Investigating the Movement Patterns of Sharks and the Significance Of

Home , Leopard shark, Nervous shark, Whiskery shark

Investigating the movement patterns of sharks and the significance of potential shark predation attempts on bottlenose dolphins (Tursiops aduncus) in the waters of south-western Australia

A thesis presented in partial fulfilment of the degree of Bachelor of Science Honours

School of Veterinary and Life Science

Murdoch University, Western Australia

Carissa King

2014

Declaration

I declare this thesis is my own account of my research and contains as its main content work which has not previously been submitted for a degree at any other tertiary institution.

……………………………………………………………………………………………….

Carissa M King

I acknowledge that a copy of this thesis will be held at Murdoch University Library.

I understand that under the provisions of s51.2 of the Copyright Act 1968, all or part of this thesis may be copied without infringement of copyrighter where such a reproduction is for the purposes of study and research.

This statement does not signal any transfer of copyright away from the author.

Signed: ……………………………………………………………………………………………………………………………………………..

Degree: Bachelor of Science with Honours in Marine Science

Thesis Title: Investigating the movement patterns of sharks and the significance of potential shark predation attempts on bottlenose dolphins (Tursiops aduncus) in the waters of south- western Australia.

Author: Carissa Marie King

Year: 2014

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Abstract

Despite their prominence as species of great interest and conservation significance, currently our understanding of shark movement patterns and their ecological role as predators on small Odontocete populations is far from complete. The first component of my research investigated the movement patterns of the four main commercial species

(sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) and several species occasionally caught off the coast of

Western Australia (Chapter 2). I analysed long-term (1994 to 2013), conventional tagging data collected by the Department of Fisheries, Western Australia to provide a detailed account of observed movement patterns. The second component of my research investigated the predatory role of sharks on bottlenose dolphins (Tursiops aduncus) off

Bunbury, Western Australia (Chapter 3). I examined the prevalence of shark bites on systematically photographed dolphins over an eight year period (2007 to 2014). I also attempted to identify the shark species responsible for the attacks by seeking the expert opinions of three independent reviewers on the bite marks.

The analyses of movement patterns from the long-term tagging data (Chapter 2) found mean displacements of < 250 km for the four main commercial species. However, occasional displacements of more than 2,000 km were also observed for all four species. Displacement was positively correlated with time at liberty, size (fork length) and release condition. The swimming speed varied significantly between species, with faster movements observed for larger Carcharhinid sharks. Furthermore, significant differences in sex ratios at release and recapture were observed for gummy and whiskery sharks. A significantly higher proportion of females were released and recaptured for both species. Although, fork length was found to significantly vary for non-recaptured and recaptured sandbar and dusky sharks, results

from the analyses were disregarded due to bias gear-selectivity and inaccurate measurements reported by fishermen. The highest recapture frequency for all other species occasionally caught was less than ten. Maximum displacements ranged from 0.70 to 1,143 km, these displacements were observed by wobbegongs (Orectolobus sp.) and copper whaler (Carcharhinus brachyurus) sharks, respectively. Maximum time at liberty ranged from 4 to 5,245 days for nervous (Carcharhinus cautus) and tiger (Galeocerdo cuvier) sharks, respectively. The estimated maximum swimming speed for occasionally caught species peaked at 0.42 km/hr for copper whaler (Carcharhinus brachyurus) sharks. Swimming speeds for all other species were less than 0.03 km/hr. No statistical analyses were completed for these species.

Analyses of the prevalence of external injuries believed to have been inflicted by sharks

(Chapter 3) found that the total bite mark frequencies of systematically photographed dolphins varied significantly among age classes (calves, juveniles, adults) with the highest frequency of injuries sustained by adults (X2 = 38.436, P = < 0.001). Bite frequencies did not differ significantly between sexes or between mothers with or without calves (X2 = 0.111, P

= 0.738; X2 = 1.316, P = 0.251, respectively). The total frequency of shark bites was significantly lower in the austral autumn and winter months than in the spring and summer

(X2 = 15.333, P = 0.002). However, the frequency of fresh injuries was higher in the summer of 2013 (n = 8), than in other seasons (range = 0 - 1). When the data for 2013 were removed from the seasonal analyses the frequency of bites in summer (pooled over years) was higher but not significantly (X2 = 3.889, P = 0.274). The total frequency of injuries did not significantly differ among years (2008 – 2013) (X2 = 4.948, P = 0.422). After evaluating the photographed bite marks on dolphins, three independent reviewers suggested that the shark species responsible for the injuries were most likely white (Carcharodon carcharias),

tiger (Galeocerdo cuvier), and several smaller Carcharhinid species (e.g., bull, Carcharhinus leucas; whaler, Carcharhinus brachyurus; dusky, Carcharhinus obscurus).

The results from Chapter 2 of the study provide a complete and meaningful representation of the movement patterns for the four main commercial species (sandbar,

Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; and gummy, Mustelus antarcticus) and several species occasionally caught off Western

Australia. The described movement patterns presented in this study can be incorporated into future conservation and management plans increasing their effectiveness and precision, ensuring west Australian shark stocks remain at target thresholds. The results from Chapter 3 refine our understanding of the interactions between sharks and small living

Odontocetes (i.e., bottlenose dolphins, Tursiops aduncus). The results from the research confirm that sharks not only scavenge but actively hunt and predate living bottlenose dolphins. The ability and significant influence of these predatory sharks to shape and alter dolphin population dynamics is likely to be more important than previously recognised.

Table of Contents

1. General Introduction ……………………………………………………………………………………………………… 1 1.1 Research Aims ……………………………………………………………………………………………….…..….…… 3

2. The movement patterns of several shark species commercially targeted off the coast of Western Australia, with a key focus on the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) ……………………………………………………………………..…………………… 5 2.1 Summary ……………………………………………………………………………………………………………………. 6 2.2 Introduction ……………………………………………………………………………….………………………………. 7 2.3 Materials and Methods …………………………………………………………….………………………………. 10 2.3.1 Data Collection ……………………………………………………………………………………………………. 10 2.3.2 Data Analyses ……………………………………………………………………………………………………… 12 2.4 Results …………………………………………………………………………………….……………………………….. 15 2.4.1 Data Summary ………………………………………………………………………………….………………… 15 2.4.1.1 Release and Recapture Data for All Commercial Species ………………………..………… 15 2.4.1.2 Release and Recapture Locations for the Four Main Commercial Species ………… 16 2.4.2 Size Composition of Non-Recaptured and Recaptured Sharks …………………………..… 18 2.4.3 Sex Ratio of Released and Recaptured Sharks ……………………………………………..……… 20 2.4.4 Displacement, Time at Liberty and Swimming Speed ……………………………………….…. 22 2.4.5 Displacement Direction ………………………………………………………………………………………. 26 2.4.6 Root-Mean Squared Displacement ……………………………………………………………………… 28 2.4.7 Generalised Linear Models ………………………………………………………………………….……… 29 2.5 Discussion ………………………………………………………………………………………………………………… 32

3. Evaluating the frequency of predation attempts by sharks on bottlenose dolphins (Tursiops aduncus) off the coast of Bunbury, Western Australia ……………………………………. 39 3.1 Summary …………………………………………………………………………………………….……………………. 40 3.2 Introduction …………………………………………………………………………………….……………………….. 41 3.3 Materials and Methods ……………………………………………………….……………………………………. 44 3.3.1 Study Site …………………………………………………………………………………….……………………… 44 3.3.2 Data Collection ……………………………………………………………………………………………………. 46 3.3.3 Injury Classification …………………………………………………….………………………………………. 48 3.3.4 Estimated Injury Age …………………………………………………………..………………………………. 49 3.3.5 Dentition and Bite Characteristics ………………………………………………………………………. 50 3.3.6 Data Analyses ………………………………………………………..……………………………………………. 51 3.4 Results ……………………………………………………………………….…………………………………….………. 52 3.4.1 Environmental Conditions …………………………………………………..………………………………. 52 3.4.2 Predation Attempts ………………………………………………….……………..…………………………. 54 3.4.2.1 Data Summary …………………………………………………………………………..……………….……. 54 3.4.2.2 Opportunistic Sightings ……………………………………………………………………………………. 55 3.4.2.3 Systematic Sightings …………………………………………………………………………..……………. 56 3.4.3 Identification of the Sharks Species Responsible ………………….……………………………… 59 3.5 Discussion …………………………………………………………………………………….…………….……………. 60

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4. Conclusions and Recommendations ………………………………………………………………….………… 67 4.1 Recommendations for Future Research ………………………………….…………………………….….. 69 4.2 Implications for Management …………………………………………………………………………….……. 70

5. Literature Cited ………………………………….……………………………………………………………..….……… 71

6. Appendix I. Summary of all occasionally caught species released but not recaptured off the west and south coast of Australia from 1994 to 2013 ………………………………………………… 80

7. Appendix II. Analysis of the residuals for the displacement distance Generalised Linear Model (GLM) for a normal distribution …………………………………………………………………………….. 82

8. Appendix III. Analysis of the residuals for the time at liberty Generalised Linear Model (GLM) for a Poisson distribution ………………………………………………………………………………………. 83

9. Appendix IV. Analysis of residuals for the speed Generalised Linear Model (GLM) for a normal distribution ………………………………………………………………………………………………………….. 84

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List of Tables

Table 2.1 The total number of sharks tagged, released and recaptured off the coast of Western Australia from 1994 to 2013. Species ordered by highest recaptures ……………….. 16

Table 2.2 The range in fork length (cm) of non-recaptured and recaptured sharks off Western Australia from 1994 to 2013. Species ordered by largest released fork length …... 19

Table 2.3 The sex ratio of released and recaptured individuals off Western Australia, from 1994 to 2013. Species ordered by largest number of released males ……………………….……… 21

Table 2.4 Results of the Chi-Square test of independence testing the experimental hypothesis that sex ratios at release and recapture do not statistically differ for the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) tagged off Western Australia from 1994 to 2013 ……………………………………………………………………………………………………………………. 22

Table 2.5 The observed displacement, time at liberty and estimated swimming speeds for the released and recaptured individuals off Western Australia from 1994 to 2013. Species ordered by maximum displacement …………………………………………………………………………………. 24

Table 2.6 Results of RAO’s and Rayleigh’s test of uniformity to test the experimental hypothesis that displacement direction within the west Australian fishery management zones (the combined West Coast Demersal Gillnet & Closed Area Zone; the Joint Authority Southern Demersal Gillnet and Demersal Longline Fishery Zone 1; and the Joint Authority Southern Demersal Gillnet and Demersal Longline Fishery Zone 2) did not significantly vary among the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) …….….. 28

Table 2.7 Results from the Generalised Linear Models fitted to the relationship between displacement distance, time at liberty, and swimming speed, and the independent factors species, size (fork length), sex and release condition for the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) tagged off Western Australia from 1994 to 2013. Time at liberty was also fitted to the GLM for displacement distance …………………………………….…….. 30

Table 3.1 The number of systematic and opportunistic sightings and total survey effort (time spent on transect) for each year from 2007 to 2014 in the Bunbury region …………………..…. 47

Table 3.2 The age classification of bottlenose dolphins, Tursiops aduncus, in the Bunbury region of south-western Australia as used by Smith (2012) and Smith et al. (2013) …..…….. 48

Table 3.3 Injury classification of bite marks on bottlenose dolphins, Tursiops aduncus, in the Bunbury region of south-western Australia based on estimated age of the wound (modified from Dwyer & Visser 2011) ………………………………………………………………………………………..…….. 50

Table 3.4 The individual identity and wound categories recorded from opportunistic sightings of bottlenose dolphins, Tursiops aduncus, off Bunbury, Western Australia between 2006 and 2013 …………………………………………………………………………………………………………………. 55

Table 3.5 Summary of the number of sharks and rays caught on drum-lines as part of the west Australian swimmer protection program implemented by the Department of Fisheries, Western Australia from January 2014 to April 2014. All species recorded as dead were dead upon hook retrieval; destroyed due to low likelihood of survival; or target species and due to size (> 300 cm TL) were destroyed (data sourced from the Department of the Premier and Cabinet 2014) …………………………………………………………………………………………………………………… 63

List of Figures

Figure 2.1 Study location and associated shark fishery zones managed by the Department of Fisheries, Western Australia. JANSF = Joint Authority Northern Shark Fishery; WANCSF = West Australian North Coast Shark Fishery; WCDGDLF = West Coast Demersal Gillnet and Demersal Longline Fishery; JASDGDLF (Zones 1 and 2) = Joint Authority Southern Demersal Gillnet and Demersal Longline Fishery ………………………………………………………………….………….. 12

Figure 2.2 Release and recapture locations for the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) tagged off Western Australia between 1994 and 2013 ………………….. 17

Figure 2.3 The size (fork length) distribution at release for non-recaptured and recaptured individuals for the four main commercial shark species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus). Arrows indicate female size at maturity with sizes attained from: McAuley et al. (2007) for sandbar sharks; Simpfendorfer et al. (2002) for dusky sharks; Simpfendorfer & Unsworth (1998) for whiskery sharks; and Walker (2007) for gummy sharks ………………………….……….. 20

Figure 2.4 The observed displacement distance (km), time at liberty (days) and estimated swimming speeds (km/hr) for the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) tagged off Western Australia from 1994 to 2013 ………………………………..………… 25

Figure 2.5 The observed displacement directions for the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) within the west Australian fishery management zones. The combined West Coast Demersal Gillnet & Closed Area Zone; the Joint Authority Southern Demersal Gillnet and Demersal Longline Fishery Zone 1; and the Joint Authority Southern Demersal Gillnet and Demersal Longline Fishery Zone 2 ………………………………………….………. 27

Figure 2.6 The estimated Root-Mean Square displacement (RMS) and time at liberty for the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) tagged off Western Australia from 1994 to 2013. Vertical lines extending from the markers indicate precision estimates (+1 SE) obtained from the jackknife method ………………………………………………….... 29

Figure 2.7 The predicted mean displacement distance, time at liberty and swimming speed from the Generalised Linear Models for each of the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) tagged off Western Australia from 1994 to 2013. Vertical lines extending from the markers indicate precision estimates (+1 SE) …………………………………….. 31

Figure 3.1 Study location and associated transects used for systematic dolphin surveys near Bunbury, south-western Australia (Image provided by Kate Sprogis) ……………………………….. 45

Figure 3.2 Categories of shark bite wounds on bottlenose dolphins, Tursiops aduncus, in the Bunbury region of south-western Australia for: a) open, wound was attained in the last two months; b) intermediate, approximately two to six months of healing; and c) scar, over six months old, wound has completely healed (see Table 3.3 for descriptions of the categories, modified from Dwyer & Visser 2011) ……………………………………………………………………….………. 49

Figure 3.3 The seasonal mean sea surface temperatures recorded by the depth sounder onboard the research vessel during systematic dolphin surveys near Bunbury, Western Australia (SU = summer; AU = autumn; WI = winter; SP = spring). Vertical lines extending from the markers indicate precision estimates (+1 SE) …………………………………………..………… 53

Figure 3.4 The seasonal values for the Southern Oscillation Index (SOI) between 2008 and 2013. Values > 8 show La Niña conditions; < - 8 show El Nino conditions (data sourced from the Bureau of Meteorology 2014b) ………………………………………………………………………………….. 54

Figure 3.5 The bite frequencies for each category of bite (fresh, intermediate, scar) and age class of dolphin for bottlenose dolphins, Tursiops aduncus, photographed systematically off Bunbury, Western Australia, from 2007 until 2014 ………………………………………………………….. 56

Figure 3.6 The number of bites in each wound age category for male and female bottlenose dolphins, Tursiops aduncus, photographed systematically off Bunbury, Western Australia, from 2007 until 2014 ……………………………………………………………………………………………………….. 57

Figure 3.7 The seasonal frequency of bite marks for each category of bite recorded on bottlenose dolphins, Tursiops aduncus, photographed systematically off Bunbury, Western Australia, from 2007 until 2014. Vertical lines extending from the columns indicate precision estimates (SE) calculated from mean values ……………………………………………………….……….…… 58

Figure 3.8 The number of bite marks in each category and total bites in each year for all bottlenose dolphins, Tursiops aduncus, photographed systematically off Bunbury, Western Australia, from 2007 until 2014 ………………………………………………………………………………………… 59

Figure 3.9 Shark bite wounds on bottlenose dolphins, Tursiops aduncus, off Bunbury, Western Australia attributed to: a) white shark (Carcharhinus carcharias); b) potential bull shark (Carcharhinus leucas); and c) tiger shark (Galeocerdo cuvier) by international experts (Dr Heithaus, International University of Florida; Professor Burgess, Florida Museum of Natural History; Dr McAuley, Department of Fisheries, Western Australia) …………………….. 60

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Acknowledgements

This thesis would not have been possible without the assistance, guidance, and input of my four dedicated supervisors Professor Neil Loneragan, Lars Bejder and Kate Sprogis from

Murdoch University, and Matias Braccini from the Department of Fisheries, Western

Australia. I would like to thank my supervisors for their continuous assistance and feedback throughout this process, especially towards the deadline. I am very thankful to them for providing me with this opportunity and for allowing me to undertake research on topics that

I am greatly passionate about.

I am very grateful to Dr. M. Heithaus from the International University of Florida, Professor

G. Burgess from the Florida Museum of Natural History, and Dr. R. McAuley from the

Department of Fisheries, Western Australia for their time and feedback to the species responsible for the predation attempts seen on the Bunbury dolphins.

I would also like to thank Adrian Hordyk for his time and assistance with R.

Finally, I would like to thank my loving parents, partner Jake and close friends for their continual support and encouragement throughout my university degree. Without them this journey would not have been possible.

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1. General Introduction

Sharks typically occupy high trophic positions in marine food webs (Cortés 1999) playing important roles influencing the dynamics and structure of biological communities (Stevens et al. 2000; Shepherd & Myers 2005; Myers et al. 2007). Their ability to influence community composition and relative abundance of prey species is thought to provide trophic stability. Reduced shark densities can lead to the release of meso-predator populations (Myers et al. 2007), an increase in competition among taxa (Fogarty &

Murawski 1998) and ultimately, a reduction or imbalance in species under the influence of predation (Pace et al. 1999). In some cases, the removal or depletion of sharks from an ecosystem can greatly reduce its stability and resilience, with the potential for cascading effects and population declines in other parts of the food web (Jackson et al. 2001; Myers et al. 2007).

Globally, there have been several reports of shark stock collapses (Camhi et al. 2009). It is estimated that regional declines of large shark populations currently exceed reductions of more than 90% (Myers et al. 2007). Research surveys from 1970 to 2005 off the east coast of the United States indicate rapid and marked declines in the abundance of at least 11 shark species (Meyers et al. 2007). A combination of habitat modification, swimmer protection programs and various forms of fishing (e.g., artisanal, traditional, recreational and commercial) are suspected to be responsible for these rapid declines. Increased pressure from commercial fisheries is suggested to be the leading factor causing these population declines (Walker 1998).

Predicting how individual communities will respond to reduced shark densities requires a comprehensive understanding of how these top-level predators influence marine

ecosystems (Strauss 1991; Heithaus et al. 2008). Sharks are able to directly influence community composition through prey ingestion and indirectly through predation risk. Risk- induced cascades may become more pronounced during times when resources are limited and meso-consumers must forgo foraging opportunities in order to manage predation risk

(Heithaus et al. 2008). Although the effects of global shark declines are expected to vary across communities (Borer et al. 2005; Frank et al. 2007) an increasing number of studies are detecting large-scale cascading effects caused by top-level predator declines (Heithaus et al. 2008).

Shark populations should therefore not be managed for demographic persistence alone, but also for the preservation of ecological processes and ecosystem stability (Pyare & Berger

2003). Shark densities should be managed so that populations are above thresholds to maintain meaningful interactions (Soulé et al. 2005). Defining interactions as meaningful and determining the level to which they should be managed is a strenuous task. The optimal protection of a species would take into account its entire range and distribution throughout the year to ensure that major migration pathways are considered (Reeves 2000). However, due to the highly migratory nature of many shark species, protection of the population covering the entire geographic range throughout the year is often not possible (Hooker &

Gerber 2004). Effective protection, however, can be provided through spatial and temporal closures of critical habitats such as mating, pupping, nursery and foraging grounds (Hooker

& Gerber 2004). The scale and extent of these closures often depends on the habitat use and movement patterns of the species to be protected (Hooker & Gerber 2004; Speed et al.

2010). Ongoing investigations regarding habitat use and movement patterns are therefore essential aspects required for managing and conserving shark species across the globe.

Movement patterns of top-level predators often vary greatly among species (e.g., Speed et al. 2010). Movements can be triggered by either biotic interactions or changing environmental conditions. The most commonly cited biotic factors known to influence movement include prey distribution and availability, competition, predator distribution, social organisation and reproductive strategies (Bonfil et al. 2005; Duffy et al. 2012).

Environmental conditions such as temperature, salinity, dissolved oxygen, tidal stage and lunar phase are also known to be important factors that influence movement (Hopkins &

Cech 2003; Heupel & Simpfendorfer 2008). However, due to the potential correlations between water quality parameters determining the primary driving force that stimulates movement is often difficult (Heupel & Simpfendorfer 2008).

1.1 Research Aims

Despite their prominence as species of great interest and conservation significance, currently our understanding of shark movement patterns and their ecological role in marine ecosystems is far from complete. In this study I aimed to describe to the movement patterns of several shark species commercially targeted off the coast of Western Australia, with a key focus on the four main species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) (Chapter 2). The second aim of my research was to investigate the predatory role of sharks on bottlenose dolphins

(Tursiops aduncus) off Bunbury, Western Australia (Chapter 3). As a secondary objective I also attempted to identify the key shark species responsible for these attacks.

In my study of movement patterns, I analysed long-term (1994 to 2013) conventional tagging data collected by the Department of Fisheries, Western Australia (DoF) to provide

detailed descriptions of observed movement patterns. These data, and a description of the methods of data collection and suggested analyses were provided by Dr Matias Braccini

(DoF). I extended this work by including an evaluation of the results and developing

Generalised Linear Models to predict how displacement distance, time at liberty and swimming speed varied with species of shark, size, gender and release condition.

In order to examine the significance of sharks as predators on dolphins, I analysed the presence of shark bites on photographed dolphins collected over eight years (2007 to 2014) of systematic dolphin surveys. Data were collected from year-round standardized boat- based surveys conducted as part of two PhD research projects (Smith 2012; K. Sprogis,

Murdoch University, unpublished data). I also attempted to identify the shark species responsible for these attacks by seeking the expert opinions of three independent reviewers on characteristics of the bite marks.

2.1 Summary

Understanding the movement patterns of commercially fished shark species is fundamental to the management of shark populations. In this study, I have analysed all available conventional tagging data collected by the Department of Fisheries, Western

Australia, from 1994 through until 2013, to investigate the movement patterns of west

Australian elasmobranches with a particular focus on the four main commercial species: sandbar (Carcharhinus plumbeus), dusky (Carcharhinus obscurus), whiskery (Furgaleus macki) and gummy (Mustelus antarcticus) sharks. As a secondary objective the movements of several occasionally caught species were also reported. Up to 2013, a total of 10,402 elasmobranches, representing 53 species, were tagged and released off Western Australia, of which 1,110 individuals, representing 16 species, were recaptured. For the four main commercial species mean displacement distances were < 250 km. However, occasional displacements of more than 2,000 km were also observed for all four species. Displacement was positively correlated with time at liberty, size (fork length) and release condition. The speed of movement varied significantly between species, with faster movements observed for larger Carcharhinid sharks. Furthermore, significant differences in sex ratios at release and recapture were observed for gummy and whiskery sharks. A significantly higher proportion of females were released and recaptured for both species. The size (fork length) of non-recaptured and recaptured sandbar and dusky sharks was found to significantly differ. Recaptures of commercial species occasionally caught were relatively low (n = 10).

Maximum displacements ranged from 0.70 to 1,143 km, these displacements were observed for wobbegongs (Orectolobus sp.) and copper whaler (Carcharhinus brachyurus) sharks, respectively. Maximum time at liberty ranged from 4 to 5,245 days for nervous

(Carcharhinus cautus) and tiger (Galeocerdo cuvier) sharks, respectively. The estimated

maximum swimming speed for occasionally caught species peaked at 0.42 km/hr for copper whaler (Carcharhinus brachyurus) sharks. Swimming speeds for all other species were less than 0.03 km/hr. No statistical analyses were undertaken for species occasionally caught.

The complete and meaningful movement patterns described and presented in this Chapter

(2) can be incorporated into future conservation and management plans increasing their effectiveness and precision, ensuring west Australian shark stocks remain above meaningful thresholds.

2.2 Introduction

Animals move over a wide range of scales in response to different triggers, such as short- term feeding requirements (Andrews et al. 2009), predator avoidance (Zaret & Suffern

1976), reproduction (Olsen 1954), and changes in environmental conditions (Francis 1988).

Movement has a large effect on the flow of genes and disease, and in delineating population structure (Whitehead et al. 2008). Movement also allows complex spatial and temporal organizations to be developed like those according to size, age and sexual segregation. In addition, the ability of species to adapt to changes in climate largely depends on their capacity to relocate to suitable habitats (Hulme 2005). Understanding movement patterns has a range of applications, from predicting possible distribution shifts resulting from climate change to setting effective management and conservation measures. For example, movement information is required for determining the spatial scale at which to manage a species. This, in turn, allows the implementation of powerful management tools, such as the establishment of spatial/temporal closures in nursery areas and spawning aggregations that enhance our ability to conserve stocks and sustain yields (Walters & Martell 2004).

The management of species of high-conservation concern such as sharks can be improved greatly by furthering our understanding of their movement patterns. Many shark species are considered apex predators (Cortés 1999) and some species have been shown to have important ecological roles (e.g., Stevens et al. 2000; Shepherd & Myers 2005). Many species are vulnerable to fishing over-exploitation due to their naturally low biological productivity

(Stevens et al. 2000). Worldwide, there have been several reported cases of shark stocks collapsing, and currently a quarter of the worlds sharks, rays and chimaeras are estimated to be threatened (Dulvy et al. 2014). Understanding the temporal and spatial distribution of sharks can allow the implementation of cost-effective management measures and a clear definition of the scale at which conservation and management efforts should be applied.

Shark movement studies have increased considerably in recent years with the advent of satellite technology and acoustic telemetry. While these developing technologies have several advantages, traditional methods such as conventional tagging still remain a cost- effective approach (Sciarrotta and Nelson 1977; Daley et al. 2002). Since 1936, conventional tagging has been used for delineating stock structures (e.g., Holden 1968), predicting growth rates (e.g., Braccini et al. 2010), estimating mortalities (e.g., McAuley et al. 2007), improving population dynamic modelling (e.g., Walker 1992), and studying movement patterns (e.g., Stevens 1990). Movement patterns exhibited by sharks are often described by quantifying displacement distance, time at liberty, displacement direction and speed

(e.g., Andrews et al. 2010, Barnett et al. 2010, Hoffmayer et al. 2014). Each component provides valuable information on different movement aspects, and when combined provides a comprehensive understanding allowing meaningful conclusions to be made.

For sharks, large-scale conventional tagging programs and databases have been established by several fishery research agencies (Francis 1989; Kohler & Turner 2001;

McAuley et al. 2007). In Western Australia (WA), large-scale tagging programs were established in 1994 by the Department of Fisheries, Western Australia. Although these programs have primarily focussed on estimating mortality rates and delineating stock structure these release-recapture databases have significant potential to provide important insight on shark movement patterns.

In Western Australia, several shark species are commercially fished though catches largely consist of sandbar (Carcharhinus plumbeus), dusky (Carcharhinus obscurus), whiskery

(Furgaleus macki) and gummy sharks (Mustelus antarcticus) (McAuley & Leary 2010). All four species are fished throughout much of their distribution due to their high abundance in tropical and temperate coastal waters; and vulnerability to multiple gear types (McAuley et al. 2006). Sandbar and dusky sharks are particularly susceptible to the effects of overfishing and commercial exploitation due to their slow growth, late onset of maturity, small litter sizes and long reproductive cycles (Simpfendorfer et al. 2002; McAuley et al. 2006).

Whiskery and gummy sharks, in contrast, are smaller demersal species endemic to Australia and due to their higher biological productivity are more resilient to the effects of overfishing

(Last & Stevens 2009). All four species are currently recovering or at acceptable biomass levels (Braccini & McAuley 2013); however, enhancing their management requires an understanding of their movements. For example, species with considerable movement could be managed as single units whereas species with restricted movement may be better managed as multiple units.

In this study, all available release-recapture information collected by the Department of

Fisheries, Western Australia from 1994 to 2013 (provided by Dr Matias Braccini), was used to investigate the movement patterns of several shark species commercially targeted off

Western Australia, with a particular focus on the four main commercial species (sandbar,

Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy,

Mustelus antarcticus). The information from tag returns was used to quantify displacement distance and direction, time at liberty and swimming speed for each species. I hypothesised that movement patterns would differ among the four main species, with movements being greatest for the Carcharhinid species. Furthermore, movement would significantly vary within and among species in accordance to the size of the individual.

2.3 Materials and Methods

2.3.1 Data Collection

From 1994 to 2013, more than 10,402 sharks from several species were conventionally tagged off Western Australia (WA) aboard commercial shark fishing and research vessels managed by the Department of Fisheries, Western Australia. Scientific dropline and longline surveys were conducted as part of the annual shark monitoring and tagging program by the

Department of Fisheries. The annual survey is conducted from May to August aboard the

R.V. Naturaliste along the continental shelf off north-western Australia. From 1994 to 2000, the survey used droplines consisting of 11 and 36 J-shaped hooks, size 12/0, baited with sea mullet (Mugil cephalus) or mackerel (family Scombridae) (refer to McAuley et al. 2005).

From 2001 onwards, droplines were replaced by longlines. Longlines were 500 m long and consisted of ~50 J-shaped hooks, size 12/0, baited with sea mullet or mackerel (half a fish

per hook), hooks were attached to a main line via 2 m metal snoods. Droplines and longlines were set in depths of 7 to 100 m (with 90% set in < 80 m), and 7 to 450 m (with 90% set in <

192 m), respectively. Droplines were typically set between 9.00 am and 4.00 pm whereas longlines were typically set between 4.00 am and 7.00 am. Soak time of droplines and longlines typically ranged from 16 to 20 hrs (median = 16.7 hrs) and between 2.5 to 6 hrs

(median = 3.5 hrs), respectively, depending on the time required for retrieving and processing the catch. Active sharks were brought onboard and tagged on the first dorsal fin with a numbered Jumbo Rototag (Dalton Supplies, Australia). Captured individuals were measured (fork length, FL, the distance from the tip of the snout to the caudal fork), sexed and examined for the presence of an open umbilical scar (open scars indicate individuals within one month of birth). Date and GPS co-ordinates of the individuals captured were also noted. Upon release the sharks condition was monitored and classed as being strong with the shark swimming off, not remaining at the surface (1); moderate with the shark remaining at the surface for a period of time before swimming off (2); or poor in which the shark remained at the surface for an extended period of time and did not appear to swim away (3).

Recapture information was retrieved from commercial fishers, as well as from recreational fishers and research staff during commercial and fishery-independent sampling.

During 1994 to 1998 (the peak of the tagging effort), commercial shark fishers were provided with tag reporting forms that included all the relevant information to be recorded

(e.g., date and GPS co-ordinates of recapture, sex, fork length, condition of shark and tag) to improve the accuracy of the recapture information.

2.3.2 Data Analyses

All release and recapture data were compiled in a Microsoft Office Word (2007) database, which was analysed in R version 3.1.0 (R Core Development Team 2014). Data analyses mostly focused on sandbar, dusky, whiskery and gummy sharks, and occasionally caught

species with complete release and recapture records. Recaptures occurring within less than a day of release (4% of recaptures) were excluded from the data set on the assumption that these individuals had not fully recovered from the tag and release process, thus altering their normal movement behaviour. A Kolmogorov-Smirnov test was used to test whether shark size (fork length) differed between non-recaptured and recaptured individuals. It is vital to note that the fork length measurements reported for recaptured individuals are considerably less accurate than those measured at release due to the variation and inaccurate measurements made by commercial fishermen. To increase accuracy erroneous measurements were disregarded (i.e., measurements that were smaller than previously published size at birth records). Sex ratios were analysed using a Pearson’s Chi-Square test of independence.

Shark movement patterns were described using displacement distance, time at liberty, speed and the direction of displacement (bearing). Displacement distances were calculated as the straight line distance between release and recapture co-ordinates (e.g., using GPS co- ordinates as start and end movement trajectory points). Hence, displacements and speed are minimum estimates. Despite these records being minimum estimates, comparisons with similar studies can still be made allowing meaningful conclusions to be drawn and providing important insight on shark movement. The number of whole days between release and recapture dates were used to estimate time at liberty. Time at liberty was also used to calculate the average speed of movement with the number of whole days being divided by displacement distance. Bearings were determined from release and recapture co-ordinates following the shortest path (i.e., great circle distance). To avoid movement trajectories crossing over land five fixed GPS co-ordinates (Exmouth, Shark Bay, Margaret River, Albany,

Streaky Bay and Port Lincoln) were used to delineate the Australian coastline. Furthermore,

as part of the bearing analyses release and recapture co-ordinates were stratified into the following fishery zones: the combined West Coast Demersal Gillnet and Demersal Longline

(WCDGDLF) and Closed Area, Joint Authority Southern Demersal Gillnet and Demersal

Longline Fishery (JASDGDLF Zone 1) and the JASDGDLF (Zone 2)(Fig. 2.1). Displacement direction was analysed using Rao’s spacing test and Rayleigh’s uniformity test. Rao’s spacing test and Rayleigh’s uniformity test were used to test whether movements were uniformly distributed or directionally biased. The results from Rao’s spacing test were used as the main indicator of uniformity as this test is more suitable for bearing data that is not uni- modal or axially bimodal (Zar 1999).

I calculated the Root-Mean Square (RMS) displacement (i.e., the square root of the mean- square displacement) (following Whitehead et al. 2008) to describe the modal and exceptional speeds and dispersal of individuals across the great range of time scales from 1 day to 3 years. Root-Mean Squared displacement is a natural component of movement analyses that weights larger movement more heavily, but as squared displacement has no intuitive meaning, RMS displacement is used as this represents the actual movement

(Whitehead et al. 2008). Standard errors of the RMS displacement were estimated using the jackknife method.

For each species, I used Generalized Linear Models (GLM) to test the effect of several factors and covariates on movement patterns, using displacement, time at liberty and swimming speed as response variables. The independent variables fitted to the GLM were: species, time at liberty, sex, fork length and condition. All continuous variables were log transformed to improve the normality of variables. A normal distribution with an identity

link function was used for displacement distance and swimming speed. A Poisson distribution with a log link function was used for time at liberty.

2.4 Results

2.4.1 Data Summary

2.4.1.1 Release and Recapture Data for All Commercial Species

Since 1994, a total of 10,402 elasmobranches representing 53 species were tagged and released off the west Australian coast (Table 2.1, Appendix I). The four main commercial species comprised 78% of the released sharks (4,289 sandbar, 2,344 dusky, 842 gummy, and

659 whiskery sharks) (Table 2.1). More than 60% of the released species occasionally caught consisted of tiger, Galeocerdo cuvier (27%); blacktip, Carcharhinus limbatus & C. tilstoni

(9%); spot tail, C. sorrah (9%); milk, Rhizoprionodon acutus (9%); scalloped hammerhead,

Sphyrna lewini (5%); and pigeye, C. amboinensis (5%) sharks.

A total of 1,111 individuals representing 16 species were later recaptured. The four main commercial species contributed 96% to the total recaptures (482, 302, 158, and 129, for dusky, gummy, sandbar and whiskery sharks, respectively). Gummy sharks had the highest recapture rate (36%) followed by dusky (21%), whiskery (20%) and sandbar (4%) sharks

(Table 2.1). From species occasionally caught only 40 individuals were recaptured of which spinner sharks, Carcharhinus brevipinna, had the highest number of recaptures (n = 10).

Only three other species had five or more recaptures: western wobbegong, Orectolobus hutchinsi; copper whaler, C. brachyurus; and tiger, G. cuvier, sharks (Table 2.1). Recapture

rates were generally less than 15% except for shortfin mako (Isurus oxyrinchus) sharks for which 33% were recaptured (Table 2.1).

Table 2.1 The total number of sharks tagged, released and recaptured off the coast of Western Australia from 1994 to 2013. Species ordered by highest recaptures.

Species Common Name No. of No. of Recaptures Released Recaptured (%) Individuals Individuals Main Commercial Species Carcharhinus obscurus Dusky 2344 482 20.60% Mustelus antarcticus Gummy 842 302 35.90% C. plumbeus Sandbar 4260 158 3.70% Furgaleus macki Whiskery 659 129 19.60%

Occasionally Caught C. brevipinna Spinner 82 10 12.20% Orectolobus sp. Western 83 7 8.40% Wobbegong C. brachyurus Copper Whaler 79 6 7.60% Galeocerdo cuvier Tiger 604 5 0.80% C. cautus Nervous 57 2 3.50% Sphyrna zygaena Smooth 15 2 13.30% Hammerhead Hypogaleus hyugaensis Pencil 14 2 14.30% Isurus oxyrinchus Shortfin Mako 6 2 33.30% C. amblyrhynchos Grey Reef 54 1 1.90% C. taurus Grey Nurse 32 1 3.10% Pristis zijsron Green Sawfish 20 1 5.00% Orectolobus sp. Wobbegong 17 1 5.90%

2.4.1.2 Release and Recapture Locations for the Four Main Commercial Species

Sandbar sharks were tagged, released and recaptured across much of the west Australian coast extending from as far north as Derby (17° 21’ 5.20”, 123° 40’ 59.88”) and as far south as Albany (35° 1’ 22.08”, 117° 52’ 53.04”) (Fig. 2.2). Although, releases of tagged dusky sharks were widely distributed across the west Australian coast recaptures were highest in

the south-west. Two individuals were, however, recaptured as far east as Kangaroo Island

(35° 49’ 59.88”, 137° 15’ 18”) in South Australian waters (Fig. 2.2).

The majority of whiskery and gummy sharks were tagged and released across the States south-west and south (Fig. 2.2). Recaptures of whiskery sharks were highest in the south- west, with only a few individuals being captured north of Geraldton (28° 46’ 27.84”, 114° 36’

32.04”), and west of Kangaroo Island (Fig. 2.2). The majority of gummy sharks were recaptured along the south coast between Albany and Streaky Bay in South Australian waters (Fig. 2.2).

Figure 2.2 Release and recapture locations for the four main commercial species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; and gummy, Mustelus antarcticus) tagged off Western Australia between 1994 and 2013.

2.4.2 Size Composition of Non-Recaptured and Recaptured Sharks

The fork length of non-recaptured dusky sharks ranged from 53 to 300 cm in length (FL) with a large proportion of sharks being juveniles (Table 2.2, Fig. 2.3). A mixture of both juveniles and adults were observed for sandbar and whiskery sharks, measurements for these species ranged from 37 to 265 cm and from 81 to 150 cm, respectively (Table 2.2, Fig.

2.3). Gummy sharks primarily consisted of adults with fork length measurements ranging from 69 to 164 cm (Table 2.2, Fig. 2.3). The fork length measurements for non-recaptured species occasionally caught ranged from 50 cm for winghead hammerhead sharks, Eusphyra blochii, to 400 cm for tiger sharks, Galeocerdo cuvier (Table 2.2).

Fork length measurements for recaptured sandbar, dusky and whiskery sharks were relatively similar, with maximum lengths of 142, 143, 142 cm, respectively (Table 2.2, Fig.

2.3). Fork length measurements for recaptured gummy sharks were slightly larger with individuals ranging from 55 – 147 cm. Recapture fork lengths for species occasionally caught ranged from 51 cm for pencil sharks, Hypogaleus hyugaensis, to 142 cm for western wobbegongs, Orectolobus sp. (Table 2.2).

Sandbar sharks showed significantly smaller fork length measurements for non- recaptured individuals (P < 0.001). Fork length measurements for dusky sharks were also found to vary significantly (P = 0.003). However, these results are suggested to be an artefact of the different gears used throughout the tagging program. Furthermore, inaccurate fork-length measurements reported by commercial fishermen for recaptured sharks further reduced the accuracy and significance of these results. Fork length measurements for non-recaptured and recaptured whiskery and gummy sharks did not vary significantly (P > 0.05).

Table 2.2 The range in fork length (cm) of non-recaptured and recaptured sharks off Western Australia from 1994 to 2013. Species ordered by largest released fork length.

Non-Recaptured Recaptured (Fork Length) Fork Length Species Common Min. Max. Min. Max. Name Main Commercial Species Carcharhinus Dusky 53 300 - 143 obscurus C. plumbeus Sandbar 37 265 - 142 Mustelus antarcticus Gummy 69 164 - 147 Furgaleus macki Whiskery 81 150 - 142

Occasionally Caught Galeocerdo cuvier Tiger 63 400 65 113 Orectolobus sp. Western 45 397 66 142 Wobbegong Pristis zijsron Green Sawfish 80 289 - - C. brachyurus Copper Whaler 70 262 130 130 C. taurus Grey Nurse 95 254 - - Isurus oxyrinchus Shortfin Mako 82 195 61 69 C. brevipinna Spinner 65 163 27 140 C. amblyrhynchos Grey Reef 67 146 - - Sphyrna zygaena Smooth 58 122 127 127 Hammerhead Orectolobus sp. Wobbegong 75 120 - - Hypogaleus Pencil 79 97 51 51 hyugaensis C. cautus Nervous 52 93 - - - No data recorded or records were erroneous.

Figure 2.3 The size (fork length) distribution at release for non-recaptured and recaptured individuals for the four commercially targeted shark species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus). Arrows indicate female size at maturity with sizes attained from: McAuley et al. (2007) for sandbar sharks; Simpfendorfer et al. (2002) for dusky sharks; Simpfendorfer & Unsworth (1998) for whiskery sharks; and Walker (2007) for gummy sharks.

2.4.3 Sex Ratio of Released and Recaptured Sharks

The overall sex ratio was 1.25 females : 1 male for released sharks and 1.40 females : 1 male for recaptured sharks (Table 2.3). Significantly more females than males were recaptured for gummy (2.97 : 1, P < 0.001) and whiskery sharks (3.41 : 1, P < 0.001, Table

2.4). In contrast, no significant differences were observed between female and male sandbar (0.81 : 1, P = 0.198) and dusky sharks (0.97 : 1, P = 0.777, Table 2.4). The sex ratio of species occasionally caught showed a relatively even ratio of females and males for each species at both release and recapture (Table 2.3). The largest contrasting sex ratio for species occasionally caught was observed by western wobbegongs (Orectolobus sp.) with a sex ratio of 1 female to 2 males (Table 2.3).

Table 2.3 The sex ratio of released and recaptured individuals off Western Australia, from 1994 to 2013. Species ordered by largest number of released males.

No. of Released No. of Recaptured Individuals Individuals Species Common Name Males Females Males Females Main Commercial Species Carcharhinus Sandbar 2034 2171 86 69 plumbeus C. obscurus Dusky 1146 1144 239 232 Mustelus antarcticus Gummy 194 648 76 226 Furgaleus macki Whiskery 143 511 29 99

Occasionally Caught Galeocerdo cuvier Tiger 256 293 2 2 Orectolobus sp. Western 44 35 4 2 Wobbegong C. brevipinna Spinner 41 38 5 5 C. amblyrhynchos Grey Reef 41 13 1 - C. brachyurus Copper Whaler 33 44 5 1 C. cautus Nervous 23 34 1 1 Pristis zijsron Green Sawfish 12 6 - - C. taurus Grey Nurse 11 17 1 - Hypogaleus Pencil 8 6 1 1 hyugaensis Sphyrna zygaena Smooth 6 8 2 - Hammerhead Orectolobus sp. Wobbegong 6 11 1 - Isurus oxyrinchus Shortfin Mako 3 3 2 - TOTAL 4001 4982 455 638 - No data recorded.

Sex Ratio Sex Ratio (Release) (Recapture) X2 P X2 P Sandbar 4.47 0.035 1.66 0.198 Dusky 0.00 1.000 0.08 0.777 Whiskery 243.72 < 0.0001 73.52 < 0.0001 Gummy 205.94 < 0.0001 37.20 < 0.0001

2.4.4 Displacement, Time at Liberty and Swimming Speed

The maximum displacements of the four main commercial species were similar in magnitude: 2056, 2588, 2277, 2540 km for sandbar, dusky, whiskery and gummy sharks, respectively (Table 2.5). A considerably larger proportion of sandbar and dusky sharks were recaptured more than 100 km from release points than whiskery and gummy sharks (Fig.

2.4). The maximum displacements for species occasionally caught ranged from 1 km

(wobbegong) to 1,143 km (copper whaler). Four species were recorded to travel distances >

250 km (tiger, spinner, shortfin mako, grey reef). All remaining species travelled less than

130 km of which four individuals of three species (copper whaler, wobbegong, nervous) were recaptured within 1 km of the release site (Table 2.5).

The maximum time at liberty for the four main commercial species ranged from 3,072 to

5,730 days, observed by sandbar and dusky sharks, respectively (Table 2.5). Considerably more sandbar and whiskery sharks were at liberty for periods between 500 to 1,000 days than dusky and gummy sharks (Fig. 2.4). The maximum time spent at liberty for species occasionally caught ranged from four (nervous shark) to 5,245 days (tiger shark) with an

additional four species (spinner, western wobbegong, shortfin mako, wobbegong) at liberty for more than 1,000 days. Maximum time at liberty exceeding 100 days was observed by four species (copper whaler, smooth hammerhead, grey reef, green sawfish). All remaining species were reported to be at liberty for less than 100 days (pencil, grey nurse, nervous)

(Table 2.5).

Maximum speeds of 1.90, 1.94, 1.71, 0.62 km/hr were attained for sandbar, dusky, whiskery and gummy sharks, respectively (Table 2.5). Overall, dusky and sandbar sharks maintained faster speeds than whiskery and gummy sharks (Fig. 2.4). Most individuals of these species, however, showed speeds < 0.1 km/hr (Fig. 2.4). Maximum speeds for species occasionally caught ranged between < 0.010 (wobbegongs) and 0.420 km/hr (copper whaler). The maximum speed reached by most species was < 0.100 km/hr (Table 2.5).

Displacement Time at Speed (km) liberty (days) (km/hr) Species Common Name Min. Max. Min. Max. Min. Max. Main Commercial Species Carcharhinus Dusky 1.14 2588.50 1 5733 < 0.01 1.94 obscurus Mustelus Gummy 0.30 2540.10 1 3410 < 0.01 0.62 antarcticus Furgaleus macki Whiskery 0.52 2278.00 1 5577 < 0.01 1.71 C. plumbeus Sandbar 1.34 2056.00 1 3072 < 0.01 1.90

Occasionally Caught C. brachyurus Copper Whaler 0.98 1143.30 33 880 < 0.01 0.42 Galeocerdo Tiger 33.92 707.56 173 5245 < 0.01 0.01 cuvier Carcharhinus Spinner 4.23 571.64 149 2640 < 0.01 0.04 brevipinna Isurus oxyrinchus Shortfin Mako 113.35 316.47 410 1242 < 0.01 0.03 C. amblyrhynchos Grey Reef 292.82 292.82 399 399 0.03 0.03 Sphyrna zygaena Smooth 99.29 122.44 43 706 0.01 0.12 Hammerhead Orectolobus Western 3.33 76.11 203 1508 < 0.01 < 0.01 hutchinsi Wobbegong Hypogaleus Pencil 59.98 59.98 66 66 0.04 0.04 hyugaensis Pristis zijsron Green Sawfish 47.15 47.15 124 124 0.02 0.02 Carcharias taurus Grey Nurse 11.74 11.74 52 52 0.01 0.01 C. cautus Nervous 0.58 0.58 4 4 0.01 0.01 Orectolobus sp. Wobbegong 0.70 0.70 1095 1095 < 0.01 < 0.01 - No data recorded.

2.4.5 Displacement Direction

Releases from the WCDGDLF and Closed Area Zone showed that a large proportion of sandbar, dusky and whiskery sharks travelled in a S - SSW bearing trajectory (Fig. 2.5). All species were also observed to travel in a NNW direction (Fig. 2.5). The displacement direction of sandbar and dusky sharks varied significantly within the zone (Table 2.6). The movement trajectory of tagged and released sharks within the JASDGDLF (Zone 1) of all four species largely followed a direct N or E bearing trajectory (Fig. 2.5). A large proportion of dusky, whiskery and gummy sharks were also observed to travel in an E to SE direction (Fig.

2.5). ROA’S spacing test confirmed that the movement trajectory of sandbar, dusky and whiskery sharks varied significantly in this zone (Table 2.6). However, Rayleigh’s test suggested that only the movements of released sandbar and dusky sharks varied significantly (Table 2.6). Displacement direction by all species within Zone 2 of the JASDGDLF predominantly followed a ENE and WSW bearing trajectory (Fig. 2.5). Rao’s spacing showed that the displacement direction of sandbar, whiskery and gummy sharks varied significantly

(Table 2.6), but Rayliegh’s test did not find any significant differences in bearing trajectory for the four species (Table 2.6).

WCDGDLF & JASDGDLF JASDGDLF Closed Area (Zone 1) (Zone 2) Test P Test P Test P statistic statistic statistic ROA’s Test Sandbar 193.10 0.001 238.29 0.001 174.43 0.010 Dusky 190.04 0.001 150.13 0.001 137.79 0.100 Whiskery 158.22 0.100 163.31 0.010 181.19 0.010 Gummy - - 137.25 0.100 180.28 0.001

Rayleigh’s Test Sandbar 0.30 0.001 0.74 0.001 0.26 0.163 Dusky 0.25 0.005 0.14 0.002 0.17 0.385 Whiskery 0.13 0.786 0.21 0.499 0.24 0.208 Gummy - - 0.20 0.485 0.11 0.048 - It was not possible to compute the RAO’s and Rayleigh’s test for gummy sharks due to the small sample size.

2.4.6 Root-Mean Squared Displacement

The root-mean square displacement distance of sandbar, dusky, whiskery and gummy sharks off Western Australia increased with time at liberty, particularly after 12 months

(Fig. 2.6). The RMS displacement was similar for all species after one month but started to differ between species after this time (Fig. 2.6). The shortest RMS displacements were estimated for whiskery sharks at each time and the longest for dusky sharks (Fig. 2.6). The estimated RMS displacement for whiskery sharks was 59 km at 6 months and 367 km at 3 years, corresponding values for dusky sharks were 223 km and 761 km (Fig. 2.6).

2.4.7 Generalised Linear Models

The GLM to examine the displacement distance of tagged sharks as a function of time at liberty, species, size, sex of shark and condition at release, fitted time at liberty, species and size as significant terms in the model that together explained 24% of the deviance

(Table 2.7, Appendix II). The model predicted mean displacement distances for sandbar and dusky sharks were similar (≈ 150 km), and at least three times further than those for whiskery and gummy sharks (≈ 30 to 50 km, Fig. 2.7).

The time at liberty of tagged sharks as a function of species, size, and release condition were fitted as significant terms in the GLM model for time at liberty and together accounted for 8% of the deviance (Table 2.7, Appendix III). The predicted mean times at liberty were longer for dusky and gummy sharks than those predicted for sandbar and whiskery sharks

(Fig. 2.7).

Species was the only term fitted in the GLM for speed of movement and accounted for

10% of the deviance (Table 2.7, Appendix IV). The mean predicted speeds were higher for sandbar and dusky sharks (0.004 to 0.005 m/sec), and lowest for whiskery sharks (< 0.001 m/sec) with an intermediate value for gummy sharks (0.002 m/sec, Fig. 2.7).

Displacement Time at Liberty Swimming Speed Distance Factor Deviance P Deviance P Deviance P Time at 516.615 < 0.001 — — — — liberty Species 135.961 < 0.001 82.777 < 0.001 275.802 < 0.001 Fork 19.997 0.003 4.533 0.033 11.908 0.043 Length Sex 0.182 0.778 0.099 0.754 1.7128 0.442 Condition 4.043 0.415 12.244 0.002 0.605 0.901 - Not fitted to the Generalised Linear Model.

2.5 Discussion

In the present study, the movement patterns of several shark species commercially targeted off the coast of Western Australia, with a key focus on the four main species

(sandbar, dusky, whiskery, gummy) were analysed and described from data collected through a long-term (1994 to 2013) conventional tagging program by the Department of

Fisheries, Western Australia. The results from the data confirmed our initial hypothesis that displacement distance, time at liberty and swimming speed between the four main species varied significantly. Displacements were found to strongly correlate with time at liberty and size of the shark. The Generalised Linear Model predictions suggested mean displacement distances for sandbar and dusky sharks were similar and considerably larger than those for whiskery and gummy sharks. Significant differences were observed between sex ratios for whiskery and gummy sharks at release and recapture, with a significantly higher proportion of females. The fork length measurements of non-recaptured and recaptured sandbar and dusky sharks were confirmed to significantly vary.

The highest recapture frequency for all species occasionally caught was recorded by spinner sharks (Carcharhinus brevipinna), having ten recaptures. Maximum displacements ranged from 0.70 to 1,143 km and were observed by wobbegongs (Orectolobus sp.) and copper whaler (Carcharhinus brachyurus) sharks, respectively. The maximum time at liberty ranged from 4 to 5,245 days for nervous (Carcharhinus cautus) and tiger (Galeocerdo cuvier) sharks, respectively. The estimated maximum swimming speed for occasionally caught species peaked at 0.42 km/hr for copper whaler (Carcharhinus brachyurus) sharks.

Swimming speeds for all other species were less than 0.03 km/hr. No statistical analyses were completed for the species only occasionally caught.

Displacement Distance and Time at Liberty for the Four Main Commercial Species

Sandbar and dusky sharks tagged in the study were predicted on average to have much larger displacements (> 100 km) than whiskery and gummy (< 50 km) sharks. However, occasional large-scale displacements of more than 2,000 km were observed for all four species. The displacement patterns observed for sandbar and dusky sharks in the study are comparable to those of sharks tracked in Chesapeake Bay, Virginia, and Mozambique, South

Africa, respectively (Grubbs 2001; Hussey et al. 2009). Mean space utilization reported by these studies for sandbar and dusky sharks ranged from 39.6 km to 275.8 km and from 1 km to 200 km, respectively (Grubbs 2001; Hussey et al. 2009). Large-scale (> 1,000 km) displacements recorded in these studies were also similar to those reported in the present study with maximum displacements of 2,800 km and 1, 374 km, for sandbar and dusky sharks, respectively.

Due to the limited literature available for whiskery and gummy shark movements, fewer comparisons are possible. However, previous conventional tagging studies on closely related species (leopard, Triakis semifasciata, and brown smoothhound sharks, Mustelus henlei) reported all recaptures (n = 3) to occur within 1 km of the release site (Hopkins & Cech

2003). Furthermore, displacements by leopard and brown smoothhound sharks after three months are suggested to typically range from 140 km to 160 km (e.g., Compagno 1984;

Talent 1985; Smith & Abramson 1990; Hopkins & Cech 2003).

In the first month after tagging, the displacement distances were small (ranging from 11 to 53 km) and did not vary greatly among the four main commercial species, indicating that the speeds of travel were relatively similar. However, the displacement distance started to diverge after 3 months and large differences were evident among the four species after 12

months (ranging from 107 to 307 km). The results fitting the Root-Mean Square displacement to time at liberty showed that sandbar and dusky sharks are predicted to move much larger distances with increased time at liberty than whiskery and gummy sharks.

Despite gummy sharks showing substantial movements after a period of one year, the large discrepancies and considerable estimated errors suggested predicted displacements to be imprecise representations of true movement. Similar durations at liberty have been reported for sandbar (Grubbs et al. 2005) and dusky sharks (Hussey et al. 2009) in

Chesapeake Bay, Virginia and Mozambique, South Africa, respectively. Time spent at liberty for these species ranged from 2 to 2,812 days and 4 to 2,525 days, respectively. Although little information appears to be available on the movement of whiskery sharks, investigations on the closely related leopard shark, Triakis semifasciata, provides some basis for comparison. Individuals of this species have been reported to be at liberty for up to

3,652 days (Smith 2001). Furthermore, conventional tagging studies conducted by Xiao et al.

(1996) reported times at liberty for tagged gummy sharks (Mustelus antarcticus) to range from 52 to 3,900 days.

Estimated Swimming Speeds for the Four Main Commercial Species

The estimated swimming speeds, based on the displacement distance from the locations of recapture and release and the time at liberty, varied significantly among the four main commercial species. The results from the GLM model of predicted swimming speeds showed that Carcharhinid sharks travelled at faster speeds on average than whiskery and gummy sharks. The swimming speeds reported for sandbar sharks in my study are similar to those published by Medved & Marshall (1983), who reported maximum speeds to range

from 1.54 to 2.00 km/hr. The swimming speeds for dusky sharks were within the range of previous estimates by Kohler et al. (1998) and Davies & Joubert (1967), who reported swimming speeds of 1.70 km/hr and 2.45 km/hr, respectively. Although, direct comparisons cannot be made with other studies for whiskery sharks, the maximum swimming speed for the closely related leopard shark, Triakis semifasciata, has been documented as 0.86 km/hr

(Nosal et al. 2013), which is about half the maximum speed recorded in the current study

(1.7 km/hr). Average speed estimates for gummy sharks presented in the present study were lower than previously record by Barnett et al. (2010), who reported an average swimming speed of 0.17 km/hr. Distinct differences in swimming speeds among species may arise from morphological, biological and behavioural differences. For example, the preference of slow or stationary prey items such as crabs, sipunculids and polychaete worms has the potential to considerably lower mean swimming speeds. In contrast, the preference of fast highly motile species such as teleosts, turtles, or small elasmobranches are likely to increase mean swimming speed.

Direction of Displacement for the Four Main Commercial Species

The bearing trajectories between release and recapture locations recorded in the study also differed significantly among the four main commercial species in each of the three commercial fishing zones. The bearing trajectory of small-scale movements (< 200 km) is thought to continually change in response to several biotic and environmental factors

(Simpfendorfer & Heupel 2004). The most commonly cited biotic factors often include predator avoidance, prey availability and distribution and competition (Simpfendorfer &

Heupel 2004). Moreover, continuously changing environmental conditions such as water temperature, salinity, dissolved oxygen and lunar phases are also known to considerably

influence displacement and thus bearing (Simpfendorfer & Heupel 2004). The direction of large-scale displacements are often considered to be more stable, having fixed trajectories in contrast to those observed at finer scales (Klimley 1993). It is likely a range of factors that facilitate and assist an individual’s survival (e.g., increased prey availability, reduced predators or favourable temperatures for breeding) may be responsible for increased trajectory stability (Klimley 1993).

The Effects of Size on Movement

Large-scale displacements were observed to be most frequently undertaken by larger individuals (> 130 cm). Size was found to be a significant term in the GLM model. These results suggest that larger individuals move longer distances than smaller conspecifics.

These findings are similar to those from previous studies on lemon sharks, Negaprion brevirostris (Morrissey and Gruber 1993) and leopard sharks, Triakis semifasciata (Ackerman et al. 2000), who also reported displacement to positively correlate to size. The large-scale movements observed by sandbar and dusky sharks in the current study are thought to reflect movement to more favourable breeding grounds located in the States north-west.

Juveniles are thought to remain in the temperate waters of the south-west for several years before attaining suitable sizes for the gradual northward migration, joining the population in the north-west as sub-adults or adults (McAuley et al. 2005).

Fork length measurements of non-recaptured and recaptured sandbar and dusky sharks were found to significantly differ, however these differences were attributed to changed gear-selectivity. The reported recapture measurements were also considered erroneous due to inaccurate measuring by commercial fishermen.

Sex Ratio’s for the Four Main Commercial Species

Results from the present study verified sex ratios at recapture differed significantly for whiskery and gummy sharks. In contrast, no significant variations were confirmed for sandbar and dusky sharks. A larger proportion of female whiskery and gummy sharks were recaptured than males. Several elasmobranch species (e.g., white and hammerhead sharks) are known to school by sex or size especially in pupping or nursery areas (Klimley 1987;

Domeier & Nasby-Lucas 2012). However, research investigating these patterns for whiskery and gummy sharks is limited.

Conclusions

Although occasional large-scale movements (> 2,000 km) were observed for all four main commercial species, most sharks were observed to travel < 200 km, indicating a degree of philopatry for all four species. Increasing evidence of philopatry in various shark species suggests management measures to be most effective at small-spatial scales with a key focus on essential areas such as nursery, foraging, breeding and pupping grounds (Hooker &

Gerber 2004; Speed et al. 2010). The implementation of spatial closures and establishment of permanent closures for breeding grounds and offshore nursery areas for the four main commercial species would enhance the protection of these species throughout important life stages and enhance their conservation. Temporary closures during breeding seasons when aggregations are ephemeral could also serve as valuable conservation measures

(Heupel & Simpfendorfer 2005). The spatial and temporal scales at which these regions should be established will need to be determined by further research. To ensure management measures remain effective, further long-term research investigating the use of

offshore areas as nurseries and breeding grounds in the south-west and north-west, respectively, for sandbar (Carcharhinus plumbeus) and dusky (Carcharhinus obscurus) sharks is required. Additionally, long-term investigations into the sexual segregations of whiskery

(Furgaleus macki) and gummy (Mustelus antarcticus) sharks should also be examined.

Describing these aspects of coastal shark ecology and behaviour for sympatric species will minimise the risk of overexploitation of these vulnerable populations.

3. Evaluating the frequency of predation attempts by sharks on bottlenose dolphins (Tursiops aduncus) off the coast of Bunbury, Western Australia.

3.1 Summary

It has been assumed that direct shark predation and the risks of shark predation on small

Odontocetes are relatively minor. Recent evidence, however, suggests that several shark species regularly hunt and prey upon a range of small Odontocetes. In this study, I investigated shark and bottlenose dolphin (Tursiops aduncus) interactions off the coast of

Bunbury, Western Australia. I analysed the prevalence of external injuries from the extensive transect dolphin surveys conducted between 2007 and 2014. A total of 69 dolphins were considered to display shark-inflicted injuries. Of these dolphins, 58 (84%) were photographed systematically (while conducting a survey), and 11 (16%) opportunistically (between surveys). Photo-identification catalogues previously compiled from quantitative surveys of the Bunbury and Busselton dolphin populations were used to identify individuals. Total bite mark frequencies of systematically photographed dolphins varied significantly among age classes (calves, juveniles, adults) with the highest frequency of injuries sustained by adults (X2 = 38.436, P < 0.001). Bite frequencies between sexes; and between mothers with and without calves were not found to significantly differ (X2 = 0.111,

P = 0.738; X2 = 1.316, P = 0.251, respectively). The total frequency of shark bites was significantly lower in the austral autumn and winter months than in the spring and summer

(X2 = 15.333, P = 0.002). However, the frequency of fresh injuries was much higher in the summer of 2013 (n = 8), than in other seasons (range = 0 - 1). When the data for 2013 were removed from the analyses, the frequency of bites although higher in summer (pooled over years) was no longer significantly higher than other seasons (X2 = 3.889, P = 0.274). The total frequency of injuries did not significantly differ among years (2008 – 2013) (X2 = 4.948, P =

0.422). Evaluation of the photographed bite marks by three independent reviewers suggested that the shark species responsible were most likely white (Carcharodon

carcharias), tiger (Galeocerdo cuvier) and several smaller Carcharhinid species. The results from this study suggest that direct shark predation and the risk of shark predation are important factors that influence the population dynamics, distribution and behaviour of the

Bunbury dolphins.

3.2 Introduction

The risk of predation is a major evolutionary driving force across a vast array of taxa (Lima

& Dill 1990). Selective pressures caused by predation influence the behaviour, physiological development and biological processes of many prey species (Lima & Dill 1990; Werner &

Peacor 2003; Dill et al. 2003). Increasing evidence suggests that a number of shark species not only scavenge on Odontocetes remains but actively hunt and predate living individuals

(Heithaus & Dill 2006; Wirsing et al. 2008). Although direct visual observations of these events are rare, fresh wounds and scars on small Odontocetes can be quantified to provide indirect measures of the predation risk posed from sharks (Wood et al. 1970; Heithaus

2001a). However, as scars and wounds represent failed predation attempts the true frequency of shark attacks on individuals is often much higher than that measured by wound frequencies (Heithaus 2001a). Despite wounds and scars providing an underestimate of predation threat, comparisons between dolphin populations facing predation from similar shark species provide a relative index of shark predation (Heithaus 2001a).

In a review of the interactions between sharks and dolphins, Heithaus (2001b) suggested that white (Carcharodon carcharius), tiger (Galeocerdo cuvier), bull (Carcharhinus leucas), sixgill (Hexanchus griseus) and sevengill (Notorynchus cepedianus) sharks were frequent predators of Odontocetes. Dusky (Carcharhinus obscurus) and oceanic whitetip

(Carcharhinus longimanus) sharks also predate on living Odontocetes occasionally (Last &

Stevens 1994; Long & Jones 1996). Stomach content analysis has confirmed Odontocete remains in shortfin mako (Isurus oxyrinchus), pacific sleeper (Somniosus pacificus), and greenland sleeper (Somnious microcephalus) sharks. Although, it is still unknown whether these remains were derived from scavenging events or attacks on living Odontocetes

(Heithaus 2001b).

Direct shark predation attempts on dolphin populations has been reported at several locations around the globe, including the Abrolhos Bank, Brazil (Bornatowski et al. 2012),

Natal, South Africa (Cockcroft et al. 1989a), Sarasota, Florida (Urian et al. 1998), and the

Adriatic Sea (Bearzi et al. 1997). In Australia, predation by sharks on bottlenose dolphins has been assessed in Moreton Bay, Queensland (Corkeron et al. 1987a), Shark Bay, Western

Australia (Heithaus 2001a), and Cockburn Sound, Western Australia (Ham 2009).

The impact of predation on prey populations depends on prey vulnerability, the biological characteristics of the prey and population immigration/emigration rates (Cooper et al. 1990;

Lancaster et al. 1991). Predation may directly reduce a population or alternatively cause a range of trait-mediated effects. Due to low reproductive rates (inter-birth period of 3 to 6 years) and high calf mortality (Connor et al. 2000; Mann et al. 2000) of Indo-Pacific bottlenose dolphins (Tursiops aduncus), population growth is usually slow with prolonged periods required for populations to recover if they are reduced. Bottlenose dolphins are also slow to reach sexual maturity, with females attaining maturity at 9 - 11 years of age and males from 11 - 15 years (Cockcroft & Ross 1989). Moreover, bottlenose dolphins often show a high degree of site fidelity and meta-population structure, which means that locally populations may be highly vulnerable to predation (Möller et al. 2002). The combination of

these traits makes populations of bottlenose dolphins particularly susceptible to predator impacts and other sources of mortality.

Dolphin abundance within the Bunbury area is thought to range from a minimum of 63

(95% confidence interval, CI = 59 - 73) individuals to a maximum of 139 (95% confidence interval, CI = 134 - 148) (Smith et al. 2013). Abundance is suggested to vary seasonally with fewer dolphins present in the area during winter (June - August) than in summer (December

- February). A seasonal influx of dolphins is also thought to occur in early autumn (March)

(Smith et al. 2013). The seasonal fluctuation in abundance is likely caused by an influx of adult males into the area during the breeding season (summer/autumn). As winter approaches, the adult males disperse. Males are often sighted travelling in much smaller groups typically consisting of less than four individuals (Möller et al. 2001; Wells et al. 2002).

The behaviour of the Bunbury dolphin population is similar to that reported for other bottlenose dolphin (T. aduncus) populations near Shark Bay, Western Australia (Mann &

Smuts 1998) and Bahia San Antonio, Argentina (Vermeulen & Cammareri 2009).

The aim of this study was to quantify trends of shark predation attempts on bottlenose dolphins (Tursiops aduncus) off Bunbury, Western Australia using the bite marks found on individuals photographed from the dolphin surveys conducted from 2007 to 2013. I investigated whether predation attempts differed between age class, sex, calf presence, seasons and years. Three independent experts were consulted in an attempt to identify the shark species responsible.

3.3 Materials and Methods

3.3.1 Study Site

Geographe Bay is located off Western Australia approximately 220 km south-west of

Perth (Fig. 3.1). The northward facing embayment extends 100 km from Cape Bouvard in the north to Cape Naturaliste in the south-west. The area typically experiences a

Mediterranean climate with cool, wet winters and warm, dry summers (Varma et al. 2010).

The average annual rainfall recorded for Bunbury from 1995 to 2014 was 734 mm (Bureau of Meteorology 2014a). The long-term annual mean maximum air temperature for Bunbury was 23.1°C and the minimum was 11.1°C. During the middle of winter (July) the mean maximum temperature was 17.3°C (minimum = 7.0°C), while during the middle of summer

(February) the mean maximum was 30.1°C (minimum = 15.9°C, Bureau of Meteorology

2014a). Sea surface temperatures within the area typically range from 14.8°C in winter to

21.6°C in summer (McMahon et al. 1997). Geographe Bay sea surface temperatures are thought to closely correspond to seasonal air temperature cycles, primarily being driven by air-sea exchange processes (Pearce & Pattiaratchi 1999). The salinity in Geographe Bay ranges from 33.1 to 37.2 ppt (SKM 2003), with the area having meagre salinity stratification

(SKM 2003).

The 2007 to 2010 study area comprised of 120 km2 of coastal waters. In 2011 the area was expanded to encompass 540 km2. The study area extended approximately 9.26 km2 offshore and 100 km2 parallel to the coast. A total of three transects (Buffalo inshore,

Backbeach inshore, Inner waters) were initially used to survey the area. However, in 2011 this was increased to six transects with the addition of Buffalo offshore, Backbeach offshore, and Busselton (Fig. 3.1). The maximum water depth recorded for offshore transects was 22

m, whilst sections of inshore transects were < 1 m (McMahon et al. 1997; K. Sprogis,

Murdoch University, pers. comm.).

The Bunbury dolphin population is continuously exposed to a range of natural and anthropogenic threats. The most harmful of these include propeller strike from boat traffic throughout the harbour, inlet and estuary, entanglement in discarded fishing gear, and habitat modification through dredging and port modifications (Smith 2012). Furthermore, these dolphins are a primary tourist attraction with facilitated interactions between humans and dolphins regularly conducted at the Bunbury Dolphin Discovery Centre (Smith 2012).

Figure 3.1 Study location and associated transects used for systematic dolphin surveys near Bunbury, south-western Australia (Image provided by Kate Sprogis).

3.3.2 Data Collection

All dolphin data and photographs were collected as part of the PhD studies of Holly Smith

(2007 - 2009) and Kate Sprogis (2010 - 2013). The research was also continued for an additional year by research associate Randall Counihan (2013 - 2014). Dorsal fin photographs were compiled to form the Busselton and Bunbury fin identification catalogues. Full details of the dolphin surveys and data collection methods are described in

Smith (2012) and Smith et al. (2013). A brief summary of this methodology is provided below.

Data were collected through year-round boat based surveys aboard a 5 m research vessel which followed predetermined transect lines within the 540 km2 study area. Surveys were conducted by two to five observers, in a Beaufort Sea State of less than three. One field day of effort was defined as a survey with each dolphin group encounter during surveys termed as a sighting. For each sighting, the GPS coordinates, environmental conditions, group size, identification and behaviour of the dolphins were recorded. A sighting ceased once all individuals had been photographed and the survey had exceeded 5 minutes. The research vessel was then repositioned back to the location from which it departed the transect and the survey recommenced. Sightings observed during a survey were considered systematic while sightings observed between surveys and off transect were considered opportunistic

(Table 3.1).

Table 3.1 The number of systematic and opportunistic sightings and total survey effort (time spent on transect) for each year from 2007 to 2014 in the Bunbury region.

Year No. of Systematic No. of Opportunistic Survey Effort Sightings Sightings (hr) 2007 220 0 248.60 2008 294 4 366.81 2009 301 5 375.09 2010 219 2 343.39 2011 227 11 339.68 2012 261 8 441.46 2013 163 26 297.62 2014 42 5 59.04 TOTAL 1727 61 2471.69

Sea surface temperature data collected throughout the study provides important background information, however, it is vital to note these temperatures were derived from the depth sounder aboard the research vessel and were not scientifically calibrated. The values reported for the Southern Oscillation Index (SOI) were attained from the Bureau of

Meteorology (2014b). Sustained negative SOI values below -8 indicate El Niño episodes.

During El Niño episodes the Pacific Trade Winds typically decrease in strength allowing warm water to accumulate in the central and eastern tropical Pacific Ocean. As a result the coastal waters off Australia are often slightly cooler. In contrast, sustained SOI values of +8 indicate La Niña episodes. La Niña episodes are associated with strong Pacific Trade Winds and warmer sea surface temperatures to the north of Australia. These conditions act as an additional warm water source for the Leeuwin Current, which transports warm, tropical water down the west coast of Australia.

Several methods were employed to accurately determine the biological characteristics of dolphins such as age and sex. Age was estimated from size and behavioural characteristics

(Table 3.2). Furthermore, the approximate date of birth for calves conceived during the study period was also recorded. Sex was determined primarily through behavioural

characteristics, with adult dolphins consistently sighted with a calf in the infant position being classed as females. Residual adults were sexed either from visual observations of the genital area or from genetic analysis of biopsy samples (Smith 2012). The age and sex of several individuals are yet to be determined.

Table 3.2 The age classification of bottlenose dolphins, Tursiops aduncus, in the Bunbury region of south-western Australia as used by Smith (2012), Smith et al. (2013).

Age Class Size Behaviour Calf 1 - 1.5m Continuously maintaining infant position under the peduncle and tail fluke of the mother

Juvenile 1.5 - 2m No longer maintaining infant position (three consecutive sightings independent of the mother), but not yet sighted with a calf of their own

Adult > 2m Sexually mature (indicated by the presence of a calf maintaining infant position)

3.3.3 Injury Classification

All photographs of delphinids exhibiting wounds or scars, semi circular in shape, having deep craters or messy lacerations were considered as evidence of a shark-dolphin interaction (following Heithaus 2001a; Luksenburg 2014). The bite marks from these photographs were also cross-referenced with bite marks on photographs from published attacks (e.g., Corkeron et al. 1987a; Heithaus 2001a; Luksenburg 2014). Dolphins photographs with shark-inflicted injuries were extracted from the data set. The dorsal fin of each injured dolphin was compared to the fins in the Busselton and Bunbury fin identification catalogues to identify individual dolphins. Identifications were primarily made using predominant fin features such as marks, indentations and scars on the leading and trailing edge of the dorsal fin (following Smith et al. 2013). Secondary features such as

pigmentation, overall fin shape, scarring on the body and peduncle were also used to assist identification.

3.3.4 Estimated Injury Age

Each photograph was examined in an effort to determine the approximate date of attack and wound age. Bottlenose dolphin healing rates typically vary with the severity of the injury, however, even the most severe wounds have been reported to almost completely heal within a period of 5 - 8 months (Corkeron et al. 1987b; Bloom & Jager 1994; Visser

1999). The age of the wound was estimated based on the last sighting of the individual prior to the wound appearing. However, as individuals were not always regularly photographed the wound age was also estimated through comparisons to previously documented wounds of known age (Corkeron et al. 1987b; Wells et al. 2008; Elwen & Leeney 2010). Injuries were classified as open, intermediate or scar, based on the approximate wound age (Fig. 3.2,

Table 3.3).

(a) (b) (c)

Wound Category Approximate Age Description (months) 1. Open < 2 Subdermal tissue apparent, at times down to the muscle; often pink colouration; usually associated with crater.

2. Intermediate 2 to 6 Contraction of epidermis evident; more than 50% change in shape from the original wound (outline of a forming scar); subdermal tissue may be evident but not predominant and wound has not completely closed.

3. Scar > 6 Completely healed wound, typically with change in original skin pigmentation colour.

3.3.5 Dentition and Bite Characteristics

Without direct visual observations it is often difficult to correctly identify the species of shark responsible for bite marks left on living Odontocetes (Long & Jones 1996). In an attempt to identify the species of shark responsible for the predation attempts, photographs of all potential shark wounds were sent to three independent reviewers (Dr M.

Heithaus, Professor G. Burgess and Dr R. McAuley). All reviewers had prior experience in identifying shark species from wounds left on prey and an extensive knowledge of the shark species found off Western Australia. A brief description of the typical dentition and bite characteristics of the most likely shark species responsible is provided below.

Potential Odontocete predators for the south-west region of Western Australia are likely to reflect those documented by Heithaus (2001b). Shark species commonly found throughout the area include white, bull, whaler, oceanic whitetips, mako, tiger and sevengill sharks (Daley et al. 2002). Bites inflicted from Carcharhinid sharks are often distinguished as being highly ovate with triangular punctures, with jaggered tears. These sharks typically show distinct separation between the upper and lower jaws (Long & Jones 1996; M.

Heithaus, Florida International University, pers. comm.). Mako sharks also have crescent shaped jaws, typically with numerous rows of extremely narrow teeth (Long & Jones 1996).

In contrast, tiger sharks have a much broader bite with a less defined arc. The upper and lower jaws of a tiger shark are typically lined by large, widely spaced teeth of equal size

(Long & Jones 1996; M. Heithaus, Florida International University, pers. comm.). These sharks tend to leave messy, slashing bites with the upper and lower jaw impressions not being clearly defined (M. Heithaus, Florida International University, pers. comm.). The dentition of sevengill sharks often includes wide, comb-shaped teeth in the lower jaw used for tearing and cutting, while the upper jaw comprises of sharp, jagged teeth (Lucifora et al.

2005).

3.3.6 Data Analyses

Data were compiled in a Microsoft Office Excel (2007) file, which was later exported to R version 3.1.0 (R Core Development Team 2014), where a Pearson’s Chi-Square test of independence was used to test for any significant differences among variables (e.g., age class, sex, presence of a calf, season and annual variations). Variations in the frequency of bite marks among age classes used all available data.

Months were assigned to the austral seasons of: summer: December - February; autumn:

March - May; winter: June - August; and spring: September - November. Years with incomplete seasonal data were excluded from statistical analyses. The seasonal analyses also excluded all bites that were classed as intermediate or scars due to the uncertainty of the season when these injuries were attained. Injuries classed as scars were also excluded from the annual analyses due to the level of imprecision in determining the true wound age.

Seasonal and annual bite frequencies per km of transect were also calculated from standardised effort. The systematic surveys covered a distance of 10,049 km from 2007 until

2009, and 16,317 km from 2010 until 2014, when additional offshore transects were added to the systematic dolphin surveys.

3.4 Results

3.4.1 Environmental Conditions

The sea surface temperatures recorded from the depth sounder ranged from a maximum of 32.1°C in February 2011 to a minimum of 8.6°C in July 2012 (Fig. 3.3). Mean sea surface temperatures recorded from the vessel appeared to show little variance across years, with the exception of distinct seasonal peaks.

30.00 Mean SST

25.00

C) 20.00 o

15.00

Mean SST ( SST Mean 10.00

5.00

0.00 SU AU WI SP SU AU WI SP SU AU WI SP SU AU WI SP SU AU WI SP SU AU WI SP 2008 2009 2010 2011 2012 2013 Season

Sustained negative Southern Oscillation Index (SOI) values below −8 were observed from winter 2009 through until autumn 2010 (Fig 3.4). Negative SOI values were also recorded from autumn 2012 through to spring 2012. Sustained positive SOI values above +8, showing

La Niña conditions were observed on two separate occasions; during the summer of

2008/09; and from the winter of 2010 to autumn 2011 (Fig. 3.4). The extremely strong La

Niña event of 2010 and 2011 raised sea surface temperatures by 2 - 4 °C above long-term averages along the coast of Western Australia (Thomson et al. 2014).

25.00 SOI 20.00

15.00

10.00

5.00 SOI Index SOI 0.00

-5.00

-10.00 SU AU WI SP SU AU WI SP SU AU WI SP SU AU WI SP SU AU WI SP SU AU WI SP 2008 2009 2010 2011 2012 2013 Season Figure 3.4 The seasonal values for the Southern Oscillation Index (SOI) between 2008 and 2013. Values > 8 show La Niña conditions; < - 8 show El Nino conditions (data sourced from the Bureau of Meteorology 2014b).

3.4.2 Predation Attempts

3.4.2.1 Data Summary

A total of 599 dolphin surveys were conducted using line transects over the eight years resulting in 1,727 systematic dolphin sightings. A total of 69 dolphins were photographed with shark-inflicted injuries. Of these individuals 64 dolphins could be accurately identified from the Busselton and Bunbury fin identification catalogues. The age structure of individuals with bite marks was 43 adults, 12 juveniles, 11 calves and three dolphins of unknown age. The sex ratio consisted of 30 females, 23 males and 16 individuals of unknown sex.

3.4.2.2 Opportunistic Sightings

Eleven of the 69 (16%) individuals postulated as having shark-inflicted injuries were sighted opportunistically (Table 3.4). The majority of these individuals were calves and juveniles, with only three adults. The sex ratio consisted of two males, five females and four individuals of unknown sex (Table 3.4). All eight open wounds (i.e., fresh) were observed during the warmer seasons, with six in summer and two in spring. Fresh and intermediate wounds were only recorded in 2012 (2), 2013 (4) and 2014 (3).

Table 3.4 The individual identity and wound categories recorded from opportunistic sightings of bottlenose dolphins, Tursiops aduncus, off Bunbury, Western Australia between 2006 and 2013.

Year Season Dolphin Most frequency Sex Age Wound Age I.D. sited location 2006* Summer Rocket Inshore Male Calf Scar

2010 Spring Cheeks Buffalo Male Adult Scar

2012 Summer Veil Inshore Female Juvenile Fresh

2012 Spring Zing Back Female Adult Fresh Beach/Buffalo

2013 Summer Enigma NA Female Juvenile Fresh

2013 Summer Chippy Inshore NA Calf Fresh

2013 Summer Buzz Inshore NA Juvenile Fresh

2013 Spring Energy Back NA Calf Fresh Beach/Buffalo

2014 Summer Eclipse Inshore Female Juvenile Fresh

2014 Summer Topping Inshore NA Calf Intermediate

2014 Summer Mrs Inshore Female Adult Fresh Iruka *Sighting observed by the Bunbury Dolphin Discovery Centre, prior to the commencement of the study.

3.4.2.3 Systematic Sightings

Fifty eight individuals postulated as having shark-inflicted injuries were sighted systematically. The majority of these individuals were adults (n = 40) with a small proportion being juveniles (n = 8) and calves (n = 7). The age for three individuals could not be determined. The sex ratio consisted of 25 females, 21 males and 12 individuals of unknown sex.

The proportion of dolphins with shark bites sighted systematically differed significantly among age classes (X2 = 38.436, P < 0.001). The total bite frequency (all wound age categories) was significantly higher on adults (73%) than juveniles (15%) and calves (13%)

(Fig. 3.5). The frequency of bites in each wound age category was also considerably higher for adults than juveniles (Fig. 3.5).

45 Calves 40 35 Juveniles 30 Adults 25 20

Frequency 15 10 5 0 Fresh Intermediate Scar Total Wounds Wound Age

Figure 3.5 The bite frequencies for each category of bite (fresh, intermediate and scar) and age class of dolphin for bottlenose dolphins, Tursiops aduncus, photographed systematically off Bunbury, Western Australia, from 2007 until 2014.

The frequency of fresh and intermediate wounds were higher on male dolphins than female dolphins, while scars were more frequent on females (Fig. 3.6). Bite frequencies for juvenile and adult sex classes were higher on females (53%) than males (47%, total n = 37).

Although, this was not significant (X2 = 0.111, P = 0.738) (Fig. 3.6).

20 Males 18 16 Females

12 10

8 Frequency 6 4 2 0 Fresh Intermediate Scar Total Wounds Wound Age

Figure 3.6 The number of bites in each wound age category for male and female bottlenose dolphins, Tursiops aduncus, photographed systematically off Bunbury, Western Australia, from 2007 until 2014.

Although bite marks were more frequently observed on adult females without calves

(61%, n = 11) than on adult females with calves (39%, total n = 18), this difference was not significant (X2 = 1.316, P = 0.251). An additional seven calves were also observed with bite marks. On one occasion both mother and calf displayed injuries believed to have been caused from a simultaneous attack.

A total of 45 fresh bites were observed systematically. The proportion of fresh bites differed significantly among season (X2 = 15.333, P = 0.002), with significantly more bites in spring and summer (September to February) than in autumn and winter (March to August)

(Fig. 3.7). An unusually high frequency of bites were observed for the summer of 2013 (n =

8) than in other years (range = 0 - 1). When 2013 was excluded from the analyses, the frequency of bites did not differ significantly among seasons (X2 = 3.889, P = 0.274).

Converting the frequency of bite marks to number per km-1 gives standardised effort rates of 0.002, 0.001, 0.003, and 0.003 km-1 for autumn, winter, spring and summer, respectively.

25 Fresh

20 Intermediate Scar 15

10 Frequency

0 Autumn Winter Spring Summer Season

The number of fresh bite marks recorded was similar in each year, except as noted above for the higher frequency in 2013 (Fig. 3.8). The total number of bite marks in all categories appeared to increase during the study period from three in 2007, to 11 in 2013. The total number of wounds attained each year were relatively similar, and were not found to significantly vary (X2 = 4.948, P = 0.422). Annual effort standardisation of the fresh and

intermediate bite marks showed that these values ranged from 0.001 bites km-1 (2008 and

2009) to 0.004 bites km-1 in 2013.

12 Fresh 10 Intermediate

Scar

8 Total Wounds

6 Frequency 4

0 2008 2009 2010 2011 2012 2013 Year

3.4.3 Identification of the Sharks Species Responsible

After reviewing the photographed dolphins with bite marks, Dr Heithaus (International

University of Florida), Professor Burgess (Florida Museum of Natural History) and Dr.

McAuley (Department of Fisheries, Western Australia), advised that a mixture of shark species were likely to be responsible for the wounds observed on the Bunbury dolphins. The species thought responsible included white and tiger sharks, and several smaller

Carcharhinid species (e.g., whaler, bull, dusky). They reached conclusions based on several photographed injuries (Fig. 3.9). Scalloped hammerhead (Sphyrna lewini) sharks were also photographed on two separate occasions during dolphin surveys within the coastal waters

of Geographe Bay. However, none of the photographed bite marks were thought to have been afflicted by this species.

(a) (b) (c)

3.5 Discussion

In this study, the prevalence of external injuries from bite marks potentially caused from sharks on the coastal bottlenose dolphin (Tursiops aduncus) population off Bunbury,

Western Australia were analysed. From the extensive, systemic sampling between 2007 and

2014, a total of 1,727 dolphin encounters were recorded. Bite marks were observed on 69 dolphins, most of these sightings (58) were recorded from photographs taken on systematic dolphin surveys. The frequency of bite marks varied significantly among dolphin age class with higher frequencies for adults than calves and juveniles. Bite mark frequencies also varied significantly among seasons, with higher numbers in spring and summer than in winter and autumn. However, this was attributed to the high frequency of fresh bites in the summer of 2013. This study also provides an insight into the shark species believed

responsible for these attacks. A large proportion of bites were believed to have been inflicted from white and tiger sharks, while several bites were thought to have resulted from a mixture of smaller Carcharhinid species such as bull, whaler and dusky sharks.

Age Class Variations

The higher frequency of bite marks recorded on adult dolphins, and hence putative predation attempts, reported in this study are similar to the findings of Kogi et al. (2004), who found higher incidences of predation on older bottlenose dolphins (T. aduncus) in

Japan; and those of Walker & Hanson (1999) for female Stejneger’s beaked whales

(Mesoplodon stejnegeri) (i.e., predation attempts appeared to increase with age for this species). Conversely, several authors have reported shark attacks to be significantly higher for calves and juvenile dolphins than adults (e.g., Wells & Scott 1990; Fernandet 1992;

Stolen & Barrow 2003). It is suspected that the neonate and calf mortalities reported in the study are underestimates attributed to several factors including the rapid decomposition of carcasses, scavenging and decreased detection probability of small sized animals (Stolen &

Barlow 2003).

The significantly higher frequency of predation attempts made on adult dolphins found in the present study may have also resulted from distinct behavioural differences among age classes. For example, mature males and non-reproductive females (Tursiops aduncus) are known to reside in small groups, travel great distances and forage in highly profitable but risky habitats (Wells 2003; Urian et al. 2009). Such behaviours can significantly increase the risk of predation and make these individuals more susceptible to shark attacks. In contrast, females with newborn calves, juveniles and smaller individuals often form large groups and

show strong site fidelity to sheltered waters, which may significantly lower the risk of an attack through increased vigilance and group protection (Norris & Dohl 1980; Mann et al.

2000).

Habitat use by bottlenose dolphins can also significantly contribute to the risk of shark predation. For example, dolphins that reside in shallow, estuarine habitats such as the Collie

River are more likely to encounter small Carcharhinid (e.g., bull, whaler, dusky) sharks

(Heupel & Simpfendorfer 2008; Ortega et al. 2009), and as a result of the dentition and often relatively small size of these shark species, predation attempts on dolphins are considered to be less successful than those made by larger sharks (Long & Jones 1996;

Heithaus 2001b). In contrast, dolphins that reside in seagrass meadows or oceanic waters, such as those of Back or Buffalo beach in the Bunbury region may significantly increase the risk of predation posed from larger tiger and white sharks (Bruce et al. 2006; Heithaus et al.

2007). Due to the dentition, agility and size of these shark species predation attempts are more likely to be successful (Heithaus 2001b). The alteration of habitat use to lower the risk of predation posed by sharks has previously been documented by Heithaus & Dill (2006).

Investigations into the shark-dolphin interactions of Shark Bay, Western Australia, found bottlenose dolphins (T. aduncus) to forage in deep and shallow habitats, across microhabitats, and within patches proportional to prey density when tiger shark abundances were low. In contrast, when tiger shark abundances increased (during summer months) foraging dolphins greatly reduced their use of dangerous, but productive, shallow patches relative to safer deep ones.

Seasonal Variations

The results from the current study suggest that the risk of predation for the Bunbury dolphin population increases during the warmer months. Bite frequencies on bottlenose dolphins (Tursiops aduncus) have also been reported to increase during the warmer months near Shark Bay, Western Australia (Heithaus 2001a); Moreton Bay, Queensland (Corkeron

1987a); and the Eastern North Pacific Ocean (Long & Jones 1996). Increased bite frequencies during summer months, particularly in 2013 may have risen through sustained warm sea surface temperatures. We suggest that the main species responsible for attacks during the warmer months are tiger sharks. Tiger sharks were by far the most abundant species caught on drum lines, implemented as part of the States bather protection program from January 2014 to April 2014, and were the most abundant species caught in Geographe

Bay and Cape Naturaliste, confirming that tiger sharks habituate the coastal waters of the south-west (Table 3.5) (Department of the Premier and Cabinet 2014). Tiger sharks are known to inhabit tropical waters throughout the year and are thought to migrate to higher latitudes during warm periods (Bigelow & Schroeder 1948; Stevens 1984; Randall 1992) though evidence of this is largely anecdotal. Heithaus (2001c) suggested that both thermal conditions and prey abundance were the main factors driving tiger shark movement.

Table 3.5 Summary of the number of sharks and rays caught on drum-lines as part of the west Australian swimmer protection program implemented by the Department of Fisheries, Western Australia from January 2014 to April 2014. All species recorded as dead were deceased upon hook retrieval; destroyed due to low likelihood of survival; or target species and due to size (> 300 cm TL) were destroyed (data sourced from the Department of the Premier and Cabinet 2014).

Total Catch Metropolitan Geographe Bay Cape Naturaliste Common Dead Released Dead Released Dead Released Dead Released Name Tiger 64 99 34 75 15 5 15 19 Shortfin 4 1 0 0 2 0 2 1 mako Dusky 0 1 0 1 0 0 0 0 Spinner 0 1 0 0 0 1 0 0 Bull 0 1 0 1 0 0 0 0 Ray 0 7 0 7 0 0 0 0 TOTAL 68 100 34 84 17 5 17 20

Furthermore, tiger sharks are known to show a high degree of dietary plasticity. Although, slow benthic animals (e.g., rays, gastropods crustaceans, and benthic and demersal teleosts), and air breathing marine vertebrates (e.g., dolphins, dugongs, turtles, sea snakes and sea birds) are thought to form the basis of their diet (Simpfendorfer et al. 2001). Due to their ability to detect and respond to short and long-term shifts in the spatial distribution of prey resources these sharks are capable of travelling large distances in short periods in response to opportunistic feeding events (Heithaus et al. 2007).

The seasonal influx of male dolphins and high abundance of neonates and newborn calves during summer months may further increase prey availability in the waters of south- western Australia providing easy targets for these sharks (Cockcroft et al. 1989a; Lowe et al.

1996; Mann & Smuts 1998).

In cooler months when tiger shark abundances decrease, the seasonal immigration of large white sharks is thought to maintain the threat of predation, especially during winter and spring when white shark abundances off the south-west are highest (Bruce et al. 2006;

Sprivulis 2014). However, physiological constraints appear to confine these sharks to cooler waters (Sprivulis 2014). The increased abundance of white sharks during cooler seasons is suggested to result from increased prey availability, in particular that of humpback whales

(Sprivulis 2014).

Calf Presence

The results attained from the present study were not able to confirm any significant differences between mothers with calves and non-reproductive females. Although, a higher proportion of non-reproductive females were observed with shark inflicted injuries. As previously discussed the socialising behaviour of non–reproductive females (e.g., formation of small groups and risky behaviour) may have significantly increased the risk of predation and consequently the frequency of injuries attained. Despite the formation of larger groups by mothers and calves the risk of predation to neonates and calves is still thought to be far greater than that for adults. Moreover, due to their inexperience and size attacks on neonates or calves are much more likely to be successful and result in fatality.

Sex Specific Variations

The frequency of bite marks and hence predation attempts did not differ between male and female dolphins suggesting that both sexes had an equal chance of being attacked. The lack of sexual dimorphism in Indo-Pacific bottlenose dolphins suggests that neither sex is an easier target based on physiological characteristics (Kemper 2004). Similar results have been reported for bottlenose dolphins off Shark Bay, Western Australia (Heithaus 2001a), and

Atlantic spotted dolphins (Stenella frontalis) off Bimini, in the Bahamas (Melillo-Sweeting et al. 2014).

Annual Variations

Overall, predation attempts across years were markedly higher in 2013 than observed throughout other years. A gradual increase in the total frequency of wounds was seen over the seven years of the study, suggesting that predation attempts on dolphins in the south- west are becoming more frequent. As previously suggested, increasing water temperatures and prey availability and distribution are likely factors altering the distribution and abundance of tiger and white sharks in the south-west. However, neither water temperature nor overall prey availability alone adequately explains the marked increase of attacks.

Conclusions

While the results from the study suggest that both sea surface temperatures and increased prey availability for sharks influence the predation risk posed to bottlenose dolphins, further study is needed to prove such a correlation. The present study does however demonstrate that the interactions between sharks and bottlenose dolphins

(Tursiops aduncus) off the coast of Bunbury are not limited to scavenging events, and provides important insight on the shark species believed responsible for these attacks.

Further long-term investigations on the seasonal abundance, dietary requirements and behaviour of large predatory sharks (e.g., tiger and white sharks) in the south-west are vital to understanding overall mortality and risk effects posed on the dolphin population of

Bunbury.

4. Conclusions and Recommendations

The first aim of the study was to describe the movements patterns of several shark species commercially targeted off the coast of Western Australia, with a key focus on the four main species (sandbar, Carcharhinus plumbeus; dusky, Carcharhinus obscurus; whiskery, Furgaleus macki; gummy, Mustelus antarcticus) (Chapter 2). The second aim of the research was to investigate the predatory role of sharks on bottlenose dolphins

(Tursiops aduncus) off Bunbury, Western Australia (Chapter 3). As a secondary objective I also attempted to identify the key shark species responsible for these attacks.

Analyses of long-term (from 1994 to 2013) conventional tagging data collected by the

Department of Fisheries, Western Australia, verified movement patterns and time at liberty varied significantly among the four main commercially fished shark species, with the larger sandbar and dusky sharks moving on average, further and faster than the smaller whiskery and gummy sharks. The results attained from the study confirmed that displacement distance was positively correlated with body length and release condition. It is suggested that large-scale movements are primarily undertaken by larger sharks due to distinct differences in predation risk, nutritional requirements and reproductive cycles than those for immature and smaller sized individuals. Furthermore, significant differences in sex ratios at release and recapture were observed for gummy and whiskery sharks. The significantly higher proportion of females at recapture suggests males and females of these species may segregate and that females are more prevalent in the fishery. Fork length measurements for non-recaptured and recaptured sandbar and dusky sharks were found to significantly vary, however, these results were disregarded due to bias gear-selectivity and inaccurate recapture measurements reported by commercial fishermen. The highest recapture

frequency for species occasionally caught was ten. Maximum displacements ranged from

0.70 to 1,143 km these displacements were observed by wobbegongs (Orectolobus sp.) and copper whaler (Carcharhinus brachyurus) sharks, respectively. Maximum time at liberty ranged from 4 to 5,245 days for nervous (Carcharhinus cautus) and tiger (Galeocerdo cuvier) sharks, respectively. The estimated maximum swimming speed for occasionally caught species peaked at 0.42 km/hr for copper whaler (Carcharhinus brachyurus) sharks.

Swimming speeds for all other species were less than 0.03 km/hr. No statistical analyses were completed for these species.

Analyses of the frequency of shark bites on bottlenose dolphins (Tursiops aduncus) near

Bunbury, Western Australia indicated that bite frequency were greater on adults than juveniles and calves, and higher in the warmer months of spring and summer than in winter and autumn. The low attack frequencies reported in this study for juveniles and calves are considered underestimates due to the rapid decomposition of carcasses, and decreased detection probability of small sized animals. However, it is possible that higher bite frequencies among older dolphins were caused from marked differences in sociality (e.g., group size, foraging behaviour and habitat use) between age classes. Bite frequencies did not vary significantly between sexes or in the presence or absence of a calf. The significant variation in bite frequencies among seasons was largely attributed to the unusually high number of fresh bites attained in the summer of 2013. Bite frequencies tended to increase over the duration of this study and were markedly higher in 2013 following sustained warm water temperatures since 2010. The presence of tiger sharks off the south-west during summer months has been confirmed by drum-line catches implemented as part of the west

Australian bather protection program. Although, the frequency of bite marks were observed

to decrease during winter months the risk of predation is thought to be maintained by the seasonal influx of white sharks.

4.1 Recommendations for Future Research

The results of this study in Chapter 2 confirm shark movement patterns off Western

Australia to differ significantly among species. The delineation of movement patterns and segregation by size and sex for these species, in particular for those that are commercially targeted are fundamental to ensure stocks remain at sustainable levels. To ensure management measures remain effective further long-term research investigating the use of offshore areas as nurseries and breeding grounds in the south-west and north-west, respectively, for sandbar (Carcharhinus plumbeus) and dusky (Carcharhinus obscurus) sharks is required. Additionally, long-term investigations into the sexual segregations of whiskery

(Furgaleus macki) and gummy (Mustelus antarcticus) sharks should also be examined.

Describing these aspects of coastal shark ecology and behaviour for sympatric species will minimise the risk of overexploitation of these vulnerable populations.

The results from Chapter 3 indicate that shark predation may be an important source of mortality for small Odontocetes in south-western Australia. These interactions are thought to considerably shape the structure and composition of the Bunbury dolphin population. In order to adequately assess these interactions long-term studies investigating the seasonal abundance, dietary requirements and behaviour of large predatory shark species (e.g., tiger and white sharks) are required. If these studies are carried out a more precise understanding of shark-dolphin interactions will emerge. Furthermore, a comprehensive

understanding of these interactions will allow more conclusive comparisons to be drawn between natural and anthropogenic sources mortality.

4.2 Implications for Management

The results from Chapter 2 of the study provide a complete and meaningful representation of the movement patterns for several commercially targeted shark species off the coast of Western Australia. The described movement patterns presented in this study can be incorporated into future conservation and management plans increasing their effectiveness and precision, ensuring west Australian shark stocks remain above meaningful thresholds.

The results from Chapter 3 of the study refine our understanding of the interactions between sharks and small living Odontocetes. The results from the research confirm sharks not only scavenge but actively hunt and predate small living Odontocetes. The ability and significant influence of these predatory sharks to shape and alter dolphin population dynamics is likely to be more important than previously recognised.

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6. Appendix I. Summary of all occasionally caught species released but not recaptured off the west and south coast of Australia from 1994 to 2013.

No. of Released Sex Ratio Fork Length Individuals at Release at Release

Species Common Name Males Females Min. Max.

Carcharhinus limbatus & C. Blacktip 214 90 120 54 202 tilstoni C. sorrah Spot Tail 205 95 108 50 114 Rhizoprionodon acutus Milk 198 47 149 41.9 76 Sphyrna lewini Scalloped 102 55 43 74 297 Hammerhead C. amboinensis Pigeye 102 57 44 54 263 S. mokarran Great Hammerhead 47 19 21 120.3 350 Negaprion acutidens Lemon 44 12 30 88 300 Trygonorrhina sp. Fiddler Ray 43 19 21 72 278 Pristis clavata Dwarf Sawfish 28 14 13 - - C. leucas Bull 24 13 10 57 83 Nebrius ferrugineus Tawny Nurse 24 16 5 212 256 Stegastoma fasciatum Zebra shark 24 13 11 189 189 Heterodontus portusjacksoni Port Jackson 18 1 16 84 104 Carcharhinus amblyrhinchoides Graceful 19 6 13 52 112 C. carcharias Great White 15 6 9 128 386 O. maculatus Spotted Wobbegong 14 10 4 91 100 Triakis semifasciata Leopard 12 6 6 130 199 Squalus sp. Spur Dog 10 - 9 46 65 O. ornatus Banded Wobbegong 10 5 5 74 208 Sutorectus tentaculatus Cobbler Wobbegong 12 3 8 47 90

C. altimus Bignose 8 2 5 73 210 Mustelus ravidus Grey Gummy 8 2 6 82 96 M. stevensi Spotted Gummy 6 2 3 59 171 C. melanopterus Blacktip Reef 4 - 4 72 96 Eusphyra blochii Winghead 2 1 1 44 45 Hammerhead Hemigaleus australiensis Weasel 2 1 1 75 144 Hexanchus nakamurai Bigeye Sixgill 1 1 - 350 350

P. microdon Freshwater Sawfish 1 1 - - - Triaenodon obesus Whitetip Reef 1 1 - 87 87 Pristiophorus cirratus Common Saw 1 - 1 59 59 Hemitriakis falcata Sicklefin 1 1 - 64 64 Hemipristis elongates Snaggletooth 1 1 - 100 100 TOTAL 2264 984 1174 - No data was recorded.

7. Appendix II. Analysis of the residuals for the displacement distance Generalised Linear Model (GLM) for a normal distribution.

8. Appendix III. Analysis of the residuals for the time at liberty Generalised Linear Model (GLM) for a Poisson distribution.

9. Appendix IV. Analysis of residuals for the speed Generalised Linear Model (GLM) for a normal distribution.