The Role of Apex Predators in Coastal Ecosystems: a Case Study Examining the Broadnose Sevengill Shark Notorynchus Cepedianus

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The role of apex predators in coastal ecosystems: a case study examining the Broadnose sevengill shark Notorynchus cepedianus

Adam Barnett (Hons)

Submitted in fulfilment of the requirements for the Degree of

Doctor of Philosophy in Quantitative Marine Science

Institute for Marine and Antarctic Studies

University of Tasmania

October 2011

DECLARATIONS

Statement of Originality

This thesis contains no material that has been accepted for a degree or diploma by the University or any other institution. To the best of my knowledge and belief, this thesis contains no material previously published or written by another person, except where due acknowledgement is madein the text.

Statement of Authority of Access

This thesis may be available for loan and limited copying in accordance with the Copyright Act 1968.

Statement Regarding Published Work Contained in Thesis

The publishers of the papers comprising Chapters 2 to 5 and 7 hold the copyright for that content, and access to the material should be sought from the respective journals. The remaining non published content of the thesis may be made available for loan and limited copying in accordance with the Copyright Act 1968.

Statement of Ethical Conduct

All research was conducted with approval from the University of Tasmania Animal Ethics Committee (#A0009120) and the Department of Primary Industries and Water (Permit #8028).

Adam Barnett

Date:_October 2011

Statement of Co-authorship

Chapters 2- 5 and 7 of this thesis have been prepared as scientific manuscripts as identified on the title page for each chapter. In all cases experimental design, field and laboratory work, data analysis and interpretation, and manuscript preparation were the primary responsibility of the candidate. However, they were carried out in consultation with supervisors and in some chapter’s collaboration with co-authors. Contributions and Institutional affiliation of the co-authors at the time of the studies are outlined below:

Chapter 2

Jayson Semmens (Institute for Marine and Antarctic Studies - IMAS) and John Stevens (CSIRO) are the primary supervisors for this PhD. Both provided advice on field techniques and manuscript preparation and participated in field work. John Stevens instructed A. Barnett on best practices for catching and handling sharks. Stewart Frusher (IMAS) commented on the manuscript.

Chapter 3

Kevin Redd (IMAS PhD student) provided technical and operating expertise to the DNA analysis. He also assisted in writing the methods section of the manuscript and commented on the overall manuscript. Jayson Semmens proposed the original concept of using DNA analysis and provided advice to manuscript preparation. John Stevens provided advice to manuscript preparation and field work. Stewart Frusher commented on the manuscript.

Chapter 4

Jayson Semmens and John Stevens provided advice to manuscript preparation. Jonah Yick (IMAS honours student) assisted in field work and laboratory analysis of stomach contents. He also had input on data analysis. Kátya Abrantes (IMAS Research Fellow) assisted in field work and advice on manuscript preparation as well as providing advice and assistance in data analysis. Stewart Frusher commented on manuscript.

Chapter 5

Jayson Semmens provided advice on experimental design, the surgical methods used to implant acoustic tags in the sharks and manuscript preparation. John Stevens provided help with collating and dealing with PAT tag data and commented on manuscript. Kátya Abrantes commented on manuscript, assisted with field work and gave statistical advice on data analysis.

Chapter 6

Currently in review, Jayson Semmens assisted with field work and commented on manuscript.

Chapter 7

Jayson Semmens provided the expertise on setting up and maintaining the VRAP. He also contributed to surgically implanting the tags in the sharks and manuscript preparation. John Stevens and Barry Bruce (CSIRO) commented on the manuscript and participated in the active tracking field work, as well as supplying equipment and advice. Kátya Abrantes contributed to field work, manuscript preparation and data analysis.

Signed: ______

Dr Jayson Semmens

Primary Supervisor Head of Institute

Fisheries, Aquaculture and Coasts (IMAS-FAC) IMAS-FAC

Institute for Marine and Antarctic Studies (IMAS) IMAS

University of Tasmania University of Tasmania

Date:______Date:______iii

ABSTRACT

Large apex predators are believed to play key roles in ecosystem structure and dynamics. However, for the vast majority of large predators their ecological roles have not been defined or quantified. In particular, there is a lack of information on large mobile marine species. The ecology of the Broadnose sevengill shark, Notorynchus cepedianus was examined to determine their role in coastal systems of Tasmania. This was addressed by conducting studies on the different aspects of N. cepedianus ecology in two coastal areas of south-east Tasmania; the Derwent Estuary and Norfolk Bay. Both these areas are designated shark protected areas. Seasonal longline sampling showed that adult and sub-adult N. cepedianus (size 105-295cm) are highly abundant in summer declining to near absence in winter. The absence of smaller size classes (<80cm) from the catches suggests that N. cepedianus are not using these coastal habitats as nursery areas. Both longline sampling and acoustic movement analysis demonstrated that N. cepedianus showed site fidelity in the use of the coastal habitats. The general pattern was for sharks to exit coastal areas over winter and return the following spring or summer. However, sexual segregation was evident with females abundant in spring and to a lesser extent occurring in winter; conversely males appear in coastal areas later in summer. Both satellite and acoustic tracking methods showed that males can make northerly migrations during winter to distances of at least 1000km. Individuals tagged in both coastal areas (Derwent Estuary and Norfolk Bay) showed low spatial (Piankas index: O = 0.34) and dietary overlap (O = 0.45), suggesting localised site fidelity and fine spatial scale resource partitioning. In general, individuals from both locations consumed the same broad dietary categories (sharks, batoids, teleosts and mammals). However, there were differences in species composition within these categories for each location. The simultaneous tracking of five chondrichthyan prey species and N. cepedianus showed similar seasonal use of coastal areas by all species. Predator and prey also showed high spatial overlap and similar habitat use patterns once they were within the coastal system. These similar movement patterns of predator and prey combined with the additional ecological information (diet, relative abundance) suggests that N. cepedianus display feeding site fidelity, moving into coastal systems following their main chondrichthyan prey. These combined approaches demonstrate that N. cepedianus probably exert significant predation pressure on prey using these protected coastal areas during summer. Natural mortality is an important, but difficult parameter to estimate in assessing commercially fished populations. However, given the common occurrence and high abundance of Notorynchus cepedianus in the Tasmanian coastal waters gazetted as shark nursery areas and the prevalence of gummy shark Mustelus antarcticus in their diet, it is likely that N. cepedianus exert significant predation pressure on this commercially important species. Therefore, Notorynchus cepedianus is competing with humans (fisheries) as the iv

top predators for common food resources, and as mortality from predation can exceed that from fisheries, this information is important for fisheries management. Overall this study is an important contribution to the ecology of N. cepedianus and marine apex predators in general, but it also illustrates the value of simultaneously recording and integrating multiple types of information to better understand predator-prey relationships, the likelihood of interactions, and to build a clearer picture of ecosystem dynamics.

Acknowledgements

First I would like to thank my two primary supervisors Jayson Semmens and John Stevens for all their support, guidance and friendship throughout this time. To John and his partner Claire, thank you for all the wonderful dinners and hospitality at your home. To Jayson, thank you for all the laughs, and especially thank you for putting up with all the problems caused with QMS. I know I could make things difficult at times. To his wife Stephanie, thanks for putting up with all the afterhours phone calls.

Thank you to Jayson and Stewart Frusher for harassing Colin Buxton to the point where he probably accepted the project after his initial trepidation just to get some peace. We caught enough sharks!!! Barry Bruce for his help in getting the project started and supplying the first tracking equipment. Russ Bradford for help and advice with PAT tags. To Jonah Yick and Andrew Pender for assistance and knowledge in all matters related to fishing and for their friendship during my time in Tassie. But a special thank you to Jonah for 2.5 years of field assistance and all the sleepless nights fishing in the cold. Also for recruiting extra volunteers when needed, the project would not have been as successful without all your help, thanks mate.

Thank you to the other PhD students at TAFI, in particular Cynthia Awruch for her friendship and helping to keep me sane when I was sometimes loosing it. All the football (soccer for ozzies) talks and the insight into the Argentinean futbal psyche, Viva Argentina! My office mate, Tim Alexander, a true gentleman, always willing to assist and take an interest in other projects. Scalpel Steve (Leporati) for pointing out the funny side of a situation and making me laugh on numerous occasions, especially his reports as the student rep at staff meetings (I still don’t understand why students can’t go to the meetings?), keep them honest Steve. And, to Jessica Andre, Zoe Doubleday, Yoda and big bird for their friendship, advice and support.

Thank you to Juerg Brunnschweiler, Zoe and Chris Dudgeon for advice on funding applications, in particular Juerg for pointing me towards Save Our Seas foundation (SOS). And a big thank you to SOS and Winifred Violet Scott Trust Fund for funding this project, their generous funding made the Rolls Royce version of the project possible. For additional tracking equipment from AATAMS, and to Nick Otway and Megan Ellis (SEACAM) for passing along detections of my sharks from their receivers in New South Wales. The Derwent Estuary Program for water salinity and temperature data.

Thank you to my honours supervisor Dr David Bellwood for first setting me on the path to becoming a scientist, not just another marine biology graduate.

Last but not least to my partner Kátya Abrantes for first encouraging me to do a PhD when I was sick of working for other people, and secondly for all her help in the field, reading manuscripts and most of all statistical advice, you taught me more about stats than anyone previously, it was like having an extra supervisor. But most of all thank you for all your love and support, I couldn’t have done it without you. Oh! And sorry for dragging you to a cold place like Tasmania.

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Table of contents

Declarations i Statement of Co-authorship ii Abstract iv Acknowledgements vi Table of Contents viii List of Tables x List of Figures xii

Chapter 1. Introduction ...... 1

Chapter 2. Seasonal occurrence and population structure of the Broadnose sevengill shark Notorynchus cepedianus in coastal habitats of south-east Tasmania 8

Introduction ……………………………………………………………………………………………………… ..9 Methods ………………………………………………………………………………………………………………10 Results ………………………………………………… ……………………………………………………………13 Discussion ……………………………………………………………………………………………………………17

Chapter 3. Non-lethal method to obtain stomach samples from a large marine predator and the use of DNA analysis to improve dietary information ...... ………………………….23 Introduction………………………………………………………………………………………………………….24 Methods……………………………………………………………………………………………………………….26 Results………………………………………………………………………………………………………………….28 Discussion ……………………………………………………………………………………………………………30

Chapter 4. Predator-prey relationships and foraging ecology of a marine apex predator with a wide temperate distribution 33 Introduction …………………………………………………………………………………………………..…… 34 Methods ...…………………………………………………………………………………………………………..35 Results ………………………………………………………………………………………………………………..38 Discussion 47

Chapter 5. Site fidelity and sex-specific migrations in a mobile apex predator: implications for conservation and ecosystem dynamics 54

Introduction 55 Methods 57 Results 63 Discussion 70

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Chapter 6. Sequential movement into coastal habitats and high spatial overlap of predator and prey suggest high predation pressure in protected areas 74

Introduction 75 Methods 77 Results 82 Discussion 86

Chapter 7. Fine-scale movements of the Broadnose sevengill shark and its main prey, the Gummy shark 91 Introduction 92 Methods 93 Results 97 Discussion 105

Chapter 8. General Discussion 110

Chapter 9. References...... 121

List of Tables

Table 3.1 PCR primers used (Kasper et al. 2004; Ratnasingham & Hebert, 2007) including primer name, sequence and annealing temperature used in DNA amplification...... 28

Table 3.2. Number of samples positively identified by their morphology (Mor) and the number of samples that were positively identified by DNA analysis that were not identified by morphology, (% DNA is the increased identification of each species from using DNA analysis). The index of relative abundance prior (% IRI) and post (% IRI DNA) DNA analysis...... 30

Table 4.1. Dietary composition of Notorynchus cepedianus from all areas sampled in Tasmania. Total represents all sites combined. The sample size (n = number of sharks containing prey) is to the right of the area sampled. Frequency of occurrence (%F), percentage of numerical importance (%N), percentage of weight (%W) and the index of relative importance (% IRI).* = Frequently used resource (FUR), noting that skate species Dentiraja lemprieri, Dipturus confusus and Dipturus sp. were pooled to represent a single FUR………………………………………………………………………………………………………………….39

Table 4.2. The major prey species from dietary studies of Notorynchus cepedianus from different geographic regions, with an emphasis on chondrichthyan prey...... 52

Table 5.1. Details of N. cepedianus fitted with acoustic and PAT transmitters. For tagging location, NBay = Norfolk Bay; Derwent = Derwent Estuary; DerwentR = Ralphs Bay (lower region of the Derwent Estuary). Date is the date of tagging and TL is total length in cm. For acoustic tags, Days = the number of days detected, % days = percentage of days detected from date of tagging until receivers removed. Ret/Rem – gives indication if sharks returned after winter or remained in coastal region through winter for the first (y1) and second (y2) years. For animals that returned, the area where they were detected is indicated (NFB/Der); Left = left the area, and did not return. Mixed = gives information on whether the animal moved between the two habitats (Derwent and Norfolk Bay) or not. For PAT tag information, P days = programmed number of days after tagging for tags to be released. R date/location = date and place of tag release: NSW= New South Wales, BS = Bass Strait. Km travelled is the shortest distance travelled, in kilometres. * = shark also fitted with an acoustic tag. † = animals killed by fisher after leaving protected areas. ** = individuals that were detected on receivers in NSW...... 60

indication if sharks returned in spring after winter or remained in coastal region through winter, short indicates that the battery life was not long enough to detect if the animal returned after winter, depending on the day it was tagged...... 80

Table 6.2. Norfolk Bay receivers, showing depth in metres they were deployed in, and which receivers were used for the three habitat analyses, indicated by the habitat they were pooled in.....82

Table 7.1. Details of sharks tagged; TL- total length in cm, cont – continuous tag, used for the actively tracked sharks, Days- number of days detected in VRAP, DP- detection period representing the time in days between first detection until last detection. P-values in bold are significant and % ratio indicates if they occurred more during the day (above 60%) or the night (below 60%). The 60 % expected is based on 14.5 hours of daylight being 60% of the hours in the day. * denotes animals omitted from Chi-square χ2 and t-test because they were not detected on more than one day...... 99

List of Figures

Fig. 1.1. Global distribution of Notorynchus cepedianus, shown by dark blue shading. Map provided with permission from Last & Stevens 2009...... 4

Fig. 2.2. Seasonal CPUE of Notorynchus cepedianus (sharks per 50 hooks per 4 hours; mean ± SE) for Norfolk Bay (top) and the Derwent Estuary (bottom). Note the difference in the y axis...... 15

Fig. 2.3. Size distribution, in percentage, of Notorynchus cepedianus caught in Norfolk Bay (grey bars, n = 326) and the Derwent Estuary (black bars, n =222). Sharks are categorised by 10 cm TL size classes...... 16

Fig. 2.4. Monthly variations in sex ratio of Notorynchus cepedianus. Data for Norfolk Bay and the Derwent Estuary is combined. Grey corresponds to proportion of females, and black to males. Numbers on top correspond to number of individuals...... 17

Fig. 4.1. Notorynchus cepedianus. Sampling locations in the south east region of Tasmania. The closest seal haul-out sites, Cape Raoul and The Friars are also indicated...... 35

Fig. 4.2. Cumulative prey curves for Notorynchus cepedianus’ diet for the Derwent Estuary and Norfolk Bay. Three taxonomic prey groups are represented (1) species, (2) broad prey groups and (3) frequently used resource species (FUR). Curves are based on the number of prey that occurred (%N)...... 42

Fig. 4.3. Catch per unit effort (CPUE = no. individuals/50hooks; ±SE) of chondrichthyan species for Norfolk Bay (black bars) and the Derwent Estuary (grey bars). The number above histogram represents the percent frequency of occurence (%F) in the diet of Notorynchus cepedianus for that location...... 44

Fig. 4.4. Catch per unit effort (CPUE = no. individuals/50hooks; ±SE) for Notorynchus cepedianus and its elasmobranch prey for 3 years in Norfolk Bay. Year 1: black bars; Year 2: grey bars; Year 3: white bars. The number above histogram represents the percent frequency of occurence (%F) in the diet of N. cepedianus for that year ...... 45

Fig. 4.5. Catch per unit effort (CPUE = no. individuals/50hooks; ±SE) of Notorynchus cepedianus and their main chondrichthyan prey per season. Seasons run in sequence from Summer 2006/07 through to Summer 2008/09...... 46

Fig. 4.6. Feeding strategy plots for Notorynchus cepedianus in (a) the Derwent Estuary and (b)

Norfolk Bay. %F = frequency of occurrence, % Pi = prey specific abundance...... 47

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Fig. 5.1. Map of study area. Filled circles represent receivers and each curtain or gate of receivers has a designated code. Dashed line is the boundary of the shark protected areas...... 58

Fig. 5.2. Five-leaf classification and regression tree explaining the number of acoustically tagged sharks detected in the study area based on spatial resource (i.e. lines, as defined in text) and month of the year. Model was calculated based on number of sharks detected in each line/group of receivers per 3-day blocks. Histograms of distribution of number of sharks/3 days are also presented below the leaves, and mean and sample sizes (in brackets) for each group are also indicated. Ranges in histograms correspond to 0 to 24 sharks...... 64

Fig. 5.3. Circular plots showing the frequency of number of N. cepedianus detected per day for each month, at each line or group of receivers. Plots cover one year, from February 2008 to January 2009...... 66

Fig. 5.4. Timeline showing the days each individual shark was detected in the protected area of southeast Tasmania, from January 2008 to July 2009. For each shark, the first point marked on the graph corresponds to the tagging day, with the exception of sharks that were tagged before January 2008. Females are in black and males in grey...... 67

Fig. 5.5. Six-leaf classification and regression tree, explaining the percentage of time each shark spent in the protected area, based on season and sex. Histograms of distribution of this percentage are also presented below the leaves, and mean and sample sizes (in brackets) are also indicated. Ranges in histograms correspond to 0 to 100%...... 68

Fig. 5.6. Release locations of PAT tags for the four male Notorynchus cepedianus, represented by stars. The three acoustic tagged males were detected in New South Wales (NSW) at receivers stationed in the coastal region between Jervis Bay and Batemans Bay...... 69

Fig. 6.1. Map of study area. Panel A is the area in south east Tasmania. Filled circles represent receivers and each curtain or gate of receivers has a designated code. Dashed line is the boundary of the shark protected areas. Panel B is Norfolk Bay; grey lines are depth contours labelled with the depth in metres. Selected receivers are labelled to allow reference to Table 6.2 and panel A to see the receivers that were grouped for the habitat analysis...... 78

Fig. 6.2. Seasonal catch per unit effort (CPUE) of the main chondrichthyans caught from longline surveys...... 83

Fig. 6.3. Time-line showing the daily detection history of chondrichthyan individuals in protected coastal areas of south east Tasmania. Note that M. antarcticus D is the three individuals that were tagged in the Derwent Estuary...... 84

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Fig. 6.4. Area use of four species in Norfolk Bay based on the number of hours each species was detected at each receiver. The dark grey shows where 50% of the hours were detected and the light grey shows where approximately 70% of hours detected. Black dots are receivers...... 85

Fig. 6.5. Circular plots showing the number of hours the three species used each of the three habitat categories over the 24 hour diel cycle. Note that the scale of the number of hours animals were detected varies on the axis between species and habitat. The legend represents the number of sharks detected in a given hour...... 86

Fig 7.1. Study area, showing Norfolk Bay and the Derwent Estuary in southeast Tasmania. Triangle represents the VRAP location. The two thick bold black lines (one in the Derwent Estuary and one in Norfolk Bay) are the movement paths of the two actively tracked N. cepedianus...... 94

Fig 7.2. Diel pattern in depth use for N. cepedianus and M. antarcticus in southeast Tasmania. Box plots show the median (line within the boxes), interquartile ranges (boxes), 10th and 90th percentiles (whiskers) and outliers ( ) of depths detected during each 1 h interval. For each species, data from the whole sampling period was pooled. Dashed area indicates nocturnal period...... 100

Fig 7.3. Diel variations in depth use for N. cepedianus (in % time) for the top (0–5 m depth), middle (5–10 m depth) and bottom (>10 m depth) depth ranges...... 102

Fig 7.4. Rose diagrams showing the angular changes of N. cepedianus for both day and night periods. Note differences in scale between the two periods...... 104

Fig 7.5. Typical depth profiles for each of the different periods of the diel cycle. Data illustrates the profile over representative 1 h periods during the day (16:00 – 17:00 h), dusk (20:00 – 21:00 h), night (01:00 – 02:00 h) and dawn (05:00 – 06:00 h) periods for the N. cepedianus individual tracked in the Derwent Estuary on the 16th March 2007...... 105

Fig. 8.1. Distribution of School sharks by age group caught in south east region of Tasmania. The number in brackets in the legend is the total number caught for that age class. Figure taken from Stevens and West 1997...... 115

Fig. 8.2. Simplistic interpretation of a section of the upper trophic levels of the food web in coastal areas of Tasmania, related to species with a commercial value...... 118

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Chapter

Introduction

THE ECOLOGICAL ROLE OF APEX PREDATORS

Large apex predators are believed to play key roles in ecosystem structure and dynamics (Estes et al. 2001; Williams et al. 2004; Heithaus et al. 2008a; Ferretti et al. 2010). However, for the vast majority of large predators their ecological roles have not been defined or quantified (Estes et al. 2001; Williams et al. 2004; Ferretti et al. 2010). In particular, there is a lack of information on large mobile marine species. This lack of information is not surprising, given that large marine predators are often elusive, have large home ranges and low population densities, thus, direct experimental analyses are difficult (Williams et al. 2004; Heithaus et al. 2008a; Baum & Worm 2009). This makes the direct assessment of foraging behaviour and predator-prey interactions near impossible for many species (Williams et al. 2004).

Predators not only affect their targeted prey species through direct predation (consumptive or lethal effects), they can also affect species by influencing the preys’ behaviour through non-consumptive interactions, also termed “risk effects”. That is, investment in anti-predator behaviour by the prey causes diminished feeding success (Dill et al. 2003; Creel & Christianson 2008; Heithaus et al. 2008a). For example, increased vigilance or foregoing foraging opportunities in productive but risky habitats can decrease the prey’s foraging ability, consequently affecting its body condition (state) (Lima & Dill 1990; Wirsing et al. 2007a; Heithaus et al. 2008a). However, indirect effects are also evident on other species at lower trophic levels that are peripheral to the apex predator (Meyers et al. 2007; Frid et al. 2008). For instance, the fear of predation may cause mesopredators (defined as predators that occupy trophic positions directly below apex predators) to select less profitable resources that are gained more safely and therefore decrease the mortality rates of other lower trophic level species (Lima & Dill 1990; Frid et al. 2008; Heithaus et al. 2008a). In the absence of predation, the ‘fear released’ mesopredators are free to forage, which can result in increased pressure on resources that previously were risky to obtain (Frid et al. 2008). A number of studies have discussed the possible consequences of mesopredators’ release after the loss of high trophic level predators, highlighting resulting problems such as trophic cascades, effects on trophic interactions and shifts in community composition (Stevens et al. 2000; Myers et al. 2007; Heithaus et al. 2008a; Frid et al. 2008; Ferretti et al. 2010).

While hypothesis concerning dire consequences to ecosystem function after the removal of apex predators abound ( e.g. see reviews by Estes et al. 2001; Heithaus et al. 2008a; Baum & Worm 2009; Ferretti et al. 2010), much of this work (not all) is based on theoretical models. Unfortunately, a paucity of empirical field studies and insufficient ecological knowledge of the apex predator in

question, makes it difficult to draw strong conclusions from some of these predictions (Alonzo et al. 2003; Ferretti et al. 2010). Only recently, studies have begun investigating the complex ecological roles that large-bodied, wide ranging predator such as sharks play (Ferretti et al. 2010). Therefore, comprehensive ecological information on large predators is imperative to complement theoretical studies. For instance, while an understanding of ecological processes requires knowledge of predator diets, of equal importance is an understanding of its space utilization, trophic relationships (risk effects and indirect effects for lower trophic species), habitat use, activity patterns, foraging strategies and determining the demographic structure of predator and prey species within key habitats. All these factors are important elements of ecology that are integral to understanding the intricate mechanics that drive ecosystems.

THE BROADNOSE SEVENGILL SHARK: AN APEX PREDATOR CASE STUDY

Broadnose sevengill sharks, Notorynchus cepedianus are members of the family Hexanchidae, also referred to as cowsharks. The group has a wide global distribution and consists of four species (Compagno et al. 2005). The most distinctive feature that sets this family apart from all other sharks is that they posses six or seven pairs of gill slits in comparison to all other species (~500 species) possessing five pairs of gill slits (Compagno et al. 2005). All four species are relatively large upper trophic level predators in their respective habitats (maximum size ranges from 140 cm TL for sharpnose sevengill shark Heptranchias perlo to 550 cm TL for the bluntnose sixgill shark Hexanchus griseus) (Compagno et al. 2005). However, in contrast to the other three species in this unique group that primarily live in deeper waters (maximum depths 600-1800 m), N. cepedianus is associated with coastal habitats (Compagno et al. 2005).

Notorynchus cepedianus is widely distributed in temperate coastal regions around the world, with the exception of the north Atlantic (Compagno et al., 2005; Last & Stevens, 2009). In Australia, their distribution ranges around southern Australia from Sydney (New South Wales) to Esperance (Western Australia), including Tasmania (Fig. 1.1) Notorynchus cepedianus is a large (up to 3 m TL) apex predator that consumes a variety of prey including marine mammals, chondrichthyans and teleosts (Ebert 2002; Lucifora et al. 2005; Braccini 2008). Given the diversity of their diet, previous studies have identified this species as one of the most important apex predators in temperate coastal systems (Ebert 2002; Lucifora et al. 2005). This species’ trophic position rivals that of other shark species considered important upper trophic predators such as tiger sharks Galeocerdo cuvier and white sharks Carcharodon carcharias (Cortés 1999). Indeed, it was ranked as the highest trophic level 3

predator (trophic level index of 4.7) out of 149 shark species, including the white (4.5) and tiger (4.1) sharks (Cortés 1999). Yet, in contrast to these species, besides dietary work, there is very little information on their ecology, behaviour or habitat use. Given their high trophic level, wide distribution and close proximity to shore, the lack of information available for this species is surprising. In fact, since the seminal work of Dr. David Ebert on the life history and biogeography of Notorynchus cepedianus in the 1980s (Ebert 1984; 1990), there have only been a couple of studies that complement his diet and reproduction work (Lucifora et al. 2005; Braccini 2008). This is a significant gap in knowledge in understanding the role of apex predators in coastal systems, especially as this species potentially influences the structure and function of coastal communities (Lima & Dill 1990; Creel & Christianson 2008). Therefore, a detailed ecological study expanding on Ebert’s earlier work is overdue.

Fig. 1.1 Global distribution of Notorynchus cepedianus, shown by dark blue shading. Map provided with permission from Last & Stevens 2009.

PROTECTED AREAS AND FISHERIES INTERACTIONS

Currently, there is an emphasis on ecosystem-based management of marine resources and apex predators are critical elements in this multispecies approach (e.g. Estes et al. 1998, Carr et al. 2002, Shears & Babcock 2002, Bascompte et al. 2005, Reisewitz et al. 2006, Crowder & Norse 2008). However, for many of these species there are increasing conservation concerns, particularly among sharks because they are slow reproducers and increasingly threatened by overexploitation (Baum et al. 2003; Myers & Worm 2003; Dulvy et al. 2008). Habitat degradation is a significant factor that is

often overshadowed by other pressing problems such as overfishing (Field et al. 2009; Kinney & Simpfendorfer 2009; Graham et al. 2010). In Australia, current fisheries management plans have recognized the importance of identifying and protecting habitats critical to the survival of shark species (Lack et al. 2004). Likewise, the mandate in the United States territorial waters is to incorporate essential fish habitats in all fishery management plans (Heupel et al. 2007). Thus, marine reserves have been considered as important components of conservation strategies for these top order predators (Baum et al. 2003; Heupel & Simpfendorfer 2005a; Kinney & Simpfendorfer 2009). However, there is a need to test the effectiveness of these areas by better understanding when and how sharks use them (Heupel & Simpfendorfer 2005a).

Since the early 1960’s, coastal areas in south east Tasmania have been protected from shark fishing. These areas function as pupping and nursery grounds for a number of chondrichthyan species over the summer period, including the commercially important gummy Mustelus antarcticus, and school Galeorhinus galeus sharks (Olsen 1954; Stevens and West 1997). Notorynchus cepedianus has a particularly interesting relationship with commercial shark fisheries, as it is one of the most common bycatch species in the southern shark fishery and is more than likely the most significant predator of the juvenile commercial important shark species using these coastal areas as nursery grounds (Olsen 1954, Stevens & West 1997). Consequently, N. cepedianus may have a considerable impact on recruitment of smaller sharks to the fishery. However, natural mortality of commercial important shark species in these areas is unknown. Thus, understanding the role and habitat use of N. cepedianus will help in evaluating the effectiveness of these areas in protecting N. cepedianus and in predicting the likely predation pressure on juvenile chondrichthyans within protected areas.

AIMS AND STRUCTURE OF THESIS

The overall objectives of this study were to determine the role and habitat use of an important apex predator, Notorynchus cepedianus in two coastal systems of south east Tasmania, and gain comprehensive ecological knowledge of N. cepedianus that can be used in future ecosystem studies and serve as a case study that contributes to the understanding of large apex predators in general. In addition, this study evaluated the effectiveness of shark protected areas in Tasmania. To achieve these goals a multi methods approach was instigated to address the key areas of a predators behaviour and resource use. These approaches have been set out in six studies that are described in the corresponding six data chapters of this thesis.

In Chapter 2, fisheries independent longline surveys were used to establish the importance of two coastal areas (Norfolk Bay and the Derwent Estuary) by estimating the number of sharks (relative abundance) and population structure of N. cepedianus when they are in these coastal areas. To address this component of the study, fishing was conducted over two years plus an extra summer to establish catch per unit effort (CPUE) to obtain seasonal relative abundance estimates and to record the population structure (size range and sex ratio) in these coastal areas.

In Chapters 3 and 4, information on N. cepedianus diet was collected to understand predator-prey relationships and formulate hypothesis on likely foraging ecology. Therefore, Chapter 3 is concerned with the methods used to gain dietary samples without killing large numbers of these animals, whilst improving the quantity and quality of dietary information by using molecular methods to achieve fine-scale taxonomic resolution of prey. Chapter 4 investigates temporal and spatial variation in diet between Norfolk Bay and the Derwent Estuary. Diet was also correlated with CPUE of the main chondrichthyan prey over time (3 years) and space (between the two study locations). Diet was also compared with previous studies from a number of geographic regions around the world to establish predictable predator-prey relationships on a global-scale.

Once the trophic ecology, demographics and relative abundance of N. cepedianus was understood then movement behaviour was needed to compare/link this information with the other components of the study to gain a clearer picture of habitat and resource use. A range of tracking techniques was used to explore movement patterns. Passive acoustic technology (coded transmitters and receivers) and conventional fisheries tags were used to determine long-term habitat use such as seasonality and site fidelity and to identify important habitats. Archival satellite tags were deployed to explore long distance movements. Migratory information also depended on the chance of acoustic tagged sharks being detected by the acoustic arrays of other studies on the mainland of Australia or conventional fishery tags being recaptured by fisheries or recreational fishers.

Chapter 5 deals with the long-term movements of N. cepedianus, such as seasonality and site fidelity. It also addresses habitat use of the two coastal areas (River/estuary and a Bay) and possible migratory behaviour once the sharks leave these coastal areas. Chapter 6 then compares the coastal movement patterns of N. cepedianus with its chondrichthyan prey species. Specifically, if prey movement determines predator movement, whether there is spatial overlap in habitat use between predator and prey, and evaluate the effectiveness of shark protected areas as a management tool in protecting shark species. The first five data chapters establish predator-prey relationships, the

These chapters have been removed for copyright or propriety reasons.

Chapter

Sequential movement into coastal habitats and high spatial overlap of predator and prey suggest high predation pressure in protected areas

INTRODUCTION

Investigating predator-prey relationships is an important component of identifying and understanding the factors that influence the structure and function of ecosystems. Much of the current information on predator-prey relationships is based on dietary analysis of the predator, particularly in marine systems, where direct observations of predatory events or predator-prey interactions are rare (Williams et al. 2004; Heithaus et al. 2008a; Kuhn et al. 2009). While a good understanding of predator-prey relationships requires knowledge of predators’ diets, information on movement patterns and habitat use of predators and their prey is equally important (Dupuch et al. 2009). For example, diet analysis confirms predation, but knowledge on the spatial use of predator and prey contributes to understanding predation pressure and spatial responses of predator and prey to each other (Heithaus et al. 2008a; Dupuch et al. 2009, Wirsing et al. 2010).

Despite the inherent difficulties in observing marine species, a number of studies have compared the spatial behaviour of large predators with that of their prey. For example, basking shark Cetorhinus maximus, humpback whale Megaptera novaeangliae and stellar sea lion Eumetopias jubatus movements were compared to the spatial use and depth-specific biomass of their plankton and fish prey using acoustic sounding methods and net surveys (Sims et al. 2005; Sims et al. 2006; Frid et al. 2007; Hazen et al. 2009). Belt transect surveys of a range of air breathing prey were also compared to abundance estimates and movement patterns of tiger sharks Galeocerdo cuvier (Heithaus et al. 2008a; Wirsing et al. 2010). Studies such as these have vastly improved our understanding of large marine predators’ spatial use in relation to their prey, providing valuable information on predator foraging behaviour and predator-prey relationships such as predation pressure exerted on prey and the prey’s behavioural response to predation. These studies also contribute to the general understanding of predation in ecosystem dynamics, e.g. regulating the effects of mesopredators and herbivores on lower trophic levels and maintaining ecosystem health, diversity and stability (Frid et al. 2008; Heithaus et al. 2008a). However, there is still a scarcity of empirical knowledge pertaining to the simultaneous spatial use of predator and prey, when both are moving freely in their natural environment (Lima 2002; Dupuch et al. 2009). Furthermore, various theoretical models of how predator and prey should move about the landscape in relation to one another have also been developed (see Laundre 2010). However, do predator and prey conform to these models in real life? More empirical data of predator and prey movements are required to continue testing such models (Frid et al. 2008; Laundre 2010; Morales et al. 2010). Given the advancement in electronic tagging technology, it is surprising that only a few studies have used electronic transmitters to simultaneously track the movement patterns of both predator and its prey (Laroche et al. 2008;

Barnett et al. 2010d Chapter 7; Laundre 2010). Studies that concurrently track predator and prey should add considerably to the current information on predator-prey spatial use. The present study addresses the clear need for more multi-species spatial studies and will contribute to the growing body of literature on predator-prey spatial use, both in aquatic and terrestrial systems, for which recent studies are finding many parallels (Wirsing and Ripple 2011).

Although not always the case (see Wirsing et al. 2010), in theory, predators should attempt to match the distribution of their prey, and prey to avoid areas of high predation risk (Lima and Dill 1990, Lima 1998; Dupuch et al. 2009). However, predator and prey distribution may vary over spatial scales. For example, in many marine systems, predator and prey distributions have high overlap at large spatial scales, but do not coincide at small spatial scales (Heithaus and Dill 2006). Therefore, the objective of this study is to investigate predator-prey relationships by determining if predator movement is linked to prey movement at two spatial scales. Specifically, the seasonal use of coastal protected areas by predator (N. cepedianus) and prey (chondrichthyan species) was investigated to compare large spatial scale movement patterns. The spatial overlap in habitat use of N. cepedianus and its prey was then examined in finer detail within a large coastal bay.

METHODS

Study area, acoustic receiver deployment

An array of 74 acoustic receivers was deployed in coastal areas of southeast Tasmania (VR2 receivers, VEMCO Ltd., Halifax, Canada) (Fig. 6.1). Chondrichthyans were tagged in two locations, Norfolk Bay and Derwent Estuary (Fig. 6.1). Norfolk Bay is a relatively shallow (average depth 15 m; max depth 20 m), semi-enclosed bay with an area of approximately 180 km2. The landscape of the area is featureless with not much structure. The substrate is mostly silt and silty sand with algae (family Caulerpaceae) and seagrass around the edges. The Derwent Estuary runs through the City of Hobart before opening into Storm Bay, and consistently reaches depths of 20-30 m, with a maximum depth of 44 m. The study area encompasses ‘shark protected areas’, so the acoustic array was deployed in a series of single curtains and gates to determine the residency of chondrichthyans in these protected areas (Fig. 6.1). The larger array was deployed from December 2007 to June 2009, with the receivers at the entrance to Norfolk Bay (Line E; Fig. 6.1) and the Derwent Estuary (Line B, Fig. 6.1) remaining in place until June 2010 (See Chapter 5 for detailed explanation of acoustic array design).

Study species: link between predator, prey and fisheries

Dietary studies from Tasmania and other geographic regions suggest a strong predator-prey link between N. cepedianus and other chondrichthyan species, particularly with sharks from the family Triakidae (see Barnett et al. 2010c Chapter 4 for summary of regional dietary studies). In Tasmania gummy sharks Mustelus antarcticus (family Triakidae) were the primary prey consumed and the main target species in the southern shark fishery (Barnett et al. 2010c Chapter 4). White-spotted spurdogs Squalus acanthias, elephant fish Callorhinchus milii and southern eagle rays Myliobatis australis were also important prey, and the first two species are common by catch in fisheries, with C. milii having a commercial value. (Barnett et al. 2010c Chapter 4). Although school sharks Galeorhinus galeus were not prevalent in N. cepedianus diet in Tasmania, this species, which is also a triakid, was included in the current study because these coastal areas are believed to be important habitats for juveniles, and they are in a population rebuilding phase after previously being the traditional target species of commercial shark fisheries in southern Australia (Olsen 1954; Stevens & West 1997). Notorynchus cepedianus have a particularly interesting relationship with shark fisheries, as apart from being a bycatch species with a commercial value, they are the most significant predators of juveniles of the commercially important shark species in protected coastal areas (Stevens & West 1997; Barnett et al. 2010c Chapter 4). Consequently, they may have a considerable impact on recruitment to the fishery.

Transmitter attachment

Sharks were caught on bottom-set longlines (Barnett et al. 2010a; Chapter 2) and acoustic individually-coded transmitters (VEMCO Ltd., Halifax, Canada) implanted into the body cavity via a 1– 2 cm incision in the abdominal wall (see Table 6.1 for tag details). The procedure was accomplished in 3–5 minutes, during which time running water was pumped over the gills. Sharks showed no ill effects from the method of capture and surgery, with all individuals swimming off instantly and powerfully after release. All methods used were approved by the University of Tasmania Animal Ethics Committee (#A0009120) and the Department of Primary Industries and Water (Permit # 8028).

Study design

The study has two components designed to assess both broad-scale and fine-scale spatial use of predator and prey in coastal areas. In the first field season (January–April 2008), 11 M. antarcticus, eight G. galeus (see Table 6.1 for details) and 20 N. cepedianus were tagged in Norfolk Bay to test fine-scale spatial overlap and habitat use of the two triakid species and N. cepedianus within the bay (see Chapter 5 for N. cepedianus details).

Additional prey species were tagged to determine if the different prey leave coastal areas for winter, as previously observed for N. cepedianus (Barnett et al. 2011; Chapter 5). Two S. acanthias were tagged in the Derwent Estuary just prior to the first winter (Table 6.1). In the second season, starting in spring (October) 2008, three M. antarcticus, six S. acanthias , three C. milii and three M. australis were tagged in the Derwent Estuary (Table 6.1). Three more M. antarcticus and two M. australis were also tagged in Norfolk Bay (Table 6.1). Due to failure to catch G. galeus, no additional individuals were tagged. To complement the spatial analysis, temporal patterns in abundance of chondrichthyan species in protected coastal areas was also estimated using seasonal longline sampling conducted at four fixed sites in both Norfolk Bay and the Derwent Estuary from summer 2006/2007 to summer 2008/2009 (methods and sampling design were identical to Chapter 2 methods).

Table 6.1. All shark tagging in Norfolk Bay (NBay) occurred between receiver lines G and F, and for the Derwent Estuary tagging was performed in Ralphs Bay except for 2 S. acanthias which were tagged at receiver Der 3 (see Fig. 6.1). Date is the day the animal was tagged. Battery life is the approximate number of days the tag was expected to transmit. TL is total length in cm. Return gives indication if sharks returned in spring after winter or remained in coastal region through winter, short indicates that the battery life was not long enough to detect if the animal returned after winter, depending on the day it was tagged.

ID Species Location Date Tag type Battery life Sex TL Return 8648 M. antarcticus NBay 30/1/08 V9-2H 160 m 71 short 12955 M. antarcticus NBay 30/1/08 V13P-1H 300 m 108 - 12956 M. antarcticus NBay 30/1/08 V13P-1H 300 m 87 - 12957 M. antarcticus NBay 30/1/08 V13P-1H 300 m 127 - 12954 M. antarcticus NBay 30/1/08 V13P-1H 300 f 90 return 8646 M. antarcticus NBay 30/1/08 V9-2H 160 f 70 short 12953 M. antarcticus NBay 30/1/08 V13P-1H 300 m 93 return 8647 M. antarcticus NBay 1/2/08 V9-2H 160 m 90 short 8643 M. antarcticus NBay 14/2/08 V9-2H 160 f 58 short 8638 M. antarcticus NBay 14/2/08 V13-1L 1000 f 81 - 1005 M. antarcticus NBay 7/4/08 V9-2H 160 f 72 - 10689 M. antarcticus NBay 18/11/08 V13-1L 1000 m 101 return 10690 M. antarcticus NBay 18/11/08 V13-1L 1000 m 85 - 10691 M. antarcticus NBay 19/11/08 V13-1L 1000 m 95 short 10687 M. antarcticus Ralphs 6/11/08 V13-1L 1000 m 112 - 10685 M. antarcticus Ralphs 12/11/08 V13-1L 1000 m 126 return 10688 M. antarcticus Ralphs 12/11/08 V13-1L 1000 f 126 - 8645 G. galeus NBay 5/2/08 V9-2H 160 m 39 short 8644 G. galeus NBay 9/2/08 V9-2H 160 f 68 no detect 8639 G. galeus NBay 14/2/08 V13-1L 1000 f 87 - 8640 G. galeus NBay 17/2/08 V13-1L 1000 f 68 - 8641 G. galeus NBay 17/2/08 V13-1L 1000 f 85 - 8650 G. galeus NBay 18/2/08 V9-2H 160 m 68 short 8649 G. galeus NBay 22/2/08 V9-2H 160 f 65 short 8651 G. galeus NBay 22/2/08 V9-2H 160 m 73 short 3772 S. acanthias Der 3 18/4/08 V7-2H 140 m 57 return 3773 S. acanthias Der 3 18/4/08 V7-2H 140 m 55 - 8652 S. acanthias Ralphs 20/10/08 V9-2H 160 m 72 short 52989 S. acanthias Ralphs 14/11/08 V9-2H 160 m 66 no detect 52990 S. acanthias Ralphs 26/11/08 V9-2H 160 m 68 short 52991 S. acanthias Ralphs 26/11/08 V9-2H 160 m 66 short 52992 S. acanthias Ralphs 26/11/08 V9-2H 160 m 73 short 10691b S. acanthias Ralphs 15/1/09 V13-1L 1000 m 70 remained 8642 M. australis Ralphs 6/11/08 V13-1L 1000 f 134 - 10686 M. australis Ralphs 12/11/08 V13-1L 1000 f 122 return 10692 M. australis Ralphs 30/11/08 V13-1L 1000 m 84 return 10693 M. australis NBay 11/12/08 V13-1L 1000 m 86 return 3147 M. australis NBay 10/1/09 V16-1L 170 m 88 short 3157 C. milii Ralphs 6/11/08 V16-1L 850 f 96 return 3145 C. milii Ralphs 14/11/08 V16-1L 850 f 88 remained 3146 C. milii Ralphs 30/11/08 V16-1L 850 f 98 no detect

Data analysis

Broad-scale analysis: seasonal use of coastal protected areas To interpret residency times in the shark protected areas, the number of days that each prey species was detected in the study area was plotted on a timeline. In addition all fishing sites were pooled and one way ANOVAs followed by Tukey honest significant difference (HSD) test were used to test for seasonal differences in Catch per Unit Effort (CPUE) for both N. cepedianus and its prey species. Here, only prey species with sufficient catch rates were analysed. Catch per unit effort was based on number of sharks caught per long line (50 hooks) per 4 hour set (Barnett et al. 2010a Chapter 2).The use of protected areas by prey species was then compared to previous movement information on N. cepedianus (Barnett et al. 2011; Chapter 5).

Fine-scale analysis: habitat use within Norfolk Bay

Spatial overlap To investigate spatial overlap of predator and prey, each VR2 receiver in Norfolk Bay (Fig. 6.1) was classified as a resource, and the number of hours N. cepedianus, M. antarcticuss and G. galeus were present at each receiver used as an indication of how often an individual and a species used that resource area. If a shark was detected at least once in any particular hour it was considered having been present during that hour. Niche overlap analysis was conducted in EcoSim 700 using Piankas index (O), permutated 1000 times. The degree of overlap is presented in a 0–1 scale, where 0 means no overlap and 1 means complete overlap.

Habitat use To compare habitat use between the predator and its prey in Norfolk Bay, receivers were pooled into three groups based on depth and location within the bay. The three groups were: shallow water, middle of the bay area (deep water) and edge areas. Edge areas were those close to land, including islands in the bay, but not as shallow as the shallow water group (see Table 6.2 and Fig. 6.1 for details of the receivers used). Data analysis was based on the number of hours each species was present in each habitat. If a shark was detected at least once in any particular hour for each day of the study then it was considered present for that hour. Hourly shark presence at each of the three habitat types was determined by grouping all hourly detections for each individual into its species and into hourly bins (i.e. 24 hourly bins). Rao’s spacing test for uniformity (circular statistics, Oriana 3

software) was used to test if the number of hours spent in each habitat varied throughout the diel cycle for each species.

Table 6.2. Norfolk Bay receivers, showing depth in metres they were deployed in, and which receivers were used for the three habitat analyses, indicated by the habitat they were pooled in.

Receiver Depth (m) Habitat E1 10 - E2 12 - E3 19 - E4 17 - F1 9 Edge F2 21 - F3 20 Middle F4 20 Middle F5 21 Middle F6 9 Edge F7 5 Shallow F8 4 Shallow F9 5 Shallow G1 14 Edge G2 16 - G3 16 Middle G4 17 Middle G5 17 Middle G6 15 Middle G7 15 - G8 14 Edge K1 14 Middle K2 14 - K3 13 - K4 13 Edge L1 15 Edge L2 15 Edge L3 15 Edge EH1 8 Shallow EH2 10 Shallow X1 6 Shallow X2 6 Shallow X3 8 Shallow DC 3 -

RESULTS

Broad-scale analysis: seasonal use of coastal protected areas

All chondrichthyan species analysed showed significant seasonal differences in CPUE (p < 0.0001). For G. galeus, M. antarcticus, S. acanthias and N. cepedianus this was primarily driven by a decline in catches during winter, although G. galeus also showed lower catches in spring (Fig. 6.2). However, unlike the other four species, the highest catch rates for Whitley’s skate Spiniraja whitleyi were in the winter (Fig. 6.2). Spiniraja whitleyi were still a significant component of the catch for the other three seasons (Fig. 6.2), and catches between the three seasons were similar (p = 0.9999).

The movement data shows a similar pattern to the variations in CPUE, with the majority of prey individuals moving out of the coastal areas in autumn and being absent during winter (Fig. 6.3). The three animals, one C. milii and two S. acanthias that remained over winter (Fig. 6.3) were only detected in the Derwent Estuary. In the first year, two M. antarcticus returned after winter and in the second year two other M. antarcticus, three M. australis and one C. milii returned (Table 6.1). In all cases, individuals returned to the location they were originally tagged. The only individual to move between the two primary study locations (Derwent Estuary and Norfolk Bay) was a S. acanthias, and no animals moved into the Pittwater area (receivers PW, Fig. 6.1). The furthest up-river animals were detected was at receiver D6 (for S. acanthias) and D7 (for C. milii) (Fig. 6.1).

3.0

N. cepedianus M. antarcticus 2.5 G. galeus S. acanthias S. whitleyi 2.0

1.5

1.0

CPUE sharks per 50 hooks 50 per sharks CPUE 0.5

0.0 Summer Autumn Winter Spring

Seasons

Fig. 6.2. Seasonal catch per unit effort (CPUE) of the main chondrichthyans caught from longline surveys.

Norfolk Bay: fine-scale analysis

Spatial overlap

Spatial overlap in area use of Norfolk Bay was low to moderate between individuals from the same species (Piankas index: M. antarcticus O = 0.34; G. galeus shark O = 0.56; N. cepedianus O = 0.55) and all individuals from the three species (O = 0.45). However, when individuals were pooled for each species and niche overlap was compared between species, spatial overlap was high (O = 0.7), indicating that although many individuals differ in spatial usage there are common areas that are used a lot by the different species. The areas of high spatial overlap were the deeper areas of the bay. In particular, the areas around receivers F2 to F5, which correspond to the deepest section of Norfolk Bay (Figs 6.1, 6.4). Mustelus antarcticus also spent time in edge areas (Fig. 6.4). The biggest difference between N. cepedianus and the other two species was their use of the entrance to the bay (line E, Figs 6.1, 6.4). In contrast to the other three species tracked in Norfolk Bay, M. Australis spent the majority of its time in edge habitats (Fig. 6.4).

M. antarcticus

G. galeus

S. acanthias M. antarcticus

S. acanthias

M. australis

C. milii

M. antarcticus D

Feb-08 Apr-08 Jun-08 Aug-08 Oct-08 Dec-08 Feb-09 Apr-09 Jun-09

Days

Fig. 6.4. Area use of four species in Norfolk Bay based on the number of hours each species was detected at each receiver. The dark grey shows were 50% of the hours where detected and the light grey shows where approximately 70% of hours detected. Black dots are receivers

Habitat use

G. galeus used both edge (Rao’s spacing test p < 0.01) and middle habitats more at night (p < 0.01) and rarely moved into shallow areas (Fig. 6.5). Mustelus antarcticus showed diel differences in habitat use for all three habitat types (Rao’s spacing test p <0.01). They used edge habitats more during the day and mid habitats more at night (Fig. 6.5). Although movement into shallow water was infrequent, when it did occur it was normally at night (Fig. 6.5). N. cepedianus also showed diel differences in habitat use (Rao’s spacing test p <0.01). However, the distinction between night and day use of edge and middle habitats is not clear cut because animals spent many hours in these habitats during both day and night (Fig. 6.5).In particular, for the middle habitat all time bins during the diel cycle had over 300 hours of shark use (Fig. 6.5). Nevertheless, N. cepedianus used the middle 85

habitat more during the day and the edge habitat more at night (Fig. 6.5). As with M. antarcticus, movement into shallow water was infrequent, but when it did occur it was normally at night (Fig. 6.5). The N. cepedianus pattern appears to be that they move over the middle and out to the edge of the bay during the day, however at night they expand their search patterns and cover more of the edge and sometimes moving into shallows. Overall, results show that all three species spend most of their time in the middle of the bay, and that they all show diel differences in habitat use.

DISCUSSION

Broad-scale movements: seasonal use of coastal protected areas

Distinct seasonal differences in the occurrence of chondrichthyan species in coastal areas was detected by both CPUE and movement analysis. There were many similarities in movement patterns of prey and N. cepedianus (Barnett et al. 2011; Chapter 5). The general pattern is for N. cepedianus and its prey to exit these coastal areas for winter and return the following spring/summer. The few instances when animals were present in winter, both N. cepedianus (Barnett et al. 2011; Chapter 5) and its prey were only detected in the Derwent Estuary. Also, receiver D7 (Fig. 6.1) was the furthest up-river both predator and prey moved (Barnett et al. 2011; Chapter 5). Evidence from N. cepedianus diet and seasonal abundance (predator and prey) combined with the similarity in movement patterns, and the high spatial overlap of predator and prey in Norfolk Bay, supports the hypothesis that N. cepedianus move into coastal systems following their main chondrichthyan prey (Barnett et al. 2010a,c; Barnett et al. 2011; Chapters 2, 4 & 5). Also, when CPUE of prey decreased over the three years in Norfolk Bay, so did that of N. cepedianus, suggesting lower resource availability resulted in fewer predators utilising the area (Barnett et al. 2010c Chapter 4). For many animals, it is difficult to distinguish habitat selection for foraging purposes from that associated with mating or predator avoidance. However, most adult apex predators do not have to invest energy into anti-predatory behaviour, and since information on population structure suggests that these coastal areas are not important mating, pupping or nursery areas for N. cepedianus (Barnett et al. 2010a Chapter 2), it is possible to separate foraging from these other behaviours.

Although a number of chondrichthyan individuals returned to the coastal areas in spring after being absent for winter, many of the transmitters had relatively short battery lives, meaning that perhaps more returned, but were not detected. Long-term monitoring using transmitters with long life batteries is required to determine the importance of these protected areas to juvenile sharks as they grow over multiple years. For example, neonate G. galeus born in the shallow waters of Pittwater are believed to move to deeper waters of adjacent bays at the end of their first summer (Stevens & West 1997). However, do they remain in these deeper bays for the next phase of their lives, or do they return to Pittwater over multiple years? Interestingly, no tagged prey species moved into Pittwater during the current study.

The occurrence of N. cepedianus in coastal areas during winter suggests that water temperature is not a strong factor in determining seasonal habitat use (Barnett et al. 2010a Chapter 2; Barnett et al. 2011 Chapter 5). But, temperature may indirectly affect the abundance of N. cepedianus if prey 87

species are departing coastal areas to find appropriate thermal conditions. Water temperature is believed to be an important factor in coastal habitat use for a number of shark species (Froeschke et al. 2010; Speed et al. 2010) with some coastal species moving into deeper waters over winter (Stevens & West 1997; Conrath & Musick 2008; Cortés et al. 2011). Of the prey species sampled in the current study, the only chondrichthyan caught in relatively high abundance during winter was the Whitley skate Spiniraja whitleyi. Although S. whitleyi were caught more during winter, I suspect that they are just as abundant throughout the year, illustrated by the similarity in CPUE for the other three seasons. However, the high abundance of N. cepedianus from spring to autumn may intimidate S. whitleyi and therefore limit opportunities to access the longlines. Although in this case the bait is an introduced resource, similar decisions between foraging opportunities and predation risk by N. cepedianus may affect foraging behaviour of chondrichthyan species in coastal areas of Tasmania. I acknowledge that this hypothesis is only speculative at present and further investigation is required. However, risk effects are believed to be just as important as predation in regulating mesopredators and maintaining the diversity and equilibrium of systems (Lima and Dill 1990; Brown et al. 1999; Heithaus et al. 2008a), particularly as non-lethal effects can affect many individuals within prey populations simultaneously (Heithaus et al. 2007b). There are numerous examples of predators preventing prey from fully exploiting resources. For example, Wirsing et al. (2007d) predict that when the risk of predation is high, dugongs adjust their foraging tactics from digging up seagrass, which causes sediment plumes and limits the dugongs’ ability to see predators, or may even attract them, to cropping the tops of the seagrass. Sea lions foraging under the threat of sleeper sharks at depth choose shallow waters, thereby underutilising important resources in deep strata (Frid et al. 2007). Mule deer Odocoileus hemionus choose less productive open area habitats over forested areas, as predation risk from pumas Puma concolor was considerably reduced (Laundre 2010). Similarly, N. cepedianus in coastal Tasmania could also provoke a fear-based system, with the constant threat of predation influencing other species’ behaviours. However, further work is needed to pursue this hypothesis.

Fine-scale habitat use: Norfolk Bay Foraging theory predicts that animals will select habitats that provide the greatest return in some form of currency, such as abundant food or protection from predators (Stephens and Krebs 1986). Accordingly, Norfolk Bay appears to be a rich source of food for N. cepedianus. However, given the high abundance of N. cepedianus, coupled with a lack of landscape features to provide shelter, it appears that Norfolk Bay is not a safe place for M. antarcticus or G. galeus. If animals trade-off

resource availability (energy gained) with predation risk, then are M. antarcticus and G. galeus mainly using the deepest area of the bay because there is more food, or alternatively, is this the safest area in an overall dangerous bay?

The growing literature on behavioural responses of prey (including spatial use) to the threat of predation (e.g. Wirsing and Ripple 2011) provides a setting for interpreting the spatial use of M. antarcticus and G. galeus in Norfolk Bay. It’s typically assumed that prey avoid predators (Lima 1998; Dupuch et al. 2009). However, an emerging view is that a prey’s spatial response to predation risk is context dependant (e.g. species and system specific), and factors such as predator hunting mode, landscape features, prey body condition (energetic state) and escape tactics of prey can determine spatial use under the threat of predation (Wirsing et al. 2010; Wirsing and Ripple 2011). Indeed, in some cases prey may select space where predators are most abundant if it is advantageous for their mode of defence or there is high energetic benefit (Wirsing et al. 2010; Wirsing and Ripple 2011). For example, when under the threat of predation from tiger sharks, bottlenose dolphins Tursiops truncatus and dugongs avoid shallow seagrass areas despite less chance of encountering tiger sharks, and use the edge of sea grass banks, where shark abundance is relatively high, but escape probability is greater due to access to deeper waters (Wirsing et al. 2010). Thus, when threatened, bottlenose dolphins and dugongs choose microhabitats that promote escape rather than avoidance (Wirsing et al. 2010). Similarly, M. antarcticus and G. galeus may opt for deeper areas of the bay if there is an antipredator advantage, e.g. if deeper areas improve escape probability when encountering N. cepedianus or allows easier detection (effectiveness of vigilance) of N. cepedianus (Brown et al. 1999). This may be the best tactic in Norfolk Bay due to the lack of any complex habitat to hide (Wirsing et al. 2010). Alternatively, the deeper areas may contain greater resources, and therefore higher energetic return for juvenile sharks, e.g. faster growth.

Results suggest that N. cepedianus and M. antarcticus expand their area use at night. Previous fine- scale tracking of N. cepedianus also suggested they were more active at night, and this may be linked with a preference for nocturnal foraging (Barnett et al. 2010a Chapter 2). If M. antarcticus are expanding their area use at night, this could be a tactic to avoid being easy targets in a featureless landscape, when N. cepedianus are most active. Alternatively, it could also be a foraging tactic. In accordance with both of these ideas, M. antarcticus may move to shallow areas (possibly riskier habitats) to forage at night, when N. cepedianus are less likely to see them (Barnett et al. 2010a Chapter 2). In response, the infrequent use of shallow areas by N. cepedianus may be a tactic to

surprise less vigilant prey (Laundre 2010). However, to further pursue this type of hypothesis, estimates of M. antarcticus prey abundance are needed to determine which areas of Norfolk Bay are more productive. Although G. galeus showed a strong preference for deeper areas, why they were detected considerably more at night and where they are during the day is unclear. Results show they are still in the bay, but they must be in areas of low receiver coverage during the day. Previous work proposed that G. galeus feed mainly at night (West and Stevens 2001), so perhaps they are detected more during the night because they are more active.

CONCLUSION

If hunting is concentrated in a relatively small area, as the spatial use of N. cepedianus in Norfolk Bay suggests, then a predator can have a significant impact on prey populations (Williams et al. 2004). Given the common occurrence and high abundance of N. cepedianus in the Tasmanian coastal waters gazetted as shark protected areas during summer, the prevalence of chondrichthyan species in their diet, and the high spatial overlap of predator-prey, it is likely that they exert significant predation pressure on these species (Barnett et al. 2010a, b; Barnett et al. 2011; Chapters 2, 4 & 5). Overall, it appears that most chondrichthyans are exposed to fishing pressure when they leave protected areas for winter. However, during the warmer months fishing pressure is reduced by spending time in protected areas, but during this time they are highly vulnerable to predation. Our results illustrate the value of simultaneously recording and integrating multiple types of information to better understand predator-prey relationships (e.g. spatial relationships) and predation pressure.

This chapter has been removed for copyright or propriety reasons.

Chapter

General Discussion

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SYNTHESIS OF MAIN RESULTS

Identifying factors that influence habitat selection at multiple spatial scales is of considerable importance in ecology (Heithaus & Dill 2006). The basic instincts for all animals are to avoid predation, feed and breed. These behaviours are driven by interactions within and between species, environmental conditions, and the biology of the species involved (Alonzo et al. 2003; Kuhn et al. 2009). An understanding of these three key behaviours should give some indication of why, when and how an animal uses a particular habitat and what is likely to influence population distribution patterns across spatial and temporal scales (Heithaus & Dill 2006).

Accordingly, the strong seasonal site fidelity and the large numbers of N. cepedianus occurring in coastal waters of south east Tasmania in summer indicates that these areas are important habitats for this species. The absence of neonates implies that these areas are not nursery grounds for this species. Initial results also indicate that these coastal habitats do not have any definite reproductive relevance, although more work is needed to clarify this point. The high catch rates also indicate that N. cepedianus is an integral component of the species composition in this coastal ecosystem. In fact, results from this study reinforce the interpretation that N. cepedianus is a top order predator in coastal temperate systems in general (Ebert 2002; Lucifora et al. 2005). The globally consistent occurrence of similar prey (e.g. triakids, myliobatids and marine mammals) shows predictable predator-prey relationships and suggests that N. cepedianus could play a role in regulating mesopredators across its global distribution. These global patterns are useful for ecosystem studies and management planning worldwide. However, the relatively low dietary overlap between sharks sampled in the two coastal locations in this study also emphasises the need to compare dietary data over fine spatial scales. Indeed, the low overlap in diet and area use highlights the possibility of habitat partitioning in these large apex predators, even though they move over large distances.

Other interesting results included the overlap in habitat use by N. cepedianus in the lower Derwent area, and the temporal sexual segregation in the use of the coastal areas considered. The lower Derwent appears to have some particular relevance in late autumn prior to the majority of N. cepedianus departing the coastal systems for winter. Two possibilities for the lower Derwent use in autumn are that prey is abundant in this region at this time, or perhaps there is a social reason for N. cepedianus congregating prior to sharks departing for winter. The most obvious behaviour would be for mating and this would coincide with the autumn peak in male abundance, after their later arrival than females to the coastal areas. Also, the modal size range of sharks caught in the Derwent Estuary was larger than that of sharks from Norfolk Bay. Further work classifying the reproductive status of females, including looking for fresh mating scars at this time of year, would be beneficial. The 111

presence of some females in coastal areas during winter is also interesting and this is discussed in the section below (fisheries interactions and management implications).

For many animals, it is difficult to distinguish habitat selection for foraging purposes from those associated with mating or predator avoidance. However, most adult apex predators do not have to invest much energy into anti-predatory behaviour, and since most reproductive behaviour is seasonal, it is often possible to separate foraging from these other behaviours. In the present study, the information collated on diets, seasonal abundances (predator and prey) and movement supports the hypothesis that N. cepedianus move into coastal systems following its main chondrichthyan prey. A similar pattern was identified in California, where N. cepedianus follows elasmobranch prey species into coastal areas in summer (Ebert 1989). Therefore, foraging is probably the primary reason that N. cepedianus use these coastal habitats. The large number of N. cepedianus in these systems suggests that if they are moving into these habitats to feed, then they have the potential to significantly influence the overall community dynamics through both direct predation and risk effects.

THE ECOLOGICAL ROLE OF MARINE APEX PREDATORS – THE NEED FOR MORE EMPIRICAL STUDIES

This study is an important contribution to the ecology of sevengill sharks and marine apex predators in general. The incorporation of movement behaviour, trophic information, population structure and abundance estimates of predator and prey allowed a much finer understanding of the habitat use and role of N. cepedianus in coastal areas of Tasmania. This study highlights the need for multi- faceted empirical approaches to understand the ecology of large mobile marine predators, and this information can then be used in broader ecosystem studies that incorporate empirical data with modelling techniques (Smout & Lindstrom 2007; Laroche et al. 2008; Frid et al. 2009).

For example, marine mammals can be significant predators in the marine food webs (Punt and Butterworth 1995; Morissette, 2006; Wirsing et al. 2008; Estes et al. 2009). However, with the exception of a few studies (in particular killer whales Orcinus orca and sea otters Enhydra lutris (Estes et al. 1998; Estes et al. 2009)) the role of marine mammals in structuring most systems remains unclear (Yodzis 2001; Morissette, 2006; Estes et al. 2009). This is partly due to insufficient behavioural information for both predator and prey (e.g. how prey respond to predation risk from marine mammals) and a lack of field based studies (Williams et al 2004; Smout & Lindstrom 2007; Estes et al. 2009). Even studies that have incorporated detailed ecological information from field based experiments (such as movement behaviour) into their models cite the need for more empirical 112

data to better understand behaviour and species interactions (Smout & Lindstrom 2007; Laroche et al. 2008; Frid et al. 2009).

The current study sets a platform for the expansion of this work to further evaluate ecosystem affects of N. cepedianus in south east Tasmania, by studying the ecology (movement, abundance, demographics and diets) of their mesopredator prey species. A series of predator-prey studies in Shark Bay, Western Australia (Heithaus et al. 2008a and references therein), where the seasonal occurrence and movement patterns of tiger sharks Galeocerdo cuvier (Wirsing et al. 2006) has been shown to influence the spatial distribution and behaviour of numerous prey including dugongs, dolphins, turtles, pied cormorants and sea snakes (Heithaus & Dill 2006; Wirsing et al. 2007a,b; Heithaus et al. 2007b; Wirsing et al. 2008; Wirsing & Heithaus 2009; Heithaus et al. 2009). For many of these species, the risk of predation had a significant effect on behaviour (risk effects), even if direct predation events are rare (Heithaus et al. 2008a). Risk effects are believed to be just as important as predation in regulating mesopredators and maintaining the diversity and equilibrium of systems (Lima and Dill 1990; Brown et al. 1999; Heithaus et al. 2008a). Notorynchus cepedianus could have a similar effect (plays a similar role) in the coastal systems of Tasmania. Their high abundance may provoke a fear based system, with the constant threat of predation influencing other species’ behaviours. Ongoing surveys and movement studies of N. cepedianus prey (e.g. chondrichthyans, marine mammals, teleosts) and, importantly, the abundance and distribution of respective food resources are needed to understand how different prey respond to predation pressure from N. cepedianus, and how predation (including risk effects) influences ecosystem dynamics.

FISHERIES INTERACTIONS AND MANAGEMENT IMPLICATIONS

Natural mortality is an important, but difficult, parameter to estimate in assessing commercially fished populations. However, given the common occurrence and high abundance of N. cepedianus in the Tasmanian coastal waters gazetted as shark nursery areas (Stevens & West 1997), and the prevalence of Mustelus antarcticus in their diet, it is likely that they exert significant predation pressure on this commercially important species. This may have a significant effect on recruitment of this species to the fishery. This impact may be even greater if predation pressure is similar in other areas where juvenile M. antarcticus are found. Notorynchus cepedianus is competing with humans (fisheries) as the top predators for common food resources (Yodzis 2001), and as mortality from predation can exceed that from fisheries (Bax 1998), this information may be important for stock assessment models.

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Interestingly, the other commercially important shark species in Tasmania, Galeorhinus galeus, was not a prominent prey item either in this study or in an earlier study by Stevens & West (1997). However, this species has been overfished, and there are fears that the breeding stock still using this region is severely depleted (Stevens & West 1997). The low numbers of G. galeus found in the diets of N. cepedianus in the present study coincided with low catch rates found for this species during this same period, suggesting that G. galeus stocks and thus recruitment capabilities are still low. The low productivity of G. galeus (slow growth, high age at maturity, high longevity and low annual fecundity) (Walker 1998) suggests that predation pressure from N. cepedianus may possibly suppress the recovery potential of G. galeus, even when fishing effort has been reduced and nursery areas protected. Further surveys specifically targeting G. galeus are required to conclusively determine if their absence from N. cepedianus diet is due to low abundances in these coastal areas.

In particular, surveys need to be conducted in the Pittwater area to determine if abundances of G. galeus have declined since previous surveys (Olsen 1954; Stevens & West 1997). School sharks are normally born between December and January, with new born pups mainly found in Pittwater and close inshore along the Seven Mile Beach area of Frederick Henry Bay (see Fig. 8.1). They remain in these inshore areas until autumn and then in winter school shark juveniles are only caught in Storm Bay (Stevens & West 1997). In subsequent summers, pups continue to use deeper bays as they grow, but after 1 year they tend to move into Norfolk and Frederick Henry Bays, and rarely return to Pittwater (Fig. 8.1). Essentially, the pups move from Pittwater to Storm Bay, using deeper habitats as they grow older (see Fig. 8.1).

The lack of movement by N. cepedianus into Pittwater (Barnett et al. 2011; Chapter 5), despite the traditionally high abundance of their chondrichthyan prey (Olsen 1954; Stevens and West 1997; Stevens and West unpublished data) suggests this is a safe area for juvenile chondricthyans. However, as juveniles grow, they face increased predation pressure in adjacent bays. The low number of 1+ year school sharks caught in Pittwater may be due to a lack of sufficient food resources. After the first summer in Pittwater, sharks may need to forage in more productive areas to expedite growth, and reduce time spent at vulnerable smaller sizes. Essentially, juveniles have to trade safety for body condition (Heupel et al. 2007).

As mentioned in chapter 6, the high abundance of juvenile chondrichthyans in these coastal areas (despite the high risk of predation) suggests that the energetic benefits for some species must outweigh the high predation risk (Heupel et al. 2007). Particularly, the non-descript nature (lack of landscape features) of Norfolk Bay means there is little structure to provide shelter for N. cepedianus. For example, juvenile M. antarcticus may trade the use of safer habitats (i.e. more 114

structure for shelter) for abundant resources to accelerate growth over the summer period, before moving out of the Norfolk Bay area in winter.

Fig. 8.1. Distribution of school sharks by age group caught in south east region of Tasmania. The number in brackets in the legend is the total number caught for that age class. Figure taken from Stevens and West 1997.

However, foraging in habitats with high predation risk as opposed to investing energy in anti- predator behaviour will depend on the body condition of the prey (Heithaus et al. 2008a). So, an alternative hypothesis is that resource scarcity often results in decreased energy state of mesopredators, which leads to increased risk taking and hence higher predation rates (Heithaus et al. 2008a). Thus, when top predators are abundant and resources are scarce, the prey is forced into riskier foraging areas and direct predation is the dominant interaction between predator and prey (Heithaus et al. 2008a). In contrast, when resources are plentiful, fit (high energy reserves) mesopredators are able to afford the cost of anti-predator behaviour, therefore choosing safer habitats in which to forage that may be energetically less profitable but off reduced predation risk.

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Although under these conditions direct predation on mesopredators would be low, their behaviour is still affected by risk effects i.e. the threat of predation still influences foraging behaviour (Heithaus et al. 2008a). The decline in M. antarcticus abundance over three years in Norfolk Bay could theoretically be linked to such a scenario (Barnett et al. 2010c Chapter 4). If M. antarcticus body condition was higher in the second and third years of the study, then they may have foraged in other areas with less plentiful resources, but where the chance of predation was lower, resulting in a reduction of numbers recorded for Norfolk Bay in comparison with the first year (see Chapter 4). To test this hypothesis, it is first necessary to identify the other areas used by prey species such as M. antarcticus and G. galeus. Then, within each area, resource availability, predation risk and the condition (state) of the prey has to be assessed and compared.

Storm Bay is potentially an important habitat for both N. cepedianus and other chondrichthyans, and it may have particular relevance during winter. Stevens and West (1997) suggest that juvenile school sharks move into this bay for winter. The absence or low numbers of many chondrichthyan species in catches during winter suggests that other species may also move to deeper waters for winter. Storm Bay may also be a corridor for deep water species (e.g. elephant fish and sawsharks) seasonally moving between deeper waters and inshore coastal regions. The detection of female N. cepedianus at the entrance of the Derwent Estuary along the border with Storm Bay throughout winter suggests Storm Bay may be a wintering site for some females. This segregation of sexes and between females over winter and spring could be related to resource partitioning. Here, males move north after summer when resources in coastal regions are less abundant, while some females move only to Storm Bay, and others move even further afield, perhaps to offshore areas. Alternatively, there might be a reproductive relevance for females in Storm Bay. The significance of this bay needs to be clarified, particularly as this area is not protected from fishing. If it does prove to be an important area, management may need to review current protected areas.

The possible impact on recruitment of commercially important species is not the only interaction that N. cepedianus has with fisheries. This species is also a prominent commercial species, albeit being generally caught as bycatch and having a market value considerably lower than the main target species. However, N. cepedianus is also linked to fisheries by being an important predator of mesopredators such as chondrichthyans and seals that compete with fisheries for other commercial species (see Box 1 Fig. 8.2 for the food web interactions). In particular, fur seal Arctocephalus pusillus numbers have recovered significantly in Tasmania since their protection in 1975 and many fishermen deem them as competitors for diminishing resources (Kirkwood et al. 2010). Similar scenarios are evident with other marine mammal species around the world (Yodzis 2001; Morissette, 2006; Estes

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et al. 2009). These species can be high level predators, competing with humans for resources, but they are also important prey to larger shark species and killer whales (Klimley et al. 2001a; Williams et al. 2004; Wirsing et al. 2008). So, from the fishing industry perspective, N. cepedianus are both villains and allies i.e. they may prey on commercial species, thus possibly affecting recruitment to the fishery, but they also aid the fishery by keeping seal numbers in check. From an ecosystem perspective (including humans), a large reduction of N. cepedianus will not just affect this species, but may also affect a wide range of target and bycatch species, which could possibly lead to changes in the nature of top-down regulation in Tasmanian waters (for reviews on top down regulation see Heithaus et al. 2008a; Baum & Worm 2009; Ferretti et al. 2010). Therefore, future assessment of the effects of large sharks should consider both natural and fishing mortality, as the interaction of both contributes to observed changes in ecosystem structure (Ferretti et al. 2010). Overall, the interactions between apex predators, mesopredators and fisheries is often complex. However, the complexities of the Tasmanian system (Fig. 8.2) makes for interesting future analysis.

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Box 1.

Fig. 8.2. Simplified interpretation of a section of the upper trophic levels of the food web in coastal areas of Tasmania, related to species with a commercial value. The fisheries and Notorynchus cepedianus are the highest predators and compete for many of the resources. However, seals also compete with the fisheries for much of the teleosts and invertebrates (e.g. cephalopods). Due to the protection of seals, N. cepedianus would be the main regulator of seal numbers, therefore assisting the fishery by removing competitors. So, although they would be significant competitors in the shark fishery, N. cepedianus would assist the teleosts and invertebrate (e.g. cephalopods, crustaceans, scallops, abalone) fisheries by regulating the mesopredators (seals and other chondrichthyans) in Tasmania. Note, that gummy and school sharks have a much higher market value than the elephant fish, sawshark and N. cepedianus in the fishery. There is no commercial value for draughtboard sharks or batoids, however they would be significant predators/competitors of invertebrates and are prey of N. cepedianus.

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FUTURE STUDIES

This thesis is the first detailed study of the ecology of N. cepedianus. Overall, results indicate that N. cepedianus are keystone predators in coastal areas of Tasmania. However, this thesis is only one of the first steps for understanding the importance of N. cepedianus on ecosystem dynamics, and further long-term studies monitoring multiple species, including their main prey and competitors are still needed. For a complete understanding on the ecology of an area, it is necessary to obtain as much information as possible on the ecology of key species so that data from other co-occurring species, including predators, prey and competitors, can be combined and the ecological processes more accurately interpreted. Thus, the information presented in this thesis constitutes an essential component of future work and will be helpful for 1) understanding the ecology and ecosystem dynamics in other coastal areas around the world where N. cepedianus are abundant and 2) as a reference for future large predator studies in general. Throughout the various chapters, I have noted the need for future research, and the following points summarise the areas that still need to be addressed:

1. Continue to investigate where Notorynchus cepedianus goes when it leaves coastal areas of Tasmania. Determine whether ales are moving to specific habitats when they migrate north to coastal NSW for winter. Establish if females travel long distances over winter, and if they have specific pupping areas.

2. Further work classifying the reproductive status of females when they are in coastal areas.

3. Investigate if neonates and juveniles are using specific nursery areas.

4. Crucial to future work is the detailed investigation of the relevance of Storm Bay for habitat use of both N. cepedianus and other chondrichthyan species. At present, commercial and recreational fishing is conducted in Storm Bay. However, if sharks are moving from protected areas to spend significant amounts of time in Storm Bay (just outside protected areas) then they are still vulnerable to exploitation.

5. More research is required to understand the role that predation plays in nursery areas (Heupel et al. 2007).

6. Define the functional role of Mesopredators in coastal ecosystems of Tasmania.

7. Examine the complex relationships between N. cepedianus and mesopredators and determine how their interactions/relationships drive ecosystem structure and dynamics.

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8. The continued collection of dietary, movement and abundance information for species in these coastal areas will also be useful for future ecosystem models. Energy budget studies of the key species will also be useful for predator-prey and ecosystem models.

9. Long-term movement study of chondrichthyan prey species to detect habitat use over multiple years. In particular, tag juvenile gummy and school sharks with long life acoustic tags to examine the importance of these protected areas to juvenile sharks as they grow, and therefore, judge the overall effectiveness of these protected coastal areas.

10. Surveys are needed to determine the size and age structure of juvenile shark populations in coastal areas. The designation of these locations as nursery areas was based on data collected during an extensive survey of bays and estuaries around Tasmania in the 1940s. A subsequent re-sampling of these areas from 1991-1997 showed that juvenile sharks were either absent from or occurred in significantly lower numbers at all sites. However, no assessment of these proposed shark nurseries have been carried out since, therefore further surveys are needed. In particular, surveys need to be conducted in the Pittwater area to determine if abundances of G. galeus have declined since previous surveys (Olsen 1954; Stevens & West 1997), and determine if predation pressure from N. cepedianus may suppress the recovery potential of G. galeus.

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