2022-2025
Projet ANR-21-CE03-0004
CONFLICTS BETWEEN LARGE MARINE PREDATORS AND HUMANS:
THE GENESIS AND MANAGEMENT OF PROBLEM INDIVIDUALS
ETHO-PREDATOR will investigate the existence of personalities (temperaments) within two taxa, killer whales and bull sharks, and elucidate the biological and ecological mechanisms driving the emergence of problem individuals (PIs) in human-marine top predator conflicts. Our results will advance sustainable and eco-friendly management of large marine predators.
Contact: Prof. Eric CLUA – eric.clua@ephe.psl.eu – Tél. +33 622802928
Problem sharks’ do exist, and it’s time to adapt shark risk management…
It is widely accepted that populations of large terrestrial animal predators (such as bears or tigers, for example) include “problem individuals” who repeatedly prey on humans. However, this phenomenon, which remained a mere hypothesis -published in 2018 in Conservation Letters – had never before been demonstrated for aquatic predators such as sharks. In our latest study, also published in Conservation Letters, we describe three case studies from three different oceans (Pacific, Caribbean and Red Seas), involving two species dangerous to humans, the Tiger shark and the Oceanic whitetip shark, and using two different methods (photo-identification and genetic analysis), that a single shark killed a first person before going on to prey on other humans. These cases represent the first irrefutable proof that certain (rare) individuals among large sharks are capable of repeating attacks on humans.
The percentage of these individuals is unknown, but this study calls for the systematization of DNA collection (by swabbing implemented by medical staff) on human victims of shark bites in order to better understand this phenomenon. This approach would enable the implementation of shark risk management strategies focusing on the strict elimination of animals for which there is evidence (via genetic matching) that they have already bitten and have a high probability – higher than their congeners – of attacking humans again. It also suggests outlawing the indiscriminate culling currently used by the authorities, which are not only ineffective but also environmentally deleterious and unethical, as they target animals that present no risk to humans.
Note: these recidivist sharks should not be equated with the concept of the “rogue shark” (“Jaws”). While they share this concept in that they repeatedly bite humans, they take no particular pleasure in doing so, and do not specialize in humans – two points which, until proven otherwise, are the stuff of science fiction.
Citation of the article:
Clua, E.E.G., Carl G. Meyer, Freeman M., Baksay S., Bidenbach H., Haguenauer A., Linnell J.D.C., Séguigne C., Surina S., Vely M., Vignaud T., Planes S. (2024). First evidence of individual sharks repeatedly targeting humans. Conservation Letters; 0
First official publication of the ANR Etho-Predator!
Dr. E. Clua (ANR coordinator) and Dr. C. Meyer (ANR scientific panel member) have joined forces to publish an opinion piece in the prestigious journal BEHAVIOUR as part of a special issue dedicated to behavior and cognition in sharks. Their study aims
to deconstruct the fallacy that sharks confuse humans with the predators instinctive prey, such as a seal or turtle. Not only has this hypothesis never been proven, but it is probably false by attempting to substitute for the simple exploratory bite of a
predator that is curious by nature but extremely cautious with respect to unnatural prey such as humans. Moreover, it underestimates the extraordinary sensory capacities of sharks, hence the attached cartoon…
Human-Marine Predator Conflicts
Increasing human encroachment on natural habitats has escalated conflicts between humans and wildlife in both terrestrial and marine environments. For example, marine mammals regularly steal (depredate) commercial fish catches, putting them at risk of being hooked or entangled, or killed by fishers seeking to protect their livelihoods. These interactions threaten vulnerable populations of marine mammals (1). A recent unprecedented spate of agonistic interactions between orcas and sailing boats in Spanish and Portuguese waters demonstrates that novel behaviors can arise in large marine predators leading to new conflicts and potential threats to humans (2).
Similarly, a recent increase in fatal shark bites in French overseas waters such as Reunion Island and New Caledonia (3) has threatened tourism-dependent local economies leading to unselective mass shark culling in an attempt to reduce shark bite risk. Mass shark culling has never been demonstrated to reduce shark bite risk and is an ethically questionable activity that may have negative repercussions on ecosystems in which large marine predators play essential roles (4).
1 – Tixier, P., Barbraud, C., Pardo, D., Gasco, N., Duhamel, G., & Guinet, C. (2017). Demographic consequences of fisheries interaction within a killer whale (Orcinus orca) population. Marine Biology, 164(8), 1-16.
2 – https://www.bbc.co.uk/news/extra/buqvasp1rr/orcas-spain-portugal
3 – https://la1ere.francetvinfo.fr/nouvellecaledonie/discours-uni-contre-abattage-requins-852144.html
4 – Ferretti, F., Jorgensen, S., Chapple, T. K., De Leo, G., & Micheli, F. (2015). Reconciling predator conservation with public safety. Frontiers in Ecology and the Environment, 13(8), 412-417.
The “problem individuals” hypothesis
Recent studies of have demonstrated the presence of “problem individuals” (PIs) within animal populations that are atypically aggressive toward humans when compared to most of their conspecifics (5). PI can be found among populations of terrestrial and marine mammals, and may also exist in shark populations (6). We do not yet fully understand the genesis of these atypical behaviours but existing evidence suggests they may stem from different personalities (temperaments) within the taxa concerned.
The presence of different personality or temperament types is well documented in a variety of terrestrial vertebrates including Humans, primates and big cats, but we know far less about personalities in marine taxa incriminated in direct conflicts with Humans. In animals, five personality traits are recognized including
i) the position of the individual on a Shyness-Boldness continuum, which corresponds to his management of novelty in its environment (without notion of risk);
ii) the position of the individual on an Exploration-Risk avoidance continuum, which corresponds to its management of a risk;
iii) its level of aggressiveness, usually towards conspecifics;
iv) its sociability, which refers to his relationships within his own species, ranging from solitary to gregarious;
v) its level of activity, which refers to its specific behaviour (especially spatial) in the context of the basic behavioural ecology of its species. The presence of personalities within a taxon depends then on three criteria:
i) the existence of significantly different behaviours in a given population,
ii) the repeatability of these differences over time and under varied conditions, and
iii) the heritability of these divergent behaviours (7). Thus the genesis of PIs likely depends on both intrinsic ethological characteristics of a given taxon, such as “boldness” and “exploration” and extrinsic environmental factors. It is likely that parental care, which is highly developed in marine mammals and non-existent in cartilaginous fish, may also play a major role in the genesis of atypical and potentially agonistic behaviours toward humans (6).
A better understanding of the biological mechanisms leading to the emergence of PIs could improve applied management of human-wildlife conflicts. For example, demonstrating the existence of PIs within populations of marine predators would enable us to manage human-wildlife conflicts more effectively by selectively removing a few individuals instead of culling large numbers of these animals and risking unintended negative consequences for marine ecosystems. A more selective approach may also reconcile humans with predators by stigmatizing only a few rare individuals and not the entire species (7). The stake of existence of PIs implies then consequent advances in scientific knowledge, efficiency of management and even conservation. Our proposed study has three main objectives that combine both fundamental and applied science components:
i) demonstrating the existence of personalities within large marine predators;
ii) exploring genetic mechanisms behind phenotypic differences;
iii) the exploration of the consequences that these personalities can have on the emergence of PIs and the survival of individuals (the two being linked) as well as improved management of human-marine wildlife conflicts. Our study will focus on two taxonomic groups that are elasmobranchs and mammals.
- Swan, G. J., Redpath, S. M., Bearhop, S., & McDonald, R. A. (2017). Ecology of problem individuals and the efficacy of selective wildlife management. Trends in Ecology & Evolution, 32(7), 518-530.
- Clua, E. E., & Linnell, J. D. (2019). Individual shark profiling: An innovative and environmentally responsible approach for selectively managing human fatalities. Conservation Letters, 12(2), e12612.
- Réale, D., Reader, S. M., Sol, D., McDougall, P. T., & Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological reviews, 82(2), 291-318..
Model species 1: The shark
Our methodological approach will be based on the choice of two model species, the bull shark Carcharhinus leucas, and the orca Orcinus orca. For these two species, the collection of field ethological data in Fiji and the Indian sector of the Southern Ocean (Antarctica – Crozet Is.) will focus on assessing two behavioural traits linked with “boldness” and “exploration” through ad hoc protocols (WP1 and WP2). All animals whose behaviour has been evaluated will be genetically sampled in order to determine the potential heritability of these behaviours (WP3) (Fig. 1).
Genetic fold: regarding WP3, analyses conducted in killer whales will aim in addition to the long-term photo-identification work to reconstruct a pedigree (parentage assignment) and detect a potential vertical transmission of certain behaviours and personalities. Analyses conducted in sharks will consist of working with genomic markers by using a ‘RadSeq’ approach that will not only be able to determine relatedness between individuals with convergent behaviours, but also potentially the molecular support of this genetic transmission (Fig. 1).
Synthesis and compliance: regarding WP4, all the results will be integrated to make the link between behaviour (WP1 and WP2) and genetics (WP3) in the expectation of answering the hypotheses. If the hypotheses are validated, the consequences of these differentiated and heritable behaviours will be apprehended in terms of the emergence of PI within the populations and taxa concerned, from the point of view of the survival of the animals and also the management of the conflicts they generate (WP4). Innovative PI management options will also be conscientiously elaborated and supported by a socio-anthropological study (see hereafter), before being presented to the concerned bodies. Various media will be used to communicate on these topics of public interest.
TEAM LEADERS
Eric CLUA
Coordinateur
Christophe GUINET
Co-Coordinateur
- Healy, T. J., Hill, N. J., Barnett, A., & Chin, A. (2020). A global review of elasmobranch tourism activities, management and risk. Marine Policy, 118, 103964.
- Tixier, P., Burch, P., Massiot-Granier, F., Ziegler, P., Welsford, D., Lea, M. A., … & Arnould, J. P. (2020). Assessing the impact of toothed whale depredation on socio-ecosystems and fishery management in wide-ranging subantarctic fisheries. Reviews in Fish Biology and Fisheries, 30(1), 203-217
- Guinet, C. (1992). Comportement de chasse des orques (Orcinus orca) autour des iles Crozet. Canadian Journal of Zoology, 70(9), 1656-1667.
Model species 1: The shark
Requin bouledogue
Carcharhinus leucas – Taille max – 4.0 m LT
The bull shark is one of three species of large sharks, along with the great white and the tiger shark Galeocerdo cuvier, responsible for more than 80% of fatal bites on humans for the past five decades. It is the main species involved in the crisis situation that has developed in Reunion Island, with 11 fatal bites between 2011 and November 2020. Among the three species mentioned above, it is the least mobile and the easiest to approach, notably thanks to artificial provisioning (“feeding”) to which it responds very well, ensuring regular access to the animals, even on a scale of several years, and without any unsuitable increased risk for the animals welfare or the sea users security when properly designed and managed1. Artificial feeding can not only be a means of access to the animals (for DNA sampling fuelling WP3) but also of carrying out multiple observations under variable conditions related to the needs of a long-term ethological study protocol. In the context of artificial feeding, we will be able to observe the same animals in different situations and over a minimum period of two years in order to meet the requirements of WP1 and 2.
KUATA (Fiji): Ethological issues – Sharks
The main objectives are to:
- Detect behavioural differences between bull shark individuals in regards to boldness/shyness, risk taking/risk avoidance; and potentially other traits such as sociability, aggressivity and level of activity (that may also have an influence on the PIs emergence);
- Collect DNA samples for each animal whose behaviour can be properly assessed.
- Brena, P. F., Mourier, J., Planes, S., & Clua, E. (2015). Shark and ray provisioning: functional insights into behavioral, ecological and physiological responses across multiple scales. Marine Ecology Progress Series, 538, 273-283..
- Brena, P. F., Mourier, J., Planes, S., & Clua, E. E. (2018). Concede or clash? Solitary sharks competing for food assess rivals to decide. Proceedings of the Royal Society B: Biological Sciences, 285(1875), 20180006.
Methods: Shark behaviour and ecology has always been very challenging to investigate due to the many difficulties arising with working in an oceanic environment as well as the complications linked with the elusive nature of sharks (1). Shark feeding, originally an eco-tourism activity, has become a real tool for scientific investigation. The effects of regular feeding on animals are minimal when properly done from an ecological point of view, and beneficial into the greater picture of conservation, and shark provisioning dives also allow for genetic sampling, tagging, or to better understand the ethology of certain species (2).
Using an ethogram for rating observations (supervised by bull sharks behaviour expert for training purposes and eliminating observer’s bias), sharks behaviour will be evaluated in various situation and compared between individual. Basically, the boldness-shyness trait is evaluated by introducing a source of novelty in the shark environment (such as a shiny drum with tuna heads inside) and the risk taking-avoidance is assessed through the presence and distance kept from divers that are considered as a potential threat.
Trait rating from observations, expert opinions and video will be compiled according to the ethogram and integrate influential factors, and allow to create a personality score for each sharks observed in each situations.
Model species 2: A large odontocete
Orque
Orcinus orca – Taille max – 9.0 m LT
The orca (also named killer whale) is an emblematic species involved in two major conflicts with humans: depredation on fish catches in industrial fisheries for decades2, and more recently direct agonistic interactions with recreational boats. The species is frequently encountered around the Crozet Archipelago (French Southern and Antarctic Lands – TAAF), both from fishing vessels and along the coast of Possession Island. In this archipelago, killer whales use complex hunting techniques such as intentional stranding on beaches to catch Southern elephant seals3 and are also heavily involved in depredation interactions with the commercial longline toothfish fishery operating offshore4. We plan to use these two phenomena to discriminate divergent behaviours and identify different personalities. Given the general difficulty of approaching these highly mobile predators in the wild, Possession Island and fishing vessels offer a unique opportunity for field based behavioural studies on killer whales.
- Tixier, P., Lea, M. A., Hindell, M. A., Welsford, D., Mazé, C., Gourguet, S., & Arnould, J. P. (2021). When large marine predators feed on fisheries catches: global patterns of the depredation conflict and directions for coexistence. Fish and Fisheries, 22(1), 31-53.
- Guinet, C., Tixier, P., Gasco, N., & Duhamel, G. (2015). Long-term studies of Crozet Island killer whales are fundamental to understanding the economic and demographic consequences of their depredation behaviour on the Patagonian toothfish fishery. ICES Journal of Marine Science, 72(5), 1587-1597
CROZET (TAAF): ETHOLOGICAL ISSUES – ORCAS
Behavioural heterogeneity between killer whale individuals of Crozet will be examined through two types of foraging behaviour: intentional stranding to capture elephant seal pups along the shore of Possession island and depredation of toothfish caught on fishing lines in offshore waters. For both situations, we will use the minimum distance at which killer whales approach an element known to be risky, the shore when hunting seals and the fishing vessel when depredating, to detect boldness and risk-taking variation across individuals. Following a methodology used to identify personality traits in species such as cetaceans, we will visually assess the frequency at which each killer whale individual enters a given distance range to these elements across repeated observations. From Possession Island, observations will be conducted from the shore of Baie Americaine, a major foraging site of killer whales during the elephant seal breeding period (between October and December) and where individuals use intentional stranding to catch seals on the beach (1,2).
- Guinet, C. (1992). Comportement de chasse des orques (Orcinus orca) autour des iles Crozet. Canadian Journal of Zoology, 70(9), 1656-1667..
- Guinet, C., & Bouvier, J. (1995). Development of intentional stranding hunting techniques in killer whale (Orcinus orca) calves at Crozet Archipelago. Canadian Journal of Zoology, 73(1), 27-33.
- Tixier, P., Lea, M. A., Hindell, M. A., Welsford, D., Mazé, C., Gourguet, S., & Arnould, J. P. (2021). When large marine predators feed on fisheries catches: global patterns of the depredation conflict and directions for coexistence. Fish and Fisheries, 22(1), 31-53.
From this site, the duration of an observation will be defined as starting and ending when individuals were first and last sighted, respectively, because either whales moved out of sight or observers had to stop their effort. From fishing vessels, observations will be conducted from the deck during depredation events when killer whales interact with fishing lines (a main line bearing baited hooks with an anchor, surface line and buoy at each end) being hauled by fishers. The duration of an observation will be the time spent hauling one line with which killer whales interacted. Distance ranges will be threefold to a represent a low/medium/high level of risk for killer whales and adjusted to each study platform. Ranges will be monitored when individuals come to the surface and the shortest of these ranges will be recorded as a unique value per individual per observation. From both the shore and the fishing vessels, observers will use an existing photo-identification catalogue to determine the ID of individuals coming to the surface3. This process will be facilitated by the limited number of individuals present during the same observation (on average between 2 and 15 at Crozet) and the limited number of IDs observers will have to be familiar with these whales (n = 89 individuals in the population in 2020). In addition, killer whale identifications will be confirmed through photographs systematically taken during observations, by a second observer from the shore and by fishery observers aboard fishing vessels.
Genetic issues
Context: The fundamental differences between the bull sharks (no parental care, no culture, no teaching, only possible inherited traits are from genetics and epigenetics, and maybe the influence of natal philopatry) and the killer whale (strong social group and family staying together, inter-dependence, teaching and culture) will help understanding the “whys” behind personality.
Objectives: The main objectives of WP3 are to:
- Link the animal behaviour with genetics through the demonstration of heritability of personality traits;
- Explore the molecular mechanisms on which such a heritability relies.
Methods: In order to limit the risk of negative interaction of DNA sampling with the sharks behaviour, we plan to use plyers to directly collect skin samples on the animals’ fins. We may also use spearguns equipped with biopsy probes to collect little tissue samples, as a backup or a complementary approach to ensure the collection of DNA from as many individual as necessary. The same approach will be implemented with killer whales using crossbow. A set of 19 skin Orca samples (corresponding to 18 individuals) are already available for genetic analyses at the CEBC.
A minimum of 12 more biopsies are to be collected during fieldtrips, both from fishing vessels and the shore. DNA samples are conserved in ethanol and sent to France for analysis. For the bull shark model, realized genetic similarities among individuals will be estimated using genome wide DNA polymorphisms. SNPs (single nucleotide polymorphisms) will be obtained using a ddRADseq method that has been successfully applied to this species as already described53.
The RAD library will be sequenced in several Hiseq sequencing lanes to ensure sufficient coverage and to obtain reliable multi-locus genotypes. For the killer whale model, a pedigree reconstruction and relatedness among individuals will be obtained using 30-50 microsatellite loci developed for the species (1).
Coordination
Benoit PUJOL
Responsable du WP
Amélie VIRICEL
Co-responsable du WP
1-Parsons, K. M., Durban, J. W., Burdin, A. M., Burkanov, V. N., Pitman, R. L., Barlow, J., … & Wade, P. R. (2013). Geographic patterns of genetic differentiation among killer whales in the northern North Pacific. Journal of Heredity, 104(6), 737-754.
Societal issues
Work packages 1, 2 and 3 will produce complementary results in terms of demonstrating the existence of personalities among each of the two taxa studied and a better understanding of the mechanisms of PI emergence within these taxa. It will be necessary to integrate these results in order to draw conclusions on two complementary axes: i) one concerning the survival and conservation of the animals, ii) the other concerning the management of the problems that they potentially pose to Humans, with the structuring idea of improving an inescapable co-habitation. The main objectives of WP4 are (for both taxa) to:
- Better understand the modalities (convergent or divergent) of PI emergence;
- Define the consequences in terms of survival (conservation) and management modalities;
- Better understand the current cohabitation dynamics and the potential improvement of this cohabitation between humans and the wildlife concerned
- Morizot B (2016) Les Diplomates. Cohabiter avec Les Loups: Sur une Autre Carte du Vivant. Marseille: Wildproject.
- Rodary E (2019) L’apartheid et l’animal. Marseille: Wildproject.
In addition to the ecological approach, the project will develop a social science approach that will aim to 1) identify the stakeholders involved in interactions with sharks and killer whales and to understand the logic of their practices, and 2) develop, based on this work, a scientific analysis framework that will propose innovative management measures. The identification of stakeholders will seek to characterize the different practices of these actors in their interactions with marine species, i.e. their knowledge, expertise, motivations and strategies. These practices may be economic (fishing, tourism, etc.), political (management of protected species, rules and regulation of marine spaces, etc.), recreational (diving, water sports, ecotourism, etc.), cultural (symbolic aspects of animals, media dimension, etc.) or scientific. These stakeholders therefore involve different actors: industrial or artisanal fisheries, tourism operators, State maritime affairs, marine area managers, tourists, researchers, etc. The objective of the project will be to define the networks of these actors and their role in the conflicts with marine predators in the two case studies. The social science approach stands as symmetrical to the ecological analysis, going beyond a nonspecific because too broad human/predator conflict approach, and able to identifying with accuracy the practices of actors that participate in the construction of these conflicts. This social science approach will furthermore develop a typology of conflicts and the kinds of regulation that are put in place (or not) in each of the two case studies. The objective here is to propose, on the basis of this typology, innovative modes of governance of marine predator species. The project is therefore intended to dialogue with scientists, managers and decision-makers with the aim of co-constructing forms of “diplomacy”1 between humans and marine predators capable of reducing conflicts and proposing new ways of coexistence between species2.
Monitoring Committee
The project intends to set up a follow-up committee which will meet at least once a year, either in person or remotely, in order to examine the adequacy between the project’s objectives and the strategy and means implemented. This committee will be able, if necessary, to suggest new directions in case of unexpected difficulties. It will also be valuable in terms of scientific publications strategy and implementation of the dissemination of the project’s achievements (WP4). The committee will be composed of four scientists internationally recognized in their respective fields of expertise who are Dr. Serge PLANES, CNRS Research Director (H-index 67), specialist in genetics, Dr. Carl MEYER, Associate Professor at the University of Hawaii (H-index 28), specialist in the behavioral ecology of great sharks, Pr Denis REALE, Professor at the Université du Québec à Montréal (H-index 54), specialist in animal ethology, and Dr John LINNELL, senior researcher at the Norvegian Institute for Nature Research (H-index 69), specialist of Human-(terrestrial)Wildlife conflicts.
Serge PLANES
Comité de suivi
Planes, S., & Fauvelot, C. (2002). Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution, 56(2), 378-399.
Carl MEYER
Comité de suivi
Meyer, C. G., Anderson, J. M., Coffey, D. M., Hutchinson, M. R., Royer, M. A., & Holland, K. N. (2018). Habitat geography around Hawaii’s oceanic islands influences tiger shark (Galeocerdo cuvier) spatial behaviour and shark bite risk at ocean recreation sites. Scientific reports, 8(1), 1-18.
Denis REALE
Comité de suivi
Réale, D., Reader, S. M., Sol, D., McDougall, P. T., & Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological reviews, 82(2), 291-318..
John LINNELL
Comité de suivi
Linnell, J. D., Odden, J., Smith, M. E., Aanes, R., & Swenson, J. E. (1999). Large carnivores that kill livestock: do” problem individuals” really exist?. Wildlife Society Bulletin, 698-705.