment around sampled section of NingalooReef

LAND

RE

EF

SEC

TIO

N

CHANNELUpwelling into channelfrom internal waveoffshore

Recirculation ofLeeuwin Currentwater to front of reef

Lagoon water exiting toocean, brought back tofront of reef

Water advectedtowards reef from

offshore


95

6.2 NUTRIENT SOURCES FOR THE REEF

Discussion of individual reef specimen groups

The isotope ratios observed in the seaweed group are consistent with the values found by

Vizzini et al. (2002) and Fry et al. (1982). The seaweed’s _15N values are indicative of

nitrate-rich waters, as discussed previously in Chapter 3.

The oyster, with a slightly higher value of both _13C and _15N, indicates its filter feeding

nature. Because _15N values of a consumer are removed from their prey by an elevation of

about 3, a _15N value of about 4.5 ‰ suggests the oyster is feeding on material with a _15N

value of about 1.5 ‰, indicative of nitrogen-fixing phytoplankton (Minagawa and Wada

1986). The _13C value of about –15 ‰ is suggestive of secondary producers, which could be

microzooplankton (Vizzini et al. 2002). Therefore these values suggest the oyster is filtering a

variety of smaller particles from the water column.

With a _15N value of about 6 ‰, the data suggests that the reef fish are feeding on material

with a _15N value of about 3 ‰. Combined with the _13C value of about –12 ‰, this data

indicates the fish are grazing on a possible combination of seaweed and algae, primary

producers and secondary producers (Fry et al. 1982 and Vizzini et al. 2002). The narrow

range of values observed in the reef fish is indicative of their narrow feeding range, being

restricted to smaller sections of the coral reef due to the their small size.

The sea cucumbers display a wide range of _13C and _15N values, which is to be expected

given their habitat: as sediment dwellers, the sea cucumbers graze upon whatever material is

found on the benthos, which could incorporate a range of settling and decomposing matter.

With a _13C average of about –12 ‰ and a _15N average of about 6 ‰, the data confirms that

the sea cucumbers could be feeding on detrital matter, settling primary or secondary

producers or decomposing organic matter (Vizzini et al. 2002 and Owens 1987).

The crayfish exhibits a _15N value of about 6 ‰ and a _13C value of about –14 ‰, indicating

it feeds on mainly secondary producers, such as small zooplankton (Vizzini et al. 2002).

The piscivores display a much higher _15N value of about 9 ‰, with a range of _13C values

between –12 and –19 ‰. This data indicates the piscivores are feeding on organisms with a

_15N value of about 6 ‰, predominately smaller fish, and the _13C and _15N values combined

indicate the food source for the piscivores also includes secondary producers, possibly large


96

zooplankton (Fry et al. 1982). The relatively wide range of values shown for the piscivores is

indicative of their larger range of feeding grounds being able to swim between the open ocean

waters and the reef system and therefore feed on a wider range of material (Fry et al. 1982).

Groupings of reef specimens and water sampling regions

From the reef specimens’ and water sampling regions’ isotope signatures, several patterns can

be discerned regarding nutrient sources within the coral reef. Because the observed values

have been shown above as comparable with those in the literature, reasonable confidence can

be placed in them as representative of their groups.

The clustering of groups of signatures into similar areas indicates the relative spatial position

and influence of offshore versus reef waters for nutrient supply. This clustering refers to the

red, green and blue circles drawn around groups on Figure 31.

The isotope ratios of the offshore waters, including the deep offshore waters (Site D from

Section 5.3.1) and rest of offshore waters (Site A from Section 5.3.1), contain the lowest of

the δ13C values and show the relative isotopic position of the offshore marine signature. This

can be seen by the position of the red circle in Figure 31, which is distinct from the green and

blue circles.

The seaweeds, piscivores and onshore water associated with the zone of elevated chlorophyll

a concentrations (Site C in Section 5.3.1) all contain similar δ13C values, as seen by the blue

circle in Figure 31. While the seaweed was sampled from within the reef system, this kind of

seaweed could be expected to be presented in the waters on the front side of the reef, and also

would be expected to contain similar isotopic ratios to the onshore water and piscivores

because the seaweed would be feeding on the same nutrient sources (i.e. photosynthesis and

uptake of inorganic nutrients). Therefore these three groups represent the δ13C signature of the

onshore waters: those ocean waters located just to the front side of the reef. The increase in

δ15N values between the seaweed, area of productivity and the piscivores indicates the trophic

level increase, from primary producer, to secondary producer and finally to carnivore.

The crayfish, sea cucumbers and smaller reef fish appear to all be clustered around similar

isotopic ratios, both for δ13C and δ15N (shown by the green circle on Figure 31). For the

crayfish and reef fish, the δ15N values indicate their feeding habits on various plankton (as


97

described above), and their similar δ13C values suggests these plankton are coming from the

same source, most likely zooplankton within the reef system. The wide range of values

observed for the sea cucumbers shows their feeding on a wide range of material, but the way

their isotopic ratios are similar to the crayfish and reef fish suggests their feeding material is

also similar. Therefore these three groups appear to illustrate the isotopic signature of the

internal reef system. It is worth noting that the δ13C ratio for these organisms is similar to that

observed in corals (Heikoop et al. 2000), possibly indicating these organisms are also feeding

on excreted coral material, although further investigation would be required to confirm this.

Finally, the oyster appears to have an isotopic signature between the onshore waters

(illustrated by the blue circle on Figure 31) and the internal reef system (shown by the green

circle on Figure 31). Because the oyster is a filter feeding organism, and therefore would be

taking a range of particulate matter from the water column being advected past it, this shows

the influence of both the oceanic water and internal reef system for providing nutrients for the

reef. Although without further data any conclusions are only speculative, it could be expected

that similar filter feeding organisms (like sea urchins, starfish and molluscs such as clams)

would display similar characteristics.

Differences between DIP and DIN for reef

The values of DIN observed on the transects are at the upper end of the range or higher than

those observed at the Abrolhos Islands (to the southwest of Ningaloo Reef), and are a little

higher than those observed in average temperate waters (Crossland 1983), indicating higher

levels of DIN in the vicinity of Ningaloo Reef. However, the values of DIP are similar to

those observed at the Abrolhos Islands but at the lower end of the range, and within the

expected range for tropical waters (Crossland 1983), suggesting the open ocean in the vicinity

of Ningaloo Reef is oligotrophic in nature. Comparison of DIN to DIP concentrations

suggests that the waters around Ningaloo Reef would be limiting in phosphate relative to

nitrate (this comparison also confirms the increasing relative abundance of nitrate compared

to phosphate from north to south in the sampling area).

The observed differences between the within-transect and between-transect trends of DIN and

DIP in the waters in front of the reef suggests that the processes governing the cycling of DIN

in these waters are not strictly coupled with the processes governing the cycling of DIP.


98

Although there is strong evidence of an export of DIN-associated material from the reef

towards the ocean, it appears that DIP is not being exported in the same way. Thus the DIP

that is advected towards the reef appears to be filtered by the reef organisms, and any DIP

obtained is efficiently stored in some form by the reef, with some amount of DIP being

exported to the lagoon waters behind the reef. Conversely, it appears that although DIN is

also filtered from the incoming ocean water by the reef, it is exported after use both towards

the ocean and towards the lagoon. This could indicate that DIP is more tightly held by the reef

system than DIN, through recycling and storage processes (as suggested by Pomeroy 1970

and Atkinson 1981), possibly due to its relatively lower concentrations in the ocean water.

The data presented in Figure 28 indicate that the limiting nutrient in these waters would be

phosphorous, a condition necessitating the efficient use and storage of phosphorous by the

reef as suggested by Atkinson (1981).

Additionally, the ratio of DIN to DIP concentrations increases from the northern transect to

the middle and southern transects, with average ratio values of 24:1, 29:1 and 32:1

respectively. This increase could possibly be explained by the concurrence of two processes:

firstly the relative storage of DIP and export of DIN from the reef, and secondly the

circulation patterns as described above, which advect lagoon water back around to the front of

the reef. These two processes acting together would bring exported DIN from the lagoon to

the front of the reef in the region of the southern transect, therefore increasing the apparent

DIN:DIP ratio without increasing the observed values of DIP.

One other possible explanation for the relatively high values of DIN observed throughout the

sampling area (compared to the values found by Crossland (1983)) is that there has been a

build-up in the local waters over time of DIN due to the reef’s export of this nutrient to the

ocean, as described above. With the incoming DIP appearing to be held more tightly by the

reef system, exports of DIN over a long period of time (even if sporadic) could cause the

observed ratio of DIN to DIP in the sampling area.

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study Conclusions

99

7 C O N C L U S I O N S

The local oceanography around Ningaloo Reef, from Norwegian Bay to just south of Point

Cloates, is very complex and consists of multiple water bodies mixing and recirculating. This

means that the area of influence for the reef is both very large, incorporating deep offshore

waters, and spatially and temporally variable. The seasonal relative strengths of the Leeuwin,

Ningaloo and local currents due to changing wind stress will significantly impact the water

influencing the reef by adjusting the relative proportions of water coming from each source

towards the reef.

These complex physical interactions are providing oceanic sources of nutrients to the reef,

however it is still uncertain how much each water mass is contributing to the reef and over

what time scale. These findings are very important for management considerations for the

reef, as activities undertaken within the water bodies that are identified as influencing the reef

could also impact on the reef, for example by the advection of pollution or by interfering with

the nutrient sources these waters are providing.

This study has indicated the importance of both the oceanic and internal sources of nutrients

for the reef, however a complete understanding of the nutrient sources and fluxes through

Ningaloo Reef is yet to be achieved, and will most likely be highly variable both temporally

and spatially. The seasonal nutrient requirements of the reef and productivity patterns will

need to be investigated further to better understand these fluxes.

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study Recommendations

100

8 R E C O M M E N D AT I O N S

Several recommendations can be made from the conclusions of this study. Firstly, a more

thorough investigation of the origins of some of the water bodies influencing Ningaloo Reef

is required to fully understand the inputs of nutrients from these sources. To further

investigate the local oceanographic environment, the following recommendations are

suggested:

• The direction and velocity of water movements should be determined in order to

characterise the origin of the water that is seen entering the channel, clarify the flow of

water from the lagoon and observed export of material from the reef towards the

ocean, and determine the exact nature of the recirculation pattern near Point Cloates.

This could be done for example with an ADCP (Acoustic Doppler Current Profiler, an

instrument to measure current velocities) probe attached to a current drogue (a device

that acts as a buoy, being advected with the currents and therefore towing any

instrumentation attached to it).

• In addition, multiple study sites should be sampled to determine if the complexity

observed at the sampling site in this study is common throughout the reef, or is

localised in the area between Norwegian Bay and Point Cloates. A suggested regime

would include at least three reef sections, one located between North West Cape and

Norwegian Bay, one located between Norwegian Bay and Point Cloates (where the

land topography could be influencing offshore processes) and one to the south of Point

Cloates but north of Point Maud (near Coral Bay). The area offshore from Coral Bay

has been studied previously and shown to contain anthropogenic impacts from the

land developments, and therefore this would hinder studies of oceanic sources of

nutrients for the reef. (A study of the relative proportions of inputs from terrestrial and

oceanic sources may be another field of interest.)

• The effect the reef is having on the local waters needs to be further investigated.

Characterisation of material contained in the observed exports from the reef, both to

the ocean and to the lagoon, would enable a better understanding of what exactly the

reef is exporting, and possibly allow further insight as to how the reef is sustaining its

internal nutrient balance by providing observations of what it produces and sends out

of the system. Therefore samples should be taken within this observed area of nitrate

export, on the ocean side of the reef, and in the lagoon waters, and analysed under a


101

dissecting microscope to see what the particulate matter is composed of –

phytoplankton, zooplankton, aggregates of organic matter (including coral mucus) and

decomposing material are all possibilities.

• Sampling regimes should be conducted over a period of time, to discern any temporal

patterns in the observed circulation patterns and also to find out if: the observed node

of increased productivity due to upwelling is advected towards the reef over time; and

also if the export of material from the reef to the ocean occurs over a distinct time

scale. The length of sampling time and regularity of sampling will depend on the

factors attempting to be described, such as seasonal variation, interannual variation or

event-specific variation.

With regard to better understanding the nutrient sources of the reef system, the following

recommendations are made:

• This study has suggested the importance of oceanic inputs of nutrients for coral reefs,

however this area of study still requires a significant amount of research. More

extensive reef specimen sampling should be undertaken for analysis of stable isotope

ratios, which should include both increased numbers of specimens and increased

representation from each trophic level present in the coral reef ecosystem. This will

allow more sophisticated interpretation of the trophic level interactions and nutrient

sources for each trophic level, providing a more sophisticated overall picture of the

reef’s nutrients. It is also very important to include analysis of the corals within the

reef, as this will indicate whether they are primarily autotrophic or heterotrophic in

nature (i.e. relying primarily on nutrient inputs from zooxanthellae or on filter feeding

particulate matter from the water column) and therefore the relative importance of

oceanic water for feeding these building blocks of the reef system.

• As part of a further investigation into nutrient sources of the coral reef, water samples

should also be taken at shorter intervals within 1km of the reef, on both the front and

back sides of the reef, and over the reef system itself, for analysis of similar

parameters to those used in this study. This will show more clearly the effects of reef

export or filtering of nutrients by the reef, and also characterise the water flowing over

the reef, allowing quantification of the productivity of the waters within and directly

adjacent to the reef system.


102

• It appears, from the literature and from this study, that phosphorous (in the form of

phosphate in this study) is used within a coral reef system differently to nitrogen (in

the form of nitrate and some particulate matter). This possibility should be further

investigated, as it will have implications on traditional theories of the limiting nutrient

for primary productivity and therefore the relative importance of safeguarding the

continued inputs of these nutrients for coral reef development.

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study References

103

9 R E F E R E N C E S

Achituv, Y. and Z. Dubinsky. 1990, 'Evolution and zoogeography of coral reefs', In:Dubinsky, Z. (Ed). Ecosystems of the World: Coral Reefs, Elsevier Science Publishers,Amsterdam, pp. 1 - 9.

Achituv, Y., I. Brickner and J. Erez. 1997, ‘Stable carbon isotope ratios in Red Seabarnacles (Cirripedia) as an indicator of their food source’, Marine Biology, vol. 130,pp. 243 – 247.

Aharon, P. and J. Chappell. 1983, 'Carbon and oxygen isotope probes of reef environmenthistories', In: Barnes, D. J. (Ed). Perspectives on Coral Reefs, Brian CloustonPublisher, Manuka, pp. 1 - 10.

Andrews, J. C. and P. Gentien. 1982, 'Upwelling as a source of nutrients for the Great BarrierReef ecosystems: a solution to Darwin's question?' Marine Ecology Progress Series,vol. 8, pp. 257 - 269.

Andrews, J. C. and G. L. Pickard. 1983, 'The physical oceanography of coral reef systems', In:Barnes, D. J. (Ed). Perspectives on Coral Reefs, Brian Clouston Publisher, Manuka,pp. 11 - 46.

Arias-Gonzalez, J. E., B. Delesalle, B. Salvat and R. Galzin. 1997, 'Trophic functioning of theTiahura reef sector, Moorea Island, French Polynesia', Coral Reefs, vol. 16, pp. 231 -246.

Atkinson, M. J. 1981, Phosphate metabolism of coral reef flats, Ph. D. Thesis, University ofHawaii.

Atkinson, M. J. 1987, 'Rates of phosphate uptake by coral reef flat communities', Limnologyand Oceanography, vol. 32, no. 2, pp. 426 - 435.

Australian Institute of Marine Science. (2003), AIMS Research: Whale shark spy-cam,[Online], Available from:<http://www.aims.gov.au/pages/about/communications/backgrounders/20030620-whale-shark-crittercam.html> [13 October 2003].

Ayling, A. L. and A. M. Ayling. 1987, Ningaloo Marine Park: Preliminary fish densityassessment and habitat survey, with information on coral damage due to Drupellacornus grazing, Sea Research, Queensland.

Birkeland, C. 1984, 'Sources and destinations of nutrients in coral reef ecosystems', (Ed).Comparing Coral Reef Survey Methods: UNESCO Reports in Marine Science Number21, United Nations Educational, Scientific and Cultural Organisation, pp. 3 - 10.

Centre for Water Research. (2003a), Protocol for the extraction of photosynthetic pigments,[Online], Available from:


104

<http://www.cwr.uwa.edu.au/services_to_industry/erl/PigmentsBackground.html> [13October 2003].

Centre for Water Research. (2003b), Extraction by grinding, [Online], Available from:<http://www.cwr.uwa.edu.au/services_to_industry/erl/Grinding.html> [13 October2003].

Charpy, L. 2001, 'Phosphorous supply for atoll biological productivity', Coral Reefs, vol. 20,pp. 357 - 360.

Checkley, D. M. and C. A. Miller. 1989, ‘Nitrogen isotope fractionation by oceaniczooplankton’, Deep Sea Research Part A. Oceanographic Research Papers, vol. 36,no. 10, pp. 1449 – 1456.

Cowley, R. (Ed.) 1999, Hydrochemistry Operations Manual Version 6, CSIRO MarineLaboratories, Hobart.

Crossland, C. J. 1983, 'Dissolved nutrients in coral reef waters', In: Barnes, D. J. (Ed).Perspectives on Coral Reefs, Brian Clouston Publisher, Manuka, pp. 56 - 68.

D'Adamo, N. and C. J. Simpson. 2001, Review of the oceanography of Ningaloo Reef andadjacent waters, Technical Report: MMS/NIN/NIN-38/2001 (Unpublished report),Marine Conservation Branch, Department of Conservation and Land Management,Fremantle.

Dauby, P. 1989, ‘The stable carbon isotope ratios in benthic food webs of the gulf of Calvi,Corsica’, Continental Shelf Research, vol. 9, no. 2, pp. 181 – 195.

D'Elia, C. F. 1977, 'The uptake and release of dissolved phosphorous by reef corals',Limnology and Oceanography, vol. 22, no. 2, pp. 301 - 315.

Done, T. J. 1983, 'Coral zonation: its nature and significance', In: Barnes, D. J. (Ed).Perspectives on Coral Reefs, Brian Clouston Publisher, Manuka, pp. 107 - 147.

Dugdale, R. C. and J. J. Goering. 1967, ‘Uptake of new and regenerated forms of nitrogen inprimary productivity’, Limnology and Oceanography, vol. 12, no. 2, pp. 196 – 206.

Erez, J. 1990, 'On the importance of food sources in coral-reef ecosystems', In: Dubinsky, Z.(Ed). Ecosystems of the world: Coral Reefs, Elsevier Science Publishers, Amsterdam,pp. 411 - 418.

Fairbridge, R. 1950, 'Recent and Pleistocene coral reefs of Australia', Journal of Geology, vol.58, pp. 330 - 401.

Froelich, A. S. 1983, ‘Functional aspects of nutrient cycling on coral reefs’, The Ecology ofDeep and Shallow Coral Reefs, vol. 1, pp 133 - 139.

Fry, B., R. Lutes, M. Northam and P. L. Parker. 1982, ‘A 13C/12C comparison of food webs inCaribbean seagrass meadows and coral reefs’, Aquatic Botany, vol. 14, pp. 389 – 398.


105

Handley, L. L. and J. A. Raven. 1992, ‘The use of natural abundance of nitrogen isotopes inplant physiology and ecology’, Plant, Cell and Environment, vol. 15, pp. 965 – 985.

Hanson, C. 2003, Phytoplankton biomass and productivity in the coastal currents of W.A.,Applied Aquatic Ecology Seminar.

Hata, H., A. Suzuki, T. Maruyama, N. Kurano, S. Miyachi, Y. Ikeda and H. Kayanne.1998, ‘Carbon flux by suspended and sinking particles around the barrier reef ofPalau, Western Pacific’, Limnology and Oceanography, vol. 43, no. 8, pp. 1883 –1893.

Hatcher, B. G. 1991, 'Coral reefs in the Leeuwin Current - an ecological perspective', Journalof the Royal Society of Western Australia, vol. 74, pp. 115 - 127.

Hearn, C. J., B. G. Hatcher, R. J. Masini and C. J. Simpson. 1986, Oceanographic Processeson the Ningaloo Coral Reef, Western Australia, Environmental Dynamics Report ED-86-171, University of Western Australia, Perth.

Hearn, C. J. and I. N. Parker. 1988, Hydrodynamic processes on the Ningaloo coral reef,Western Australia, Proceedings of the Sixth International Coral Reef Symposium, vol.2, pp. 497 - 502.

Heikoop, J. M., J. J. Dunn, M. J. Risk, I. M. Sandeman, H. P. Schwarcz and N. Waltho. 1998,‘Relationship between light and the δ15N of coral tissue: examples from Jamaica and

Zanzibar’, Limnology and Oceanography, vol. 43, no. 5, pp. 909 – 920.

Heikoop, J. M., J. J. Dunn, M. J. Risk, T. Tomascik, H. P. Schwarcz, I. M. Sandeman and P.W. Sammarco. 2000, ‘δ15N and δ13C of coral tissue show significant inter-reef

variation’, Coral Reefs, vol. 19, pp. 189 – 193.

Hopley, D. 1983, 'Morphological classification of shelf reefs: a critique with special referenceto the Great Barrier Reef', In: Barnes, D. J. (Ed). Perspectives on Coral Reefs, BrianClouston Publisher, Manuka, pp. 180 - 199.

JGOFS. 1994, Core Measurement Protocols: Reports of the Core Measurement WorkingGroups, Joint Global Ocean Flux Study.

Johannes, R. E. 1964, 'Uptake and release of dissolved organic phosphorous byrepresentatives of a coastal marine ecosystem', Limnology and Oceanography, vol. 9,no. 2, pp. 224 - 234.

Johannes, R. E. 1967, 'Ecology of organic aggregates in the vicinity of a coral reef',Limnology and Oceanography, vol. 12, no. 2, pp. 189 - 195.

Johannes, R. E., S. L. Coles and N. T. Kuenzel. 1970, 'The role of zooplankton in the nutritionof some Scleractinian corals', Limnology and Oceanography, vol. 15, no. 4, pp. 579 -586.

Kinsey, D. W. 1979, Carbon turnover and accumulation by coral reefs, Ph. D. Thesis,University of Hawaii, Honolulu.


106

Kinsey, D. W. 1983, 'Standards of performance in coral reef primary production and carbonturnover', In: Barnes, D. J. (Ed). Perspectives on Coral Reefs, Brian CloustonPublisher, Manuka, pp. 209 - 220.

Koseff, G. 15 August 2003, Internal waves near coral reefs, Perth, Pers. comm.

Lenanton, R. C. J., F. Valesini, T. P. Bastow, G. B. Nowara, J. S. Edmonds and M. N.Connard. ‘The use of stable isotope ratios in whitebait otolith carbonate to identify thesource of prey for Western Australian penguins’, Journal of Experimental MarineBiology and Ecology, vol. 291, no. 1, pp. 17 – 27.

Mann, K. H. 2000, Ecology of Coastal Waters, with implications for management, BlackwellScience Inc., Malden, USA.

McClelland, J. W. and J. P. Montoya. 2002, ‘Trophic relationships and the nitrogen isotopiccomposition of amino acids in plankton’, Ecology, vol. 83, no. 8, pp. 2173 – 2180.

Minagawa, M., and E. Wada. 1986, ‘Nitrogen isotope ratios of red tide organisms in the EastChina Sea: a characterisation of biological nitrogen fixation’, Marine Chemistry, vol.19, pp. 245 – 260.

Muscatine, L. and C. F. D'Elia. 1978, 'The uptake, retention and release of ammonium by reefcorals', Limnology and Oceanography, vol. 23, no. 4, pp. 725 - 734.

Muscatine, L. and I. R. Kaplan. 1994, ‘Resource partitioning by reef corals as determinedfrom stable isotope composition part II: δ15N of zooxanthellae and animal tissue

versus depth’, Pacific Science, vol. 48, no. 3, pp. 304 – 312.

Mwashote, B. M. and I. O. Jumba. 2002, 'Quantitative aspects of inorganic nutrient fluxes inthe Gazi Bay (Kenya): implications for coastal ecosystems', Marine Pollution Bulletin,vol. 44, pp. 1194 - 1205.

Notes. 2001, 'Atoll morphometry controls lagoon nutrient regime', Limnology andOceanography, vol. 46, no. 2, pp. 456 - 461.

Nybakken, J. W. 2001, Marine Biology: An Ecological Approach, Benjamin Cummings, SanFrancisco.

Odum, H. T. and E. P. Odum. 1955, 'Trophic structure and productivity of a windward coralreef community on Eniwetok Atoll', Ecological Monographs, vol. 25, no. 3, pp. 291 -320.

Owens, N. J. P. 1987, ‘Natural variations in 15N in the marine environment’, Advances inMarine Biology, vol. 24, pp. 390 – 443.

Pearce, A. 1991, 'Eastern boundary currents of the southern hemisphere', Journal of the RoyalSociety of Western Australia, vol. 74, pp. 35 - 45.

Pearce, A. and C. Pattiaratchi. 1999, 'The Capes Current: a summer countercurrent flowingpast Cape Leeuwin and Cape Naturaliste, Western Australia', Continental ShelfResearch, vol. 19, pp. 402 - 420.


107

Peterson, B. J. and B. Fry. 1987, 'Stable isotopes in ecosystem studies', Annual Review ofEcological Systems, vol. 18, pp. 293 - 320.

Pilson, M. E. Q. and S. B. Betzer. 1973, 'Phosphorous flux across a coral reef', Ecology, vol.54, no. 3, pp. 581 - 588.

Pomeroy, L. R. 1970, 'The strategy of mineral cycling', Annual Review of Ecology andSystematics, vol. 1, pp. 171 - 190.

Preston, T. 1992, 'The measurement of stable isotope natural abundance variations', Plant,Cell and Environment, vol. 15, pp. 1091 - 1097.

Probyn, T. A., H. N. Waldron and A. G. James. ‘Size-fractionated measurements of nitrogenuptake in aged upwelled waters: implications for pelagic food webs’, Limnology andOceanography, vol. 35, no. 1, pp. 202 – 210.

Rougerie, F., J. A. Fagerstrom and C. Andrie. 1992, 'Geothermal endo-upwelling: a solutionto the reef nutrient paradox?' Continental Shelf Research, vol. 12, no. 7/8, pp. 785 -798.

Royal Australian Navy Hydrographic Survey. 1985, North West Cape to Point Maud,Commonwealth of Australia, Wollongong.

Sargent, M. C. and T. S. Austin. 1949, 'Organic productivity of an atoll', AmericanGeophysical Union Transcripts, vol. 30, no. 2, pp. 245 - 249.

Simpson, C. J. and R. J. Masini. 1986, Tide and seawater temperature data from the NingalooReef tract, Western Australia, and the implications for coral mass spawning, Bulletin253, Department of Conservation and Environment, Perth.

Smith, R., A. Huyer, J. Godfrey and J. Church. 1991, 'The Leeuwin Current off WesternAustralia, 1986 - 1987', Journal of Physical Oceanography, vol. 21, pp. 323 - 345.

Smith, S. V. 1983, Net production of coral reef ecosystems, The Ecology of Deep andShallow Coral Reefs, vol. 1, pp 127 - 131.

Sorokin, Y. 1990, 'Aspects of trophic relations, productivity and energy balance in coral-reefecosystems', In: Dubinsky, Z. (Ed). Ecosystems of the world: Coral Reefs, ElsevierScience Publishers, Amsterdam, pp. 401 - 410.

Storrie, A. and S. Morrison. 1998, The Marine Life of Ningaloo Marine Park and Coral Bay,Department of Conservation and Land Management, Perth.

Survey of water quality, groundwater, sediments and benthic habitats at Coral Bay, NingalooReef, Western Australia: a report to the Department of Conservation and LandManagement, 1995, Western Australian Department of Environmental Protection,Perth.


108

Taylor, J. G. and A. F. Pearce. 1999, 'Ningaloo Reef Current observations and implicationsfor biological systems: Coral spawn dispersal, zooplankton and whale sharkabundance', Journal of the Royal Society of Western Australia, vol. 82, pp. 57-65.

Thompson, R. 1984, 'Observations of the Leeuwin Current of Western Australia', Journal ofPhysical Oceanography, vol. 14, pp. 623 - 628.

Tribble, G. W., M. J. Atkinson, F. J. Sansone and S. V. Smith. 1994, 'Reef metabolism andendo-upwelling in perspective', Coral Reefs, vol. 13, pp. 199 - 201.

Vizzini, S., G. Sara, R. H. Michener and A. Mazzola. 2002, ‘The role and contribution of theseagrass Posidonia oceanica organic matter for secondary consumers as revealed bycarbon and nitrogen stable isotope analysis’, Acta Oecologica, vol. 23, no. 4, pp. 277 –285.

Waser, N. A., K. Yin, Z. Yu, K. Tada, P. J. Harrison, D. H. Turpin and S. E. Calvert. 1998,‘Nitrogen isotope fractionation during nitrate, ammonium and urea uptake by marinediatoms and coccolithophores under various conditions of N availability’, MarineEcology Progress Series, vol. 169, pp. 29 – 41.

Webb, K. L., W. D. DuPaul, W. J. Wiebe, W. Sottile and R. E. Johannes. 1975, 'Enewetak(Eniwetok) Atoll: Aspects of the nitrogen cycle on a coral reef', Limnology andOceanography, vol. 20, no. 2, pp. 198 - 210.

Wiebe, W. J., R. E. Johannes and K. L. Webb. 1975, 'Nitrogen fixation in a coral reefcommunity', Science, vol. 188, no. 4185, pp. 257 - 259.

Woo, L. M. (2003), Statement of proposed project, [Online], Centre for Water Research,Available from: <http://www2.cwr.uwa.edu.au/~woo/work.htm> [10 October 2003].

Woo, L. M. and C. B. Pattiaratchi. 2003, 'Summer surface circulation on the Gascoynecontinental shelf', Unpublished material.

Wooster, W. and J. Reid. 1963, 'Eastern Boundary Currents', In: Hill, M. (Ed). The Sea,Pergamon Press, pp. 253 - 279.

Yamamuro, M., H. Kayenne and M. Minagawa. 1995, ‘Carbon and nitrogen stable isotopes ofprimary producers in coral reef ecosystems’, Limnology and Oceanography, vol. 40,no. 3, pp. 617 – 621.

Yamamuro, M., H. Kayanne and H. Yamano. 2003, ‘δ15N of seagrass leaves for monitoring

anthropogenic nutrients increases in coral reef ecosystems’, Marine Pollution Bulletin,vol. 46, no. 4, pp. 452 – 458.

I

1 0 AP P E N D I C E S

1 0 . 1 DESCRIPTION OF SAMPLE POSITION, DEPTH, FILTRATION,ANALYSIS PERFORMED AND CTD DROP FOR EACH STATIONSITE

Sample = number given to each filter paper or sample tubeStation = station number as recorded by on-board computerDepth = water depth from surfaceFiltered? = passed through a 37_m mesh before analysis?Analysis = parameter that sample was tested forTransect Position = which transect and distance from reef in kilometresCTD Drop? = CTD probe deployed at this station?

SAMPLE STATION DEPTH FILTERED? ANALYSISTRANSECTPOSITION

CTDDROP?

001 NWC432 1M no POC, PON, isotopes middle 1km no002 NWC432 15M no POC, PON, isotopes middle 1km no003 NWC432 1M no chlorophyll a middle 1km no004 NWC432 30M no POC, PON, isotopes middle 1km no005 NWC432 30M no chlorophyll a middle 1km no006 NWC432 15M no chlorophyll a middle 1km no007 NWC432 1M yes POC, PON, isotopes middle 1km no008 NWC432 15M yes POC, PON, isotopes middle 1km no009 NWC432 30M yes POC, PON, isotopes middle 1km no010 NWC432 1M no DIN, DIP middle 1km no011 NWC432 15M no DIN, DIP middle 1km no012 NWC432 30M no DIN, DIP middle 1km no

013 NWC433 0.8M no POC, PON, isotopes south 1km yes014 NWC433 15.5M no POC, PON, isotopes south 1km yes015 NWC433 30M no POC, PON, isotopes south 1km yes016 NWC433 0.8M yes POC, PON, isotopes south 1km yes017 NWC433 15.5M yes POC, PON, isotopes south 1km yes018 NWC433 30M yes POC, PON, isotopes south 1km yes019 NWC433 0.8M no chlorophyll a south 1km yes020 NWC433 15.5M no chlorophyll a south 1km yes021 NWC433 30M no chlorophyll a south 1km yes022 NWC433 0.8M no DIN, DIP south 1km yes023 NWC433 15.5M no DIN, DIP south 1km yes024 NWC433 30M no DIN, DIP south 1km yes

025 NWC434 1M no POC, PON, isotopes north 1km yes026 NWC434 20M no POC, PON, isotopes north 1km yes027 NWC434 1M yes POC, PON, isotopes north 1km yes028 NWC434 20M yes POC, PON, isotopes north 1km yes029 NWC434 1M no chlorophyll a north 1km yes030 NWC434 20M no chlorophyll a north 1km yes031 NWC434 1M no DIN, DIP north 1km yes032 NWC434 20M no DIN, DIP north 1km yes

033 NWC435 1M no chlorophyll a north 2km yes034 NWC435 1M no POC, PON, isotopes north 2km yes035 NWC435 34M no chlorophyll a north 2km yes036 NWC435 18M no DIN, DIP north 2km yes

II

037 NWC435 34M no DIN, DIP north 2km yes038 NWC435 18M no POC, PON, isotopes north 2km yes039 NWC435 34M no POC, PON, isotopes north 2km yes040 NWC435 18M no chlorophyll a north 2km yes041 NWC435 1M yes POC, PON, isotopes north 2km yes042 NWC435 1M no DIN, DIP north 2km yes043 NWC435 34M yes POC, PON, isotopes north 2km yes044 NWC435 18M yes POC, PON, isotopes north 2km yes

045 NWC436 1M no chlorophyll a north 3km yes046 NWC436 1M no DIN, DIP north 3km yes047 NWC436 1M no POC, PON, isotopes north 3km yes048 NWC436 30M no DIN, DIP north 3km yes049 NWC436 1M yes POC, PON, isotopes north 3km yes050 NWC436 15M no POC, PON, isotopes north 3km yes051 NWC436 15M yes POC, PON, isotopes north 3km yes052 NWC436 15M no chlorophyll a north 3km yes053 NWC436 30M no chlorophyll a north 3km yes054 NWC436 15M no DIN, DIP north 3km yes055 NWC436 30M no POC, PON, isotopes north 3km yes056 NWC436 30M yes POC, PON, isotopes north 3km yes

057 NWC437 1M no DIN, DIP north 4km yes058 NWC437 1M no chlorophyll a north 4km yes059 NWC437 15M no chlorophyll a north 4km yes060 NWC437 1M no POC, PON, isotopes north 4km yes061 NWC437 30M no chlorophyll a north 4km yes062 NWC437 15M no DIN, DIP north 4km yes063 NWC437 1M yes POC, PON, isotopes north 4km yes064 NWC437 30M no DIN, DIP north 4km yes065 NWC437 15M no POC, PON, isotopes north 4km yes066 NWC437 15M yes POC, PON, isotopes north 4km yes067 NWC437 30M no POC, PON, isotopes north 4km yes068 NWC437 30M yes POC, PON, isotopes north 4km yes

069 NWC438 1M no chlorophyll a north 5km yes070 NWC438 18M no chlorophyll a north 5km yes071 NWC438 36M no chlorophyll a north 5km yes072 NWC438 1M no DIN, DIP north 5km yes073 NWC438 18M no DIN, DIP north 5km yes074 NWC438 1M no POC, PON, isotopes north 5km yes075 NWC438 18M no POC, PON, isotopes north 5km yes076 NWC438 1M yes POC, PON, isotopes north 5km yes077 NWC438 36M no DIN, DIP north 5km yes078 NWC438 36M no POC, PON, isotopes north 5km yes079 NWC438 18M yes POC, PON, isotopes north 5km yes080 NWC438 36M yes POC, PON, isotopes north 5km yes

081 NWC439 1M no chlorophyll a north 10km yes082 NWC439 40M no chlorophyll a north 10km yes083 NWC439 80M no chlorophyll a north 10km yes084 NWC439 120M no chlorophyll a north 10km yes085 NWC439 1M no DIN, DIP north 10km yes086 NWC439 40M no DIN, DIP north 10km yes087 NWC439 80M no DIN, DIP north 10km yes088 NWC439 120M no DIN, DIP north 10km yes089 NWC439 1M no POC, PON, isotopes north 10km yes

III

090 NWC439 40M no POC, PON, isotopes north 10km yes091 NWC439 120M no POC, PON, isotopes north 10km yes092 NWC439 80M no POC, PON, isotopes north 10km yes093 NWC439 40M yes POC, PON, isotopes north 10km yes094 NWC439 1M yes POC, PON, isotopes north 10km yes095 NWC439 80M yes POC, PON, isotopes north 10km yes096 NWC439 120M yes POC, PON, isotopes north 10km yes

097 NWC440 1M no DIN, DIP middle 2km yes098 NWC440 1M no chlorophyll a middle 2km yes099 NWC440 18M no chlorophyll a middle 2km yes100 NWC440 34M no chlorophyll a middle 2km yes101 NWC440 1M no POC, PON, isotopes middle 2km yes102 NWC440 1M yes POC, PON, isotopes middle 2km yes103 NWC440 18M no DIN, DIP middle 2km yes104 NWC440 34M no DIN, DIP middle 2km yes105 NWC440 18M no POC, PON, isotopes middle 2km yes106 NWC440 18M yes POC, PON, isotopes middle 2km yes107 NWC440 34M no POC, PON, isotopes middle 2km yes108 NWC440 34M yes POC, PON, isotopes middle 2km yes

109 NWC441 1M no chlorophyll a middle 3km yes110 NWC441 17M no chlorophyll a middle 3km yes111 NWC441 35M no chlorophyll a middle 3km yes112 NWC441 1M no DIN, DIP middle 3km yes113 NWC441 1M no POC, PON, isotopes middle 3km yes114 NWC441 17M no DIN, DIP middle 3km yes115 NWC441 1M yes POC, PON, isotopes middle 3km yes116 NWC441 35M no DIN, DIP middle 3km yes117 NWC441 17M no POC, PON, isotopes middle 3km yes118 NWC441 17M yes POC, PON, isotopes middle 3km yes119 NWC441 35M no POC, PON, isotopes middle 3km yes120 NWC441 35M yes POC, PON, isotopes middle 3km yes

121 NWC442 1M no chlorophyll a middle 4km yes122 NWC442 20M no chlorophyll a middle 4km yes123 NWC442 1M no DIN, DIP middle 4km yes124 NWC442 20M no DIN, DIP middle 4km yes125 NWC442 1M no POC, PON, isotopes middle 4km yes126 NWC442 1M yes POC, PON, isotopes middle 4km yes127 NWC442 20M no POC, PON, isotopes middle 4km yes128 NWC442 40M no DIN, DIP middle 4km yes129 NWC442 40M no chlorophyll a middle 4km yes130 NWC442 40M no POC, PON, isotopes middle 4km yes131 NWC442 20M yes POC, PON, isotopes middle 4km yes132 NWC442 40M yes POC, PON, isotopes middle 4km yes

133 NWC443 1M no chlorophyll a middle 5km yes134 NWC443 29M no chlorophyll a middle 5km yes135 NWC443 1M no DIN, DIP middle 5km yes136 NWC443 58.5M no chlorophyll a middle 5km yes137 NWC443 29M no DIN, DIP middle 5km yes138 NWC443 1M no POC, PON, isotopes middle 5km yes139 NWC443 1M yes POC, PON, isotopes middle 5km yes140 NWC443 29M no POC, PON, isotopes middle 5km yes141 NWC443 29M yes POC, PON, isotopes middle 5km yes142 NWC443 58.5M no DIN, DIP middle 5km yes

IV

143 NWC443 58.5M no POC, PON, isotopes middle 5km yes144 NWC443 58.5M yes POC, PON, isotopes middle 5km yes

145 NWC444 1M no chlorophyll a middle 10km yes146 NWC444 34M no chlorophyll a middle 10km yes147 NWC444 67M no chlorophyll a middle 10km yes148 NWC444 102M no chlorophyll a middle 10km yes149 NWC444 1M no DIN, DIP middle 10km yes150 NWC444 1M yes POC, PON, isotopes middle 10km yes151 NWC444 1M no POC, PON, isotopes middle 10km yes152 NWC444 34M no DIN, DIP middle 10km yes153 NWC444 34M no POC, PON, isotopes middle 10km yes154 NWC444 34M yes POC, PON, isotopes middle 10km yes155 NWC444 67M no DIN, DIP middle 10km yes156 NWC444 67M yes POC, PON, isotopes middle 10km yes157 NWC444 67M no POC, PON, isotopes middle 10km yes158 NWC444 102M no DIN, DIP middle 10km yes159 NWC444 102M no POC, PON, isotopes middle 10km yes160 NWC444 102M yes POC, PON, isotopes middle 10km yes

161 NWC445 1M no chlorophyll a south 10km yes162 NWC445 34M no chlorophyll a south 10km yes163 NWC445 66M no chlorophyll a south 10km yes164 NWC445 1M no DIN, DIP south 10km yes165 NWC445 34M no DIN, DIP south 10km yes166 NWC445 34M no POC, PON, isotopes south 10km yes167 NWC445 1M no POC, PON, isotopes south 10km yes168 NWC445 66M no DIN, DIP south 10km yes169 NWC445 66M no POC, PON, isotopes south 10km yes170 NWC445 34M yes POC, PON, isotopes south 10km yes171 NWC445 1M yes POC, PON, isotopes south 10km yes172 NWC445 66M yes POC, PON, isotopes south 10km yes

173 NWC446 1M no chlorophyll a south 5km yes174 NWC446 29M no chlorophyll a south 5km yes175 NWC446 58M no chlorophyll a south 5km yes176 NWC446 1M no DIN, DIP south 5km yes177 NWC446 29M no DIN, DIP south 5km yes178 NWC446 29M no POC, PON, isotopes south 5km yes179 NWC446 58M no DIN, DIP south 5km yes180 NWC446 1M no POC, PON, isotopes south 5km yes181 NWC446 58M no POC, PON, isotopes south 5km yes182 NWC446 1M yes POC, PON, isotopes south 5km yes183 NWC446 58M yes POC, PON, isotopes south 5km yes184 NWC446 29M yes POC, PON, isotopes south 5km yes

185 NWC447 1M no chlorophyll a south 4km yes186 NWC447 22M no chlorophyll a south 4km yes187 NWC447 38M no chlorophyll a south 4km yes188 NWC447 1M no DIN, DIP south 4km yes189 NWC447 22M no DIN, DIP south 4km yes190 NWC447 38M no DIN, DIP south 4km yes191 NWC447 1M no POC, PON, isotopes south 4km yes192 NWC447 22M no POC, PON, isotopes south 4km yes193 NWC447 38M no POC, PON, isotopes south 4km yes194 NWC447 1M yes POC, PON, isotopes south 4km yes195 NWC447 22M yes POC, PON, isotopes south 4km yes

V

196 NWC447 38M yes POC, PON, isotopes south 4km yes

197 NWC448 1M no chlorophyll a south 3km yes198 NWC448 15M no chlorophyll a south 3km yes199 NWC448 30M no chlorophyll a south 3km yes200 NWC448 1M no DIN, DIP south 3km yes201 NWC448 15M no DIN, DIP south 3km yes202 NWC448 30M no DIN, DIP south 3km yes203 NWC448 1M no POC, PON, isotopes south 3km yes204 NWC448 30M no POC, PON, isotopes south 3km yes205 NWC448 15M no POC, PON, isotopes south 3km yes206 NWC448 1M yes POC, PON, isotopes south 3km yes207 NWC448 30M yes POC, PON, isotopes south 3km yes208 NWC448 15M yes POC, PON, isotopes south 3km yes

209 NWC449 1M no chlorophyll a south 2km yes210 NWC449 15M no chlorophyll a south 2km yes211 NWC449 30M no chlorophyll a south 2km yes212 NWC449 1M no DIN, DIP south 2km yes213 NWC449 15M no DIN, DIP south 2km yes214 NWC449 30M no DIN, DIP south 2km yes215 NWC449 1M no POC, PON, isotopes south 2km yes216 NWC449 15M no POC, PON, isotopes south 2km yes217 NWC449 30M no POC, PON, isotopes south 2km yes218 NWC449 1M yes POC, PON, isotopes south 2km yes219 NWC449 15M yes POC, PON, isotopes south 2km yes220 NWC449 30M yes POC, PON, isotopes south 2km yes

221 NWC450 1M no chlorophyll a lagoon top no222 NWC450 3M no chlorophyll a lagoon top no223 NWC450 1M no DIN, DIP lagoon top no224 NWC450 1M no POC, PON, isotopes lagoon top no225 NWC450 1M yes POC, PON, isotopes lagoon top no226 NWC450 3M no DIN, DIP lagoon top no227 NWC450 3M no POC, PON, isotopes lagoon top no228 NWC450 3M yes POC, PON, isotopes lagoon top no

229 NWC451 1M no chlorophyll a lagoon middle no230 NWC451 2.5M no chlorophyll a lagoon middle no231 NWC451 1M no DIN, DIP lagoon middle no232 NWC451 1M no POC, PON, isotopes lagoon middle no233 NWC451 1M yes POC, PON, isotopes lagoon middle no234 NWC451 2.5M no DIN, DIP lagoon middle no235 NWC451 2.5M no POC, PON, isotopes lagoon middle no236 NWC451 2.5M yes POC, PON, isotopes lagoon middle no

237 NWC452 1M no chlorophyll a lagoon bottom no238 NWC452 2.5M no chlorophyll a lagoon bottom no239 NWC452 1M no DIN, DIP lagoon bottom no240 NWC452 1M no POC, PON, isotopes lagoon bottom no241 NWC452 2.5M no DIN, DIP lagoon bottom no242 NWC452 1M yes POC, PON, isotopes lagoon bottom no243 NWC452 2.5M no POC, PON, isotopes lagoon bottom no244 NWC452 2.5M yes POC, PON, isotopes lagoon bottom no

VI

10.2 POSITION IN LATITUDE AND LONGITUDE OF EACH WATER ANDREEF ORGANISM SAMPLING SITE

Position (water sampling or organism sampling) Latitude Longitude

North transect – 1km 22o 42.07’ S 113o 37.88’ E






Middle transect – 1km 22o 42.36’ S 113o 38.12’ E






South transect – 1km 22o 42.70’ S 113o 38.06’ E






Inside lagoon – top point 22o 41.80’ S 113o 39.15’ E

Inside lagoon – middle point 22o 42.00’ S 113o 39.2’ E

Inside lagoon – bottom point 22o 42.20’ S 113o 39.35’ E

Reef sampling 5/5/03 no. 1 22o 38.15’ S 113o 37.80’ E

Reef sampling 5/5/03 no. 2 22o 38.91’ S 113o 35.94’ E

Reef sampling 8/5/03 22o 34.00’ S 113o 39.4’ E

Reef-lagoon channel pass 22o 36.73’ S 113o 38.80’ E

VII

10.3 IDENTIFICATION OF REEF ORGANISM SAMPLES

SampleNumber

Sample Group forAnalysis

Species Identification

ORG1 Piscivores Lethrinus miniatus (Red-throated emperor)

ORG2 Piscivores Variola louti (Coronation trout)

ORG3 SeaweedSargassum sp. (seaweed) – Accurate identification not

possible

ORG4 Not used – data not received Acropora hyacinthus (scleractinian coral)

ORG5 Seaweed Seaweed/algae – Accurate identification not possible

ORG6 Not used – data not receivedFamily Alcyoniidae, cf. Lobophytum sp. (soft coral) –

Accurate identification not possible

ORG7 Not used – data not received Nardoa galatheae (seastar)

ORG8 Sea cucumbers Holothuria atra (small sea cucumber)

ORG9 SeaweedSargassum sp. (seaweed) – Accurate identification not

possible

ORG10 Seaweed Seaweed/algae – Accurate identification not possible

ORG11 Piscivores Euthynnus affinis (Bonito tuna)

ORG12 Sea cucumbers Holothuria atra (small sea cucumber)

ORG13 Crayfish Panulirus ornatus (Coral crayfish)

ORG14 Reef fish possibly parrotfish – Accurate identification not possible

ORG15 Piscivorespossibly groper or cod – Accurate identification not

possible

ORG16 Reef fish Plectorhinchus flavomuculatus (reef fish)

ORG17 Not used Sea cucumber – had to be thrown away, re-hydrated

ORG18 Sea cucumbers Holothuria whitmaeei (large sea cucumber)

ORG19 Not used – data not received Echinometra mathaei (sea urchin)

ORG20 Oyster Pinctada margaritifera (oyster)

ORG21 Not used – data not received Family: Fungiidae – Accurate identification not possible

ORG22 Not used – data not received Pocillopora damicornis (scleractinian coral)

ORG23 Not used – data not received Tectus pyramis (cone shell)

ORG24 Reef fishlike Convict surgeonfish – Aconthusus triostegus –


ORG25 Reef fishpossibly another surgeonfish – Accurate identification not

possible

ORG26 Reef fishlike Convict surgeonfish – Aconthusus triostegus –


Documents

Oceanic Inputs to Coral Reefs: Ningaloo Reef Case Study · The coral reef ‘paradox’ has been the subject of much study, and various mechanisms have been proposed to explain how