Caitlin L. Young B

Temporal and spatial variation in the reproduction and growth of greentail prawns (Metapenaeus bennettae) in NSW – implications for improved assessment and management

Caitlin L. Young B. Marine Sc Masters of Science (Research) Thesis

Evolution & Ecology Research Centre School of Biological, Earth & Environmental Sciences The University of New South Wales

November 2016 1

THE UNIVERSITY OF NEW SOUTH WALES

Thesis/Dissertation Sheet

Surname or Family name: YOUNG

First name: CAITLIN Other name/s: LEIGH

Abbreviation for degree as given in the University calendar: MSc

School: Biological, Earth & Environmental Sciences Faculty: Science

Title: Temporal and spatial variation in the reproduction and growth of greentail prawns (Metapenaeus bennettae) in NSW – implications for improved assessment and management

Abstract 350 words maximum: (PLEASE TYPE)

To understand a species’ growth, abundance and reproductive behaviour it is essential that they be examined at relevant spatial and temporal scales to avoid spurious patterns. In light of the transition from single-target species fisheries management to a more holistic ecosystem based approach, these data in relation to dynamic environmental conditions are critical for assessing the impacts of exploitation and for developing appropriate management approaches. The greentail prawn, Metapenaeus bennettae, is an estuarine-dependent prawn and unlike other penaeids, completes its entire lifecycle within the estuarine environment, meaning changes in environmental conditions and other anthropogenic pressures have a much greater consequence on the sustainability of this commercially exploited species. The objectives of this research were to remedy the lack of information on the reproductive biology, abundance and growth of Metapenaeus bennettae and how their reproductive development could be influenced by environmental conditions.

Sampling on a single night or day within a month is common in studies of growth, reproduction and abundance of aquatic invertebrates, but patterns from month-to-month may be confounded by variability at smaller time- scales. Using hierarchical sampling in two estuaries our first experiment revealed that variation in the proportion of mature/ripe female and mean abundance of Metapenaeus bennettae was often largest at the smallest temporal scales of nights and weeks than months or seasons. Variation in the size-frequency distributions was, however, greater at the scale of months and seasons.

Although lunar phase is considered a key driver of reproductive development and spawning activity in prawns, across smaller-temporal scales other processes may have significant influences, especially in estuarine environments, which subjected to irregular and often rapid changes in abiotic variables. Our second experiment examined the effects of lunar phase and other abiotic variables on the reproductive development of this estuarine-dependent prawn. We found that salinity, turbidity, water temperature and lunar phase each had a significant independent influence on the likelihood of a female prawn being ripe throughout the spawning period.

Future studies on species like penaeids with the potential for high variability in reproduction and population structure, should incorporate fine-scale temporal sampling. Fluctuating abiotic variables such as lunar phase, salinity, turbidity and water temperature affect the success of reproductive development and spawning of Metapenaeus bennettae, providing a basis for improving their assessment and management in New South Wales.

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‘I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project's design and conception or in style, presentation and linguistic expression is acknowledged.’

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Date ……………………………………………...... Preface

This thesis is a compilation of my own work, with guidance from supervisors Dr Faith Ochwada-Doyle (NSW DPI), Prof Iain M. Suthers (UNSW), Dr Douglas Rotherham (Text Lab) and Dr. Charles Gray (WildFish Research). The design of the research presented here was personally conceptualized with the assistance of my supervisors. This thesis consists of four chapters prepared as stand-alone manuscripts, one of which (Chapter 2) has already been published in a peer-reviewed symposium proceedings and another (Chapter 3) is currently under review for publication. Each of the chapters is therefore self-contained and some repetition occurs among them. To prevent unnecessary duplication, a single reference list is provided. The contributions of my co-authors to the published chapter are detailed below.

Chapter 2: Young CL, Rotherham D, Johnson DD, Gray CA (2013). Small-scale variation in reproduction and abundance of greentail prawn, Racek and Dall, 1965. Journal of Crustacean Biology 33: 651-659.

Chapter 3: Young CL, Suthers IM, Johnson DD, Gray CA, Ocwada-Doyle FA. Don’t blame it on the moonlight: abiotic drivers of reproductive development in an estuarine dependent prawn. Submitted to Estuaries and Coasts, [submitted].

Dr D. Rotherham, D.D. Johnson, Dr C.A. Gray, Prof I. M. Suthers and Dr F.A. Ochwada-Doyle provided intellectual input and conceptual advice on sampling design, data analysis and interpretation. All co-authors edited and proof-read the final manuscripts.

Cover photo: Trawl net and gantry of research vessel ‘Predator’ on Tuggerah Lakes, New South Wales (Photo: © Caitlin Young). 2

Acknowledgements

Firstly I would like to gratefully acknowledge my supervisors Faith Ochwada-Doyle and Iain Suthers. Faith, I am incredibly thankful you decided to take me on as your student half way through my candidature. It’s not easy trying to make sense of someone’s half-finished research, all the while providing ideas and guidance to ‘bring it home’ and being an ever- encouraging and empowering voice right to the end. Your ability to be a supervisor, colleague and friend simultaneously has been a god-send and I am sincerely grateful. Iain, thank you for standing by me from day one of this slightly drawn-out and bumpy journey; your encouragement and commitment to me as a student and your genuine love for the greentail prawn and all things ‘marine’ is inspiring and I am thankful you took me on and gave me a chance to grow as a scientist. To my supervisors Doug Rotherham and Charles Gray, who started with me but could not finish with me for reasons outside of their control, thank you. You have continually pushed me forward and have always encouraged me to be the best scientist I can be and given me opportunities I will be forever grateful for. This project was generously funded by Fisheries Research and Development Corporation.

A huge thank you to my office mates who assisted with my sampling and have heard me bang on about greentail prawns for way too long. Your support and encouragement has meant more than you know. A massive shout out to DJ (Daniel Johnson) who has pretty much taught me all I know when it comes to fisheries and sampling, and Smokes (Julian Hughes) who has been a well-spring of advice and suffered countless hours of mind-numbing conversations about my research, I honestly don’t think I could have done this without either of you.

To my friends and amazing family (Kesbys, Beddoes and Youngs!), this wouldn’t have been possible without your love, support and encouragement. Thank you for sticking by me and believing in me. Finally, thank you to my husband Ben, you are my biggest cheer squad and I am beyond grateful for the unending emotional support, reassurance and inspiration you have given me.

Thesis Abstract

To understand a species’ growth, abundance and reproductive behaviour in order to appropriately manage their sustainability, it is essential that they be examined at relevant spatial and temporal scales to avoid spurious conclusions about patterns. In light of the transition from single-target species fisheries management to a more holistic ecosystem based approach, data on these parameters in relation to dynamic environmental conditions are critical for assessing the impacts of exploitation and for developing appropriate management approaches. The greentail prawn, Metapenaeus bennettae, is an estuarine-dependent prawn which, unlike other penaeids, completes its entire lifecycle within the estuarine environment meaning changes in environmental conditions and other anthropogenic pressures have a much greater consequence on the sustainability of this commercially exploited species. The objectives of this research were to address the lack of information on the reproductive biology, abundance and patterns of growth of Metapenaeus bennettae in New South Wales, examine how their reproductive development can be influenced by environmental conditions and the potential implications for improving their assessment and management.

Sampling on a single night or day within a month is common in studies on the growth, reproduction and abundance of aquatic invertebrates, but patterns from month-to-month may be confounded by variability at smaller time-scales. Using hierarchical sampling in two estuaries our first experiment revealed that variation in the proportion of mature/ripe female and mean abundance of Metapenaeus bennettae was often largest at the smallest temporal scales of nights and weeks than months or seasons. Variation in the size-frequency distributions was, however, greater at the scale of months and seasons. Understanding the relevant spatial and temporal scales for accurate determination of the life history characteristics of populations is crucial for stock assessments and evaluating appropriate harvest strategies for fisheries.

rapid changes in abiotic variables. Our second experiment examined the effects of lunar phase and other abiotic variables on the reproductive development of this estuarine-dependent prawn and whether these abiotic variables could be influencing its reproductive behaviour at small temporal scales. We found that salinity, turbidity, water temperature and lunar phase each had a significant independent influence on the likelihood of a female prawn being ripe throughout the spawning period. Our findings suggest that because these variables vary from day-to-day, they could be affecting the success of reproductive development and spawning of M. bennettae at small scales. Further research is required to determine if this is also the case with other estuarine crustaceans and whether the patterns uncovered here are consistent among other estuaries.

Table of Contents

Preface...... 2

Acknowledgements ...... 3

Thesis Abstract ...... 4

Table of Contents ...... 6

List of Figures ...... 8

List of Tables ...... 10

Chapter 1: General Introduction ...... 12

1.1 The Challenge of Managing Fisheries Sustainably ...... 12

1.2 The importance of designing appropriate experiments to gather critical life history data. 15

1.3 Reproductive activity and the environment ...... 17

1.4 The Greentail Prawn...... 20

1.5 The need to better understand NSW stocks of M. bennettae ...... 24

1.6 Objectives ...... 26

Chapter 2: Small-scale variation in growth and reproduction of greentail prawn Metapenaeus bennettae (Racek & Dall 1965) ...... 28

Abstract ...... 28

2.1 Introduction ...... 29

2.2 Materials and Methods ...... 31

2.3 Results ...... 36

2.4 Discussion ...... 51

Chapter 3: Don’t blame it on the moonlight: abiotic drivers of reproductive development in an estuarine dependent prawn ...... 55

Abstract ...... 55

3.1 Introduction ...... 56

3.2 Materials and methods ...... 57

3.3 Results ...... 63

3.4 Discussion ...... 74

Chapter 4: General Discussion ...... 82

4.1 Ecosystem based fisheries management ...... 82

4.2 Matching process with the scale of observation ...... 83

4.3 Implications for management of M. bennettae ...... 86

4.4 Future direction and conclusions ...... 88

References Cited ...... 91

List of Figures

Figure 1.1. The recorded distribution of M. bennettae in the coastal waters of eastern Australia (green dotted line)...... 22

Figure 1.2. Commercial prawn trawler (Photo: © Renee du Preez)...... 23

Figure 1.3. Commercial landings reported from New South Wales between 1978/79 and 2014/15 (Stewart et al. 2015). It’s important to note that major reporting changes, indicated by the red lines, are associated with changes in temporal scales of reporting and have no influence over total tonnes caught...... 25

Figure 2. 1. Location of estuaries where M. bennettae were sampled within New South Wales (Tuggerah Lake and Lake Macquarie). Approximate location of sampling sites within each lake indicated by the shaded oval areas and corresponding number...... 33

Figure 2.2. Proportion of total females of M. bennettae in each stage of ovarian development (shading: Stage 1, white; Stage 2, grey; Stage 3, light grey; Stage 4, black; see text for description of each stage) caught in Tuggerah Lake and Lake Macquarie in spring (October and November) 2006, and summer (January and February) 2007. Stage 4 females were caught only in Tuggerah Lake on Day 4 in November. Data are pooled across sites sampled in each night. 39

Figure 2.3. Proportion of total males of M. bennettae in each stage of testis development (shading: Stage 1, white; Stage 2, black; see text for description of each stage) caught in Tuggerah Lake and Lake Macquarie in spring (October and November) 2006, and summer (January and February) 2007. Data are pooled across sites sampled in each night...... 41

Figure 2.4. Mean abundance (± SE) of M. bennettae sampled at different temporal scales at each site in Tuggerah Lake and Lake Macquarie in spring (October and November) 2006, and summer (January and February) 2007...... 46

Figure 2.5. Size-frequency distributions of populations of female M. bennettae sampled from Tuggerah Lake and Lake Macquarie. Data are pooled across nights, weeks and sampling trips in each month...... 48

Figure 2.6. Size-frequency distributions of populations of male M. bennettae sampled from Tuggerah Lake and Lake Macquarie. Data are pooled across nights, weeks and sampling trips in each month...... 49

Figure 3.1. Location of Tuggerah Lake where M. bennettae were sampled within New South Wales. Approximate location of sampling sites within the lake are indicated by the shaded oval areas and corresponding number...... 59

Figure 3.2. Mean: a) turbidity (± SE), b) salinity (± SE) and c) water temperature (± SE) at which ripe and not ripe female M. bennettae were caught. Turbidity estimates are categorised into 3 levels, 1 being low turbidity (~0 mg/L suspended solids), 2 being moderate turbidity (~100mg/L – 300mg/L suspended solids) and 3 being high turbidity (~300mg/L -800mg/L suspended solids)...... 68

Figure 3.3. The proportion of ripe female M. bennettae caught across each of the 4 different lunar phases (1st quarter, full moon, 3rd quarter and new moon). Data are pooled across sampling sites and seasons...... 70

Figure 3.4. Mean turbidity and salinity (± SE) at which ripe and not ripe male M. bennettae were caught during the 4 different lunar phases: 1st quarter, full moon, 3rd quarter and new moon. Turbidity estimates are categorised into 3 levels, 1 being low turbidity (~0 mg/L suspended solids), 2 being moderate turbidity (~100mg/L – 300mg/L suspended solids) and 3 being high turbidity (~300mg/L -800mg/L suspended solids). Data are pooled across sampling sites and seasons...... 73

List of Tables

Table 1.1. Table showing a range of examples of how lunar phase affects reproductive timing of many animals from various habitats...... 18

Table 2.1. Numbers of females and males of M. bennettae caught in each estuary at each site, night, week, month and season...... 37

Table 2.2. Results of ANOVA (df = degrees of freedom; MS = Mean sum of squares; F = the F- statistic) and components of temporal variance (CV) calculated separately for mature female and male M. bennettae sampled from Tuggerah Lake and Lake Macquarie. Statistically significant differences, *p<0.05; **p<0.01; ***p<0.001, † = variances were heterogeneous, so p was set at 0.01 to reduce the probability of Type I error (Underwood 1997)...... 42

Table 2.3. Results of ANOVA (df = degrees of freedom; MS = Mean sum of squares; F = the F- statistic) and components of temporal variance (CV) for the mean numbers of M. bennettae caught at each site in Tuggerah Lake and Lake Macquarie. Statistically significant differences, *p<0.05; **p<0.01; ***p<0.001, † = variances were heterogeneous, so p was set at 0.01 to reduce the probability of Type I error (Underwood 1997)...... 45

Table 2.4. Results of Kolomogorov-Smirnov (K-S) tests examining differences in size-frequency distributions of male and female M. bennettae between the temporal scales of nights, weeks, months and seasons in Tuggerah Lake and Lake Macquarie. Statistically significant differences, *p<0.05; **p<0.01; ***p<0.001, na = not analysed owing to insufficient data...... 50

Table 3.1. Numbers of females and males of M. bennettae caught in each of the four lunar phases at each site, month and season. Data are pooled across replicate sampling nights within each lunar phase...... 65

Table 3.2. The results of the generalised linear model (GLM) used to examine the influence of the categorical variable lunar phase (4 levels: 1st quarter (reference level for this factor in the GLM), full moon, 3rd quarter and new moon) as well as that of the continuous variables turbidity, salinity and water temperature on the reproductive development of female M. bennettae. The model assumed a binomial distribution and tested the null hypothesis that βi = 0 for each retained parameter or interaction term, where βis were the partial regression coefficients, using partial z-tests (α = 0.05)...... 67

Table 3.3. The results of Tukey’s post-Hoc test (α = 0.05) comparing different levels of each lunar phase (4 levels: 1st quarter, full moon, 3rd quarter and new moon) in a pair-wise manner...... 69

Table 3.4. The results of the generalised linear model (GLM) used to examine the influence of the categorical variable lunar phase (4 levels: 1st quarter (reference level for this factor in the GLM), full moon, 3rd quarter and new moon) as well as that of the continuous variables turbidity, salinity and water temperature on the reproductive development of male M. bennettae. The model assumed a binomial distribution and tested the null hypothesis that βi = 0 for each retained parameter or interaction term, where βis were the partial regression coefficients, using partial z-tests (α = 0.05)...... 72

Chapter 1: General Introduction

1.1 The Challenge of Managing Fisheries Sustainably

Global human consumption of living aquatic resources has been increasing steadily for the past several decades, reaching a peak in 2012 of 136 thousand tonnes (FAO Fisheries and

Aquaculture Department 2014). In response to the rising demand, global production of aquatic resources is also on the increase (Watson et al. 2014). Excluding aquaculture and inland capture, wild capture of marine species alone has risen substantially from approximately 16 million tonnes in the 1950s to almost 80 million tonnes in 2012 (FAO Fisheries and Aquaculture

Department 2014). Not only is the human population dependent on aquatic resources as a food source, but the most recent estimate states that the livelihood and income of 58.3 million people are also dependent on the sustainability of fisheries (Eggert and Greaker 2009; FAO

Fisheries and Aquaculture Department 2014).

The increasing economic value of the fisheries sector has also resulted in rapid advances in fishing technology including more efficient and stronger gears and larger, faster, safer vessels with premium navigation equipment, on-board freezers and most importantly sounders to locate fish (Ghee-Thean et al. 2012). These technologies provide almost unlimited access to this wild resource and have contributed to their depletion (Swartz et al. 2010). Approximately

90% of the world’s fish stocks are considered to be fully exploited, over exploited or recovering from depletion making effective management more important than ever (FAO Fisheries and

Aquaculture Department 2014).

Although fishing poses one of the greatest threats to future sustainability of our aquatic resources, changes in environmental conditions can also have a substantial effect on the growth, reproductive capacity, mortality and distribution of many exploited species (Botsford et al. 1997). Rising ocean temperatures and ocean acidification associated with climate change are already affecting many marine fish species around the world (Engelhard et al. 2014;

Kortsch et al. 2015; Sydeman et al. 2015; Nagelkerken et al. 2016). Other processes such as El

Niño-Southern Oscillation (ENSO) alter oceanic and coastal conditions and can affect fish production on a global scale. For the largest single-species fishery in the world, for example, annual catches of the Peruvian anchovita (Engraulis ringens) have ranged from 94,000 tonnes to 13 million tonnes since the 1970’s and this fluctuation has mainly been attributed to ENSO

(Jacobson et al. 2001). Not only does a change in environmental conditions affect fish production directly, but it can also affect fish production indirectly by negatively impacting ecosystems and key habitats, such as coral reefs (Spalding and Brown 2015), estuarine seagrass beds, mangrove ecosystems and wetlands (Lotze et al. 2006; Beaumont et al. 2011) which are crucial to the life cycles of many aquatic species. Considering all these pressures, future sustainability of fisheries depends on effective management of fishing activity, which in turn requires an understanding of environmental changes and their effect on the productivity of exploited stocks.

A prime example of how effective management of fishing activity should work synergistically with an understanding of the environment and its effect on the productivity of exploited stocks is that of the Barents Sea cod (Gadus morhua) stock; currently the world’s largest cod stock and one of the most commercially important (Vasilakopoulos and Marshall 2015). Although many of the world fish stocks are currently at historical lows, the Barents Sea cod stock has

recently increased significantly with spawning stock biomass now at a record high. Kjesbu et al.

(2014) demonstrates that successful management decisions alone were not responsible for the increase but an understanding of shifting climatic conditions (ocean temperature) along with management actions (reduction in fishing mortality) caused this much needed stock biomass growth. Anthropogenic pressures and changes in environmental conditions will only escalate in the future so it is more imperative than ever to ensure that fisheries managers, globally, employ a holistic approach and manage for change (Rice and Garcia 2011).

This holistic approach to management, where multi species interactions and the influences of the physical environment are considered, is referred to as Ecosystem-based fishery management (EBFM). This approach has not always been adopted and it has been proposed that out-dated methods such as single target species management may have actually contributed to global overfishing and stock depletion (May 1984). EBFM is a new direction for managing fisheries, making the ecosystem the priority rather than the target species, with the overall objective to sustain healthy ecosystems and, thus, the fisheries they support (Pikitch et al. 2004).

To further define the overall objective of managing fisheries sustainably, sustainable fisheries are those in which fish populations do not decline over time due to fishing practices and their potential interaction with other species and changes in environmental conditions. To establish such fisheries, key biological information such as abundance, growth, reproduction, movements and stock structure of harvested species needs to be gathered. These data and information on how they may be affected by changing environmental conditions are critical for

assessing the impacts of exploitation and for developing appropriate management approaches. Data gaps continue to be obstacles to establishing sustainable fisheries. In

Australia alone, out of the 238 stock status assessments that were undertaken nationally in

2014 by Fisheries Research and Development Corporation (FRDC) and the Australian Bureau of Agricultural and Resource Economics and Sciences (ABARES), 29% were classified as undefined stocks, meaning that there is limited information available to undertake the assessment (Flood et al. 2014).

1.2 The importance of designing appropriate experiments to gather critical life history data

Information on key biological parameters such as abundance, growth and reproduction, which are some of the most influential on the productivity of marine populations, is crucial for the effective management of global fisheries including stock assessments and evaluating appropriate harvest strategies (Trippel 1999; Campana and Thorrold 2001). Information, however, needs to be collected across a range of spatial and temporal scales to truly understand life-history strategies (Stearns 1976) and what processes may be affecting them

(Underwood et al. 2000). Understanding how these biological parameters vary across different spatial and temporal scales is a logical first step in establishing hypotheses about the biotic

(species interactions) or abiotic (environmental) processes that could be affecting aquatic organisms (Benedetti-Cecchi 2003). Indeed, pilot experiments are an important (but often overlooked) first step in designing studies of any organism. Identifying appropriate spatial and temporal scales of sampling is necessary for rigorous design and analysis of biological and ecological experiments. Variability at small spatial or temporal scales can confound comparisons over larger areas or longer periods of time. Although many studies have

recognised the problems of confounding in space (Hurlbert, 1984), much less attention has been paid to avoiding equivalent temporally confounding effects (Stewart-Oaten et al. 1986).

Further, problems of confounding in space or time have rarely been examined in studies of the reproductive biology of marine organisms (Rotherham and West 2009), especially exploited ones.

For marine invertebrates, in particular, there is limited research on temporal and spatial variability in reproduction and also abundance. Despite this limited knowledge, sampling on a single day (or night) within a calendar or lunar month, for several months or seasons is found extensively throughout the literature (e.g. Kramarsky-Winter and Loya 1998; McQuaid and

Phillips 2006; Berger 2009; Brogger et al. 2010). This experimental design, however, doesn’t take into account that patterns of reproduction and abundance across these larger temporal scales of months and seasons could be confounded by variation at smaller time-scales (e.g. day-to-day or night-to-night). Indeed, results from Morrisey et al. (1992b) revealed significant variation in abundance of cumaceans was found at smaller scales of days and weeks but not at the larger scales of seasons. If seasons were then to be compared based on one day or one week of sampling it would lead to confounding conclusions and potentially compromised management recommendations. Although this is an example of small-scale variation in the abundance of organisms, these findings highlight the importance of designing experiments that have the ability to detect such small-scale variation. They also highlight how understanding variation at different spatial and temporal scales is crucial in describing not only the abundance of organisms but suggest that such an understanding could also be crucial for other key biological parameters such as the reproductive condition of exploited populations.

1.3 Reproductive activity and the environment

Information on the reproductive biology of aquatic organisms, in particular, and knowledge of the environmental cues that drive reproductive development forms a necessary foundation of stock assessments and enables the development and evaluation of harvest strategies to aid the management goals of sustainable fisheries (Ricker 1954; Beverton and Holt 1957). This is not only true for economically important species, but also for species that coexist in similar environments and are harvested secondarily or contribute to the trophic food webs and the ecosystems of primary fishery targets (Pikitch et al. 2004).

Since most wild populations experience variable environmental conditions that fluctuate spatially and temporally, timing and synchrony of reproductive activity is generally an important component for the fitness, survival and longevity of a species (Brommer et al. 2002).

Lunar phase, for example, is one of the environmental variables that is commonly thought to play a significant role in reproductive timing and this has been illustrated for many terrestrial, marine, estuarine, air-borne and amphibious animals (Table 1.1).

Table 1.1. Table showing a range of examples of how lunar phase affects reproductive timing of many animals from various habitats.

Habitat/Class Lunar influence Reference Badger (Meles meles) shows Terrestrial increased reproductive activity (Dixon et al. 2006) around the new moon Oocytes of rabbitfish (Siganidae) are Marine under final maturation stage around (Takemura et al. 2004) the 3rd quarter moon Cichlid (Neolamprologus pulcher) Estuarine ovarian investment and spawning (Desjardins et al. 2011) peaked in the 1st quarter moon Moluccan megapode (Megapodius (Baker and Dekker Aves wallacei) show peak egg-laying in the 2000) week following the full moon Large spawning events are more frequent around the full moon in Amphibia anurans and there are peak arrivals of (Grant et al. 2009) urodeles to breeding sites during new and full moons

However, lunar periodicity is not the only environmental variable known to affect the reproduction of aquatic organisms over small temporal scales. Organisms in estuarine environments, in particular, can be exposed to swift changes in environmental conditions.

Estuaries are the transition zones between terrestrial, freshwater and marine habitats and this characteristic makes them dynamic ecosystems that are subject to a host of abiotic variables

(Mann 1982). Variables such as temperature, salinity and turbidity vary considerably in estuarine environments and can fluctuate on shorter time scales than lunar periodicity (e.g. from day-to-day) because they are driven by wind speed and direction (Lawson et al. 2007), rainfall (Racek 1959; Ives et al. 2009), tidal exchange and currents (Roy et al. 2001). While it is well known that these variables can affect the behaviour and catch rates of marine invertebrates in particular (Dall et al. 1990; Stoner 1991; Ligas et al. 2011; Munga et al. 2013), the degree to which these environmental variables affect reproductive activity in these animals is relatively unknown. One of the few examples showing this interaction between the reproduction of marine invertebrates and the environment found that recruitment of crab species (primarily Cancer spp.) in northern California was positively correlated with temperature, and negatively correlated with salinity on a weekly time scale. On a daily time scale, crab recruitment was associated with sharp increases in temperature (Wing et al. 1995).

The majority of studies concerning the reproduction of marine invertebrates and their interactions with the environment, however, focus on the larval and juvenile stages rather than the reproductive development of adults (Aziz and Greenwood 1981; Preston 1985;

Kuklinski et al. 2013) even though the level of spawning success of adults in exploited populations continues to be a common biological reference point for fisheries management

(Hilborn and Stokes 2010).

The red king crab (Paralithodes camtschaticus) fishery in Bristol Bay, formerly one of the most profitable fisheries in the world, provides a great example of how knowledge of environmental changes and their effect on reproduction, and ultimately productivity of exploited populations, can aid in fisheries management and the establishment of sustainability of stocks. After its collapse in the mid-1980s, management enforced strict harvest guidelines in an effort to rebuild the stock; however, these efforts have had little effect. The relatively recent research of Loher and Armstrong (2005) on the abundance and distribution of ovigerous female red king crabs indicated that there might be more going on than just over exploitation of these animals.

Extremely low water temperatures seem to inhibit egg incubation and are therefore avoided by reproductive females, thus influencing the abundance and distribution of stocks as pools of cold water move around and ocean temperatures change. These findings explain some of the population dynamics and recruitment patterns of the red king crab and Loher and Armstrong

(2005) suggest that management would benefit if interactions between this species and changing environmental conditions could be identified and predicted.

1.4 The Greentail Prawn

The greentail prawn, Metapenaeus bennettae (Racek and Dall, 1965) (previously known as the greasyback prawn), is a prime example of a commercially exploited species that requires sustainable management practices that are guided by information from sampling designs carried out at appropriate temporal and spatial scales as well as information on how the environment could be affecting its reproductive success. This species is a shallow-water, estuarine dependent prawn endemic to the central and southern coastal waters of eastern

Australia (Grey 1983); its distribution extends from Rockhampton in Queensland down to

Gippsland Lakes in eastern Victoria (Figure 1.1). Both juvenile and adult M. bennettae are efficient osmoregulators which allows them to complete their entire lifecycle within closed waters, unlike other penaeids (Morris and Bennett 1952). Replenishment of stocks by larvae from the ocean is virtually non-existent (Racek 1959) and estuarine processes such as predation from other fish species (Salini et al. 1990), changes in environmental conditions and anthropogenic pressures have a much greater effect on the survival of this species.

Earlier research in the state of New South Wales, eastern Australia (NSW) (Figure 1.1) suggests that the general period of reproduction and greatest abundance of M. bennettae extends from spring to early autumn, with some suggesting that spawning may occur around the full moon

(Morris and Bennett 1952; Racek 1959). In the last 30 years, the little research that has been conducted on the reproductive biology of M. bennettae has only focused on populations from southern Queensland (Courtney et al. 1995; Courtney and Masel 1997) which have been proven to be a genetically different population to those found in central NSW (Salini 1987).

The general reproductive period of Queensland stocks seems to extend a little longer than those in NSW, ranging from early spring to late autumn with bi-annual recruitment (Courtney et al. 1995). Egg production of the Queensland stock was also found to vary inexplicably among the months and years sampled (Courtney and Masel 1997). Consequently, there is a need to explore the reproductive activity of M. bennettae in NSW and identify any temporal and spatial variability in reproduction as well as any drivers of this potential variability, to ensure that the sustainability of NSW stocks is maintained.

NSW

Figure 1.1. The recorded distribution of M. bennettae in the coastal waters of eastern Australia (green dotted line).

In NSW, M. bennettae are targeted primarily by commercial fishers during early summer. One category of existing NSW commercial fisheries is classified as “Estuary General”. This is a diverse multi-species, multi-method fishery that operates out of many NSW estuaries. The majority of the catch of M. bennettae is taken using prawn seine nets by Estuary General fishers in the Wallis Lake and the Central Coast region of NSW, with a small proportion taken by the Estuary Prawn Trawl Fishery (Figure 1.2.) (Stewart et al. 2015).

Figure 1.2. Commercial prawn trawler (Photo: © Renee du Preez).

1.5 The need to better understand NSW stocks of M. bennettae

In NSW, M. bennettae, are harvested mainly as a ‘key secondary’ species in the Estuary

General Fishery and as by-product in Estuary Prawn Trawl Fishery (Fisheries 2003a; Fisheries

2003b). ‘Primary’ and ‘key secondary’ species are both targeted species according to the

Fisheries Management Strategy Reports and therefore CPUE is a good indicator of abundance.

These fisheries also target other commercially important species such as eastern king prawns

(Penaeus plebejus), school prawns (Metapenaeus macleayi) and yellowfin bream

(Acanthopagrus australis) (Rowling et al. 2010). Metapenaeus bennettae is an important component of the diet of commercially important species such as yellowfin bream, dusky flathead (Platycephalus fuscus), common estuary stingray (Dasyatis fluviorum) and porcupine fish (Dicotylichthys punctulatus) (Dall et al. 1990). In the last decade, average annual commercial landings have decreased by more than 50% (Figure 1.3.), with little proportional changes in effort (Stewart et al. 2015). Despite these declines and the uncertain exploitation status of M. bennettae (Rowling et al. 2010; Stewart et al. 2015), knowledge of this species’ biology remains inadequate to maintain the future sustainability of stocks in NSW. A lack of contemporary data on the reproductive behaviour, size structure and abundance of M. bennettae continues to hinder improved assessment of the status of this resource. Further, behavioural and physiological rhythms are poorly understood not only for M. bennettae, but also adult penaeids in general (Courtney et al. 1996).

Figure 1.3. Commercial landings reported from New South Wales between 1978/79 and 2014/15 (Stewart et al. 2015). It’s important to note that major reporting changes, indicated by the red lines, are associated with changes in the commercial catch record form or changes in temporal scales of reporting (change from monthly to daily reporting) and have no influence over total tonnes caught.

1.6 Objectives

This research project aims to redress the lack of information on the reproductive biology of M. bennettae in general as well as the paucity of specific information on the environmental conditions that influence their reproductive development. The project represents a first step towards improving the assessment and management of this species in NSW and forms the foundations for future experiments investigating the reproductive biology of any species with the potential for high temporal variability in reproductive patterns. In this thesis I will address two objectives; (1) to examine temporal and spatial variability in reproductive condition, relative abundance and size structure at different scales; and, (2) to examine what environmental variables could be driving the variation.

The first objective was to examine short-term temporal and spatial variation in the reproductive condition, relative abundance and size-structure of populations of M. bennettae in order to design appropriate sampling strategies. This chapter is now published as: Young CL,

Rotherham D, Johnson DD, Gray CA (2013) “Small-scale variation in reproduction and abundance of greentail prawn, Racek and Dall, 1965” in the Journal of Crustacean Biology 33:

651-659, and will improve our understanding of the magnitude of confounding effects caused by small-scale temporal variability in patterns of reproduction and abundance. It will also identify appropriate sampling intervals for longer-term studies of M. bennettae.

The second objective was to examine variation in the reproductive condition of M. bennettae across four replicate lunar cycles and across natural gradients of turbidity, salinity and water temperature. This chapter will identify some of the environmental variables affecting the 26

success of reproductive development and spawning of M. bennettae in NSW and illustrate how an understanding of these interactions can aid in the management of this exploited species.

This chapter is currently under review for publication in Estuaries and Coasts.

Both chapters are prepared for publication as independent studies, and therefore some repetition of background and methods is evident in each.

This study was conducted in two large coastal lagoons on the central coast of NSW, Lake

Macquarie and Tuggerah Lakes. These two lagoons are large, barrier estuaries and are typical of many such estuaries on the east coast of Australia. Lake Macquarie covers over 100 km2and is the largest such lagoon in Australia; and Tuggerah Lakes covers in excess of 70 km2, putting it amongst the six largest estuaries in NSW (Roy et al. 2001). These estuaries are popular for residential development and tourism (Dredge 2001). They also sustain high recreational fishing pressure, with recreational catches of penaeid prawns representing approximately 36% of the commercial catch in Tuggerah Lakes (Reid and Montgomery 2005) and Lake Macquarie being marked as a recreational fishing haven since 2002 (Ochwada-Doyle et al. 2014).

Chapter 2: Small-scale variation in growth and reproduction of greentail prawn Metapenaeus bennettae (Racek & Dall 1965)

Abstract

Sampling on a single night or day within a month is common in studies of reproduction and abundance of aquatic invertebrates, but patterns from month-to-month may be confounded by variability at smaller time-scales. We used hierarchical sampling in two estuaries to test the hypothesis that temporal variability in reproductive condition, relative abundance and size- structures of populations of Metapenaeus bennettae would be greater at the larger scales of months and seasons than at smaller scales of weeks and nights. In both estuaries, variation in the proportion of mature/ripe females and mean abundance of M. bennettae was often largest at the temporal scales of nights and weeks, but variation in the size-frequency distributions was generally greater at the scale of months and seasons. Our results demonstrate that future studies on any species with the potential for high temporal variability in reproduction and population structure, like penaeids, should incorporate or examine the need for small-scale temporal sampling.

Keywords: Penaeid; Hierarchical experimental design; Temporal variability; Spatial variability;

Variance

2.1 Introduction

Observations on the reproduction and abundance of organisms over different temporal and spatial scales are necessary in understanding life-history strategies (Stearns 1976) and in developing models to explain the processes creating such patterns (Underwood et al. 2000).

Such observations also provide an important basis for the sustainable management of harvested populations and conservation of biodiversity (Holloway 1993; Manriquez and

Castilla 2001; Schofield et al. 2010).

Although many studies have examined patterns of reproduction of aquatic invertebrates at time-scales of weeks (i.e. among lunar phases e.g. Young 1978; Skov et al. 2005), months

(Aragon-Noriega 2005; Grange et al. 2011), seasons (Macpherson and Raventos 2004; Simoes et al. 2010) and years (Crocos et al. 2001; Velazquez 2003), few have focussed on smaller temporal scales (e.g. daily or semi-lunar, Courtney et al. 1996; Coma and Lasker 1997). Indeed, a common approach has been to sample on a single day (or night) within a calendar or lunar month, for several months or seasons (Courtney and Masel 1997; Kramarsky-Winter and Loya

1998; Calvo and Templado 2004; McQuaid and Phillips 2006; Berger 2009; Rotherham and

West 2009; Brogger et al. 2010). This approach, however, ignores the potential for patterns of reproduction and abundance from month-to-month (and season-to-season) to be confounded by variation at smaller time-scales (e.g. day-to-day or night-to-night). A well-known example of short-term temporal variation in abundance of marine benthos and its implication for the design of sampling programs was provided by Morrisey et al. (1992b) where significant variation in abundance of cumaceans was found at smaller scales of days and weeks but not at the larger scales of seasons.

Information concerning patterns of reproductive biology and abundance of aquatic organisms is used in stock assessments as well as in developing and evaluating harvest strategies for fisheries. Although it is well documented that abundances of aquatic invertebrates can vary over small spatial and temporal scales (Morrisey et al. 1992a; b; Desmond et al. 2002; Guijarro et al. 2012), it has been less recognised that this may also be true for reproductive condition.

For example, Kumar et al. (2003) found that fecundity of female Portunus armatus (previously

Portunus pelagicus; Lai et al. 2010) increased gradually over the first 2 months of summer, before declining rapidly by the last month of the season. This implies that designing experiments that have the ability to detect such small-scale variation is crucial in describing key biological parameters such as fecundity (Kumar et al. 2003), recruitment (Hamer and

Jenkins 2004), size at maturity (Aragón-Noriega and Alcántara-Razo 2005), growth

(Montgomery et al. 2010) and mortality (Nevarez-Martinez et al. 2006) of exploited populations.

The greentail prawn, Metapenaeus bennettae (Racek and Dall 1965), is endemic to waters of eastern Australia (from 23°S to 37°S) and the target of commercial and recreational fisheries.

Unlike most other penaeids, M. bennettae is capable of completing its entire lifecycle within estuaries (Morris and Bennett 1952). Nevertheless, knowledge of the biology of M. bennettae is largely limited (e.g. Morris and Bennett 1952; Dall 1957; Courtney and Masel 1997) and a lack of data on its reproduction and growth in New South (NSW) has contributed to uncertainty about the exploitation status of the species (Rowling et al. 2010).

Here, we examine variation in reproductive condition, relative abundance and size-structures of populations of M. bennettae at different temporal scales using a hierarchical sampling design in two estuaries in NSW. The general hypothesis tested was that temporal variation associated with these parameters would be larger at the scales of months and seasons than at the smaller scales of weeks and nights. Our aims were to: (i) redress the lack of research examining the potential for short-term temporal variability to confound patterns of reproduction and abundance of invertebrates; and (ii) identify appropriate sampling intervals for longer-term studies of M. bennettae.

2.2 Materials and Methods

2.2.1 Study locations and experimental design

This mensurative experiment was done in two adjacent (separated by ~10 km), large, permanently open barrier estuaries on the central coast of NSW, Tuggerah Lakes (33°21′S,

151°30′E; surface area ~80 km²) and Lake Macquarie (33°06′S, 151°36′E; surface area ~109 km²). Both are relatively shallow (mean depth ~7 and 2 m, respectively), microtidal, estuaries connected to the ocean via relatively narrow entrances (Roy et al. 2001) (Figure 2.1.).

In each estuary, three randomly selected sites separated by two to eight kilometres were selected over predominately flat, unvegetated sediment in depths ranging from 1 to 5 m.

Substrates within both estuaries are sand with fringing beds of seagrass, typical of barrier estuaries (Roy et al. 2001). Each site was sampled on two randomly selected nights, in each of two randomly selected weeks, in each of two consecutive months, in each of two consecutive 31

seasons (i.e. spring: October and November 2006, summer: January and February 2007; with a total of eight nights of sampling at each site per season). These seasons fall within the general period of reproduction and greatest abundance of M. bennettae in Tuggerah Lake (Racek

1959). Nights of sampling within a week were separated by a minimum of one day (i.e. 24 hours) or maximum of three days (i.e. 72 hours); and weeks within a month could have been separated by as many as three weeks. Sampling was done at night between 2000 h and 0200 h because M. bennettae remain buried in sediment during the day (Dall 1957), and so very few individuals can be caught (Morris and Bennett 1952; Rotherham et al. 2008).

On each night of sampling, six non-overlapping, replicate tows (each lasting exactly 5 min at a speed of 1.2 m.s-1) were done at each site with a beam trawl that had a beam length of 3 m and a vertical opening of 0.8 m (~ 900 m2 of swept area per tow). The trawl was configured with 41-mm diamond-shaped mesh in the body and 20-mm square-shaped mesh in the codend (Rotherham et al. 2008). After each replicate tow, M. bennettae were identified (Jones and Morgan 2002) and sorted from the catch, placed in labelled plastic bags, and frozen.

Where catches were large, a subsample containing a maximum of 100 randomly-selected prawns per site was retained; however, all M. bennettae caught in each replicate tow were counted.

2.2.2 Examination of prawns

In the laboratory, prawns were defrosted and measured for carapace length (CL - the straight line distance between the base of the eye orbit and the posterior edge of the carapace) using electronic callipers. Sex was determined by examining the thoracic sternite and/or the first abdominal somite and identifying the presence of either the thelycum (female genitalia) or petasma (male genitalia), respectively. Prawns were examined macroscopically to determine their stage of gonad development. Female prawns were assigned to one of four stages of ovarian development based on the criteria of Tuma (1967): Stage 1 (undeveloped), ovary thin and translucent; Stage 2 (developing), ovary ivory-yellow and slightly enlarged; Stage 3

(mature), ovary yellow-orange and occupying a large proportion of the abdomen; and Stage 4

(ripe), ovary olive-green and extending throughout the abdomen into the carapace. The histological characteristics of recently-spawned female penaeids have been shown to be difficult to distinguish from those of females that have not spawned (Courtney et al. 1996). No

female prawns were subsequently classified as Stage 5 (spent) and, instead, all females with these macroscopic ovarian characteristics were grouped with Stage 1 (undeveloped) and analysed accordingly. Two stages were used to classify male testis development: Stage 1

(undeveloped), sperm sack translucent; and Stage 2 (mature/ripe), white gelatinous mass present in the sperm sack.

2.2.3 Data Analyses

A nested analysis of variance (ANOVA) was performed separately for each sex in each estuary to estimate variation in the mean proportion of prawns classified as mature or ripe (i.e. females, Stage 3 and 4; males, Stage 2). Prior to performing the ANOVA, Cochran’s C test was carried out to check for homogeneity of variances. The ANOVA included the four nested temporal scales (nights, weeks, months and seasons), which were all considered as random factors. However, for these analyses, it was necessary to pool data across replicate tows (n = 6) at each site each night because there were many replicates in which mature or ripe prawns were not caught. Thus, ‘sites’ became the replicate samples for each night, resulting in n = 3 and the residual statistic gave a measure of spatial variation. To estimate temporal variation in mean abundance independently from its interactions with spatial variation, mean abundance was also analysed separately for each site in each estuary using the same four-factor ANOVA model.

Analysis of significance values alone can sometimes generate misleading patterns of the relative importance of individual factors (Graham and Edwards 2001), therefore components of variation for each temporal scale were extracted from ANOVAs (Underwood 1997) to show 35

how much variation could be ascribed to each different factor and where necessary, were corrected for negative values (Fletcher and Underwood 2002).

All analyses were done on untransformed data because components of variation needed to be extracted from the true variances. Although ANOVA tests are fairly robust to heterogeneous variances in large, balanced designs like this one (Underwood 1997), alpha (α) was set to p =

0.01 to reduce the risk of Type I errors (Underwood 1997).

Differences in size-frequency distributions between nights in each week, weeks in each month, months in each season, and seasons, were examined separately for each sex and estuary using

Kolmogorov-Smirnov (K-S) tests (Sokal and Rohlf 1995). To perform these tests, it was necessary to pool data across replicate tows and sites, although pooled samples with less than

25 individuals were not analysed. Data were also pooled across each estuary and K-S tests carried out to examine differences in the size frequency distributions for each sex between estuaries.

2.3 Results

Totals of 5,292 and 5,319 individuals of M. bennettae were caught in Tuggerah Lakes and Lake

Macquarie, respectively. Of these, 1,968 individuals (1,010 males and 958 females) from

Tuggerah Lakes and 1,907 individuals (941 males and 966 females) from Lake Macquarie were kept for examination (Table 2.1.).

Table 2.1. Numbers of females and males of M. bennettae caught in each estuary at each site, night, week, month and season.

Estuary Season Month Week Night Female Male Site 1 Site 2 Site 3 Site 1 Site 2 Site 3 1 10 12 3 16 18 13 Week 1 2 13 33 32 24 37 35 October 1 21 41 32 38 Week 2 2 12 37 8 14 22 8

Spring

1 54 27 48 38 Week 1 2 32 27 27 32 24 31 November 1 48 46 54 32 30 48 Week 2 2 43 46 46 58 46 46 Tuggerah

Lakes 1 11 13 4 10 30 27 Week 1 2 27 10 10 15 9 15 January 1 7 8 3 12 12 11 Week 2 2 7 23 6 5 38 12

Summer

1 33 16 26 12 24 18 Week 1 2 13 12 3 6 9 3 February 1 5 17 2 11 13 3 Week 2 2 9 8 13 4 8 13

Total sex 958 1010

1 88 80 19 83 73 12 Week 1 2 31 22 2 29 17 8 October 1 14 37 1 45 36 3 Week 2 2 9 19 11 16 27 8

Spring

1 30 45 15 33 47 14 Week 1 2 26 35 15 21 19 9 November 1 24 40 16 25 9 6 Week 2 2 43 35 11 45 26 4 Lake

Macquarie 1 30 4 20 11 Week 1 2 27 11 3 23 19 5 January 1 17 9 4 17 15 3 Week 2 2 22 24 2 19 30 6

Summer

1 14 14 23 14 Week 1 2 24 13 23 23 11 18 February 1 13 14 11 19 11 13 Week 2 2 14 4 1 17 7 2

Total sex 966 941

2.3.1 Patterns of gonadal development

In both estuaries, the largest proportions of mature or ripe females (Stage 3 and 4) in samples were found on most nights (and weeks) sampled during November (Figure 2.2.). Nevertheless, there was no clear pattern in the gonadal development of female prawns from month to month in either estuary. Indeed, the proportion of female prawns in each stage of development varied considerably from night to night and week to week within an estuary. For example, while the proportion of mature or ripe females appeared to peak in November, the first night sampled in Tuggerah Lakes during this month actually contained the second lowest proportion of mature females of all the nights sampled. By comparison, large proportions

(>~0.6) of mature male prawns were sampled across most nights, weeks and months in both estuaries during the study (Figure 2.3.).

2.3.2 Scales of variation in mean proportion of mature or ripe females

In Tuggerah Lakes, ANOVA detected significant differences (p<0.01) in the mean proportion of mature or ripe females of M. bennettae at the scale of nights, with differences between nights also accounting for most of the temporal variation (Table 2.2.). In contrast, no significant differences in the mean proportion of mature/ripe females at any temporal scale in Lake

Macquarie were detected; however, the temporal components of variation in the mean proportion of mature/ripe females was also greatest at the smallest temporal scale of nights; i.e., nights were more variable than weeks or seasons (Table 2.2.).

There were no significant differences in the mean proportions of mature males at any of the temporal scales in either estuary (Table 2.2.). Nevertheless, patterns in the variation of reproductive condition of males differed between estuaries. In Tuggerah Lake, variation was greatest at the scale of nights (Table 2.2.). In Lake Macquarie, however, variation in the reproductive condition of males varied more from season-to-season than night-to-night (Table

2.2.). Interestingly, the residual variance (which is a spatial component measuring variation in the proportion of mature prawns among replicate sites) was greater than the variance at any of the temporal scales examined for both female and male M. bennettae.

Table 2.2. Results of ANOVA (df = degrees of freedom; MS = Mean sum of squares; F = the F-statistic) and components of temporal variance (CV) calculated separately for mature female and male M. bennettae sampled from Tuggerah Lake and Lake Macquarie. Statistically significant differences, *p<0.05; **p<0.01; ***p<0.001, † = variances were heterogeneous, so p was set at 0.01 to reduce the probability of Type I error (Underwood 1997).

Source Mature or ripe females Mature males df MS F CV MS F CV

Tuggerah Lake

Season 1 0.004 0.050 0.000 0.195 2.030 0.004 Month(S) 2 0.082 2.180 0.002 0.096 11.550 0.007 Week(M(S)) 4 0.038 0.250 0.000 0.008 0.070 0.000 Night(W(M(S))) 8 0.153 3.68 ** 0.024 0.117 2.800 0.013 Residual 32 0.042 0.042 0.042 0.042 Total 47

Cochran's C-test 0.255 0.434 †

Lake Macquarie

Season 1 0.254 3.940 0.008 0.654 30.280 0.026 Month(S) 2 0.065 0.690 0.000 0.022 1.970 0.001 Week(M(S)) 4 0.094 0.920 0.000 0.011 0.310 0.000 Night(W(M(S))) 8 0.103 2.010 0.015 0.036 0.930 0.000 Residual 32 0.051 0.051 0.039 0.038 Total 47

Cochran's C-test 0.293 0.493 †

2.3.3 Scales of variation in mean abundance

Temporal patterns in mean numbers of M. bennettae were inconsistent between estuaries and among sites within each estuary (Table 2.3., Figure 2.4.). In Lake Macquarie, there were significant differences (p<0.01) at the scale of seasons and weeks at Site 1, with differences between seasons also accounting for most of the temporal variation. At Site 2, however, significant differences (p<0.001) were detected at the scale of nights; with most of the temporal variance explained by differences at this scale. Although no differences were detected by ANOVA, the scale of nights also contributed most to the overall variation in mean abundance of M. bennettae at Site 3.

In Tuggerah Lake, there were significant differences in mean abundance at temporal scales smaller than seasons at all sites. At Sites 1 and 3, there were significant differences (p<0.01) at the scale of weeks, with most temporal variance explained by this scale. At Site 2, however, a significant difference (and most temporal variance) was found at the scale of nights. Since seasonal variation was combined with monthly variation when correcting for the negative component of variation for seasons, differences between months made the largest relative contribution to temporal variance at Site 3, despite the significant differences detected between weeks.

2.3.4 Size Structure

Samples from Lake Macquarie contained proportionally fewer large prawns than those from

Tuggerah Lakes, with a statistically significant difference between size-frequency distributions 43

for both males (K-S test; D = 0.556; p<0.001) and females (K-S test; D = 0.398; p<0.001) (Figure

2.5. and Figure 2.6.). Within each estuary, the mean (± SE) size for females (Tuggerah Lakes:

19.7 (± 0.12); Lake Macquarie: 16.8 (± 0.10)) was larger than that of males (Tuggerah Lakes:

16.4 (± 0.06); Lake Macquarie: 14.0 (± 0.06)). Overall, male:female sex ratios were similar between Tuggerah Lake (1.05:1) and Lake Macquarie (0.97:1).

Table 2.3. Results of ANOVA (df = degrees of freedom; MS = Mean sum of squares; F = the F-statistic) and components of temporal variance (CV) for the mean numbers of M. bennettae caught at each site in Tuggerah Lake and Lake Macquarie. Statistically significant differences, *p<0.05; **p<0.01; ***p<0.001, † = variances were heterogeneous, so p was set at 0.01 to reduce the probability of Type I error (Underwood 1997).

Source Site 1 Site 2 Site 3 Df MS F CV MS F CV MS F CV

Tuggerah Lake

Season 1 1183.01 0.20 0.00 3800.17 1.72 33.23 5969.26 0.50 0.00 Month(S) 2 5775.47 2.22 68.29 2205.21 1.83 41.79 11839.51 3.53 272.01 Week(M(S)) 4 2605.72 18.42*** 205.35 1202.15 1.36 26.63 3354.64 11.56** 255.38 Night(W(M(S))) 8 141.47 1.28 5.18 882.54 14.29*** 136.80 290.09 1.02 0.72 Residual 80 110.39 110.39 61.75 61.75 285.79 285.79 Total 95

Cochran's C-test 0.6784† 0.3700 † 0.5290 †

Lake Macquarie

Season 1 46684.26 188.3** 967.42 4887.76 14.93 95.01 11.34 0.10 0.00 Month(S) 2 247.93 0.02 0.00 327.43 0.18 0.00 110.30 1.53 0.21 Week(M(S)) 4 10797.66 8.07** 495.25 1788.61 1.67 19.39 72.24 0.89 0.00 Night(W(M(S))) 8 1338.03 1.90 105.40 1068.82 13.61*** 165.05 81.51 1.43 3.57 Residual 80 705.63 705.63 78.54 78.54 57.02 57.02 Total 95

Cochran's C-test 0.3256† 0.5002 † 0.4891 †

The size-frequency distributions of female prawns were significantly different between nights within a week on only two and three occasions in Tuggerah Lake and Lake Macquarie, respectively. Similarly, significant night-to-night differences in size-frequency distributions of male prawns were detected in only one week of sampling in both estuaries (Table 2.4.).

The greatest variation in the size frequencies of both male and female prawns was observed at a scale of months and seasons, with significant differences detected between most months and both seasons (Table 2.4.). In Tuggerah Lake, a greater proportion of larger males and females were found in summer, with the recruitment of a second cohort of smaller (juvenile) prawns observed in February. In Lake Macquarie, a greater proportion of larger males and females were found during spring and there was no recruitment of a second cohort of prawns during February as observed in Tuggerah Lake (Figure 2.5. and Figure 2.6.).

Figure 2.5. Size-frequency distributions of populations of female M. bennettae sampled from Tuggerah Lake and Lake Macquarie. Data are pooled across nights, weeks and sampling trips in each month.

Figure 2.6. Size-frequency distributions of populations of male M. bennettae sampled from Tuggerah Lake and Lake Macquarie. Data are pooled across nights, weeks and sampling trips in each month.

Temporal Tuggerah Lake Lake Macquarie scale Females Males Females Males Night 1 vs. 2 ns ns *** * 3 vs. 4 ns * ns ns 5 vs. 6 ns ns ** ns 7 vs. 8 * ns ** ns 9 vs. 10 ns ns ns ns 11 vs. 12 na ns ns ns 13 vs. 14 *** na ns ns 15 vs. 16 na ns na ns

Week 1 vs. 2 ns ns ns ns 3 vs. 4 ns ns ns ns 5 vs. 6 ** *** ns *** 7 vs. 8 *** ns * ns

Month 1 vs. 2 ** ns ** ns 3 vs. 4 *** ** *** ***

Season 1 vs. 2 *** *** *** ***

2.4 Discussion

Variation in female reproductive condition and abundance of M. bennettae were often greatest at the smallest temporal scales examined (between nights and weeks). Indeed, small- scale temporal and spatial variability in abundance of aquatic organisms is common (Olabarria and Chapman 2002; Fraschetti et al. 2005; Rotherham et al. 2011) and apart from Site 1 in

Lake Macquarie, most of the variation in mean abundance was in fact found to be at the smaller scales of nights and weeks. Small-scale temporal patterns in abundance have also been reported for other penaeid species, with peaks and troughs in catch rates coinciding with particular lunar phases (Courtney et al. 1996). Although this study cannot be used to draw any direct conclusions regarding the catch rates of M. bennettae and its correlation with lunar phase, it highlights the need for smaller temporal scales to be considered in any future sampling of the abundance of penaeid populations.

In both Tuggerah Lake and Lake Macquarie, most of the variation in female reproductive condition was between nights within a week rather than between weeks, months or seasons.

This relatively non-descript pattern of gonad development at the larger temporal scales (from month-to-month and season-to-season) was also true for males in Tuggerah Lake. In contrast, variation in the proportion of mature males caught in Lake Macquarie was greatest between seasons, rather than between nights. These results reinforce the importance of hierarchical sampling designs in identifying the relevant scales for examining important demographic characteristics of organisms (Morrisey et al. 1992b; Underwood 1997; Rotherham and West

2009).

Sampling on a single night within a month (or week) is common in many previous studies of invertebrates (e.g. Courtney and Masel 1997; Kramarsky-Winter and Loya 1998; Calvo and

Templado 2004; McQuaid and Phillips 2006; Berger 2009; Rotherham and West 2009; Brogger et al. 2010). Our results show that this approach is inadequate for accurately describing patterns of reproduction of M. bennettae from month to month. The pattern of ovarian development of female prawns from month to month often depended on the particular night and week sampled. So, if we had followed the usual approach of sampling on only a single night within a month, our conclusions about temporal peaks in reproductive activity of M. bennettae could have potentially been erroneous.

Despite sampling the duration of the spawning period, not all ovarian stages were well represented in catches. Stage 4 (ripe) gonads accounted for less than 1% of mature female prawns sampled. Courtney (1996) observed a similar pattern in the reproductive condition of eastern king prawns (Penaeus plebejus Hess 1865) and suggested that this stage is either of short duration, or the catchability of such females is reduced. In contrast, large proportions

(>~0.6) of mature male prawns were sampled across most nights, weeks and months in both estuaries and could be a necessary response to the short duration of ripe females. Open thelycum penaeids, such as M. bennettae, mate when the female exoskeleton is hard and female ovaries are ripe and are thought to spawn soon after mating (Penn 1980; Yano et al.

1988; Dall et al. 1990). Consequently males would need to be ripe and ready to mate frequently through time, which could explain these high instances of ripe males. Further research is needed to examine these hypotheses.

In both Tuggerah Lake and Lake Macquarie, spatial variation in the mean proportion of mature or ripe female and male prawns caught was larger than the temporal variation at any of the scales examined. Habitat is fairly uniformly distributed in Tuggerah Lake (Roy et al. 2001), and the sampling sites selected in Lake Macquarie were of similar depth, predominantly unvegetated and planar. Therefore spatial variability in the distribution of prawns in both estuaries may also be influenced by other factors and needs to be investigated through future studies

This study cannot provide evidence for any particular process causing the observed spatial and short-term temporal variation in abundance or reproductive condition as such evidence is best provided by manipulative experiments rather than mensurative studies (Underwood et al.

2000). The variation may, however, be the result of the influence of biotic processes such as predation (Minello and Zimmerman 1983), rates of reproduction (Desmond et al. 2002), lunar periodicity in reproductive condition (Courtney et al. 1996) or natural mortality (O'brien 1994).

Abiotic processes such as localised water movements (Palmer et al. 1996), sea surface temperature (Aragón-Noriega and Alcántara-Razo 2005) or wind circulation (Ligas et al. 2011) can also affect lifecycles and migrating behaviour in various species of prawn, particularly in shallow estuarine and coastal waters. Similarly, sudden changes in climate, excess rainfall, river flooding and a rapid decrease in salinity may affect spawning patterns of M. bennettae (Dall

1957), possibly forcing prawns to leave estuarine waters for the ocean (Salini 1987). These processes operate continually at small temporal and spatial scales to modify distributions and abundances of organisms (Morrisey et al. 1992b).

In contrast to patterns of abundance and reproductive condition, variations in size-frequency distributions of male and female M. bennettae were generally greater at the larger (months and seasons) temporal scales examined. This result is an expected pattern and most likely a consequence of temporal patterns in growth. Further, the lack of small-scale temporal variation in size distributions of prawns indicates that the observed variation in reproductive condition was not due to differences in the sizes of prawns caught, but rather, the effect of biotic or abiotic processes and their interaction (Thrush 1991).

Very little is known about the behavioural, growth and reproductive rhythms of M. bennettae.

This study demonstrates the need for future sampling to be undertaken on replicate nights within a given temporal scale when designing longer-term studies of the reproductive biology and abundance of M. bennettae or similar penaeid species. This study also indicates that at each time of sampling there must be replicate sites randomly, or at least haphazardly, scattered across the most representative portion of the estuary. It is essential that patterns of abundance and reproductive condition of organisms be examined at relevant spatial and temporal scales for accurate determination of the life history characteristics of populations.

Such information is also crucial for stock assessments and evaluating appropriate harvest strategies for fisheries.

Chapter 3: Don’t blame it on the moonlight: abiotic drivers of reproductive development in an estuarine dependent prawn

Abstract

Lunar phase is regarded as a key driver of reproductive development and spawning activity in prawns, but across smaller-temporal scales other processes may have a significant influence.

Here, we examined the effects of lunar phase and other abiotic variables on the reproductive development of an estuarine-dependent prawn, Metapenaeus bennettae (Racek & Dall). We found that salinity, turbidity, water temperature and lunar phase each had a significant independent influence on the likelihood of female prawns being ripe throughout the spawning period. The likelihood of catching a ripe female increased on the new moon and first quarter of the moon and also during conditions of high salinity, high water temperature and low turbidity. For male prawns, however, significant interactions between salinity and lunar phase and also between turbidity and lunar phase were detected. These interactions indicated that salinity and turbidity have variable effects among the different lunar phases. Such complex relationships of reproductive timing and spawning success of M. bennettae, and potentially other aquatic species, are most likely adaptive responses to the highly variable conditions of estuarine environments.

Keywords: Penaeidae; Metapenaeus bennettae; reproduction; abiotic driver; lunar phase

3.1 Introduction

Lunar periodicity plays a significant role in the reproductive timing of many animals (e.g.

Cowgill et al. 1962; Baker and Dekker 2000; Dixon et al. 2006; Grant et al. 2009; Desjardins et al. 2011). The lunar cycle alone can cause a number of different environmental shifts such as changes in nocturnal ambient light, gravitational changes and shifting geomagnetic fields, which can then act as environmental cues for animals to synchronise reproduction (Takemura et al. 2004; Grant et al. 2009; Desjardins et al. 2011). Many marine animals, in particular, take advantage of these cues to avoid predation (Foster 1987; Acosta and Iv 1999; Ligas et al. 2011), maximise spawning success or enhance dispersal of larvae (Counihan et al. 2001; Takemura et al. 2004; Skov et al. 2005). Despite the widespread effect that lunar phase can have on the reproductive activity of marine organisms, there is no one particular phase that consistently affects reproductive timing more than another; peaks and troughs of reproductive lunar rhythms vary among different organisms depending on their life histories (e.g. Kojis 1986;

Courtney et al. 1996; Desjardins et al. 2011).

In addition to lunar periodicity, organisms in estuarine environments are subjected to irregular and often rapid changes in abiotic variables. For example, temperature, salinity and turbidity are usually driven by wind speed and direction (Lawson et al. 2007), rainfall (Racek 1959), tidal exchange and currents (Roy et al. 2001), which operate on smaller time scales than lunar periodicity (e.g. diurnal). Although previous research indicates that abiotic factors such as salinity, temperature, and turbidity can affect the behaviour and catch rates of marine invertebrates (Dall et al. 1990; Stoner 1991; Ligas et al. 2011; Munga et al. 2013), the extent to which these factors affect reproduction in wild populations are poorly understood.

Recent research on the estuarine-dependent prawn, Metapenaeus bennettae, in New South

Wales (NSW, Australia) suggested that factors other than lunar periodicity were important in driving reproduction (Young et al. 2013) because variation in the reproductive condition of females was larger at the temporal scale of nights compared to weeks, months or seasons.

That is, the proportion of ripe females varied more from night-to-night than from week-to- week or season-to-season. These results suggest that abiotic or biotic processes (and their interactions) operating at small temporal scales may influence reproduction in M. bennettae.

The results also highlighted the need for appropriate replication at hierarchical temporal scales in future studies examining the reproductive biology of M. bennettae.

In this study, we examined variation in the reproductive condition of male and female M. bennettae across four replicate lunar cycles and across natural gradients of turbidity, salinity and water temperature, in an eastern Australian estuary using a mensurative experimental design. The hypothesis tested was that reproductive development of M. bennettae was affected not only by lunar phase, but also by other abiotic variables including turbidity, salinity and water temperature.

3.2 Materials and methods

3.2.1 Study location and experimental design

The study location, experimental design and methodology are similar, but with minor differences, to those described elsewhere (see Young et al. 2013). The experiment was carried out in Tuggerah Lake (33°21′S, 151°30′E; surface area ~80 km²), a large, barrier estuary on the

central coast of NSW. Tuggerah Lake is a shallow (mean depth ~2 m), microtidal estuary that is connected to the ocean via a relatively narrow entrance (Roy et al. 2001) (Figure 3.1.).

Three sites were randomly selected over predominately flat, unvegetated sediment, the most predominant substrate within Tuggerah Lakes (Roy et al. 2001), and separated by 2-8 km and at depths ranging from 1-4 m. Each site was sampled on two randomly selected nights, in each of the four lunar phases, during two consecutive months in two consecutive seasons (i.e. spring: October and November 2011, summer: January and February 2012; with a total of 16 sampling nights per season). These seasons represent the general reproductive period of M. bennettae and the period when they occur at their greatest abundances in Tuggerah Lake

(Racek 1959; Young et al. 2013).

Metapenaeus bennettae remain buried in sediment throughout the day (Dall 1957) and are hard to catch during this time (Morris and Bennett 1952; Rotherham et al. 2008) so sampling was done at night (between 2000 h and 0200 h). On each night of sampling, six non- overlapping, replicate tows (each lasting 5 min at a speed of ~1.2 m.s-1) were carried out at each site with a beam trawl that had a vertical and horizontal opening of 0.8 m and 3 m, respectively. The trawl was configured with 41 mm diamond-shaped mesh in the body and 12 mm knotless netting hung on the bar (i.e. square shaped) in the codend (Rotherham et al.

2008). After each replicate tow was completed, M. bennettae were sorted from the catch, placed in labelled plastic bags and put on ice immediately.

3.2.2 Examination of prawns

The carapace length (CL - the straight line distance between the base of the eye orbit and the posterior edge of the carapace) of each sampled M. bennettae was measured using electronic callipers; sex was determined by examining the thoracic sternite and identifying the presence of either the thelycum (female genitalia) or petasma (male genitalia). Both male and female M. bennettae were assigned a moult stage (soft or hard) and the presence or absence of a spermatophore was determined for every female sampled.

Prawns were examined macroscopically to determine their stage of gonad development.

Female prawns were assigned to one of four stages of ovarian development based on the criteria of Tuma (1967): Stage 1 (undeveloped), ovary thin and translucent; Stage 2

(developing), ovary ivory-yellow and slightly enlarged; Stage 3 (mature), ovary yellow-orange and occupying a large proportion of the abdomen; and Stage 4 (ripe), ovary olive-green and extending throughout the abdomen into the carapace. The histological characteristics of recently-spawned female prawns have proven difficult to distinguish from those that have not spawned and subsequently reabsorbed their ovaries (Courtney et al. 1996). Thus, no female prawns were classified as Stage 5 (spent). The female prawns that were caught in mid- transition from one stage to the next were assigned a combination stage (e.g. Stage 1/2 or

Stage 3/4). Two stages were used to classify male testis development: Stage 1 (undeveloped), sperm sack translucent; and Stage 2 (mature/ripe), white gelatinous mass present in the sperm sack.

3.2.3 Collection of abiotic data

In order to examine any possible correlations between environmental factors and the reproductive development of M. bennettae, data were collected for several environmental parameters. Wind speed and wind direction data were obtained through the Bureau of

Meteorology from the Norah Head weather station (33°28′S, 151°58′E), which is the closest in proximity to Tuggerah Lake (<3 km). Wind speed and direction were also recorded with a portable wind meter, twice, at each site during sampling to validate readings from the weather station. Banas et al. (2005) highlighted that wind speed 5-33 hours before sampling is a good predictor of the concentration of suspended solids in the water column of micro-tidal lagoons dominated by fine particle sediment, comparable with the properties of Tuggerah Lake (Roy et al. 2001). Given the location of the selected sampling sites, we assumed wind direction would also influence water disturbance. A turbidity key was therefore created to estimate the mean turbidity for each site and sampling trip using wind speed and wind direction data collected over the 24hrs prior to sampling and calculations of fetch. Based on the findings of Banas et al.

(2005), turbidity estimates were conservatively categorised into 3 levels, 1 being low turbidity

(~0 mg/L suspended solids), 2 being moderate turbidity (~100mg/L – 300mg/L suspended solids) and 3 being high turbidity (~300mg/L -800mg/L suspended solids).

Temperature and salinity monitors were also deployed at the three sites at the beginning of the sampling period and remained in the water (suspended ~1m from the bottom) throughout the duration of the study. The monitors measured temperature and salinity every 10 minutes.

These data were then collated and an average was calculated from all measurements for each sampling day (24 h period).

3.2.4 Data Analyses

Generalized linear models (GLMs) were used to examine the influence of the categorical variable lunar phase (4 levels: 1st quarter, full moon, 3rd quarter and new moon) as well as that of the continuous variables turbidity, salinity and water temperature and the interactions between all the variables on the reproductive development of male and female M. bennettae.

A separate GLM was used for each sex. Reproductive development was treated as a binary response variable (1 = ripe, i.e. Stage 2 males and Stage 4 females, and 0 = not ripe, i.e. Stage 1 males and Stages 1-3 females) in the GLMs and the models consequently assumed a binomial distribution. The predictor variables examined in the full models were initially selected in the interest of reducing collinearity among predictors (assessed using variance inflation factors

(Zuur et al. 2010)) and reducing linear separation (Davidson and MacKinnon 1993). Models were then reduced towards parsimony on the basis of Akaike Information Criteria (AIC) (Boyce et al. 2002; Field et al. 2005). For the final parsimonious models, the influence of each retained parameter or interaction term on reproductive development was then examined using partial z-tests (α = 0.05). These tested the null hypothesis that βi = 0 for each retained parameter or interaction term, where βis were the partial regression coefficients for the retained parameters and interaction terms.

Where the influence of lunar phase was shown to be independently significant, Tukey’s post-

Hoc tests (α = 0.05) were used to compare different levels of each lunar phase in a pair-wise manner. For each sex, all 4-way and all 3-way interactions were omitted on the basis of AIC values. This was also the case for all 2-way interactions between the continuous variables.

Where an interaction between a continuous variable and lunar phase was retained in a model

and shown to have a significant influence, bar charts were plotted to show the mean value of each significant continuous variable at which ripe or not ripe M. bennettae were encountered during each lunar phase.

3.3 Results

A total of 2131 M. bennettae were caught throughout the sampling period, 1167 males and

964 Females (Table 3.1.). Catches of M. bennettae were larger over the summer months and peaked in January (Table 3.1.). Overall, a greater number of prawns were caught on the sampling nights coinciding with the new moon (Table 3.1.). Over the 4 months of sampling, larger numbers of prawns were caught at Site 1 with a peak in mean numbers caught per trawl observed at Site 3 during each new moon across most of the sampling period. Patterns of abundance were inconsistent among sites; however, there was no significant spatial difference in the number of females or males of M. bennettae with ripe gonads detected (Binomial GLM;

Factor: Site (3 levels); P (>|z|) >0.05). The sex ratio of males to females was consistent over the entire sampling period, being around 1.5. However, there were six nights of sampling, mainly during November, when numbers of females exceeded the number of males that were caught

(Table 3.1.).

Turbidity varied considerably across the whole sampling period, increasing sometimes from relatively low turbidity to high turbidity within 24 hours. Salinity ranged from 17.3‰ to 37.9‰ and also varied noticeably between consecutive sampling days (up to 3‰). Water temperature ranged from 16.3°C to 24.8°C with a general rise in temperature from spring to summer, as expected. However, there was also considerable smaller-scale variability in water temperature,

regularly rising and falling up to 4°C between lunar phases within both of the sampling seasons.

Season Month Site Female Male

1st full 3rd new 1st full 3rd new quarter moon quarter moon quarter moon quarter moon Site 1 3 5 23 42 3 4 24 52 October Site 2 2 3 8 4 8 6 15 6 Site 3 4 6 9 6 5 8 5 13 Spring

Site 1 71 30 40 21 40 34 36 48 November Site 2 7 10 12 9 4 3 11 20 Site 3 20 22 23 36 12 15 18 36

Site 1 23 17 47 29 31 20 62 52 January Site 2 26 11 22 35 29 18 42 41 Site 3 17 24 11 48 32 20 19 63 Summer

Site 1 11 35 22 26 10 50 24 33 February Site 2 4 20 20 21 7 27 36 17 Site 3 5 20 29 25 11 28 29 40

Total 193 203 266 302 192 233 321 421

3.3.1 Abiotic influence on reproductive development

For the reproductive development of females, the GLM detected significant independent effects of all four factors (lunar phase, turbidity, salinity and water temperature). None of the low-order interactions were retained in the model based on AICs. Turbidity had a negative influence on reproduction (P<0.05), i.e. the more turbid the water, the lower the chance of a female prawn being ripe. In contrast, salinity and water temperature had a significant positive effect (P<0.05) on reproductive development of females, i.e. the more saline or warmer the water, the greater the chance of a female prawn being ripe (Table 3.2.; Figure 3.2.). The post- hoc test on lunar phase showed that for female prawns sampled during the 1st quarter of the moon, there was a greater statistical likelihood of being ripe compared to those caught during the full moon (Table 3.3, Figure 3.3.). Similarly, females caught during the new moon were more likely to be ripe than those caught during the full moon and the 3rd quarter (Figure 3.3.).

Female M.bennettae (n=964) β (S.E.) P (>|z|)

Intercept -4.872 (1.546) 0.002 **

LUNAR PHASE 3rd Quarter -0.426 (0.219) 0.052

LUNAR PHASE Full Moon -0.845 (0.274) 0.002 **

LUNAR PHASE New Moon 0.151 (0.216) 0.485

SALINITY 0.085 (0.018) 3.04E-06 ***

TEMPERATURE 0.141 (0.058) 0.015 *

TURBIDITY -0.774 (0.164) 2.32E-06 ***

Table 3.3. The results of Tukey’s post-Hoc test (α = 0.05) comparing different levels of each lunar phase (4 levels: 1st quarter, full moon, 3rd quarter and new moon) in a pair-wise manner.

Female M.bennettae (n=964) β (S.E.) P (>|z|)

3rd Quarter - 1st Quarter -0.426 (0.220) 0.315

Full Moon - 1st Quarter -0.845 (0.274) 0.013 *

New Moon - 1st Quarter 0.151 (0.216) 1.000

Full Moon - 3rd Quarter -0.420 (0.253) 0.583

New Moon - 3rd Quarter 0.577 (0.212) 0.039 *

New Moon - Full Moon 0.996 (0.277) 0.002 **

For the reproductive development of males, both the lunar phase x salinity and lunar phase x turbidity interactions were found to be significant (Table3. 4.). These interactions indicate that turbidity and salinity had inconsistent effects on the likelihood of encountering ripe males among the different lunar phases. Ripe males were generally caught at higher average turbidity during the new moon than other moon phases. For the 1st quarter and full moon, there was little discernible difference in the average salinity at which ripe and non-ripe males were caught (Figure 3.4.). During the 3rd quarter and new moons, however, ripe males were caught at higher average salinities than non-ripe males (Figure 3.4.). It should be noted that the biological relevance of the significant differences described above for male M. bennettae remains equivocal given the mainly large standard errors (and thus confidence intervals) around average turbidity and salinity at each lunar phase. The only factor that was not involved in a significant interaction and also had a significant independent effect on male ripeness was water temperature, lower water temperature being associated with a greater chance of male prawns being ripe (Table 3.4.).

Male M.bennettae (n=1167) β (S.E.) P (>|z|)

Intercept 13.741 (4.777) 0.004 **

LUNAR PHASE 3rd Quarter -14.209 (6.011) 0.018 *

LUNAR PHASE Full Moon -6.683 (6.471) 0.302

LUNAR PHASE New Moon 97.111 (89.518) 0.278

SALINITY -0.170 (0.079) 0.031 *

TEMPERATURE -0.398 (0.142) 0.005 **

TURBIDITY 0.731 (0.387) 0.059

LUNAR PHASE 3rd Quarter: SALINITY 0.241 (0.083) 0.004 **

LUNAR PHASE Full Moon: SALINITY 0.090 (0.131) 0.493

LUNAR PHASE New Moon: SALINITY -0.868 (0.779) 0.265

LUNAR PHASE 3rd Quarter: TEMP 0.372 (0.207) 0.072

LUNAR PHASE Full Moon: TEMP 0.315 (0.251) 0.210

LUNAR PHASE New Moon: TEMP -3.922 (3.547) 0.269

LUNAR PHASE 3rd Quarter: TURBIDITY -0.448 (0.642) 0.486

LUNAR PHASE Full Moon: TURBIDITY -1.423 (0.646) 0.027 *

LUNAR PHASE New Moon: TURBIDITY 6.737 (5.502) 0.221

Figure 3.4. Mean turbidity and salinity (± SE) at which ripe and not ripe male M. bennettae were caught during the 4 different lunar phases: 1st quarter, full moon, 3rd quarter and new moon. Turbidity estimates are categorised into 3 levels, 1 being low turbidity (~0 mg/L suspended solids), 2 being moderate turbidity (~100mg/L – 300mg/L suspended solids) and 3 being high turbidity (~300mg/L - 800mg/L suspended solids). Data are pooled across sampling sites and seasons.

3.4 Discussion

As predicted by our hypothesis, lunar phase did not have a sole influence on the reproductive development of females of M. bennettae. Indeed, all four abiotic variables (turbidity, salinity, water temperature and lunar phase) had a significant effect on whether or not a female prawn was ripe. High salinity, high water temperature, low turbidity and the 1st quarter and new moon phases all increased the likelihood of encountering a ripe female. For the reproductive development of males, both the lunar phase x salinity and lunar phase x turbidity interactions were found to be significant, indicating that turbidity and salinity had inconsistent effects on the likelihood of encountering ripe males among the different lunar phases.

In contrast to these findings, previous research suggested that spawning of M. bennettae was largely influenced by lunar phase, particularly the full moon, and was probably driven by moonlight, rather than any other environmental shifts triggered by lunar phase (Morris and

Bennett 1952; Racek 1959). Nevertheless, it is unclear whether these particular studies included replicate nights of sampling within each lunar phase. Consequently, their results may be confounded owing to smaller scale temporal variation (Young et al. 2013). Further, unlike our study, they did not quantitatively investigate the effects of additional abiotic variables.

If levels of moonlight are more influential than other environmental shifts triggered by lunar phase, as previous research suggested (Morris and Bennett 1952; Racek 1959), then levels of artificial light from urbanised areas also have the potential to confound the effect of lunar phase on organisms. Because M. bennettae complete their entire lifecycle within the estuarine environment, they are more exposed to artificial light from urban developments than other 74

penaeid species that spawn in offshore oceanic waters. The urban development surrounding

Tuggerah Lakes may contribute to the complex relationship observed between lunar phase and the reproductive timing of M. bennettae. Previous reports of lunar periodicity in penaeid reproductive activity may have come from areas with relatively low artificial light pollution or from times when urban development was minimal. Although moonlight is not the sole environmental influence triggered by lunar phase, where moonlight is the necessary cue for reproductive events, artificial lighting is likely to hinder synchronization among breeders, and may negatively affect reproductive success (Grant et al. 2009).

Early discoveries showed the effects of lunar periodicity on the reproductive timing of marine organisms (Amirthalingam 1928; Aiyar and Panikkar 1937; Racek 1959); however, daily and semi-lunar rhythms have generally been poorly established for penaeid prawns. The small number of studies supporting the presence of such rhythms have focused on only single abiotic factors, without considering the many other environmental variables that could also affect reproductive timing at smaller scales (e.g. Courtney et al. 1996). Prior to our study, evidence that penaeid prawns undergo fluctuations in reproductive behaviour at smaller time scales and irrespective of lunar phase was limited.

A particular study that was carried out in the early 90’s initially suspected that significant increases in the reproductive activity of Penaeus stylirostris around the new moon were due to stronger tidal currents that provoked increased mixing of lagoon substrates and waters.

However, because there were two major tidal episodes and only one significant reproductive peak, it was concluded that P. stylirostris has an endogenous reproductive cycle (Holtschmit

and Romero 1991). This study did not consider whether the lunar cycle and tidal currents, or any other environmental variable, could have an interactive effect on reproductive timing.

In this present study three other abiotic variables were examined alongside lunar phase. First of all, turbidity had a negative effect on female reproductive development. We did not, however, measure turbidity directly. Turbidity was estimated using wind speed and direction to predict levels of suspended solids, which is a justified and reliable method (Banas et al.

2005). Despite a lack of research on the effects of turbidity on reproductive development of penaeids, a few studies have considered how turbidity might affect larvae and juveniles (Dall

1957; Young 1978). For example, Dall (1957) suggested post larvae and early juvenile prawns favour sheltered localities with minimal water disturbance. Moreover, Young (1978) found that less turbid water was associated with increased seagrass growth and that juvenile abundance of M. bennettae was strongly correlated with seagrass cover. Thus, it is a reasonable hypothesis that ovarian development and spawning times of M. bennettae might coincide with lower turbidity levels. Lower turbidity levels at times of spawning would ensure that eggs don’t disperse too far from estuarine spawning grounds with any associated water movement, giving larvae the best chance of staying close to these suitable nursery habitats. Both Banas et al.

(2005) and Lawson et al. (2007) found that increased water movement promotes higher turbidity, with both of these driven mainly by wind speeds. The locomotive power of penaeid larvae is limited and highly influenced by any form of water movement or disturbance. Thus, if larvae are forced out of the sheltered, estuarine habitat, they may perish (Racek 1959).

Another important result was that salinity had a positive effect on the maturity of females of

M. bennettae. Racek (1959) also found that salinity played a significant role in the reproductive

development and spawning of M. bennettae. He found that a rapid drop in salinity following extensive flooding triggered the migration of M. bennettae into offshore waters (areas with higher salinity: approaching 35‰) to spawn. In contrast, Courtney and Masel (1997) found that over short time periods (< one lunar month) egg production of M. bennettae was greater in areas with lower salinity (30-32‰). However, their sampling sites were within Moreton Bay, which has a greater oceanic influence (Young and Carpenter 1977) than in a coastal lagoon such as Tuggerah Lakes. Courtney and Masel (1997) also considered relatively high levels of salinity to be greater than 32‰, which was much higher than the mean salinity (±SE) at which ripe females were caught in the present study (Figure 3.2.).

In addition to salinity, water temperature also had a positive influence on the reproductive development of female prawns. The effects of water temperature on maturity and ovarian development of penaeids are widely established in the literature, especially at larger temporal

(seasonal) and spatial scales (latitudes). The results of this study show similar trends to that of many other studies, where a rise in water temperature (commonly between 22°C and 25°C) is paralleled by peak ovarian development and spawning activity (e.g. Penn 1980; Aragón-

Noriega and Alcántara-Razo 2005; Castilho et al. 2007).

An interesting study carried out in the mid-80s showed the combined effects of both salinity and water temperature on the reproductive success of M. bennettae (Preston 1985). Preston

(1985) found that embryos of M. bennettae showed an irreversible tolerance adaptation to both ambient salinity and temperature and this adaptation persisted at least as far as the first mysis larval stage. They hypothesised that limits of tolerance of eggs and larvae may be determined by the salinities and temperatures at which the parent populations developed

gonads, the internal osmotic environment in which ovaries developed and yolk deposits were formed, or both. Preston (1985) also found that the survival of the eggs of M. bennettae was significantly less in a coastal lagoon where there were daily fluctuations in temperature (3°C) and salinity associated with freshwater inflow (5‰) and tidal flushing (3‰) compared to the laboratory where constant conditions were maintained. Similar fluctuations may explain why our earlier study showed that most variation in reproductive condition occurred at the smaller time scales of days and weeks rather than larger time scales of months and seasons (Young et al. 2013). It may also explain why both salinity and temperature had a significant effect on the likelihood of encountering a ripe female of M. bennettae in the present study.

Considering the reproductive activity of male M. bennettae, not only were the effects of turbidity and salinity inconsistent among lunar phases, large standard errors around average turbidity and salinity among lunar phases were also noted. This suggests that the interactive effect of salinity, turbidity and lunar phase are either too complex to tease apart from this study, that they are not biologically important or it may suggest that males are almost always reproductively viable despite varying environmental conditions. Ogle (1992) showed that environmental conditions had no influence over the reproductive development of captive male

P. vannamei. With this is mind and considering the large proportions of ripe male M. bennettae Young et al. (2013) sampled across most nights, weeks and months in Tuggerah

Lakes, it is plausible to assume that these environmental variables have little influence over the reproductive development of male M. bennettae. Further, in contrast to closed thelycum penaeids, open thelycum penaeids, such as M. bennettae, mate when the female exoskeleton is hard and female ovaries are ripe and are thought to spawn soon after mating (within a few hours) because spermatophores are attached externally and are easily dislodged (Penn 1980;

Yano et al. 1988; Dall et al. 1990). This would mean that if females are spawning in response to 78

daily fluctuations in key environmental variables, males would need to be ripe and ready to mate frequently through time, which could explain high instances of ripe males and their relatively unabated reproductive development patterns.

Other biotic and abiotic processes that were not considered here may also influence reproductive timing of males and females of M. bennettae. For example, food availability and nutrition (Racek 1959; Ogle 1992) as well as localised water movements and tides (Dall 1957;

Palmer et al. 1996) have been shown to have a strong influence on the reproductive behaviour and life cycles of various prawn species.

In conclusion, we have shown that lunar phase, salinity, turbidity and temperature each influenced female reproductive activity independently. The influence of these variables on male reproductive activity was, however, more complex and interactive. Invertebrates display a wide range of reproductive patterns and a reproductive season is not necessarily fixed for a species but can vary with environmental conditions (Kuklinski et al. 2013). In environments that are highly variable, like the estuarine environment, reproduction across multiple seasons may be an adaptation to increase the likelihood of successful recruitment (Hadfield and

Strathmann 1996). These environments are subject to irregular and often rapid changes in temperature, salinity and turbidity and manipulative experiments are needed to determine the extent to which these abiotic variables are driving reproductive development. Nevertheless, from our findings we can suggest that because these variables vary from day-to-day, they could be affecting the success of reproductive development and spawning of M. bennettae at small scales. Further research is required to determine if this is also the case with other

estuarine crustaceans and whether the patterns uncovered here are consistent among other estuaries.

From an ecosystem-based management perspective, these findings not only give us an understanding of how environmental variables can affect the reproduction and success of M. bennettae stocks but how they can potentially affect the behaviour and possibly reproductive success of other organisms within the same estuarine ecosystem. Lunar rhythmicity in organisms, for example, can be categorised into either ‘innate’ or ‘apparent’(Ikegami et al.

2014). Organisms that fall within the ‘innate’ category are those that have active lunar-related rhythmicity, such as the European eel Anguilla Anguilla, whose downstream spawning migration is triggered by moonless nights between 3rd quarter and new moon (iMiyai et al.

2004). The organisms that are categorised as ‘apparent’ are influenced by the lunar-related change in behaviour of ‘innate’ organisms and therefore their lunar rhythmicity can disappear if other influential species are removed from the ecosystem (Ikegami et al. 2014).

Consequently, understanding the effects of lunar periodicity in specific organisms can contribute greatly to a more holistic understanding of the whole ecosystem and its management. This cascade effect could also be true, not only for lunar rhythmicity, but for many other environmental variables, such as: water temperature, salinity and turbidity. More research needs to be carried out to determine if the reproductive patterns, evident in M. bennettae, may actually be caused by behavioural and/or reproductive patterns of other organisms or whether the reproductive patterns of M. bennettae are affecting the other organisms that share its ecosystem. Even so, information on relationships between abiotic environmental variables and reproductive activity, such as that specifically provided by this

study, can contribute to better stock assessment and effective ecosystem-based management of exploited fisheries populations such as M. bennettae.

Chapter 4: General Discussion

4.1 Ecosystem based fisheries management

Fishing pressure poses a substantial threat to many marine species across the globe, however, it is not the only factor influencing the sustainability of exploited stocks (Brander 2007).

Changes in environmental conditions and how species respond to these changes can also contribute greatly to abundance, growth, reproductive development and successful recruitment (Jacobson et al. 2001; Engelhard et al. 2014; Kortsch et al. 2015). Understanding how marine species are affected by naturally occurring environmental change is just as critical to the sustainable management of these resources as understanding the extent and detriment of anthropogenic pressure (Botsford et al. 1997). A holistic, or ecosystem based, approach to fisheries management (EBFM), where an understanding of multi-species interactions and the influences of the physical environment is prioritized over managing single target species

(Pikitch et al. 2004), represents a current and future focus of fisheries management.

Unfortunately, for many exploited species including, Metapenaeus bennettae there is little known about key biological parameters and the effect of fishing and environmental variability

(e.g. Morris and Bennett 1952; Dall 1957; Courtney and Masel 1997). As a first step to improving the assessment and management of any species, there is a need to understand how key biological parameters vary spatially and temporally and what environmental processes could be influencing their variability.

4.2 Matching process with the scale of observation

This thesis successfully examined the potential for fine-scale variability to confound broader patterns of reproduction and abundance of M. bennettae and the importance of appropriate sampling intervals for future studies. This thesis also identified the environmental variables that affect the reproductive development and spawning of M. bennettae and revealed how an understanding of these interactions can assist future management of this exploited species.

The results reported in Chapter 2 showed that the reproductive condition and abundance of female M. bennettae varied significantly at the smallest temporal scales sampled (between nights and weeks). In both Lake Macquarie and Tuggerah Lakes, mean abundance and female reproductive condition varied most between nights within a week than between weeks, months or seasons. Patterns in male reproductive condition were different in the two estuaries; variation in male reproductive condition was greatest between days within a week in Tuggerah lakes. In contrast, this variation was greatest between seasons in Lake Macquarie.

Spatial variation (among sampling sites) in reproductive condition of females and males was larger than the temporal variation at any of the scales examined. As expected, length frequency varied greatest between months, and this was presumably due to growth.

Chapter 3 went on to further investigate this variability in reproductive activity by examining the environmental processes that might be influencing the reproductive condition of M. bennettae at this fine scale. Four key environmental variables that have been shown to influence reproduction in other marine organisms were examined: lunar phase (Counihan et al.

2001; Takemura et al. 2004; Desjardins et al. 2011), turbidity (Gray et al. 2012; Gyory et al.

2013), salinity (Preston 1985; Berger 2009) and temperature (Aragón-Noriega and Alcántara-

Razo 2005; Beyrend-Dur et al. 2011). Although lunar phase is regarded as one of the main drivers for reproductive development in marine organisms (Ikegami et al. 2014), it did not have a sole influence on reproductive development of M. bennettae. Indeed, all four variables had a significant effect on the reproductive development of females. Since these environmental variables fluctuate on a daily basis, they may have been responsible for small-scale temporal and spatial variation in female reproductive development observed - possibly affecting the ultimate success and extent of reproduction and spawning of M. bennettae. Invertebrates display a wide range of reproductive patterns and a reproductive season is not necessarily fixed for a species but can vary with environmental conditions (Kuklinski et al. 2013). In environments that are highly variable, like the estuarine environment, reproduction across multiple seasons may be an adaptation to increase the likelihood of successful recruitment

(Hadfield and Strathmann 1996).

The interactive effect of turbidity, salinity and lunar phase on male reproductive development indicates that the effects of these environmental variables are complex, and may suggest that males are always reproductively viable. Ogle (1992) also showed that environmental conditions had no influence over the reproductive development of captive male P. vannamei.

With this is mind and considering that large proportions of ripe male M. bennettae were sampled across most nights, weeks and months (Chapter 2), it is plausible to assume that these environmental variables have little influence over the reproductive development of male

M. bennettae. Further, closed thelycum penaeids mate following moulting when their exoskeleton is soft and they can store spermatophores for several days or weeks before

spawning. Therefore these closed thelycum species may be expected to have broader patterns

(lunar) in reproductive state (Courtney et al. 1996; Rothlisberg 1998). In contrast, open thelycum penaeids, such as M. bennettae, mate when the female exoskeleton is hard and are thought to spawn soon after mating (within a few hours) because spermatophores are attached externally and are easily dislodged (Penn 1980; Dall et al. 1990). This would mean that if females are spawning in response to daily fluctuations in key environmental variables, males would need to be ripe and ready to mate frequently through time, which could explain these high instances of ripe males that was observed here and their relatively unabated reproductive development patterns.

Overall, the findings of this thesis highlight the importance of hierarchical sampling designs in identifying relevant temporal and spatial scales for examining key biological parameters such as the abundance and reproductive condition of M. bennettae and potentially many other aquatic organisms. This thesis also confirms that reproductive development and spawning of

M. bennettae is significantly influenced by not only lunar phase but also changes in other estuarine environmental conditions such as turbidity, salinity and water temperature. Future sampling of M. bennettae should include replicate nights within a given temporal scale (e.g. lunar month) and replicate sites spread across the estuary. Knowledge of temporal and spatial reproductive patterns and potential drivers for this variation is essential for determining whether implementing closures to commercial fishing would be a viable and appropriate management tool as well as defining the timing and extent of such closures. Commercial fishing closures are a common management tool used to control the impacts of fishing pressure and reduce the risk of over exploitation, particularly in penaeid prawn fisheries

(Watson et al. 1993).

4.3 Implications for management of M. bennettae

Courtney and Masel (1997) suggested that penaeid species are likely to become more vulnerable to overfishing with increasing latitude. They asserted that P. esculentus is more likely to experience recruitment overfishing in Moreton Bay than M. bennettae because it produces significantly fewer eggs as a result of a small population of adult females spawning over a brief period. We could make the same comparison with Moreton Bay (Queensland) M. bennettae stocks and NSW stocks. In NSW there is a smaller population of adult spawners and they spawn over a shorter period of time than QLD stocks (Stewart et al. 2015), therefore NSW stocks are more likely to experience recruitment over fishing than QLD stocks. To reduce the effect of recruitment overfishing in penaeid fisheries, it is important to understand the temporal and spatial components of egg production in order to monitor the level of fishing effort focused on spawning stocks (Penn et al. 1995; Gracia 1996).

The current Fisheries Management Regulation plan for Tuggerah Lakes (including Budgewoi and Munmorah Lakes), together with surrounding creeks and tributaries, states that commercial prawn seine nets and prawn running nets are the only net methods to be used to catch prawns and that prawn seine nets are only to be operated from sunrise to sunset. This current management plan is in place to reduce fishing pressure on these estuarine prawn stocks by eliminating prawn trawlers and limiting the majority of fishing effort to day-time hours when prawns are less likely to be caught. The declining annual commercial landing trends (Figure 1.3.) together with the declining catch per unit effort (CPUE), especially in the last decade (Stewart et al. 2015), suggests this management is still not adequate.

Over 50 years ago, Racek (1959) suggested that a management plan involving a closed season of commercial fishing in NSW estuaries between October 1st and Dec 15th would allow M. bennettae a period to mate and spawn before being caught. The findings of this thesis propose that a closed season may not actually have the desired effect of preventing further overfishing and rebuilding the stock because reproductive development and therefore spawning and recruitment varies more from day-to-day than season-to-season. So although temporal closures of commercial fishing could be implemented relatively easily to account for the influence of lunar phase, the significant influence of turbidity, water and salinity and the unpredictable and rapid nature of changes in these environmental parameters could mean that any form of temporal fishing closures may not be an ideal management option for NSW

M. bennettae stocks.

From an EBFM perspective, these findings not only give us an understanding of how environmental variables can affect the reproduction and success of M. bennettae stocks but how they can potentially affect the behaviour and possibly reproductive success of other organisms within the same estuarine ecosystem. Lunar rhythmicity in organisms, for example, can be categorised into either ‘innate’ or ‘apparent’(Ikegami et al. 2014). Organisms that fall within the ‘innate’ category are those that have active lunar-related rhythmicity, such as the

European eel Anguilla Anguilla, whose downstream spawning migration is triggered by moonless nights between 3rd quarter and new moon (iMiyai et al. 2004). The organisms that are categorised as ‘apparent’ are influenced by the lunar-related change in behaviour of

‘innate’ organisms and therefore their lunar rhythmicity can disappear if other influential species are removed from the ecosystem (Ikegami et al. 2014). For example, the spawning of brittle star Ophiopholis aculeata was shown to closely follow spawning of various Ascidians

(Ascidia callosa, Halocynthia pyriformis) and it was suggested that these synchronous heterospecific spawning events follow a lunar periodicity but species such as the brittle star could be receiving a cue from lunar rhythmicity of the ascidian species and the release of their gametes (Mercier and Hamel 2010). Consequently, understanding the effects of lunar periodicity in specific organisms can contribute greatly to a more holistic understanding of the whole ecosystem and its management. This cascade effect could also be true, not only for lunar rhythmicity, but for many other environmental variables, such as: water temperature, salinity and turbidity. More research needs to be carried out to determine if the reproductive patterns, evident in M. bennettae, may actually be caused by behavioural and/or reproductive patterns of other organisms or whether the reproductive patterns of M. bennettae are affecting the other organisms that share its ecosystem.

4.4 Future direction and conclusions

There are many potential directions for estuarine research that can build upon the results of this thesis. For example, there were a number of environmental variables that could not be examined in this study due equally to a lack of sampling resources and the fact that generalized linear models are often limited in terms of the number of variables that can be logically included in a single model (Fox 2008). Availability of food, for instance, could be another factor driving the reproductive development of M. bennettae and causing small-scale temporal and spatial variation in their reproductive activity. Some previous studies on invertebrate reproduction have found that ovarian maturation and egg formation can be delayed when food is limited (Berger 2009; Mondy et al. 2014). Although water movements in shallow barrier estuaries such as Tuggerah Lakes are most commonly dominated by wind 88

stress rather than tides (Roy et al. 2001), tidal activity could be an additional environmental variable affecting the reproductive development and behaviour of M. bennettae. Despite the close alignment between tidal fluctuation and lunar phase, tidal dominance by one lunar phase is not constant; it switches between the new and full moon approximately every seven months and some invertebrates have been shown to adjust their spawning so larvae are released with the higher amplitude high tides, regardless of lunar phase (Skov et al. 2005).

Rainfall and wind data were also excluded from the final model on the basis of collinearity with water temperature and turbidity, respectively (Chapter 3). It is therefore possible to assume rainfall and wind would have a similar influence as their respective retained variable on the reproductive development of M. bennettae. It’s important to note at this point that statistical models show us patterns rather than causal relationships (Fox 2008) so manipulative experiments are also needed to determine the extent to which these abiotic variables drive female reproductive development (Underwood 1997).

From yet another perspective of EBFM, future research into other environmental influences must be accompanied by other ecosystem studies on multi-species interactions such as competition and predation to improve our understanding of the function and structure of the whole ecosystem and how the success of M. bennettae might impact other economically important species (Pikitch et al. 2004). Metapenaeus bennettae is harvested as a secondary target in fisheries targeting species such as eastern king prawns (Penaeus plebejus), school prawns (Metapenaeus macleayi) and yellowfin bream (Acanthopagrus australis) (Rowling et al.

2010). M. bennettae is also an important component of the diet of commercially important species such as yellowfin bream, dusky flathead (Platycephalus fuscus), common estuary stingray (Dasyatis fluviorum) and porcupine fish (Dicotylichthys punctulatus) (Dall et al. 1990).

A better understanding of the interactions between these species and M. bennettae could therefore mitigate the effects of anthropogenic and naturally occurring pressures on natural assemblages of species in estuarine ecosystems and aid in the sustainable management of M. bennettae and other commercially important species.

In light of a growing global population and rising demand of aquatic resources there is an urgent need to for effective management of exploited stocks (Botsford et al. 1997). For penaeid stocks in particular, an understanding of the relationship between spawning stock and recruitment is essential to prevent recruitment over fishing. To achieve this it is necessary to identify drivers of reproduction and study these patterns over long periods of time (Courtney et al. 1995). This thesis has made some progress in pin-pointing the temporal and spatial variability in abundance, reproductive development and spawning of M. bennettae in NSW, as well as identifying some of the significant environmental drivers of these patterns. However, these patterns need to be monitored over longer periods of time and across a range of different estuaries to determine if the findings reported here are geographically and temporally consistent. This study forms the necessary foundations for a broader, state-wide assessment of M. bennettae and with the increasing shift from single target species fisheries management to EBFM, results from this thesis will make a valuable contribution to the management of the whole estuarine ecosystem.

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