caulerpa taxifolia in moreton bay - Centre for Marine Science ...

CAULERPA TAXIFOLIA IN MORETON BAY- 

DISTRIBUTION AND SEAGRASS INTERACTIONS 

JANE THOMAS, BSC 

THESIS SUBMITTED TO THE DEPARTMENT OF BOTANY, 

THE UNIVERSITY OF QUEENSLAND, 

AUSTRALIA 

FOR THE PARTIAL FULFILMENT OF BACHELOR OF SCIENCE (HONOURS). 

26 MAY 2003 

SUPERVISORS: DR JAMES UDY (CENTRE FOR MARINE STUDIES) 

DR SUSANNE SCHMIDT (DEPARTMENT OF BOTANY) 

WORD COUNT: 8550

STATEMENT 

The work presented in this thesis is, to the best of my knowledge and belief, 

original, except as acknowledged in the text, and the material has not been 

submitted, either in whole or in part, for a degree at this or any other University. 

Jane Thomas 

May 2003 

Jane Thomas 

-ii-

ACKNOWLEDGEMENTS 

Thanks to my supervisors, James Udy and Susanne Schmidt, as well as the head 

of the Marine Botany Group, Norm Duke and the rest of the MarBots for being 

such a supportive, helpful and generally great bunch of people – I couldn’t have 

done it without the practical and moral support from you guys. Thanks to 

everyone who read this thesis at various stages and helped with comments, edits 

and coffee – I think everyone in MarBot knows I have a double-shot alpine latte 

first-thing in the morning! 

My field crew – Kathryn, Big Dan, Little Dan, Chris, Shano and Todd for driving 

boats, collecting seagrass and algae and getting wet with me. Kath, Kev and 

Shano from Moreton Bay Research Station for their help, sympathy, chocolate 

and erm, poetry. Nicola Udy and John Esdaile from Qld Parks and Wildlife 

Service for letting me know when they found my algae out in the field. 

Chris Roelfsema (the Crazy Dutchie) and Big Dan for introducing me to the big 

bad world of GIS and ArcView, and Diana Kleine (the Other Crazy Dutchie) for 

help with graphic design. 

My mum for her unconditional love and support and for looking after me, 

especially in the last few months. 

Bill Dennison and Judy O’Neil for getting me interested in marine plants in the 

first place (and for giving me a job when I finish!) and Tim Carruthers for helpful 

advice and support, even from the other side of the world. 

Jane Thomas 

-iii-

TABLE OF CONTENTS 

1. ABSTRACT ............................................................ 1 

2. INTRODUCTION.................................................... 2 

2.1 GENERAL BIOLOGY .................................................................................4 

2.2 CAULERPA TAXIFOLIA IN QUEENSLAND.......................................................4 

2.3 ECOLOGICAL IMPACTS OF CAULERPA TAXIFOLIA PROLIFERATION.....................5 

2.4 OBJECTIVES OF THE PRESENT STUDY ...........................................................6 

3. MATERIALS AND METHODS ................................... 7 

3.1 STUDY AREA ..........................................................................................7 

3.2 BENTHIC SURVEYS...................................................................................9 

Jane Thomas 

3.2.1 Selection of sites.........................................................................9 

3.2.2 Survey technique and analyses...................................................9 

3.3 RECIPROCAL TRANSPLANTS.....................................................................11 

3.3.1 Site description.........................................................................11 

3.3.2 Experimental design, measurements and analyses.....................11 

3.4 SEAGRASS AQUARIA EXPERIMENTS............................................................12 

3.4.1 Effect of Caulerpa taxifolia extract on three seagrass species .....12 

3.4.2 Experimental design .................................................................15 

3.4.3 Effect of Caulerpa taxifolia extract on Zostera capricorni ..........15 

3.4.4 PAM fluorometry......................................................................16 

3.4.5 Pigment analysis and biomass measurements ...........................16 

3.4.6 Statistical analyses....................................................................17 

4. RESULTS ..............................................................18 

4.1 BENTHIC SURVEYS.................................................................................18 

4.1.1 Overall in Moreton Bay............................................................18 

4.1.2 Western Moreton Bay...............................................................21 

4.1.2.1 Caulerpa taxifolia distribution in 2003....................................21 

4.1.2.2 Change in Caulerpa distribution 1998-2003............................22 

-iv-

Jane Thomas 

4.1.3 Southern Moreton Bay..............................................................23 



4.1.4 Pumicestone Passage................................................................25 



4.1.5 Eastern Moreton Bay ................................................................27 



4.2 RECIPROCAL TRANSPLANTS.....................................................................29 

4.3 EFFECT OF CAULERPA TAXIFOLIA EXTRACT ON SEAGRASSES...........................30 

4.3.1 Shoot density of three seagrass species .....................................30 

4.3.2 Maximum leaf length of three seagrass species .........................32 

4.3.3 PAM fluorometry and leaves per shoot of three seagrass species. 34 

4.3.4 Effect of Caulerpa taxifolia extract on Zostera capricorni ..........34 

5. DISCUSSION ........................................................36 

5.1 COMPARISON WITH OTHER CAULERPA TAXIFOLIA POPULATIONS ..................36 

5.2 FACTORS AFFECTING CAULERPA TAXIFOLIA DISTRIBUTION IN MORETON BAY..37 

5.2.1 Water temperature ...................................................................39 

5.2.2 Caulerpa taxifolia and seagrass interactions..............................40 

5.2.2.1 Water quality ............................................................................40 

5.2.2.2 Physical disturbance .................................................................41 

5.2.2.3 Accumulation of sulphide in sediments ...................................42 

5.2.2.4 Caulerpa taxifolia toxins..........................................................43 

5.3 CONCLUSIONS AND RECOMMENDATIONS.................................................44 

6. REFERENCES.........................................................46 

7. APPENDIX............................................................58 

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1. ABSTRACT 

Caulerpa taxifolia in Moreton Bay 

Caulerpa taxifolia is a green macroalga that has gained notoriety in the last two decades 

as an invasive species following its introduction and subsequent invasion of large areas 

of the north-western Mediterranean Sea. It is native to Moreton Bay in south-east 

Queensland, where it shares its soft-sediment niche with seven species of seagrass. The 

current distribution of C. taxifolia in Moreton Bay was mapped, and compared with its 

distribution five years ago to detect any changes. To explore interactions between 

C. taxifolia and Moreton Bay seagrasses, experiments investigated the effect of 

C. taxifolia extract and of physical disturbance on seagrasses. 

There was a significant increase in C. taxifolia distribution in Moreton Bay in the last 

five years, particularly in western and southern regions with more sites and increased 

cover. In western Moreton Bay, C. taxifolia mainly colonised bare sediments, while 

in the southern Bay and Pumicestone Passage it replaced seagrass. It is interesting to 

note that at the sites where C. taxifolia cover decreased in western Moreton Bay, it 

was replaced by seagrass, which indicates the potential for seagrasses to recover after 

colonisation by C. taxifolia. There were dense populations present around Dunwich 

at North Stradbroke Island in eastern Moreton Bay, however C. taxifolia was only 

present at low densities on the eastern banks. 

Planthouse experiments showed some significant results, with seagrass shoot 

density being negatively affected by the addition of C. taxifolia extract, however the 

results were highly variable. Reciprocal transplants of C. taxifolia and the seagrass 

Zostera capricorni indicated that Z. capricorni is more susceptible to physical 

disturbance than C. taxifolia, which can utilise disturbance as an opportunity for 

expansion. 

Five processes are hypothesised to synergistically affect C. taxifolia distribution and 

seagrass interactions in Moreton Bay, including sustained high seawater temperatures, 

water quality decline, physical disturbance, allelopathic interactions from C. taxifolia 

toxins, and the accumulation of sulphide in the sediments. 

Jane Thomas -1- 

Abstract

2. INTRODUCTION 


The marine macroalga Caulerpa taxifolia (Vahl) C. Agardh (Bryopsidales, 

Chlorophyta) grows anchored in soft sediments throughout tropical and subtropical 

waters (Huisman, 2000; Phillips and Price, 2002). C. taxifolia has gained notoriety 

following its introduction and subsequent invasion of large areas of the north-western 

Mediterranean Sea over the last two decades (Meinesz and Hesse, 1991; Meinesz et 

al., 2001). In the last three years, additional introductions have been recorded off the 

coast of California in the United States, and in several locations in Australia (Dalton, 

2000; Kaiser, 2000; Schaffelke et al., 2002; Williams and Grosholz, 2002) (Figure 1). 

C. taxifolia is widely used as an aquarium plant as it is decorative, fast-growing and 

robust and the multiple introductions of C. taxifolia are almost certainly the result of 

accidental release from private or public aquaria into the sea (Jousson et al., 1998; 

Jousson et al., 2000; Wiedenmann et al., 2001; Primary Industries and Resources SA, 

2002). C. taxifolia is out-competing and replacing seagrasses in the Mediterranean 

Sea, and occurs with seagrasses at other introduction sites in the U.S.A. and Australia 

(de Villèle and Verlaque, 1995; NSW Fisheries, 2002; Williams and Grosholz, 2002). 

C. taxifolia is native to Queensland, Australia and is distributed throughout Moreton 

Bay in south-east Queensland (Phillips and Price, 2002), where it shares its shallow 

soft-sediment niche with seven species of seagrass (Hyland et al., 1989; Udy et al., 

1999). Anecdotal evidence has suggested that C. taxifolia has expanded its range 

within Moreton Bay within the last five years, and preliminary research has indicated 

that C. taxifolia may out-compete the seagrass Zostera capricorni Aschers. 

(Potamogetonales, Magnoliophyta) at Fisherman Islands in western Moreton Bay 

(Thomas, 2002a). 


Introduction



Introduction 

C. taxifolia native distribution 

C. taxifolia introductions 

Figure 1. Distribution of native and introduced Caulerpa taxifolia populations around the world.

2.1 GENERAL BIOLOGY 


The morphology of the Caulerpa thallus is a horizontal creeping stolon from which 

the photosynthetic fronds and anchoring rhizoid pillars arise. All Bryopsidophyceaen 

macroalgae, including Caulerpa are coenocytic, that is, the protoplasm is 

multinucleate and continuous and not separated by internal cell walls, although 

internal support structures are present (Clayton and King, 1990). Fragmentation is an 

efficient mode of reproduction for coenocytic green macroalgae, and fragments as 

small as 2 mm may propagate into full-size plants (Brück and Schnetter, 1993; 

Walters and Smith, 1994; Smith and Walters, 1999). 

Caulerpa contains a suite of toxic secondary metabolites, the major one of which is a 

sesquiterpenoid called caulerpenyne (Amico et al., 1978; Paul and Fenical, 1986; 

1987). The array of toxins in C. taxifolia are antiviral (Nicoletti et al., 1999), 

neurotoxic (Brunelli et al., 2000), cytotoxic and cell growth inhibitors (Barbier et al., 

2001). They also display active or toxic effects on phytoplankton (Lemée et al., 

1997), marine ciliate protists (Ricci et al., 1999) and fertilised eggs of the major 

Mediterranean herbivore, the sea urchin Paracentrotus lividus (Lamarck) (Pedrotti et 

al., 1996; Pesando et al., 1996; Pesando et al., 1998; Pesando et al., 1999). 

Additionally, adult P. lividus preferentially avoid grazing on C. taxifolia (Lemée et 

al., 1993; Boudouresque et al., 1996; Lemée et al., 1996). This implies that these 

toxins are active on eukaryotes and prokaryotes alike, and there is some evidence that 

they are toxic to angiosperm plants, including seagrasses (Guerriero et al., 1994). 

2.2 CAULERPA TAXIFOLIA IN QUEENSLAND 

C. taxifolia has been recorded from the Queensland coast since the 1850s and occurs 

from Cape York to the Gold Coast (Harvey, 1860; Cribb, 1958; Huisman, 2000; 

Phillips and Price, 2002). It has been recorded from south-east Queensland since 

1909, and from Moreton Bay since 1950 which implies that it is most likely a native 

species (Phillips and Price, 2002; Qld Herbarium, 2002). 

Numerous genetic studies have suggested that the so-called invasive “aquarium- 

Mediterranean” strain of C. taxifolia originated in Moreton Bay, using techniques 

such as allozyme surveys (Benzie et al., 2000), DNA fingerprints (Wiedenmann et al., 

2001), ITS sequences (Jousson et al., 2000; Meusnier et al., 2001; Famà et al., 2002; 


Introduction


Meusnier et al., 2002; Schaffelke et al., 2002), and the presence/absence of a 

chloroplast DNA intron located in the rbcL gene (Famà et al., 2002). In addition to 

these genetic similarities, the “aquarium-Mediterranean” strain also shares a robust 

morphology and cold tolerance with the Moreton Bay population (Meinesz et al., 

1995; Komatsu et al., 1997; Phillips and Price, 2002). 

2.3 ECOLOGICAL IMPACTS OF CAULERPA TAXIFOLIA PROLIFERATION 

In the Mediterranean, C. taxifolia apparently out-competes two native seagrasses, 

Posidonia oceanica (Linnaeus) Delile and Cymodocea nodosa (Ucria) Aschers. (de 

Villèle and Verlaque, 1995; Ceccherelli and Cinelli, 1997). It has been suggested that 

the observed responses of P. oceanica to C. taxifolia presence (decrease in leaf 

number, width and longevity, and increase in leaf turnover) may be the result of 

allelopathy from C. taxifolia secondary metabolites (de Villèle and Verlaque, 1995; 

Dumay et al., 2002). 

Endemic Mediterranean macroalgae are also deleteriously affected by the presence of 

C. taxifolia, with a decline in the productivities of Cystoseira barbata f. aurantia 

(Kützing) Giaccone (Fucales, Phaeophyta) and Gracilaria bursa-pastoris (Gmelin) 

Silva (Gracilariales, Rhodophyta), which has also been attributed to the toxins 

contained in C. taxifolia (Ferrer et al., 1997). The reduction of other common species 

of Mediterranean macroalgae has also been associated with the presence of 

C. taxifolia (Verlaque and Fritayre, 1994). 

Although C. taxifolia in Moreton Bay does not currently exhibit the invasiveness of 

that in the Mediterranean, the genetic, morphological and physiological similarities 

between the invasive “aquarium-Mediterranean” strain and the Moreton Bay 

population of C. taxifolia indicates the potential for the expansion of this 

opportunistic macroalga in Moreton Bay. The current study presents an opportunity 

to study C. taxifolia in its native habitat as a way of understanding its ecological 

characteristics. As C. taxifolia is native to Moreton Bay, it seems likely that natural 

controls on its expansion are present, although these may be compromised by 

declining water quality from anthropogenic causes. 


Introduction


2.4 OBJECTIVES OF THE PRESENT STUDY 

The present study was designed to investigate the current distribution of C. taxifolia in 

Moreton Bay and to compare this with its distribution five years ago, to detect any 

changes in its spatial distribution between 1998 and 2003. Interactions between 

C. taxifolia and Moreton Bay seagrass species were explored using replicated 

manipulative experiments. These were designed to investigate the potential of toxins 

in C. taxifolia extract to affect seagrasses, and to examine the effects of physical 

disturbance on C. taxifolia and seagrass. 


Introduction


3. MATERIALS AND METHODS 

3.1 STUDY AREA 

Moreton Bay is a shallow subtropical 1523 km 2 embayment adjacent to the city of 

Brisbane in south-east Queensland, Australia (approximately 27.5º S, 153.3º E) 

(Figure 2). It is largely enclosed and sheltered to the east by a series of barrier sand 

islands (Moreton, North and South Stradbroke Islands). Moreton Bay exhibits strong 

east-west and north-south gradients in water quality due to terrigenous inputs in the 

western and southern areas from its 21,220 km 2 catchment area, and increased oceanic 

flushing in the eastern and northern Bay (Neil, 1998; Dennison and Abal, 1999). 

South-east Queensland supports a population of more than 2 million people, most of 

whom are located within the Moreton Bay catchment area (Skinner et al., 1998). This 

region has been the fastest-growing region of Australia for the past decade, and has 

been one of the most rapidly growing areas in the world over the last 50 years 

(Skinner et al., 1998). As much of the population growth is occurring on the coastal 

floodplain and along the river estuaries, increased pressure on the catchment and 

Moreton Bay is to be expected from increased sewage, intensive land use and more 

demands on the waterways (Dennison and Abal, 1999). 

Despite these pressures and changes, Moreton Bay supports a high diversity of habitat 

types, with soft sediment areas supporting extensive seagrass meadows (25,000 ha) 

and mangrove forests (14,000 ha), and hard substrates supporting diverse coral and 

macroalgal communities (Abal et al., 1998; Dennison and Abal, 1999). These 

habitats in turn support a high biological diversity of other species, resulting in a 

unique assemblage of southern temperate and northern tropical species (Davie and 

Hooper, 1998). 

All field experiments and plant collections for the planthouse experiments were 

performed at Dunwich, North Stradbroke Island, a site with relatively good water 

quality (Dennison and Abal, 1999) (Figure 2). 


Materials and Methods

Caboolture 

Caboolture 

River 

Pine 

River 

Brisbane 

city 

Brisbane 


�� N 

Bribie 

Island 

Deception 

Bay 

Bramble 

Bay 

Brisbane Brisbane 

River 

N 

MORETON 

BAY 

Waterloo 

Bay 

Logan 

River 

0 

20 

LANDSAT ETM 21/3/2003 

GEOIMAGE 

Moreton Moreton 

Island Island 

Dunwich 

North 

Stradbroke 

Island 

40 km 

Figure 2. Map of Moreton Bay in south-east Queensland, showing the location of the 

field experiments and collections, in One Mile Harbour, Dunwich, North Stradbroke 

Island. 



3.2 BENTHIC SURVEYS 

3.2.1 Selection of sites 


In 1998, approximately 1000 sites with less than 5 m water depth across Moreton Bay 

were surveyed for benthic species and cover, including seagrass and algal species 

(Udy et al., 1999). Of these sites, 44 had some cover of Caulerpa macroalgae 

(species not recorded). The current study re-surveyed all 44 sites which had Caulerpa 

present in 1998, as well as 148 adjacent sites which previously recorded no cover of 

Caulerpa species, giving a total of 192 sites surveyed in both 1998 and 2003. In the 

current surveys (2003), the species of Caulerpa were also recorded. An additional 26 

sites were quantitatively surveyed in 2003. Reports from Queensland Parks and 

Wildlife marine park rangers and from staff and students from the Marine Botany 

Group at The University of Queensland resulted in a further 25 sites where presence 

of C. taxifolia was recorded. For the purposes of analysis, Moreton Bay was divided 

up into four regions (eastern Moreton Bay, Pumicestone Passage, southern Moreton 

Bay and western Moreton Bay) (Figure 3). 

3.2.2 Survey technique and analyses 

Geographic coordinates (latitude and longitude) were available for each site, and sites 

were relocated using a handheld global positioning system (GPS). At each site, a 10 

m snorkel transect was performed to estimate and record species composition and 

percent cover of benthic species such as macroalgae and seagrasses, and substrate 

type such as bedrock, sand and mud. A modified Braun Blanquet scale was used to 

estimate percent cover, with cover estimated to the nearest 5% (Mueller-Dombois and 

Ellenberg, 1974). The spatially explicit data enabled the use of geographic 

information systems (GIS) technology to produce detailed maps and conduct spatial 

analysis of each region along with benthic characteristics, using ArcView GIS 

Version 3.2 software package. 

Change in percentage cover of Caulerpa 1998 – 2003 was analysed using a dependent 

samples t-test for all of Moreton Bay and also for each region. A grouped 

independent t-test was used to compare sites with increased cover to those with 

reduced cover. 



A 

Brisbane city 

Survey site 


Bribie 

Island 

B 

Moreton 

Bay 

Moreton 

Island 

North 

Stradbroke 

Island 

Figure 3. Location of sites surveyed in 2003 for Caulerpa taxifolia. These were separated into the 

regions A: Pumicestone Passage; B: western Moreton Bay; C: eastern Moreton Bay; and D: southern 

Moreton Bay. 


Materials and Methods 

D 

C

3.3 RECIPROCAL TRANSPLANTS 

3.3.1 Site Description 


To examine competitive interactions and the effect of physical disturbance, reciprocal 

transplant experiments were performed between a monospecific C. taxifolia bed and a 

monospecific Zostera capricorni seagrass bed in similar water depth (~80 cm at low 

tide) in One Mile Harbour, Dunwich, North Stradbroke Island (Figure 2, page 8). 

3.3.2 Experimental design, measurements and analyses 

In the reciprocal transplant experiment, a 122 mm diameter stainless steel corer was 

used to take a core to a sediment depth of 10 cm. Four C. taxifolia cores were 

removed, leaving holes in the sediment. Four Z. capricorni cores were then taken and 

placed in the holes left by the C. taxifolia cores. The C. taxifolia cores were then 

placed in the holes left by the cores in the Z. capricorni patch. Transplant controls 

consisted of four cores of C. taxifolia replaced in their original holes, and was 

repeated for Z. capricorni (Figure 4). The location of the cores were marked using 

galvanised tent pegs with floating plastic chain attached and these were inserted in the 

middle of the core. Survivorship of the cores was recorded three months after the 

commencement of the experiment. Frond density and the distance grown away from 

the original core were also recorded for the C. taxifolia cores. Due to poor 

survivorship of the Z. capricorni cores, other measurements could not be used. 

Results were analysed using a general linear model. 

Caulerpa taxifolia Zostera capricorni 

Figure 4. Conceptual diagram depicting experimental design of the reciprocal transplant experiment. 



3.4 SEAGRASS AQUARIA EXPERIMENTS 


Conceptual diagrams of these two experiments are shown in Figures 5, 6, 7 and 8. 

3.4.1 Effect of Caulerpa taxifolia extract on three seagrass species 

This experiment was designed to investigate the effects of C. taxifolia extract on three 

Moreton Bay seagrass species: Z. capricorni, Syringodium isoetifolium (Aschers.) 

Dandy (Potamogetonales, Magnoliophyta) and Cymodocea serrulata (R. Br.) Aschers 

(Potamogetonales, Magnoliophyta). Cores of these three seagrass species were 

collected from One Mile Harbour, Dunwich, North Stradbroke Island (Figure 2, page 

8), using 106 mm diameter stainless steel corers. Intact cores were transferred into 

black plastic flower pots lined with ziplock bags, and transported to the Moreton Bay 

Research Station, Dunwich, North Stradbroke Island in bins full of seawater. 

Intact cores were placed into aerated polyvinylchloride (PVC) tanks (1.5 m x 60 cm 

x 30 cm). Three cores (one of each species) were randomly placed in each tank (12 

tanks in total) and left to acclimate for approximately one month prior to the 

initiation of experiments. Approximately 80% of incident light passed through the 

roof of the planthouse. The addition of 50% neutral density shadecloth reduced the 

light reaching the seagrasses to approximately 40% of incident light, which 

simulated ambient light conditions and is above the minimum light requirement for 

seagrasses (Duarte, 1991; Dennison et al., 1993; Longstaff, 2003). The whole 

planthouse was enclosed by clear plastic screens to prevent freshwater 

contamination from precipitation. Each individual tank system consisted of two 

tanks; a lower water storage tank (~300 L) and an upper tank (~250 L) in which the 

seagrass cores were situated. Water was pumped up from the lower tank using 12 V 

bilge pumps, and airstones in each upper tank ensured that the water was well 

aerated. Both tanks were filled with fresh seawater collected from One Mile 

Harbour, North Stradbroke Island. Water loss from the tanks occurred due to 

evaporation and to compensate for this, carbon-filtered fresh water was added as 

required to maintain seawater salinity (~36 ‰). 



A. 


Figure 6. A: Planthouse at Moreton 

Bay Research Station, North 

Stradbroke Island; and B: Three 

seagrass species acclimating in 

aquarium. 

Figure 5. Conceptual diagram depicting the experimental design for the seagrass aquaria experiment, using three species 

of seagrass, Cymodocea serrulata, Syringodium isoetifolium and Zostera capricorni.. 


Materials and Methods 

B.

A. 


B. 

C. 

Figure 8. Zostera capricorni seagrass 

treatments. A: control; B: Low C. taxifolia 

dose; and C: High C. taxifolia dose. 

Figure 7. Conceptual diagram depicting the experimental design for the seagrass aquaria experiment, using Zostera 

capricorni seagrass. 



3.4.2 Experimental design 


60 cores of C. taxifolia (106 mm diameter) were collected and washed and ground into 

a homogeneous paste using an electric blender. This paste was applied to the surface of 

the sediment of the pots of seagrass using a cut-off 60 ml syringe. Three treatments, 

replicated in four tanks, were 1) control (no C. taxifolia extract added); 2) low dose of 

C. taxifolia extract; and 3) high dose of C. taxifolia extract. The three cores of seagrass 

in each tank were subjected to the same treatment to prevent contamination. The low 

dose of C. taxifolia extract treatment consisted of the equivalent of one core of 

C. taxifolia biomass per core of seagrass (30 ml of C. taxifolia extract), and the high 

dose of C. taxifolia extract consisted of the equivalent of four cores of C. taxifolia 

biomass per core of seagrass (120 ml of extract). 

Prior to initiation of the experimental treatments, initial measurements were taken of 

seagrass shoot density of each core, the number of leaves per shoot of 10 haphazardlychosen 

shoots within each core, and the maximum leaf length of the longest leaf of 10 

haphazardly-chosen shoots in each core. These measurements were repeated each 

week for the three-week duration of the experiment. Fluorescence using the PAM 

(pulse-amplitude modulated) fluorometer was also measured prior to experimental 

treatments. Fluorescence was measured every three days for the duration of the 

experiment. This experiment was terminated when it became apparent that the 

seagrass cores, particularly those of Z. capricorni were experiencing stress that was 

independent of the experimental treatments. 

3.4.3 Effect of Caulerpa taxifolia extract on Zostera capricorni 

Due to the variability of response of Z. capricorni in the experiment with three 

seagrass species, the above experiment was repeated using only Z. capricorni and 

with the following additional changes to the experimental design (Figures 7 and 8). 

Larger cores were collected (36 in total; 150 mm diameter) and acclimation was 

limited to one week in an attempt to reduce the stress to the seagrass that was apparent 

after five weeks of acclimation in the previous experiment. 

An additional 36 Z. capricorni shoots were haphazardly collected at the same time 

and from the same area as the cores. These shoots were analysed for pigment 

concentration, for comparison with shoots harvested from the experimental cores at 




the middle and at the conclusion of the experiment. The mean and standard error of 

these 36 shoots were used as the initial values for all the treatments. 

PAM fluorometry and shoot density measurements were performed every three and 

seven days, respectively. Maximum leaf length and the number of leaves per shoot 

were not measured. At the conclusion of the experiment, one random core from each 

tank was analysed for biomass. Half the water in the tanks was exchanged for fresh 

seawater every two weeks for the five-week duration of the experiment. 

3.4.4 PAM fluorometry 

The photochemical response of the seagrasses to the treatments was determined using 

a PAM fluorometer (Walz, Germany) which provides rapid and non-destructive 

photosynthetic measurements (Schreiber and Bilger, 1987). Maximum Photosystem 

II quantum yield (Fv /Fm ratio) was measured by emitting a saturating pulse of light to 

the dark-adapted photosystem. The resulting emitted fluorescence will be at a 

maximum and the photochemical efficiency or yield was calculated as 

(Fv /Fm) = (Fm – Fo)/Fm 

where Fo is initial fluorescence, Fm is maximum fluorescence and Fv is the difference 

between them (Schreiber et al., 1994). 

The fluorescence signal was measured just above the leaf sheath at the base of whole 

seagrass shoots. Measurements were taken on three haphazardly-chosen shoots in 

each core. Fluorescence signals were measured every three days for the duration of 

the experiment, and measurements were started approximately one hour after sunset 

each evening which removed the need to dark-adapt each shoot. 

3.4.5 Pigment analysis and biomass measurements 

At the conclusion of the experiment, one random core from each of the 12 tanks was 

immediately separated into above- and below-ground biomass. Above-ground 

biomass consisted of all live shoots, and below-ground biomass consisted of rhizomes 

and roots. The samples were washed in a 500 µm sieve to remove adhering sediment 

and dried in a drying oven at 65˚C overnight to obtain dry weight. 




For chlorophyll analysis, a 2 cm section of the second-youngest seagrass leaf was 

clipped off 2 cm above the leaf sheath. Sample surface area and wet weights were 

determined prior to analysis. The leaf sections were macerated with a razor blade 

then ground in a darkened room using a mortar and pestle in 10 ml of 90% acetone. 

The extracts were stored at 0 °C in the dark for 24 hours and then centrifuged in an 

IEC Centra-3C centrifuge at 2400 rpm for 15 minutes to settle any suspended 

material. Absorbances of the extracts were measures in a Pharmacia LKB Ultrospec 

III spectrophotometer at 725, 663 and 645 nm (Dennison, 1990). Chlorophyll a and b 

concentrations were calculated from these absorbances (Arnon, 1949). 

3.4.6 Statistical analyses 

Six tanks were located along the north-east wall of the planthouse and six along the 

south-west wall (Figure 9). To test for any potential difference in light regime 

received by the two rows of tanks, ‘Block’ was included as a factor in the repeated 

measures analysis of variance (ANOVA) model. Tank arrangement had a negligible 

effect on the response variables, therefore measurements were pooled. PAM 

fluorometry, shoot density, morphology (leaves per shoot and maximum leaf length), 

and pigment values were analysed using a repeated measures analysis of variance 

(ANOVA) model. All measurements within a tank were pooled. Biomass values 

were analysed using a one-way ANOVA model and a Fisher’s post-hoc LSD test was 

used to test for differences between means. 

N 

Block 1 

Block 2 

Figure 9. Conceptual diagram depicting the arrangement of the tanks within the planthouse at Moreton 

Bay Research Station, North Stradbroke Island. 



4. RESULTS 

4.1 BENTHIC SURVEYS 

4.1.1 Overall in Moreton Bay 


In the 1998 surveys, only the genus of Caulerpa was recorded, not the species. The 

2003 surveys did record species, however only C. taxifolia was found on the surveys. 

In the 1998-2003 comparison, only the genus Caulerpa will be referred to. It is likely 

that the majority of the Caulerpa occurrences in 1998 were indeed C. taxifolia 

(J. Udy, pers. comm.). 

A total of 218 sites were quantitatively surveyed in 2003 for C. taxifolia cover. Of 

these, 71 sites had an average of 55% cover of C. taxifolia. There were an additional 

25 sites where C. taxifolia was reported by other sources, resulting in 96 sites where 

Caulerpa was present in 2003, compared with 44 out of more than 1000 sites 

surveyed in 1998 (Figure 10). 

Of the 218 sites surveyed in 2003, 192 had been previously surveyed in 1998, 

allowing for analysis of change in Caulerpa spatial distribution and cover over this 

five-year period (Table 1). There was a net gain of 12 sites where Caulerpa was 

observed in 2003 (56 sites) compared to 1998 (44 sites). However, the sites where 

C. taxifolia was found in 2003 were not always the same sites at which Caulerpa was 

found in 1998. Cover of Caulerpa increased at 55 sites, and reduced at 27 sites. The 

magnitude of the increase in cover, when it occurred, was significantly higher 

(p = 0.047) than the magnitude of any reduction in cover (Table 4.1.1 in Appendix, 

page 58). Percent cover of Caulerpa increased at all but one site where it was present 

in both 1998 and 2003 (Table 1). There was a significant increase (p = 0.0002) in 

cover of Caulerpa over the entire Moreton Bay area, and also regionally in the 

western Moreton Bay (p = 0.019) and southern Moreton Bay (p = 0.001) regions. 


Results

Brisbane city 

Bribie 

Island 

C. taxifolia distribution 2003 

Present 

Absent 


Moreton 

Bay 

Moreton 

Island 

North 

Stradbroke 

Island 

Figure 10. Map of Moreton Bay showing locations of Caulerpa taxifolia presence/absence. 


Results

Table 1. Summary of benthic survey results. 

Mean % 

cover of 

additional 

sites 

No. of sites 

with 

anecdotal 

reports of 

C. taxifolia 

presence in 

2003 

Mean % cover 

change of sites 

with increased 

Caulerpa cover 

since 1998 

Mean % cover 

change of sites 

with reduced 

Caulerpa cover 


Mean change 

in % cover of 

Caulerpa 


Mean % 

cover of 


in 2003 

Mean % 

cover of 

Caulerpa in 

1998 

Net no. of sites 

lost (–) or 

gained (+) 

Caulerpa since 

1998 

No. of sites 

with 


in 2003 

No. of sites 

with 

Caulerpa in 

1998 

No. of sites 

surveyed 

1998 and 

2003 


– 13 95 

(n = 6) 

– -5 -5 

(n = 1) 

4 1 0 -1 5 

(n = 1) 

Eastern 

Moreton Bay 

5 26 

(n = 4) 

+9 

(n = 9) 

-39 -80 

(n = 1) 

11 

(n = 9) 

22 2 9 +7 50 

(n = 2) 

Pumicestone 

Passage 


Results 

2 67 

(n = 3) 

+61 

(n = 15) 

+55 -7 

(n = 8) 

69 

(n = 15) 

64 12 15 +3 14 

(n = 12) 

Southern 

Moreton Bay 

5 60 

(n = 2) 

+47 

(n = 31) 

+25 -34 

(n = 17) 

59 

(n = 32) 

102 29 32 +3 34 

(n = 29) 

Western 

Moreton Bay 

25 66 

(n = 15) 

+45 

(n = 55) 

+23 -26 

(n = 27) 

54 

(n = 56) 

Total 192 44 56 +11 29 

(n = 44)

4.1.2 Western Moreton Bay 


4.1.2.1 Caulerpa taxifolia distribution in 2003 

105 sites were quantitatively surveyed in 2003 for C. taxifolia cover in the western 

Moreton Bay region. 34 sites had an average of 56% cover (eight of these sites had 

100% cover). During 2002-3, there were also five additional sites where C. taxifolia 

was reported by other sources (Figure 11). These sites were located east of Fishermen 

Islands, near the mouth of the Brisbane River. Dense populations were present from 

Fishermen Islands south to Manly. However, no C. taxifolia was observed south of 

Manly to Wellington Point. 

Brisbane 

River 

Fisherman 

Islands 

Wynnum 

Manly 

Mud 

Island 

Wellington 

Point 

Figure 11. Map of western Moreton Bay region showing 

distribution of Caulerpa taxifolia in 2003. 

C. taxifolia cover 2003 

Absent 

Present (anecdotal) 

1-25% cover 

26-50% cover 

51-75% cover 

76-100% cover 


Results


4.1.2.2 Change in Caulerpa distribution 1998-2003 

102 of the 105 sites surveyed in the western Moreton Bay region in 2003 were 

previously surveyed in 1998. Of these 102 sites, 32 had an average of 59% cover of 

C. taxifolia. In 1998, 29 sites had Caulerpa present with an average of 34% cover. 

Caulerpa cover increased by an average of 47% at 31 sites since 1998, and 19 of these 

had no Caulerpa in 1998. Conversely, Caulerpa was absent from 16 out of 17 sites 

where it occurred in 1998, with an average reduction of 34% cover. Cover of 

Caulerpa increased at 12 out of 13 sites at which it was present in both 1998 and 2003 

(Figure 12). There was no Caulerpa east of Fisherman Islands in 1998, however in 

2003, eight sites had C. taxifolia in this area. Although Caulerpa distribution and 

cover were variable between 1998 and 2003, there was a significant overall increase 

(p = 0.0194) in Caulerpa cover between 1998 and 2003. Caulerpa is generally 

colonising bare sediment in this region, with an average decline of 38% bare substrate 

cover at the sites where Caulerpa had increased. There was an average increase of 

43% seagrass cover at the sites where Caulerpa cover had reduced. 

Brisbane 

River 

Fisherman 

Islands 

Wynnum 

Manly 



Mud 

Island 

Figure 12. Map of western Moreton Bay region showing 

change in cover of Caulerpa 1998-2003. 

Change in cover of 

C. taxifolia 1998-2003 

Reduction 76-100% cover 




No change (absent both years) 

Increase 1-25% cover 





Results

4.1.3 Southern Moreton Bay 



70 sites were quantitatively surveyed in 2003 for C. taxifolia cover in the southern 

Moreton Bay region. 18 sites had an average of 69% cover (five of these sites had 

100% cover). During 2002-3, there were also two additional sites where C. taxifolia 

was reported by other sources (Figure 13). C. taxifolia was distributed across the 

whole southern Moreton Bay region, with dense populations at Cleveland, Victoria 

Point and in the Pelican Banks area. 

Cleveland 

Victoria Point 

Macleay 

Island 

Russell 

Island 

Pelican 

Banks 

North 

Stradbroke 

Island 

Figure 13. Map of southern Moreton Bay region showing distribution of Caulerpa 

taxifolia in 2003. 


Absent 


1-25% cover 

26-50% cover 

51-75% cover 

76-100% cover 


Results



64 of the 70 sites surveyed in the southern Moreton Bay region in 2003 had 

previously been surveyed in 1998. Of these 64 sites, 15 had an average of 69% cover 

of C. taxifolia in 2003. In 1998 only 12 sites had Caulerpa present with an average of 

14% cover. Cover of Caulerpa increased by an average of 61% at 15 sites since 

1998, and 11 of these sites had no Caulerpa five years ago (Figure 14). Conversely, 

Caulerpa was absent from eight sites in 2003 where it was present in 1998, resulting 

in an average reduction of 7% cover. Caulerpa cover increased by an average of 45% 

at all four sites at which it was present in both 1998 and 2003. There was a net gain of 

sites and cover of Caulerpa, resulting in a significant increase (p = 0.0011) in 

Caulerpa cover between 1998 and 2003. Caulerpa is replacing seagrasses and bare 

sediment in this region, with an average decline of 38% seagrass cover and 22% bare 

substrate cover at the sites where Caulerpa had increased. 

Cleveland 

Victoria Point 

Macleay 

Island 

Russell 

Island 

Pelican 

Banks 

North 

Stradbroke 

Island 

Figure 14. Map of southern Moreton Bay region showing change in cover of 

Caulerpa 1998-2003. 













Results

4.1.4 Pumicestone Passage 



33 sites were quantitatively surveyed in 2003 for C. taxifolia cover. 13 sites had an 

average of 16% cover. During 2002-3, there were also five additional sites where 

C. taxifolia was reported by other sources (Figure 15). The majority of these 

additional sites were located at the southern end of Pumicestone Passage and around 

Sandstone Point in northern Deception Bay. However, one site was reported at the 

northern end of Pumicestone Passage. Although cover was not quantitatively 

assessed at these additional sites, reports suggest cover ranged from moderate (~20%) 

to dense (up to 70%). 

Pumicestone 

Passage 

Bribie 

Island 

Sandstone Point 

Deception Bay 

Figure 15. Map of Pumicestone Passage region showing distribution 

of Cauerpa taxifolia in 2003. 


Absent 


1-25% cover 

26-50% cover 

51-75% cover 

76-100% cover 


Results



22 of the 33 sites surveyed in the Pumicestone Passage region in 2003 had previously 

been surveyed in 1998. Of these 22 sites, nine had an average of 11% cover of 

C. taxifolia in 2003. The number of sites with Caulerpa increased by seven sites, as in 

1998 only two sites had Caulerpa. Cover of Caulerpa increased by an average of 9% at 

nine sites since 1998, and eight of these did not have Caulerpa five years ago (Figure 

16). Caulerpa cover reduced at only one site since 1998, from 80% cover to absent. 

There was an increase in Caulerpa spatial distribution from 1998 to 2003, however this 

change was not significant (p = 0.9914). The large reduction in cover at one site 

influenced this result. When this site was removed from the analysis, there was a 

significant increase (p = 0.048) in cover of Caulerpa since 1998 in the Pumicestone 

Passage region. Caulerpa is replacing seagrasses in Pumicestone Passage, with an 

average decline of 14% seagrass cover at the sites where Caulerpa increased. 

Pumicestone 

Passage 

Bribie 

Island 

Sandstone Point 

Deception Bay 

Figure 16. Map of Pumicestone Passage region showing change in 

cover of Caulerpa 1998-2003. 













Results

4.1.5 Eastern Moreton Bay 


4.1.5.1 2003 Caulerpa taxifolia distribution 

There was an average of 95% C. taxifolia cover at six out of the 10 sites quantitatively 

surveyed in 2003 in the eastern Moreton Bay region. During 2002-3, there were also 

13 additional sites where C. taxifolia was reported by other sources (Figure 17). 

These sites mainly occurred on the eastern banks, with one site at Point Lookout on 

the oceanic side of North Stradbroke Island. Although quantitative cover was not 

recorded at these sites, the anecdotal reports suggest that C. taxifolia occurs only 

sparsely on the banks and is ephemeral in its temporal distribution. 

Moreton 

Banks 

Peel 

Island 

Amity 

Banks 

Moreton 

Island 

Dunwich 

North 

Stradbroke 

Island 

Point Lookout 

Figure 17. Map of eastern Moreton Bay region showing distribution 

of Caulerpa taxifolia in 2003. 


Absent 


1-25% cover 

26-50% cover 

51-75% cover 

76-100% cover 


Results


4.1.5.2 Change in Caulerpa distribution since 1998 

In eastern Moreton Bay in 1998, only one site out of 53 had Caulerpa present with 

5% cover. No Caulerpa was present at this site or at three additional adjacent sites 

in 2003 (Figure 18). Due to the low number of sites and low percentage of 

Caulerpa cover in 1998, there was no significant change (p = 0.391) in Caulerpa 

cover over the last five years. 

Moreton 

Banks 

Peel 

Island 

Amity 

Banks 

Moreton 

Island 

Dunwich 

North 

Stradbroke 

Island 

Point Lookout 

Figure 18. Map of eastern Moreton Bay region showing change in cover of 

Caulerpa 1998-2003. 













Results

4.2 RECIPROCAL TRANSPLANTS 


None of the Z. capricorni transplants (transplanted into C. taxifolia and into 

Z. capricorni) survived the three-month duration of the experiment (Table 2). All of 

the C. taxifolia transplanted into C. taxifolia (controls) survived, while 50% of the 

C. taxifolia transplanted into Z. capricorni survived. Due to the low survivorship of 

the transplants in general, there was no significant effect of treatment (p = 0.907) or 

species (p = 0.869) on survival. 

Destination 

of transplant 

Source of transplant 

% survival Z. capricorni C. taxifolia 

Z. capricorni 0% 50% 

C. taxifolia 0% 100% 

Of the original four C. taxifolia cores transplanted into Z. capricorni, two (50%) were 

still alive after three months. Of the two surviving C. taxifolia cores transplanted into 

the Z. capricorni bed, one core doubled the original number of fronds and expanded 

by an average of 18 cm away from the perimeter of the original core. The other 

surviving core maintained the original frond number, and expanded an average of 14 

cm away from the perimeter of the original core (Figure 19). This experiment 

suggests that Z. capricorni is more susceptible to small-scale physical disturbance 

than C. taxifolia, and that physical disturbance to C. taxifolia can result in its 

colonisation and expansion. 

% of original 

frond density 

Table 2. Percentage of transplants surviving after three months. 

200 

100 

24 cm 

13 cm 

20 cm 

14 cm 

20 cm 

14 cm 

17 cm 

15 cm 

Original core 

Growth away 

from perimeter 

of original core 

Figure 19. Change in frond density 

and distance of growth away from 

the original core after three months 

of the two surviving Caulerpa 

taxifolia cores transplanted into 

Zostera capricorni. 


Results


4.3 EFFECT OF CAULERPA TAXIFOLIA EXTRACT ON SEAGRASSES 

In the first experiment with three seagrass species, shoot density and maximum leaf 

length of the seagrass Syringodium isoetifolium were the only variables that were 

significantly affected by the addition of C. taxifolia extract (Table 4.3 in Appendix, 

page 58). In the second experiment with Z. capricorni, shoot density was significantly 

affected by the addition of C. taxifolia extract (Table 4.3.4.2 in Appendix, page 60). 

4.3.1 Shoot density of three seagrass species 

There was a significant difference (p = 0.010) in seagrass species response to exposure 

to C. taxifolia extract (Table 4.3.1.1 in Appendix, page 58). S. isoetifolium was the 

seagrass species most affected by the addition of C. taxifolia extract, with a significant 

reduction (p = 0.007) in shoot density (Figure 20; Table 4.3.1.2 in Appendix, page 59). 

Z. capricorni had the greatest decline in shoot density of all species. One control core 

and one core of high C. taxifolia extract treatment died before the end of the 

experiment. Although there was a greater decline of Z. capricorni, there was no 

significant difference (p = 0.384) between treatments. Shoot density of Cymodocea 

serrulata was most affected by exposure to high concentration of C. taxifolia extract but 

overall this species was the least affected by exposure to C. taxifolia extract and there 

was no significant difference between treatments (p = 0.372). Fisher’s post-hoc LSD 

test showed that S. isoetifolium subjected to the high dose of C. taxifolia extract was 

significantly less than the shoot densities of both the control (p = 0.009) and low dose of 

C. taxifolia extract (p = 0.044). 


Results

% of original shoot density 



120 

100 

80 

60 

40 

20 

120 

100 

0 

0 7 

Time (days) 

14 

80 

60 

40 

20 

0 

120 

100 

80 

60 

40 

20 

0 

Cymodocea serrulata 

Syringodium isoetifolium 

0 7 14 

Time (days) 

Zostera capricorni 

0 7 14 

Time (days) 


A 

B 

C 

a 

a 

Figure 20. Shoot density responses of three 

seagrass species, A: Cymodocea serrulata; 

B: Syringodium isoetifolium; and C: Zostera 

capricorni to three different concentrations of 

Caulerpa taxifolia extract (error = standard 

error of the mean). Different letters at the 

end of the graph (a, b) indicate a significant 

difference (p < 0.05) according to the 

repeated measures ANOVA conducted for 

each of the three species. 

a 

b 

b 

a 

a 

a 

a 

Control 

Low C. taxifolia dose 

High C. taxifolia dose 


Results


4.3.2 Maximum leaf length of three seagrass species 

Maximum leaf length was significantly different (p = 0.000) between species (Figure 

21; Table 4.3.2.1 in Appendix, page 59). S. isoetifolium was the seagrass species 

most affected by the addition of C. taxifolia extract, with a significant reduction 

(p = 0.000) in maximum leaf length (Table 4.3.2.2 in Appendix, page 59). 

Z. capricorni maximum leaf length was highly variable, due to the loss of one control 

core and one high C. taxifolia treatment core and there was no significant difference 

(p = 0.069) between treatments. Cymodocea serrulata was least affected by the 

treatments (p = 0.462). Fisher’s post-hoc LSD test showed that the maximum leaf 

length of S. isoetifolium subjected to the low dose of C. taxifolia treatment was 

significantly lower (p = 0.004) than the high dosage treatment which was significantly 

lower (p = 0.000) than the control. However this result may be an artefact of the 

random variability of the initial measurements (on day 0 – prior to application of 

experimental treatments) in which S. isoetifolium exposed to the low C. taxifolia 

treatment already had a lower maximum leaf length than the high dosage treatment 

and the control, hence the C. taxifolia may have only enhanced a trend that was 

already present in the cores. 


Results

Maximum leaf length (mm) 



120 

100 

80 

60 

40 

20 

0 

120 

100 

80 

60 

40 

20 

120 

100 

0 

0 7 

Time (days) 

14 

80 

60 

40 

20 

0 

Cymodocea serrulata 

0 7 14 

Time (days) 

Syringodium isoetifolium 

Zostera capricorni 

0 7 14 

Time (days) 


Figure 21. Maximum leaf length responses of 

three seagrass species, A: Cymodocea serrulata; 

B: Syringodium isoetifolium; and C: Zostera 


Caulerpa taxifolia extract (error = 1 standard 

error of the mean). Different letters at the end of 

the graph (a, b, c) indicate a significant difference 

(p < 0.05) according to the repeated measures 

ANOVA conducted for each of the three species. 

A 

B 

C 

a 

a 

c 

b 

a 

a 

a 

Control 




Results


4.3.3 PAM fluorometry and leaves per shoot of three seagrass species 

The photosynthetic response and the number of leaves per shoot were significantly 

different between species (p = 0.000 for both variables). For all species there was no 

significant effect of treatment on these variables (p = 0.212 and p = 0.192, 

respectively) (Table 4.3 in Appendix, page 58). 

4.3.4 Effect of Caulerpa taxifolia extract on Zostera capricorni 

A repeated measures ANOVA showed a significant effect (p = 0.024) of treatment on 

shoot density of Z. capricorni, and Fisher’s post-hoc LSD test showed that the shoot 

density of the low treatment was significantly lower than the control (p = 0.030) and 

high treatments (p = 0.011) (Figure 22; Table 4.3.4.1 in Appendix, page 60). Treatment 

had no significant effect on the other variables measured (PAM fluorometry, biomass 

and pigment concentration) (Table 4.3.4.2 in Appendix, page 60). 


100 

90 

80 

70 

60 

0 7 14 

Time (days) 

21 28 35 

Control 



Figure 22. Shoot density response of Zostera 


Caulerpa taxifolia extract (error = 1 standard error 

of the mean). 

There was no significant effect (p = 0.210) of treatment on the photosynthetic 

response of Z. capricorni, and these measurements were discontinued when the 

continuing declining health of the seagrass made the photosynthetic response data 

unreliable (Figure 23). Although there was no significant difference in yield with 

treatment, there was a significant effect of tank arrangement in the planthouse. Six 

tanks were located along the north-east wall of the planthouse and six along the southwest 

wall (Figure 9, page 17). To test for any difference in light regime received by 

the two rows of tanks, ‘Block’ was included as a factor in the ANOVA, and 

significantly affected the photosynthetic response of Z. capricorni, both independently 


Results


(p = 0.000) and in interaction with treatment (p = 0.000) (Table 4.3.4.3 in Appendix, 

page 60). 

Fisher’s post-hoc LSD test showed that the photosynthetic response of the high 

C. taxifolia dose treatments in Block 1 (along the north-east wall) were significantly 

lower than the high C. taxifolia dose treatments in Block 2 (along the south-west wall) 

(p = 0.000), and the same result was obtained for the low C. taxifolia treatment (p = 

0.000). There was very little difference between the minimum mean (729 for the low 

C. taxifolia dose treatment in Block 1) and the maximum mean obtained (773 for the 

high C. taxifolia dose treatment). The random allocation of treatments to tanks 

resulted in an uneven block design, with one control tank, two low C. taxifolia dose 

treatment tanks and three high C. taxifolia treatment tanks located in Block 1. Block 

2 contained three control tanks, two low C. taxifolia dose treatment tanks and one 

high C. taxifolia treatment tank. This uneven design, with the lack of tank replicates 

of the control and high C. taxifolia dose treatments may make this apparent 

significance unreliable. 

Effective quantum yield (Fv /Fm) 

850 

800 

750 

700 

650 

600 

550 

0 

7 14 21 28 35 

Time (days) 

Control 



Figure 23. Photosynthetic response of Zostera 


Caulerpa taxifolia extract (error = 1 standard error 

of the mean). 


Results

5. DISCUSSION 


There was a significant increase in sites and cover of C. taxifolia in Moreton Bay in 

the last five years, particularly in western and southern regions. In western Moreton 

Bay, C. taxifolia appeared to mainly colonised bare sediments, while in the southern 

Bay and Pumicestone Passage it apparently replaced seagrass. It is interesting to note 

that at the sites where C. taxifolia cover decreased in western Moreton Bay, it 

appeared to be replaced by seagrass, which indicates the potential for seagrasses to 

recover after colonisation by C. taxifolia. There were dense populations present 

around Dunwich at North Stradbroke Island in eastern Moreton Bay, however 

C. taxifolia was only present at low densities on the eastern banks. 

The planthouse experiments showed some significant results, with seagrass shoot 

density being negatively affected by the addition of C. taxifolia extract, however the 

results were highly variable. Reciprocal transplants of C. taxifolia and the seagrass 

Z. capricorni indicated that Z. capricorni is more susceptible to physical disturbance 

than C. taxifolia, which may utilise disturbance as an opportunity for expansion. 

It appears that C. taxifolia and seagrass interactions in Moreton Bay are not 

unidirectional as in the Mediterranean Sea, but are dynamic and changes can occur in 

both directions (de Villèle and Verlaque, 1995). Five processes are hypothesised to 

synergistically affect C. taxifolia distribution and seagrass interactions in Moreton 

Bay. These are high water temperature, water quality decline, physical disturbance, 

allelopathic interactions from C. taxifolia toxins, and the accumulation of sulphide in 

the sediments, a by-product of anaerobic metabolism which is toxic to seagrasses 

(Jorgensen, 1983; Carlson et al., 1994; Goodman et al., 1995; Azzoni et al., 2001) 

(Figure 24, page 38). 

5.1 COMPARISON WITH OTHER CAULERPA TAXIFOLIA POPULATIONS 

The Moreton Bay populations of C. taxifolia are intermediate in biomass, structure 

and morphology between the “invasive-Mediterranean” strain and tropical 

populations (Table 3). In the Mediterranean, biomass of C. taxifolia (480 – 700 g DW 

m -2 ) is much higher than in Moreton Bay (59 – 76 g DW m -2 ) which is higher than 

tropical populations (0.046 g DW m -2 ). Although frond density is much lower in 


Discussion


tropical regions (37 fronds m -2 ), the densities reported in Moreton Bay (4837 – 22,037 

fronds m -2 ) and the Mediterranean (5100 – 13,920 fronds m -2 ) are comparable 

(Garrigue, 1994; Meinesz et al., 1995; Thomas, 2002a). The higher biomass in the 

Mediterranean due to generally longer frond length and increased frond branching 

(Meinesz et al., 1995; Pillen et al., 1998; Thomas, 2002a). The most recent genetic 

study on C. taxifolia supports this hypothesis that the Moreton Bay C. taxifolia is 

intermediate between the “invasive-Mediterranean” strain and tropical populations, 

suggesting that the “invasive-Mediterranean” strain is derived from Moreton Bay 

populations which are in turn derived from tropical populations, involving subspeciation 

at each of these founder events (Meusnier et al., 2002). However, 

Caulerpa is well known to exhibit considerable morphological plasticity in response 

to environmental conditions such as light, temperature and water motion, and this 

would also be an important factor in the differences between tropical, Moreton Bay 

and Mediterranean populations of C. taxifolia (Calvert, 1976; Koehl, 1986; Ohba and 

Enomoto, 1987; Ohba et al., 1992; Collado-Vides and Robledo, 1999). 

Frond density 

(fronds m -2 ) 

Frond length 

(cm) 

Biomass 

(g DW m -2 ) 

Reference 

Moreton Bay 4837 – 22,037 10 – 15 59 – 76 [1], [2] 

Mediterranean Sea 5100 – 13,920 5 – 40 480 – 700 [3] 

New Caledonia 37 2 – 10 1.8 [4] 

Table 3. Comparison of morphology, structure and biomass of Caulerpa 

taxifolia in Moreton Bay, the Mediterranean Sea and tropical New Caledonia. 

References: [1] This study; [2] Thomas, 2002a; [3] Meinesz, et al., 1995; 

[4] Garrigue, 1994. 

5.2 FACTORS AFFECTING CAULERPA TAXIFOLIA DISTRIBUTION IN MORETON BAY 

C. taxifolia in Moreton Bay does not currently exhibit the invasiveness of the 

Mediterranean populations, with considerable temporal and spatial variability in its 

distribution within Moreton Bay. However, the devastating ecological consequences 

of its widespread invasion of the Mediterranean makes it imperative to better 

understand factors that affect its distribution in its native habitat. A number of 

processes are hypothesised to affect C. taxifolia in Moreton Bay (Figure 24). 


Discussion


Figure 24. Conceptual diagram outlining the processes hypothesised to 

affect Caulerpa taxifolia distribution in Moreton Bay, and its potential 

interactions with seagrasses. 


Discussion

5.2.1 Water temperature 


Anecdotal evidence from professional fishermen has suggested that the distribution of 

C. taxifolia in Moreton Bay varies inter-annually (G. Savige, pers.comm.). A possible 

cause of this temporal variability could be changes of water temperature interseasonally. 

Surface water temperature data for Moreton Bay shows that the previous 

two winters (2001 and 2002) were warmer than preceding years (Figure 25; 

Ecosystem Health Monitoring Program, unpub. data). Temperature is one of the most 

important abiotic factors affecting macroalgal growth (Graham and Wilcox, 2000). 

C. taxifolia in the Mediterranean Sea displays high biomass and density in summer 

with some die-off evident over winter (Meinesz et al., 1995). Sustained high seawater 

temperatures have been associated with high population abundance of Caulerpa 

sertularioides (S.G. Gmelin) M. Howe in Mexico (Scrosati, 2001). Moreton Bay 

experiences similar minimum winter temperatures to the Mediterranean Sea, and these 

two populations of C. taxifolia exhibit similar cold tolerance thresholds (Komatsu et 

al., 1997; Chisholm et al., 2000; Phillips and Price, 2002). The 1998 and 2003 

benthic surveys were conducted at similar times of the year (over summer), and the 

warmer winters preceding the 2003 surveys combined with the cooler winters 

preceding the 1998 surveys may have resulted in less die-off of C. taxifolia in winter. 

This may be partially responsible for the overall increase in C. taxifolia distribution 

observed since 1998 in Moreton Bay. 

Surface water temperature (° C) 

30 

25 

20 

15 

10 

Jan-96 

Cool winters 

Jul-96 

Jan-97 

Jul-97 

1998 

surveys 

Jan-98 

Jul-98 

Jan-99 

Jul-99 


Discussion 

Jan-00 

Jul-00 

Jan-01 

Warm winters 

Time 

Figure 25. Surface water temperatures of Moreton Bay from 

January 1996 to May 2003 (Ecosystem Health Monitoring Program, 

unpub. data). Values are means ± one standard error of the mean. 

Jul-01 

Jan-02 

Jul-02 

2003 

surveys 

Jan-03


5.2.2 Caulerpa taxifolia and seagrass interactions 

5.2.2.1 Water quality 

The significant increase of C. taxifolia cover and spatial distribution in western and 

southern areas of Moreton Bay suggest that C. taxifolia distribution may be linked to 

Moreton Bay water quality. There is an east-west and a north-south gradient in water 

quality across Moreton Bay, with eastern and northern areas having generally better 

water quality as they receive greater oceanic flushing and less nutrient and sediment 

inputs (Dennison and Abal, 1999). In contrast, western and southern Moreton Bay are 

more impacted by human pressures, with sediment, stormwater and sewage inputs 

from adjacent rivers resulting in lower and more variable light penetration in these 

regions (Dennison and Abal, 1999; Longstaff, 2003). These gradients may help to 

explain localised changes in C. taxifolia distribution across Moreton Bay. 

In Moreton Bay, low water quality affects seagrasses primarily by light attenuation in 

the water column, principally from suspended sediment and, to a lesser extent, 

phytoplankton (Longstaff, 2003). This reduces not only the quantity but also the 

quality of light reaching seagrass (Dawes, 1998). Macroalgae, including C. taxifolia 

are typically tolerant of lower light conditions than are seagrasses which generally 

require up to 10 times more light than macroalgae (Lüning, 1990; Duarte, 1991; 

Dennison et al., 1993). Thus a decline in water quality in Moreton Bay may give 

C. taxifolia a competitive advantage, even though it is a native species. Alternatively, 

the opportunistic C. taxifolia may colonise the niche left vacant from seagrass loss 

due to poor water quality. Studies in the Mediterranean have associated C. taxifolia 

proliferation with urban wastewater discharge and seagrass loss, with C. taxifolia able 

to utilise the decaying seagrass vegetation in the sediment as a nutrient source 

(Chisholm et al., 1997; Chisholm and Moulin, 2003). 

C. taxifolia has significantly increased its distribution in southern and western 

Moreton Bay. In southern Moreton Bay it has replaced seagrass, while in western 

Moreton Bay it has mainly colonised bare sediment. Turbidity in southern Moreton 

Bay was at a minimum in 1998 but has been increasing since then (Qld 

Environmental Protection Agency, unpub. data) which may have contributed to the 

seagrass loss and C. taxifolia increase in this region. At the sites where C. taxifolia 


Discussion


cover decreased in western Moreton Bay, it was replaced by seagrass, which indicates 

the potential for seagrasses to recover after colonisation by C. taxifolia. Western 

Moreton Bay has exhibited an improvement of water quality since 2000 (Counihan et 

al., 2002) which could enhance recovery of seagrass beds in the region. 

The seagrass Halophila spinulosa (R. Br.) Aschers. (Hydrocharitales, Magnoliophyta) 

was often seen growing with C. taxifolia (pers. obs.). As the deepest-growing seagrass 

species in Moreton Bay (Young and Kirkman, 1975; Abal et al., 1998), it is the most 

vulnerable to reductions in water quality. H. spinulosa usually forms the deep edge of 

the seagrass meadows, with the shallow areas dominated by other species (Abal et al., 

1998). Monitoring of seagrass depth range has suggested that C. taxifolia is replacing 

H. spinulosa at the deep edge of seagrass meadows at sites east of Fisherman Islands in 

western Moreton Bay, and in One Mile Harbour at Dunwich at North Stradbroke Island 

Counihan et al., 2002; N. Udy, pers. comm.; pers. obs.). 

5.2.2.2 Physical disturbance 

Commercial digging for bait worms occurs in four areas in western Moreton Bay 

seagrass beds which are specifically zoned for commercial bloodworm gathering 

(Environmental Protection Agency Qld, 2003) (Figure 26). Commercial bloodworm 

harvesting involves digging up several square metres of seagrass to harvest the 

worms, and the seagrass sods must be replaced after digging. Recent colonisation by 

C. taxifolia has occurred in two of these zones (Figure 26). Previously these areas, 

immediately to the east of Fisherman Islands, were dominated by Z. capricorni, with 

Halophila spinulosa and Halophila ovalis (R. Br.) Hook. (Hyland et al., 1989; Udy et 

al., 1999). The susceptibility of Z. capricorni to physical disturbance suggested by 

this study may provide colonisation opportunities for C. taxifolia, which is able to 

utilise physical disturbance as an opportunity for growth. C. taxifolia has been 

observed growing in recently-dug plots immediately to the east of Fisherman Islands 

(pers. obs.) and this physical disturbance may facilitate the fragmentation and 

therefore spread of C. taxifolia. Shoot density of Z. capricorni is less when growing 

with C. taxifolia in this region, in addition to a decline of Z. capricorni shoot density 

over time when growing with the alga (Thomas, 2002a). 


Discussion

Brisbane 

River 

Fisherman 

Islands 

Wynnum 

Manly 




Figure 26. Map of Western Moreton Bay region showing 

distribution of Caulerpa taxifolia in 2003, and locations of 

commercial bloodworm gathering areas. 

5.2.2.3 Accumulation of sulphide in sediments 

Mud 

Island 

LEGEND 


Absent 


1-25% cover 

26-50% cover 

51-75% cover 

76-100% cover 

Location of commercial 

bloodworm gathering area 

Location of areas 

colonised by C. taxifolia 


Increased flux of organic matter to the sediments stimulates anaerobic bacterial 

metabolism, particularly bacteria utilising sulphate (SO4 2- ) as a terminal electron 

acceptor, reducing it to sulphide (S 2- ) (Jorgensen, 1983). The sulphate-sulphide 

reactions are the main pathway of organic matter transformation in marine sediments 

(Howarth and Teal, 1979; Howarth and Giblin, 1983; Howes et al., 1984). 

Eutrophication and anthropogenic influences may enhance anaerobic sediment 

processes in two ways (Duarte, 2002). First, the reduction of seagrass primary 

production due to shading from suspended sediments and phytoplankton blooms 

reduces the amount of oxygen produced by seagrasses. Seagrasses pump oxygen out 

of their roots to maintain an oxidised zone in their rhizosphere and so decrease 

exposure to the toxic by-products of anaerobic metabolism such as sulphide. A 


Discussion


reduction in the amount of oxygen transported by seagrasses to the rhizosphere would 

allow anaerobic processes to dominate in this area. Second, the increased primary 

production from macroalgae and phytoplankton that is often associated with 

eutrophication leads to a greater input of organic matter to the sediment which 

enhances anaerobic microbial activity. 

Sediments colonised by C. taxifolia in Moreton Bay had typical anaerobic 

characteristics, ie. black colour and sulphide smell (pers. obs.). High sulphide 

concentrations in sediments colonised by C. taxifolia have also been observed in the 

Mediterranean (Chisholm et al., 1997; Fernex et al., 2001) which implies that 

sulphide is not toxic to C. taxifolia as it is to some seagrasses (Carlson et al., 1994; 

Goodman et al., 1995; Azzoni et al., 2001). The leakage of photosynthetically-fixed 

dissolved organic carbon (DOC) from C. taxifolia rhizoids into the surrounding 

sediment further stimulates anaerobic bacterial metabolism, including nitrogen 

fixation and sulphate reduction (Thomas, 2002b; Chisholm and Moulin, 2003). 

5.2.2.4 Caulerpa taxifolia toxins 

The toxins in C. taxifolia represent another potential mechanism for competing with 

seagrass. This was explored with planthouse experiments, and no significant effect on 

growth and physiology of the seagrasses Z. capricorni and Cymodocea serrulata was 

demonstrated. The main toxin in Caulerpa, caulerpenyne, is apparently degraded in the 

presence of light, oxygen and chlorophyll. However, it is unknown if the degradation 

products are also toxic (Guerriero et al., 1994). A wound-activated transformation of 

caulerpenyne into potentially more toxic forms has also been observed (Jung and 

Pohnert, 2001). However, the toxins may still be active in the sediment as marine 

sediments are typically anoxic and dark. The methodology used in the planthouse 

experiments may not have exposed the seagrass to the potentially toxic compounds, as 

the mechanical damage to C. taxifolia during production of the extract and the 

application of it to the light-exposed sediment surface may have reduced the amount of 

toxins in the extract. Additionally, the application of the C. taxifolia extract to the 

sediment surface may have prevented the toxins from reaching the seagrass roots. In 

situ, the C. taxifolia rhizoids and seagrass roots are in close enough proximity for 

exposure to the toxins (pers. obs.). The role of C. taxifolia toxins in allelopathic 

interactions has been explored using seawater containing C. taxifolia extract, however 


Discussion


the role of the toxins in sediment allelopathic interactions suggested by Thomas (2002a) 

has not been attempted prior to the current study. 

There was some effect of C. taxifolia extract observed on the seagrass Syringodium 

isoetifolium, with a reduction of shoot density and maximum leaf length. In contrast, 

there was a general lack of effect of C. taxifolia extract on Cymodocea serrulata. 

S. isoetifolium has a more aerobic rhizosphere than C. serrulata and so may be more 

susceptible to increased anaerobic conditions caused by the addition of organic matter 

in the form of the C. taxifolia extract (Perry, 1997). 

The relative lack of response of the high C. taxifolia treatment on shoot density of 

Z. capricorni, when compared to the control and the low C. taxifolia treatment in the 

second planthouse experiment is difficult to explain and will require further 

investigation. 

5.3 CONCLUSIONS AND RECOMMENDATIONS 

This study has suggested that C. taxifolia is expanding its range in Moreton Bay, 

possibly at the expense of seagrasses. With the potential for water quality 

improvement throughout the Bay from reduced sediment loads and improved 

wastewater treatment, it is possible that seagrasses could re-colonise areas where 

C. taxifolia is distributed. 

South-east Queensland is one of the fastest-growing regions in Australia (Qld 

Department of Local Government and Planning, 2001). The population of the 

region was 2.3 million people in 2000 and is projected to increased to 3.4 million by 

2021 (Qld Department of Local Government and Planning, 2001). A general 

decline in water quality would be expected from this population increase due to 

increased inputs of nutrients and sediments from sewage discharge, run-off and 

disturbance. This could lead to further reductions in seagrass distribution and 

facilitate the spread of C. taxifolia. 

Minimising physical disturbance to areas where dense populations of C. taxifolia 

exist could assist controlling its expansion in Moreton Bay. This could include the 

installation of boat moorings to prevent fragmentation of the alga by boat anchors, 


Discussion


and restriction of commercial bait gathering activities to areas where 

C. taxifolia is absent. 

Ecological interactions between Moreton Bay seagrasses and C. taxifolia are clearly 

dynamic, complex and subject to considerable temporal and spatial variation. A 

number of processes likely operate synergistically. Monitoring of C. taxifolia and 

seagrass distribution in Moreton Bay is recommended to more clearly define longterm 

patterns in their interactions. This should be combined with monitoring of water 

quality parameters and water temperature to establish any correlation between 

C. taxifolia expansion and water quality decline or temperature increase. Experiments 

exploring the role of C. taxifolia toxins and of sulphide in sediments may help to 

pinpoint a mechanism of interaction with seagrasses. 


Discussion

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7. APPENDIX 


Table 4.1.1. A summary of the dependent samples t-test 

results for the benthic surveys. * represents a significant 

difference (p < 0.05). 

Region df t p 

Western Moreton Bay 101 -2.376 0.019* 

Southern Moreton Bay 

Pumicestone Passage 

63 -3.404 0.001* 

- all sites 21 -0.010 0.991 

- minus one site with reduced cover 20 -2.097 0.049* 

Eastern Moreton Bay 3 1.000 0.391 

All Moreton Bay 191 -3.774 0.000* 

Table 4.3. Summary of results from the planthouse experiments using three seagrass species. Values are mean ± one 

standard error. Values in shaded boxes were significantly affected by the treatment (p < 0.05). 

Seagrass species Treatment PAM fluorometry 

(Fv /Fm ratio) 

Initial Final Initial Final Initial Final Initial Final 

Shoot density 

(% of original) 

Factor SS df MS F p 

Treatment 9398.3 2 4699.2 5.3436 0.011* 

Species 9614.3 2 4807.1 5.4664 0.010* 

Treatment*Species 1166.3 4 291.6 0.3316 0.854 

Error 23743.6 27 879.4 

Time 5330.9 1 5330.9 24.1537 0.000* 

Time*Treatment 697.1 2 348.5 1.5792 0.225 

Time*Species 470.8 2 235.4 1.0667 0.358 

Time*Treatment*Species 441.9 4 110.5 0.5006 0.735 

Error 5959.1 27 220.7 

Leaves per shoot Max. leaf length 

(mm) 

Cymodocea serrulata Control 661±13.4 708±14.5 100±0.0 93.7±3.17 2.5±0.13 2.35±0.10 61.6±2.9 52.3±4.6 

Low C. taxifolia dose 696±21.9 720±17.9 100±0.0 85.2±13.78 2.4±0.17 2.27±0.09 57.4±3.4 49.4±2.3 

High C. taxifolia dose 719±8.5 676±41.7 100±0.0 63.1±21.5 2.2±0.06 2.07±0.36 58.4±4.0 58.6±12.1 

Syringodium isoetifolium Control 763±3.0 730±18.3 100±0.0 84.9±7.8 1.8±0.13 1.6±0.03 71.9±11.3 56.5±8.3 



Zostera capricorni Control 692±15.0 494±191.3 100±0.0 54.1±23.48 2.1±0.21 2.4±0.13 68.3±16.6 81.8±12.5 



Table 4.3.1.1. A summary of the repeated measures ANOVA for 

shoot density response of three seagrass species. * represents a 

significant difference (p < 0.05). 


Appendix


Table 4.3.1.2. A summary of the repeated measures 

ANOVA for shoot density response of Syringodium 

isoetifolium. * represents a significant difference (p < 0.05). 


Treatment 5565.4 2 2782.7 8.8876 0.007* 

Error 2817.9 9 313.1 

Time 968.8 1 968.8 3.2489 0.105 


Error 2683.9 9 298.2 


maximum leaf length response of three seagrass species. * represents a 



Treatment 4750 2 2375 2.842 0.060 

Species 220386 2 110193 131.875 0.000* 

Treatment*Species 21728 4 5432 6.501 0.000* 

Error 254018 304 836 

Time 23987 2 11994 24.940 0.000* 

Time*Treatment 5447 4 1362 2.832 0.024* 

Time*Species 19225 4 4806 9.994 0.000* 

Time*Treatment*Species 9457 8 1182 2.458 0.012* 

Error 292393 608 481 

Table 4.3.2.2. A summary of the repeated measures ANOVA 

for maximum leaf length response of Syringodium isoetifolium. 

* represents a significant difference (p < 0.05). 


Treatment 24908.8 2 12454.4 12.769 0.000* 

Error 114117.8 117 975.4 

Time 40290.2 2 20145.1 34.322 0.000* 


Error 137346.2 234 586.9 


Appendix


Table 4.3.4.1. A summary of the repeated measures 

ANOVA for shoot density response of Zostera capricorni. 

* represents a significant difference (p < 0.05). 


Treatment 3413 2 1706 4.169 0.024* 

Error 13506 33 409 

Time 3901 4 975 16.054 0.000* 

Time*Treatment 1195 8 149 2.459 0.016* 

Error 8018 132 61 

Table 4.3.4.2. Summary of results from the planthouse experiments using Zostera capricorni. Values are mean ± one 

standard error. Values in shaded boxes were significantly affected by the treatment (p < 0.05). 

Treatment PAM fluorometry 

(Fv /Fm ratio) 

Initial Final Initial Final Final Final Final Final Final 

Shoot density 

(% of original) 

Biomass 

(g DW m -2 ) 

Biomass 

(above:below 

ground ratio) 

Chlorophyll 

(mg chl a+b g -1 ) 


photosynthetic response of Zostera capricorni. * represents a 



Block 91798 1 91798 25.8 0.000* 

Treatment 11265 2 5633 1.6 0.210 

Block*Treatment 81730 2 40865 11.5 0.000* 

Error 362472 102 3554 

Time 1873689 8 234211 158.8 0.000* 

Time*Block 102893 8 12862 8.7 0.000* 

Time*Treatment 22323 16 1395 0.9 0.515 

Time*Block*Treatment 76349 16 4772 3.2 0.000* 

Error 1203225 816 1475 

Chlorophyll 

(mg chl a+b dm -2 ) 


Appendix 

Chl a:b ratio 

Control 798±0.81 638±24.96 100±0.0 82.8±7.41 286±35.7 0.16±0.01 1.95±0.24 1.73±0.17 1.90±0.14 

Low C. taxifolia dose 795±4.62 627±45.57 100±0.0 71.0±8.89 312±49.9 0.15±0.04 1.67±0.33 1.78±0.21 2.11±0.03 

High C. taxifolia dose 797±3.55 635±23.47 100±0.0 89.0±2.84 334±11.4 0.16±0.01 1.570±0.06 1.728±0.11 2.043±0.03

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