African Journal of Marine Science Seasonal variability ...

This article was downloaded by: [Antonin Blaison] On: 26 July 2015, At: 01:53 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: 5 Howick Place, London, SW1P 1WG

African Journal of Marine Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tams20

Seasonal variability of bull and tiger shark presence on the west coast of Reunion Island, western Indian Ocean ab

b

c

d

e

fg

a

A Blaison , S Jaquemet , D Guyomard , G Vangrevelynghe , T Gazzo , G Cliff , P Cotel & M a

Soria a

IRD La Réunion, UMR MARBEC (IRD/IFREMER/UM/CNRS), Parc Technologique Universitaire, Sainte-Clotilde, Ile de La Réunion, France b

Université de La Réunion, Saint-Denis, Ile de La Réunion, France

c

Comité Régional des Pêches Maritimes et des Elevages Marins de La Réunion (CRPMEM), Le Port Cedex, Ile de La Réunion, France

Click for updates

d

Squal'Idées, Stella, Ile de La Réunion, France

e

WEST, Saint Gilles, Ile de La Réunion, France

f

KwaZulu-Natal Sharks Board, Umhlanga, South Africa

g

Biomedical Resource Unit, University of KwaZulu-Natal, Durban, South Africa Published online: 24 Jul 2015.

To cite this article: A Blaison, S Jaquemet, D Guyomard, G Vangrevelynghe, T Gazzo, G Cliff, P Cotel & M Soria (2015) Seasonal variability of bull and tiger shark presence on the west coast of Reunion Island, western Indian Ocean, African Journal of Marine Science, 37:2, 199-208, DOI: 10.2989/1814232X.2015.1050453 To link to this article: http://dx.doi.org/10.2989/1814232X.2015.1050453

PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/termsand-conditions

African Journal of Marine Science 2015, 37(2): 199–208 Printed in South Africa — All rights reserved

Copyright © NISC (Pty) Ltd

AFRICAN JOURNAL OF MARINE SCIENCE

ISSN 1814-232X EISSN 1814-2338 http://dx.doi.org/10.2989/1814232X.2015.1050453

Seasonal variability of bull and tiger shark presence on the west coast of Reunion Island, western Indian Ocean§

Downloaded by [Antonin Blaison] at 01:53 26 July 2015

A Blaison1,2*, S Jaquemet2, D Guyomard3, G Vangrevelynghe4, T Gazzo5, G Cliff6,7, P Cotel1 and M Soria1 1 IRD La Réunion, UMR MARBEC (IRD/IFREMER/UM/CNRS), Parc Technologique Universitaire, Sainte-Clotilde, Ile de La Réunion, France 2 Université de La Réunion, Saint-Denis, Ile de La Réunion, France 3 Comité Régional des Pêches Maritimes et des Elevages Marins de La Réunion (CRPMEM), Le Port Cedex, Ile de La Réunion, France 4 Squal’Idées, Stella, Ile de La Réunion, France 5 WEST, Saint Gilles, Ile de La Réunion, France 6 KwaZulu-Natal Sharks Board, Umhlanga, South Africa 7 Biomedical Resource Unit, University of KwaZulu-Natal, Durban, South Africa * Corresponding author, e-mail: [email protected]

A fisheries-independent survey using longlines and drumlines, and an acoustic telemetry study, revealed that bull sharks Carcharhinus leucas and tiger sharks Galeocerdo cuvier occur throughout the year off the west coast of Reunion Island. The research, which commenced in 2011, was conducted in response to an increase in the rate of shark attacks. Juvenile, subadult and young adult tiger sharks of 111–390 cm total length (TL) were caught in all months except July; the sex ratio was 1:1 (M:F; n = 61). All bull sharks taken, except one (183 cm TL), were mature (205–329 cm TL), with a sex ratio of 0.7:1 (M:F; n = 54), and catches occurred throughout the year except in May and August, with the highest CPUE in September. Presence/absence of a total of 46 tagged tiger sharks and 36 tagged bull sharks was monitored by means of 42 acoustic receivers distributed along the west coast of the island. Tagged tiger sharks were detected in all months, with seasonal variation between sexes. Detections of males remained low throughout the year but with a peak in winter, whereas detections of females were low in May and August only and peaked in summer. Tagged bull sharks of both sexes were more abundant in winter than in summer, with females present year round. The reasons for the apparent differences in seasonality found in longline and drumline catches compared to acoustic monitoring are discussed. Keywords: acoustic telemetry, CPUE, shark attack, total length

Introduction There is a long history of shark attack on surfers, bodyboarders and spearfishermen in tropical coastal waters (Vangrevelynghe 1994; Landron 2006; Hazin et al. 2008; Lagabrielle et al. 2012). Coastal communities often demand intervention to reduce the risk of further attacks, especially if an unusually high number of incidents have occurred in a short space of time (Curtis et al. 2012). A wide range of mitigation measures to decrease the risks of shark attack have been implemented, including short-term targeted shark fishing, long-term deployment of shark-fishing devices such as gillnets or drumlines, use of shark repellents and, more recently, scientific studies to understand better the biology, ecology and behaviour of sharks (Cliff and Dudley 1992; Wetherbee et al. 1994; Nel and Peschak 2006; Beschta and Ripple 2009; Cliff and Dudley 2011; O’Connell et al. 2011, 2014; Hazin and Afonso 2014). In general, knowledge of apex shark predators remains scarce compared to their terrestrial counterparts (Beschta and Ripple 2009). A better understanding of the ecological role of sharks in marine §

ecosystems is essential to find a balance between mitigation measures and healthy marine ecosystems (Stevens et al. 2000; Ferretti et al. 2010; Lucifora et al. 2011). At Reunion Island there was an average of 1.23 attacks per year between 1980 and 2011 (Squal’Idées unpublished data). This figure rose to 5.0 per year between 2011 and 2013, during which time 15 attacks occurred. Consequently, Reunion Island now has one of the highest rates of shark attack in the world (Burgess 2014). Two species were involved in these attacks, the tiger shark Galeocerdo cuvier (Péron & Lesueur, 1822) and the bull shark Carcharhinus leucas (Müller & Henle, 1839) (Vangrevelynghe 1999; Werbrouck et al. 2014). Local authorities decided to implement a suite of actions focused on these two species. These actions included research on shark behaviour and shark–human interactions in the coastal zone, education of residents and tourists about the risk of shark attack, and a targeted shark-fishing programme in collaboration with local fishermen. The ongoing research programmes, which

This article is based on a paper presented at the ‘Sharks International 2014’ conference, held 2–6 June 2014, Durban, South Africa, and is part of a special issue ‘Advances in Shark Research’ edited by DA Ebert, C Huveneers and SFJ Dudley African Journal of Marine Science is co-published by NISC (Pty) Ltd and Taylor & Francis

Blaison, Jaquemet, Guyomard, Vangrevelynghe, Gazzo, Cliff, Cotel and Soria

commenced in 2011, include shark-tagging operations to study shark movements and activity patterns along the coast. Shark-fishing operations were implemented to improve knowledge of various aspects of shark biology and ecology. Prior to these interventions, both species had been recorded at Reunion Island and included in biodiversity lists (Letourneur 1998; Letourneur et al. 2004), but no local scientific studies were conducted to investigate their ecology and behaviour. As a consequence, no data were available on abundance, habitat use, or patterns of occurrence, to assist authorities to manage appropriately the human safety risk in coastal waters. Using data collected during the fishing and tagging programmes, the aims of this study were to characterise for the first time the populations of tiger and bull sharks at Reunion Island, based on their size and sex, and to gain a preliminary insight into their temporal distribution along the west coast of the island.

offshore (Figure 1). There are two distinct seasons: the austral summer with warm air temperatures and heavy rains (November–April), and the austral winter with cooler temperatures and infrequent rain (May–October). Sea surface temperatures average 28 °C in summer and 23 °C in winter (Conand et al. 2007). Fringing coral reefs occur along 12% of the coast (Montaggioni and Faure 1980). The marine fauna is diverse with a fish community composed mainly of coral reef-, shallow water-, deep water-, and oceanic species (Letourneur 1998). Although more than 50 species of sharks have been recorded in the vicinity of the island (Letourneur et al. 2004), no information is available on their spatial and temporal distribution and abundance. Large predatory species, such as the white shark Carcharodon carcharias, oceanic whitetip shark Carcharhinus longimanus, shortfin mako shark Isurus oxyrinchus, tiger shark, and bull shark, have been recorded at Reunion Island (Fricke et al. 2009).

Material and methods

Data collection Data were obtained from four different bull and tiger shark research programmes carried out on the west coast of the island between October 2011 and April 2014; some of these programmes were ongoing at the time of writing (see http:// www.info-requin.re/ for a summary of the programmes). The CHARC programme (Connaissances de l’écologie et de l’HAbitat de deux espèces de Requins Côtiers sur la côte

Study area Reunion Island is a young oceanic island (21°07′ S, 55°32′ E) that lies in the Madagascar hotspot of biodiversity (Myers et al. 2000). The geomorphology of the island is characterised by an absence of an island shelf, except on the leeward west coast where it extends up to 5 km

AFRICA

Sainte Marie Le Porte

Saint Paul

INDIAN OCEAN 21° S

Leeward coast


200

REUNION

Saint Gilles Trois Bassins

REUNION Sainte Rose

Saint Leu

Etang Salé

55°30’ E

LEGEND

Saint Louis Saint Pierre

VR2W receiver Marine protected area Isobath (Hydrorun) [Isobath interval: 5 m (0–50 m); 10 m (50–200 m); 50 m (200–1 000 m); 100 m (1 000–2 800 m)]

Figure 1: Network of VR2W receivers deployed along the west coast of Reunion Island from 2011 to 2014

African Journal of Marine Science 2015, 37(2): 199–208


ouest de La Réunion; January 2012–April 2015) focused on the ecology, habitat use and behaviour of the two species using acoustic telemetry; the CAPREQUIN programme (CAPturabilité des REQUINS côtiers; January 2014–March 2015) investigated the effect of drumlines as a potential fishing method to reduce the risk of shark attacks; the CIGUATERA programme (September 2013–August 2014) assessed the concentrations of biotoxins in shark tissues; and the WEST programme (initiated in May 2013) aimed to reduce the risk of shark attack through the capture and removal of some individuals. The last three programmes used the animals killed by fishing to provide morphological and biological information and samples for various ongoing analyses. These analyses were for substances such as biotoxins, including ciguatera, and trace elements, with a view to a possible resumption of marketing of shark meat for human and animal consumption. Fishing methods Sharks were captured with both surface- and bottomset longlines, as well as drumlines, deployed along the west coast of Reunion Island between Le Port and St Pierre (Figure 1). This is the leeward coast where most of nautical activities, including bathing and surfing, occur, and where most shark attacks have occurred since 2011. Each longline consisted of a mainline of 2–3 km to which were attached 50 to 100 16/0 circle hooks, set approximately 10 m apart. Squid Loligo spp. and mackerel species Scomber spp. were used as bait. The duration of each longline set was short – averaging two hours – in order to minimise the mortality both of sharks and of bycatch. The bottom longline was retrieved with a hydraulic line-hauler. Drumline-setting techniques followed those of South Africa’s KwaZulu-Natal Sharks Board (Dudley et al. 1998), but using a 16/0 or 20/0 circle hook and the tuna species Katsuwonus pelamis and Thunnus albacares, as well as milkfish Chanos chanos, as bait. Although the drumlines were on the water continuously, they were baited on certain days only. During their deployment, each drumline was fitted with a ‘real-time’ satellite alert system, called the ‘Catch-A-LiveTM’ system (Perry et al. 2014) to facilitate successful release of bycatch. All sharks caught were sexed and total length (TL) measured. During the CHARC programme, all sharks were tagged and released. During the CIGUATERA programme, all sharks were euthanised and dissected. During the CAPREQUIN and WEST programmes, 50% of sharks caught were tagged and released and the other 50% were retained and dissected; this was based on body length, with all individuals larger than 250 cm for tiger sharks and 150 cm for bull sharks retained. Hooks were removed from the sharks before release. Tagging methods and acoustic telemetry When a shark was caught on a longline or a drumline, the dropper line was unclipped from the main line and attached to a separate buoy to facilitate handling by the tagging team. The shark was then brought alongside the tagging boat and a rope noose attached to the caudal peduncle. The shark was rolled onto its back and maintained in this position to induce tonic immobility, then sexed and

201

measured. An external ‘roto’ tag (conventional identification tag) was attached to the first dorsal fin and an acoustic tag was inserted surgically into the abdominal cavity. In the WEST programme, a speargun was used to anchor the acoustic tag into the dorsal musculature below the first dorsal fin. This method was used to tag sharks when the scientific team was not present to perform the necessary surgery. Two VEMCO acoustic tags were used, either a V16TP-4H (pulse interval of 40–80 s, power output of 150–162 dB and battery life of 845 days) or a V16-5H (pulse interval of 40–80 s, power output of 150–162 dB and battery life of 482 days). These acoustic tags were complemented by a network of 38 VR2W receivers deployed in nearshore waters along the west coast of the island in water depths of between 10 m and 60 m. Another four receivers were attached to FADs further offshore (Figure 1). Of the 38 nearshore receivers, 21 were deployed 500 m offshore on moorings in a mean bottom depth of 19 m (SD 5) and 17 were deployed 1 500 m offshore on delimitation buoys of the marine protected area (MPA) in a mean bottom depth of 44 m (SD 18). Receivers on moorings were attached 1 m from the bottom and receivers on MPA buoys were attached at a depth of 20 m. Data were retrieved from the receivers every four months. Sixteen range tests with a V16-4H tag were carried out in September 2012 and November and December 2013 at 11 different sites within the network of receivers. On average, the maximum detection distances with more than 90% efficiency were 50–150 m for receivers on moorings and 200–300 m for receivers on MPA buoys. The distances from the coast or from the nearest coral reef were different from one site to another and sea conditions varied from one day to another. These environmental factors can significantly reduce detection efficiencies (Mathies et al. 2014), but no specific study was carried out on the effect of such factors on VR2W range detection along the west coast of Reunion Island. Data analysis Size distribution and sex ratios Size distribution was compared between sexes for both species using the non-parametric Mann–Whitney test and sex ratios were compared using the Chi-square (χ2) test. Estimates of shark presence Monthly variations in shark presence were assessed using both catch per unit effort (CPUE) and the percentage of tagged sharks detected along the coast by acoustic receivers. Fishing effort was calculated by multiplying the number of hooks by the fishing duration in hours. This method was applied to combine information from the two fishing methods that used a different number of hooks and fishing times. Mean monthly CPUE was calculated from October 2011 to April 2014. All receivers were used to determine the daily number of detections of tagged sharks. If a tag code was detected only once per hour, or less, within a 24-hour period, it was excluded to eliminate possible false detections. The percentage of the total number of tagged sharks that was detected daily was calculated for each species and sex and averaged for each month.

202


For each species and sex, monthly variations in mean CPUE and in mean percentages of sharks detected were investigated using the Kruskal–Wallis non-parametric analysis of variance. Non-parametric multiple comparison tests (post hoc Duncan tests) were carried out when significant differences were found. All data were analysed with Statistica 6.1 software (StatSoft, Inc.).

per fishing event per month (n = 186 fishing events, H = 15.9, p = 0.143; Figure 3). The mean CPUE per fishing event per month was 0.0062 sharks hook–1 h–1 (SD 0.0277), ranging from zero in July to a peak in December, which was due mostly to a single day in December 2012 when the catch rate peaked at 0.3040 sharks hook–1 h–1. There were significant differences in monthly catch rates of bull sharks (n = 186 fishing events, H = 27.8, p = 0.030; Figure 4). Catch rates were significantly higher in September (MC Inter = 0.00, dl = 174). CPUE in all other months was lower and the months did not differ significantly. No bull sharks were caught in May and August.

Results


In 186 fishing events (deployments of baited gear), 180 sharks were captured between October 2011 and April 2014 (Table 1). Of these, 82 sharks were tagged with both conventional and acoustic tags (74 internal and 8 external) and 34 were retained and dissected (Table 2). A total of 20 sharks were tagged with conventional tags only (not detailed in Table 2) and 44 were released without tagging. Size distributions and sex ratios Tiger sharks ranged in size between 111 and 390 cm TL (n = 61, Figure 2). There was no significant difference in the size of males and females (n = 61, U = 443.5, p = 0.610). The sex ratio did not differ significantly from 1:1 (nmale = 31, nfemale = 30, χ2 = 0.66, p = 3.390; Table 2). Bull sharks ranged between 183 and 329 cm TL (Figure 2). Females were significantly larger than males (n = 54, U = 199.5, p = 0.003). The sex ratio was 0.7:1 M:F (nmale = 21, nfemale = 33, χ2 = 2.67, p = 0.050; Table 2). Monthly variation in shark presence based on CPUE There was no significant difference in CPUE of tiger sharks Table 1: Catches of tiger sharks Galeocerdo cuvier and bull sharks Carcharhinus leucas in four research programmes from October 2011 to April 2014

Programme CHARC Caprequin Ciguatera West Total

Catch (number) Tiger sharks Bull sharks 76 32 18 3 25 9 7 10 126 54

Monthly variation in shark presence using acoustic telemetry For the acoustic analysis, data from September 2012 to August 2013 only were used, as this was the period when all 42 receivers were deployed and the highest number of tagged sharks was present (n = 73). During this period there were 4 087 detections of tiger sharks, 65% of which were from 14 of the 19 tagged females and 35% from 13 of the 20 males. Five females and seven males were never detected after tagging. Females were more abundant than males throughout the year (nfemale = 365, nmale = 365, U = 45 084, p < 0.0001), except for the months of May and August during which there was no significant difference between the sexes. The percentage of tagged females detected was significantly different between months (nfemale = 365 observations, H = 81.7, p < 0.0001; Figure 5). The percentages were signifi cantly higher from January to March and lower in April, May, August, November and December (MC Inter = 22.22, dl = 353). The percentage of tagged males was also signifi cantly different between months (n = 365 observations, H = 139.3, p < 0.0001; Figure 5). No males were detected in September, October and December, whereas the percentage of tagged males was significantly highest from May to July (MC Inter = 4.39, dl = 353). During the study period, there were 102 361 detections of bull sharks, 69% of which were from 19 of 22 tagged females and 21% from 8 of the 12 tagged males. Three females and four males were never detected after tagging. Females were more abundant than males (nfemale = 365, nmale = 365, U = 30 111, p < 0.0001), except in August

Table 2: Summary of tiger sharks Galeocerdo cuvier and bull sharks Carcharhinus leucas examined in tagging and reproduction programmes from October 2011 to April 2014

Parameter Number of females Mean size (cm TL) Size range (cm TL) Number of males Mean size (cm TL) Size range (cm TL) Total number Sex ratio M:F

Measured and sexed 30 298 111–390 31 303 111–385 61 1:1

Tiger sharks Tagged (conventional and acoustic) 22 284 111–387 24 295 111–366 46 1.1:1

Dissected

Measured and sexed

8 337 285–390 8 329 289–385 16 1:1

33 288 183–329 21 265 214–305 54 0.7:1

Bull sharks Tagged (conventional and acoustic) 24 289 183–329 12 274 240–305 36 0.5:1

Dissected 9 282 205–325 9 253 214–300 18 1:1

203


Tiger sharks The tiger sharks observed on the west coast of Reunion Island comprised mainly young adults and some subadults of both sexes, based on size-at-first maturity of 310 cm TL for males and 320 cm TL for females (Kohler et al. 1995, 1996; Heithaus 2001). These sharks were slightly smaller than those sampled in Western Australia (Heithaus 2001); Gulf of Mexico, USA (Branstetter et al. 1987); and Hawaii (Whitney and Crow 2006). Fishing methods and hook size could explain this difference; at Reunion Island, hooks were smaller than those used in Australia or Hawaii. The number of opened hooks found during our fishing programmes (about 15 hooks, over the four fishing programmes; AB and

Mean Mean +/− SD Min–max

0.30 0.25

18

14

0.20 0.15

28

33

22

0.10 0.05

19

18

0.00

11

11

15

7

3

1

2

3

4

5

6 7 8 MONTH

9

10 11 12

Figure 3: Box plot of tiger shark catch rate per fishing event per month at Reunion Island from 2011 to 2014. Data labels indicate the number of fishing events for tiger sharks in each month

Bull sharks

Female

Female

16

17

14

14 12

10

10 8

7

6 4

5

4

3

2

2

18

5

−0.05

Tiger sharks

FREQUENCY


Discussion

co-authors unpublished data) suggests that the equipment used was not suitable for catching very large tiger sharks. Although it was impossible to determine the shark species responsible for opening the hooks, we suspect that some may have been tiger sharks larger than those caught in this study.

CPUE (sharks hook–1 h –1)

when the difference was not significant. The percentages of tagged females were significantly different between months (n = 365 observations, H = 174.8, p < 0.0001; Figure 6), being significantly higher from March to September and with a peak in September, and significantly lower from October to February (MC Inter = 92.00, dl = 353). The percentages of tagged males were significantly different between months (n = 365 observations, H = 226.6, p < 0.0001; Figure 6), being significantly higher from May to August and lower from September to January (MC Inter = 77.78, dl = 353).

0

0

Male

1

0

Male

16

14

14

12

12 10 8

7

7

6

5

4 2

2

1

100

2

2 0

150

200

250

300

350 400 100 150 TOTAL LENGTH (cm)

0

0

200

250

300

350

400

Figure 2: Size distribution of tiger and bull sharks caught during the four programmes. Data labels represent sample size and dotted lines represent the size at first maturity for bull sharks (Cruz-Martinez et al. 2004) and tiger sharks (Kohler et al. 1996; Heithaus 2001)

CPUE (sharks hook–1 h –1)

204


0.12 0.10 0.08 0.06

14

0.04 0.02

*

33 18

0.00 1

2

3

3 19

11

4

5

11

5

15

7

6 7 8 MONTH

9

22

10 11 12

Figure 4: Box plot of bull shark catch rate per fishing event per month at Reunion Island from 2011 to 2014. Data labels indicate the number of fishing events in each month. Asterisk indicates the month that differed significantly from the others

SHARK PRESENCE (% detected)

22 20 18 16 14 12 10 8 6 4 2 0 −2

* Female 28 *

30

*

31

30


30

31 31

31

This hypothesis is supported by fishers who report catches of tiger sharks larger than 400 cm TL (Fisheries Committee of Reunion pers. comm.). The tiger shark sex ratio of 1:1 found at Reunion Island is similar to that from studies elsewhere in the world (Heithaus 2001; Whitney and Crow 2006). Tiger shark catch rate did not show a clear seasonal pattern, although it tended to be higher in summer months. Conversely, acoustic data revealed seasonal variations for both sexes, with highest percentages of female detections from January to March and of males from May to June. There was a higher abundance of females than males in most months of the year. These results indicate that male and female tiger sharks are present off Reunion Island throughout the year, with some sexual segregation. Females tend to come closer inshore during summer, and males during winter. Although other studies did not explicitly mention sexual segregation, they highlighted differential behaviour within a single population. Off Hawaii, some tagged tiger sharks confined their movements to inshore waters, while others were either

Male

31

31

28

30

*

31

30

31 31

1

2

3

4

5

6

7

8

9

10

11 12

MONTH

1

30

2

3

4

*

31 31

*

31

5

31

6

7

8

30

30

31

9

10 11

12

Figure 5: Box plot of daily percentage of tagged female and male tiger sharks detected around Reunion Island over a 12-month period. Numbers indicate the number of detection days in each month. Asterisks indicate months that were significantly different from the others

Female 60 * 31

50 40

* 30

*

31

*

30

Mean Mean +/− SD

Min–max

*

31

*

28

*

31

31

31

28

30

Male

*

30

70

SHARK PRESENCE



28

31

31 31

30

*

30

*

31

30

*

31 30

31

20 10 0 1

2

3

4

5

6

7

8

9

10

11

12

MONTH

1

2

3

4

5

6

7

8

30

31

9

10

31

11 12

Figure 6: Box plot of daily percentage of tagged female and male bull sharks detected around Reunion Island over a 12-month period. Numbers indicate the number of detection days in each month. Asterisks indicate months that were significantly different from the others



primarily offshore or used both coastal and pelagic environments (Holland et al. 1999, 2001; Lowe et al. 2006). The influence of environmental factors on seasonality in inshore waters remains unknown and will need further investigation. A peak in female abundance during summer and male abundance during winter may be temperature-dependent, because a clear, seasonal temperature signal occurs inshore at Reunion Island (Conand et al. 2007). This result is similar to that for Western Australia, where temperature rather than prey availability was proposed as the main factor explaining the strong seasonality in tiger shark abundance (Heithaus 2001; Wirsing et al. 2006). Off Hawaii, seasonal variation in tiger shark abundance is less marked and has been attributed to prey behaviour and availability (Tricas et al. 1981; Lowe et al. 2006; Meyer et al 2010). Based on the first record of a single pregnant female from Reunion Island and on other literature from the western Indian Ocean, Jaquemet et al. (2013) suggested that the tiger shark mating period might occur in late winter and pupping the following summer. Therefore, the seasonal patterns found in the current study might be related to reproduction, with the presence of females inshore in summer being associated with the pupping period. It is uncertain why males are present inshore in winter, however. As the majority of tagged adult tiger sharks were considered to be young (i.e. close to the size at first maturity), the confirmation of any link between the seasonality of tiger shark presence in inshore waters and reproductive behaviour is subject to the collection of additional information, particularly with regard to older adults. Bull sharks The predominance of large bull sharks in this study indicates that the west coast of Reunion Island is a habitat used by adults of both sexes, based on size-at-first maturity of 190 cm for males and 200 cm for females (Cruz-Martinez et al. 2004). Sex-biased differences in size distribution in this study confirmed previous observations that female bull sharks tend to be larger than males (Neer et al. 2005; Carlson et al. 2010). The mean size of bull sharks caught was higher than found elsewhere. In Florida, the mean size for males and females was 125–180 cm, with a maximum size of 249 cm (Snelson et al. 1984). In the northern Gulf of Mexico, the largest bull shark caught was 268 cm (Branstetter and Stiles 1987; Cruz-Martinez et al. 2004; Carlson et al. 2010). On the east coast of South Africa, the largest bull shark caught by protective shark nets was 263 cm (Cliff and Dudley 1991), although a more recent study in the Breede River on the south coast of South Africa reported a bull shark of 400 cm (McCord and Lamberth 2009). A study off southern Mozambique recorded sizes of ~250 cm (Daly et al. 2014). The only known population with individuals larger than 250 cm was discovered in 2012 in Costa Rica (Arauz et al., Programa Restauración de Tortugas Marinas [PRETOMA], unpublished data). The reasons for these regional size differences remain unclear. Generally, it is assumed that populations with bigger individuals are often more pristine (i.e. unexploited by fisheries) than populations under fishing pressure (Shin and Cury 2004). However, in the North-West Atlantic Ocean, a study of size variation in bull sharks did not show significant changes over a 15-year fishing period (Carlson et al. 2012).

205

Evidence of reproductive activity in Reunion waters was provided by the capture of an adult male with fresh mating scars on the claspers (July 2013) and three pregnant females with early stage embryos (June 2013 and April 2014; AB and co-authors unpublished data) and one with larger embryos (August 2012; J-F Nativel, Ocean Prévention Réunion, pers. comm.). No juveniles were captured in the present study, raising the question of the location of younger individuals. Given that the fishing effort was confined to the west coast, it is possible that juveniles inhabit other coastal areas of the island. Reunion fishers report catches of juvenile bull sharks in nearshore waters in areas close to river mouths and in harbours (D Guyomard, Fisheries Committee of Reunion, pers. comm.). These coastal fishers use beach-seines, longlines, ‘surf-casting’ handlines, or drumlines with smaller hooks. These shorebased catches suggest that juvenile bull sharks inhabit extremely shallow water, presumably to avoid predation by their adult conspecifics. Other studies have shown habitat partitioning based on state of maturity (Simpfendorfer et al. 2005; Curtis 2008), with juvenile bull sharks inhabiting what are commonly referred to as ‘nursery areas’ in coastal shallow waters, including estuaries. Off Reunion, the location of any bull shark nursery area remains unknown but an inshore location seems the most plausible. Catch rate showed no clear seasonality, with higher values in September but no catches in May and August. Analysis of acoustic data demonstrates bull shark presence throughout the year but with strong seasonal patterns in both female and male abundance. Females were present throughout the year and with a peak from March to September (autumn and winter). Males were also more abundant in winter but were absent in September and October. A seasonal pattern has also been observed off Fiji, where bull shark abundance was lower from October to December and higher from January to March (Brunnschweiler and Baensch 2011) and off Florida, where bull shark catch rates were higher in summer and lower in winter (Snelson et al. 1984). Off southern Mozambique, where bull sharks moved towards lower latitudes in winter and returned to the study site in summer, Daly et al. (2014) concluded that the seasonal variations observed were driven primarily by seasonal changes at the study site, but they did not distinguish between the influence of spatiotemporal fluctuations in food resources and the effects of reproductive activity. At Reunion, our observations represent the first evidence of bull shark reproduction, but further investigation is required to confirm the seasonality of these activities. Comparison of the two methods to determine seasonality In this study, differences were observed in the results obtained from the two research methods (CPUE and acoustic telemetry) for both species. For tiger sharks, no seasonal variation was found using CPUE but was observed using acoustic data. For bull sharks, seasonal variation was observed using both methods, although was more pronounced using acoustic data. Tiger sharks were easier to catch than bull sharks, possibly because we had a better understanding of where to fish or because they might have taken the baits more readily, resulting in higher CPUE for


206


this species. Despite this, bull sharks were clearly the more common of the two species inshore, which was evident in the greater number of acoustic detections. In Hawaii, Meyer et al. (2009), using acoustic telemetry, reported arrhythmic tiger shark movement patterns, whereas strong seasonal variation in tiger shark abundance was found in Western Australia using catch rate data (Heithaus 2001; Wirsing et al. 2006). The differences found in seasonal pattern during these two studies might be due to site-specific differences or to the methods used. We propose several factors that might explain the difference observed between the two methods in Reunion. First, fishing efforts were irregular from month to month, mainly due to weather conditions, especially during austral winter swells, but also due to the number of individuals needed for the different projects. Secondly, in some months a large number of tiger sharks was caught and tagged in a short space of time and so, for the rest of the month, no further targeting of this species was undertaken and efforts focused exclusively on bull sharks, which brought about changes in the fishing methods. Tiger sharks were more easily caught on offshore longlines and bull sharks were more easily caught on inshore drumlines and bottom longlines (AB and co-authors unpublished data). Thirdly, different hook sizes and types of baits were used throughout the different fishing programmes. It has been shown that hook size and bait type have a significant influence on tiger shark catch rate (Heithaus 2001), and hypothetically could have affected bull shark catch rate as well. These sampling biases may collectively have masked any seasonal pattern of occurrence of both shark species that may exist at Reunion Island. By contrast, acoustic telemetry data obtained from receivers deployed mostly close to the shore indicated seasonal variations in shark presence. Given the predominantly inshore distribution of the receivers, however, we may have underestimated tiger shark presence at Reunion Island because this species is known to move widely (Holland et al. 1999, 2001; Meyer et al. 2009) and our best fishing areas were generally more than 2 km offshore of most of the receivers. In addition to the factors mentioned above, differences in bull shark seasonal patterns, as revealed by catch rate and by acoustic telemetry, might be explained by the effectiveness of our fishing techniques potentially being influenced by (i) environmental factors, (ii) feeding behaviour, or (iii) the life cycle of bull sharks. At Reunion, the highest monthly catch rate in the current study occurred in September, when sea temperature is lowest (Conand et al. 2007). Simpfendorfer et al. (2005) found a different pattern, with a significant positive effect of sea temperature on bull shark CPUE. However, that study was of immature bull sharks only, and it is possible that temperature effects might differ according to life-history stage. The second potential factor is the difficulty of catching bull sharks. Observations in the current study revealed that bull sharks are more selective feeders than previously described (Sadowsky 1971; Tuma 1976; Snelson et al. 1984; Heithaus et al. 2002, 2009) and that bait quality might have a strong influence on their catchability (AB and co-authors pers. obs.). The third potential factor could be the influence of a particular reproductive stage in adult bull sharks, during which there

may be a reduced tendency to feed, thereby decreasing their catchability. Little is known about feeding behaviour during different reproductive stages, such as mating, gestation, or pupping. To obtain further information, a study has commenced on tiger and bull shark reproduction using data collected from animals dissected both in this study and by others. From preliminary information, we hypothesise that bull shark mating and gestation in Reunion could begin in autumn and occur mostly in winter. Following this hypothesis, it is possible that low catch rates in winter, despite a higher percentage of detected sharks, was the consequence of reduced feeding activity due to reproductive drivers. Finally, a recent study on factors affecting the detection range of acoustic receivers has shown strong seasonal variation in range detections, mainly due to currents and episodic weather events (Mathies et al. 2014). These biases in acoustic detections linked to environmental conditions might influence the stronger seasonality observed from acoustic telemetry data compared to that observed in catch rate results for both species. Unfortunately, we were unable to quantify this effect in this study, but we plan to deploy more offshore receivers with stationary control tags to better understand the detection efficiency of the network of receivers. In conclusion, the present study provides the first information on the temporal presence of tiger and bull sharks on the west coast of Reunion Island. Using two techniques, we found seasonal variation in both species, which remain difficult to explain. Ongoing research on reproduction, trophic ecology, and connectivity with other populations in the South-West Indian Ocean should help to better understand the effect of life-history stage and environmental factors on these seasonal variations. In addition, to increase our knowledge of seasonal variation in shark presence, the network of VR2W receivers will be widened to cover the entire coast of Reunion Island, as well as additional offshore sites. We hope that this research will provide information to better orientate the shark attack mitigation programmes and prevent a cull of sharks that could have unanticipated consequences for the functioning of the coastal ecosystems of the island (Rosenblatt et al. 2013). Acknowledgements — We thank the French government, the Reunion regional government and the European Union which provided the necessary funds for this research. We are grateful to all members of the institutions and associations involved in the different shark programmes (IRD-CHARC, CRPMEM, WEST, ECOMAR, Globice, Kélonia, ARVAM, CROSS, Squal’Idées, RNMR, Ifremer, LRS, PRR), as well as all volunteers who assisted in various programmes and made our work possible. Finally, we thank anonymous reviewers and the guest editor for their comments and advice, which helped to improve this paper.

References Beschta RL, Ripple WJ. 2009. Large predators and trophic cascades in terrestrial ecosystems of the western United States. Biological Conservation 142: 2401–2414. Branstetter S, Musick JA, Colvocoresses JA. 1987. A comparison of the age and growth of the tiger shark, Galeocerdo cuvier, from off Virginia and from the northwestern Gulf of Mexico. Fishery



Bulletin 85: 269–279. Branstetter S, Stiles R. 1987. Age and growth estimates of the bull shark, Carcharhinus leucas, from the northern Gulf of Mexico. Environmental Biology of Fishes 20: 169–181. Brunnschweiler JM, Baensch H. 2011. Seasonal and long-term changes in relative abundance of bull sharks from a tourist shark feeding site in Fiji. PLoS ONE 6: e16597. Brunnschweiler JM, Queiroz N, Sims DW. 2010. Oceans apart? Short-term movements and behaviour of adult bull sharks Carcharhinus leucas in Atlantic and Pacific Oceans determined from pop-off satellite archival tagging. Journal of Fish Biology 77: 1343–1358. Burgess GH. 2014. ISAF [International Shark Attack File] 2013 worldwide shark attack summary report. Florida Museum of Natural History, Gainesville, Florida. Carlson JK, Hale LF, Morgan A, Burgess G. 2012. Relative abundance and size of coastal sharks derived from commercial shark longline catch and effort data. Journal of Fish Biology 80: 1749–1764. Carlson JK, Ribera MM, Conrath CL, Heupel MR, Burgess GH. 2010. Habitat use and movement patterns of bull sharks Carcharhinus leucas determined using pop-up satellite archival tags. Journal of Fish Biology 77: 661–675. Cliff G, Dudley SFJ. 1991. Sharks caught in the protective gill nets off Natal, South Africa. 4. The bull shark Carcharhinus leucas Valenciennes. South African Journal of Marine Science 10: 253–270. Cliff G, Dudley SFJ. 1992. Protection against shark attack in South Africa, 1952 to 1990. Australian Journal of Marine and Freshwater Research 43: 263–272. Cliff G, Dudley SFJ. 2011. Reducing the environmental impact of shark-control programs: a case study from KwaZulu-Natal, South Africa. Marine and Freshwater Research 62: 700–709. Conand F, Marsac F, Tessier E, Conand C. 2007. A ten-year period of daily sea surface temperature at a coastal station in Reunion Island, Indian Ocean (July 1993–April 2004): patterns of variability and biological responses. Western Indian Ocean Journal of Marine Science 6: 1–16. Cruz-Martínez A, Chiappa-Carrara X, Arenas-Fuentes V. 2004. Age and growth of the bull shark, Carcharhinus leucas, from southern Gulf of Mexico. Journal of Northwest Atlantic Fishery Science 35: 367–374. Curtis TH. 2008. Distribution, movements and habitat use of bull sharks (Carcharhinus leucas, Müller and Henle 1839) in the Indian River lagoon system, Florida. PhD thesis, University of Florida, USA. Curtis TH, Bruce BD, Cliff G, Dudley SFJ, Klimley AP, Kock A et al. 2012. Responding to the risk of white shark attack. Updated statistics, prevention, control methods, and recommendations. In: Domeier ML (ed.), Global perspectives on the biology and life history of the great white shark. Boca Raton, Florida: CRC Press. pp 477–509. Daly R, Smale MJ, Cowley PD, Froneman PW. 2014. Residency patterns and migration dynamics of adult bull sharks (Carcharhinus leucas) on the East Coast of southern Africa. PLoS ONE 9: e109357. Dudley SFJ, Haestier RC, Cox KR, Murray M. 1998. Shark control: experimental fishing with baited drumlines. Marine and Freshwater Research 49: 653–661. Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK. 2010. Patterns and ecosystem consequences of shark decline in the ocean. Ecology Letters 13: 1055–1071. Fricke R, Mulochau T, Durville P, Chabanet P, Tessier E, Letourneur Y. 2009. Annotated checklist of the fish species (Pisces) of La Réunion, including a Red List of threatened and declining species. Stuttgarter Beiträge zur Naturkunde A, Neue Serie 2: 1–168.

207

Hazin FHV, Afonso AS. 2014. A green strategy for shark attack mitigation off Recife, Brazil. Animal Conservation 17: 287–296. Hazin FHV, Burgess GH, Carvalho FC. 2008. A shark attack outbreak off Recife, Pernambuco, Brazil: 1992–2006. Bulletin of Marine Science 82: 199–212. Heithaus MR. 2001. The biology of tiger sharks (Galeocerdo cuvier) in Shark Bay, Western Australia: sex ratio, size distribution, diet, and seasonal changes in catch rates. Environmental Biology of Fishes 61: 25–36. Heithaus MR, Delius BK, Wirsing AJ, Dunphydaly MM. 2009. Physical factors influencing the distribution of a top predator in a subtropical oligotrophic estuary. Limnology and Oceanography 54: 472–482. Heithaus M[R], Frid A, Dill L. 2002. Shark-inflicted injury frequencies, escape ability, and habitat use of green and loggerhead turtles. Marine Biology 140: 229–236. Holland KN, Bush A, Meyer CG, Kajiura S, Wetherbee BM, Lowe CG. 2001. Five tags applied to a single species in a single location: the tiger shark experience. In: Sibert JR, Nielsen J (eds), Electronic tagging and tracking in marine fisheries. Dordrecht: Kluwer. pp 237–247. Holland KN, Wetherbee BM, Lowe CG, Meyer CG. 1999. Movements of tiger sharks (Galeocerdo cuvier) in coastal Hawaiian waters. Marine Biology 134: 665–673. Jaquemet J, Smale MJ, Blaison A, Guyomard D, Soria M. 2013. First observation of a pregnant tiger shark (Galeocerdo cuvier) in Reunion Island, western Indian Ocean. Western Indian Ocean Journal of Marine Science 11: 205–207. Kohler NE, Casey JG, Turner PA. 1995. Length-weight relationships for 13 species of sharks from the western North Atlantic. Fishery Bulletin 93: 412–418. Kohler NE, Casey JG, Turner PA. 1996. Length-length and lengthweight relationships for 13 shark species from the Western North Atlantic. NOAA Technical Memorandum NMFS-NE-110. Lagabrielle E, Loiseau N, Verlinden N, Chabanet P, Soria M. 2012. Analyse des conditions environnementales et des usages de la mer associés aux attaques de requin à l’île de la Réunion entre 1980 et 2011. Program CHARC report. IRD, La Réunion. Landron F. 2006. Etude des attaques de requins sur les pratiquants de sports de glisse à La Réunion. PhD thesis, Caen University, France. Letourneur Y. 1998. Composition, structures et réseaux trophiques des peuplements de poissons de la côte au vent de l’île de la Réunion. Cybium 22: 267–283. Letourneur Y, Chabanet P, Durville P, Taquet M, Teissier M, Parmentier M et al. 2004. An updated checklist of the marine fish fauna of Reunion Island, South-Western Indian Ocean. Cybium 28: 199–216. Lowe CG, Wetherbee BM, Meyer CG. 2006. Using acoustic telemetry monitoring techniques to quantify movement patterns and site fidelity of sharks and giant trevally around French Frigate Shoals and Midway Atoll. Atoll Research Bulletin 543: 281–303. Lucifora LO, García VB, Worm B. 2011. Global diversity hotspots and conservation priorities for sharks. PLoS ONE 6: e19356. Mathies H, Ogburn MB, McFall G, Fangman S. 2014. Environ mental interference factors affecting detection range in acoustic telemetry studies using fixed receiver arrays. Marine Ecology Progress Series 495: 27–38. McCord M, Lamberth S. 2009. Catching and tracking the world’s largest Zambezi (bull) shark Carcharhinus leucas in the Breede Estuary, South Africa: the first 43 hours. African Journal of Marine Science 31: 107–111. Meyer CG, Clark TB, Papastamatiou YP, Whitney NM, Holland KN. 2009. Long-term movements of tiger sharks (Galeocerdo cuvier) in Hawaii. Marine Ecology Progress Series 381: 223–235. Meyer CG, Papastamatiou YP, Holland KN. 2010. A multiple


208


instrument approach to quantifying the movement patterns and habitat use of tiger (Galeocerdo cuvier) and Galapagos sharks (Carcharhinus galapagensis) at French Frigate Shoals, Hawaii. Marine Biology 157: 1857–1868. Montaggioni LF, Faure G. 1980. Récifs coralliens des Mascareignes: Océan Indien. Collection des Travaux du Centre Universitaire. La Réunion: Université Française de l’Océan Indien. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858. Neer JA, Thompson BA, Carlson JK. 2005. Age and growth of Carcharhinus leucas in the northern Gulf of Mexico: incorporating variability in size at birth. Journal of Fish Biology 67: 370–383. Nel DC, Peschak TP (eds). 2006. Finding a balance: white shark conservation and recreational safety in the inshore waters of Cape Town, South Africa. Proceedings of a specialist workshop, 29–30 May 2006, Cape Town, South Africa. WWF South Africa Report Series–2006/Marine/001 Annexure 1. O’Connell CP, Abel DC, Gruber SH, Stroud EM, Rice PH. 2011. Response of juvenile lemon sharks, Negaprion brevirostris, to a magnetic barrier simulating a beach net. Ocean & Coastal Management 54: 225–230. O’Connell CP, Stroud EM, Pingguo He. 2014. The emerging field of electrosensory and semiochemical shark repellents: mechanisms of detection, overview of past studies, and future directions. Ocean & Coastal Management 97: 2–11. Perry C, Pino F, Guyomard D, Bodilis G. 2014. Real time alert innovation for maximising the “survival rate at releasing” of large sharks and other marine species: the “smart drumline” developed in Reunion Island. Paper presented at the Sharks International 2014 Conference, Durban, South Africa, 2–6 June 2014. Abstract available at http://www.sharksinternational.org/Pages/ ProgramInformation [accessed 4 May 2015]. Rosenblatt AE, Heithaus MR, Mather ME, Matich P, Nifong JC, Ripple WJ, Silliman BR. 2013. The roles of large top predators in coastal ecosystems: new insights from long term ecological research. Oceanography 26: 156–167. Sadowski V. 1971. Notes on the Bull shark, Carcharhinus leucas, in the lagoon region of Cananéia, Brazil. Boletim do Instituto Oceanográfico 20: 71–78. Simpfendorfer CA, Freitas GG, Wiley TR, Heupel MR. 2005. Distribution and habitat partitioning of immature bull sharks

(Carcharhinus leucas) in a southwest Florida estuary. Estuaries 28: 78–85. Shin YJ, Cury P. 2004. Using an individual-based model of fish assemblages to study the response of size spectra to changes in fishing. Canadian Journal of Fisheries and Aquatic Sciences 61: 414–431. Snelson FF, Mulligan TJ, Williams SE. 1984. Food habits, occurrence and population structure of the bull shark, Carcharhinus leucas, in Florida coastal lagoons. Bulletin of Marine Science 34: 71–80. Stevens J, Bonfil R, Dulvy NK, Walker PA. 2000. The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57: 476–494. Tricas TC, Taylor LR, Naftel G. 1981. Diel behavior of the tiger shark, Galeocerdo cuvier, at French Frigate Shoals, Hawaiian Islands. Copeia 1981: 904–908. Tuma RE. 1976. An investigation of the feeding habits of the bull shark, Carcharhinus leucas, in the Lake Nicaragua, Rio San Juan System. In: Thorson TB (ed.), Investigation of the ichthyofauna of Nicaraguan lakes. Lincoln, Nebraska: School of Life Sciences, University of Nebraska-Lincoln. pp 533–538. Vangrevelynghe G. 1994. Les attaques de requins à La Réunion, mythes et réalités. A propos de 12 cas d’accidents liés aux requins. PhD thesis, Lille II University, France. Vangrevelynghe G. 1999. Attaques de requins à l’île de La Réunion (sud-ouest de l’Océan Indien). In: Seret B, Sire J-Y (eds), Proceedings of the 3rd Meeting of the European Elasmobranch Association, 27–29 May, Boulogne-sur-Mer, France. Paris: French Ichthyological Society and IRD. pp 78–81. Werbrouck A, Vangrevelynghe G, Landron F, Charlier P, Loire C, Gauthier C. 2014. Expertise médicolégale des victimes d’attaques et de morsures de requins à la Réunion. La Revue de Médecine Légale 5: 110–121. Wetherbee BM, Lowe CG, Crow GL. 1994. A review of shark control in Hawaii with recommendations for future research. Pacific Science 48: 95–115. Whitney NM, Crow GL. 2006. Reproductive biology of the tiger shark (Galeocerdo cuvier) in Hawaii. Marine Biology 151: 63–70. Wirsing AJ, Heithaus MR, Dill LM. 2006. Tiger shark (Galeocerdo cuvier) abundance and growth in a subtropical embayment: evidence from 7 years of standardized fishing effort. Marine Biology 149: 961–968.

Manuscript received June 2014, revised March 2015, accepted April 2015