Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE (Open Access)

Short-term response of research activities on white shark behaviour

Yuri Niella https://orcid.org/0000-0003-1878-6091 A B * , Brett Simes C , Andrew Fox D , Andrew Wright E , Matt Waller F , Madeline Riley B , Lauren Meyer B , Michael Drew G , Hugh Pederson H and Charlie Huveneers B
+ Author Affiliations
- Author Affiliations

A School of Natural Sciences, Faculty of Science and Engineering, Macquarie University, North Ryde, Sydney, NSW 2113, Australia.

B Southern Shark Ecology Group, College of Science and Engineering, Flinders University, Adelaide, SA 5042, Australia.

C South Australian Department for Environment and Water, Adelaide, SA 5000, Australia.

D Rodney Fox Shark Expeditions, Adelaide, SA 5031, Australia.

E Calypso Star Charters, Port Lincoln, SA 5606, Australia.

F Adventure Bay Chartres, Port Lincoln, SA 5606, Australia.

G South Australian Research and Development Institute – Aquatic Sciences, Adelaide, SA 5024, Australia.

H Innovasea, Bedford, NS B4B 0L9, Canada.

* Correspondence to: yuri.niella@gmail.com

Handling Editor: Aaron Wirsing

Wildlife Research 50(4) 260-271 https://doi.org/10.1071/WR22004
Submitted: 27 January 2022  Accepted: 27 September 2022   Published: 4 November 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: Researchers studying animals need to ensure that sampling procedures and the methods they use are as harmless and non-disruptive as possible, particularly when their focal species are threatened or protected. White sharks (Carcharodon carcharias) are Vulnerable under the IUCN Red List, protected globally, and are frequently studied by marine ecologists.

Aims: To assess white shark responses to research activities (i.e. tagging and biopsy procedures, and electric deterrent trials) conducted at the Neptune Islands Group Marine Park (South Australia, Australia).

Methods: Trends in shark residency following research activities were assessed by comparing shark abundance (number of sharks detected by acoustic receivers and sighted by cage-diving operators) before, during, and after scientific expeditions, and to natural fluctuations in the absence of research activities using 8 years (2013–2021) of acoustic tracking and daily sighting reports from a wildlife tourism industry.

Key results: Number of white sharks and residency decreased after sampling. However, changes observed following research activities were similar to natural fluctuations, suggesting that these changes reflected natural variations rather than being due to sharks responding negatively to the research activities.

Conclusions: Our study showed that external tagging, biopsies, or deterrent trials do not affect short- and long-term residency or abundance of white sharks, probably owing to the research activities being minimally intrusive and to sharks having efficient immune systems and remarkable ability to heal from injuries.

Implications: Re-evaluating study methods forms part of the researcher’s responsibilities to ensure best practice and to abide by national and international codes for the care and use of animals for scientific purposes.

Keywords: acoustic telemetry, animal welfare, biopsy sampling, cage-diving, research impacts, shark deterrents, white sharks, wildlife tourism.


References

Beauchamp TL, DeGrazia D (2019) ‘Principles of animal research ethics.’ (Oxford University Press)

Becerril-García, EE, Hoyos-Padilla, EM, Micarelli, P, Galván-Magaña, F, and Sperone, E (2019). The surface behaviour of white sharks during ecotourism: a baseline for monitoring this threatened species around Guadalupe Island, Mexico. Aquatic Conservation: Marine and Freshwater Ecosystems 29, 773–782.
The surface behaviour of white sharks during ecotourism: a baseline for monitoring this threatened species around Guadalupe Island, Mexico.Crossref | GoogleScholarGoogle Scholar |

Black, C, Merly, L, and Hammerschlag, N (2021). Bacterial communities in multiple tissues across the body surface of three coastal shark species. Zoological Studies 60, e69.
Bacterial communities in multiple tissues across the body surface of three coastal shark species.Crossref | GoogleScholarGoogle Scholar |

Bruce, B, and Bradford, R (2015). Segregation or aggregation? Sex-specific patterns in the seasonal occurrence of white sharks Carcharodon carcharias at the Neptune Islands, South Australia. Journal of Fish Biology 87, 1355–1370.
Segregation or aggregation? Sex-specific patterns in the seasonal occurrence of white sharks Carcharodon carcharias at the Neptune Islands, South Australia.Crossref | GoogleScholarGoogle Scholar |

Bruce, BD, and Bradford, RW (2013). The effects of shark cage-diving operations on the behaviour and movements of white sharks, Carcharodon carcharias, at the Neptune Islands, South Australia. Marine Biology 160, 889–907.
The effects of shark cage-diving operations on the behaviour and movements of white sharks, Carcharodon carcharias, at the Neptune Islands, South Australia.Crossref | GoogleScholarGoogle Scholar |

Butcher, PA, Piddocke, TP, Colefax, AP, Hoade, B, Peddemors, VM, Borg, L, and Cullis, BR (2019). Beach safety: can drones provide a platform for sighting sharks? Wildlife Research 46, 701–712.
Beach safety: can drones provide a platform for sighting sharks?Crossref | GoogleScholarGoogle Scholar |

Chin, A, Mourier, J, and Rummer, JL (2015). Blacktip reef sharks (Carcharhinus melanopterus) show high capacity for wound healing and recovery following injury. Conservation Physiology 3, cov062.
Blacktip reef sharks (Carcharhinus melanopterus) show high capacity for wound healing and recovery following injury.Crossref | GoogleScholarGoogle Scholar |

Criscitiello, MF (2014). What the shark immune system can and cannot provide for the expanding design landscape of immunotherapy. Expert Opinion on Drug Discovery 9, 725–739.
What the shark immune system can and cannot provide for the expanding design landscape of immunotherapy.Crossref | GoogleScholarGoogle Scholar |

Crozier, GKD, and Schulte-Hostedde, AI (2015). Towards improving the ethics of ecological research. Science and Engineering Ethics 21, 577–594.
Towards improving the ethics of ecological research.Crossref | GoogleScholarGoogle Scholar |

Curtis TH, Bruce BD, Cliff G, Dudley SFJ, Klimley AP, Kock A, Lea RN, Lowe CG, McCosker JE, Skomal GB, Werry JM, West JG (2012) Responding to the risk of white whark attack. Updated statistics, prevention, control Methods, and recommendations. In ‘Global perspectives on the biology and life history of the white shark’. (Ed. ML Domeier) pp. 477–510. (CRC Press)

Dawkins, MS (2006). A user’s guide to animal welfare science. Trends in Ecology & Evolution 21, 77–82.
A user’s guide to animal welfare science.Crossref | GoogleScholarGoogle Scholar |

DeGrazia, D, and Beauchamp, TL (2019). Beyond the 3 Rs to a more comprehensive framework of principles for animal research ethics. ILAR Journal 60, 308–317.
Beyond the 3 Rs to a more comprehensive framework of principles for animal research ethics.Crossref | GoogleScholarGoogle Scholar |

Department of Sustainability Environment Water Population and Communities (2013) ‘Recovery plan for the white shark (Carcharodon carcharias). (Department of Sustainability Environment Water Population and Communities)

Drenner, SM, Clark, TD, Whitney, CK, Martins, EG, Cooke, SJ, and Hinch, SG (2012). A synthesis of tagging studies examining the behaviour and survival of anadromous salmonids in marine environments. PLoS ONE 7, e31311.
A synthesis of tagging studies examining the behaviour and survival of anadromous salmonids in marine environments.Crossref | GoogleScholarGoogle Scholar |

Fenwick, N, Griffin, G, and Gauthier, C (2009). The welfare of animals used in science: how the ‘Three Rs’ ethic guides improvements. The Canadian Veterinary Journal 50, 523–530.

Francis, MP, Duffy, C, and Lyon, W (2015). Spatial and temporal habitat use by white sharks (Carcharodon carcharias) at an aggregation site in southern New Zealand. Marine and Freshwater Research 66, 900–918.
Spatial and temporal habitat use by white sharks (Carcharodon carcharias) at an aggregation site in southern New Zealand.Crossref | GoogleScholarGoogle Scholar |

Gallagher, AJ, Meyer, L, Pethybridge, HR, Huveneers, C, and Butcher, PA (2019). Effects of short-term capture on the physiology of white sharks Carcharodon carcharias: amino acids and fatty acids. Endangered Species Research 40, 297–308.
Effects of short-term capture on the physiology of white sharks Carcharodon carcharias: amino acids and fatty acids.Crossref | GoogleScholarGoogle Scholar |

Gauthier, ARG, Chateauminois, E, Hoarau, MG, Gadenne, J, Hoarau, E, Jaquemet, S, Whitmarsh, SK, and Huveneers, C (2020). Variable response to electric shark deterrents in bull sharks, Carcharhinus leucas. Scientific Reports 10, 17869.
Variable response to electric shark deterrents in bull sharks, Carcharhinus leucas.Crossref | GoogleScholarGoogle Scholar |

Gorkin, R, Adams, K, Berryman, MJ, Aubin, S, Li, W, Davis, AR, and Barthelemy, J (2020). Sharkeye: real-time autonomous personal shark alerting via aerial surveillance. Drones 4, 18.
Sharkeye: real-time autonomous personal shark alerting via aerial surveillance.Crossref | GoogleScholarGoogle Scholar |

Guttridge, TL, van Dijk, S, Stamhuis, EJ, Krause, J, Gruber, SH, and Brown, C (2013). Social learning in juvenile lemon sharks, Negaprion brevirostris. Animal Cognition 16, 55–64.
Social learning in juvenile lemon sharks, Negaprion brevirostris.Crossref | GoogleScholarGoogle Scholar |

Heupel, MR, Simpfendorfer, CA, and Bennett, MB (1998). Analysis of tissue responses to fin tagging in Australian carcharhinids. Journal of Fish Biology 52, 610–620.
Analysis of tissue responses to fin tagging in Australian carcharhinids.Crossref | GoogleScholarGoogle Scholar |

Hoppitt, W, and Laland, KN (2008). Social processes influencing learning in animals: a review of the evidence. Advances in the Study of Behavior 38, 105–165.
Social processes influencing learning in animals: a review of the evidence.Crossref | GoogleScholarGoogle Scholar |

Huveneers C, Niella Y (2022) Residency of white sharks, Carcharodon carcharias, at the Neptune Islands Group Marine Park (2021-2022). Report to the Department of the Environment, Water and Natural Resources.

Huveneers, C, Rogers, PJ, Beckmann, C, Semmens, JM, Bruce, BD, and Seuront, L (2013a). The effects of cage-diving activities on the fine-scale swimming behaviour and space use of white sharks. Marine Biology 160, 2863–2875.
The effects of cage-diving activities on the fine-scale swimming behaviour and space use of white sharks.Crossref | GoogleScholarGoogle Scholar |

Huveneers, C, Rogers, PJ, Semmens, JM, Beckmann, C, Kock, AA, Page, B, and Goldsworthy, SD (2013b). Effects of an electric field on white sharks: in situ testing of an electric deterrent. PLoS ONE 8, e62730.
Effects of an electric field on white sharks: in situ testing of an electric deterrent.Crossref | GoogleScholarGoogle Scholar |

Huveneers, C, Holman, D, Robbins, R, Fox, A, Endler, JA, and Taylor, AH (2015). White sharks exploit the sun during predatory approaches. The American Naturalist 185, 562–570.
White sharks exploit the sun during predatory approaches.Crossref | GoogleScholarGoogle Scholar |

Huveneers, C, Watanabe, YY, Payne, NL, and Semmens, JM (2018a). Interacting with wildlife tourism increases activity of white sharks. Conservation Physiology 6, coy019.
Interacting with wildlife tourism increases activity of white sharks.Crossref | GoogleScholarGoogle Scholar |

Huveneers, C, Whitmarsh, S, Thiele, M, Meyer, L, Fox, A, and Bradshaw, CJA (2018b). Effectiveness of five personal shark-bite deterrents for surfers. PeerJ 6, e5554.
Effectiveness of five personal shark-bite deterrents for surfers.Crossref | GoogleScholarGoogle Scholar |

Huveneers, C, Jaine, FRA, Barnett, A, et al. (2021). The power of national acoustic tracking networks to assess the impacts of human activity on marine organisms during the COVID-19 pandemic. Biological Conservation 256, 108995.
The power of national acoustic tracking networks to assess the impacts of human activity on marine organisms during the COVID-19 pandemic.Crossref | GoogleScholarGoogle Scholar |

Jepsen, N, Thorstad, EB, Havn, T, and Lucas, MC (2015). The use of external electronic tags on fish: an evaluation of tag retention and tagging effects. Animal Biotelemetry 3, 49.
The use of external electronic tags on fish: an evaluation of tag retention and tagging effects.Crossref | GoogleScholarGoogle Scholar |

Kempster, RM, Egeberg, CA, Hart, NS, Ryan, L, Chapuis, L, Kerr, CC, Schmidt, C, Huveneers, C, Gennari, E, Yopak, KE, Meeuwig, JJ, and Collin, SP (2016). How close is too close? The effect of a non-lethal electric shark deterrent on white shark behaviour. PLoS ONE 11, e0157717.
How close is too close? The effect of a non-lethal electric shark deterrent on white shark behaviour.Crossref | GoogleScholarGoogle Scholar |

Kessel, ST, Fraser, J, van Bonn, WG, Brooks, JL, Guttridge, TL, Hussey, NE, and Gruber, SH (2017). Transcoelomic expulsion of an ingested foreign object by a carcharhinid shark. Marine and Freshwater Research 68, 2173–2177.
Transcoelomic expulsion of an ingested foreign object by a carcharhinid shark.Crossref | GoogleScholarGoogle Scholar |

Klinard, NV, Halfyard, EA, Fisk, AT, Stewart, TJ, and Johnson, TB (2018). Effects of surgically implanted acoustic tags on body condition, growth, and survival in a small, laterally compressed forage fish. Transactions of the American Fisheries Society 147, 749–757.
Effects of surgically implanted acoustic tags on body condition, growth, and survival in a small, laterally compressed forage fish.Crossref | GoogleScholarGoogle Scholar |

Krogh, M, and Reid, D (1996). Bycatch in the protective shark meshing programme off south-eastern New South Wales, Australia. Biological Conservation 77, 219–226.
Bycatch in the protective shark meshing programme off south-eastern New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |

Legaspi, C, Miranda, J, Labaja, J, Snow, S, Ponzo, A, and Araujo, G (2020). In-water observations highlight the effects of provisioning on whale shark behaviour at the world’s largest whale shark tourism destination. Royal Society Open Science 7, 200392.
In-water observations highlight the effects of provisioning on whale shark behaviour at the world’s largest whale shark tourism destination.Crossref | GoogleScholarGoogle Scholar |

Macolm H, Bruce BD, Stevens JD (2001) ‘A review of the biology and status of white shark in Australian waters.’ (CSIRO Marine Research)

Meeuwig, JJ, and Ferreira, LC (2014). Moving beyond lethal programs for shark hazard mitigation. Animal Conservation 17, 297–298.
Moving beyond lethal programs for shark hazard mitigation.Crossref | GoogleScholarGoogle Scholar |

Meyer, CG, Dale, JJ, Papastamatiou, YP, Whitney, NM, and Holland, KN (2009). Seasonal cycles and long-term trends in abundance and species composition of sharks associated with cage diving ecotourism activities in Hawaii. Environmental Conservation 36, 104–111.
Seasonal cycles and long-term trends in abundance and species composition of sharks associated with cage diving ecotourism activities in Hawaii.Crossref | GoogleScholarGoogle Scholar |

Meyer, L, Fox, A, and Huveneers, C (2018). Simple biopsy modification to collect muscle samples from free-swimming sharks. Biological Conservation 228, 142–147.
Simple biopsy modification to collect muscle samples from free-swimming sharks.Crossref | GoogleScholarGoogle Scholar |

Meyer, L, Pethybridge, H, Beckmann, C, Bruce, B, and Huveneers, C (2019). The impact of wildlife tourism on the foraging ecology and nutritional condition of an apex predator. Tourism Management 75, 206–215.
The impact of wildlife tourism on the foraging ecology and nutritional condition of an apex predator.Crossref | GoogleScholarGoogle Scholar |

Meyer, L, Apps, K, Bryars, S, Clarke, T, Hayden, B, Pelton, G, Simes, B, Vaughan, LM, Whitmarsh, SK, and Huveneers, C (2021). A multidisciplinary framework to assess the sustainability and acceptability of wildlife tourism operations. Conservation Letters 14, e12788.
A multidisciplinary framework to assess the sustainability and acceptability of wildlife tourism operations.Crossref | GoogleScholarGoogle Scholar |

Meyer, L, Barry, C, Araujo, G, Barnett, A, Brunnschweiler, JM, Chin, A, Gallagher, A, Healy, T, Kock, A, Newsome, D, Ponzo, A, and Huveneers, C (2022). Redefining provisioning in marine wildlife tourism. Journal of Ecotourism 21, 210–229.
Redefining provisioning in marine wildlife tourism.Crossref | GoogleScholarGoogle Scholar |

Nazimi, L, Robbins, WD, Schilds, A, and Huveneers, C (2018). Comparison of industry-based data to monitor white shark cage-dive tourism. Tourism Management 66, 263–273.
Comparison of industry-based data to monitor white shark cage-dive tourism.Crossref | GoogleScholarGoogle Scholar |

Neves, V, Silva, D, Martinho, F, Antunes, C, Ramos, S, and Freitas, V (2018). Assessing the effects of internal and external acoustic tagging methods on European flounder Platichthys flesus. Fisheries Research 206, 202–208.
Assessing the effects of internal and external acoustic tagging methods on European flounder Platichthys flesus.Crossref | GoogleScholarGoogle Scholar |

Palmer, A, and Greenhough, B (2021). Out of the laboratory, into the field: perspectives on social, ethical and regulatory challenges in UK wildlife research. Philosophical Transactions of the Royal Society B: Biological Sciences 376, 20200226.
Out of the laboratory, into the field: perspectives on social, ethical and regulatory challenges in UK wildlife research.Crossref | GoogleScholarGoogle Scholar |

Perry, CT, Pratte, ZA, Clavere-Graciette, A, Ritchie, KB, Hueter, RE, Newton, AL, Fischer, GC, Dinsdale, EA, Doane, MP, Wilkinson, KA, Bassos-Hull, K, Lyons, K, Dove, ADM, Hoopes, LA, and Stewart, FJ (2021). Elasmobranch microbiomes: emerging patterns and implications for host health and ecology. Animal Microbiome 3, 61.
Elasmobranch microbiomes: emerging patterns and implications for host health and ecology.Crossref | GoogleScholarGoogle Scholar |

Pratt, H, and Carrier, J (2001). A review of elasmobranch reproductive behaviour with a case study on the nurse shark, Ginglymostoma cirratum. Environmental Biology of Fishes 60, 157–188.
A review of elasmobranch reproductive behaviour with a case study on the nurse shark, Ginglymostoma cirratum.Crossref | GoogleScholarGoogle Scholar |

Reisinger, RR, Oosthuizen, WC, Péron, G, Cory Toussaint, D, Andrews, RD, and de Bruyn, PJN (2014). Satellite tagging and biopsy sampling of killer whales at subantarctic Marion Island: effectiveness, immediate reactions and long-term responses. PLoS ONE 9, e111835.
Satellite tagging and biopsy sampling of killer whales at subantarctic Marion Island: effectiveness, immediate reactions and long-term responses.Crossref | GoogleScholarGoogle Scholar |

Rigby CL, Barreto R, Carlson J, Fernando D, Fordham S, Francis MP, Herman K, Jabado RW, Liu KM, Lowe CG, Marshall A, Pacoureau N, Romanov E, Sherley RB, Winker H (2019) Carcharodon carcharias. The IUCN Red List of Threatened Species, e.T3855A2878674. Accessed on 17 October 2022 https://doi.org/
| Crossref |

Russell WMS, Burch RL (1959) ‘The principles of humane experimental technique.’ (Universities Federation for Animal Welfare)

Ryklief, R, Pistorius, PA, and Johnson, R (2014). Spatial and seasonal patterns in sighting rate and life-history composition of the white shark Carcharodon carcharias at Mossel Bay, South Africa. African Journal of Marine Science 36, 449–453.
Spatial and seasonal patterns in sighting rate and life-history composition of the white shark Carcharodon carcharias at Mossel Bay, South Africa.Crossref | GoogleScholarGoogle Scholar |

Schilds, A, Mourier, J, Huveneers, C, Nazimi, L, Fox, A, and Leu, ST (2019). Evidence for non-random co-occurrences in a white shark aggregation. Behavioral Ecology and Sociobiology 73, 138.
Evidence for non-random co-occurrences in a white shark aggregation.Crossref | GoogleScholarGoogle Scholar |

Simmons, P, and Mehmet, MI (2018). Shark management strategy policy considerations: community preferences, reasoning and speculations. Marine Policy 96, 111–119.
Shark management strategy policy considerations: community preferences, reasoning and speculations.Crossref | GoogleScholarGoogle Scholar |

Soulsbury, CD, Gray, HE, Smith, LM, Braithwaite, V, Cotter, SC, Elwood, RW, Wilkinson, A, and Collins, LM (2020). The welfare and ethics of research involving wild animals: a primer. Methods in Ecology and Evolution 11, 1164–1181.
The welfare and ethics of research involving wild animals: a primer.Crossref | GoogleScholarGoogle Scholar |

Speed, CW, O’Shea, OR, and Meekan, MG (2013). Transmitter attachment and release methods for short-term shark and stingray tracking on coral reefs. Marine Biology 160, 1041–1050.
Transmitter attachment and release methods for short-term shark and stingray tracking on coral reefs.Crossref | GoogleScholarGoogle Scholar |

Tate, RD, Cullis, BR, Smith, SDA, Kelaher, BP, Brand, CP, Gallen, CR, Mandelman, JW, and Butcher, PA (2019). Corrigendum to: The acute physiological status of white sharks (Carcharodon carcharias) exhibits minimal variation after capture on SMART drumlines. Conservation Physiology 7, coz090.
Corrigendum to: The acute physiological status of white sharks (Carcharodon carcharias) exhibits minimal variation after capture on SMART drumlines.Crossref | GoogleScholarGoogle Scholar |

Theberge, MM, and Dearden, P (2006). Detecting a decline in whale shark Rhincodon typus sightings in the Andaman Sea, Thailand, using ecotourist operator-collected data. Oryx 40, 337–342.
Detecting a decline in whale shark Rhincodon typus sightings in the Andaman Sea, Thailand, using ecotourist operator-collected data.Crossref | GoogleScholarGoogle Scholar |

Thiele, M, Mourier, J, Papastamatiou, Y, Ballesta, L, Chateauminois, E, and Huveneers, C (2020). Response of blacktip reef sharks Carcharhinus melanopterus to shark bite mitigation products. Scientific Reports 10, 3563.
Response of blacktip reef sharks Carcharhinus melanopterus to shark bite mitigation products.Crossref | GoogleScholarGoogle Scholar |

Thonhauser, KE, Gutnick, T, Byrne, RA, Kral, K, Burghardt, GM, and Kuba, MJ (2013). Social learning in Cartilaginous fish (stingrays Potamotrygon falkneri). Animal Cognition 16, 927–932.
Social learning in Cartilaginous fish (stingrays Potamotrygon falkneri).Crossref | GoogleScholarGoogle Scholar |

Towner A, Smale MJ, Jewell O (2012) Boat strike wound healing in Carcharodon carcharias. In ‘Global perspectives on the biology and life history of the white shark’. (Ed. ML Domeier) pp. 77–84. (CRC Press)

Vila Pouca, C, Heinrich, D, Huveneers, C, and Brown, C (2020). Social learning in solitary juvenile sharks. Animal Behaviour 159, 21–27.
Social learning in solitary juvenile sharks.Crossref | GoogleScholarGoogle Scholar |

Wilson, RP, and Mcmahon, CR (2006). Measuring devices on wild animals: what constitutes acceptable practice? Frontiers in Ecology and the Environment 4, 147–154.
Measuring devices on wild animals: what constitutes acceptable practice?Crossref | GoogleScholarGoogle Scholar |

Wood SN (2017) ‘Generalized additive models: an introduction with R.’ 2nd edn. (Chapman and Hall/CRC)