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Diet and Reproductive Biology of Pelagic Sharks in Southern Australia: Understanding Their Ecology to Enhance Policy Development and Conservation Management

Diet and Reproductive Biology of Pelagic Sharks in Southern Australia: Understanding Their Ecology to Enhance Policy Development and Conservation Management

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Diet and reproductive biology of pelagic in southern : understanding their ecology to enhance policy development and conservation management

SARDI Publication Number F2009/XXX SARDI Research Report Series No. XX

SARDI Publication Number F2009/000162-1 SARDI Research Report Series No. 362

Final Report to the Department for Environment & Heritage Wildlife Conservation Fund

P. J. Rogers1,2 and C. Huveneers1,2

1. SARDI Aquatic Sciences, 2. Flinders University of South Australia

May 2009

Diet and reproductive biology of pelagic sharks 2

Diet and reproductive biology of pelagic sharks in southern Australia: understanding their ecology to enhance policy development and conservation management

P. J. Rogers & C. Huveneers

May 2009

SARDI Publication Number F2009/000162-1 SARDI Research Report Series No. 362

Diet and reproductive biology of pelagic sharks 3

This publication may be cited as: Rogers, P.J & Huveneers, C. (2009). Diet and reproductive biology of pelagic sharks in southern Australia: understanding their ecology to enhance policy development and conservation management. Final Report to Wildlife Conservation Fund. South Australian Research and Development Institute (Aquatic Sciences), Adelaide, 31pp. SARDI Publication Number F2009/000162-1

South Australian Research and Development Institute SARDI Aquatic Sciences 2 Hamra Avenue West Beach SA 5024 Telephone: (08) 8207 5400 Facsimile: (08) 8207 5481 www.sardi.sa.gov.au

DISCLAIMER The authors warrant that they have taken all reasonable care in producing this report. The report has been through the SARDI internal review process, and has been formally approved for release by the Chief of Division. Although all reasonable efforts have been made to ensure quality, SARDI does not warrant that the information in this report is free from errors or omissions. SARDI does not accept any liability for the contents of this report or for any consequences arising from its use or any reliance placed upon it.

Copyright. SARDI Aquatic Sciences This work is copyright. Except as permitted under the Copyright Act 1968 (Commonwealth), no part of this publication may be reproduced by any process, electronic or otherwise, without the specific written permission of the copyright owners. Neither may information be stored electronically in any form whatsoever without such permission.

Printed in Adelaide: May 2009

SARDI Aquatic Sciences Publication Number F2009/000162-1 SARDI Research Report Series No. 360

Authors: P. J. Rogers & C. Huveneers Reviewers: S. Goldsworthy & B. Page Approved by: J. Tanner

Signed: Date: 18 May 2009 Circulation: Public Domain Diet and reproductive biology of pelagic sharks 4

Table of Contents

EXECUTIVE SUMMARY ...... 6 BACKGROUND ...... 7 NEED ...... 8 OBJECTIVES ...... 8 OBJECTIVE 1. COLLECT INFORMATION ON THE DIET, TROPHIC INTERACTIONS AND REPRODUCTIVE BIOLOGY OF PELAGIC SHARKS OFF SOUTHERN AUSTRALIA...... 9 MATERIALS AND METHODS ...... 9 Sampling ...... 9 Laboratory analysis ...... 9 Relative measures of prey quantity...... 11 Comparison of prey contribution ...... 11 Reproductive status...... 11 RESULTS...... 12 Size structure ...... 12 Relative measures of prey quantity...... 15 Comparison of prey contributions ...... 21 Reproductive status...... 23 OBJECTIVE 2: GREATER PUBLIC AND SCIENTIFIC UNDERSTANDING OF THE ECOLOGICAL ROLES AND SIGNIFICANCE OF PELAGIC SHARKS IN SOUTH AUSTRALIAN WATERS...... 28 DEVELOPMENT OF A PROJECT WEBSITE ...... 28 DISCUSSION...... 30 CONCLUSIONS ...... 31 ACKNOWLEDGEMENTS...... 31 REFERENCES...... 32

List of Tables TABLE 1. PREY COMPOSITION OF SHORTFIN MAKOS (ISURUS OXYRINCHUS) ...... 15 TABLE 2. PREY COMPOSITION OF COMMON THRESHERS (ALOPIAS VULPINUS) ...... 18 TABLE 3. PREY COMPOSITION OF BRONZE WHALERS ( BRACHYURUS) ...... 19 TABLE 4. PREY COMPOSITION OF SMOOTH HAMMERHEAD (SPHRYNA ZYGAENA)...... 20

Diet and reproductive biology of pelagic sharks 5

List of Figures FIGURE 1. KEY REGIONS WHERE SAMPLES WERE COLLECTED DURING THIS STUDY...... 10 FIGURE. 2. LENGTH-FREQUENCY DISTRIBUTION OF SHORTFIN MAKOS (ISURUS OXYRINCHUS) SAMPLED DURING THE STUDY (N = 28)...... 12 FIGURE. 3. LENGTH-FREQUENCY DISTRIBUTION OF COMMON THRESHERS (ALOPIAS VULPINUS) SAMPLED DURING THE STUDY (N = 24)...... 13 FIGURE. 4. LENGTH-FREQUENCY DISTRIBUTION OF BRONZE WHALERS (CARCHARHINUS BRACHYURUS) SAMPLED DURING THE STUDY (N = 46)...... 14 FIGURE. 5. LENGTH-FREQUENCY DISTRIBUTION OF SMOOTH HAMMERHEADS (SPHRYNA ZYGAENA) SAMPLED DURING THE STUDY (N = 22)...... 14 FIGURE.6. PREY ITEMS IN STOMACHS OF SHORTFIN MAKOS COLLECTED AT PORT MACDONNELL. TOP IMAGE SHOWS AN ARROW NOTOTODARUS GOULDI (ML= 26 CM, 551 G), WHICH WAS CONSUMED BY A SHORTFIN MAKO (41.92 KG, 162 CM, TL) AND THE BOTTOM IMAGE SHOWS TWO LARGE BARRACOUTA (THYRSITES ATUN) (88 AND 120 CM, TL) CONSUMED BY SHORTFIN MAKOS (64.92 KG, 220 CM, TL)..... 16 FIGURE. 7. SCARRING CAUSED BY SQUID SUCKERS ON SHORTFIN MAKOS TAKEN DURING THE GAMEFISHING COMPETITION AT PORT MACDONNELL ...... 17 FIGURE. 8. TOP PLOT. COMPARISON OF INDEX OF RELATIVE IMPORTANCE (IRI) ESTIMATES FOR PREY TAXA FOR FOUR SHARK . BOTTOM PLOT. TWO-DIMENSIONAL MULTI-DIMENSIONAL SCALING (MDS) PLOT OF PREY BY SHARK SPECIES...... 22 FIGURE.9. IMMATURE REPRODUCTIVE ORGANS OF FEMALE JUVENILE SHORTFIN MAKOS COLLECTED OFF PORT MACDONNELL...... 23 FIGURE. 10 (TOP) CLASPERS OF JUVENILE AND (BOTTOM) MATURING (64.92 KG, 2.2 M, TL) MALE SHORTFIN MAKOS COLLECTED OFF PORT MACDONNELL...... 24 FIGURE. 11. (CLOCKWISE FROM TOP LEFT). IMMATURE TESTES OF A COMMON THRESHER TAKEN IN SA (TOP LEFT AND RIGHT). COMMON THRESHER TAKEN OFF (138 KG, 387 CM, FL) DURING A GAMEFISHING COMPETITION. (BOTTOM RIGHT) SUSPECTED PELAGIC THRESHER...... 25 FIGURE. 12. PREGNANT FEMALE BRONZE WHALER CARCHARHINUS BRACHYURUS (308 KG, 288 CM, TL) COLLECTED FROM A METROPOLITAN BEACH IN ADELAIDE...... 26 FIGURE 13. BRONZE WHALER (CARCHARHINUS BRACHYURUS) (595 MM, TL) SHOWING . 27 FIGURE 14. BRONZE WHALER (CARCHARHINUS BRACHYURUS) (530 –603 MM, TL)...... 27 FIGURE 15. ‘LILLY THE MAKO’ WEB PAGES FROM HENRYTHESEALION.COM...... 29

Diet and reproductive biology of pelagic sharks 6

EXECUTIVE SUMMARY 1. This report provides preliminary data on the biology and ecology of pelagic shark species in Southern Australia, which are required to: (1) assess the conservation and management status; and (2) augment trophodynamic models of the eastern Great Australian Bight (GAB) ecosystem;

2. A total of 122 individual pelagic sharks were examined. These included 25 Common Threshers (Alopias vulpinus), one Pelagic Thresher (Alopias pelagicus) (to be confirmed) 28 Shortfin Makos (Isurus oxyrinchus), 46 Bronze Whalers (Carcharhinus brachyurus), and 22 Smooth Hammerheads (Spyryna zygaena);

3. Shortfin Makos ranged in length between 102 and 302 cm, TL and body weights of 8– 223 kg. Most were <200 cm, TL. Stomachs mostly contained whole , whole/pieces of arrow squid (Nototodarus gouldi) and barracouta (Thyrsites atun);

4. Common Threshers ranged in length between 139 and 252 cm, TL and body weights of between 6.4 and 56.0 kg. Most were <250 cm, TL. Stomachs mostly contained Australian (Engraulis australis), and partially digested fish;

5. Bronze Whalers ranged in length between 85 and 301 cm, TL and body weights of between 4.8 and 307.8 kg. Most were <200 cm, TL. Sardine (Sardinops sagax) was the most commonly consumed prey. Southern calamary (Sepioteuthis australis) were also important dietary components. Bronze Whalers and Common Threshers fed on similar sized clupeids;

6. Most sharks examined were immature or belonged to size ranges below published sizes of maturity for other regions. A pregnant Bronze Whaler weighing 308 kg and was 288 cm, TL contained 20 near-term embryos between 530–603 mm, TL. Embryo weights ranged between 944.55–1308.28 g;

7. Trophic data collected during this study will be integrated into ECOPATH models, and the outputs will be used to inform management processes in Australian State and Commonwealth managed pelagic fisheries;

8. Project web-pages were developed on www.henrythesealion.com as a collaborative initiative between staff from SARDI Aquatic Sciences, Flinders University, and SA Department for Environment and Heritage. The aim of this initiative was to increase public awareness and enhance the profiles of southern Australia’s unique top marine predator populations (including pelagic sharks). Following the inclusion of the pelagic shark information sections, there were > 2,500 new visits to the website;

9. Future research, fisheries management and conservation assessment processes for pelagic sharks in this region need to be coordinated and optimised, through collaboration between researchers, managers and industry stakeholders to improve the current arrangements for these species in Australian State, Commonwealth and adjacent International waters.

Diet and reproductive biology of pelagic sharks 7

BACKGROUND In Australia, the Environmental Protection Biodiversity and Conservation Act (EPBC, 1999) has reporting requirements that require fisheries to undergo assessment processes relating to impacts on ecosystems and Threatened species. Given the declining global trends in pelagic shark populations (Baum et al. 2003; Myers and Worm 2003; Baum and Myers 2005; Myers et al. 2007) and their importance to the structure and functioning of marine ecosystems, key species in Australian State and Commonwealth waters should be considered in this process.

Recently Shortfin Makos (Isurus oxyrinchus) and the Common Threshers (Alopias vulpinus) were Red-listed by the International Union of Conservation and Nature (IUCN) as Vulnerable Threatened, and by the Convention on Migratory Species (CMS) following evidence of widespread population declines (Dulvy et al. 2008). In Australian management jurisdictions these species currently have no protection status. Shortfin Makos and Common Threshers are top order predators in southern Australian waters, yet their interactions with lower trophic levels remain poorly resolved. This is partly because they are highly mobile and difficult to study.

Recreational and game fishers around Australia target Shortfin Makos and Common Threshers, and take them incidentally while targeting other species. Neither species is targeted by commercial fisheries in Australia, yet they are taken as in several fisheries. Despite this, historical fisheries data is limited, and there is minimal information available with which to assess the status of these pelagic shark populations in Australia. This gap reduces the accuracy of Ecosystem Based Fisheries Management (EBFM) approaches for fisheries.

During this study we focussed on the biology and feeding ecology of Shortfin Makos and Common Threshers and collected preliminary data on Smooth Hammerheads (Sphryna zygaena) and Bronze Whalers (Carcharhinus brachyurus). There is no information available in the scientific literature on the biology of Smooth Hammerhead populations in Australian waters. Bronze Whalers support a seasonal commercial fishery in South Australian (SA) State waters, with an annual catch of ~70–130 tonnes per annum (Jones 2008). Awareness of the life history traits of Whaler spp. has led to concern regarding the long-term sustainability of their populations. A recent Commonwealth funded review of whaler shark fisheries identified several aspects that required attention (Jones 2008). Information will be incorporated in trophodynamic models for assessing and managing local fisheries, and Diet and reproductive biology of pelagic sharks 8

outcomes will assist Australian State and Commonwealth Government fisheries management agencies.

NEED This project provides data on the ecology of pelagic shark species in SA, which are required to: (1) assess their conservation and management status; (2) develop trophodynamic models for ecosystems in the eastern Great Australian Bight (GAB) and (3) develop recovery plans in the future.

OBJECTIVES This report is presented in two sections based on the following objectives:

1. Collect information on the diet, trophic interactions and reproductive biology of pelagic sharks off SA.

2. Facilitate greater public and scientific understanding of the ecological roles and significance of pelagic sharks;

Diet and reproductive biology of pelagic sharks 9

OBJECTIVE 1. COLLECT INFORMATION ON THE DIET, TROPHIC INTERACTIONS AND REPRODUCTIVE BIOLOGY OF PELAGIC SHARKS OFF SOUTHERN AUSTRALIA.

In this section, we report on the diet samples and reproductive data. Some biological samples and length data are also summarised.

Materials and Methods

Sampling A total of 122 pelagic sharks were examined from commercial catches in the GAB and Spencer Gulf, and during game fishing competitions at Port MacDonnell in SA and in Sydney, New South Wales between 2007 and 2009. These included 25 Common Threshers (Alopias vulpinus), one Pelagic Thresher (Alopias pelagicus) (to be confirmed) 28 Shortfin Makos (Isurus oxyrinchus), 46 Bronze Whalers (Carcharhinus brachyurus), and 22 Smooth Hammerheads (Spyryna zygaena). Figure 1 shows the regions where sharks were sampled from catches. Sharks were measured by total length (TL) and/or fork length (FL), weighed (kg), sexed and where possible, assessed for sexual maturity. During satellite tagging fieldwork lengths of Shortfin Makos were estimated to accuracies of ~10 cm using the known dimensions of the tagging sling as a guide. When sharks could not be weighed on commercial vessels, weights were estimated using published length–weight relationships for each species. This applied to most of the Common Threshers, Bronze Whalers and some of the Shortfin Makos. Foreguts (anterior of oesophagus to pyloric sphincter) were removed, placed in labelled zip-lock bags, and frozen.

Laboratory analysis Stomachs were thawed and the contents were washed through 0.5 and 1 mm sieves. Identification of prey was based on intact prey and remaining hard items, including beaks, otoliths and exo-skeletal remains. Recognisable soft prey items were identified to the lowest taxonomic level possible. Flesh with knife cuts and hook marks were omitted from samples. Wet mass of each prey item (±0.01 g) was recorded using an electronic balance. The presence of sucker scars on Shortfin Makos attributed to interactions with cephalopods was recorded and photographed. Diet and reproductive biology of pelagic sharks 10

Figure 1. Key regions where samples were collected during this study.

Diet and reproductive biology of pelagic sharks 11

Relative measures of prey quantity The relative contributions of different prey items to each shark species’ diet were estimated using the measures of Preti at al. (2000). These included: Percentage numerical importance (%N) = number of one prey divided by the total number of all prey x 100, the percentage frequency of occurrence (%F) = number of stomachs containing prey of one taxon divided by the total number of stomachs that contained prey x 100, and percentage weight (%W) = weight of one prey divided by the total weight of prey x 100 (Preti et al. 2001). The index of relative importance (IRI) was calculated and expressed as:

%IRI = (%N + %W) x %F

Comparison of prey contribution Multi-dimensional scaling was undertaken using a Bray-Curtis similarity matrix and 4th root transformation of the prey abundance (N) data using the Primer software package (PRIMER version 5.1.2). Analysis of similarities (ANOSIM) matrices were used to investigate pair-by- pair, and within shark species similarities in prey consumed. Differences in the contributions of prey taxa to diet were determined using Similarity Percentages (SIMPER), which indicated the proportion of the difference between the diets explained by each prey taxon.

Reproductive status The reproductive status of sharks was assessed for samples that were collected from commercial catches and during two gamefishing competitions. In cases where full dissections were not possible, or where there were time or logistical limitations (e.g. lack of freezer facilities, time or weather on commercial vessels or time at competition during weigh- ins), only rapid assessment of reproductive status were undertaken. This involved visual assessment of reproductive organs, macroscopic assessment of clasper size, calcification in males and mating scars.

A pregnant Bronze Whaler taken by a recreational fisher in Gulf St Vincent was dissected at SARDI Aquatic Sciences. This included a detailed examination and description of the size, weight and sex ratio of developing embryos, yolk mass-embryo mass ratios (%), compartmentalization and characteristics of the uteri.

Diet and reproductive biology of pelagic sharks 12

Results

Size structure Shortfin Mako (Isurus oxyrinchus) — A total of 28 Shortfin Makos were examined. Shortfin Makos ranged in length between 102 and 302 cm, TL and body weights of between 8 and 223 kg (Fig. 2). Sharks taken at Port MacDonnell (n = 14) in May 2008 ranged in length between 135 and 220 cm, TL and body weights ranged between 24.6 and 65 kg. Nine juveniles between 150 and 200 cm, TL and one neonate (101 cm, TL), were examined and released during satellite tagging trips in the GAB between March and June 2008.

Four Shortfin Makos ranging in length between 267 and 302 cm, TL and body weights of between 143 and 223 kg were examined during a gamefishing competition in Sydney in July 2008. Two sharks were mature males and two were large females. Two other large Shortfin Makos, one female and one male were not available for full dissections.

Of the Shortfin Makos examined, 67% of males and 92% of females were smaller than a published median size at maturity for waters (180.9 TL in males, 280.1 in females) (Francis and Duffy 2005).

Figure. 2. Length-frequency distribution of Shortfin Makos (Isurus oxyrinchus) sampled during the study (n = 28).

Diet and reproductive biology of pelagic sharks 13

Common Thresher (Alopias vulpinus) — 24 Common Threshers were collected from commercial catches, and one mature male (387cm, 138 kg) was collected at a gamefishing competition. Specimens from commercial catches ranged in length between 139 and 252 cm, TL and body weights of between 6 and 56 kg (Fig. 3). Most were <250 cm, TL.

Males ranged in size between 7.77–138 kg and 148–387 cm, TL, and females ranged between 7–31 kg and 139–252 cm, TL. Approximately 75% of males and all females were smaller than the expected size of smallest mature individuals based on estimates for the species in the northern Pacific Ocean (NOAA, http://swfsc.noaa.gov).

Figure. 3. Length-frequency distribution of Common Threshers (Alopias vulpinus) sampled during the study (n = 24).

Bronze Whalers (Carcharhinus brachyurus) — A total of 46 Bronze Whalers were sampled from commercial catches and were caught by gamefishers. Specimens ranged in length between 85 and 301 cm, TL and body weights of between 5 and 308 kg (Fig. 4). Most Bronze Whalers examined were <200 cm, TL.

A total of 21 female and 17 male Bronze Whalers were sexed. All males and 90% of females were considerably smaller than published estimates of the median size of maturity, and size of smallest mature individuals for C. brachyurus in Africa and South America (Walter and Ebert 1991; Lucifora et al. 2005). The mean sizes of females and males were 147 and 128 cm, TL, respectively, and mean estimated weights were 29 and 16 kg, respectively. Further data is required to assess size and age at maturity of this species in Australian waters. Diet and reproductive biology of pelagic sharks 14

Figure. 4. Length-frequency distribution of Bronze Whalers (Carcharhinus brachyurus) sampled during the study (n = 46).

Smooth Hammerhead (Sphryna zygaena) — A total of 22 Smooth Hammerheads were sampled from commercial catches. Specimens ranged in length between 98 and 168 cm, TL and most were between 130 and 160 cm, TL (Fig. 5). No estimate of size at maturity was available for this species.

Figure. 5. Length-frequency distribution of Smooth Hammerheads (Sphryna zygaena) sampled during the study (n = 22).

Diet and reproductive biology of pelagic sharks 15

Relative measures of prey quantity Shortfin Mako (Isurus oxyrinchus) — A total of 16 stomachs of Shortfin Makos were sampled and of these 13 contained prey items. Stomachs of two Shortfin Makos were examined during a gamefishing competition in Sydney. One was completely everted, and the other contained only partially digested bait and berley; both were excluded from subsequent dietary analyses. A total of 12 stomachs from juveniles and one stomach of a sub-adult Shortfin Mako were analysed during a gamefishing competition at Port MacDonnell. All contained prey items including whole cephalopods and whole/pieces of arrow squid (Nototodarus gouldi) and barracouta (Thyrsites atun) (Table 1, Fig. 6). Partially digested fish, and assorted hard-parts including opercular plates, otoliths, cephalopod eye lenses, and squid beaks were also present. Circular scarring on the skin was a prominent feature of juvenile Shortfin Makos (Fig. 7). The most likely cause was the suckers of cephalopods (e.g. Omastrephids). This provides more evidence that cephalopods are key prey of juvenile Shortfin Makos in this region.

Much of the unidentified teleost material in stomachs was heavily digested. Unidentified teleosts formed the most abundant category (%N = 38) and the prey with the highest frequency (Table 1). T. atun accounted for the greatest weight (%W = 92) and second highest frequency. T. atun were present in most stomachs examined and they had the highest relative importance. Parasitic worms (Nematode sp.) were consistently present in stomachs of Shortfin Makos when T. atun flesh, eye lenses and vertebrae were present. In future years, further effort will be made to improve the spatial and temporal coverage of diet sampling and the representation of dietary dynamics across all life history stages.

Table 1. Prey composition of Shortfin Makos (Isurus oxyrinchus) Prey taxa N %N Wt g %Wt F %F IRI Unid. teleosts 32.00 38.55 183.40 1.88 11.00 84.62 3420.96 Thrysites atun 11.00 13.25 9031.56 92.35 10.00 76.92 8123.22 Unidentified baitfish 19.00 22.89 1.00 7.69 flesh 1.00 1.20 13.17 0.13 1.00 7.69 10.30 (Scombridae) Ommastrephid 3.00 3.61 0.00 0.00 6.00 46.15 166.82 Nototodarus gouldi 17.00 20.48 551.70 5.64 7.00 53.85 1406.63 Diet and reproductive biology of pelagic sharks 16

Figure.6. Prey items in stomachs of Shortfin Makos collected at Port MacDonnell. Top image shows an arrow squid Nototodarus gouldi (ML= 26 cm, 551 g), which was consumed by a Shortfin Mako (41.92 kg, 162 cm, TL) and the bottom image shows two large barracouta (Thyrsites atun) (88 and 120 cm, TL) consumed by Shortfin Makos (64.92 kg, 220 cm, TL). Diet and reproductive biology of pelagic sharks 17

Figure. 7. Scarring caused by squid suckers on Shortfin Makos taken during the gamefishing competition at Port MacDonnell.

Diet and reproductive biology of pelagic sharks 18

Common Threshers (Alopias vulpinus) – 24 stomachs of Common Threshers were sampled from commercial catches, and one large male was collected during a fishing competition off Sydney. Of these, 16 (64%) contained prey items, eight were empty and one was excluded because the contents were fishing bait or berley. Stomachs mostly contained Australian anchovy (Engraulis australis), partially digested fish, yellow eyed nannygai (Centroberyx australis) and Australian herring ( georgianus) (Table. 2) Numerically, Australian anchovy formed the most abundant category (%N = 77.16) and they were the prey with the highest frequency and greatest weight, %F and IRI score. ( sagax) was the second highest prey in terms of relative importance (IRI) and %W (Table 2). The stomach of the large male (138 kg, 387 cm TL) collected off Sydney contained one small frigate mackerel (Auxis thazard), but it was possibly bait and was excluded from the analysis.

Table 2. Prey composition of Common Threshers (Alopias vulpinus)

Prey taxa N %N Wt %Wt F %F IRI Unid. teleosts 6.00 2.59 42.20 4.78 5.00 31.25 230.04 Sardinops sagax 37.00 15.95 144.18 16.31 4.00 25.00 806.57 Engraulis australis 179.00 77.16 636.70 72.04 9.00 56.25 8392.48 Centroberyx australis 8.00 3.45 0.08 0.01 1.00 6.25 21.61 Arripis georgianus 2.00 0.86 60.60 6.86 1.00 6.25 48.24

Diet and reproductive biology of pelagic sharks 19

Bronze Whaler Carcharhinus brachyurus — A total of 41 stomachs of Bronze Whalers were examined from samples collected on commercial vessels in the Great Australian Bight, and Spencer Gulf. Of these 33 (80%) contained prey items. Bronze Whalers consumed a broad variety of prey (minimum = 19 groups) (Table 3). Sardine (Sardinops sagax) was the most commonly consumed prey (N= 223, IRI = 7114, 92%) and comprised 83% by number and 74% by weight of prey items. A total of 15 stomachs contained S. sagax. Other important prey of Bronze Whalers included southern calamary (Sepioteuthis australis) (IRI = 346), unidentified teleosts (IRI = 152) and other cephalopods (Table 3). Two sharks consumed other elasmobranchs and skates (Rajidae). Sepia () were also found. One stomach sampled contained the heavily decomposed head of a sergeant baker Latropiscis purpurissatus, which was not weighed. The stomach of the pregnant bronze whaler sampled from the Adelaide metropolitan beach in February contained the heads of large snapper (Pagrus auratus) with knife cuts and was excluded from further analysis.

Table 3. Prey composition of Bronze Whalers (Carcharhinus brachyurus) Prey taxa N %N Wt %Wt F %F IRI Unid. teleosts 10.00 3.70 44.75 1.33 10.00 30.30 152.41 Unid. baitfish 1.00 0.37 Sardinops sagax 223.00 82.59 2494.65 73.91 15 45.45 7113.72 Engraulis australis 2.00 0.74 24.57 0.73 1 3.03 4.45 Scomber australasicus 1.00 0.37 6.00 0.18 1 3.03 1.66 Monocanthidae 1.00 0.37 3.89 0.12 1.00 3.03 1.47 Merlangius sp 1.00 0.37 3.20 0.09 1.00 3.03 1.41 Latropiscis purpurissatus 1.00 0.37 0.00 0.00 0.00 0.00 Labridae 1.00 0.37 24.76 0.73 1.00 3.03 3.35 Pagrus auratus 1.00 0.37 7.70 0.23 1.00 3.03 1.81 Unidentified ceph. 2.00 0.74 11.19 0.33 0.00 0.00 0.00 N. gouldi 1.00 0.37 0.55 0.02 1 3.03 1.17 Teuthidae 5.00 1.85 33.70 1.00 4 12.12 34.55 sp. 2.00 0.74 0.16 0.00 2 6.06 4.52 Sepia sp 2.00 0.74 3.52 0.10 2 6.06 5.12 Sepioteuthis australis 13.00 4.81 479.02 14.19 6 18.18 345.58 Brachyurans 1.00 0.37 3.36 0.10 1.00 3.03 1.42 Elasmobranch (Rajidae) 1.00 0.37 76.27 2.26 1.00 3.03 7.97 Elasmobranchs 1.00 0.37 158.00 4.68 1.00 3.03 15.31 Diet and reproductive biology of pelagic sharks 20

Smooth Hammerhead (Sphryna zygaena) — A total of 21 stomachs of Smooth Hammerheads were examined from samples collected from commercial catches in the Great Australian Bight and southern Spencer Gulf. A total of 19 stomachs contained prey items (90%) (Table 4). Smooth Hammerheads consumed a variety of different teleosts and cephalopods (Minimum = 21 groups). A total of 88 prey items were found and unidentified teleosts were the most heavily consumed (IRI = 14390) (Table 4). Smooth hammerheads preyed on a wide variety of cephalopods, with the most important being the arrow squid (Nototodarus gouldi) and southern calamary (Sepioteuthis australis). Sepia sp. (cuttlefishes) were present.

Table 4. Prey composition of smooth hammerhead shark (Sphryna zygaena)

Prey taxa N %N Wt %Wt F %F IRI Unid. teleosts 31.00 35.23 428.54 15.26 15.00 285.00 14390.06 Thrysites atun 2.00 2.27 528.30 18.82 1.00 19.00 400.71 Unid. baitfish 3.00 3.41 Engraulis australis 6.00 6.82 22.91 0.82 4.00 76.00 580.20 Pempheris multiradiata 1.00 1.14 3.30 0.12 1.00 19.00 23.82 Belone sp. 1.00 1.14 0.90 0.03 1.00 19.00 22.20 Monocanthidae 1.00 1.14 0.00 0.00 0.00 0.00 0.00 Sygnathidae 1.00 1.14 7.66 0.27 1.00 19.00 26.77 Centroberyx australis 1.00 1.14 12.80 0.46 1.00 19.00 30.25 Rexea solandri 1.00 1.14 1.20 0.04 1.00 19.00 22.40 Unidentified cephalopods 1.00 1.14 229.96 8.19 1.00 19.00 177.22 Loliginidae 1.00 1.14 0.40 0.01 1.00 19.00 21.86 Ommastrephid 1.00 1.14 0.10 0.00 1.00 19.00 21.66 Nototodarus gouldi 11.00 12.50 762.25 27.15 3.00 57.00 2260.08 Teuthidae 4.00 4.55 21.59 0.77 1.00 19.00 100.97 Sepia sp. 2.00 2.27 0.20 0.01 1.00 19.00 43.32 Sepia apama 2.00 2.27 0.00 0.00 0.00 0.00 0.00 Sepioteuthis australis 14.00 15.91 652.78 23.25 3.00 57.00 2232.15 Isopoda 2.00 2.27 70.00 2.49 1.00 19.00 90.56 Asteroidea 1.00 1.14 0.00 0.00 1.00 19.00 21.59 Decapoda 1.00 1.14 64.60 2.30 1.00 19.00 65.31

Diet and reproductive biology of pelagic sharks 21

Comparison of prey contributions A total of 34 different prey taxa were identified from the stomachs of the four shark species examined. Comparisons of the IRI of different prey taxa between shark species showed that despite being similar in body size, juvenile Shortfin Makos off Port MacDonnell consumed larger teleosts and cephalopods than Common Threshers collected in the GAB, which ate smaller prey, such as Australian anchovy (Fig. 8). Bronze Whalers and Common Threshers fed on similar sized clupeids, with sardine (S. sagax) being the dominant prey of Bronze Whalers. Southern calamary were also important in the diet of Bronze Whalers. Stomachs of Smooth Hammerheads contained a broad range of bony fishes and cephalopods. We expect that with further sampling over broader spatial and temporal scales, and with larger body sizes, the diversity of prey of each species will increase.

The MDS plot of prey abundance data indicates that Shortfin Makos and Smooth Hammerheads were similar in terms of prey taken (Fig. 8). This was largely explained by the presence of cephalopods and T. atun in the diets. All pair-wise comparisons of shark species indicated significant differences in prey taken, with Bronze Whalers and Common Threshers being the most similar (P<0.03). SIMPER indicated that the consumption of S. sagax explained most of the differences (63%) in Bronze Whaler diets, in common threshers (76%), and unidentified teleosts in Smooth Hammerheads (74%). Unidentified teleosts, T. atun, and Ommastrephid () explained similar degrees (30–36%) of within- species similarity in Shortfin Makos. The same key prey taxa drove the between-shark prey species differences. Analyses of dissimilarity indicated Shortfin Makos and Common Threshers had the highest average dissimilarities (89%) and Shortfin Mako and Smooth Hammerheads had the lowest (64%).

Diet and reproductive biology of pelagic sharks 22

Figure. 8. Top plot. Comparison of Index of Relative Importance (IRI) estimates for prey taxa for four shark species. Bottom plot. Two-dimensional multi-dimensional scaling (MDS) plot of prey by shark species. Diet and reproductive biology of pelagic sharks 23

Reproductive status Shortfin Mako — A total of 28 Shortfin Makos including 13 females and 15 males were sexed. Of the 13 examined during the gamefishing competition at Port MacDonnell, 12 were sexed. Of these 11 were juveniles. Of four small females examined and dissected (22.84– 43.64 kg, 142–165 cm, TL), all had minimal ovarian development (Fig. 9). Seven males were immature and ranged in size between 21.7–40kg and 135–172 cm, TL. Claspers were small, highly flexible and had no calcification (Fig 10). One large male (65kg, 2.2 m, TL) had elongated claspers (clasper length, CL = 8.5 cm) that were partly calcified (Fig. 10).

Four large Shortfin Makos were taken during a gamefishing competition in Sydney. Two were females (162.5 and 177 kg, 283 and 267 cm, TL). One was dissected and had limited reproductive development. Two large mature males weighed 143 and 200.2 kg and were 276 and 302 cm TL, respectively, and had elongated calcified claspers.

Figure.9. Immature reproductive organs of female juvenile Shortfin Makos collected off Port MacDonnell. Diet and reproductive biology of pelagic sharks 24

Figure. 10 (top) Claspers of juvenile and (bottom) maturing (64.92 kg, 2.2 m, TL) male Shortfin Makos collected off Port MacDonnell. Diet and reproductive biology of pelagic sharks 25

Thresher Sharks (Alopias spp.) — Three dissections were undertaken on Thresher Sharks (Alopias spp). These included a juvenile male (199 cm, TL) Common Thresher taken on a commercial vessel, one mature male (138 kg, 387 cm, FL) taken during a gamefishing competition, and what was suspected to be a Pelagic Thresher (to be genetically confirmed) also taken on a commercial vessel (Fig. 11). The juvenile male Common Thresher had undeveloped claspers (CL = 4 cm), with no calcification and poorly developed gonads (Fig. 11). The large male taken off Sydney had elongate, calcified claspers (CL = 33 cm). The female Pelagic Thresher (17 kg, 212 cm, TL) had minimal ovarian development.

Figure. 11. (Clockwise from top left). Immature testes of a Common Thresher taken in SA (top left and right). Common Thresher taken off Sydney (138 kg, 387 cm, FL) during a gamefishing competition. (Bottom right) Pelagic Thresher (to be confirmed).

Diet and reproductive biology of pelagic sharks 26

Bronze Whalers – Pregnant female – characteristics of embryos A pregnant Bronze Whaler taken by a recreational fisher was examined in January 2009. This shark weighed 308 kg and was 288 cm, TL (239 cm, FL) (Fig. 12). The liver weighed 30 kg. The had two compartmentalized uteri that each contained ten near-term embryos and 18 had a placenta attached (Fig. 13). The size range of near-term embryos was 530 – 603 mm, TL, with a mean of 580 mm ±0.22 mm, TL (Fig. 14). There were no significant differences between sizes (t = 0.9, df = 18, p-value = 0.4) or weights (t = -0.6, d.f. = 18, p- value = 0.6) of male and female embryos. Embryo weights (with placenta) ranged between 945–1308g, with a mean 1184± 0.5 g. Claspers of embryos were readily identifiable. Placental weights ranged between 55 and 94 g with a mean of 77±0.2g. There were no significant differences in placental weights between sexes (t = -0.5, d.f. = 14, p-value = 0.6). Placental mass-pup mass ratios ranged between 5 and 8% with a mean of 7±0.1.

Figure. 12. Pregnant female Bronze Whaler Carcharhinus brachyurus (308 kg, 288 cm, TL) collected from a metropolitan beach in Adelaide.

Diet and reproductive biology of pelagic sharks 27

Figure 13. Bronze Whaler (Carcharhinus brachyurus) embryo (595 mm, TL) showing placenta.

Figure 14. Bronze Whaler (Carcharhinus brachyurus) embryos (530–603 mm, TL). Diet and reproductive biology of pelagic sharks 28

OBJECTIVE 2: GREATER PUBLIC AND SCIENTIFIC UNDERSTANDING OF THE ECOLOGICAL ROLES AND SIGNIFICANCE OF PELAGIC SHARKS IN SOUTH AUSTRALIAN WATERS

Development of a project website A website on top marine predators was developed as a collaborative initiative between SARDI Aquatic Sciences, Flinders University, and SA Department for Environment and Heritage. The aim of this project was to increase public awareness and enhance the profiles of southern Australia’s unique top marine predator populations to maintain their long-term survival and recovery. It represented an extension of http://www.henrythesealion.com and now provides ‘easy to read’ background information on pelagic sharks using images and information collected during this study and related investigations of the migration pathways and critical of Shortfin Makos. The website was launched by the Environment and Conservation Minister Jay Weatherill on 16/9/08. It received considerable local media coverage and has helped to educate the general public regarding the ecological roles and significance of pelagic sharks and other top predators in South Australian waters. Information about Shortfin Makos, such as ‘Lilly the Mako’ is provided online and there is public access to maps of satellite tagging tracks. Lilly and five other satellite tagged sharks, including four Shortfin Makos and one , are also shown on http://www.seaturtle.org.

Mr Weatherill said the online system on http://www.henrythesealion.com would allow teachers to access information for geography and biology classes. Since the pelagic shark information webpages went online there have been > 2,500 visits to the website up until 19 February 2009. Local schools have shown interest in including aspects of the webpage in teaching programs. Further educational extension will be undertaken on http://www.henrythesealion.com for a range of marine predators. The author also gave presentations about the importance of pelagic sharks and other top predators in South Australia’s marine ecosystems to members of the general public during the Public Sector Week at SARDI Aquatic Sciences in 2008, and presented findings via a poster at the Oceania Chondrichthyan Society Conference in Sydney in September 2008. Diet and reproductive biology of pelagic sharks 29

Figure 15. ‘Lilly the Mako’ web pages from henrythesealion.com. Diet and reproductive biology of pelagic sharks 30

DISCUSSION The low encounter rates and high mobility’s of pelagic sharks makes them difficult to study. Because of this, we were limited to a preliminary description of the variation in diet and reproductive status of mostly juvenile sharks. A broad array of prey types were identified and we highlighted that more information and resources are required to assess the diet and size/age at maturity of coastal and oceanic pelagic shark species found in southern Australian waters.

Findings during our diet study expanded our understanding of the trophic roles of four pelagic shark species in the Great Australian Bight and off the Bonney Coast in SE SA. Juvenile Shortfin Makos preyed on large teleosts and squids, whereas Common Threshers showed a preference for smaller prey, such as Australian anchovy, despite these shark species being of similar body sizes. Dominant prey items of the Shortfin Makos were barracouta (Thrysites atun) and this species sometimes had anchovies in their stomachs. This suggests that juvenile Shortfin Makos may occupy a trophic level above same-sized Common Threshers. This apparent divergence between the two species was supported by results of the analysis of dissimilarities.

Multivariate analyses of prey abundance suggested that Smooth Hammerheads occupy a similar ecological niche and trophic level to Shortfin Makos. This could be resolved further using stable isotope analyses. This dietary similarity was based on the consumption of cephalopods and T. atun, but Smooth Hammerheads also have a ‘generalist’ predatory strategy suited to mid- to -inner shelf bentho-pelagic-niches where there is a broader variety of prey available. Unidentified teleosts, dominated the diet composition of Smooth Hammerheads, so a large proportion of their diet could not be resolved. Genetic methods of prey identification may need to be employed if this pattern continues. The high frequency of Omastrephids in stomachs of juvenile Shortfin Makos, in conjunction with the prevalence of sucker scars on their lateral dermal surfaces, showed that squid are important dietary components off the South-east of South Australia. Bronze Whalers and Common Threshers occupy similar inshore-mid shelf niches in the GAB and Spencer Gulf and both consumed clupeids, yet they differed in that sardine (S. sagax) and southern calamary (S. australis) were the dominant prey of Bronze Whalers. Both species have been observed to aggregate to feed and this may partially explain their use of small pelagic fishes and squids, which also form predictable seasonal aggregations between spring and autumn.

The majority of pelagic sharks we examined were immature. Our observations regarding the sexual maturity of Shortfin Makos in southern Australia were aligned with published studies Diet and reproductive biology of pelagic sharks 31

(Francis and Duffy 2005; Bishop et al. 2006). Due to the small sample sizes of each species, it is unlikely that our observations reflected all spatial components of these populations and further sampling is required to better understand the complete range of ontogenetic variation in reproductive status. Analysis of the pregnant Bronze Whaler showed that individuals of this species may produce a relatively small number of pups. This warrants consideration, as pup production is likely to be an important factor in mediating population growth in long-lived, late maturing marine species. Similarly, Dusky Whalers (Carcharhinus obscurus) produce small numbers of pups and are considered one of the ‘slowest’ shark species in terms of their relative propensity to recover from exploitation by fisheries (Cortes 2000). These issues warrant consideration for these two species, which are exposed to fishing mortality in this region.

Conclusions In future years, considerable effort will be made to improve the spatial and temporal coverage of biological sampling to enhance our knowledge of the ontogenetic variability in diet and reproductive status of these coastal and oceanic shark species. We aim to achieve this through integration of relevant State and Commonwealth government fishery observer and research programs. The trophic data we collect will also be included in ECOPATH ecosystem models, and outputs will be used to inform management processes in Australian State and Commonwealth managed fisheries. Given the important ecological roles and documented global population declines of some pelagic shark species, research and fishery management processes should be closely coordinated in Australian State and Commonwealth waters to reduce the levels of uncertainty regarding the management and conservation of these species.

ACKNOWLEDGEMENTS This project was only possible due to the contributions and good-will of the commercial, recreational and game fishers in South Australia and New South Wales. In particular we wish to thank Dennis and Kerry Heineke and all member of The Port MacDonnell and Sydney Game Fishing Clubs for their cooperation and assistance, Seaeagle Fisheries, Mark Reynolds, Geoff McDonald, The Fish Factory, Neil Evans, Murray Williams, Glen Wright, Greg Barea, and SARDI staff including Derek Hamer, Alex Ivey, Richard Saunders, Mathew Lloyd, Brenton Ebert, and PIRSA Fisheries for valuable assistance in collecting samples. Laurent Seurant (FUSA and SARDI/MISA) assisted with the dissection of the pregnant Bronze Whaler. Tim Cloak provided information regarding the capture and release of the pregnant Bronze Whaler. This project was funded by a grant application prepared and Diet and reproductive biology of pelagic sharks 32

submitted by S. D. Goldsworthy, B. Page, P. J. Rogers, C. Huveneers, and S. M. Jones to Wildlife Conservation Fund (SA Department for Environment and Heritage) provided funds, and SARDI Aquatic Sciences and Flinders University provided logistical support.

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