Pomatomus Saltatrix, in Eastern Australia

Ecology of tailor, Pomatomus saltatrix, in eastern Australia

Hayden Thomas Schilling

A thesis submitted in fulfilment of the requirements for the degree of

Doctor of Philosophy

School of Biological, Earth and Environmental Sciences

Faculty of Science

University of New South Wales, Australia

December 2019

Thesis/Dissertation Sheet

Surname/Family Name : Schilling Given Name/s : Hayden Thomas Abbreviation for degree as give in the University : PhD calendar Faculty : Faculty of Science School : School of Biological, Earth and Environmental Sciences Thesis Title : Ecology of tailor, Pomatomus saltatrix, in eastern Australia

Abstract (350 words maximum): Pomatomus saltatrix is a highly popular and heavily fished globally distributed mesopredatory fish known by a variety of common names (tailor, bluefish, elf, enchova and shad). The southwest Pacific (eastern Australian) population of P. saltatrix has been the subject of anecdotal declines in size, abundance and catch rates. Despite this there is a lack of ecological knowledge for this population. The aim of this research is to increase knowledge of the understudied southwest Pacific Ocean population of P. saltatrix. Samples were collected over 3 years from commercial and recreational fishing sectors.

P. saltatrix in the southwest Pacific displayed fast, almost linear early growth with no visible asymptotic length. The Schnute growth equation provided the best fit and yielded parameter values of a = 0, b = 2.49, size at age 1 = 25.46 cm fork length (FL) and size at age 4 = 46.34 cm FL. The instantaneous total mortality rate (Z) was estimated to be 1.62 and the instantaneous natural mortality rate (M) was estimated to be 0.82.

We explored the dietary variation using a classification tree analysis. Body size and latitude had the greatest influence on the diet of P. saltatrix, with significant diet shifts occurring at 8 and 30 cm FL. The importance of latitude was likely related to the East Australian Current and its separation from the continental shelf.

We used otolith chemistry to evaluate the use of estuarine and marine environments by juvenile P. saltatrix. It was found that 24 – 52% of adult P. saltatrix had a juvenile period characterised by the marine environment. This suggests that P. saltatrix show considerable plasticity in juvenile habitat use.

It was found that P. saltatrix have asynchronous oocyte development and may spawn multiple times during two distinct spawning events. The late summer spawning event in northern NSW was shown to be highly important for larval transport to the southern portion of the species distribution.

P. saltatrix in the southwest Pacific show a life history pattern generally consistent with most other global populations of P. saltatrix except the northwest and east Atlantic populations.

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Hayden Schilling

Abstract

Pomatomus saltatrix is a globally distributed pelagic mesopredator which is exploited heavily throughout its range. Despite the implementation of strict management strategies, the southwest Pacific Ocean (eastern Australian) population has limited published information about the life history of this important fishing species. This thesis has 4 main chapters which investigate growth and mortality, diet, juvenile habitat use and the reproductive biology of the southwest Pacific Ocean population of P. saltatrix, locally known as tailor.

By validating a whole otolith ageing technique and using a model selection process with 8 candidate growth models, I showed that the Schnute growth equation provided the best fit and yielded parameter values of a = 0, b = 2.49, size at age 1 = 25.46 cm fork length (FL) and size at age 4 = 46.34 cm FL. P. saltatrix in the southwest Pacific had a similar growth rate to other global populations, with the exception of the northwest Atlantic population which shows a considerably faster growth rate. Using a length frequency representative of harvested P. saltatrix and a catch curve analysis, instantaneous total mortality rate (Z) for the southwest Pacific population was estimated to be 1.62. Comparison with other global populations showed the northwest Atlantic population to have both the lowest natural mortality (M) and Z, together with the largest maximum biological age (14 y). All other populations were similar with higher mortality and maximum ages of 6 – 10 years. Z was driven largely by M for most populations, although fishing mortality (F) was highest in the east Indian and southwest Pacific populations.

The dietary niche of P. saltatrix in eastern Australia was explored using a classification tree analysis to identify key factors driving diet variation. P. saltatrix was shown to be an opportunistic generalist predator which exhibited increased baitfish consumption, and decreased crustacean consumption, with increasing size. The classification tree analysis showed that body size and latitude had the greatest influence on the diet of P. saltatrix, with significant ontogenetic diet shifts occurring at 8 and 30 cm fork length (FL). While piscivory is evident in the majority of P. saltatrix diets by ~8 cm FL, crustaceans are almost entirely absent from the diet after ~30 cm FL. The importance of latitude was likely related to the broad-scale oceanography in the study region, including the East Australian Current and its separation from the continental shelf.

Otolith chemistry was used to evaluate the use of estuaries and the coastal marine environment by juvenile P. saltatrix in eastern Australia. Otolith chemical signatures of juveniles from 12 estuaries, spanning 10° of latitude, were characterised using laser ablation- inductively coupled plasma-mass spectrometry. Based upon multivariate otolith elemental signatures, fish collected from most estuaries could not be discriminated from one another. This was attributed to the varying influence of marine water on otolith elemental composition in fish from all estuaries. Using a reduced number of estuarine groups, the multivariate juvenile otolith elemental signatures and univariate Sr:Ca ratio suggest that between 24 and 52 % of adult P. saltatrix had a juvenile period influenced by the marine environment. Elemental profiles across adult (age-1) otoliths highlighted a variety of life history patterns, not all consistent with a juvenile estuarine phase. Furthermore, the presence of age-0 juveniles in coastal waters was confirmed from historical coastal trawl data. Combining multiple lines of evidence suggests considerable plasticity in juvenile life history for P. saltatrix in eastern Australia, through their utilisation of both estuarine and coastal nurseries.

A reproductive biology survey across the whole population and an analysis of historical larval fish abundance, found a second distinct spawning period in late summer in NSW in addition to the recognised spring spawning in QLD. Ovaries displayed asynchronous oocyte development suggesting fish spawn multiple times per season. Fecundity showed an exponential relationship with fish length with estimates of batch fecundity ranging from 99,488 to 1,424,425 eggs per fish. When combined with a length frequency of the population, the majority of eggs were produced by fish < 40 cm fork length. Length at 50 % maturity (L50) was estimated at 30.2 and 31.5 cm FL for male and female tailor respectively, suggesting that raising the NSW minimum legal length (MLL) from 30 cm total length TL to 35 cm TL to match the QLD MLL could significantly improve recruitment. The sex ratio was found to have shifted in the last 40 years to a female dominated population (1.58 females :1 male). An oceanographic particle tracking model revealed that larvae from the different spawning events are dispersed differently, with the late summer spawning period supplying the most recruits to the southern portions of the species distribution, suggesting that the multiple spawning periods have developed as a result of selection over time as surviving larvae from the different spawning periods are transported differently by the ocean currents.

P. saltatrix in the southwest Pacific (eastern Australia) show a life history pattern generally consistent with most other global populations of P. saltatrix except the northwest Atlantic population which grows larger, older and matures later.

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Acknowledgements

I would like to thank my wonderful team of supervisors Iain Suthers, John Stewart, Julian Hughes, Jason Everett and James Smith for supporting me the whole way though. Everyone in the FAMER lab at UNSW and DPI Fisheries at SIMS always made me feel welcome and were always happy to have a chat or help me.

I am so grateful for the experience I gained in so many things over the last few years. Thanks to Iain for the experience I gained onboard the RV Investigator despite the 4 voyages not being related to my project. Thanks to DPI for the chance to see the non-academic side of research and help with a variety of research from measuring fish in the middle of the night at the fish markets to tagging bull sharks in Sydney Harbour.

Thanks Bronwyn Gillanders and Patrick Reis-Santos for all your help and support with the otolith chemistry work. Many volunteers helped with my fieldwork for which I am grateful, especially Matthew Hyatt, Chris Stanley and Chris Setio for road tripping it and helping catch baby tailor up and down the NSW coast. The northern NSW would have been very lacking without the help of Ben van der Woude who sampled northern NSW regularly for this research. Extending the research into Queensland wouldn’t have been possible without the support of Lenore Litherland from QLD Department of Fisheries and Agriculture. Your assistance with sampling and training on how to read tailor otoliths was very appreciated.

Thanks Mum and Dad for all your support. I really do appreciate it.

Thanks Alex for all your help in so many ways, from catching lots of fish to always giving me a reason to smile.

This work was funded by an Australian Research Council Linkage Project (LP150100923), NSW Department of Primary Industries and the NSW Recreational Fishing Trust. I was supported by an Australian government Research Training Program Scholarship. Hornsby Shire Council and an Ecological Society of Australian student research award also supported fieldwork. Thanks to the Australian Society of Fish Biology for supporting me in attending multiple conferences with student travel awards.

This research includes computations using the Linux computational cluster Katana supported by the Faculty of Science, UNSW Australia. Thank you to UNSW Stats Central for helping with the growth models, Jim Craig (NSW DPI) for converting the QLD length frequencies from total length to fork length, Petra Kuhnert (CSIRO) for providing the R ‘diet’ package used in Chapter 3 and Moninya Roughan and Colette Kelly for providing the ROMS model used in Chapter 5.

All the research in this thesis was approved by the NSW Department of Primary Industries Fisheries Ethics Committee (ACEC# 14/14) and fish were collected under a NSW DPI Scientific Collection Permit (P03/0086(F)-8.1).

I would like to dedicate this thesis to my grandfather Donald Brander who passed away while I was away on the RV Investigator in 2015. I hope that the research in this thesis will have an impact and help ensure that tailor continues to be an important recreational fishery in Australia.

Table of Contents Abstract ...... i

Acknowledgements ...... iv

List of figures ...... xi

List of tables ...... xiv

1 General Introduction ...... 1

1.1 Ecology of Pelagic Mesopredators ...... 1

1.2 Pomatomus saltatrix – A Global Mesopredator ...... 5

1.3 Pomatomus saltatrix in Australia ...... 6

1.4 Thesis Aim ...... 12

1.5 Thesis Chapters ...... 13

2 Growth and mortality of Pomatomus saltatrix in the southwest Pacific Ocean (eastern Australia), with a global review ...... 15

2.1 Abstract ...... 15

2.2 Introduction ...... 16

2.3 Methods ...... 20

2.3.1 Fish Collection ...... 20

2.3.2 Comparison Between Whole and Sectioned Otoliths ...... 21

2.3.3 Age and Growth Rate Determination ...... 22

2.3.4 Natural Mortality Estimation ...... 25

2.3.5 Total Mortality Estimation from Length and Age Compositions ...... 25

2.3.6 Global Life History Comparison...... 28

2.3.7 An Individual Outlier ...... 29

2.4 Results ...... 30

2.4.1 Morphometric Relationships ...... 30

2.4.2 Comparison Between Whole and Sectioned Otoliths ...... 30

2.4.3 Growth Modelling ...... 32

2.4.4 Age Structure and Mortality Estimations ...... 35

2.4.5 Global Life History Comparison...... 36

2.5 Discussion ...... 40

2.5.1 Age Determination and Growth Rates ...... 40

2.5.2 Mortality ...... 44

2.5.3 Concluding Remarks ...... 47

3 Latitudinal and ontogenetic variation in the diet of a pelagic mesopredator (Pomatomus saltatrix), assessed with a classification tree analysis ...... 48

3.1 Abstract ...... 48

3.2 Introduction ...... 49

3.3 Materials and Methods ...... 51

3.3.1 Sample Collection and Processing ...... 51

3.3.2 Diet Analysis ...... 51

3.4 Results ...... 53

3.4.1 Classification Tree ...... 53

3.4.2 Predator Prey Size ...... 57

3.5 Discussion ...... 58

3.5.1 Ontogenetic Diet Patterns ...... 58

3.5.2 Latitudinal Variation ...... 59

3.5.3 Feeding Strategy ...... 60

3.5.4 Classification Tree Framework ...... 62

3.5.5 Conclusion ...... 63

4 Evaluating estuarine nursery use and life history patterns of Pomatomus saltatrix in eastern Australia ...... 64

4.1 Abstract ...... 64

4.2 Introduction ...... 65

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4.3 Methods ...... 67

4.3.1 Fish Collection ...... 67

4.3.2 Otolith Element Analysis ...... 69

4.3.3 Statistical Analysis ...... 70

4.3.4 Historical Offshore Length Frequency Analysis ...... 72

4.4 Results ...... 73

4.4.1 Juvenile Estuarine Elemental Signatures ...... 73

4.4.2 Juvenile Life Period Chemical Signatures from Adult Otoliths ...... 76

4.4.3 Otolith Elemental Profiles ...... 78

4.4.4 Historical Coastal Trawl Data ...... 79

4.5 Discussion ...... 80

4.5.1 Juvenile Otolith Chemistry Differences ...... 80

4.5.2 Assigning Adults to Estuaries ...... 82

4.5.3 Elemental Profiles ...... 83

4.5.4 Conclusion ...... 85

5 Resolving patterns of spawning in tailor (Pomatomus saltatrix) and the implications for connectivity ...... 86

5.1 Abstract ...... 86

5.2 Introduction ...... 87

5.3 Methods ...... 91

5.3.1 Fish Sampling ...... 91

5.3.2 Sex Ratio ...... 91

5.3.3 Fecundity ...... 92

5.3.4 Maturity ...... 93

5.3.5 Historical Larval Fish Surveys ...... 94

5.3.6 Drivers and Patterns of GSI ...... 94

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5.3.7 Particle Tracking ...... 96

5.4 Results ...... 99

5.4.1 Sex Ratio ...... 99

5.4.2 Fecundity ...... 99

5.4.3 Egg Size Distributions ...... 100

5.4.4 Maturity ...... 101

5.4.5 Larval Fish Distribution and Abundance ...... 103

5.4.6 Patterns of GSI ...... 104

5.4.7 Drivers of GSI ...... 105

5.4.8 Larval Dispersal ...... 105

5.5 Discussion ...... 109

5.5.1 Maturity ...... 109

5.5.2 Fecundity ...... 111

5.5.3 Sex Ratio ...... 112

5.5.4 Patterns and Drivers of GSI ...... 114

5.5.5 Larval Dispersal ...... 115

5.5.6 Conclusion ...... 117

6 General Discussion ...... 118

6.1 Life History Model for Tailor, Pomatomus saltatrix, in Eastern Australia ...... 118

6.1.1 Annual Migration and Spawning ...... 118

6.1.2 Larval Dispersal and Recruitment ...... 119

6.1.3 Juvenile Phase ...... 120

6.1.4 Maturity and Entrance to the Fishery ...... 121

6.1.5 Mortality and Age Structure ...... 121

6.2 Comparison with Other Local Mesopredators ...... 122

6.3 Comparison to Other Pomatomus saltatrix Populations ...... 124

6.4 Future Research ...... 125

6.5 Concluding Remarks ...... 127

7 Literature Cited ...... 128

8 Appendices ...... 149

8.1 Supplementary Material for Chapter 1 ...... 149

8.2 Supplementary Material for Chapter 2 ...... 151

8.3 Supplementary Material for Chapter 3 ...... 163

8.4 Supplementary Material for Chapter 4 ...... 166

8.5 Supplementary Material for Chapter 5 ...... 171

List of figures

Figure 1.1 Auximetric plot showing a comparison of the Brody growth constant “K” and asymptotic length (L∞) from von bertalanffy growth equations...... 3

Figure 1.2 A comparison of von Bertalanffy growth curves for a variety of pelagic mesopredators, highlighting the variability in life history displayed by this functional group.. .. 4

Figure 1.3 Distribution of Pomatomus saltatrix in the southwest Pacific Ocean (eastern Australia)...... 9

Figure 1.4 Fishers targeting tailor, Pomatomus saltatrix, at Fraser Island during the annual spawning aggregations...... 10

Figure 1.5 Average predicted relative density of tailor along the east coast of Australia (0–200 m bathymetry) during spring (blue line); summer (red line); autumn (orange line); and winter (green line)...... 11

Figure 2.1 Global distribution of Pomatomus saltatrix (in black) overlaid on the average annual sea surface temperature...... 16

Figure 2.3 Validation of annual increment formation for Pomatomus saltatrix in eastern Australia showing: a) the marginal increment ratio for fish with 1 visible increment, b) the edge type of the otolith for otoliths with 1 and 2 visible increments, c) the marginal increment ratio for fish with 2 visible increments, and d) the thickness of otolith translucent edges for otoliths with 1 and 2 visible increments...... 32

Figure 2.4 Size at age (biological age) for Pomatomus saltatrix in the southwest Pacific population (eastern Australia; n = 3,390)...... 33

Figure 2.5 Size at age for juvenile Pomatomus saltatrix, which were aged using daily increments with a logistic growth curve (n = 61)...... 35

Figure 2.6 Representative length composition of harvested Pomatomus saltatrix in eastern Australia...... 36

Figure 2.7 Comparison of the growth curves of different population of Pomatomus saltatrix around the world (Table 2.4)...... 37

Figure 2.8 Visual representation of the growth rates of each population up to age 5...... 38

Figure 3.1 The 1 standard error classification tree for Pomatomus saltatrix diet composition, yielding a cross-validated error rate of 0.746 (SE = 0.036)...... 54

Figure 3.2 Terminal node bootstrapped predictions and the 95 % bootstrap percentile intervals for the pruned classification tree...... 55

Figure 3.3 Proportion (by dry weight) of prey groups by predator size...... 56

Figure 3.4 Quantile regression scatterplots showing prey size (Standard or Carapace length) against predator fork length...... 57

Figure 4.1 Map of location of the estuaries where juvenile Pomatomus saltatrix were collected...... 68

Figure 4.2 Element:Ca ratios (mean ± 1 standard error) from a spot analysis at the edge of otoliths from juvenile (Age-0) Pomatomus saltatrix collected in different estuaries...... 74

Figure 4.3 A visual representation of the continuum of Sr:Ca (mmol mol-1) values observed in the spot analyses of the juvenile section from adult otoliths...... 77

Figure 4.4 Examples of profiles of Sr:Ca and Ba:Ca from 1 year old Pomatomus saltatrix from the core to the edge of otoliths showing different life history patterns...... 78

Figure 5.1 Map of eastern Australia showing zones where Pomatomus saltatrix were collected for analysis of reproductive biology...... 90

Figure 5.2 Relationship between batch fecundity (±SE) and fork length for female Pomatomus saltatrix...... 99

Figure 5.3 Proportion of total egg production by fork length for female Pomatomus saltatrix in eastern Australia...... 100

Figure 5.4 Proportion of mature Pomatomus saltatrix by fork length. The red points and curve represents females and the blue points and curve represents males...... 101

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Figure 5.6 Mean female gonad index by zones for Pomatomus saltatrix...... 104

Figure 5.7 Density of particles at settlement time (500 degree days) in 1 degree bins...... 106

Figure 5.8 Percentage of settled larvae on the continental shelf (location <200m depth at 500 degree days) originating from each of the modelled spawning events...... 108

Figure 6.1 A summary of movement for all tagged Pomatomus saltatrix (tailor) in eastern Australia...... 119

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List of tables

Table 2.1 Collection information for the two otolith datasets used to estimate the age of Pomatomus saltatrix in eastern Australia...... 20

Table 2.2 Sample sizes of the datasets used to generate length frequency distributions for Pomatomus saltatrix in eastern Australia...... 26

Table 2.3 Results of the precision and bias comparisons within and between otolith preparation methods using 71 otoliths from the NSW dataset...... 31

Table 2.4 Summary of published life history parameters for global populations of Pomatomus saltatrix...... 39

Table 3.1 Summary of the fish length and latitudinal patterns in Pomatomus saltatrix diet composition identified as terminal nodes in the classification tree...... 55

Table 3.2 Quantile regression parameters, standard errors and P values for the test H0 = 0, relating prey lengths to Pomatomus saltatrix length...... 57

Table 4.1 Summary of PERMANOVA results for the multivariate analysis of edge otolith elemental compositions of juvenile Pomatomus saltatrix collected in different estuaries...... 73

Table 4.2 Summary of total correct cross-validated individuals of juvenile Pomatomus saltatrix classified back to the estuary in which they were caught, based upon otolith elemental chemistry and CAP analysis (Canonical analysis of principal coordinates)...... 75

Table 5.1 Length at 50% maturity estimates for each sex...... 102

Table 5.2 Percentage of particles settling on the continental shelf in each degree of latitude from the various spawning events...... 107

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1 General Introduction

1.1 Ecology of Pelagic Mesopredators

Pelagic mesopredators are fish and small sharks between 40 cm and 1.5 m in length (Forcada et al. 2009, Reum and Essington 2013, Hughes et al. 2014), which prey upon forage fish such as sardine, anchovy and jack mackerel and are themselves prey for large sharks and marine mammals. Mesopredators are essential components of ecosystems. By predating on lower trophic levels they often exert control over prey species populations while in turn providing biomass to the higher apex predators (large fish/sharks and marine mammals). Apex predators can heavily influence whole ecosystems and their over-harvest can release mesopredators from predation control, which in turn consume large numbers of lower trophic level species (Prugh et al. 2009, Ellingsen et al. 2015). This has been observed in both terrestrial and aquatic ecosystems with a range of trophic cascades being documented following the release of mesopredators (Ritchie and Johnson 2009, Newsome et al. 2017). Although the ecological role of mesopredators is increasingly being recognised in terrestrial ecosystems (Gordon et al. 2015, Newsome and Ripple 2015, Gordon et al. 2017), the role of pelagic mesopredators remain relatively unacknowledged. In pelagic ecosystems, ontogenetic diet shifts are common and mesopredators are best described by size rather than species (Heupel et al. 2014), Brodie et al. (2018).

Pelagic and benthopelagic mesopredators are the second largest harvested functional group in our oceans (after medium sized demersal/benthic fish), accounting for one third of global landings (34% by tonnage; Zeller and Pauly 2015). Despite this large impact, ecological knowledge of pelagic mesopredators is often limited to highly important fisheries (such as tuna; Murua et al. 2017) or to age and growth of some minor commercially important species (Hughes et al. 2008, Stewart et al. 2013). Ecological knowledge is often lacking for the recreationally important and minor commercial species (Adams et al. 2014). This is due to a combination of the difficulty in sampling these species due to large home ranges and often migratory behaviour and the high diversity within the mesopredator group (Post 2013). While there are relatively few forage fish species in each region, there is often a large diversity of mesopredators which all share the forage fish resources (Bakun 2006), this results in many mesopredator species with little species-specific ecological knowledge.

In addition to their value as harvested species, mesopredators often have large impacts with Consumption:Biomass ratios (Q:B) of 4 – 10 meaning they consume 4 – 10x their own body weight per year (Griffiths et al. 2010, Hughes et al. 2014), with small tuna having a Q:B ratio up to 20 (Essington 2003). Juveniles also have greater consumption than adults of the same species with up to 4 times higher Q/B ratios (Lawson et al. 2018). Coupled with their greater abundance, juvenile pelagic mesopredators form an important yet relatively unknown part of many ecosystems.

Pelagic mesopredators exhibit a range of life history patterns and this is best shown using growth as an example. Auximetric plots are double logarithmic plots of the Brody growth coefficient K and the asymptotic length L∞ from von Bertalanffy growth equations (Pauly 1979, Murua et al. 2017). These plots can be used to visualise different growth strategies and show the variation in K (growth rate) at a given body size as well as the inverse relationship between

K and L∞. A large K would reach its asymptotic length faster than a species with a similar asymptotic length with a small K value. Using the r package “rfishbase” (Boettiger et al. 2012) it is possible to extract K and L∞ growth parameters from FishBase (Froese and Pauly 2018) for all species (n = 33,538). I have extracted this data and selected only pelagic mesopredators by sub-setting all species to select only those with a habitat classified as “pelagic”, a predatory diet and a asymptotic size of between 30 and 150 cm (n = 241). The resulting plot shows that K for pelagic mesopredators varies by more than an order of magnitude at any size and only shows a weak relationship to asymptotic length (Figure 1.1). This is highly significant as it shows that at any given size, pelagic mesopredators can have vastly different growth rates and life history strategies.

To highlight this large variation displayed by pelagic mesopredators in terms of K and L∞ I have selected a few example species. Figure 1.1 highlights the range of K and L∞ within pelagic mesopredator with the resulting growth curves for some example species shown in Figure 1.2. Coryphaena hippurus which displays the fastest growth pattern of any pelagic mesopredator, maturing in the 1st year and rarely living more than 3 years (Schwenke and Buckel 2008). Seriola lalandi also has a high growth rate but does survive to older ages (Gillanders et al. 1999). On the other hand, Brama Brama grows steadily, almost linearly with little reduction in growth rates and can live more than 10 years (Lobo and Erzini 2001). Other fish such as Arripis trutta and Pomatomus saltatrix have a smaller maximum length and are typically associated with coastal beach habitats (Robillard et al. 2009, Hughes et al. 2017).

Figure 1.1 Auximetric plot showing a comparison of the Brody growth constant “K” and asymptotic length (L∞) from von bertalanffy growth equations. Using data from FishBase (Froese and Pauly 2018) extracted using the R package “rfishbase” (Boettiger et al. 2012). Red dots are pelagic mesopredators (n = 241) and grey dots are all species (n = 33,538) in fishbase. Pelagic mesopredators were defined as fish with L∞ between 30 and 150 cm, from a pelagic habitat and with a predatory diet. Note the log10 scale on both axes. The growth curves of the highlighted species are shown in Figure 1.2 as a further example of the variety evident in the life history patterns within the pelagic mesopredator guild.

Figure 1.2 A comparison of von Bertalanffy growth curves for a variety of pelagic mesopredators, highlighting the variability in life history displayed by this functional group. The same species are identified in Figure 1.1 for comparison. The x-axis (Age) was truncated for each species at 13 or the oldest reported fish in the cited literature (whichever was earlier). Data sources are as follows: Arripis trutta (Australian Salmon) from Hughes et al. (2017), Coryphaena hippurus (Dolphinfish) from Schwenke and Buckel (2008), Brama brama (Ray’s bream) from (Lobo and Erzini 2001), Pomatomus saltatrix (bluefish) from Robillard et al. (2009) and Seriola lalandi from Gillanders et al. (1999).

While pelagic mesopredators display a variety of life histories as highlighted above, they often fill a functionally similar niche with high consumption of baitfish (Lawson et al. 2018), creating intense top-down pressure on lower trophic levels (Hughes et al. 2014). For example on the east coast of the USA, bluefish Pomatomus saltatrix has the potential to account for all the natural mortality of juvenile striped bass Morone saxatilis (Buckel et al. 1999). By focusing on individual species and understanding the trophic demand and how it is related to life history, broader findings about mesopredators and their impact and role in ecosystems can be made.

1.2 Pomatomus saltatrix – A Global Mesopredator

Pomatomus saltatrix is one of few globally distributed pelagic mesopredators. Taxonomically, it is the sole species within the family Pomatomidae and has a worldwide distribution. It is found in the Indian, Atlantic and Pacific Oceans and the Mediterranean Sea (Juanes et al. 1996). Despite supporting only a minor commercial catch (~20,000 t global catch; FAO 2017), it is a popular sportfish in many regions and forms the basis of artisanal fisheries in south America, Africa and the Mediterranean region. The populations of P. saltatrix experience different levels of fishing pressure which fish in the Mediterranean being heavily exploited, with the species rarely observed with a total length larger than 30 cm (Ceyhan et al. 2007). This is contrasted by the northwest Atlantic population where it is subject to lower fishing pressure and is regularly observed larger than 60 cm total length (Robillard et al. 2009). The worldwide exploitation of this species highlights the importance of understanding the biology of this species.

P. saltatrix is known by various common names across the seven main populations of the species (Briggs 1960, Juanes et al. 1996). These names are bluefish (northwest Atlantic and Mediterranean), tassergal (east Atlantic), enchova (southwest Atlantic), shad or elf (west Indian) and tailor (east Indian and southwest Pacific; Figure 2.1). Although there is some limited genetic transfer between the northern hemisphere populations (Miralles et al. 2014a), they are genetically distinct populations (Goodbred and Graves 1996) which shared a common ancestor approximately 50,000 years ago (Miralles et al. 2014b). The general life history of all seven populations is largely consistent although, both similarities and differences in life history traits are evident between the seven populations. P. saltatrix in all populations undergo annual coastal migrations to spawning areas (either one or two spawning areas) from which larvae are distributed by coastal boundary currents. It is currently believed that larvae recruit to both estuarine and coastal habitats in all populations except the eastern Pacific (Juanes et al. 1996). In the northwest Atlantic and west Indian Oceans, juveniles prey upon small crustaceans and fish while the adults are aggressive piscivores (van der Elst 1976, Buckel et al. 1999, Lucena et al. 2000).

The northwest Atlantic population appears to have a different life history to all the other populations which show similar patterns of age, mortality and reproduction. Fish from the northwest Atlantic population are regularly caught at sizes up to 90 cm TL (Robillard et al. 2009), while fish from southern hemisphere populations are rarely caught larger than 60 cm TL

(Leigh et al. 2017). As a further contrast, P. saltatrix from the Mediterranean are rarely caught above 30 cm TL due to intense overfishing in the Mediterranean (Ceyhan et al. 2007). The northwest Atlantic population also matures at ~45cm TL (Robillard et al. 2008), compared to ~25 cm FL in most other populations (van der Elst 1976, Bade 1977, Ceyhan et al. 2007). While this has not been shown conclusively, this may reflect the lower fishing pressure resulting in higher proportions of larger, older fish in the northwest Atlantic population, allowing them to delay investment in reproduction. Differences in reproduction appear to exist between populations with some debate over spawning patterns (Juanes et al. 1996, Miskiewicz et al. 1996, Robillard et al. 2008). It is thought that, although most populations show two cohorts of recruitment, there is a single protracted spawning period during which the populations are migrating (Robillard et al. 2008). This results in variable recruitment and may result in the appearance of two size cohorts which has been observed in most populations (Ward and Staunton-Smith 2002, Callihan et al. 2008, Robillard et al. 2008).

1.3 Pomatomus saltatrix in Australia

Pomatomus saltatrix is found along both the east coast (southwest Pacific Ocean) and west coast (eastern Indian Ocean) of Australia south of approximated 24°S. It is a highly popular recreational fishery, mainly targeted by shore-based fishers (Leigh et al. 2017). While the two populations are genetically distinct and are not thought to mix (Nurthen et al. 1992, Goodbred and Graves 1996), P. saltatrix has recently been observed in both South Australian and Tasmanian waters (Atlas of Living Australia 2018), suggesting that one or both of the populations are expanding south and the eastern Indian and western Pacific Ocean populations may one day have overlapping distributions in southern Australia.

This expanding southern distribution of both Australian populations is due to climate warming. Both the southeast and southwest of Australia has been identified as global change hotspots in terms of marine warming (Hobday and Pecl 2014). The strengthening East Australian Current (EAC; Ridgway 2007) in particular is facilitating poleward movement of many species, particularly small fish and their pelagic mesopredators (Champion et al. 2018). The rapid and numerous changes which are being caused by tropicalisation cannot be accurately quantified if we do not understand the ecology of the species which are already present in temperature latitudes.

While neither the eastern Indian or southwest Pacific Ocean populations of P. saltatrix have been subject to the intense study of the northwest Atlantic population, the ecology of the east Indian population has been studied more than the southwest Pacific Ocean population. In the east Indian population, P. saltatrix is mainly targeted by commercial fishers in the northern part of the distribution and recreational fishers in the southern portion of the population (Smith et al. 2013). This stock grows relatively fast, attaining sexual maturity in their second year at approximately 320 mm total length (Smith et al. 2013). Although there are multiple sub-populations within the eastern Indian Ocean population there is evidence of some mixing and fish from all sub-populations exhibit northward migratory behaviour during winter (Lenanton et al. 1996, Edmonds et al. 1999, Young et al. 1999). Spawning occurs on inner shelf waters between spring and autumn with eggs and larvae being transported northwards via coastal ocean currents, particularly the Capes Current which is particularly strong during the spawning season (Lenanton et al. 1996). Juveniles are found in both estuarine and coastal habitats and rarely move more than 25 km and generally remain in sheltered waters (Young et al. 1999). The overall life history is generally consistent with populations of P. saltatrix around the world.

The southwest Pacific population is found along the eastern coast of Australia, most commonly north of 36°S but the full distribution ranges from Fraser Island in the north (24°S) down to Victoria in the south (38°S) with occasional occurrences in Tasmania (42°S; Figure 1.3). Prior to this current study, most ecological knowledge of P. saltatrix from the southwest Pacific (eastern Australia) is from a single MSc thesis from 4 decades ago, focused on the northern part of the distribution (north of 28.5°S; Bade 1977), plus some studies focused on the northern annual spawning aggregations off Fraser Island. These studies included a tagging study of estuarine juveniles in the north which showed estuarine residency as juveniles (Morton et al. 1993) and two descriptions of the fishery in the north of the species range (Pollock 1984, Zeller et al. 1996). Two further studies examined egg and larval distributions in order to inform spawning and recruitment (Miskiewicz et al. 1996, Ward et al. 2003), and a genetics study used enzyme loci to identify that the southwest Pacific population consists of a single stock and is distinct from the east Indian ocean population off Western Australia (Nurthen et al. 1992). The genetic separation between the eastern Indian (western Australian) and southwest Pacific (eastern Australian) populations was later confirmed by a more extensive survey of genetics from different populations of P. saltatrix which used restriction fragment length polymorphism analysis of mitochondrial DNA (Goodbred and Graves 1996).

Like the other populations of P. saltatrix around the world, the southwest Pacific population has anecdotal reports of declines in size, abundance and catch rates in recent decades. This was linked to large numbers of fishers targeting the annual spawning migration (Leigh and O'Neill 2004; Figure 1.4). This has resulted multiple stock assessments and changes in the management of the fishery, particularly in terms of the introduction of a minimum legal length, bag limits and gear restrictions (Leigh and O'Neill 2004, Leigh et al. 2017). Full details of managements changes can be seen in Supplementary Table 8.1.1.

The original MSc thesis by Bade (1977) focused upon the northern portion of the distribution and made several broad findings. It was found that length at sexual maturity was between 26 and 28 cm fork length, the species is primarily a piscivorous predator which preys upon a wide variety of fish species. The primary spawning season was of long duration with a peak in September and October with a possible indication of a secondary spawning event in late summer. Larvae in eastern Australia are thought to be dispersed south by the East Australian Current (Miskiewicz et al. 1996). Oocyte development was consistent with more than one spawning event per season. Following the work of Bade (1977), further research is needed as the original study was largely biased towards the northern portion of the distribution and used relatively small sample sizes. Specific gaps of knowledge for this population of P. saltatrix include the growth rate, dietary variation, juvenile habitat use (the western Pacific populations is the only population of the species thought to be restricted to estuarine habitats as juveniles) and there is currently debate around two recruitment peaks resulting either from an extended spawning period or two distinct spawning periods (Miskiewicz et al. 1996, Ward et al. 2003).

Figure 1.3 Distribution of Pomatomus saltatrix in the southwest Pacific Ocean (eastern Australia). The thick dark lines shows the latitudinal range of the population. It is mostly resticted to shallow coastal waters within this region. Fraser Island in the north is a known annual spawning site which is targetted heavily by fishers.

Figure 1.4 Fishers targeting tailor, Pomatomus saltatrix, at Fraser Island during the annual spawning aggregations. Image from QLD Department of Fisheries and Agriculture.

As concurrent research to the work presented in the current thesis, two other studies on southwest Pacific P. saltatrix were conducted. The first study compiled 40 years of citizen science tagging programs (managed by state fisheries departments) in order to describe the migratory behaviour of the southwest Pacific population (Brodie et al. 2018). Using a point process model framework, implemented using generalised additive mixed models, environmental variables including sea surface temperature (SST) and sea level anomaly were correlated with presence of P. saltatrix. It was found that P. saltatrix abundance has a non- linear response to SST with abundance peaking at 21.5°C (Brodie et al. 2018). Using these modelled drivers of P. saltatrix abundance, it was possible to predict the seasonal abundance of P. saltatrix along the whole latitudinal distribution (Figure 1.5). From the recapture data, it was also evident that there is complexity within the movement patterns with highly variables movements distances observed between fish and limited southern dispersal, even after the annual spawning event in the north (Brodie et al. 2018).

The second concurrent study on the western Pacific population of P. saltatrix was a bioenergetics study which measured oxygen consumption at various temperatures (18 – 30°C) and body sizes (18 – 1035 g) to determine mass and temperature specific resting metabolic rate (gO2 g−1 d−1; Lawson et al. 2018). It was found that juvenile P. saltatrix consume 5.7% of their body weight daily (or an annual Q:B of 20.6). This declines with size to 2.1 % body weight daily (or a Q:B of 7.7). This finding highlights the important predatory impact that P. saltatrix can have upon other species in the environment and aligns with findings in the northwest Atlantic population which estimated that consumption juvenile P. saltatrix can account for up to 24% of the mortality of the bay anchovy (Buckel et al. 1999). Bioenergetics modelling of P. saltatrix also highlighted the need for detailed dietary information when estimating consumption as estimates can be inaccurate if they do not include variation such as ontogeny of diet and a variety of prey taxa (Lawson et al. 2018).

24°S

26°S

28°S

30°S

Latitude 32°S

34°S

36°S

0.0 0.001 0.002 0.003 0.004 0.005 0.006 -2 Relative Density (fish km ) Figure 1.5 Average predicted relative density of tailor along the east coast of Australia (0–200 m bathymetry) during spring (blue line); summer (red line); autumn (orange line); and winter (green line). Predictions for tailor were made using the temporally constrained model with SST averaged for each season (1985–1991) and latitude. Reproduced from Brodie et al. (2018) with permission.

Combining the threats from climate change with the increasing anthropogenic threat from a growing coastal population (Smith et al. 2008), and the popularity of mesopredators as fished species (although this may be declining in eastern Australia; Leigh et al. 2017), understanding the ecology of this region, in particular the mesopredators, is critical if they are to be effectively managed in the future. These reasons highlight the need for a detailed study on the ecology of P. saltatrix in southeast Australia.

1.4 Thesis Aim

The overall aim of this thesis was to investigate and quantify the life history of the important pelagic mesopredator, Pomatomus saltatrix, in eastern Australia, where it is exploited both commercially and recreationally despite a lack of species-specific ecological knowledge.

Specifically, I aim to:

1) Quantify the growth and mortality of P. saltatrix in the southwest Pacific Ocean (eastern Australia) population and compare to other global populations, 2) Investigate seasonal, latitudinal and ontogenetic variation in the diet of P. saltatrix in the southwest Pacific Ocean (eastern Australia), 3) Test the hypothesis of exclusive estuarine habitat use by juvenile P. saltatrix in the southwest Pacific Ocean (eastern Australia) which contrasts all other global populations of the species, and 4) Investigate the reproductive biology of P. saltatrix in the southwest Pacific Ocean (eastern Australia) and evaluate the current protection of this species.

These aims will contribute to the sustainable management of this popular exploited species by providing quantitative assessments life history stages and providing essential species-specific knowledge which will inform future stock assessments. Parts of this thesis also contributed to studies on the consumption rates and migration of this population which were described in section 1.3 (Brodie et al. 2018, Lawson et al. 2018).

1.5 Thesis Chapters

In chapter 2, I validate a method to estimate age and model the growth of P. saltatrix in eastern Australia using size at age estimates derived from whole otoliths. Using an age-length key and representative length frequencies of harvested P. saltatrix, the age composition and mortality of the population was calculated. This chapter also includes a review of growth and mortality for this globally distributed species.

In chapter 3, I quantify the diet of P. saltatrix over its lifecycle and east Australian distribution. Using a novel classification tree analysis, I identify significant shifts in diet which occur with both ontogeny and latitude. This chapter has been published in Marine Biology:

Schilling HT, Hughes JM, Smith JA, Everett JD, Stewart J, Suthers IM (2017) Latitudinal and ontogenetic variation in the diet of a pelagic mesopredator (Pomatomus saltatrix), assessed with a classification tree analysis. Marine Biology 164: 75 doi 10.1007/s00227- 017-3105-1

In chapter 4, I use the elemental composition of P. saltatrix otoliths to investigate juvenile habitat use. I test the assumption that all juvenile P. saltatrix in eastern Australia exclusively use estuarine environments before emigrating to coastal habitats at upon maturity. This assumption contrasts with other populations of the same species and has previously been identified as an inconsistency in life history deserving of attention (Juanes et al. 1996). This chapter has been published in a special issue of Marine Ecology Progress Series:

Schilling HT, Reis-Santos P, Hughes JM, Smith JA, Everett JD, Stewart J, Gillanders BM, Suthers IM (2018) Evaluating estuarine nursery use and life history patterns of Pomatomus saltatrix in eastern Australia. Marine Ecology Progress Series 598: 187-199 doi 10.3354/meps12495

In chapter 5, I investigate the reproductive strategy of P. saltatrix in eastern Australia using historical larval fish abundance data, a gonadosomatic index survey and macroscopic staging of gonads. Larval dispersal was modelled using a particle tracking model based upon release times and locations determined from surveys of reproductive biology. The reproductive biology half of this chapter has been published in Marine Environmental Research:

Schilling HT, Smith JA, Stewart J, Everett JD, Hughes JM, Suthers IM (2018) Reduced exploitation is associated with an altered sex ratio and larger length at maturity in southwest Pacific (east Australian) Pomatomus saltatrix. Marine Environmental Research 147:72-79 doi 10.1016/j.marenvres.2019.02.012

Chapter 6 summarises the main findings of the thesis. This chapter is used to give an overview of the entire lifecycle for this population and then relate this back to other populations of P saltatrix.

The data chapters are written as four stand-alone manuscripts (Chapters 2 to 5) for publication in peer-reviewed journals. Each chapter is self-contained and subsequently, there will be some repetition. Cited literature is compiled in a single list at the end of the thesis to avoid duplication (Chapter 7). Supplementary material for each chapter is included in appendices (Chapter 8).

2 Growth and mortality of Pomatomus saltatrix in the southwest Pacific Ocean (eastern Australia), with a global review

2.1 Abstract

Pomatomus saltatrix is one of few globally distributed pelagic mesopredators that is exploited heavily throughout its range. Despite the implementation of strict management strategies, the southwest Pacific Ocean (eastern Australian) population has limited published estimates of the key life history parameters of mortality and growth. By validating a whole otolith ageing technique and using a model selection process with 8 candidate growth models, we showed that the Schnute growth equation provided the best fit and yielded parameter values of a = 0, b = 2.49, size at age 1 = 25.46 cm fork length (FL) and size at age 4 = 46.34 cm FL. P. saltatrix in the southwest Pacific show a similar growth rate to other global populations of P. saltatrix. Using a length frequency representative of harvested P. saltatrix and a catch curve analysis, instantaneous total mortality rate (Z) for the southwest Pacific population was estimated to be 1.62. Comparison with other global populations showed the northwest Atlantic population to have both the lowest natural mortality (M) and Z, together with the largest maximum biological age (14 y). All other populations were similar with higher mortality and maximum ages of 6 – 10 years. Z was driven largely by M for most populations, although fishing mortality (F) was highest in the east Indian and southwest Pacific populations. Despite being geographically and genetically distinct populations, P. saltatrix demonstrates a generally consistent life history strategy of fast growth and high mortality.

Keywords: bluefish, tailor, life history, whole otolith, Schnute growth curve, model selection

2.2 Introduction

Pomatomus saltatrix (Linnaeus, 1766) has many common names including bluefish, tailor, elf, shad, tassergal and anchova. It is a highly mobile pelagic mesopredatory fish with a cosmopolitan distribution. It is found throughout subtropical and temperate latitudes (Figure 2.1). There are 8 major populations, which are located in the west Mediterranean Sea, east Mediterranean/Black Sea, the northwest Atlantic, east Atlantic, southwest Atlantic, west Indian, east Indian and southwest Pacific Oceans (Juanes et al. 1996). The circumglobal distribution has been shaped by paleoclimate, water temperatures and water depths and has resulted in almost no genetic mixing between these populations (Goodbred and Graves 1996, Miralles et al. 2014b).

Pacific Indian Ocean Ocean

Figure 2.1 Global distribution of Pomatomus saltatrix (in black) overlaid on the average annual sea surface temperature. These population ranges (except southwest Pacific) are based upon the following reported ranges: east Indian Ocean (Smith et al. 2013), northwest Atlantic Ocean (Robillard et al. 2009), west Indian Ocean (Govender 1999, Mann 2000), Mediterranean Sea (Sabatés et al. 2012), southwest Indian Ocean (Haimovici and Krug 1996) and the east Atlantic population (Champagnat 1983).

As a traditional food source and artisanal fishery species (Silvano and Begossi 2005), P. saltatrix is targeted primarily by recreational fishers for both sport and food, although commercial operations continue to harvest a significant quantity (14,731 t in 2015; FAO 2017). P. saltatrix is found around surf beaches and headlands as well as in bays and estuaries (Pollock 1984, Zeller et al. 1996, Potts et al. 2016, Schilling et al. 2017) where it is targeted by both recreational fishers using both bait and lures, and commercial fishers using mesh nets or baits. During the 20th century many global populations of P. saltatrix were noted to be in decline, most likely due to overexploitation (Northeast Fisheries Science Center 1997, Maggs et al. 2012, Nieto et al. 2015, Leigh et al. 2017). This prompted the introduction of numerous regulations and research plans for the species including seasonal closures, size limits and bag limits and commercial quotas, which resulted in most stocks showing signs of stabilising or improvement (Maggs et al. 2012, Northeast Fisheries Science Center 2015, Leigh et al. 2017). Very little is known about the east Atlantic population with almost all knowledge resulting from a single source (Champagnat 1983).

P. saltatrix has a consistent early life history across the distinct populations. Adult P. saltatrix undertake an annual coastal migration into the prevailing current to spawn (Juanes et al. 1996, Shepherd et al. 2006, Brodie et al. 2018). The eggs and larvae produced are subsequently transported by coastal currents to downstream areas where juveniles recruit to estuarine and nearshore habitats (Juanes et al. 1996, Callihan et al. 2008, Schilling et al. 2018). Although their early life history has broad commonalities, the distinct P. saltatrix populations are observed to have differences in subsequent growth and mortality rates (Juanes et al. 1996). These differences are particularly clear in comparative estimates of instantaneous natural mortality (M). For example, for the northwest Atlantic population, M is estimated to be 0.2 (Northeast Fisheries Science Center 2015), whilst for the southwest Pacific (eastern Australia) population, M is estimated to be between 0.95 and 1.5 (Leigh et al. 2017). As most estimates of M are derived from the maximum age in each population, the differences in mortality estimates are reflected in the maximum age observed in global populations: in the northwest Atlantic fish aged 12 years or older are relatively common (Robillard et al. 2009), however, the other populations rarely contain fish older than 6 – 8 years (van der Elst 1976, Ceyhan et al. 2007, Smith et al. 2013, Leigh et al. 2017). It is currently uncertain why the fish in some populations get considerably older, but it could potentially be due to different methodologies used to estimate age or it could be due to differing mortality from predators.

Given the potential for such large variability in life history parameters amongst the global populations, it is prudent to estimate parameters specifically for each population. The east Indian Ocean, southwest Pacific Ocean (eastern and western Australian) and east Atlantic P. saltatrix populations are the only stocks without peer-reviewed studies on their growth and mortality rates. Two Australian stocks are genetically distinct (Nurthen et al. 1992). Both stocks are monitored by combing data from logbooks, recreational harvest estimates, collections of annual length and age data (using whole otoliths) and a juvenile recruitment index collected via a citizen science program (east Indian Ocean population; Smith et al. 2013, Leigh et al. 2017). These monitoring programs were introduced following fishery management concerns about exploitation levels, which were supported by fisher concerns about declines in catch rate that were linked to large numbers of fishers targeting annual migrations. The data collected through these monitoring programs have been used for stock assessments (Smith et al. 2013, Leigh et al. 2017).

A key aspect of stock assessments is age estimation, which defines the important fishery parameters of growth and mortality, the two most influential demographic characteristics controlling the productivity of fish populations (Campana and Thorrold 2001). If these parameters are not accurately understood, fished populations may be at risk of severe overfishing. As an example, the age of orange roughy (Hoplostethus atlanticus) was severely underestimated in the late 20th century which resulted in some orange roughy fisheries collapsing. This was due to the original age process estimating a maximum age of 20 -30 years (Mace et al. 1990), when it is now known the species can live over 100 years (Smith et al. 1995, Andrews et al. 2009). This resulted in an incorrect understanding of the population demography, leading to a much higher fishing rate than was appropriate as it was thought the stocks would be more resilient than they actually were (Clark 2001). On the other hand, if demography including growth and mortality rates are well understood fisheries can be managed sustainably, for example the life cycle of the eastern Rock lobster (Sagmariasus verreauxi) is well understood and it is now possible to accurately forecast sustainable annual catch limits (Cetina-Heredia et al. 2019). Examples such as this highlight the need for accuracy in age and growth rate estimates for fisheries.

In Australia, for P. saltatrix, growth and mortality are calculated using whole otoliths. However, the use of whole otoliths has not been fully validated as an ageing method for P. saltatrix in Australia. Hence, there remains some uncertainty surrounding the growth, mortality and age-

18 structure of Australian P. saltatrix populations. Hoyle et al. (2000) and Brown et al. (2003) validated the annual periodicity of growth checks in whole otoliths in eastern Australia using fluorescent marking methods (Brown et al. 2003) and Marginal Increment Analysis (Hoyle et al. 2000). Despite the validated formation of growth checks, there was limited comparisons of whole and sectioned otoliths. This is despite sectioned otoliths being the preferred method of age estimation in the northwest Atlantic population where they have been shown to have validated annuli and high precision (Robillard et al. 2009).

As P. saltatrix is an ecologically important mesopredator, and an economically important fishery species, therefore it is important to understand its key life history parameters. The aims of this study are to 1) Validate the use of whole otoliths as an appropriate ageing tool; 2) Estimate growth and mortality rates for the southwest Pacific (eastern Australia) population; and 3) Compare these key life history parameters with other global populations of P. saltatrix to identify key differences and potential drivers of differences in life history.

2.3 Methods

2.3.1 Fish Collection

To model growth using size at age data, otoliths were collected from 4049 Pomatomus saltatrix in eastern Australia (25 – 37°S) that were sourced from both the commercial and recreational fishing sectors in conjunction with targeted sampling of undersized fish (Table 2.1). In New South Wales (NSW), fish from the commercial sector were sampled from ports of landing (the Sydney Fish Market and regional fishermen’s co-operatives) along the coast. NSW recreationally harvested fish were sampled through beach surveys and donations of biological material from a recreational citizen science program (NSW Department of Primary Industries Research Angler Program). Where possible, all fish were measured for fork length (FL) to the nearest 0.1 cm, total length (TL) to the nearest 0.1 cm, weight to the nearest g and sex. Otoliths were removed by dissection in the laboratory, cleaned in fresh water and stored dry.

Table 2.1 Collection information for the two otolith datasets used to estimate the age of Pomatomus saltatrix in eastern Australia.

Dataset Queensland (QLD) New South Wales (NSW) Sample dates 15/1/2013 – 16/11/2016 3/7/2014 – 1/12/2017 Sample size 2158 1891 Minimum fork length (mm) 210 39 Maximum fork length (mm) 750 807 Latitude range (°S) 25 – 28 28 – 37

In QLD, fish were sampled between the NSW – QLD border and Baffle Creek (24.5°S) through the Fisheries Queensland Fishery Monitoring Program following (Fisheries Queensland, 2013). Commercial catches, to be representative of the QLD harvest, were routinely sampled year- round from fishers’ residences and seafood processors. Recreational catches, to be representative of the QLD harvest, were routinely sampled year-round from boat ramp surveys, roving beach surveys, competition sampling and the Keen Angler Program. Whole fish or fish frames were measured for FL to the nearest 1 cm, and, where possible, sex was recorded. Otoliths were removed from a subset of fish (with an annual calendar year cap of 10 otoliths per each 1 cm FL length class bin), cleaned in fresh water and stored dry.

2.3.2 Comparison Between Whole and Sectioned Otoliths

To validate the use of whole otoliths as an ageing method for P. saltatrix, increment counts (not ages) from whole otoliths were compared to increment counts from sections of the same otoliths in a blind reading (randomised order). Increments were defined as opaque rings on the otoliths (Supplementary Figure 8.2.1). Age estimates from sectioned otoliths have been fully validated and show high precision in the northwest Atlantic P. saltatrix stock (Robillard et al. 2009). There were 71 otoliths selected for this validation task. Using the NSW Department of Primary Industries (DPI) Fisheries database, 5 fish were randomly selected from each 5 cm FL size bin (16 bins; 0 cm to 80 cm), if there were less than 5 otoliths then all available were used. The left otolith was used for consistency except when it was broken. Whole otoliths were read by immersing the otolith in water and illuminating them using reflected light.

Interpretation of the otolith increment macrostructure were done according to the fish ageing protocols for the Fisheries Queensland Fish Ageing Facility (Department of Primary Industries and Fisheries 2007, 2008). Briefly, this involves counting the number of increments between the primordium and the otolith edge, starting with the first increment approximately forming near the anterior edge of the antirostrum (Brown et al. 2003) and an edge classification assigned as new, medium or wide. New is defined as < 20 % width of previous translucent zone or increment not fully visible around the whole edge of the otolith; medium is defined as 20 – 70 % width of previous translucent zone; and wide is >70% width of previous translucent zone. Images were taken using a dissecting microscope (Leica M80, Switzerland) with HD camera at 7.5x magnification. For each otolith, there were two whole otolith readings done without knowledge of fish length or sample data. Whole otolith readings were completed by a qualified single reader; that is, they had passed a competency test on a reference collection at the Fisheries Queensland Fish Ageing facility (Department of Primary Industries and Fisheries 2007, 2008).

To prepare a sectioned sample, an otolith was embedded in resin and sectioned transversely across the primordium with a low speed saw to 30 – 35 µm thickness. The section was polished to remove saw marks, covered with mounting medium (Safety Mount #4, Fronine, Australia) and a coverslip. Sectioned otoliths were read using the procedure described by Robillard et al. (2009) except reflected light was used and the sections were not burnt. For each sectioned otolith, two counts were made without knowledge of fish length or sample data. An example

21 of an otolith read using both methods is included in the Supplementary Material (Supplementary Figure 8.2.1).

Within method and between method comparisons were conducted using age bias plots and average percent error (APE). As recommended by McBride (2015), bias was assessed using a combination of a maximally pooled method (McNemar 1947), a diagonally pooled method (Evans and Hoenig 1998) and an unpooled method (Bowker 1948).

APE was defined as:

푛 푅 |푥푖푗 − 푥̅𝑗 | ∑푗=1 ∑푖=1 푥푗̅ (2.1) 퐴푃퐸 = 100 × 푛푅

where 푥푖푗 is the ith age for the jth fish, 푥푗̅ is the mean age for the jth fish, R is the number of times that each fish was aged (assumed to be the same for all fish, here R = 2), and n is the number of aged fish in the sample (Beamish and Fournier 1981), here n = 71. Bias and precision calculations were all conducted using the ‘FSA’ package in R (Ogle 2018).

2.3.3 Age and Growth Rate Determination

Age estimates were collated for two otolith collections, taken from NSW and QLD (Table 2.1), which are the two states in eastern Australia where P. saltatrix is most abundant and exploited. All otoliths were read using whole otoliths following the Fishery Monitoring Fish Ageing Protocols (Department of Primary Industries and Fisheries 2007, 2008), except for three otoliths which were broken, but had intact cores, and so were read from sectioned otoliths. For the QLD collection, otoliths are read annually, after a reader passes a competency test on a reference collection. Readers must exceed a set level of precision and bias for increment count and edge type (Department of Primary Industries and Fisheries 2007, 2008). After reading the annual sample, a reader must re-read 200 otoliths and pass the same prescribed level of precision and bias for increment count and edge type before the data are added to the database. For the NSW collection, otolith reading was conducted in batches by a single

22 qualified reader (having recently passed the QLD competency test described above). After every batch of otolith readings, 200 random otoliths were re-read and tested for precision and bias to ensure consistent interpretation before the data were entered into the database.

Annual formation of increments has been validated for sectioned P. saltatrix otoliths in the northwest Atlantic using marginal increment analysis up to age 8 (MIA; Robillard et al. 2009). For this study, to validate annual increment formation in eastern Australia, MIA and assessment of the otolith edge were conducted on the whole otoliths in the NSW dataset. Measurements of the distance from the most recent increment to the edge of the whole otoliths were made to calculate the marginal increment ratio (MIR) and the otolith edge as classified as being translucent or opaque. For otoliths which displayed translucent edges, the thickness of the translucent edge was recorded. The translucent edge widths were defined relative to the width of the previous translucent increment as narrow (5 – 30 %), medium (30 – 60 %) and wide (>60 %). MIA and edge type analysis was restricted to fish with 1 or 2 visible increments to ensure sufficient sample sizes each month. All otoliths were examined using the camera and microscope setup described above. The MIA classification rules were slightly different to the edge classification rules used in the ageing analysis (to conform to local Fisheries standards) but as the sole purpose of the MIA was to confirm the annual formation of otolith increments this has no effect on the ageing process.

Daily increments in P. saltatrix have previously been validated in the North Atlantic (Nyman and Conover 1988). To provide a better estimate of juvenile growth rate in eastern Australia, a subset of 61 otoliths from age-0 fish were hand polished with fine lapping paper until daily increments could be counted. These fish ranged in size from 3.9 cm to 19.5 cm FL.

The ageing process followed that documented in Department of Primary Industries and Fisheries (2008), the full details of which are in Section 8.2. Briefly, Fish with a wide marginal increment observed during the months of increment formation had 1 added to their increment count to account for the delay in the increment formation in that fish. This adjustment corrects the age of fish in which the otolith increment should have formed in the last month but is not yet visible as it is often hard to see on the very edge of the otolith (Department of Primary Industries and Fisheries 2007, 2008). Before calculating growth rates, all annually aged fish had 0.5 added to the number of observed increments to generate a more accurate biological age to be used in the size-at-age relationship (places fish in the centre of the age bin). This was to

23 logically place fish in the middle of the age ‘bin’. For example, when a fish shows 2 annual increments, it is most likely be between 2 and 3 years old, rather than exactly 2 years old. Multiple growth models were fitted to the size-at-age data using a model selection method based upon AICc values (Burnham and Anderson 2003). Models were fitted using the nls function in R v3.4.3 (R Core Team 2017). Eight models were fitted: von Bertalanffy, linear, logistic, power, Schnute variation 1, Schnute variation 2 (equivalent to Gompertz), Schnute variation 3 and Schnute variation 4 (Supplementary Table 8.2.1). Age class 0 (years) fish that did not have their age in days estimated were excluded from growth model analyses (n = 659).

Juvenile growth rates were calculated using the same model selection process described above but only using otolith which were daily aged. We present the best fitting model in addition to the linear model which is more interpretable for the general public. The model selection results including AICc can be seen in Supplementary Table 8.2.1.

Due to the error structure of the initial models being heteroscedastic (the age-0 fish being aged on a different scale (days) to the annuli aged fish (years)), generalised non-linear least squares with separate variance parameters for age-0 (daily aged fish) and adult (annually aged fish) were used to refit the best model and get more accurate error estimations. Specifically, this was done by specifying constant variance within each group (age-0 fish and annuli aged fish). This was done using the ‘gnls’ function in the ‘nlme’ R package (Pinheiro et al. 2017). Due to model convergence difficulties fitting nested sex dependant growth models with the generalised non-linear least squares method, growth rates between sexes were visually compared and minimal difference was observed (Supplementary Figure 8.2.2): therefore, both sexes were pooled and their growth modelled together.

2.3.4 Natural Mortality Estimation

Natural mortality (M) was estimated using the equation:

−0.916 푀 = 4.899푡푚푎푥 (2.2)

Where tmax is the maximum observed age (years; age reached by 0.6% of the population) of fish in the dataset (Then et al. 2015). This equation was refitted using the original data from Then et al. (2015) to estimate error around the predicted estimate of M. This was done using Monte Carlo simulation in the ‘predictNLS’ function from the ‘propagate’ R package (Spiess 2017). No adjustment of maximum age for sample size was necessary as the sample size in this study was sufficient (Hoenig 2017). Estimating natural mortality from non-linear equations derived from multi-species analysis is standard practise for fisheries scientists when populations specific estimates are not available (Quinn and Deriso 1999). This specific equation (2.2) was derived from a metanalysis style analysis of over 200 fish species worldwide in order to determine the most appropriate estimator of natural mortality when there is no direct measurements for a population (Then et al. 2015), therefore I believe it is the most appropriate estimate to use for P. saltatrix. The main assumption of doing this is that we assume that P. saltatrix follow the observed relationship between maximum age and natural mortality rates calculated for other species. While we can not confirm this assumption, this is still the best estimate currently available for this population.

2.3.5 Total Mortality Estimation from Length and Age Compositions

The fishery for P. saltatrix in eastern Australia is comprised of both recreational and commercial harvests in multiple management jurisdictions. To estimate instantaneous total mortality (Z), an overall catch composition was compiled by combining weighted length frequencies representative of annual commercial and recreational catches from both NSW and QLD (Litherland et al. 2016).

To generate representative length frequencies for the QLD commercial P. saltatrix fishery, gill net, tunnel net and ocean beach net catches were sampled year-round as described above. Commercial catch records were used to post weight the length samples using spatial and

25 temporal stratification and are considered representative of the harvest (Fisheries Queensland 2013).

To generate representative length frequencies for the QLD recreational P. saltatrix fishery, line catches were sampled year-round as described above. Recreational catch estimates from the state-wide recreational fishing survey (Webley et al. 2015) were used to post weight the length samples using spatial stratification and are considered representative of the harvest (Fisheries Queensland 2013). All fish were measured for fork length to the nearest cm (FL) and the percentage of catch generated for each 1 cm FL bin (Table 2.2). The length frequency, was supplied as the percentage of catch per 2 cm total length (TL) class bins length). These TL bins percentages were back converted to FL using our fork length and total length relationship (equation 2.4) and the proportion method of Booth and Isted (1997). Briefly, this method involves all possible TL measurements between 0 and 90 cm (nearest 0.1 cm) for P. saltatrix were converted into FL using equation 2.4. The proportion of these TL measurements in each FL centimetre size class was noted and used to construct a TL-FL key in the form of a matrix which was then multiplied by the number of measurements within each TL size class, generating the predicted FL length frequency data.

Table 2.2 Sample sizes of the datasets used to generate length frequency distributions for Pomatomus saltatrix in eastern Australia.

State Sample Period Sector Number of Number of fish catches measured sampled NSW July 2014 - June Commercial 371 14,461 2017 Recreational 97 850

QLD January 2014 - Commercial 222 6,049 December 2015 Recreational 1,272 10,418

Total 1,962 31,778

To generate a NSW commercial harvest length frequency, samples of NSW commercial fishing catches were measured to the nearest cm (FL) in various locations along the coast (Table 2.2). The state-wide commercial catch records and gradings were used to scale up length frequency samples based upon latitude, sample grade and month, similar to the QLD data (Stewart et al. 2018).

The recreational length frequencies for NSW were determined by measuring fish caught by recreational fishers (Table 2.2). These measured fish came from a combination of boat ramp surveys, walking beach surveys and fish donated by recreational anglers through the NSW DPI Research Angler Program.

Age compositions were generated using a combined age-length key that was created using all of the aged fish from both NSW and QLD otolith collections (NSW and QLD) and the combined representative harvest length frequency. All length frequencies were binned to 2 cm FL bins to correspond to the coarsest bins in any dataset (the QLD datasets). Ages were assigned to fish using the method described in Isermann and Knight (2005).

The length composition of the population was assumed to be captured by the length composition of the harvest (above a certain size) and was used to estimate Z using the Chapman-Robson method (Chapman and Robson 1960). The first age group included was 1 year older than the age of peak abundance as recommended by Smith et al. (2012). The Chapman-Robson estimator presented by Hoenig et al. (1983) is

1 1 + 푇̅ − 푇 − 퐶 푁 (푁 − 1)(푁 − 2) 푍̂ = log푒 ( ) − (2.3) 푇̅ − 푇퐶 푁[푁(푇̅ − 푇퐶) + 1][푁 + 푁(푇̅ − 푇퐶) − 1]

Where 푇̅ is the mean age of fish in the sample that are greater than or equal to age TC ; TC is the age of full recruitment; and N is the sample size of fish greater than or equal to age TC . The first term transforms the Chapman–Robson estimate of survival into an estimate of Z; the second term reduces the bias that is induced by the transformation. Age compositions and Z were calculated using the ‘FSA’ package in R (Ogle 2018).

Fishing mortality (F) was calculated by subtracting M from Z.

2.3.6 Global Life History Comparison

Comparing the life history parameters of the 8 major global populations of P. saltatrix, required compiling the most recent estimates of growth and mortality from the 5 populations from east Atlantic, northwest Atlantic, southwest Atlantic, west and east Indian Oceans. The two populations (east and west) of the Mediterranean Sea show the same life history and so were considered together (Ceyhan et al. 2007, Sabatés et al. 2012). These data were combined with the estimates from this study of the southwest Pacific Ocean population.

In assembling the data, peer-reviewed literature was used when available, however, there are no estimates of total or fishing mortality available for the eastern Atlantic population. The growth model provided for the east Atlantic population (Champagnat 1983) did not match the size–at-age data or the fitted curve, therefore parameters for this equation were recalculated using the size-at-age data in Champagnat (1983). The von Bertalanffy growth curve was fitted using the ‘FSA’ package in R v3.4.3 (R Core Team 2017, Ogle 2018).

All reported growth models for global P. saltatrix populations took the form of the von Bertalanffy growth function (VBGF), however, the parameters of the VBGF were not compared because some of these growth models had large |t0| values (>1). This suggests poor modelling of juvenile growth and therefore a questionable k growth parameter (Supplementary Table

8.2.2). This is because if the t0 value is not accurate the slope of the growth curve (the rate of growth) is likely to be biased (either too shallow or too steep). Therefore, comparisons of size- at-age and growth rates were made between populations rather than making comparisons of poorly fitting VBGF parameters in some populations. Comparisons of growth rates between populations therefore consisted of: 1. A comparison of size-at-ages 1 – 5 years, and 2. Growth in the year preceding each of these ages. These ages were chosen because the growth equations for each population fit the data reasonably well across this age range. Size-at-age was calculated directly from the growth reported equations. All populations were constrained to a biologically-relevant size 0 cm FL at age 0 to overcome the poor fits to juvenile growth in the reported studies using the VBGF to provide an estimate of growth rate in the first year.

Most of the previous reported estimates of M for P. saltatrix were based on non-linear regression models which have been shown to be less accurate than the model presented by Then et al. (2015). M for each population was therefore recalculated using the oldest observed fish in each population and equation 2.2 (Then et al. 2015), however the original estimates of

M for each population are also reported. Using these non-linear equations, combined with the maximum age (defined as the age reached by 0.6 % of fish), is standard practice for populations where there is no other method to estimate M (Quinn and Deriso 1999). For each population Z was taken from the literature which employed a catch curve method. A range of possible F values was calculated as described above using Z and both the original and recalculated M estimates for each population.

2.3.7 An Individual Outlier

A single large P. saltatrix (90 cm FL, 103 cm TL, 7.8 kg, female) was donated to the NSW DPI Research Angler Program in May 2018, after the study’s sampling period had finished. This fish was captured during November 2017 in the atypical environment of an intermittently closed and open lagoon (ICOLL) on the NSW south coast (St George’s Basin; 35.12°S, 150.60°E). This fish was by far the largest individual recorded in the current study and was estimated to be double the maximum biological age for the other 4049 aged fish (14 years; Supplementary Figure 8.2.3, Supplementary Figure 8.2.4) and bigger than all 31,778 fish measured as part of the length frequency sampling. It was also abnormal in its growth structure. The exceptional size and longevity of this individual may be due to its atypical collection environment, and as such was a clear outlier. As an outlier, this individual was not included in the statistical comparisons of whole and sectioned otoliths or growth models. However, the implications of the information derived from this fish are discussed.

2.4 Results

2.4.1 Morphometric Relationships

Using the sampled fish from the NSW portion of the southwest Pacific population, the relationship between total length (TL; cm) and fork length (FL; cm) was described by (r2 = 0.997, P < 0.001):

푇퐿 = 1.117퐹퐿 − 0.216 (2.4)

And the relationship between FL (cm) and weight (W; g) was described by (r2 = 0.998, P < 0.001):

푊 = 0.0103퐹퐿3.0815 (2.5)

2.4.2 Comparison Between Whole and Sectioned Otoliths

No significant bias was observed between the mean whole increment counts and mean sectioned otolith increment counts for up to 6 increments (Figure 2.2, Table 2.3). The differences in mean increment counts between both methods were all ≤1 increment and spread evenly across predicted ages up to 6 (Figure 2.2a) and sizes up to 80 cm (Figure 2b). Five otoliths were available in all length classes except for the following: 60.1 - 65 cm FL (4 otoliths), 65.1 – 70 cm FL (3 otoliths), 70.1 – 75 cm FL (3 otoliths), and 75.1 – 80 cm FL (3 otoliths).

The variable appearance of the whole otoliths was reflected by a medium precision when re- reading the otoliths (APE = 4.51; Table 2.3). Nonetheless, there was agreement in increment counts for 92.6 % of otoliths. For the otoliths with inconsistent counts, there was a maximum difference of one between the first and second readings. The APE for sectioned otoliths was also acceptable, although greater than whole otoliths (APE = 6.678; Table 2.3) and it suggests sectioned otoliths can also be used accurately.

In the otolith from the exceptionally large P. saltatrix, 8 increments were observed in the whole otolith but, when sectioned, there were 13 increments clearly visible (Supplementary

Figure 8.2.3). The otolith was also considerably more opaque than otoliths from all the smaller fish and was an irregular shape compared to otoliths from most large P. saltatrix.

Figure 2.2 Comparison of increment counts on Pomatomus saltatrix otoliths which were read using both whole and sectioned methods showing: a) Comparison of mean whole otolith increment counts and mean sectioned otolith increment counts, and b) The difference between sectioned and whole increment counts fork length (cm). The solid blue line represents a LOESS smoother while the grey band represents the 95% confidence region in both plots. The dashed lines represent the relationship if there was no difference. Note a jitter has been applied to all points to prevent overlap (n = 81).

Table 2.3 Results of the precision and bias comparisons within and between otolith preparation methods using 71 otoliths from the NSW dataset. df is degrees of freedom, APE is average percent error.

Bias test Precision McNemar Evans-Hoenig Bowker df Chi.sq p df Chi.sq p df Chi.sq p APE Whole re- 1 1.000 0.317 1 1.000 0.317 5 3 0.700 4.508 read Sectioned 1 1.333 0.248 1 1.333 0.248 5 6.667 0.246 6.678 re-read Mean whole 1 0.000 1.000 1 0.000 1.000 2 0.667 0.717 8.332 and mean sectioned

2.4.3 Growth Modelling

Using whole otoliths, both MIA and assessment of otolith edge types analysis throughout the year confirmed that 1 annulus was formed per year, which is consistent with other global populations. For the southwest Pacific population, this annulus was shown to form between September and January (Figure 2.3).

The best fitting growth model was the Schnute growth model variation 3 (a = 0 in original Schnute equation; Supplementary Table 8.2.1). This model is expressed as:

1 푡 − 푇 ⁄푏 푏 푏 푏 1 (2.6) 푌(푡) = [푦1 + (푦2 − 푦1 ) ] 푇2 − 푇1

where b = 2.486 ± 0.03, age 1 (T1) = 1, age 2 (T2) = 4, size at age 1 (y1) = 25.464 ± 0.14, size at age 2 (y2) = 46.340 ± 0.14 (Figure 2.4; estimates are mean ± standard error). This model has no asymptotic length unlike the VBGF.

Figure 2.4 Size at age (biological age) for Pomatomus saltatrix in the southwest Pacific population (eastern Australia; n = 3,390). The solid black line shows the fitted Schnute growth curve (variation 3). The dashed blue line shows the fitted von Bertalanffy growth curve. Note the semi-transparent points which show the density of data.

The VBGF did not accurately describe growth of smaller or large fish (Figure 2.4). As the VBGF is the standard growth curve in all fish growth literature we have reported the results, however we do not recommend the use of these values. There was large variance in the parameter estimates: the best fitting parameters (with 95% CI) were L∞ = 104.4 cm FL (87.26,

-1 135.45), k = 0.100 year (0.067, 0.135) and t0 = -1.98 (-2.31, -1.68).

Using only the data from the fish that had their daily ages estimated (sizes: 3.9 – 19.5 cm; ages: 32 – 236 days), juvenile P. saltatrix grew approximately 0.08 cm day-1 (linear regression; r2 = 0.873, n = 61, P < 0.01). The best fitting growth curve between fork length (FL; cm) and age (d; days) is given by the logistic equation (n = 61, P < 0.01):

퐿 퐹퐿 = ∞⁄ (2.7) (1 + 푒−푘(푡−푡0))

Where L∞ = 20.486 ± 1.323, k = 0.020 ± 0.002 and t0 = 94 ± 7.800 (Figure 2.5; estimates are mean ± standard error).

Figure 2.5 Size at age for juvenile Pomatomus saltatrix, which were aged using daily increments with a logistic growth curve (n = 61).

2.4.4 Age Structure and Mortality Estimations

Ninety five percent of the harvest in eastern Australia (southwest Pacific Ocean population) was between 28 and 46 cm FL which represents fish aged 1 – 3 years old, with the majority of the harvest being 2 and 3 years of age (Figure 2.6). The larger minimum legal length (MLL) in QLD (35 cm TL), compared with NSW (30 cm TL), resulted in the QLD harvest having proportionally more 3 year old and less 1 year old fish than NSW. Very few large old fish were collected from eastern Australia in the present study with just 35 individuals sampled > 60 cm FL and 11 fish > 5 years of age (Figure 2.4, Figure 2.6). The largest (and oldest) P. saltatrix sampled was 80.7 cm FL and 7 years old (Figure 2.4, Figure 2.6).

Figure 2.6 Representative length composition of harvested Pomatomus saltatrix in eastern Australia. Each bar represents a 2 cm length class (n = 31,778).

Natural mortality (M) of P. saltatrix in the southwest Pacific was estimated to be 0.82 (Equation 2.2; 95% CI 0.77 - 0.88). Using ages 3 – 7, total mortality (Z) was estimated to be 1.62 (95% CI 1.43 - 1.82). Fishing mortality (F) was therefore estimated to be 0.8 (possible range: 0.55 – 1.05).

2.4.5 Global Life History Comparison

Except for the P. saltatrix population in the northwest Atlantic, which showed low estimates of both M and Z, all other global P. saltatrix populations had high estimates of M (0.59 – 0.82) and moderate to high estimates of Z (0.90 – 1.62; Table 2.4). This pattern is driven by the maximum observed age in each population, with the northwest Atlantic population containing the oldest fish. Growth was similar between all populations up to approximately age 3: after this age, the northwest Atlantic and east Atlantic populations showed larger size at each subsequent age (Figure 2.7 & Figure 2.8). All populations, except the southwest Atlantic and east Atlantic, showed that fast growth plateaued after age 2 (Figure 2.7). Juvenile growth (< 1

36 year) was poorly described by the VBGF with |t0| values > 1 in all the populations except for the east Indian, east Atlantic and northwest Atlantic Ocean populations (Figure 2.7; Supplementary Table 8.2.2).

Figure 2.7 Comparison of the growth curves of different population of Pomatomus saltatrix around the world (Table 2.4). All populations except southwest Pacific Ocean (eastern Australia) are taken from the literature as follows: east Atlantic (Champagnat 1983), southwest Atlantic Ocean (Brazil; Haimovici and Krug 1996), Mediterranean Sea (Ceyhan et al. 2007), west Indian Ocean (South Africa; Govender 1999), northwest Atlantic Ocean (Robillard et al. 2009), east Indian Ocean (west Australian; Smith et al. 2013) and are restricted to the sizes modelled in the original research.

Figure 2.8 Visual representation of the growth rates of each population up to age 5. Growth in previous year was determined by using the fitted growth curve for each population in Figure 2.7. All populations were assumed to be 0 cm FL at age 0 to overcome the poorly fit juvenile growth in the published growth curves

Table 2.4 Summary of published life history parameters for global populations of Pomatomus saltatrix. Size at age is the predicted fork length (cm) from each of the published growth equations for each population. Tmax is the maximum observed age in the population. M is natural mortality, Z is total mortality and F is fishing mortality Recalculated M was estimated using the non-linear equation of Then et al. (2015), which has been shown to be more accurate than the equations used by the original studies. The range of F values was calculated by subtracting both the original and recalculated M estimates from Z for each population.

-1 -1 Region Size at Size at Size at Size at Size at tmax Original Recalculated Z (yr ) F (yr ) References age 1 age 2 age 3 age 4 age 5 M (year-1) M (year-1; Then et al. 2015) 27.1 41.7 52.3 60.1 65.9 14 (Robillard et al. Northwest 2009, Northeast 0.2 0.44 0.34 0 – 0.14 Atlantic Fisheries Science Center 2015) Mediterranean 27.0 35.5 42.9 49.2 54.6 6 0.21 0.82 0.90 0.08 – 0.69 (Cengiz et al. 2013) Eastern 21.1 37.1 50.1 60.5 68.9 9 Recalculated from 0.65 Atlantic Champagnat (1983) 15.3 31.6 42.7 50.2 55.4 8 (Haimovici and Southwest 0.24 0.73 1.01 0.28 – 0.77 Krug 1996, Lucena Atlantic et al. 2002) 31.4 39.8 47.4 54.4 60.7 6 (Govender 1999, West Indian 0.4 0.82 1.09 0.27 – 0.69 Mann 2000) East Indian 23.6 36.8 45.1 50.4 53.6 10 0.42 0.59 1.22 0.8 – 0.63 (Smith et al. 2013) Southwest 25.46 34.6 41.1 46.3 50.8 7 (Leigh et al. 2017) , 1.3 0.82 1.62 0.32 – 0.8 Pacific this study

2.5 Discussion

The southwest Pacific Ocean (eastern Australian) Pomatomus saltatrix population is characterised by fast, non-asymptotic growth up to the normal maximum reported age (7 years) for the species in this region. Modelled growth of the species fails to reach an asymptotic length due to high mortality rates, resulting in low numbers of old, large fish. A review of growth and mortality in P. saltatrix found two main patterns among global populations. All of the populations show fast growth and high mortality rates, except for the northwest and eastern Atlantic Ocean populations. The northwest Atlantic population has fast growth but considerably lower mortality rates, which is reflected by higher proportions of large, old fish not found elsewhere. The similarities in life history, displayed over such a broad geographical range are representative of the successful life history of this species as a pelagic mesopredator.

2.5.1 Age Determination and Growth Rates

Our study validates the use of whole otoliths for accurate age estimation of P. saltatrix. Increments counted in whole otoliths show close agreement with those counted in sectioned otoliths up to estimated age 6. Whole otoliths have been used for ageing P. saltatrix in the Mediterranean, east Indian, west Indian, and the southwest Pacific populations (Govender 1999, Ceyhan et al. 2007, Leigh et al. 2017), which are regions where large, old individuals are relatively scarce. Marginal increment and edge type analyses both showed 1 annulus forming per year: this agrees with previous validation using sectioned otoliths reported from the northwest Atlantic (Robillard et al. 2009) and southwest Pacific (Hoyle et al. 2000). Our study found formation of increments occurred earlier in the year (~November) compared with a previous marginal increment analysis (December – January), likely due to the use of sectioned otoliths (Hoyle et al. 2000). In the current study, we conclude that whole otoliths are a valid method of age determination in the southwest Pacific up to age 6. This conclusion is made despite the study’s limitations i.e. it only validated the first two increments, although it did show high agreement to sectioned otolith counts which have been validated to 8 years in the northwest Atlantic. The current validation combines with the previous validation work of the first increment and increment periodicity in the southwest Pacific (Hoyle et al. 2000, Brown et al. 2003), and high agreement (>95 %) between increment counts in sectioned and whole

40 otoliths up to age 4 in the northwest Atlantic (Sipe and Chittenden 2002). Despite the close agreement between whole and sectioned otoliths up to 6 increments, there was a large difference in increment counts between whole and sectioned otoliths in the largest fish. This was due to the difficulty in interpreting whole otoliths of large fish, particularly increments near the otolith edge. It is therefore recommended that whole otoliths be used for routine ageing of P. saltatrix in Australia, but that the otoliths from fish larger than 70 cm FL are sectioned to ensure unbiased age assignment.

The daily growth analysis showed a fast juvenile growth rate of ~ 0.08 cm d-1, which is slower than the reported juvenile growth rate in the northwest Atlantic (0.09 – 0.21 cm d-1; Juanes et al. 1996), faster than juvenile growth in the east Indian Ocean based upon tagging (0.02 - 0.04 cm d-1; Young et al. 1999), and aligns with previous estimates for the western Pacific (0.075 – 0.13 cm d-1) based upon length frequencies (NSW SPCC 1981). The differences between these populations could potentially be due to the low productivity of the east Indian Ocean, in comparison to the high productivity of the northwest Atlantic (Longhurst et al. 1995, Reygondeau et al. 2013).

The model selection process used in our current study found the classic VBGF was not well suited to describing growth for the southwest Pacific Ocean (eastern Australian) population. This is because it did not accurately describe juvenile growth and failed to find an asymptotic length (Figure 2.4). The current study found that a model without an asymptotic length (Schnute variation 3) was more accurate. While few studies of growth in fish suggest models with no asymptotic lengths, in this case it is consistent with the high mortality rates estimated for the southwest Pacific population whereby few fish survive long enough to provide size-at- age data from large old fish. Despite the overall better fit provided by the Schnute variation 3 growth model, this model still underestimated growth of larger, older classes of fish. Indeed, if the growth curve was projected out to 14 years (the estimated age of the exceptionally large ‘landlocked’ individual), the fitted curve is still an underestimate of the observed size-at-age of this fish (Supplementary Figure 8.2.4). We did not find significantly different growth rates for male and female P. saltatrix despite the fact that they do have different life history aspects, females have been shown to mature later than males (Schilling et al. 2019). No differences in growth rates have also been observed in the northwest Atlantic population (Robillard et al. 2009) but have been observed in the Mediterranean (Ceyhan et al. 2007). I believe that the two sexes may have slightly different growth rates but as both sexes grow fast, the differences

41 are too small to be detected using growth models primarily based upon annual ages which hide a lot of small variability.

All previous studies of P. saltatrix growth provide estimates of the VBGF parameters, however, these model parameters are likely to be biased by poorly modelled juvenile growth (Figure 2.7, Supplementary Table 8.2.2), and therefore should not be compared. Our comparison of growth rates shows all populations except the southwest Atlantic share an initial fast growth rate (20 – 30 cm in the first year) before slowing in the second year. The different growth rate observed in the southwest Atlantic population may be due to ageing errors; i.e. with the first annual increment being misidentified as a result of the use of scales instead of otoliths to derive age estimates. If this was the case, then growth pattern of this population would be likely to match the pattern observed in most other populations. The northwest Atlantic population has rapid initial growth that is maintained longer than the other populations, potentially due to delayed investment in reproduction, as this population has a larger size at maturity than the other populations (van der Elst 1976, Champagnat 1983, Robillard et al. 2008; Chapter 5).

This result contrasts with previously reported research which suggested that there were three main groups in terms of growth rates for global P. saltatrix populations (Juanes et al. 1996). The original groups proposed consisted of the northwest Atlantic and east Atlantic populations as the fastest growing and with the greatest longevity; the southwest Pacific (eastern Australian), east Indian (west Australian), west Indian (South African) and Mediterranean populations as the slowest growing; while the southwest Atlantic (Brazilian) and Black Sea populations possessed growth rates intermediate between the other two groups (Juanes et al. 1996). Instead, this study proposes only two main groups: firstly, the northwest Atlantic and east Atlantic populations as the populations of sustained fast growth; and the other populations, which all show similar growth patterns.

The difference between the findings presented here and the previously suggested P. saltatrix population groupings by growth rate, is likely to be a result of differing ageing methodologies. The current study examined growth mostly based on otolith age estimates, whereas studies cited in Juanes et al. (1996) were based mostly upon scale age estimates which have since been shown to be unreliable for ageing older P. saltatrix (Sipe and Chittenden 2002). It is also possible that the interpretation of increments (and conversion to ages) used may not have

42 been consistent across the different studies. In addition, the growth rates of the east Atlantic and southwest Atlantic populations were calculated in the original studies using different methods to the other populations. Most growth estimates in our comparison, used otoliths, however the east Atlantic growth rate was calculated from length frequency data (Champagnat 1983) and the southwest Atlantic growth rate was calculated using scales (Haimovici and Krug 1996). Comparisons involving these growth rates should be interpreted cautiously as differences between these rates and the other populations may be caused by the different ageing methods.

Differences in population growth rates in other species have previously been linked to temperature with faster growth occurring in higher temperature environments due to increased metabolic rate (Morrongiello and Thresher 2015). Given that all global P. saltatrix populations experience similar average annual water temperature (Goodbred and Graves 1996; Figure 2.1), it is considered unlikely that variations in environmental temperature are driving the difference in growth between the northwest Atlantic population and the other populations of P. saltatrix. However, migrations are not considered when simply looking at average annual sea surface temperature over the whole species distribution and all populations of P. saltatrix migrate. For example, the southwest Pacific P. saltatrix population is heavily influenced by sea surface temperature, with abundance peaking at 21.5°C (Brodie et al. 2018). Population-specific studies may be required to fully understand the importance of environmental temperature for driving basic life history parameters, such as growth, in P. saltatrix populations.

It is also possible that growth rates are not a response to temperature but rather regional productivity. The northwest Atlantic and east Atlantic populations which appear to have the highest growth rates are also two of the regions with the highest regional productivity (Behrenfeld et al. 2006, Stock et al. 2017), which may be promoting the fast growth. On the other hand, the southwest Atlantic population also occurs in an area with high regional productivity and does not have a higher growth rate. The southwest Pacific population occurs in an area of moderate productivity while the west and east Indian Ocean and Mediterranean populations occur in areas of low productivity. Despite this variation in regional productivity, the growth rates are remarkably consistent between all the populations. This suggests that while the areas of high productivity may be promoting faster growth in the northwest Atlantic

43 and east Atlantic populations, the productivity is not the primary driver of growth rates differences among different population of P. saltatrix.

I believe the most likely cause of these differing growth rates is fishery induced evolution with the populations with higher levels of Z (either from M or F) investing in reproduction earlier and therefore slowing growth (Kuparinen and Merilä 2007, Quince et al. 2008a, Quince et al. 2008b). This is shown by the northwest Atlantic and east Atlantic populations having the lowest mortality and the fastest growth rates. This idea is further discussed in section 2.5.2.

2.5.2 Mortality

The current study’s estimate of M of 0.82 for P. saltatrix in the southwest Pacific (eastern Australia), calculated using the maximum age equation of Then et al. (2015), is lower than the estimate from a recent stock assessment for the species (Leigh et al. 2017). The stock assessment by Leigh et al. (2017) estimated M of P. saltatrix in eastern Australia to be between 0.95 and 1.5, with a stochastic model estimating the most likely value to be 1.3. It was noted that the stock assessment model made many assumptions and values of M below 0.95 returned unrealistic population levels in the early 2000’s and hence was restricted in the lower limit. It is possible that the true value of M lies between these two estimates, and the most robust estimate is arguably one achieved by comparing different approaches. This would match the estimate of M from a previous stock assessment on this population which estimated M to be 0.8 – 1.3 although these values only applied to fish up to three years of age (Leigh and O'Neill 2004). As the fishing pressure on P. saltatrix in eastern Australia is considered to be declining (Leigh et al. 2017), Z is likely to decrease, making M the key driver of mortality for this stock. As Z is quite high, it is likely that this population is quite vulnerable to stress from years of low recruitment success as it depends on annual recruitment to boost the population (Fogarty et al. 1991). This was identified in the recent stock assessment as a key challenge for this species and a most likely contributing factor to the anecdotal declines seen previously in this population (Leigh et al. 2017).

While we did observe a single, exceptionally large individual, this fish was considered to be an outlier from the population because of its size (far exceeding the length of 31,778 fish sampled) and age (14 years estimated by sectioned otolith, which made it the oldest out of

4,049 fish sampled for age estimation). This individual was not used to provide the maximum age for the population in our estimate of M as it was not considered to be representative of the population. The exceptional size and longevity of this individual was attributed to its atypical collection environment of an intermittently closed estuary system on the NSW south coast: despite the normal habitat for adult P. saltatrix being coastal marine waters (Brodie et al. 2018, Schilling et al. 2018). While P. saltatrix in eastern Australia are an exploited stock, and the estimates of M given by nonlinear equations (such as Equation 2) are likely overestimates (Hoenig 2017), we believe that an estimate of M generated using the age of this single large fish (maximum age = 14, M = 0.2) would be a major underestimation of M for this population. Despite the unique nature of this fish, it does provide evidence that P. saltatrix in the southwest Pacific, under some circumstances, have potential longevity similar to that observed in the northwest Atlantic population.

The global populations of P. saltatrix have a fairly consistent M (0.53 – 0.82), with the exception of the northwest Atlantic population (M = 0.2 – 0.44). The low M of the northwest Atlantic population suggests that this population potentially could occupy a higher trophic position or be subject to less predation compared to the other populations. Indeed, estimates of mean ecosystem trophic level in the northwest Atlantic (~2.9 - 4) do differ slightly from that estimated in south-eastern Australia (~3.5 - 4; Branch et al. 2010). While these trophic level estimates do not cover the entire distribution of P. saltatrix in either population, they do suggest that the regions may have a different trophic structure: however note that Branch et al. (2010) did not assess other regions where P. saltatrix are found. To better assess this hypothesis more data is needed on the diets of top predators and P. saltatrix in all populations so that a food web analysis of these ecosystems can be conducted. This would greatly improve our understanding of what is driving the differences in M between global populations of P. saltatrix.

Estimates of total mortality (Z) are also reasonably consistent among global populations (0.90 – 1.62), once again with the exception of the northwest Atlantic population which has by far the lowest Z estimate of 0.34. The southwest Pacific (eastern Australian) population has the highest Z which is likely driven by continued heavy recreational fishing pressure on annual spawning aggregations in the north of their distribution and the combination of variable recruitment and few age classes (Pollock 1984, Zeller et al. 1996, Leigh et al. 2017). It should be noted that catch curve analyses of Z assume constant vulnerability, constant recruitment

45 and an unbiased sample, however these cannot be assumed for this population, particularly recruitment which is thought to be variable (Leigh et al. 2017). The current study combined multiple fishery sectors, but despite this had only 5 age classes (ages 3 – 7) with which to estimate Z. This means that the estimate of Z in this study should be interpreted cautiously as its heavy reliance on fishery-dependent samples means that it may not be representative of the population overall. All global populations of P. saltatrix show similar spawning migration patterns and so consequently, they are also subject to various management strategies which attempt to limit fishing pressure (Maggs et al. 2012). The Mediterranean population appears to be the only population (except the east Atlantic) that is not subject to strict management. While the Mediterranean population does not have the highest estimate of Z, it is over- exploited, with the majority of the harvest consisting of small fish due to the lack of a minimum size limit (Ceyhan et al. 2007, Cengiz et al. 2013).

Differences in the life history parameters of growth and mortality are potentially driving differences in other life history parameters, including reproductive age. In the populations of P. saltatrix that have sustained fast growth and largest longevity, length at 50% female maturity (L50) is 45.1 cm FL in the northwest Atlantic population (Robillard et al. 2008) and 38.0 cm FL in the east Atlantic population (Champagnat 1983). In the other populations L50 ranges from 25 – 31.5 cm FL (van der Elst 1976, Bade 1977, Smith et al. 2013, Chapter 5) and is reflected in the slowing growth rates by age 2. This is a strong evolutionary signal and reflects the lower Z (possibly M) in the northwest Atlantic population (and potentially the east Atlantic; Swain et al. 2007). With higher survival, these populations may delay the start of its reproductive development to increase investment in somatic growth and therefore be larger at first spawning with potentially higher fecundity in the first spawning season (Figure 5.2).

Changes to total mortality rates (both reductions and increases) can have significant effects for fished populations. The increasing pressure of rising mortality rates has previously been shown to select for earlier maturity in fished populations (Kuparinen and Merilä 2007, Swain 2011). Similarly when this high mortality pressure is reduced, the age (and size) at maturity can increase as the fish are under less pressure to mature earlier and can invest more in early growth (Schilling et al. 2019). If the ageing process and growth rates for a species are not accurate, then these warning signs of changes in life history traits may go unrecognised resulting in potentially catastrophic fisheries collapses as seen in the northern cod Gadus

46 morhua (Olsen et al. 2004). Therefore, it is vital that age estimate of fish species is done with the highest possible accuracy.

2.5.3 Concluding Remarks

P. saltatrix in the southwest Pacific (eastern Australia) show fast growth and high mortality which is consistent with the global pattern of growth and mortality for most P. saltatrix populations. The northwest Atlantic (and potentially east Atlantic) population appears to have a different life history, with a lower mortality rate and sustained fast growth rate that results in a higher proportion of older and larger fish in the population. This study demonstrates a generally persistent life history strategy in a globally distributed mesopredator, across multiple isolated populations with differences potentially driven by variation in population M.

3 Latitudinal and ontogenetic variation in the diet of a pelagic mesopredator (Pomatomus saltatrix), assessed with a classification tree analysis

This chapter has been published in Marine Biology, the reference is:

3.1 Abstract

Pelagic mesopredators are abundant in many marine ecosystems and exert strong top-down influence on food webs. We explored the dietary niche of Pomatomus saltatrix in eastern Australia, using a classification tree analysis to identify key factors driving diet variation. P. saltatrix was shown to be an opportunistic generalist predator which exhibited increased baitfish consumption, and decreased crustacean consumption, with increasing size. The classification tree analysis showed that body size and latitude had the greatest influence on the diet of P. saltatrix, with significant ontogenetic diet shifts occurring at 8 and 30 cm fork length (FL). While piscivory is evident in the majority of P. saltatrix diets by ~ 8 cm FL, crustaceans are almost entirely absent from the diet after ~ 30 cm FL. The importance of latitude was likely related to the broad-scale oceanography in the study region, including the East Australian Current and its separation from the continental shelf. The classification tree analysis is a powerful framework for identifying important variables in diet composition.

Keywords: gut content analysis, piscivory, East Australian Current, baitfish, tailor, bluefish

3.2 Introduction

Predators exert a top-down influence on marine communities through direct and indirect interactions with other trophic groups (Heithaus et al. 2008), and declines in the population of marine predators have large impacts on ecosystem function (Baum and Worm 2009). Pelagic fish in the marine environment are logistically hard to sample due to their high mobility, but top pelagic predators such as tuna and billfish have been subject to relatively high research efforts due to their international commercial importance (Olson et al. 2010, Olson et al. 2014). Pelagic mesopredators (mid-size predatory fish of < 1m length), occupy an important trophic niche but have been studied only occasionally, despite their often high commercial and ecological value. Importantly, large variation in the diet of mesopredators has been observed in those few studies. As an example, in dolphinfish (Coryphaena hippurus), the importance of prey such as mesopelagic fish, cephalopods and flyingfish was found to vary over five regions of the eastern Pacific Ocean, highlighting the dynamic pelagic food web and ecosystem structure (Olson and Galvan-Magana 2002).

The relative abundance of pelagic mesopredators has a substantial impact on the lower trophic levels (Prugh et al. 2009, Ritchie and Johnson 2009). While it is known that the abundance of mesopredators is related to anthropogenic impacts and the presence or absence of top predators (Eriksson et al. 2011), the impact of mesopredators on lower trophic levels is uncertain due to the wide variety of life-history strategies found in mesopredators (Frid et al. 2012), and relative lack of research into pelagic mesopredators. In order to understand the interactions between pelagic mesopredators and lower trophic levels, more detailed species- specific dietary knowledge is required.

In eastern Australia, pelagic mesopredators include species such as Pomatomus saltatrix (tailor), Seriola lalandi (yellowtail kingfish), Sarda australis (Australian bonito) and Arripis trutta (eastern Australian salmon). A. trutta is the only mesopredator in eastern Australia with a detailed dietary study (Hughes et al. 2013), which showed that A. trutta diet varied with latitude, season and fish length. The local marine environment is changing with a strengthening East Australian Current (Suthers et al. 2011, Wu et al. 2012), creating an urgent need to improve our understanding of mesopredator diets which are likely to vary due to changing environments.

Pomatomus saltatrix is a pelagic mesopredator with a global distribution, making it a key predator in many marine ecosystems (Juanes et al. 1996). It has a variety of common names (bluefish, tailor, elf, anchova) and is an important recreational and commercial species with a total global harvest of approximately 20, 000 t (FAO 2017). Previous research into various populations around the world has shown P. saltatrix consume large proportions of invertebrates in early life stages before shifting to piscivory and a diet dominated by small fish (Juanes and Conover 1994, Buckel et al. 1999, Lucena et al. 2000). As a dominant predator in both estuarine and coastal environments, P. saltatrix can reduce the prey availability for other predators due to their aggressive nature of feeding (Hartman and Brandt 1995). For example, they are estimated to consume up to 24% of the US anchovy stock in a year (Buckel et al. 1999). No previous studies have examined the diet of P. saltatrix over its whole life history using gut contents, and in Australia there have been no published studies into their diet (but see Bade 1977 which notes they have a highly piscivorous diet but lack a preference for specific prey). As an abundant mesopredator in a changing marine ecosystem, it is important that the diet of P. saltatrix is examined as a whole, including both the juvenile estuarine and adult coastal stages of its life-history in Australia.

Dietary analysis can be done in a variety of ways (Baker et al. 2014), but classification trees have been used recently as an effective exploratory and predictive non-parametric framework for analysing diet data (Kuhnert et al. 2012, Olson et al. 2014). They can incorporate uncertainty into variable importance measures, predicted prey proportions, and partial dependence plots that explore the relationships between variables and predicted prey proportions. Despite the advantages of this framework and studies that have demonstrated its usefulness (Olson et al. 2014, Alegre et al. 2015, Duffy et al. 2015), it is still only used occasionally. Using a classification tree approach, the aim of this study was to investigate latitudinal, seasonal and ontogenetic variation in the diet of Pomatomus saltatrix in eastern Australia.

3.3 Materials and Methods

3.3.1 Sample Collection and Processing

Pomatomus saltatrix were sampled by a variety of methods between July 2014 and July 2016 along the coast of eastern Australia between 37° S and 27.8° S latitude (n = 1437). These methods included monthly samples from commercial catches, donations from recreational fishermen, bycatch from estuarine trawling, and targeted fishing for juveniles. As P. saltatrix is a coastal or estuarine species, all fish were captured within 2 nm of the coast or within estuaries. Juveniles (< 26 cm) were caught entirely from within estuaries and represent the important early estuarine component of their lifecycle. There was no bias in size collections with fish of all sizes collected in all latitudes across multiple years. After capture all fish were immediately put on ice or frozen before being processed.

The gut contents were processed following the method provided in Hughes et al. (2013), with the addition of dry weights being recorded for each prey type in each stomach. Briefly, prey items were identified, counted and sorted into taxonomic groups before being dried for 72 h at 60° C, to determine taxa-specific dry weight. Loose otoliths and vertebrae were not included in analyses that involved dry weights as they accumulate in stomachs due to slower decomposition and would lead to overestimated proportions (Hyslop 1980). Despite this, loose otoliths and vertebrae were included in the analysis of frequency of occurrence as they are a valid indicator that the predator consumed that prey (Baker et al. 2014). Items identified as bait were excluded from analysis, and most tailor are caught without using bait.

3.3.2 Diet Analysis

To explore spatial, seasonal and ontogenetic structure within the diet data we used a classification tree approach described by Breiman et al. (1984) and expanded upon by Kuhnert et al. (2012). The classification tree was created using the R ‘diet’ package (Kuhnert et al. 2012), which implements the ‘rpart’ classification tree package (Therneau et al. 2015).

The classification tree analysis is a non-parametric approach which regressively partitions data based upon a greedy algorithm method (see Kuhnert et al. 2012 for full details). Excluding empty stomachs, the prey proportions eaten by an individual predator are represented as a categorical variable for each prey type, with observation weights equal to the proportion (by

51 dry weight) of the prey type consumed (Kuhnert et al. 2012). The split criterion used in this case was the Gini index of diversity (Breiman et al. 1984). A large tree was grown and later pruned using the “1 standard error” rule, and variable importance measures were calculated to identify the important predictor variables (Breiman et al. 1984). No evidence of spatial autocorrelation was found when a semivariogram was examined and uncertainty was incorporated into predicted diet compositions using a bootstrap technique with 500 replications for each node of the tree (Kuhnert et al. 2010, Kuhnert et al. 2012).

A preliminary tree included the variables: predator fork length (FL: continuous), latitude (continuous), habitat (categorical: estuary or coast) and season (categorical: four seasons). Habitat was found to be highly correlated with fork length and was removed from the final analysis.

The relationship between predator and prey size is useful for understanding predatory interactions as it often reveals morphological and behavioural characteristics of the predator (Scharf et al. 2000). This relationship was quantified using quantile regression done with the ‘quantreg’ R package (Koenker 2016). Only whole prey or prey able to be assembled whole from pieces were used in this analysis. Prey were measured using standard length (fish) or carapace length (crustaceans). The ‘wild’ bootstrapping method described by Feng et al. (2011) was used with 1000 replications to calculate standard error and p-values.

3.4 Results

A total of 1437 stomachs were analysed. 39 % of the fish were sampled from coastal habitats (the remaining 61 % from estuarine habitats), and 968 (67.4 %) were empty. Fish from both coastal and estuarine habitats had a similar percentage of empty stomachs. There was no pattern in the number of empty stomachs with relation to latitude. A total of 47 prey taxa were identified with the majority of these being teleosts (most commonly Hyperlophus sp. and Sardinops sagax) or small crustaceans (most commonly mysid shrimp or penaeid prawns). Diet data are expressed by frequency of occurrence and dry weight which is detailed in Supplementary Table 8.3.1. While habitat was not included in the statistical analysis, guts from larger P. saltatrix within estuaries (> 15 cm) contained higher proportions of mullet compared to the small P. saltatrix and all P. saltatrix on the coast. The larger estuarine P. saltatrix also showed evidence of cannibalism containing smaller P. saltatrix.

3.4.1 Classification Tree

The final classification tree included Pomatomus saltatrix fork length, latitude and season as covariates (Fig. 1, cross-validated error (CV) rate = 0.746, SE = 0.036). The CV error rate suggests some difficulty in classifying individual fish (a value of 1 would indicate a classification tree is unlikely to be useful), but this is only a guide (and has a role in selecting the best tree) and we explored the value of the tree by comparing with raw data. We concluded the tree was valid because it gave interpretable splits in the data which agreed with patterns in the raw data. The tree was useful because it objectively identified important covariates and ‘breakpoints’ where the diet shifted. In contrast, traditional diet analyses arbitrarily select a point where there may be a dietary difference, and then test the difference across the boundary. The most important covariate for explaining branches in the classification tree (i.e. patterns in the diet of P. saltatrix) was fish length, followed by latitude, with only a weak influence of season (Figure 3.1). This suggests that the diet of P. saltatrix is most influenced by ontogenetic changes rather than seasonal or temporal variation. A summary of the important patterns revealed by the classification tree are shown in Table 3.1. Using the Gini diversity index (D) which drives the splits in the tree, the overall diet diversity of P. saltatrix was moderately high (D = 0.783). The range of diet diversity at the nodes included in the final tree was also high (D = 0.091 – 0.826). This means that in some instances the prey taxa consumed

53 were not very diverse (e.g. P. saltatrix < 8 cm consumed predominately mysids) and in others many types of prey were consumed.

Figure 3.1 The 1 standard error classification tree for Pomatomus saltatrix diet composition, yielding a cross-validated error rate of 0.746 (SE = 0.036). The prey category with the highest proportion dry weight is displayed at each terminal node. Co-variates in the tree are abbreviated; Latitude (Lat), Fish Length (Len) and Season (Seas). Variable importance rankings for each covariate are inset. Node numbers are labelled according to the naming convention of Breiman et al. (1984). A legend for prey grouping abbreviations is also shown.

P. saltatrix length was the most important covariate and was used for the first two splits in the tree (Figure 3.1, Variable Importance (VI) = 1.00). The initial split of the full dataset partitioned 52 small P. saltatrix (< 8.1 cm fork length) from 282 larger (> 8.1 cm fork length) P. saltatrix (Figure 3.1). The small fish had a very low diet diversity because they had large proportions of mysid shrimp in their diet (Figure 3.2– Node 2, D = 0.259). The second split separated fish at 29.5 cm (Figure 3.1). The fish smaller than 29.45 cm had a higher proportion of smaller prey such as Hyperlophus sp., mysid shrimp and penaeid prawns in their diet compared to the larger fish whose diet had higher proportions of larger fish such as Sardinops sagax and carangids such as Trachurus novaezelandiae (Figure 3.2– Nodes 96, 97, 49, 25, 13). A further split using fish length was made to the fish within the < 29.45 cm cluster (Figure 3.1), such that fish < 14.6 cm had more crustaceans in the diet (Figure 3.2– Nodes 96, 97, 49). These patterns are similar to those observed in the raw diet proportions where these were aggregated into 4 cm size bins, revealing that P. saltatrix shifted to a diet heavily dominated by fish at a small size (Figure

3.3). The development of piscivory was early (by ~8 cm) and it was observed in fish as small 5.1 cm fork length.

Table 3.1 Summary of the fish length and latitudinal patterns in Pomatomus saltatrix diet composition identified as terminal nodes in the classification tree. The most important prey items driving these differences are listed in each box (by proportion of dry weight). Where boxes are merged it represents no effect of latitude on that size class. The number of P. saltatrix (n; excluding empty stomachs) for each box is shown

P. saltatrix fork length

Latitude < 8 cm 8 – 30 cm > 30 cm Sprats Anchovies North of 29.5 ° S Sprats Scads Mysids (n = 19) Prawns Mysids (n = 121) 29.5 °-35 ° S (n = 52) Mullets Sardines Blue mackerel Sprats (n = 77) South of 35 ° S (n = 49)

Figure 3.2 Terminal node bootstrapped predictions and the 95 % bootstrap percentile intervals for the pruned classification tree. Refer to Figure 3.1 for prey group codes

Figure 3.3 Proportion (by dry weight) of prey groups by predator size.

Latitude was also important in classifying diet differences between individuals (VI = 0.68), providing two secondary splits (Figure 3.1). North of -29.7° S and south of –34.9° S, diets were low in diversity and had higher proportions of Hyperlophus spp.

Season was shown to have much lower importance (VI = 0.11), only splitting one of the lower branches of the final tree (Figure 3.1). This split identified that for P. saltatrix < 14.55 cm, the diets were dominated by mysid shrimp in autumn while during spring and summer the proportions of penaeid prawns increased. It is worth noting that small fish are not found throughout the whole year, and therefore a full seasonal comparison of small P. saltatrix was not possible (there was no winter sample). This is because of the spring/summer spawning season and fast growth rates (Bade 1977, Zeller et al. 1996).

3.4.2 Predator Prey Size

Quantile regression identified that prey length increased with P. saltatrix length (Table 3.2). There was a trend was for larger prey with increased size of P. saltatrix. Median prey size (50th quantile) and minimum prey size (5th quantile) increased with the size of P. saltatrix at similar rates while maximum prey size (95th quantile) increased at a faster rate, resulting in a divergent pattern (Figure 3.4, Table 3.2).

Figure 3.4 Quantile regression scatterplots showing prey size (Standard or Carapace length) against predator fork length. The regression lines represent the 5th, 50th and 95th quantiles. The type of dot represents the major prey types.

Table 3.2 Quantile regression parameters, standard errors and P values for the test H0 = 0, relating prey lengths to Pomatomus saltatrix length. Tau is the quantile of interest.

Tau Fixed Effect Value Standard Error t-value P(>|t|)

0.05 Intercept -0.90512 0.7559 -1.19741 0.2344

Fork Length 0.12093 0.02488 4.86102 < 0.001 0.5 Intercept 1.75934 0.34338 5.12352 < 0.001

Fork Length 0.10788 0.01595 6.76198 < 0.001 0.95 Intercept 0.49289 0.70981 0.69441 0.48928

Fork Length 0.36548 0.05602 6.52417 < 0.001 57

3.5 Discussion

Pomatomus saltatrix is an important mesopredator in the east Australian pelagic food web, switching from small crustaceans to a variety of prey particularly zooplanktivores. Although a large number of prey taxa were identified, the diets of medium and large P. saltatrix were dominated by pelagic zooplanktivorous fish (primarily clupeids Hyperlophus sp. and Sardinops sagax), and the diets of small P. saltatrix included mostly mysid and penaeid crustaceans. This is consistent with studies of many coastal predators including P. saltatrix in Brazil, South Africa and the eastern US which have found pelagic zooplanktivores in the diet (Lucena et al. 2000, Szczebak and Taylor 2011, Potts et al. 2016). Overall, the wide variety of prey consumed by P. saltatrix infers a predominately piscivorous diet, based upon a flexible and possibly opportunistic feeding strategy.

3.5.1 Ontogenetic Diet Patterns

The classification tree analysis identified fish length (i.e. ontogeny) as the most important variable in shaping the diet of P. saltatrix (Figure 3.1). Using the branches that split using length, three broad diet compositions can be identified. P. saltatrix smaller than ~ 8 cm fork length (FL) had diets almost exclusively made up by mysid shrimp (Figure 3.2 – Node 2), fish 8 - 30 cm had diets where penaeid prawns and fish were found in roughly equal proportions, with fish prey increasing with increasing P. saltatrix size (Figure 3.2 – Nodes 49, 25, 13); and P. saltatrix > 30 cm had diets comprised almost exclusively of fish (Figure 3.2 – Nodes 14, 30, 31). These broad ontogenetic patterns are also observed in the raw diet proportions (Figure 3.3), which provides support that the classification tree approach accurately identified the important shifts in diet with ontogeny. These size groupings of P. saltatrix (< 8 cm; 8-30 cm; > 30 cm) may reflect of a combination of increasing mouth gape and increasing predatory ability (through increased swimming speed) with length (Shimose et al. 2013). The previous work on small (<15 cm TL) P. saltatrix in other populations has shown that the proportion of fish in the diet increases and the proportion of crustaceans decreases with P. saltatrix size (Juanes and Conover 1994). Conversely mature fish have a diet dominated by pelagic fish (Lucena et al. 2000, Szczebak and Taylor 2011). A similar pattern of increasing percentage of teleost prey in the diet has been observed in many pelagic fish species, both mesopredators and top

58 predators, including east Australian salmon (Hughes et al. 2013), mackerel tuna E. affinis (Griffiths et al. 2009) and Pacific bluefin tuna (Thunnus orientalis) (Shimose et al. 2013).

The ontogenetic diet shift also reflects a habitat shift, at ~ 27 cm P. saltatrix move from the estuaries out to the coastal environment (Morton et al. 1993). The smaller fish in the estuaries consumed higher proportions of mysid shrimp, penaeid prawns and estuarine fish (Ambassidae and Gobiidae). This is consistent with previous research that shows P. saltatrix target the most abundant prey within the estuarine environment (Juanes and Conover 1995). The larger fish (> 40 cm FL) from the coastal environment had higher proportions of Sardinops sagax, carangids and Scomber australasicus. Compared to the coastal fish and estuarine juveniles, larger P. saltatrix within estuaries consumed higher proportions of mullet and showed evidence of cannibalism.

The smallest P. saltatrix that showed evidence of piscivory was 5.1 cm fork length, and teleost prey formed the majority of the diet by 8cm (Figure 3.3). This shift is comparable to the population of P. saltatrix in and around the Hudson River in the US, which start to show piscivory between 40 and 70mm total length (Juanes et al. 1993, Juanes and Conover 1994). This pattern is also similar to Arripis trutta – a co-occurring mesopredator in eastern Australia - which show evidence of piscivory in fish as small as 5 cm, although fish did not make up a large proportion of the diet until A. trutta were greater than 20 cm fork length (Hughes et al. 2013).

3.5.2 Latitudinal Variation

Latitude was also shown to influence the variation in P. saltatrix diet and likely reflects the spatial distribution of possible prey types. The taxa that showed the strongest effect of latitude were Sardinops sagax and Hyperlophus sp. Between 30 and 34° S Sardinops sagax was found in higher proportions, and Hyperlophus was more common both north and south of this range. This is likely due to the regional oceanography which will influence baitfish distributions (Scales et al. 2014) ,and thus the diet of P. saltatrix. As P. saltatrix is known to migrate north to spawn (Zeller et al. 1996), it is possible that individuals may exhibit distinct “southern ” and “northern” diets depending on their current location and the availability of baitfish which is driven by the oceanography. Between 30 and 34° S, the warm oligotrophic East Australian Current (EAC) separates from the coast (Godfrey et al. 1980, Cetina-Heredia et al. 2014)

59 forming the Tasman Front which acts as a barrier between the warmer oligotrophic waters to the north and the more eutrophic Tasman Sea waters to the south. This influences the connectivity and dispersal of coastal organisms (Roughan et al. 2011), microbial community composition (Seymour et al. 2012), the size-structure of zooplankton communities (Baird et al. 2008) and the distribution of fisheries such as southern bluefin tuna (Hobday and Hartmann 2006). The EAC separation zone and eddy field (Everett et al. 2012) result in upwelling events (Roughan and Middleton 2002, Everett et al. 2014) which have previously been linked to increased presence of yellowfin tuna due to increased abundance of prey (Young et al. 2001). The shift in diet composition of P. saltatrix in this region is consistent with a previous stable isotope study which found the diets of predatory fish vary between the oligotrophic waters of the Coral Sea and the cooler nutrient-rich Tasman Sea in the same region (Revill et al. 2009). This is similar to South Africa where it has been shown that P. saltatrix may change their diets in relation to changing oceanography and prey distributions rather than move with the changing oceanography (Potts et al. 2016).

3.5.3 Feeding Strategy

P. saltatrix in eastern Australia is an opportunistic predator but is generally piscivorous. This is consistent with previous research into other populations (Buckel et al. 1999). It has been noted that when compared to other co-occuring species in similar niches P. saltatrix can been seen as more specialised (Lucena et al. 2000), whereby P. saltatrix do not consume many types of crustaceans. When compared to the local co-occurring mesopredator A. trutta, P. saltatrix can be seen as more specialised, despite consuming a variety of prey. P. saltatrix relies more on teleost prey than A. trutta (Hughes et al. 2013) despite the species having the same prey availability. The variety of prey types which were observed, combined with the high proportions of the most abundant prey sources (eg: Clupeidae family) suggest that this is an opportunistic predator that will feed upon a wide variety of available fish prey (and crustaceans as juveniles), which is consistent with the feeding strategy observed in some US estuaries (Juanes et al. 1993).

The majority of prey items were pelagic in nature, but demersal prey such as gobies and portunid crabs were also observed. The presence of these demersal organisms (particularly within samples caught within estuaries) suggests occasional foraging near the seabed (Taylor

2008). The high proportion of mysids (which are found in swarms near the benthos) consumed by juvenile P. saltatrix supports the idea of foraging near the seabed. While consuming mysid shrimp, P. saltatrix would be competing with other juvenile species eg: (mulloway; Argyrosomus japonicas) which use mysid shrimp as a prey source (Taylor et al. 2006). The dual feeding on both pelagic and demersal prey reveals its opportunistic feeding strategy, a response to the distribution of available prey sources. A brief study on local dolphinfish Coryphaena hippurus revealed a diet higher in invertebrates and fish associated with drifting clumps of algae, representing the true pelagic nature of C. hippurus (Dempster 2004). While there are no other local mesopredators with dietary studies (except A. trutta discussed above), yellowtail kingfish (Seriola lalandi) in South Africa have been found to have a diet dominated by small pelagic fish including Sardinops sp. and crustaceans such as crab megalopa larvae (Dunn 2014), if this is representative of the Australian population it would show some overlap with both A. trutta and P. saltatrix, which both prey upon Sardinops sagax (Hughes et al. 2013). Although it is also possible that it would have very little overlap as amberjack (Seriola dumerili), another close relative to the Australian yellowtail kingfish (Seriola lalandi), has been found to be only partially dependant on the pelagic foodweb despite being considered a “pelagic” species (Andaloro and Pipitone 1997). Additional information on the Australian species would provide valuable insight into the possible niche partitioning occurring in the region. Small baitfish such as Sardinops sp. and Engraulis sp. are highly important prey sources for mesopredators around the world. While there are no data for the Australian bonito (Sarda australis), the Atlantic bonito (Sarda sarda) is a specialist predator of Clupeiforms (Campo et al. 2006), which would likely have large dietary overlap with the other pelagic mesopredators (including P. saltatrix and A. trutta). It is likely that there is some form of environmental variable controlling the distribution of mesopredators rather than prey availability, as they all prey upon similar fish. These insights highlight the importance of detailed dietary knowledge on a regional scale.

Prey in stomachs that contained multiple prey items were often of the same prey type and stage of digestion. Combined with observations of P. saltatrix viciously attacking schools of baitfish (Bade 1977), this pattern of consumption is suggestive of a “gorging” feeder, tending to selectively target prey species that are aggregated rather than actively hunting single prey items (Hughes et al. 2013). P. saltatrix is known to occasionally regurgitate its stomach contents upon capture (Bade 1977), which likely contributed to the high proportion of empty stomachs observed in this study (67.4 %).

P. saltatrix has extremely strong and sharp teeth which are present at all sizes, allowing prey larger than the predator’s mouth to be bitten into small pieces which can then be swallowed (Bemis et al. 2005). This feeding strategy has previously been noted in P. saltatrix with them being highly aggressive and destructive to prey populations, often biting the tail off and then abandoning the rest of the prey (Bade 1977). The act of ‘chopping’ up the prey was observed in this study with many prey items being found in pieces. Conservative estimates of total prey size may have underestimated the upper bounds of the prey size quantile regression. The pattern of eating larger prey as a predator grows, while continuing to eat small prey, is similar to the predator-prey size relationships observed in other global populations of P. saltatrix (Juanes 2016). This pattern is thought to be a function of increased capture efficiency with increasing predator size, while small prey continue to be an important energetically rich prey source (Scharf et al. 1998). This non-selective feeding behaviour is characteristic of an opportunistic predator and is common in many marine predators (Scharf et al. 2000). Previous work in the northwest Atlantic calculated the relationship between P. saltatrix length and P. saltatrix mouth gape (Juanes et al. 1994). If we compare this relationship with our quantile regression relationships for prey size (Figure 3.4), the mouth gape – fish length relationship roughly matches the minimum prey size quantile and P. saltatrix do not target prey smaller than their mouth gape. The median prey size increases at the same rate as mouth gape, staying approximately 2 cm larger than the mouth gape while the 95th quantile increases at a faster rate than mouth gape increases, suggesting a behavioural change as the P. saltatrix start to aggressively bite larger and larger prey items. The upper size range of prey sizes is lower than is estimated for P. saltatrix in the eastern US (Scharf et al. 2000). This difference in prey sizes may suggest P. saltatrix holds a slightly different trophic position in the east Australian and eastern US ecosystems. A further study could test this hypothesis by comparing trophic position by investigating N and C isotopes from the different populations.

3.5.4 Classification Tree Framework

The classification tree framework successfully provided a non-subjective way of evaluating the importance of each covariate in the model, and identified ‘breakpoints’ in the continuous covariates (fish length and latitude), indicating where a substantial change in the P. saltatrix diet occurred (Figure 3.1, Table 3.1). This is an important improvement over the traditional approach where the breakpoints need to be identified prior to analysis. Both the classification

62 tree and logistic regression identified approximately the same size (8 cm FL) at which piscivory becomes common, indicating the accuracy of the classification tree. A key advantage of using the framework provided by Kuhnert et al. (2012) was the bootstrapping procedure which took into account the dependence between samples from the same catch. The procedure reduced the importance placed upon single catches where all fish had been preying on an overall rare item, which ensures the results aren’t skewed by rare feeding events. In our case only one catch was observed to feed upon octopus but it was found in very high proportions within that catch (9 out of 10 fish).

3.5.5 Conclusion

This is the first paper to examine the diet of P. saltatrix over its entire life-cycle using gut contents. Using a classification tree analysis, we have shown it to be an opportunistic predator with a highly flexible feeding strategy with a preference for common schooling pelagic fish. Variation in diet was most strongly linked to ontogeny and P. saltatrix size, rather than latitude or seasonal effects. Further research would benefit from an analysis of prey selectivity by comparing the distribution and abundance of prey species with the observed consumed prey. These findings are important in light of changing ecosystems, as they show that some pelagic mesopredators, such as P. saltatrix, are highly flexible in their prey sources and may be able to change prey sources if necessary.

4 Evaluating estuarine nursery use and life history patterns of Pomatomus saltatrix in eastern Australia

This chapter has been published in Marine Ecology Progress Series, as part of a special issue on Innovative use of sclerochronology in marine resource management, the reference is:

4.1 Abstract

Estuaries provide important nursery habitats for juvenile fish, but many species move between estuarine and coastal habitats throughout their life. We used otolith chemistry to evaluate the use of estuaries and the coastal marine environment by juvenile Pomatomus saltatrix in eastern Australia. Otolith chemical signatures of juveniles from 12 estuaries, spanning 10° of latitude, were characterised using laser ablation-inductively coupled plasma-mass spectrometry. Based upon multivariate otolith elemental signatures, fish collected from most estuaries could not be successfully discriminated from one another. This was attributed to the varying influence of marine water on otolith elemental composition in fish from all estuaries. Using a reduced number of estuarine groups, the multivariate juvenile otolith elemental signatures and univariate Sr:Ca ratio suggests that between 24 and 52% of adult P. saltatrix had a juvenile period influenced by the marine environment. Elemental profiles across adult (Age-1) otoliths highlighted a variety of life history patterns, not all consistent with a juvenile estuarine phase. Furthermore, the presence of Age-0 juveniles in coastal waters was confirmed from historical length frequency data from coastal trawls. Combining multiple lines of evidence suggests considerable plasticity in juvenile life history for P. saltatrix in eastern Australia by utilising both estuarine and coastal nurseries. Knowledge of juvenile life history is important for the management of coastal species of commercial and recreational importance like P. saltatrix.

Keywords: Otolith chemistry, Elemental profiles, Bluefish, Tailor, Strontium, Barium

4.2 Introduction

Estuaries function as nursery grounds for juveniles of many coastal fish species providing refuge, food and habitat (Beck et al. 2001, Able 2005). Many species subsequently emigrate from estuaries to join adult populations in coastal waters, with the duration of the estuarine life history stage ranging from months to years (Gillanders et al. 2003, Fodrie and Herzka 2008). Assessing connectivity between estuarine and coastal environments is critical for the management of coastal species but is a complex task, due to the constraints and logistical difficulties of mark-recapture studies using juvenile fish. An alternative approach is to use the elemental composition of fish otoliths or other calcified structures which allows insights into how species use estuarine and coastal environments through their life history (Gillanders et al. 2003, Brown 2006, Izzo et al. 2016).

In recent decades, otolith chemistry has become an increasingly popular tool to investigate multiple aspects of fish life history. As fish otoliths are biologically inert and grow continuously, trace elements from the surrounding environment are incorporated on the growing surface of the otolith (Campana and Thorrold 2001). Since water masses are known to vary in their environmental conditions over time and space, fish collected in different environments are expected to have different otolith elemental composition (Campana et al. 2000). These elemental “signatures” or ‘fingerprints” have been used to successfully identify natal origins and nursery estuaries of adult fish (Gillanders and Kingsford 1996, Gillanders 2002a, Vasconcelos et al. 2011, Reis-Santos et al. 2013), discriminate between populations (Rooker et al. 2001, Tanner et al. 2016) and determine mixed stock composition (Munch and Clarke 2008, Geffen et al. 2011).

Otoliths are also used as environmental chronometers of temporal variation in elemental concentrations. Through analysis of elemental profiles from the core to the edge of otoliths, a continuous record of how elements change in concentration throughout the life of a fish may be revealed (Campana and Thorrold 2001). In particular, profiles of strontium and barium have been used successfully in reconstructing environmental and estuary-ocean migration histories for individual fish (Elsdon and Gillanders 2005a, Fowler et al. 2016), as concentrations of these elements are strongly influenced by salinity (Secor and Rooker 2000, Walther and Limburg 2012). If fish movement occurs over a large salinity gradient it is more likely to be detected and hence most research has focussed on migrations between freshwater and marine environments. However, studies reconstructing habitat use and environmental life histories

65 along narrow salinity gradients are becoming more common (Tanner et al. 2013, Williams et al. 2017).

Tailor, or bluefish (Pomatomus saltatrix; Linnaeus, 1766) is a globally distributed pelagic mesopredator which is fished commercially and recreationally throughout its range. Stark differences in life history patterns exist between populations (Juanes et al. 1996); particularly in growth rates and average maximum size (L∞). For example, L∞ in the west Atlantic Ocean is more than double that in the Mediterranean (Ceyhan et al. 2007, Robillard et al. 2009). In general, adult P. saltatrix undertake annual migrations along the coast before spawning at sea with larvae then distributed by ocean currents to downstream areas (Juanes et al. 1996). While larvae recruit to both estuarine and coastal areas in most global populations, in eastern Australia larvae have only been documented to recruit to estuaries (Miskiewicz et al. 1996) where they remain until they emigrate to coastal marine waters at approximately 27 cm fork length (FL; Morton et al. 1993, Zeller et al. 1996), corresponding to approximately 1 year of age (Dodt et al. 2006, Schilling unpublished data). This contrasts with the life history of other populations, namely in the eastern Indian Ocean and western Atlantic Ocean populations which have both coastal and estuarine recruitment (Lenanton et al. 1996, Able et al. 2003, Callihan et al. 2008). It is likely that juvenile tailor in eastern Australia use both estuarine and coastal habitats, and this discrepancy in juvenile habitat use has previously been identified as warranting further attention (Juanes et al. 1996).

Otolith chemistry is an ideal tool to investigate life history plasticity and the use of estuarine and coastal juvenile habitats by P. saltatrix. The broad goal of this study was to use otolith chemistry techniques to gain insight into the life history of P. saltatrix in eastern Australia, specifically estuarine-ocean movements, and to compare these to the life history patterns exhibited by populations elsewhere. Specifically, we tested whether 1) Otoliths of juvenile P. saltatrix from different estuaries had characteristic elemental signatures; 2) Adult P. saltatrix could be assigned to juvenile habitats types based upon the elemental signatures from the juvenile area of their otoliths; and, 3) Elemental profiles from the core to the edge of adult P. saltatrix support movement between estuaries and ocean habitats.

4.3 Methods

4.3.1 Fish Collection

Juvenile Pomatomus saltatrix (n = 360, Age-0) were collected from 12 estuaries along the east coast of Australia over two southern hemisphere summers (2014/15 and 2015/16, Figure 4.1; Supplementary Table 8.4.1). Fish were collected from two haphazardly selected sites at least 1 km apart within each estuary. As P. saltatrix were not found in all estuaries for both years some estuaries only had fish collected from one summer. Fish were collected with baited handlines and frozen prior to dissection in the laboratory.

Adult P. saltatrix (n = 121, Age-1) were also collected from both estuarine and coastal habitats along the east coast of Australia during the 2015/16 summer (to match the 2014/15 juvenile cohort; Table S1). These fish were collected by commercial fishers or donated by recreational fishers. All fish were frozen prior to dissection. To confirm fish were from the correct cohort, the age of all fish were estimated from whole otoliths viewed using a light microscope under water with reflected light. This estimated age was subsequently confirmed after transverse sectioning for otolith chemical analysis (see below) and viewing the section under reflected light (Robillard et al. 2009; Chapter 2). Only fish aged 1 were selected for subsequent analysis. The age at sexual maturity of P. saltatrix in eastern Australia is 1 and it occurs at approximately 27 cm FL (Bade 1977, H. Schilling unpublished data).

Figure 4.1 Map of location of the estuaries where juvenile Pomatomus saltatrix were collected. The dashed lines represent the regions where offshore trawl samples were conducted during the 1990’s. These trawls were conducted at two depths; 5 – 27 m and 64 – 77 m (Graham et al. 1993a, b, Graham and Wood 1997). Each black circle represents the capture location of a 1 year old P. saltatrix used in the elemental profile analysis.

4.3.2 Otolith Element Analysis

To characterise the elemental signatures of P. saltatrix from each estuary, sagittal otoliths were embedded in indium spiked (115In) resin (~40 ppm) and sectioned transversely. The sections were then polished using fine lapping paper and fixed to microscope slides with 115In spiked thermoplastic glue (~200 ppm; Hughes et al. 2016), and subsequently cleaned and sonicated with ultrapure water. Otolith sections were analysed at Adelaide Microscopy (The University of Adelaide) using a New Wave UP-213-nm laser ablation system connected to an Agilent 7500cs inductively coupled plasma-mass spectrometer (ICP-MS). The laser was run using a spot size of 30 µm, at a frequency of 5 Hz and fluence of 7 J cm-2. This corresponded to ~20 days of otolith material. A single spot was ablated on the outer edge of each otolith along the proximal surface, beside the sulcal groove. Spots at the outer edge of the juvenile otoliths were used to characterise the elemental fingerprint of each estuary (i.e. representative of collection site) as this is the material most recently incorporated into the otolith (Elsdon et al. 2008). An inner spot was also ablated on otoliths of adult (Age 1) fish along the same axis as the outer spot, and corresponded to ablation of material accreted when these fish were juveniles. These inner spots were located c. 250 µm from the core, which was the average distance that the corresponding edge spots in juveniles were from the core. The elemental signature of these inner spots should be indicative of the habitat adult fish used as juveniles. The element concentrations measured, and their associated dwell times were 7Li (150 ms), 24Mg (100 ms), 43Ca (100 ms), 55Mn (150 ms), 63Cu (100 ms), 66Zn (100 ms), 88Sr (100 ms), 115In (10 ms), 138Ba (100 ms), and 208Pb (150 ms). 43Ca was used as an internal standard and 115In was analysed solely to detect any contamination by resin or thermoplastic glue.

Otolith sections of 12 adult fish were randomly selected for analysis of elemental profiles from the core to the edge. The profiles were run at a scan speed of 3 µm s-1 using the same instrument settings described above but only for the elements 43Ca, 55Mn, 88Sr, 115In and 138Ba. There is no experimental validation of the relationship between salinity and otolith elemental concentrations for P. saltatrix, so it was assumed that the element:calcium ratios on the edges of otoliths represent capture environment, and the average Sr:Ca ratios of the edges of otoliths from adults collected from coastal marine waters were used as reference criteria for characterising the estuarine or coastal marine environments (Milton et al. 2008). The resulting average Sr:Ca from fish captured in coastal marine environments was 2.18 mmol mol-1. We therefore defined Sr:Ca ratios greater than this value to represent coastal marine environments and any value below this value to represent estuarine or brackish environments.

Ba:Ca thresholds were calculated in the same way but there was no difference between edge otolith Ba:Ca of fish from estuarine and coastal collection areas (Welch Two sample t-test: t28=1.42, p = 0.176), therefore Ba:Ca was not used to characterise environments fish had spent time in.

Periodic ablations on certified reference materials (glass standard NIST 612 and carbonate standard MACS-3) were used to calibrate elemental concentrations, correct mass bias and instrument drift, and to assess external precision. Prior to data collection and before each ablation, background concentrations of elements within the sample chamber were measured for 40 s. A washout delay of 30 s was used between each ablation to allow the chamber to purge and prevent samples becoming cross-contaminated. Raw count data for the spot analyses were processed using the GLITTER software program (Griffin et al. 2008). Profile data reductions were performed manually using spreadsheet software (Microsoft Excel). All elemental data were expressed as ratios to 43Ca (in mmol mol−1) to account for fluctuations in the ablation yield (Munro et al. 2008). In the few cases where data fell below the limit of detection, the raw data were used since substituting values with an arbitrary number has been shown to bias data due to non-random patterns in the distribution of small values (Helsel 2006, Schaffler et al. 2014, Lazartigues et al. 2016).

4.3.3 Statistical Analysis

PERMANOVA and Canonical Analysis of Principal coordinates (CAP) were used to analyse the elemental data, using the PERMANOVA+ for PRIMER software (Anderson et al. 2008). Prior to analysis, the elemental variables in each dataset were normalised and assumptions checked using shade plots which confirmed the equal spread of variance within each dataset (Clarke et al. 2014).

The factors in the PERMANOVA analysis were ‘estuary’ (fixed), ‘year’ (fixed) and ‘site’ (random, nested within estuary), and ‘fork length’ was included as a covariate because otolith chemistry can vary with ontogeny (Beer et al. 2011). Euclidean distances were used to calculate the resemblance matrix. Type I sum of squares was used in the analysis so that the factor ‘estuary’ was fitted to the data after the covariate. Permutations were conducted on residuals under a reduced model, rather than on raw data, to avoid inflated Type 1 error rates associated with

70 covariates in multivariate analyses (Anderson et al. 2008). P-values were generated using 9999 permutations. This PERMANOVA analysis was done on the multivariate (elemental ‘signature’) data as well as univariate element data.

CAP was used to visualise multivariate differences in otolith elemental signatures between estuaries, and to determine how accurately juvenile individuals could be allocated to their collection estuary. The goal of this was to assign juvenile of known estuaries back to area of collection so a full baseline of all estuaries in which tailor may be found in was not necessary. Following initial analysis which found most estuaries could not be discriminated accurately (see results for details), three groups were formed to improve discrimination accuracy. These groups represent the most marine-dominated estuary in NSW (highest salinity; Jervis Bay; mean = 35.0, min = 32.5, max = 36.0, SD = 0.7; CSIRO 1994), the estuary with the largest freshwater input in NSW (lowest salinity; Clarence River; mean = 22.7, min = 5.4, max = 35.7, SD = 9.2; NSW Office of Environment and Heritage 2012) and the ‘other estuaries’ which were a mix of smaller estuaries of variable freshwater input and size (mean = 30.8, min = 6.4, max = 35.7, SD = 3.7; NSW Office of Environment and Heritage 2012).. These three groups were selected as a parsimonious representation of the potential types of estuarine habitat used by juvenile P. saltatrix. CAP allows additional samples to be placed onto the canonical axes of an existing CAP model and to thereby classify each of the new unknown origin samples to an existing group. Using this procedure, the elemental signatures from the juvenile section of otoliths of 121 adult fish were added onto the existing CAP model to identify the most likely nursery origins of the adult fish [i.e. whether they had a marine influenced signature (Jervis Bay) or an estuarine influenced signature (Clarence River or ‘Other Estuaries’)]. Fish that had signatures which placed them outside the boundaries of the current CAP analysis were removed (n = 3) as this suggests that they came from areas that were not characterised in our analysis.

As an additional concurrent univariate analysis, the Sr:Ca values from the spot analyses of the juvenile section of adult otoliths were arranged to visualise the spectrum of Sr:Ca values observed within juvenile regions, aiming at representing sites used by juveniles relative to the 2.18 mmol mol-1 Sr:Ca ratio break between coastal marine and estuarine environments.

Otolith elemental profile data from age-1 tailor were smoothed with a 7 point moving average and plotted relative to distance from the primordium. Fish with similar profiles of both Sr:Ca

71 and Ba:Ca were considered to be representative of different P. saltatrix life histories. Despite no difference in Ba:Ca being observed in our saline estuarine and coastal samples described above, high Ba:Ca values were still interpreted as to be indicative of high freshwater influence.

4.3.4 Historical Offshore Length Frequency Analysis

To provide additional support for the findings from the otolith chemistry analyses regarding habitat use and life history patterns, a re-analysis of historical trawl data was undertaken. This was necessary as the life history understanding in eastern Australia is that juveniles are all restricted to estuaries, this dataset shows that P. saltatrix juveniles have in fact been observed outside estuaries. Length frequency and abundance data for P. saltatrix was compiled from a multi-species dataset from two sets of research voyages conducted by the RV Kapala between 1990 – 1992 and 1995 – 1996. The original aim of the research voyages was to determine the relative abundances and size composition of prawns and associated bycatch species on trawling grounds in the Newcastle and Clarence River regions (Graham et al. 1993a, b, Graham and Wood 1997). The trawls were conducted in coastal waters of two regions, near the Clarence River (Northern NSW; 28.5° – 29.5° S; Figure 4.1) and near Newcastle/Tuncurry (Central NSW; 32° - 33° S; Figure 4.1). Within these regions both inshore (5 – 27 m depth) and offshore (64 – 77 m depth) trawl transects were conducted. The trawling was conducted with three 22 m headline Florida Flyer prawn nets towed in a triple-rig arrangement. Fish were measured onboard the RV Kapala for fork length.

4.4 Results

4.4.1 Juvenile Estuarine Elemental Signatures

Variations in juvenile otolith element:Ca ratios among estuaries were evident (Figure 4.2). For instance, higher Ba:Ca and Mn:Ca were found in otoliths from Clarence River than from the other estuaries sampled. Using multivariate PERMANOVA, significant differences were found between estuaries as well as between sites (nested within estuary; Table 4.1). Fork length as a covariate was also significant. Pairwise tests of estuaries revealed that only some estuaries were significantly different to each other (Supplementary Table 8.4.2). The significant effects of estuary and site show that variation in otolith chemistry of Pomatomus saltatrix could be used for discrimination of groups in some situations. Overall, univariate PERMANOVAs found a significant effect of estuary for Mg, significant site (nested within estuary) effects for Mn, Sr and Ba, and a significant estuary*year interaction for Sr (See Supplementary Table 8.4.3 for full univariate PERMANOVA results).

Table 4.1 Summary of PERMANOVA results for the multivariate analysis of edge otolith elemental compositions of juvenile Pomatomus saltatrix collected in different estuaries. There were >9000 unique permutations for each term in the model.

df MS Pseudo-F P(perm) Fork Length 1 106.46 8.2391 0.0001 Estuary 11 26.595 1.6642 0.0479 Year 1 18.699 2.6345 0.1735 Site(Estuary) 14 13.174 1.9321 0.0012 Estuary*Year 3 10.657 2.3534 0.2458 Year*Site(Estuary) 2 4.159 0.60998 0.6741 Residuals 327 6.8183 Total 359

Figure 4.2 Element:Ca ratios (mean ± 1 standard error) from a spot analysis at the edge of otoliths from juvenile (Age-0) Pomatomus saltatrix collected in different estuaries. All units are in mmol mol-1. Estuaries are arranged by latitude and are abbreviated as followed: Cla = Clarence River, PS = Port Stephens, HR = Hunter River, HB = Hawkesbury River, SH = Sydney Harbour, GR = Georges River, PH = Port Hacking, SR = Shoalhaven River, JB = Jervis Bay, Cly = Clyde River, MR = Moruya River, WI = Wagonga Inlet. These otolith elemental ratios may represent contributions from a variety of sources including the water, diet and other physiological influences.

This study was unable to successfully classify fish to estuaries of capture based on their multivariate otolith elemental signatures (with only 31% of individuals correctly classified), but classification success varied greatly among estuaries (Table 4.2). Classification accuracies for Jervis Bay, Wagonga Inlet and Clarence River were the highest (68.4, 52.0 and 50.0% accuracy respectively), and as Jervis Bay and Clarence River correspond to estuaries with different freshwater flow (highest and lowest salinity), further classification analysis was undertaken (see methods for full justification). Classification analysis using only three groups (Jervis Bay, Clarence River and ‘Other Estuaries’) had an improved overall classification rate of 86%. Individual classification success for each group was Jervis Bay 73%, Clarence River 62% and ‘Other Estuaries’ 89%. While the overall classification accuracy for both the CAP analysis with 12 groups and the CAP analysis with three groups was approximately three times better than random, the higher allocation accuracies from the three group analysis allowed the results to be interpreted in a more biologically meaningful way.

Estuary % Allocated Correctly Clarence River 50.0 Port Stephens 14.3 Hunter River 32.0 Hawkesbury River 31.0 Sydney Harbour 4.4 Georges River 36.7 Port Hacking 20.0 Shoalhaven River 4.8 Jervis Bay 68.4 Clyde River 38.1 Moruya River 21.1 Wagonga Inlet 52.1

4.4.2 Juvenile Life Period Chemical Signatures from Adult Otoliths

Using the CAP analysis, the chemical composition of the juvenile area of each adult’s otolith was used to classify fish to the three major estuary groups (Jervis Bay, Clarence River and ‘Other Estuaries’). A random classification of fish would result in ~33% assigned to each group. Assuming that most estuaries available for P. saltatrix would have signatures similar to the ‘Clarence’ (high freshwater) or ‘Other’ groups, classification of fish from estuarine nursery areas would likely result in more fish assigned to these two groups. However, the majority of the adult fish were classified as having juvenile otolith elemental ‘signatures’ most similar to the ‘Jervis Bay’ group, and thus most resembling the marine environment (51.6 % Jervis Bay, 30.3 % Clarence River and 18.0 % ‘Other Estuaries’). This suggests that both coastal and estuarine environments are important juvenile habitats.

The spot analysis of juvenile regions within the adult otoliths revealed a range of Sr:Ca values (1.46 – 2.84; Figure 4.3). These spots provide a snapshot of the juvenile phase of many fish and also suggest that juvenile P. saltatrix utilise a wide range of salinity environments. 24 % of the spots from the juvenile section of the adult otoliths were above the 2.18 mmol mol-1 ratio marine water threshold for Sr:Ca. This was less than the percentage of spots considered to have a signature most similar to the marine environment from the multivariate analysis (52 %), but is corroborative that a substantial proportion of the fish sampled were influenced by the marine environment during their juvenile period.

Figure 4.3 A visual representation of the continuum of Sr:Ca (mmol mol-1) values observed in the spot analyses of the juvenile section from adult otoliths. The numbers on the x-axis index ranked individual Pomatomus saltatrix. The dotted line shows the calculated threshold between estuarine and coastal waters (2.18 mmol mol-1).

4.4.3 Otolith Elemental Profiles

All elemental profiles of adult P. saltatrix showed elevated levels of manganese at the start (Supplementary Figure 8.4.1), indicating that the profile started at the core of the otolith (Brophy et al. 2004). Distinct shifts in elemental concentration were observed in the profiles of some otoliths. Sr and Ba profiles showed variation between individual fish but four main patterns were evident (Figure 4.4). While over half of the profiles showed a pattern of initially high Ba concentration which then progressively declined along the profile until approximately 350 µm from the otolith core (Figure 4.4b, Figure 4.4c, Supplementary Figure 8.4.2), other fish did not have this initial spike of Ba (Figure 4.4a, Figure 4.4d, Supplementary Figure 8.4.2). Sr concentrations initially declined in all fish (until approximately 350 µm from the otolith core) before subsequently increasing again once (Figure 4.4b, Supplementary Figure 8.4.2) or twice (Figure 4.4a, Supplementary Figure 8.4.2) throughout the life history at approximately 650 and 900 – 1000 µm from the core.

Figure 4.4 Examples of profiles of Sr:Ca and Ba:Ca from 1 year old Pomatomus saltatrix from the core to the edge of otoliths showing different life history patterns. Profiles were created using a 7 point moving average. The dashed horizontal line represents the calculated reference criteria for Sr:Ca in coastal environments based upon the end points of the profiles from adults caught in coastal environments (2.18 mmol mol-1). These otolith elemental ratios may represent contributions from a variety of sources including the water, diet and other physiological influences.

4.4.4 Historical Coastal Trawl Data

The RV Kapala voyages collected 3050 P. saltatrix. The fish ranged in size from 9 to 37 cm FL with the majority being between 11 and 20 cm FL (Figure 4.5), smaller than the age 1 size of 27 cm at which fish would emigrate from estuaries (Morton et al. 1993). These juvenile fish were only caught in the nearshore coastal trawls and not the deeper offshore trawls.

Figure 4.5 Compiled length frequency data of Pomatomus saltatrix in coastal trawls from surveys conducted by the RV Kapala in Central NSW (dashed line; n = 1533) and Northern NSW (solid line; n = 1517) during 1990-92 and 1995-96 (Graham et al. 1993a, b, Graham and Wood 1997). The vertical dotted line represents size at Age-1 when P. saltatrix were previously assumed to emigrate to coastal marine waters (Morton et al. 1993, Zeller et al. 1996).

4.5 Discussion

Pomatomus saltatrix in eastern Australia show greater life history plasticity than previously hypothesised. Otolith chemistry analysis of both juveniles and adults revealed a more complex and variable life history than expected, which highlights the use of both coastal and estuarine environments during the juvenile phase of P. saltatrix in this region. The multiple lines of evidence, including the better than random assignment of fish to estuary of capture, range of Sr:Ca values in the juvenile region of adult otoliths, the evidence of estuary-coast movement in some profiles, and the presence of juvenile tailor in offshore trawls show that, P. saltatrix use a mix of estuarine and coastal areas during their juvenile stage, with some individuals potentially only using coastal habitats as seen in other P. saltatrix populations globally (Lenanton et al. 1996, Callihan et al. 2008). This further highlights the importance of both estuaries and coastal regions as habitats for juvenile fish (Able 2005, Nagelkerken et al. 2015, Sheaves et al. 2015).

4.5.1 Juvenile Otolith Chemistry Differences

The elemental signatures in P. saltatrix otoliths differed significantly among estuaries and among sites within estuaries, indicating that there are inter-individual patterns in habitat use at various spatial scales. The lack of consistent differences between all estuaries concurs with previous research in the region (including for the same set of estuaries), which found differences in the otolith chemistry of Pagrus auratus and Pelates sexlineatus from some but not all estuaries (Gillanders 2002a, Sanchez-Jerez et al. 2002). Estuaries are variable environments, influenced by both terrestrial and marine inputs (Roy et al. 2001), and the consequent variation in water chemistry is often reflected in otolith chemistry (Elsdon and Gillanders 2003, 2004). Water quality and chemistry within an estuary can vary temporally and spatially, and this variability influences the estuarine signatures from the otoliths. Nonetheless, it is not uncommon for otoliths from some estuaries to have similar elemental signatures, particularly in studies with larger numbers of source sites (Gillanders 2002a, Marriott et al. 2016). It is possible that the lack of distinct otolith chemistry signatures between estuaries found in this study is due to P. saltatrix visiting multiple source estuaries. While this study suggests movement of juveniles between estuarine and coastal habitats, previous tag- recapture work suggests there is no evidence for movements between estuaries (Morton et al. 1993). Recapture studies are often biased by high sampling effort in close proximity to release

80 locations (Gillanders et al. 2001). However due to the high popularity of P. saltatrix with fishers, fishing effort in this region is uniformly high, and no tag was returned from an estuary other than the estuary in which a fish was tagged. It is thus considered unlikely that the otolith elemental signature of juvenile P. saltatrix is being influenced by individuals spending time in multiple estuaries.

It is noted that Jervis Bay, the most marine dominated estuary, had the lowest average Sr:Ca ratio in the juvenile otoliths. While there was no significant effect of fish length found in the univariate Sr PERMANOVA (Supplementary Table 8.4.3), the fish from Jervis Bay were, on average, the smallest (Supplementary Table 8.4.1) and there was therefore possibly some size- related intrinsic effects on otolith chemistry here such as ontogenetic changes in diet (Buckel et al. 2004, Engstedt et al. 2012) or differing physiology in small P.saltatrix (Grammer et al. 2017). Indeed, decreases in Ba:Ca and Sr:Ca have previously been demonstrated in P. saltatrix when switching diet from prawns to fish (Buckel et al. 2004). Fish from Clarence River may have had a higher proportion of crustaceans in their diet (due to their small size) than the fish from some of the other estuaries (Schilling et al. 2017), and this may have been reflected by the high Ba:Ca levels found for this group. This pattern, however, was not seen in similarly small fish collected from Jervis Bay conversely suggesting that diet had limited impact on Ba:Ca ratios in this group (Izzo et al. 2018). Nevertheless, these patterns could simply reflect the higher freshwater input in Clarence River compared with Jervis Bay.

Due to the large variation in the otolith chemistry of individual P. saltatrix within all the estuaries sampled, it was not possible to link P. saltatrix individuals to a particular source estuary and we rejected our initial hypothesis that P. saltatrix otoliths have estuary specific elemental signatures.

Within estuary variation has previously been observed in multiple estuaries (Dorval et al. 2005) including some of the same estuaries sampled in this study (Gillanders 2002b, Sanchez-Jerez et al. 2002). There are two possible explanations for the within estuary (site) differences observed in the current study. First, perhaps the highly mobile nature of P. saltatrix may result in groups of individuals spending enough time in different areas within an estuary to pick up different chemical signatures. Alternatively, it is possible that there are multiple distinct P. saltatrix schools within an estuary which do not mix with one another and, thus, pick up different chemical signatures. While juvenile P. saltatrix are pelagic predators (Schilling et al.

2017), and known to roam widely around estuaries (Morton et al. 1993), differences in chemical composition resulting from pollutants have been observed in P. saltatrix within a single estuary (Sydney Harbour; Manning et al. 2017). These spatial differences support the idea that juvenile P. saltatrix are resident enough that the bioaccumulation of chemicals is different between areas within a single estuary and, thus, intra-estuary differences in otolith chemistry could be observed in some circumstances.

4.5.2 Assigning Adults to Estuaries

The ability to assign individual fish back to specific juvenile sites requires a site-specific baseline of elemental fingerprints. To subsequently discern the contribution of individual nursery habitats to adult populations would require a library of otolith chemistry signatures of all potential source sites (Elsdon et al. 2008). While this study did not have such a library, we were able to test the ability to discriminate P. saltatrix source sites using our sampled sites. Although the ability to discriminate individual estuaries based upon juvenile P. saltatrix otolith elemental signatures was generally poor, it was still possible to distinguish between three main groups; ‘Jervis Bay’ (the most ‘marine’ estuary), ‘Clarence River’ (the estuary with the largest freshwater input) and ‘Other Estuaries’ (other estuaries influenced by variable freshwater flows and marine influences). The allocation of signatures from the juvenile section of adult otoliths back to these groups showed that more than half of these fish had juvenile life stage signatures most similar to the ‘Jervis Bay’ group (51.6 %). This indicates that a large proportion of adult P. saltatrix have multi-elemental signatures in the juvenile section of their otoliths that are most similar to those found in juveniles from a marine dominated estuary. The three fish that were unable to be allocated to any of our three groups may indicate that there was a missing juvenile habitat not sampled, if so, it is likely to be another coastal marine group, (possibly a northern group) as our estuary groups encompassed many types of estuaries. We believe it is unlikely that there is another marine group as a previous study showed that the eastern Australian population is a well-mixed stock along the coast (Nurthen et al. 1992). It is likely these three fish (< 2 % of analysed fish) were outliers in the LA-ICP-MS analysis. The univariate analysis of Sr:Ca from the spots in the juvenile section of adult otoliths suggested 24 % of the sampled fish had a significant marine influence in their juvenile life history stage. Combined the univariate (Sr) and multi-element analysis of the spots are in

82 support that a large proportion (24 – 52 %) of fish were subject to high marine influence at the time that portion of the otolith was being laid down.

The sizes of P. saltatrix collected by the RV Kapala from coastal marine waters confirm that juvenile (Age-0, <27 cm) P. saltatrix inhabit coastal marine environments, providing the first documented evidence of juveniles in coastal environments. The presence of juveniles in the coastal marine environment is also consistent with a strong marine-influenced signature in P. saltatrix otoliths demonstrated by the spot analyses in their juvenile section. This re-affirms the suggestion that a large portion of juvenile P. saltatrix spend sufficient time in marine dominated waters to possess a marine influenced signature, either in coastal waters or near the entrances to estuaries where coastal water is present. This is particularly clear in the wide range of Sr:Ca values observed in the juvenile section of adult otoliths. These findings conform with the life history patterns observed in other populations of P. saltatrix worldwide that use both estuarine and coastal nursery habitats (Lenanton et al. 1996, Able et al. 2003, Callihan et al. 2008), and are further supported by our elemental profile analyses.

4.5.3 Elemental Profiles

Our exploratory analysis to determine the suitability of elemental profiles on P. saltatrix otoliths revealed multiple patterns in 1 year old fish. Assuming the general relationship of increasing Sr and decreasing Ba with salinity (Campana 1999, Elsdon et al. 2008), some of the observed patterns correspond to the previously documented life history of P. saltatrix in eastern Australia, that they spawn in marine environments (high Sr and low Ba) before recruiting to estuaries (lower Sr and higher Ba) and then upon a period of time return to the marine environment (rising Sr and lower Ba; Bade 1977, Morton et al. 1993, Zeller et al. 1996). Only 58 % of the fish showed Ba rising to a high level initially, while the remaining 42 % only showed a small or negligible rise, suggesting some fish may never enter the less saline regions of estuaries. While the Ba peaks only encompassed a small time period indicating that lower salinity estuarine use is limited, the higher Ba concentrations are similar to those recorded in previous research on estuarine fish (Milton et al. 2008, Macdonald and Crook 2010). The Sr profiles show numerous spikes during the juvenile phase which suggests movement between estuarine/brackish waters and the coastal marine environments. Overall, results indicate that while some juvenile P. saltatrix recruit to estuarine or more freshwater environments others

83 do not, and they may stay in waters of approximately marine salinity or move between estuaries and the coastal marine environment multiple times. This is consistent with the results from the spot analyses and historical trawl samples discussed above which showed that juveniles are not restricted to estuarine environments. All fish except one (fish 3, Supplementary Figure 8.4.2) were caught in coastal environments and as such the end point of the profiles should represent a marine environment.

Low Ba concentrations at the end of the profile reflecting the marine environment when the fish was caught would be expected, and this pattern was observed. Conversely high Sr concentrations would be expected at the end point of the profiles, and was observed, although there were exceptions. As there is a lag between otolith chemistry and fish movement as new otolith material forms, these two exceptions may be due to recent movement between estuarine and coastal environments (Elsdon et al. 2008). The lag in incorporating elements such as Sr into the otolith can be over 20 days in some species (Elsdon and Gillanders 2005b, Engstedt et al. 2012), which makes it possible that short temporal scale or recent movements between different environments are missed or not fully represented in the elemental profiles.

It is increasingly being shown that otolith chemistry is influenced by numerous intrinsic (e.g. growth and diet) and extrinsic (e.g. temperature, salinity) factors in addition to a simple relationship with water chemistry (Sturrock et al. 2014, Sturrock et al. 2015, Grammer et al. 2017). A recent meta-analysis highlighted this by demonstrating that whilst salinity was the primary driver of both Ba and Sr, Sr was also influenced by factors including the ecological niche, condition, diet and ontogeny of individual species (Izzo et al. 2018). As such it is important to note that factors such as diet may be influencing the Sr:Ca profiles presented here (Engstedt et al. 2012). While experimental validation of the variation in otolith Sr and Ba concentrations is important in order to determine the resolution at which movement between the coast and estuaries (or even within estuaries) can be effectively determined, it is possible to use wild caught fish from known environments to define reference chemical composition thresholds assuming the otolith edge is representative of capture location. Sr:Ca ratios of P. saltatrix from both estuarine and coastal environments have previously been used to generate reference criteria representative of estuarine (3 - 12 salinity; 1.68 mmol mol-1) and coastal environments (~ 35 salinity; 2.2 mmol mol-1) around Chesapeake Bay, USA (Takata 2004). The coastal reference value from this study was similar to ours and suggests that Sr:Ca ratio ~ 2.2 mmol mol-1 is an appropriate reference level for coastal environments. Sr:Ca values lower than

1.68 mmol mol-1 were rarely observed in our study, probably because the salinity in the estuaries sampled in the current study (NSW Office of Environment and Heritage 2012) is rarely as low as those observed in Chesapeake Bay (Takata 2004). The lack of difference in Ba concentrations between the coastal and estuarine caught fish in this study is possibly because the estuarine regions where P. saltatrix were collected were higher in salinity (> 25) than regions where salinity is low enough to produce the high Ba:Ca signal commonly observed in other studies (Macdonald and Crook 2010). Overall, analysis of otolith Sr:Ca and Ba:Ca profiles can be used to trace estuarine-ocean movement in P. saltatrix, and concur with both the spot analyses and re-analysis of historical coastal length frequencies to indicate that the life history of P. saltatrix in eastern Australia is more facultative than previously thought, a finding shared with several studies which have investigated life history patterns in fish (Milton et al. 2008, Gillanders et al. 2015, Condini et al. 2016).

4.5.4 Conclusion

Analysis of the otolith chemistry of Pomatomus saltatrix from eastern Australia revealed a more plastic life history than previously hypothesised. Due to the weight of evidence from the otolith chemistry analysis, we rejected our initial hypothesis that the juvenile life history region of adult otoliths would have characteristic estuarine signatures. This study has shown that P. saltatrix in eastern Australia use both estuarine and coastal habitats as part of their juvenile development. Furthermore, the use of coastal habitats by juvenile P. saltatrix was supported by both otolith elemental profiles and historical length frequencies. These findings further corroborate the applicability of otolith chemistry to evaluate life history patterns and confirm previously undocumented complexity within fish species life histories.

5 Resolving patterns of spawning in tailor (Pomatomus saltatrix) and the implications for connectivity

This biology in this chapter has been published in Marine Environmental Research, the reference is:

The dispersal modelling component is currently under review in Fisheries Oceanography.

5.1 Abstract

Tailor, Pomatomus saltatrix, is an important pelagic mesopredatory fish in eastern Australia and is one of seven major populations of this species around the world. Reproduction patterns of tailor in this region were uncertain with both extended spawning and multiple spawning periods previously being suggested for the population. A survey of gonadosomatic index (GSI; index of spawning potential) across the whole population, found a second distinct spawning period in late summer in NSW in addition to the recognised spring spawning in QLD. Analysis of a recently released historical archive of larval fish abundance also revealed two peaks in larval abundance providing further support for the two distinct spawning periods observed in the GSI analysis. Ovaries were sampled to determine spawning strategy, fecundity and length at 50% maturity (L50). Ovaries displayed asynchronous oocyte development suggesting fish spawn multiple times per season. Fecundity showed an exponential relationship with fish length with estimates of batch fecundity ranging from 99,488 to 1,424,425 eggs per fish. When combined with a length frequency of the population, the majority of eggs were produced by fish <40 cm fork length (FL). L50 was estimated at 30.2 and 31.5 cm FL for male and female tailor respectively, suggesting that raising the NSW minimum legal length (MLL) from 30 cm total length TL to 35 cm TL to match the QLD MLL could significantly improve recruitment. The sex ratio was found to have shifted in the last 40 years to a female dominated population (1.58 females :1 male). An oceanographic particle tracking model revealed that larvae from the different spawning events are dispersed differently, with the late summer spawning period supplying the most recruits to the southern portions of the species distribution. This suggests

86 that the multiple spawning periods have developed through selection to maximum dispersal of larvae.

Keywords: Reproductive biology, sex ratio, fecundity, particle tracking, larval dispersal

5.2 Introduction

Fisheries managers frequently incorporate species-specific reproductive biology into management plans and often do this by the introduction of spatial closures to protect spawning aggregations, or with minimum length limits to maximise the chances of fish reproducing before they can be harvested. It is important that the reproductive biology of individual species, particularly spawning strategies are understood in order to properly protect and manage harvested species (Rowe and Hutchings 2003). Spawning and larval transport are key processes for ecological connectivity and sustainability for harvested fish stocks.

Fish species show a variety of spawning strategies, ranging from a single short annual spawning event to a protracted spawning during which each fish can release eggs multiple times or even continuously. Different strategies have different ecological implications, for example species may concentrate spawning in a single localised event to increase the chance of fertilization or they may spread spawning effort over broad spatial and temporal scales to increase larval survival (Winemiller and Rose 1992). Numerous advantages have been identified for species which spawn over long periods or multiple times within the spawning period. As ovaries can only hold a limited number of eggs, and by spawning multiple times the volumetric ovary capacity can be exceeded (Burt et al. 1988). This strategy also spreads the risk of predation on the larvae over a longer time period and conversely spreads out the impact of the larvae on their prey (Lambert and Ware 1984). Importantly, multiple spawning spreads the risk of spawning the eggs at a time of unfavourable climatic, hydrographic or feeding conditions (McEvoy and McEvoy 1992). It has also been shown that larval cohorts spawned at different times of the year can result in very different population dynamics, in particular growth and feeding can be significantly different between cohorts within the same year class (Scharf et al. 2006, Taylor and Able 2006). Spawning in multiple events can also indicate

87 possible meta-populations within stocks with some portion of the stock spawning in different locations or at different times to others (Stephenson 1999). By quantifying the reproductive patterns of each species, fisheries managers can make better informed management decisions

To quantify the reproductive patterns of fish species, commonly used methods include surveys of histology, gonadosomatic indices (GSI), egg and larval presence, and juvenile recruitment peaks to infer reproductive strategies of species. These methods give good estimates of many aspects of reproductive biology, but they often provide little insight into larval dispersal or the connectivity mechanisms which link the spawned larvae to the observed patterns in juvenile recruitment.

One approach to understanding the connectivity mechanisms of larval dispersal is by using high resolution oceanographic data in biophysical models parameterised with species specific information (Gallego et al. 2007, Hinrichsen et al. 2011). By tracking particles within the biophysical model, it is possible to identify particularly important areas for larval production in terms of transport to juvenile habitats (Everett et al. 2017, Munroe et al. 2018). High resolution hydrodynamic models provide a mechanism to examine the physical factors which shape observed distributions of larvae and settled juveniles. More than 500 biophysical models have been successfully applied in many systems (Nolasco et al. 2018), for example, the Southern Ocean (Fraser et al. 2018), coastal boundary currents (Everett et al. 2017) and seas such as the Mediterranean Sea (Andrello et al. 2013). These models have provided insight into transport mechanisms for a variety of organisms including kelp (Coleman et al. 2011, Fraser et al. 2018), invertebrates (Everett et al. 2017, Munroe et al. 2018) and fish (Paris et al. 2005, Santos et al. 2018).

Pomatomus saltatrix is a globally distributed mesopredatory fish which is heavily fished by recreational and artisanal fishers. P. saltatrix has a variety of common names including tailor, bluefish, elf, shad, tassergal and anchova (Juanes et al. 1996; Figure 2.1). There are seven major populations of P. saltatrix, identified by regional separation, and all these populations show a shared life history in terms of habitat use. P. saltatrix juveniles primarily inhabit estuarine and near-shore coastal habitats before emigrating to mostly coastal habitats as adults (Able et al. 2003, Callihan et al. 2008, Schilling et al. 2018). In all populations, the species undertakes annual migrations to spawning regions where the larvae are transported away by coastal ocean currents (Hare and Cowen 1993, Juanes et al. 1996, Brodie et al. 2018).

However, differences between global populations are evident in the spawning periods and the number of recruitment cohorts. The northwest Atlantic population has 2 spawning periods (in separate locations (Robillard et al. 2008)) which correspond to 2 main recruitment cohorts (Scharf et al. 2006, Callihan et al. 2008). In comparison, the west Indian, east Indian and southwest Atlantic populations have only one recorded spawning period and corresponding recruitment period (Juanes et al. 1996).

The southwest Pacific (eastern Australian) population, which has been the subject of increasing attention due to anecdotal declines in both abundance and size (Leigh et al. 2017), was originally believed to have a single spawning period (Pollock 1984, Zeller et al. 1996). This conflicted, however, with the two distinct cohorts observed in collected larvae and in recruiting juveniles in estuarine environments (NSW SPCC 1981, Miskiewicz et al. 1996) and led to a second undescribed spawning period/location being hypothesised (Miskiewicz et al. 1996). Further egg and larvae surveys in the north of the distribution suggested a single extended spawning period rather than two discrete periods (Ward et al. 2003). While this stock has recently been assessed as being ‘sustainable’ (Litherland et al. 2016), there are still important questions surrounding the reproductive biology and early life history of this population which may influence future management decisions. Currently the stock is managed across two states (New South Wales (NSW) and Queensland (QLD); Figure 5.1) with a combination of commercial catch limits and gear restrictions, minimum legal lengths (30 cm total length (TL) in NSW; 35 cm TL in QLD), possession limits (20 fish) and temporal-spatial closures (1 month around the recognised QLD Fraser Island spawning area).

The overall goal of this study was to investigate the reproductive biology of P. saltatrix in eastern Australia and to evaluate the current protection of this species. Specifically, this study aimed to: 1) quantify the length at 50% maturity, fecundity and sex ratio of P. saltatrix in eastern Australia; 2) combine GSI surveys and an analysis of a national larval fish database to test the opposing spawning period hypotheses proposed by the Miskiewicz et al. (1996) and Ward et al. (2003); and 3) use an oceanographic particle tracking model to investigate larval dispersal from the different spawning events.

Figure 5.1 Map of eastern Australia showing zones where Pomatomus saltatrix were collected for analysis of reproductive biology.

5.3 Methods

5.3.1 Fish Sampling

Tailor (Pomatomus saltatrix) were sampled from the east coast of Australia from 37°S to 24.8°S from July 2014 to December 2017 (n = 4,049; Figure 5.1). As part of a larger study, these fish were sampled from a combination of commercial catches, recreational fishing donations, roving beach surveys and targeted fishing for small estuarine tailor (Chapter 2). Where possible all fish were measured for fork length (FL; 0.1 cm), total length (TL; 0.1 cm) and weight (g). The gonads were removed and weighed to the nearest 0.01 g. Sex and gonad stage was determined macroscopically using the criteria for tailor in Zeller et al. (1996). Latitude and longitude of capture was also recorded. As soon as possible after capture, fish were placed on ice and then frozen prior to processing and analysis in the laboratory. As P. saltatrix is a nearshore species, all fish were captured from marine waters within 2 nm of the coast or within estuaries.

5.3.2 Sex Ratio

To calculate an overall sex ratio, all fish below 23cm FL were removed from analysis due to possible misclassification of sex in fish with immature gonads. This left 3,245 fish. A chi- squared test was conducted using R v3.4.3 (R Core Team 2017) to test if the sex ratio was significantly different from 1:1. To test for changes in the sex ratio since 1977 when the sex ratio of the population was first investigated and a 1:1 sex ratio was observed (Bade 1977), a randomisation test was conducted using the data from the current study. A subsample of 285 fish (the sample size in the original study by Bade (1977)) was randomly taken from the current dataset 2,000 times, and the sex ratio of this subset was recorded and the P-value from a chi- squared test calculated. This randomisation test was done to ensure that a small sample size (like that of Bade 1977) was not likely to indicate a 1:1 sex ratio in the current observed sex distribution. The proportion of samples with a p-value < 0.05 was used to determine the likelihood of the sex ratio being different to 1:1.

Latitudinal differences in sex ratio were tested by conducting chi-squared tests by latitude by using zones (Figure 5.1), defined as southern QLD (north of 27.5°S), northern NSW (27.5°S – 31°S), central NSW (31°S – 34°S) and southern NSW (south of 34°S).

5.3.3 Fecundity

To calculate the relationship between batch fecundity (BF) and fish length, ovaries from a subset of ‘mature’ (Stage 3 – visible eggs, n = 18) and ‘spawning’ (Stage 4 – hydrated eggs, n = 5) female fish were removed and fixed in 10% formalin, before being transferred to 70% alcohol. While the use of preservatives has previously shown to alter egg size and weight (Klibansky and Juanes 2007), the treatment of all ovaries was consistent. Ovary stage was determined by the macroscopic criteria in Zeller et al. (1996). Due to logistical constraints, all fish used for fecundity estimates were caught in waters south of 28°S and few stage 4 ovaries were available for fecundity estimates. To calculate BF for each fish, the entire ovary was weighed to the nearest 0.0001 g and a random subsample (~0.15 g) taken from the ovary and weighed. The eggs in the subsample were separated from one another by immersing a plastic jar, containing the subsample and ethanol, in an ultrasonic cleaning bath (FXP4, Ultrasonics Australia Pty Ltd) for 30 min (Barnes et al. 2013). The separated eggs were then poured into a petri dish and scanned using a flatbed scanner (CanoScan 8600F). The eggs were then counted and diameters measured using ImageJ software v1.48 (Schneider et al. 2012) following the procedure described by Friedland et al. (2005), similar to the approach in (Klibansky and Juanes 2008). The females used for this calculation ranged from 29.1 cm FL to 73.9 cm FL. The size frequency of the samples can be seen in Figure 5.2.

A pilot study of 5 ovaries was used to identify an appropriate number of subsamples, and all subsequent ovaries had 3 subsamples (1 from each of the anterior, centre and posterior of the ovary). Subsampling was done so variation in the density of eggs throughout the ovary was accounted for. All ovaries had multiple replicates so that the BF estimate for each ovary had an associated standard error. If multiple batches of eggs were evident in an ovary, the largest size mode of eggs in each ovary was assumed to represent a single batch of eggs to be shed during one spawning event, and this was the batch used in the calculation of BF. BF (eggs per fish) was calculated using the following equation:

퐵퐹 = (푊푔/푊푆푆) × 푁푠푠 (5.1)

Where Wg is gonad weight (g), Wss is subsample weight (g) and NSS is the number of eggs counted in the subsample.

Proportion of total egg production by fork length was calculated by combining the fitted BF-FL relationship with a representative length frequency for the population (Chapter 2). The representative length frequency used 2 cm bins for FL, therefore this has been carried into this analysis. To ensure an accurate representation of the relationship between FL and proportion of total egg production in terms of the actual population, only size classes greater than the size class of peak abundance (32 cm FL) were used. This controls for minimum legal lengths and data skewing resulting from the fisheries dependent sampling used in generating the length frequency data.

5.3.4 Maturity

Length at 50% maturity (L50) was modelled using logistic regression which was implemented using a generalised linear model with binomial distribution and logit link function in R v3.4.3 (R Core Team 2017). Fish with gonads ≥ Stage 3 based upon Zeller et al. (1996) were classified as mature and fish with gonads ≤ Stage 2 were classified immature. The criteria used (Zeller et al. 1996) was not dependant on season of sampling as fish did not need to have ripe gonads to be classified as mature and therefore, we did not need to restrict the analysis to fish collected in certain months. Fish for which maturity stage was not recorded were not included in the analysis. The samples collected in in this study showed a strong spatial pattern, with no fish in mature condition (visible eggs) collected south of 30.3°S and very few fish ≤ 30cm TL collected north of this point, resulting in the majority of fish > 30 cm TL north of 30.3°S being mature and none south of 30.3°S showing visible eggs. This pattern could confound an analysis of L50, due to the maturation process appearing to differ with location. Therefore, two sets of binomial regressions were conducted. The first set used all the fish available in this study (n = 2,196). The second set of models were run using a subset of the data which removed all fish >25 cm FL and south of 30.3°S (n = 1,640). This removed the confounding effect of large southern fish which did not appear to mature at any length and allowed a more accurate model of L50 to be developed. Male and female fish were modelled separately to calculate population estimates of L50 for each sex.

Bootstrapping was used to calculate 95% confidence intervals for L50. Each model was bootstrapped 10,000 times using the code provided in Harry et al. (2013) which was based upon the method described by (Walker 2005) and implemented using the R packages “MASS”

(Venables and Ripley 2002), “psyphy” (Knoblauch 2014), “boot” (Davison and Hinkley 1997, Canty and Ripley 2017) and “RCurl” (Duncan Temple Lang and the CRAN team 2018).

5.3.5 Historical Larval Fish Surveys

The Australian National Ichthyological Monitoring and Observing database (Smith et al. 2018), was used to identify net tows along east Australia, between 1983 and 2015, that collected P. saltatrix. These tows ranged from 27.4°S to 34.1°S latitude, and 102 tows contained P. saltatrix (Supplementary Figure 8.5.1). Seasonal and monthly abundances (m-3) of P. saltatrix were plotted to evaluate the presence of larvae and possibly identify recruitment cohorts. The database is a combination of various research programs which collected larval fish and therefore the spatial and temporal coverage has patchy resolution, so these data provide only supplementary evidence of patterns in P. saltatrix reproduction. Data from all years were combined and binned into months and Southern Hemisphere seasons to examine seasonal patterns.

5.3.6 Drivers and Patterns of GSI

A gonadosomatic index (GSI) was calculated for each fish using the equation of Zeller et al. (1996):

9 퐺푊 ×10 퐺푆퐼 = (5.2) 퐹퐿3

Where GW is gonad weight (g) and FL is fork length (mm). Using this index allows the results of this study to be comparable with previous surveys of GSI on the same species (Zeller et al. 1996).

For the analysis of GSI, all fish < 23 cm FL were removed from analysis. This was done to remove any fish smaller than the smallest observed mature fish. Fish without gonad weights (only macroscopic stage information) were also removed prior to analysis. A total of 1,437 fish were left for analysis. To identify spawning periods within regions the distribution of tailor was broken up into latitudinal zones, as described above (Figure 5.1). GSI was averaged by month

94 and the monthly mean was plotted with standard error. This division of regions is consistent with the southeast QLD survey of GSI reported by Zeller et al. (1996) and NSW/QLD management border. No difference in monthly GSI was observed between central and southern NSW, so these regions were combined for clarity in the plot. Historical southern QLD GSI data (Zeller et al. 1996), was used to supplement the three months of current GSI data from southern QLD due to logistical constraints on the current sampling.

To identify any environmental drivers of reproduction, a generalised additive mixed model

(GAMM) was calculated with log10(GSI) as the response variable. A range of variables including oceanographic variables have previously been found to be important for both migration of this species (Brodie et al. 2018) and drivers of reproduction in other species (Carscadden et al. 1997, Sims et al. 2004), and therefore a range of physical and oceanographic variables were considered as explanatory variables. These were location of capture (estuarine or ocean), latitude, month, sex, sea surface temperature (SST), Chlorophyll a, Mean Sea Level Anomaly (MSLA), eddy kinetic energy (EKE) and day length. We obtained measurements of monthly SST and Chlorophyll a (OC3) from MODIS-Aqua using NASA's OceanColor Web. MSLA and EKE (derived from altimetry from NASA/CNES (Jason-1 and 2) and ESA (ENVISAT) satellites) were extracted from the Integrated Marine Observing System (IMOS) Data Portal (http://imos.aodn.org.au/imos/). For all satellite products, the data were averaged for a 20 km x 20 km region centred over the continental shelf.

I tested all variables for collinearity (r2 >0.6) and found SST and Latitude were highly correlated, so two models, each with one of the two variables were run and their fit compared. Using the process detailed below I ran a model with spatiotemporal variables (Month and latitude) and a model with only environmental variables. There was no correlation between the other variables. Sex was a categorical variable and all other variables were continuous. Latitude and Month were made into a tensor spline, with latitude fit with a thin plate regression spline, and month with a cyclic cubic regression spline. The ends of the cyclic spline meet, which means a smooth transition between December and January is modelled. A thin plate spline was used for the other continuous variables and were included in a GAMM with a random effect for ‘fishing trip’ (a unique combination of site of capture and date of capture). If linear relationships were found for any variables then the thin plate spline was removed. This factor incorporates any residual dependency of GSI in fish that were captured at the same time (i.e. potentially part of the same school). Model selection was done using manual backwards

95 selection whereby I started with a full model and I progressively removed the variable with the highest p-value in order to minimise the AIC. This model selection resulted in the best model including a tensor spline of Latitude and Month, a categorical variable for Sex, and the random effect of Site*Date. The Environmental variable model used the same variables except included a thin plate regression spline with SST instead of the Latitude*Month term. The best model included s(SST), s(EKE), MSLA and Sex as well as a random effect of Site*Date.

While the GSI values analysed in the GAMM used a value for each fish, to display a summary by month by region, the southern NSW and central NSW regions were combined by averaging as both regions did not display high GSI values at any time.

5.3.7 Particle Tracking

To investigate oceanographic larval dispersal from the identified spawning periods, a particle tracking simulation was run using PARCELS (Lange and van Sebille 2017). This simulation incorporated the velocity fields from an east Australian Regional Oceanographic Model (ROMS; Kerry et al. 2016). The model domain extends from Fraser Island in the north (25.25°S) to south of the NSW/Victoria border (41.55°S) and approximately 1000m offshore, encompassing the EAC system from where it is most coherent to where it separates from the coast and forms an energetic eddy field in the Tasman Sea. The model is eddy resolving, has a 2.5-5km cross- shore resolution and a 5km alongshore resolution, with 30 vertical s-levels. The model simulation covers a 22-year period (1994 – 2016) and has a similar configuration to the 10-year simulation described in Kerry et al. (2016). Although the ROMS simulation is free running, as it is nested within the most recent BlueLink Reanalysis (BRAN3p5; Oke et al. 2013) its boundaries are constrained by observations.

Particles were released every 0.5° latitude on the 100m isobath from 26 – 30°S to encompass all locations P. saltatrix in spawning condition was observed. 100 particles were released from each location every 7 days for 22 years (the duration of the ROMS model). These particles were then subset to only include relevant months based upon the spawning seasons. Using the results from the GSI surveys, the release locations and months were subset to simulate the observed spawning periods. Three spawning events were modelled, a spring QLD (26 – 27.5°S release locations) spawning event, a spring NSW (28.5 – 30°S) spawning event and a late

96 summer NSW (28.5 – 30°S) spawning event. The particles from the 28°S release were not included in either spawning event to provide some spatial separation between groups. The spring spawning event spanned August – December inclusive and the late summer spawning event combined February and March releases, as determined by the GSI surveys.

Each particle included a small Brownian motion walk function which added natural variation to the movement of each particle and ensured no two particles followed the exact same path. The paths of each particle were interpolated using 5min steps based upon the velocity fields from the ROMS model. The model was run using surface velocities as P. saltatrix larvae are found almost exclusively at the surface (Miskiewicz et al. 1996).

As larval growth rates are highly temperature dependant (Houde 1989, Green and Fisher 2004), the duration of tracking for each particle (settlement time) was temperature dependant and estimated using degree-days (DD; thermal constant; Neuheimer and Taggart 2007). With this approach, each particle is assumed to settle when the cumulative sum of daily temperatures experienced by that particle reaches the thermal constant (Everett et al. 2017). Larval growth in P. saltatrix has been shown to be both temperature and size dependant with larvae growing faster in both warmer waters and at larger sizes, resulting in an exponential growth curve in the larval size range (Hare and Cowen 1995, 1997). Growth and temperature data were combined from various sources to estimate a thermal constant for various stages of development. Larvae (2.1mm) hatch from eggs at 39 DD (Deuel et al. 1966), growth from the yolk sack occurs at a rate of 0.039 °C/day until 2.9mm (59.3 DD; Deuel et al. 1966), at which point the growth rate growth changes to 0.003 mm/°C/day which results in an exponential shaped curve with settlement occurring at 500 DD (10.7 mm). This growth rate closely matches observed growth rates in larval P. saltatrix (Hare and Cowen 1995, Juanes et al. 1996). For a typical water temp of 22°C this means larvae will settle after 23 days which matches the observed transition from larvae to juvenile in this species (Hare and Cowen 1994). A settlement time of 500 DD was used as it is just before the transition from larvae to juvenile whereby swimming would become vastly more important than passive drift from ocean currents (Hare and Cowen 1994, Neira et al. 1998). Larval settlement from each spawning event was quantified by finding the percentage of particles which successfully settled in 1° latitude bins. Larvae which were not on the continental shelf (≤ 200m depth) at settlement were considered as mortalities in the analysis. As swimming is not included in the model, estimates of survival are likely to be conservative with actual settlement likely to be higher due

97 to shoreward swimming. Therefore, the estimates presented are conservative lower estimates of settlement but likely fully represent latitudinal transport distance. Larval mortality is known to be highly variable and was not included in this simulation (Houde 1989).

5.4 Results

5.4.1 Sex Ratio

The sex ratio in the sample of 3,245 tailor was 1.58:1 females to males (61% to 39% respectively). This ratio was significantly different from 1:1 with significantly more female fish

2 (χ 1 = 164.67, P = <0.001). All latitudinal zones showed a significant female biased sex ratio (southern NSW P = 0.001; central NSW P = 0.006; northern NSW P < 0.001, southern QLD P < 0.001). The randomisation test using 2,000 resamples of 285 fish from the current database found that 96.7 % of re-samples had a sex ratio significantly different from 1:1. All resamples showed a female:male ratio greater than 1 (Supplementary Figure 8.5.2).

5.4.2 Fecundity

Batch fecundity (BF) estimates ranged from 99,488 eggs for a 39.2 cm Fork Length (FL) fish to 1,424,425 eggs for a 73.6 cm FL fish. There was a strong exponential relationship between BF and FL (Figure 5.2; P < 0.001) in the form of:

퐵퐹 = 58,060푒0.0435퐹퐿

Figure 5.2 Relationship between batch fecundity (±SE) and fork length for female Pomatomus saltatrix. The solid line and circles represent the southwest Pacific (eastern Australia) population and the dashed line and triangles represent the northwest Atlantic population. The northwest Atlantic population points and fitted line were extracted from Robillard et al. (2008) using the “digitize” R package (Poisot 2011) .

The relationship between the proportion of eggs produced and FL for southwest Pacific (eastern Australian) population showed a steep decline, with the majority (64 %) of eggs produced by fish < 40 cm FL (Figure 5.3).

Figure 5.3 Proportion of total egg production by fork length for female Pomatomus saltatrix in eastern Australia. Egg production in each size class was calculated using the BF-FL relationship (Figure 5.2) and the P. saltatrix length frequency distribution in Chapter 2.

5.4.3 Egg Size Distributions

Most eggs observed in Stage 3 (‘mature’) and Stage 4 (‘spawning’) ovaries were between 0.4 and 0.8 mm diameter with the largest observed eggs being 0.95 mm diameter. The median egg size was 0.59 mm diameter. At least one clear mode was visible in all analysed ovaries and the size range of the modes was consistent between subsamples of the same ovary. Some ovaries displayed multiple modes (Supplementary Figure 8.5.3).

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5.4.4 Maturity

No fish above Stage 2 (i.e. with visible eggs) were observed south of 30.3°S. A strong pattern of decreasing GSI with latitude was observed (Supplementary Figure 8.5.4). The smallest mature female fish was 28.2 cm FL and the smallest mature male fish was 26.5 cm FL. When using all fish to model length at 50% maturity (L50), male L50 was 34.4 cm FL (95 % CI: 33.5 – 35.4 cm;

Table 5.1) and female L50 was 36.6 cm FL (95 % CI: 35.6 – 37.8 cm; Table 5.1). When the large immature fish from the southern portion of the distribution were removed, the L50 for males was 30.2 cm FL (95 % CI: 29.4 – 30.9 cm; Figure 5.4, Table 5.1) and the L50 for females was 31.5 cm FL (95 % CI: 30.6 – 32.4 cm; Figure 5.4, Table 5.1).

Figure 5.4 Proportion of mature Pomatomus saltatrix by fork length. The red points and curve represents females and the blue points and curve represents males. The coverage of the datapoints are shown at the top and bottom of the plot. Note the male data points are slightly offset vertically for visual clarity. The horizontal dotted line represents 50% maturity.

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Table 5.1 Length at 50% maturity estimates for each sex. All males and females shows the results using the entire dataset while the “Large Southern Immature Fish Removed” dataset shows the results from the more accurate dataset which excludes fish > 25cm from south of 30.3°S which were never observed to mature.

Group L50 (95 % CI; cm FL) N All Data All Males 34.4 (33.5 – 35.4) 1223 All Females 36.6 (35.6 – 37.8) 1568 Large Southern Immature Fish Removed Subset Males 30.2 (29.4 – 30.9) 996 Subset Females 31.5 (30.6 – 32.4) 1235

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5.4.5 Larval Fish Distribution and Abundance

102 tows collected from 1986 – 2015 contained P. saltatrix larvae (Supplementary Figure 8.5.1) out of a total of 2,991 tows on the continental shelf. They were found in all months except February, July, August and December. Abundances ranged from 0.0005 – 0.17 larvae m- 3 when P. saltatrix larvae were present. The highest abundances were in October with high abundances also observed between March and May (Figure 5.5).

Figure 5.5 Pomatomus saltatrix larval abundance from the Australian National Ichthyological Monitoring and Observing database (Smith et al. 2018), using only tows from on the continental shelf (<200m; n = 102). The numbers above or below each boxplot represent the number of tows which contained P. saltatrix / the number of total tows in each month. Abundance was calculated only using the tows in which P. saltatrix was present. Note the log10 scale on the y-axis.

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5.4.6 Patterns of GSI

As expected, female GSI increased with increasing macroscopic stage from stage 1 (‘immature’) to stage 4 (‘spawning’) before declining in stage 5 (‘spent’) ovaries. Stage 5 ovaries had a low GSI and were rarely observed (Supplementary Figure 8.5.5).

Strong seasonal patterns in GSI were seen in northern NSW and southern QLD (Figure 5.6). A single spring/early summer spawning period (August – December) was observed in both southern QLD and northern NSW. A second late summer spawning period (February – March) was observed in the northern NSW region. The GSI provided no evidence of any spawning activity in central or southern NSW.

Figure 5.6 Mean female gonad index by zones for Pomatomus saltatrix. Different zones are shown in different colours and line types as follows: Southern QLD (north of 27.5°S; orange, dotted), Southern QLD 1996 (north of 27.5°S; blue, dot-dash; from Zeller et al. 1996), Northern NSW (27.5°S – 31°S; green, dashed) and Central/Southern NSW (south of 31°S; pink, solid). Data for central and southern NSW were combined for display as both displayed low GSI values in all months. Note no female fish were sampled from northern NSW in November.

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5.4.7 Drivers of GSI

The GAMM found significant effects of both sex and the tensor spline between latitude and month (P < 0.001). Male fish had significantly lower GSI values than female fish across all months (P < 0.001, Supplementary Figure 8.5.6). The GAMM predicted a seasonal pattern in GSI with a peak occurring in September and October with the spatial extent retreating over time with a southern most observed peak predicted at 27°S in May and June (Supplementary Figure 8.5.7). The Final Model Selection table is provided as Supplementary Table 8.5.1.

The environmental variable GAMM showed also found Males had significantly lower GSI values, GSI values decreased with increased MSLA while also showing non-linear effects of SST and EKE. SST showed a peak at approximately 21.5°C while GSI decreased when EKE was below 0.3. The full model selection table can be seen in

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Supplementary Table 8.5.2.

5.4.8 Larval Dispersal

The larval dispersal simulated by the particle tracking model showed almost exclusive southward dispersal except for 0.03 % of particles from the southern QLD release which were dispersed northward (Figure 5.7, Table 5.2). A high proportion of particles in each spawning period were dispersed offshore, particularly south of the separation zone where the East Australian Current separates from the Australian mainland (Figure 5.7).

The distribution of particles from each spawning event differed with the spring QLD spawning having a higher density of particles settling on the continental shelf than both NSW spawning events (Figure 5.7; Table 5.2). The spring NSW spawning event had the widest dispersal of particles with no high density areas of settlement (Figure 5.7). The late summer NSW spawning event extended dispersal furthest south with moderate dispersal offshore (Figure 5.7).

The spring QLD spawning event had the highest percentage of larvae settle on the continental shelf (20.89 %) with more than double the NSW spawning events of spring and late summer (9.49 % and 8.86 % respectively; Table 5.2). Despite this, the NSW spawning events had proportionally more settled larvae at the higher latitudes (>33°S; Table 5.2). The late summer NSW spawning event was the most important for the southernmost settlement locations (37 – 39°S; Figure 5.8).

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Figure 5.7 Density of particles at settlement time (500 degree days) in 1 degree bins. The black dots show the release location of the particles and the black line shows the 200m depth contour. Panel A) shows the particle distribution for the known spring spawning in southern Queensland. Panel B) shows the particles distribution for spring spawning in northern NSW and panel C) shows the particles distribution for a late summer spawning in northern NSW. Note the non-linear colour scale for density.

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Table 5.2 Percentage of particles settling on the continental shelf in each degree of latitude from the various spawning events. Spring spawning events include August – December and the late summer NSW spawning period includes February and March.

Settlement Latitude (°S) Spring QLD Spring NSW Summer NSW 25 – 26 0.03 0 0 26 – 27 1.61 0 0 27 – 28 4.72 0.0006 0 28 – 29 3.61 0.32 0.47 29 – 30 2.33 0.91 1.42 30 – 31 1.97 1.49 1.66 31 – 32 2.11 1.57 1.64 32 – 33 2.15 1.90 1.09 33 – 34 1.32 1.49 0.90 34 – 35 0.56 0.81 0.65 35 – 36 0.29 0.51 0.35 36 – 37 0.11 0.29 0.27 37 – 38 0.06 0.17 0.36 38 – 39 0.004 0.02 0.06 Total Percentage Settled 20.89 9.49 8.86

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100% 90% 80% 70% 60% 50% 40% 30% 20% 10% Percentage of Settled Larvae of Settled Percentage 0% 26 27 28 29 30 31 32 33 34 35 36 37 38 39 Settlement Latitude (°S) Spring QLD Spring NSW Summer NSW

Figure 5.8 Percentage of settled larvae on the continental shelf (location <200m depth at 500 degree days) originating from each of the modelled spawning events. Each bar represents the total larvae successfully settled in a 1° latitude bin.

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5.5 Discussion

This study showed strong latitudinal and temporal patterns in the reproductive biology of Pomatomus saltatrix in eastern Australia. It also supported the hypothesis of two distinct spawning events, with an initial spawning event occurring between 30°S and 25°S in spring and a second spawning event, described for the first time here, occurring between 28 and 30°S in late summer. The two spawning events are separated by a pause in spawning in January. A shift in sex ratio of the population towards female fish was also found compared with that historically recorded (Bade 1977). Maturity (L50) was revealed to occur at 30.2 and 31.5 cm FL for males and females respectively which is 4 cm larger than 40 years ago (Bade 1977). A particle tracking model which simulated dispersal of larvae from all spawning events highlighted the importance of the late summer northern NSW spawning event which contributed with a large proportion of larvae to the southern extent of the species distribution compared to the spring spawned larvae. This study demonstrates how reproductive biology and particle tracking models can be combined to better understand the dynamics of important fishery species.

5.5.1 Maturity

No fish were observed with macroscopically visible eggs in their gonads from south of 30.3°S, resulting in many large fish south of this latitude with immature ovaries. This suggests that gonad maturation and spawning are tightly regulated by an environmental cue (or cues) which varies with latitude and that such cue(s) are not sufficiently strong to induce the full sexual maturation and spawning gonad development south of 30.3°S. Average water temperatures during spring-summer (the spawning season) in southern NSW (18-23°C) are lower than those of waters further north where spawning has been shown to occur at this time of year (22 – 27°C). It is thus possible that maturation of the P. saltatrix gonads in eastern Australia may depend on water temperatures remaining above a certain critical level for a period of time. The lack of fish displaying mature gonads in the south may indicate skipped spawning or partial migration in this population (Fowler et al. 2016) or a possible metapopulation structure as discussed in section 5.5.5.

After removal of these large immature fish from the maturity model, L50 was estimated to be

30.2 and 31.5 cm FL for male and female fish respectively. This is 4 cm larger than the L50

110 estimated by Bade (1977) and this may indicate that the size at maturity may have increased in response to decreases in fishing pressure on this population in recent decades (Leigh et al. 2017), Alternatively this result could be due to the larger sample size in the current study but we consider this unlikely as very few fish were mature at L50 sizes reported in Bade (1977). The sampling areas of fish included in the maturity analysis in both Bade (1977) and the current study overlapped substantially, the current study included fish 1.6° further south which is a small difference considering the highly migratory nature of P. saltatrix in the region (Brodie et al. 2018). All fish included in both maturity analyses were line caught. The comparable sampling regimes support our finding which highlights how even “conservative” management actions can change the reproductive biology of species if it changes the pressure that they encounter. Reduced length at maturity has previously been observed under circumstances of increased pressure in other species (Sharpe and Hendry 2009, Kodama et al. 2014, Kokkonen et al. 2015). For example, the northern cod population showed a dramatic reduction in age and length at maturity prior to the populations’ collapse in the 1990’s (Olsen et al. 2004).

Currently the legal minimum legal lengths (MLL) in eastern Australia are 30 cm (NSW) and 35 cm (QLD) total length (TL). The size at maturity lies over 30cm total length (~34 cm TL). Increasing the NSW legal MLL to match the QLD MLL (35 cm TL) would help more fish reach reproductive size, potentially increasing recruitment by increasing total egg production as these smaller fish contribute a large proportion of total egg production. This supports a previous recommendation which suggested raising the MLL to 40 cm TL (Leigh and O'Neill 2004), resulting in the QLD MLL being raised to 35 cm TL from 30 cm TL.

The reduced fishing mortality on P. saltatrix could potentially have wider ecosystem consequences. P. saltatrix of legal size (> 30 cm Total Length) primarily prey upon baitfish (Schilling et al. 2017) and if there is a greater biomass of P. saltatrix then the direct predation pressure on baitfish will increase (Hughes et al. 2014). This will also create increased competition with other pelagic mesopredators such as Arripis trutta and Seriola lalandi which share this resource (Hughes et al. 2013, Dunn 2014). While baitfish are not commonly thought of as a limiting resource, it is possible that in some areas they could becoming a limiting resource resulting in localised declines in mesopredator abundance. On the other hand, if baitfish are not a limiting resource then the increased biomass of P. saltatrix could flow up the food chain with increased prey (P. saltatrix) available for higher trophic level predators such as dolphins and sharks. Without accurate biomass estimates of P. saltatrix prey in relation to the

111 biomass requirements of mesopelagic predators including P. saltatrix which are currently only available for Arripis trutta (Hughes et al. 2014) it is impossible to assess the impact that reduced fishing mortality of P. saltatrix will have on the ecosystem as a whole.

5.5.2 Fecundity

The observed positive relationship between batch fecundity and fish length is consistent with that for most other fish species (Barneche et al. 2018). At a given size, fish in the southwest Pacific (eastern Australian) population produce more eggs than fish from the northwest Atlantic population (Robillard et al. 2008). While both populations show a similar pattern of increasing fecundity, the southwest Pacific population matures earlier (31.5 cm FL and ~45 cm FL respectively) and as such begins producing eggs earlier in life. While the original paper by Robillard et al. (2008) did identify that the exponential trend line may not be accurate for the BF and FL relationship in the northwest Atlantic population, all but one data point fell below the southwest Pacific fecundity relationship (Figure 5.2). The fitted relationship of the east Australian population is similar to that observed in the west Indian Ocean (South African) population (van der Elst 1976). The higher fecundity at a given length of the southwest Pacific and west Indian Ocean populations compared with the northwest Atlantic populations may be indicative of the higher mortality in these populations driving earlier investment in reproduction (Jørgensen et al. 2007; Chapter 2). This is also reflected in the length at maturity estimates with the northwest Atlantic population having the length at 50% maturity estimate over 15 cm larger than all other populations of P. saltatrix (Robillard et al. 2008).

Egg production in the P. saltatrix population in the southwest Pacific (eastern Australia) is dominated by the smaller size classes (< 40 cm FL) and this is largely driven by the high mortality rate leading to higher abundances of the smaller fish compared to large fish (Chapter 2). While this contrasts with some research suggesting that larger fish are proportionally more important to fecundity due to the positive non-linear relationship between fish length and fecundity (Hixon et al. 2014, Barneche et al. 2018), it highlights the importance of MLLs that ensure fish reach sizes at which they can reproduce before they can be legally harvested. Catch and release mortality of P. saltatrix in Australia has been shown to be low (8%) which supports the use of MLLs as a management tool (Broadhurst et al. 2012). If mortality on the southwest Pacific (eastern Australian) population of P. saltatrix was reduced, the proportion of eggs

112 produced by the larger fish may increase which could greatly improve recruitment as it has been shown for many species that larger, older fish produce better quality eggs (Barneche et al. 2018). The high proportion of eggs produced by small fish has previously been observed in the west Indian Ocean population (South Africa) of P. saltatrix where the population is also subject to very high mortality (van der Elst 1976).

5.5.3 Sex Ratio

It is likely the sex ratio of P. saltatrix in the southwest Pacific Ocean (eastern Australia) has changed in last 40 years. Bade (1977) found a 1:1 sex ratio for the species. There is now a significantly higher proportion of female tailor (1.58:1) than there was 40 years ago, and a randomisation test showed that there is only a 3.3% chance that a sample size equal to the original study (n = 285) would not have detected a sex ratio significantly different to 1:1 if the sex ratio was consistent with the current population.

This female-biased population is similar to the current west Australian population (east Indian Ocean) where an overall 1.5:1 female:male ratio was also observed between 1991 and 2010 (Smith et al. 2013). Variable sex ratios have been observed in populations of P. saltatrix around the world. The west Indian and the northwest Atlantic Ocean populations show a 1:1 sex ratio (van der Elst 1976, Boreman 1983), although areas such as North Carolina have been identified as having higher proportions of female fish (Lassiter 1962), similar to the female bias observed in the current east Australian population. The Mediterranean population has a female biased population (1.38:1; Ceyhan et al. 2007). The northwest Atlantic population with its 1:1 sex ratio is different from the other populations and this is consistent with the different life history observed in that population which also possesses the lowest mortality and highest proportions of old fish in any P. saltatrix population (Northeast Fisheries Science Center 2015; Chapter 2).

A female biased sex ratio may be optimal in a population as eggs are more energetically demanding to produce and physically larger than sperm. This mean that in an equal sex ratio scenario, it is possible that there is an undersupply of eggs being produced. This could be compensated by having increased numbers of females which would increase the likelihood of successful fertilization.

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The apparent change in observed sex ratios in the east Australian population is unlikely to be driven by sampling as both the original study (Bade 1977) and the current study used the same fishery dependent sampling methods. It is therefore likely that this shift has two potential causes. Firstly, it may be a result of the changing environment in the region. The East Australian region is one of the fastest changing marine environments with it being identified as a global marine warming hot spot (Hobday and Pecl 2014), and this shifted temperature regime may have impacted the sex ratio of P. saltatrix in the region. Environmentally driven sex determination generally affects the newly fertilized egg with the environmental temperature of the egg determining the likelihood of each sex (Conover and Heins 1987). If the changing temperature is driving this shift in sex ratio it would be highly significant because while shifts towards male dominated populations have been observed (Conover and Heins 1987), a shift towards a female dominated population has not been observed in any teleost species as a result of changing environmental temperature (Ospina-Álvarez and Piferrer 2008). Secondly, when fish populations are subject to heavy fishing pressure, as the southwest Pacific (eastern Australia) population historically was, exploitation may drive populations towards a 1:1 sex ratio (Conover and Van Voorhees 1990). Historical fishing may have driven the sex ratio to 1:1 and with the recent reduction in fishing pressure, the sex ratio may be returning to an original female biased ratio. The fact that the northwest Atlantic population of P. saltatrix has a 1:1 sex ratio with low exploitation may suggest that reduced exploitation does not result in more females. It may simply be a natural swing towards more females in a system which is highly flexible including natural fluctuations of the sex ratio. This would be consistent with the more females observed in the north Atlantic population in North Caroline during the 1960’s (Lassiter 1962) and differing sex ratio observed in the 1970’s in the southwest Pacific population (Bade 1977). This shifting sex ratio is a question which deserves further investigation potentially through breeding experiments with temperature treatments to test if temperature influences the sex ratio.

It should be noted that as >95% of my samples were caught using line fishing, it is possible that there is some sampling bias. If males and females have different catchability by line fishing driven by behavioural or habitat differences, then it is possible the female biased sex ratio presented here could be wrong. As our sampling was consistent with the study of Bade (1977) we believe a shift in sex ratio has occurred. The sex ratio of fish caught by haul and mesh nets was 30males:30 females, which is equal but also a very low sample size compared to over 1000 for the line fishing.

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5.5.4 Patterns and Drivers of GSI

This study has documented for the first time a previously undescribed spawning period which occurs in late summer in northern NSW, which is consistent with the hypothesis proposed by Miskiewicz et al. (1996) rather than that of a single extended spawning period proposed by Ward et al. (2003). The current research also extends the previous latitudinal extent of spawning in this species to 30°S (in NSW), spawning was previously thought to be limited to southern QLD, in particular Fraser Island during spring and early summer (Zeller et al. 1996). P. saltatrix larvae were only found in a low number of tows in the historical larval fish database, this is most likely caused by the surface-dwelling behaviour of P. saltatrix larvae. Traditionally many samples for larval fish, sample down to depths of 50 or 100m and do not effectively sample top 1m of water where P. saltatrix larvae are found.

Male fish had significantly lower GSI than female fish and this is expected with eggs being larger and costlier to produce than sperm. This difference in GSI is also seen in the west Indian Ocean (South African) population of P. saltatrix (van der Elst 1976) as well as in other local species such as garfish (Hughes and Stewart 2006). The spatial and temporal variables were the most parsimonious explanation of GSI, and no environmental variables were selected in the best model. This does not mean that the environment does not provide cues, or influence GSI, but rather that these cues are best explained by how they correlate with month and latitude. A strong spatial and seasonal pattern in GSI was observed in the model, which suggests that the fish are responding strongly to their environment; possibly a combination of temperature (as suggested by Ward et al. (2003)), light (Migaud et al. 2010) and/or chemical cues (Stacey 2003). The GAMM which included SST showed that GSI peaked at approximately 21.5°C and declined when EKE was less than 0.3. MSLA also had a significant negative effect with areas with low MSLA generally showed higher GSI. This preferred temperature aligns with abundance which has previously been shown to peak at 21.5°C for this population (Brodie et al. 2018). Despite this, the decline above 21.5°C contrasts Ward et al. 2003 which suggested spawning occurred up to 23°C. It is possible spawning continues about 21.5°C but the model we present suggests that fish are in the peak spawning condition when the SST is 21.5°C.

The final GAMM model which included latitude (Supplementary Figure 8.5.7) produced different visual patterns to the observed GSI in each zone (Figure 5.6). GAMMs with a month

115 variable will naturally smooth across fine scale temporal patterns as seen in the GSI observations. The GAMM could possibly be enhanced with the use of higher resolution weekly data. Regardless the GAMM model shows that the major patterns in GSI are month and latitude.

5.5.5 Larval Dispersal

The particle tracking model revealed that the spring QLD spawning event was highly important for overall population recruitment. This spawning event had the highest percentage of larvae which settled on the continental shelf and were therefore more likely to find suitable juvenile habitat and survive. Conversely, both NSW spawning events were important for recruitment in the southern portion of the species distribution with both spring and late summer NSW spawning events having higher percentages of settlement south of 34°S than the spring QLD spawning. The late summer NSW spawning event had the highest percentage of particles which settled south of 37°S, and it is likely this spawning event drives the recruitment in the southern Australian state of Victoria where commercial catch of P. saltatrix is small and often variable (Litherland et al. 2016). A further analysis of interannual variability and larval dispersal would provide more insight into the drivers of recruitment for the southern portion of the population.

The model also revealed that the spring QLD spawning event produced large numbers of particles that settled north of the East Australian Current (EAC) separation zone before they could be advected offshore. These movement of these particles were often driven by onshore currents which resulted in low velocities and short dispersal distances due to interactions with the land. The greater offshore dispersal evident in the NSW spawning events was driven by the EAC separation zone resulting in high concentrations of particles that were advected offshore at approximately 35°S. This could be examined in more detail by using the paths of individual particles that get advected offshore and entrained into eddies. These eddies are very common along the east coast of Australia, particularly south of the EAC separation zone (Everett et al. 2012). Climate change is driving oceanographic changes in this region with the flow of the EAC intensifying and separating from the coast further south, thus changing particle dispersal patterns (Cetina-Heredia et al. 2014). This has large implications for the larval transport of many species which utilise this western boundary current for dispersal to higher latitudes.

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Indeed, increased dispersal of many species if already being observed with the increasing tropicalisation of some temperate regions as tropical fish larvae are transported further south (Vergés et al. 2014, Vergés et al. 2016).

While this dispersal model can not predict recruitment of P. saltatrix due to the influences of unquantified factors such as mortality, suitable habitat availability and swimming ability of the larvae, to achieve this predictive ability the first step would be to quantify monthly recruitment along the entire east coast of Australia, similar to the quantification of recruitment conducted along the northeast coast of the US (Wuenschel et al. 2012). Once recruitment is quantified, the predictive ability of our dispersal model could be tested and if the predictive ability is high enough it could potentially be used to forecast high and low regions of recruitment.

As P. saltatrix are capable of multiple spawning times in a year, it is highly likely that the same fish spawn in more than one of the spawning events. These multiple spawning events are possibly utilising the seasonal variation in the EAC which creates different larval dispersal patterns from each spawning event, similar to that of herring, Clupea raseragus, in the northwest Atlantic (Lambert and Ware 1984). By having distinct temporal and spatial spawning events the probability of larvae being distributed along the entire southeast coast of Australia is increased. This is highlighted by the different proportional contributions from each spawning event when analysed by settlement latitude. This differential survival has likely produced the two distinct spawning events through selection of surviving larvae based upon the different oceanic transport. The late summer NSW spawning utilises the seasonally stronger EAC and appears highly important for larval supply in the higher latitudes.

Multiple spawning events produce the potential for metapopulations to develop within the stock (Kritzer and Sale 2004). This is also potentially suggested by the presence of non- spawning females in the south during the spawning season. If it is not a case of partially migration and skipped spawning, then it is possible that this is a different metapopulation which has a different unrecognised breeding pattern. While an analysis of tagging data did show complexity within the migration of P. saltatrix there was little evidence of P. saltatrix making multiple spawning movements (Brodie et al. 2018). While an early genetic study found the southwest Pacific (east Australian) population to be a single genetic stock (Nurthen et al. 1992), within stock population dynamics have not been fully assessed, and it is possible that different groups of fish are spawning in the different spawning events, producing cohorts

117 originating from different metapopulations. If this is the case, the single population model currently used to manage this stock may be inappropriate and should be tested, potentially though non-genetic discriminatory techniques such as otolith elemental chemistry and/or shape analysis of spawning fish from from both spawning events, both of which techniques have been shown to effectively discern metapopulations and subpopulation level structure (Wright et al. 2006).

5.5.6 Conclusion

P. saltatrix are broadcast spawners with asynchronous oocyte development capable of multiple spawning events in a year, with GSI surveys and historical larval fish abundances both supporting two distinct spawning periods per year. A previously unrecognised spawning period was identified in northern NSW during late summer, and this period is likely to be key for recruitment of juvenile P. saltatrix in the southern portion of the species distribution, with few larvae from the spring spawning events reaching southern NSW. The results on length-at- maturity indicate that the recruitment of P. saltatrix in eastern Australia could be increased by raising the minimum legal length of P. saltatrix in NSW from 30 cm TL to 35 cm TL, which would match the current QLD minimum legal length.

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6 General Discussion

6.1 Life History Model for Tailor, Pomatomus saltatrix, in Eastern Australia

To bring the research in each chapter together with previous and concurrent research on tailor, Pomatomus saltatrix, in eastern Australia, this chapter will describe the life cycle of the population. This will be followed by a short summary of the life history differences observed in common co-occurring pelagic mesopredators in eastern Australia and between the global populations of P. saltatrix. Some areas of potential further research are identified, both for the east Australian population and globally for this species.

6.1.1 Annual Migration and Spawning

Tagging studies show P. saltatrix greater than 30 cm total length (TL) undertake extensive annual migrations along the east coast of Australia (Pollock 1984, Zeller et al. 1996, Brodie et al. 2018). This migration is driven by season and temperature, with P. saltatrix favouring water 21.5°C (Brodie et al. 2018). While most recorded movements are northward during winter and spring (Figure 6.1), this is probably an artefact of sampling effort due to the heavy fishing pressure around the Fraser Island spawning grounds in the northern region during late winter and spring (Brodie et al. 2018). P. saltatrix return south as the water warms throughout summer and autumn.

Previous research had suggested either a single extended spawning period (Ward et al. 2003) or two distinct spawning periods (Miskiewicz et al. 1996) for P. saltatrix in eastern Australia. The work presented here has found there are two temporally separate spawning periods and it is possible that with migration fish may spawn in multiple events. (Chapter 5). The first is prolonged and extends from August – December, extending from Fraser Island in Queensland (~25°S; QLD) into northern New South Wales (~30°S; NSW). The second spawning period is a previously undescribed shorter spawning event in late summer (February – March) in NSW (27.5 - 30°S). Examination of the size frequency of eggs within ovaries revealed asynchronous development of oocytes and each fish is capable of multiple spawning (Chapter 5). The presence of spawning in NSW means that spawning is occurring in multiple management jurisdictions and may require additional cross-jurisdictional management arrangements in addition to the current 1 month spatial closure on Fraser Island during the spawning season.

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Figure 6.1 A summary of movement for all tagged Pomatomus saltatrix (tailor) in eastern Australia. Movement and direction of recaptured tailor by season. Only movements >48 km (mean recapture distance; n = 250) are included to improve visibility of maps. Arrows indicate the direction travelled, with northerly arrows arching right and southerly arrows arching left. Tailor were recaptured in each season, with 149 (671 total) recaptures in spring, 25 (114 total) in summer, 27 (210 total) in autumn, and 48 (472 total) in winter. Reproduced from Brodie et al. (2018) with permission.

6.1.2 Larval Dispersal and Recruitment

Once spawned, larvae are dispersed south via the East Australian Current (EAC) which is a western boundary current which runs southwards from the Coral Sea along the east Australia until it separates from the coast between 31 – 33°S and into the Tasman Sea (Suthers et al. 2011). The spring QLD, spring NSW and late summer NSW spawning events produce larvae that are dispersed differently by the varying seasonal nature of the EAC (Chapter 5).

Based upon passive drift and temperature dependent growth, larvae from the spring QLD spawning event were shown to have the highest proportion of settlement on the continental shelf (double both NSW spawning events). This is driven by onshore currents and the increased distance from the separation zone compared to the NSW spawning events (Chapter 5), and it is thus very likely that the spring QLD spawning event drives recruitment in the northern half of the species distribution. Larvae from the spring NSW spawning period have the highest proportion of larvae which settle between 33 and 37°S and the late summer NSW spawned larvae provide most of the larvae settling south of 37°S. By spawning multiple times, P. saltatrix maximise the latitudinal dispersal of their larvae (Chapter 5).

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6.1.3 Juvenile Phase

Juvenile P. saltatrix recruit to both estuarine and coastal habitats at ~3 cm length (~30 days old) and are not restricted to estuarine environments in eastern Australia as previously thought (NSW SPCC 1981, Miskiewicz et al. 1996). Recruitment occurs in two main cohorts, arriving in summer (from the spring spawning) and autumn (from the late summer spawning; NSW SPCC 1981).

Both tagging studies and otolith chemistry analyses have shown juvenile P. saltatrix to be highly mobile within estuaries (Morton et al. 1993, Schilling et al. 2018). While otolith chemistry can not consistently discriminate juveniles from different estuaries, it was possible to discriminate between different salinity environments (freshwater, estuarine and marine; Schilling et al. 2018). Elemental transects of Sr:Ca and Ba:Ca within otoliths showed movement of individuals between environments of varying salinity, possibly in and out of estuaries during the 1st year of life (Schilling et al. 2018).

The diet of newly recruited P. saltatrix consists primarily of mysid shrimp and small fish from the family Gobiidae (Schilling et al. 2017). Once the recruits reach approximately 8 cm fork length (FL), the diet shifts to a mixed crustacean and fish diet with the dominant prey items being penaeid prawns, anchovies and sprats (Schilling et al. 2017). Overall, the proportion of fish in the diet increases with fish size (Figure 3.3).

As juveniles, P. saltatrix have considerable ecosystem impact due to their consumption of large numbers of prawns and small fish. Using respirometry and calorific content experiments, it was calculated that juvenile P. saltatrix consume over 20 times their own body weight annually (Lawson et al. 2018). In terms of magnitude, in Sydney Harbour, this equates to a maximum daily consumption of almost 500 kg equating to an annual 77 tonnes year-1. To put this into perspective, this is larger than the entire estimated summer recreational fishing harvest from Sydney Harbour or double the historical commercial harvest (Lawson 2016).

This high consumption rate results in a fast linear juvenile growth rate (~0.8mm day-1), reaching ~25.5 cm FL after just 1 year (Chapter 2).

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6.1.4 Maturity and Entrance to the Fishery

At approximately 27 cm FL, juvenile P. saltatrix join the coastal adult population (Morton et al. 1993) and reach 50% maturity at 30.2 and 31.5 cm FL for males and females respectively (Chapter 5). At 30 cm FL the diet of P. saltatrix also shifts to a fish dominated diet comprised mostly of sprats, anchovies and small carangids (Schilling et al. 2017). While this work found no apparent asymptotic length for P. saltatrix due to the lack of old fish in the population, growth continues at between 10 – 15 cm FL per year (Chapter 2). Adult tailor undergo seasonal migrations along the coast to spawning areas (Brodie et al. 2018), and although genetic work has previously determined the population to be of a single stock (Nurthen et al. 1992), there is the possibility of meta-populations within this stock due to the presence of multiple spawning events (Chapter 5).

The current minimum legal lengths for P. saltatrix in eastern Australia are 30 cm total length (TL) in NSW and 35 cm TL in QLD (Leigh et al. 2017). This corresponds to approximately 27 and 32 cm FL respectively, and results in 50 % maturity occurring after the entrance to the fishery in NSW and before entrance to the fishery in QLD.

6.1.5 Mortality and Age Structure

In eastern Australia, P. saltatrix are harvested by various methods with the most popular being line fishing for both recreational and commercial fishers. The size structure of harvested tailor is dominated by small fish (<45 cm FL) , which is assumed to be representative of the population. The population is dominated by young fish with very few fish older than 4 years old (Chapter 2) and therefore shows signs of age class truncation. This is due to the high mortality rate which results in ~80% annual mortality. Natural and fishing mortality have approximately equal contributions to the total mortality rate (Chapter 2).

While there are bag limits for fishers (20 fish in QLD, 10 fish in NSW), tailor in eastern Australia have low catch and release angling mortality (8%; Broadhurst et al. 2012) and total mortality rates could likely be substantially decreased by reducing the bag limits, increasing the minimum legal lengths and encouraging more catch and release fishing.

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6.2 Comparison with Other Local Mesopredators

The waters off eastern Australia support a diverse range of mesopredators. From reef associated snapper (Pagrus auratus) to fully pelagic dolphinfish (Coryphaena hippurus) and small tuna (Thunnus alalunga). Locally, P. saltatrix is important as both an ecological and fishing species. While there are species which occupy similar niches to P. saltatrix in the region, there are differences between the species. Within the pelagic guild, the most similar species are Australian salmon (Arripis trutta), kingfish (Seriola lalandi), bonito (Sarda australis), dolphinfish (C. hippurus).

Australian salmon (A. trutta) occupy the most similar trophic niche to P. saltatrix and are commonly found at the same sizes at similar locations (although at different times of the year). While A. trutta grow slower and reach a smaller maximum size they have the same juvenile life history. Juvenile A. trutta recruit to estuaries, bays and nearshore environments before joining a coastal population which undertakes annual migrations following the annual expansion and contraction of the East Australian Current. A gradual northward migration with size and age has also been observed (Hughes et al. 2016). Maturity and diet are also similar with shifts in diet occurring at similar sizes to P. saltatrix (Hughes et al. 2013). Despite this, A. trutta and P. saltatrix are rarely observed at the same time due to the cooler temperature preference of A. trutta compared with P. saltatrix. As P. saltatrix avoid the cool water, A. trutta prefer it.

While research into the life history of Australian bonito (S. australis) is sparse, it has been shown that they grow faster than P. saltatrix, reaching maturity at ~40 cm TL, during the first year (Stewart et al. 2013). It is also hypothesised, based upon tag-recapture data and lack of observed spawning condition fish, that the largest S. australis move away from the inshore coastal areas off NSW during spring/summer and that these fish spawn during that time (Stewart et al. 2013). While there is no dietary information for S. australis, a closely related species Sarda sarda have a clupeoid dominated diet (Campo et al. 2006) and it is likely that S. australis share a very similar diet to most of the other pelagic mesopredators in eastern Australia, with a prey preference of small pelagic baitfish. The offshore movement of spawning adults differentiates the life history from P. saltatrix which spawn in near coast areas.

Kingfish (S. lalandi) are abundant schooling pelagic fish often observed near reefs. Abundance of S. lalandi has been shown to peak at 22.5°C Sea Surface Temperature (SST) and shows a positive relationship with sea surface height (Brodie et al. 2015). While there is no local diet

123 information available for S. lalandi, it is highly likely that their diet shows high overlap with both A. trutta and P. saltatrix as in south Africa the diet of S. lalandi is dominated by Sardinops sp. and crustaceans, prey consumed by both A. trutta and P. saltatrix. The growth rate of S. lalandi is also fast with no observed asymptotic length, similar to P. saltatrix in the region (Stewart et al. 2004), compared to P. saltatrix the growth rate is faster with larger size at each age.

C. hippurus (dolphinfish) are a fully pelagic species which prefers warmer water with abundance peaking at 24.5°C SST (Brodie et al. 2015). While also data deficient in the eastern Australian region, it is believed they have extremely fast growth reaching almost 1m in the first year but rarely surviving more than 3 years (Figure 1.2; Schwenke and Buckel 2008). The diet of C. hippurus reflects the true pelagic nature, with their diet being dominated by invertebrates and fish often associated with drifting clumps of algae, suggesting they use floating objects as attractants for prey (Dempster 2004). This behaviour is exploited by local fisherman through the use of Fish Aggregation Devices (FADs) which attract the dolphinfish (Brodie et al. 2017).

While the species discussed above are all commonly observed in coastal waters off eastern Australia, there is distinct niche separation. P. saltatrix and A. trutta are coastal associated but P. saltatrix prefer warmer water than A. trutta which have a more southern distribution. S. lalandi, S. australis and C. hippurus are more pelagic with C. hippurus being truly pelagic and rarely encountered near the coast and also preferring warmer water. S. australis also move between coastal and pelagic habits, possibly as part of spawning migrations. A more detailed examination of the ecological links, such as niche separation and potential competition, between the pelagic mesopredators in the eastern Australian region will require more species specific knowledge as many of these species are lacking in biological knowledge, particularly in terms of early life history and diet.

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6.3 Comparison to Other Pomatomus saltatrix Populations

P. saltatrix shows a similar life history between the different global populations. The main differences occur in reproductive patterns and mortality rates.

Female size at 50 % maturity (L50) ranges from 25.0 cm TL in the west Indian Ocean population (van der Elst 1976) to 48.0 cm TL in the northwest Atlantic population (Robillard et al. 2008).

Female L50 is 29.2 cm TL in the east Indian population (Smith et al. 2013), 36.6 cm TL in the Mediterranean (Villegas-Hernández et al. 2015), 38 cm TL in the east Atlantic population (Champagnat 1983) and 35.0 – 39.9 cm TL in the southwest Atlantic (Haimovici and Krug 1996).

The southwest Pacific (eastern Australian) population is in the middle with a female L50 of 31.2 cm FL (equivalent to 34.6 cm TL; Chapter 5).

Growth rates for P. saltatrix have been calculated for all populations using otoliths (except the east Atlantic and southwest Atlantic populations) and are similar with most populations reaching ~25 cm FL at age 1 and continuing to grow approximately 10 – 15 cm year-1 subsequently (Chapter 2). While the growth rates for the east Atlantic (northwest African) and southwest Atlantic (South American) populations is similar these estimates were generated using different methods to the other studies (length frequency data as opposed to otoliths) and should be used with caution (Champagnat 1983).

While the growth rate of the various global populations is similar, mortality rates and age structures vary among populations. The northwest Atlantic population has the lowest mortality rate and this is reflected in the high proportion of older (>5 year old) fish captured as part of the fishery (Chapter 2). Fish this old are rare in all other populations (with the possible exception of limited data from the east Atlantic population). Natural and fishing mortality are both low in the northwest Atlantic population compared with the other populations and this is potentially linked to the larger L50. Fish in this population are under less evolutionary pressure to reproduce quickly compared to other populations, all of which were very heavily exploited in the 20th century and may have been driven to earlier reproduction (van der Elst 1976, Leigh et al. 2017). The southwest Pacific (eastern Australian) population has the highest instantaneous total mortality rate (1.62; ~80 % annual mortality) compared with the other populations and it has a population dominated by young fish (<3 years old). A population dominated by young fish is consistent with all other global populations except that in the northwest Atlantic (and potentially the east Atlantic).

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Adult P. saltatrix in all populations show coastal migrations to spawning areas where larvae are spawned and then distributed by ocean boundary currents (van der Elst 1976, Hare and Cowen 1993, Juanes et al. 1996, Brodie et al. 2018). These larvae settle in coastal and estuarine habitats in all populations. The northwest Atlantic, east Atlantic, southwest Pacific (eastern Australian) and east Indian ocean populations have been shown to have two spawning periods (Champagnat 1983, Robillard et al. 2008, Smith et al. 2013). The western Indian, Mediterranean and southwest Atlantic populations have only a single spawning peak (van der Elst 1976, Haimovici and Krug 1996, Ceyhan et al. 2007). These spawning patterns result in each population having one or two recruitment cohorts. Two cohorts have been observed in all populations with two spawning periods (NSW SPCC 1981, Callihan et al. 2008, Smith et al. 2013).

Diet is consistent in all populations with juveniles preying upon crustaceans before transitioning to fish with increasing size (Juanes and Conover 1994, Lucena et al. 2000, Harding and Mann 2001, Szczebak and Taylor 2011, Schilling et al. 2017).

6.4 Future Research

This work presents a comprehensive investigation of P. saltatrix life history in eastern Australia and will inform sustainable management of the population. There are however, several areas of further research which would provide insight into more specific aspects of the ecology of P. saltatrix. Some of the key questions which remain:

Mortality rates, particularly natural mortality (M), differ between populations. I believe this could be confirmed through food web analyses which would show that P. saltatrix occupy a relatively higher trophic position in the northwest Atlantic population and that this population is under less pressure from predators than the other populations.

A lab experiment validating the uptake and incorporation of elements into P. saltatrix otoliths would allow elemental transects within otoliths to be used more quantitatively to reconstruct migration histories of this species. This would shed further light on the plasticity in juvenile life histories possessed by tailor in this region (Schilling et al. 2018) and allow otolith chemistry to be used confidently in other populations of P. saltatrix.

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Limited data are available for the eastern Atlantic population in northwest Africa. All primary sources found for this population were over 30 years old and not accessible to many people (in French). Further research on this population including current assessments of growth, age structure and maturity would greatly enhance the global comparison of this species

It was hypothesized in a recent stock assessment that interannual variation in recruitment may have been a key cause of the decline observed in the eastern Australian P. saltatrix population which is now improving (Leigh et al. 2017). Analysis of the particle tracking model presented in this work could be extended to test for differences in larval dispersal over the last two decades in terms of oceanographic changes to test this hypothesis.

The shifted sex ratio observed in the eastern Australian population of P. saltatrix should be investigated using a laboratory experiment with controlled temperature treatments. This would test whether the warming water which has been documented in the region (Hobday and Pecl 2014) is driving the shift towards a female dominated population. An example lab experiment would be keeping groups of P. saltatrix at different temperatures (18°C, 21°C, 24°C, 27°C) while they spawn and investigating the sex ratio at each temperature. Nothing is known about sex determination in P. saltatrix but increases in temperature have been linked to increased proportions of males in other species (Conover and Heins 1987, Ospina-Álvarez and Piferrer 2008).

Large tailor are occasionally reported in St George’s Basin which is an intermittently open lake in southern NSW (35°S). We acquired a large individual (93 cm FL, 103 cm TL) from this location and determined it to be an outlier to the general population as it showed immature ovaries, despite being > 100 cm total length and at an estimated 14 years old was double the maximum age of all other fish aged in this population (7 years; Chapter 2). I hypothesise that juvenile tailor which periodically recruit to this estuary (Chapter 5), are subsequently unable to emigrate to marine waters as they may be unable to locate the very small estuary entrance to the coast or the entrance may be closed. They are therefore resident in an estuary with abundant food, no natural predators and reduced fishing pressure (St George’s Basin has been a Recreational Fishing Haven since 2002). This could be tested by acoustically tagging tailor within the estuary or investigating the otolith chemistry of some of the large tailor caught within the estuary to provide evidence that individuals present in the estuary never leave.

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6.5 Concluding Remarks

This thesis provides the first comprehensive scientific study of east Australian P. saltatrix in over 40 years. With recent concern for the population in eastern Australia, this research comes at a critical time and will be vital for future management of the population as it continues to be harvested both commercially and recreationally.

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8 Appendices

8.1 Supplementary Material for Chapter 1

Supplementary Table 8.1.1 Management measures applied to the tailor in eastern Australia, specifically Queensland (Qld) and New South Wales (NSW) waters. Taken directly from Schilling et al. (2019) and Leigh et al. (2017) with permission. Data originally sourced from state government legislation.

Date State Measure 1877 Qld Minimum legal weight 6 ounces 1877 – 1974 Qld Various measures relating to fishing gear and practices; e.g., mesh size, net length, allowed species, closed seasons, power of inspectors 1887 QLD Minimum legal weight 8 ounces (Queensland Fisheries Act 1887) 1902 – 1994 NSW Various measures relating to fishing gear and practices; e.g., mesh size, net length, closed seasons, prohibition of explosives and poisons 1914 Qld Minimum legal size 10 inches total length (The Fish and Oyster Act of 1914) 1957 Qld Minimum legal size 12 inches total length (Fisheries Act 1957) 16 Dec 1976 Qld Minimum legal size abolished (Fisheries Act 1976) 8 Mar 1990 Qld Minimum legal size 30 cm total length (Amendment of Fisheries Organization and Marketing Regulations 1990) 1 Sep 1990 Qld Seasonal fishing closure on Fraser Island between 400 m north of Waddy Point and 400 m south of Indian Head for the month of September 11 Jun 1993 NSW Minimum legal size 30 cm total length (Fisheries and Oyster Farms Act 1935 – Regulation no. 199, 1993) 11 Jun 1993 NSW Recreational bag limit 20 fish (Fisheries and Oyster Farms Act 1935 – Regulation no. 199, 1993) 1995 Qld Closure to commercial net fishing of many beaches around populated areas; most of Moreton Bay (all of Moreton Bay at weekends); Great Sandy Strait at weekends; and the eastern (ocean beach) shore of Fraser Island from 1 April to 1 September 1 Sep 2001 NSW Commercial net fishing ban, except for incidental catch up to 100 kg per fisher per day taken using ocean hauling nets and 50 kg per fisher per day using any other nets, in the Ocean Hauling and Estuary General Fisheries 1 May 2002 Qld Recreational bag limit (in-possession limit) 20 fish; 30 for fishers staying on Fraser Island for 72 hours or more 1 May 2002 Qld Total allowable commercial catch (TACC) 120 t, except for incidental catch up to 100 kg per fisher per day 1 Aug 2002 Qld Seasonal fishing closure on Fraser Island extended to cover both August and September 1 Sep 2003 Qld Closure to commercial net fishing on Fraser Island between Tooloora Creek and the northern end of North Ngkala Rocks from

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1 April to 1 September (already closed the rest of the year in 1995) 20 Sep 2003 Qld Closure to commercial net fishing on northern beaches of North Stradbroke Island from 20 September to 1 April 1 Mar 2009 Qld Marine Parks (Moreton Bay Zoning Plan 2008 closed many areas near Brisbane to fishing where tailor were commonly caught 1 Mar 2010 Qld Minimum legal size increased to 35 cm total length, bag limit (in- possession limit) set at 20 (no variation for extended stay on Fraser Island 12 Sep 2014 NSW Bag Limit (daily limit) reduced from 20 to 10; in-possession limit (home freezer limit) remains 20

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8.2 Supplementary Material for Chapter 2

Growth curves for separate sexes

1mm 1mm

Supplementary Figure 8.2.1 A comparison of a single otolith showing the a) whole and b) sectioned methods of reading Pomatomus saltatrix otoliths from eastern Australia. This is the same otolith in both images (6 increments). From the core to the edge, the red marks indicate the core, each incr ement and the edge of the otolith. Interpretation of the otolith increment macrostructure were done according to the fish ageing protocols for the Fisheries Queensland Fish Ageing Facility (Department of Primary Industries and Fisheries, 2007, 2008). Whole otolith readings were completed by a qualified single reader; that is, they had recently passed a competency test on a reference collection at the Fisheries Queensland Fish Ageing facility (Department of Primary 152 Industries and Fisheries, 2007, 2008). Readers must exceed a set level of precision and bias for increment count and edge type (Department of Primary Industries and Fisheries, 2007, 2008).

Supplementary Figure 8.2.2 Fitted Schnute growth curves for Pomatomus saltatrix in eastern Australia by sex. The black line shows the fitted model for both sexes combined. The red line shows the fitted growth curve for only female fish (a = 0, b = 2.60, size at age 1 = 26.36, size at age 3 = 41.49), and the blue line shows the fitted line for only the male fish (a = 0, b = 2.44, size at age 1 = 25.15, size at age 3 = 40.36).

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1mm

Supplementary Figure 8.2.3 A comparison of the otolith from the exceptionally large P. saltatrix from St George’s Basin showing the a) whole and b) sectioned methods of reading Pomatomus saltatrix otoliths. From the core to the edge, the red marks indicate the core, each increment and the edge of the otolith. Note the thickness of the whole otolith making the increments very hard to observe.

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Supplementary Figure 8.2.4 Fitted Schnute 3 growth curve for Pomatomus saltatrix in eastern Australia including the large outlier. The black line shows the fitted growth curve for the population using the fitted values (a = 0, b = 2.49, size at age 1 = 25.46 cm, size at age 4 = 46.3 cm).

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Supplementary Table 8.2.1 Growth models used in the model selection process to find the best fitting model for Pomatomus saltatrix growth in eastern Australia.

Growth Model Equation Parameters Full Model AICc Full Model ΔAICc Juvenile Model Juvenile Model AICc ΔAICc Y(t) =length at age t 527.02 3.85 k = Brody growth Von Bertalanffy coefficient −푘(푡−푡0) (Beverton and 푌(푡) = 퐿∞(1 − 푒 ) t =age 20326.55 161.79 Holt 1957) t0 = age at size 0 L∞ = average maximum length Y(t) =length at age t 527.84 4.67 t =age Linear 푌(푡) = 푚푡 + 푏 20343.04 178.28 b = intercept m = gradient of slope Y(t) =length at age t 523.17 0 퐿 t =age 푌(푡) = ∞ ⁄ −푘(푡−푡0) Logistic (1 + 푒 ) L∞ = average maximum 20410.03 245.27 length t0 = age at size 0 Y(t) =length at age t 528.62 5.45 t =age c = curvilinear Power 푌(푡) = 푑 + 푑푥푐 20178.95 14.19 0 parameter d = growth parameter d0 = intercept Model did not NA Schnute variation 1⁄ converge 1 − 푒−푎(푡−푇1) 푏 1 (a≠0, b≠0) ( ) 푏 푏 푏 20386.47 221.71 푌 푡 = [푦1 + (푦2 − 푦1 ) −푎(푇 −푇 )] (Schnute 1981) 1 − 푒 2 1 Y(t) =length at age t t =age Schnute variation a = growth parameter 524.55 1.38 2 (a≠0, b=0) −푎(푡−푇1) b = growth parameter 푦2 1−푒 [log( ) −푎(푇 −푇 )] (Schnute 1981) 푦2 1−푒 2 1 T1 = Arbitrary age 1 20378.06 213.3 푌(푡) = 푦1 푒 equivalent to T2 = Arbitrary age 2 (Gompertz 1825) y1 = size at T1 Schnute variation Model did not NA 1 y2 = size at T2 3 (a=0, b≠0) 푡 − 푇 ⁄푏 converge 푏 푏 푏 1 20164.76 0 (Schnute 1981) 푌(푡) = [푦1 + (푦2 − 푦1 ) ] 푇2 − 푇1

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Schnute variation 푦 푡− 푇 [log( 2) 1 ] 4 (a=0, b=0) 푦 푇 − 푇 20492.24 327.48 푌(푡) = 푦1 푒 1 2 1 (Schnute 1981)

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Supplementary Table 8.2.2 Summary of published von Bertalanffy growth curve estimates for the populations of P. saltatrix. k, L∞ and t0 are parameters in the von Bertalanffy growth equation.

-1 Region k (yr ) L∞ (cm) t0 (yr) References Northwest Atlantic 0.311 81.5 -0.30 Robillard et al. (2009) Mediterranean 0.150 88.3 -1.43 (Cengiz et al. 2013) Recalculated from Eastern Atlantic 0.214 104.3 -0.05 Champagnat (1983) West Indian 0.094 124.7 -2.09 Govender (1999) East Indian 0.464 59.2 -0.10 Smith et al. (2013) Southwest Atlantic 0.387 66.2 0.32 Haimovici and Krug (1996) Southwest Pacific NA NA NA This study von Bertalanffy growth curve parameter estimates are not given here for the southwest Pacific population due to this study finding that the growth model is not appropriate for this population. Some populations show large t0 estimates (|t0| > 1) which suggests that the model may also not be appropriate for the juvenile (< 1 year old) portion of the populations.

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Details of age calculation – NOTE this is a direct extract from Department of Primary Industries and Fisheries (2008):

Age Estimation

The Long Term Management Program (LTMP) differentiates between three types of age offish; age class, age group and biological age (DPI&F 2007). Age class, which is expressed in whole years, is the number of birthdays a fish is assumed to have had. Age class is important as it is required in the calculation of biological age and helps in the construction of the age group allocation matrix. Age group, which is also expressed in whole years, is the maximum age class fish would reach within a designated sampling season. Age group is the preferred age type used in routine analyses because it groups fish in the same cohort together, irrespective of when they were caught during a sampling season. Biological age is expressed in months (e. g. 30) or decimal years (e. g. 2. 5) Figure 7 shows the relationship between age class, age group and biological age relative to the sampling season, birth date and period of increment formation for tailor.

Data required for estimating age

The following data are required from each otolith or fish to estimate age:

• increment count; • edge classification; • capture month

The following data are required for the species, and are used to construct age class and age group allocation matrices (Figures 8, 9):

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• a defined period of opaque zone formation i.e. the months when otoliths with "new" or "wide" edge classifications are common; • a nominal birth date; • a designated sampling season

For tailor

• the defined period of opaque zone formation extends from August to December (see note below) • the nominal birth date is 1 September, based on a spawning season extending from July to October (Ward et al. 2003) • the designated sampling season is January 1st to December 31st i.e. calendar years (Figure 7).

Period of opaque zone formation in tailor

The period of opaque zone formation is difficult to define for tailor. The results of Hoyle et al. (2000) indicated that the mean width of the marginal increment (the distance between the outer edge of the outermost translucent zone and the otolith margin) was smallest during December, January and February, indicating the increment was newly formed, though this pattern was not consistent for all otoliths (e. g. when there was only one translucent zone). Importantly, the system of edge classification used by Hoyle et al. (the mean width of the marginal increment), is not directly comparable with the edge classification used by LTMP. An edge measured as wide by Hoyle et al., could have been classified as new by the LTMP protocol. Both methods however, indicate a single peak in new increment formation which supports the idea of an annual increment formation (Figure 8).

LTMP data from otoliths read using the current protocol (2005-current) indicate that the proportion of edges that are classified as new increases from August to November, with a corresponding decrease in the proportion of edges classified as wide (Figure 8). This pattern suggests that opaque zones are forming (becoming visible) during those months. It is currently assumed that opaque zone formation continues through into December; however, few otoliths

160 have been sampled in December. When more data are available for December and January, the period of opaque zone formation should be re-examined.

Age class

When estimating age class, it is important to take into account that:

1. the marginal opaque zone (i.e. a new increment) does not become visible in all fish in the population at exactly the same time (i.e. can vary by several months between individuals). 2. All cohorts of tailor move from one age class to the next on the nominal birth date of 1 September (i.e. irrespective of when increments form).

The matrix in Figure 9 is used to estimate the age class of each fish by identifying the necessary adjustment of the increment count based on the fish's capture month, and its edge classification.

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In August, which is during the period of opaque zone formation and prior to the nominal birth date, fish with an opaque zone on the margin of their otolith (i.e. a new) are assumed to have laid down that opaque zone prior to the corresponding birth date. In September to December, which is during the period of opaque zone formation and after the nominal birth date, fish with a wide translucent zone on the margin of their otolith (i.e. wide edge), are assumed to have been on the verge of forming a new opaque zone.

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Age group

When estimating age group, it is important to take into account that:

1. The marginal opaque zone (i. e. a new increment) does not become visible in all fish in the population at exactly the same time (i. e. can vary by several months between individuals). 2. All cohorts of tailor move from one age group to the next on 1 January (i.e. irrespective of when increments form)

The age group in Tailor is equal to the age class +1 for all edge types in the months between the start of the sampling season and the birth date.

Age in months (Am) (Biological Age)

It is necessary to estimate age class before estimating biological age. The time between the capture date and the previous birthday is then added to the age class using the following formulae (note: these formulae output the age in months):

If Cm < Bm Am = (age class x 12) + (Cm – Bm+ 12)

If Cm ≥ Bm Am = (age class x 12) + (Cm – Bm)

Where: Am = biological age; Cm = capture month; Bm = biological birth month (e.g. 9 = September).

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8.3 Supplementary Material for Chapter 3

Supplementary Table 8.3.1 Prey taxa consumed (% dry weight (DW) and % frequency occurrence (FO)) by Pomatomus saltatrix in 3 size classes, between July 2014 and June 2016. Fish with empty stomachs were not included in the analysis but have been listed in the table as additional information.

Family (or higher taxon) Prey Small (< 15 cm FL) Medium (15 ≤ 30 cm FL) Large (> 30cm FL) Total

% FO % DW % FO % DW % FO % DW % FO % DW

Teleosts Ambassidae Ambassis jacksoniensis 0.50 0.97 1.69 0.17 0.82 0.04 Ambassis marianus 0.85 0.30 0.27 0.04 Unidentified Ambassid 2.01 6.05 4.24 0.11 2.18 0.07 Antherinidae Unidentified Antherinidae 0.50 0.04 0.27 0.01 Carangidae Trachurus novaezelandidae 0.50 1.69 4.99 5.92 6.90 3.27 6.50 Clupeidae Hyperlophus vittatus 13.07 22.29 20.34 11.35 5.26 2.87 15.80 4.45

Hyperlophus translucidus 0.66 0.02 0.54 0.02 Sardinops sagax 0.50 9.32 13.29 16.44 13.63 10.08 13.36 Dinolestidae Dinolestes lewini 0.66 0.88 0.27 0.73 Engraulidae Engraulis australis 4.02 5.38 10.17 13.95 7.89 4.83 8.72 6.20 Gobiidae Arenigobius bifrenatus 0.50 1.37 0.27 0.02 Gobiopterus semivestitus 4.52 3.48 2.45 0.06 Unidentified Goby 1.51 0.77 2.54 1.07 1.63 0.17 Hemirampidae Hyporhamphus australis 1.69 3.02 3.95 4.51 2.18 4.22

Unidentified Garfish 1.69 0.99 1.32 0.94 1.36 0.93 Monocanthidae Unidentified Leatherjacket 0.66 0.10 0.27 0.08 Mugilidae Mugil cephalus 1.32 6.42 0.54 5.36

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Myxus elongates 0.66 1.85 0.27 1.54 Unidentified Mullet 1.01 0.03 3.39 0.72 3.29 14.21 3.00 11.97 Pempheridae Pempheris compressa 0.66 0.79 0.27 0.66 Pomatomidae Pomatomus saltatrix 4.24 2.59 1.32 1.60 1.91 1.73 Pricanthidae Priacanthus blochii 0.66 1.23 0.27 1.03 Scombridae Scomber australasicus 1.69 18.42 5.92 7.81 3.00 9.27 Sillaginidae Sillago flindersi 1.69 19.77 0.54 2.96 Sillago maculate 0.66 2.76 0.27 2.31 Unidentified Whiting 1.32 1.04 0.27 0.90 Sparidae Unidentified Sparid 0.66 1.54 0.27 1.26 Synodontidae Unidentified Synodontidae 0.66 0.06 0.27 0.05 Larval Fish 1.51 0.08 1.69 0.05 1.36 0.01 Unidentified Teleost 16.08 28.97 14.40 3.98 23.03 14.48 20.44 12.90

Crustaceans Callianassidae Trypaea australiensis 1.01 0.47 0.53 0.06 Mysidae Unidentified Mysid 29.65 5.95 2.54 0.03 13.03 0.02 Penaeidae Metapenaeus macleayi 3.02 4.67 5.08 3.80 3.19 0.64 Unidentified Prawn 9.55 15.16 4.24 1.00 6.38 0.33

Portunidae Ovalipes australiensis 0.50 1.37 0.27 0.02 Portunus pelagicus 0.85 0.02 0.27 0.01 Unidentified Crab 0.66 0.01 0.27 0.01 Unidentified crustaceans 0.85 0.42 0.27 0.01

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Cephalopods Unidentified Octopus. 2.63 5.46 1.06 4.56 Unidentified Squid 0.50 0.56 1.69 0.42 1.32 0.38 1.32 0.38

Other Polychaeta Unidentified Polychaete 1.51 0.32 0.80 0.01 Pyrosomatidae Unidentified Pyrosome 0.66 0.01 0.27 0.01 Sipunculidae Unidentified Peanut worm 0.66 0.01 0.27 0.01 Zosteraceae Zostera capricorni 0.66 0.01 0.27 0.01 Fishing Hook 0.50 0.72 0.85 0.06 0.54 0.01 Unidentified Material 0.50 0.05 0.66 5.66 1.06 0.01

Total dry mass (g) 12.3993 114.7767 640.5871 767.76 Number of non-empty stomachs 199 118 152 469 Number of empty stomachs 367 262 339 968

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8.4 Supplementary Material for Chapter 4

Supplementary Figure 8.4.1 Elemental profiles from the core to the edge of the otolith showing Mn:Ca ratios for all 12 Pomatomus saltatrix which were analysed. Profiles were created using a 7 point moving average. Elements are expressed as a ratio to calcium and units are in mmol mol-1.

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Supplementary Figure 8.4.2 Elemental profiles from the core to the edge of the otolith, for strontium and barium, for all 12 Pomatomus saltatrix which were analysed. Profiles were created using a 7 point moving average. The dashed horizontal line represents the calculated reference criteria for Sr:Ca in coastal environments based upon the end points of the profiles from adults caught in coastal environments (2.18 mmol mol-1). Elements are expressed as a ratio to calcium and units are in mmol mol-1. These otolith elemental ratios represent contributions from a variety of sources including the water, diet and other physiological influences.

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Supplementary Table 8.4.1 Summary of age 0 and age 1 Pomatomus saltatrix used in the LA-ICP-MS spot analysis.

Estuary/Region Sample Size Fork Length Range Mean Fork Length (cm) (cm) Age 0 P. saltatrix Botany Bay 30 11 – 18.2 13.9 Clarence River 28 5.1 – 19.3 9.7 Clyde River 21 8.8 – 18 14.0 Hawkesbury River 58 9.4 – 23.2 14.7 Hunter River 25 9 – 16.4 12.3 Jervis Bay 19 4.2 – 9.5 6.6 Moruya River 19 10.9 – 15.7 13.6 Port Hacking 25 9.3 – 18.3 12.9 Port Stephens 21 13.1 – 21.8 18.2 Shoalhaven River 21 11.1 – 19.1 15.7 Sydney Harbour 45 5.7 – 24.6 12.9 Wagonga Inlet 48 9.7 – 21.2 12.3 Age 0 total 360 4.2 – 24.6 13.7 Age 1 P. saltatrix North (< 29.5° S) 45 26.8 – 38.1 31.4 Central (29.5 – 33° 52 26.9 – 36.5 31.7 S) South (> 33°S) 24 26.3 – 38.9 30.9 Age 1 total 121 26.3 – 38.9 31.5

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Supplementary Table 8.4.2 Multivariate pairwise PERMANOVA results showing the estuaries which were significantly different to one another. Estuary pairs which were not significantly different (P > 0.05) to one another are not shown.

Estuary Pair t P(Perm) Unique Permutations Botany Bay, Wagonga Inlet 1.499 < 0.001 24 Port Hacking, Clarence River 2.790 < 0.001 24 Port Stephens, Wagonga Inlet 1.335 < 0.001 24 Hawkesbury River, Clarence River 1.878 0.010 720 Hawkesbury River, Jervis Bay 1.845 < 0.001 120 Clyde River, Hunter River 1.832 < 0.001 6 Clarence River, Jervis Bay 2.026 < 0.001 9915 Jervis Bay, Hunter River 1.652 0.024 9950 Moruya River, Hunter River 1.572 < 0.001 6

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Supplementary Table 8.4.3 Univariate PERMANOVA results. All terms had greater than 9000 unique permutations. Significant effects are shown in bold.

Element Li Mg Mn Cu df MS Pseudo-F P(perm) MS Pseudo-F P(perm) MS Pseudo-F P(perm) MS Pseudo-F P(perm) Fork Length 1 6.7424 5.8353 0.0376 45.2210 37.1830 0.0002 33.0920 14.4320 0.0021 0.5274 0.9653 0.3544 Estuary 11 2.6854 1.9471 0.1200 4.3704 2.8369 0.0444 3.5359 1.2232 0.3411 1.6412 2.8260 0.0913 Year 1 1.6040 1.2044 0.3274 6.5413 12.517 0.0095 0.1806 0.3714 0.5979 0.0199 0.5743 0.4753 Site(Estuary) 14 1.1652 1.2650 0.2394 1.2366 1.7160 0.0775 2.3559 3.0738 0.0014 0.5274 0.5256 0.8395 Estuary*Year 3 0.4208 0.4550 0.6991 1.9336 8.3093 0.1179 0.6682 1.1395 0.4878 1.2812 2.3702 0.3089 Year*Site(Estuary) 2 1.1738 1.2744 0.2233 0.1996 0.2770 0.6945 0.6059 0.7906 0.4135 0.5140 0.5122 0.4934 Residuals 327 0.9211 0.7206 0.7664 1.0035 Total 359 Zn Sr Ba Pb MS Pseudo-F P(perm) MS Pseudo-F P(perm) MS Pseudo-F P(perm) MS Pseudo-F P(perm) Fork Length 1 0.6516 0.6812 0.4238 6.7378 2.0909 0.1649 8.0106 2.3849 0.1518 2.7102 6.7379 0.1022 Estuary 11 0.7394 0.8319 0.6039 5.7540 1.3703 0.2936 7.7541 1.7508 0.1700 0.8826 2.4498 0.1032 Year 1 6.8658 2.8932 0.1645 0.0352 0.2981 0.6259 3.3141 3.8768 0.1188 0.0207 3.8914 0.0864 Site(Estuary) 14 0.9557 0.9802 0.4239 3.3269 4.7940 0.0001 3.4707 5.3218 0.0001 0.3758 0.3602 0.8374 Estuary*Year 3 2.3824 1.0358 0.5330 5.0415 26.7740 0.0409 0.1617 11.8820 0.0935 0.0489 23.1910 0.1077 Year*Site(Estuary) 2 1.9922 2.0432 0.1052 0.1515 0.2183 0.7940 0.0230 0.0352 0.9539 0.0118 0.0113 0.9009 Residuals 327 0.9750 0.6940 0.6522 1.0432 Total 359

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8.5 Supplementary Material for Chapter 5

Supplementary Table 8.5.1 GAMM Model selection table for full GAMM Model including Latitude. All models included the Side_Date random effect. The response variable for all models was Log(GSI). The included variables were a latitude*Month tensor spline (Latitude*Month), chlorophyll a (Chl), eddy kinetic energy (EKE), mean sea level anomaly (MSLA), day length (daylength), sex and Estuary or Ocean captured (Estuary/Ocean). Variables bounded by a s() were used as a smoothed term. ΔAIC is the difference in AIC from the best model.

Model Description Model Design AIC ΔAIC

Full Model (Latitude*Month+ s(Chl) + s(MSLA) + s(EKE) + 381.28 24.56 Estuary/Ocean + Sex

Removed s(MSLA) (Latitude*Month) + s(Chl) + s(EKE) + 372.18 15.46 Estuary/Ocean + Sex

Removed s(Chl) (Latitude*Month+ s(EKE) + Estuary/Ocean + 363.44 6.72 Sex

Removed Estuary_Ocean (Latitude*Month) + s(EKE) + Sex 360.68 3.96

Removed s(EKE) - Best Model (Latitude*Month) + Sex 356.72 0

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Supplementary Table 8.5.2 GAMM Model selection table for full GAMM Model including SST. All models included the Side_Date random effect. The response variable for all models was Log(GSI). The included varabiles were sea surface temperature (SST), eddy kinetic energy (EKE), mean sea level anomaly (MSLA), day length (daylength), sex and Estuary or Ocean captured (Estuary/Ocean). Variables bounded by a s() were used as a smoothed term. ΔAIC is the difference in AIC from the best model.

Model Description Model Design AIC ΔAIC

Full Model s(SST) + s(EKE) + MSLA + s(Chl) + s(daylength) + 501.20 17.79 Sex + Estuary/Ocean

Removed s(day_length) s(SST) + s(EKE) + MSLA + s(Chl) + Sex + 495.08 11.67 Estuary/Ocean

Removed s(Chl) – Best s(SST) + s(EKE) + MSLA + Sex + Estuary/Ocean 483.41 0 Model

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Supplementary Figure 8.5.1 Larval distribution of Pomatomus saltatrix from the Australian National Ichthyological Monitoring and Observing database (Smith et al. 2018). Each dot represents a tow which contained P. saltatrix (n =102). Colour represents the year of the sample and size of the dot is the abundance of P. saltatrix (m-3).

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Supplementary Figure 8.5.2 Histogram showing the observed sex ratios from the 2,000 resamples used in the randomisation test which drew 285 fish from the dataset used in the current study (n = 3,245). The dashed red line marks the 1:1 sex ratio where female and male fish are in equal proportions. There was a higher proportion of females than males in all resamples.

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Supplementary Figure 8.5.3 Example size frequency histograms from 2 subsamples from different ovaries using 0.01mm size bins (from a stage 4 ovary). A) the egg size distribution of an ovary which displayed only one mode of eggs. B) The egg size distribution of an ovary which displayed multiple modes of eggs (from a stage 3 ovary). Note the different scale on the y-axis is caused by differing sizes of the subsample.

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Supplementary Figure 8.5.4 Sample Distribution by Gonadosomatic Index for Pomatomus saltatrix. Each dot represents an individual fish. Note the dots are semi-transparent to show overlapping samples.

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Supplementary Figure 8.5.5 Gonadosomatic Index (GSI) by macroscopic stage as per Zeller et al. (1996) for female Pomatomus saltatrix. The width of the ‘violin’ is proportional to the number of samples with that Gonad Index in a stage. The maximum width of each ‘violin’ is the same so the widths represent the proportions within each stage and not of the total dataset.

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Supplementary Figure 8.5.6 Observed GSI by month for both male (blue) and female (pink) Pomatomus saltatrix. Each month shows the mean (± SE) for all collected fish in each month for each sex.

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Supplementary Figure 8.5.7 Graphical representation of the two-dimensional smoother between Latitude and Month produced by the GAMM of GSI. Pink represents high GSI and green represents low GSI.

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Supplementary Figure 8.5.8 Partial effects plot of SST () for the environmental variable GAMM.

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Supplementary Figure 8.5.9 Partial effects plot of eddy kinetic energy (EKE) for the environmental variable GAMM.

182