Mar Biol (2010) 157:537–544 DOI 10.1007/s00227-009-1339-2

ORIGINAL PAPER

Behavioural inertia places a top marine predator at risk from environmental change in the Benguela upwelling system Lorien Pichegru • Peter G. Ryan • Robert J. M. Crawford Carl D. van der Lingen • David Gre´millet

•

Received: 16 January 2009 / Accepted: 30 October 2009 / Published online: 5 December 2009 Ó Springer-Verlag 2009

Abstract In variable environments, organisms are bound to track environmental changes if they are to survive. Most marine mammals and seabirds are colonial, central-place foragers with long-term breeding-site fidelity. When confronted with environmental change, such species are potentially constrained in their ability to respond to these changes. For example, if environmental conditions deteriorate within their limited foraging range, long-lived species favour adult survival and abandon their current breeding effort, which ultimately influences population dynamics. Should poor conditions persist over several seasons, Communicated by S. Garthe. L. Pichegru Centre National de la Recherche Scientifique, DEPE-IPHC, 23 rue Becquerel, 67087 Strasbourg, France L. Pichegru (&)
P. G. Ryan
D. Gre´millet DST/NRF Centre of Excellence at the Percy FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch 7701, South Africa e-mail: [email protected] R. J. M. Crawford Department of Environmental Affairs and Tourism, Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, South Africa R. J. M. Crawford Marine Research Institute, University of Cape Town, Rondebosch 7701, South Africa C. D. van der Lingen Marine Research Institute, University of Cape Town, Rondebosch 7701, South Africa D. Gre´millet Centre National de la Recherche Scientifique, CEFE-UMR 5175, 1919 Route de Mende, 34293 Montpellier cedex 5, France

breeding-site fidelity may force animals to continue breeding in low-quality habitats instead of emigrating towards more profitable grounds. We assessed the behavioural response of a site-faithful central-place forager, the Cape gannet Morus capensis, endemic to the Benguela upwelling system, to a rapid shift in the distribution and abundance of its preferred prey, small pelagic shoaling fish. We studied the distribution and the abundance of prey species, and the diet, foraging distribution, foraging effort, energy requirements, and breeding success of gannets at Malgas Island (South Africa) over four consecutive breeding seasons. Facing a rapid depletion of preferred food within their foraging range, Cape gannets initially increased their foraging effort in search of their natural prey. However, as pelagic fish became progressively scarcer, breeding birds resorted to scavenging readily available discards from a nearby demersal fishery. Their chicks cannot survive on such a diet, and during our 4-year study, numbers of breeding birds at the colony decreased by 40% and breeding success of the remaining birds was very low. Such behavioural inflexibility caused numbers of Cape gannets breeding in Namibia to crash by 95% following over-fishing of pelagic fish in the 1970s. In the context of rapid environmental changes, breeding-site fidelity of long-lived species may increase the risk of local or even global extinction, rendering these species particularly vulnerable to global change.

Introduction Animals face environmental changes, often over relatively short time periods, and their capacity to adapt to these changes determines the fate of their populations (The Red-Queen Hypothesis—Ridley 1994). Ideally, animal

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behaviour should track environmental changes at the same pace. In terms of patterns of environmental change, oceans are more variable than terrestrial habitats (Hunt et al. 1999). Coupled with this, across the world’s oceans, safe breeding sites for species forced to breed on land (birds and some mammals and reptiles) are scarce relative to the large expanses of potential foraging areas. This shortage of island breeding sites has led to the aggregation in colonies of many species during the breeding season (Wagner et al. 2000; Coulson 2002). Central-place foraging by such species imposes time and energy constraints on adults provisioning offspring (Orians and Pearson 1979). If environmental conditions deteriorate, these energetic constraints might influence population dynamics. Most marine species that are land-bound when breeding have developed life-history traits that help them to buffer environmental variability. These include a flexible foraging behaviour (e.g. Weimerskirch et al. 1993; Gre´millet et al. 1998; Iverson et al. 2006), whereby if environmental profitability decreases, breeding adults can increase their foraging effort in an attempt to meet the energy requirements of their offspring (Pinaud et al. 2005; Pichegru et al. 2007). However, should environmental conditions deteriorate beyond a certain threshold, adults typically prioritize their own survival and abandon their current breeding attempt (Erikstad et al. 1998). Many marine mammals and birds return to the same colony for successive breeding attempts. This fidelity to breeding site enhances population persistence in habitats where productivity is predictable from 1 year to another (i.e. temporal autocorrelation in site quality, Schmidt 2004) by allowing individuals to maximize their use of ‘public information’ and to refine their breeding strategies (Boulinier and Danchin 1997; Doligez et al. 2003), while accumulating detailed knowledge of their foraging environment (Gre´millet et al. 1999). In the context of global change, however, if foraging conditions deteriorate consistently for a protracted period, behavioural inertia (such as colony fidelity) may result in animals breeding in lowquality habitats rather than emigrating towards more profitable areas. This inertia may increase the risk of local extinction (Matthiopoulos et al. 2005). Cape gannets (Morus capensis) are colonially breeding seabirds, endemic to the Benguela upwelling system, which prey mainly on sardines (Sardinops sagax) and anchovies (Engraulis encrasicolus) (Berruti et al. 1993). The regional standing stocks of both of these small pelagic species have decreased substantially since the early 2000s (van der Lingen et al. 2006). In addition, an abrupt eastward shift in the spawning distribution of anchovies started in 1996 and has persisted since then (Roy et al. 2007). Over the past decade, there has also been a progressive southward and eastward displacement of sardines away from the

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gannet colony at Malgas Island, South Africa (Coetzee et al. 2008). Adult Cape gannets are faithful to their breeding site (Klages 1994), most of which are situated in the productive Benguela region, which historically supported large pelagic fish population (van der Lingen et al. 2006). Breeding birds could exploit abundant food supplies within close reach (Gre´millet et al. 2004; Adams and Navarro 2005). Eighteenth century maps of Saldanha Bay indicate that a gannet colony has been on Malgas Island for more than 250 years (Burman and Levin 1974). By investigating the foraging behaviour of breeding Cape gannets at Malgas Island over four consecutive years, following the change in anchovy and sardine distribution, we examined how a site-faithful, central-place forager responded to a rapid deterioration of its foraging environment. We hypothesized that local colony site fidelity would keep adult gannets in the same breeding area, and their behavioural flexibility will not compensate for the lack of food, which may have severe demographic consequences.

Materials and methods The foraging behaviour of Cape gannets breeding at Malgas Island, Saldanha Bay (33°030 S, 17°550 E), was studied during four consecutive austral summers (October–January) from 2002/2003 to 2005/2006 under permits issued by South African National Parks. Fish availability and gannet diet The distribution and abundance of the gannets’ preferred prey, sardines and anchovies, were determined from hydroacoustic surveys conducted by Marine and Coastal Management (South African Department of Environment and Tourism) each year from mid-October to the beginning of December. These surveys consist of transects perpendicular to the coast extending from close inshore across the continental shelf to the 200-m isobath, from Hondeklip Bay on the West Coast, 300 km north of Malgas Island, to Port St Johns on the East Coast, 1 200 km east of Malgas Island. Fish densities along transects were estimated using echointegration techniques, and species composition and size frequency distributions of pelagic fish were determined from mid-water trawls (see Barange et al. 1999 for details). Throughout the study, 30–50 gannet regurgitations were collected once a month at Malgas Island following methods described by Berruti et al. (1993). Randomly selected gannets were captured at the edge of the colony with a hook immediately after returning from the sea, and inverted over a bucket, into which they usually regurgitated their stomach contents. The breeding status of birds sampled was not systematically known, but the diets of breeding and

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non-breeding birds do not differ (Berruti 1991). Prey species were identified and weighed and their proportions by mass to the overall diet samples determined for each month. We calculated the average contribution by mass of each prey species for each breeding season (pooling monthly diet samples from September to February, see Crawford 2005). Data logger deployments and analysis of foraging patterns Adults tending small chicks (2–4 weeks old) were equipped with GPS data-loggers (Newbehavior, Technosmart, Rome, Italy), weighing 65 g, about 2% of adult body mass. Birds were caught at their nest site when both partners were present, so that the chick did not stay unattended while its parent was handled, and equipped for a single foraging trip to minimize pseudo-replication. Devices were attached at the birds’ lower back with Tesa tape, minimising damage to the plumage (Wilson et al. 1997). Handling lasted 4– 7 min from capture to release and took place in shade to avoid heat stress, while covering the bird’s head to reduce handling stress. Loggers recorded latitude and longitude at 10 s-intervals, allowing calculation of speed and flight path. When adults returned, they were recaptured and the loggers removed. This technique has been used previously on Cape gannets without any apparent impact on the welfare of the animals (Gre´millet et al. 2004; Pichegru et al. 2007). Foraging range was calculated from GPS positions associated with feeding behaviour [i.e. positions where the birds were flying (speed [ 10 km h-1) and displaying a sinuous path, see details and validation of method in Gre´millet et al. (2004, 2006)]. From these data, the average foraging parameters (trip duration, foraging path length, maximum distance from the nest and time spent flying) and the total foraging area (MCP—Minimum Convex Polygon—100%) used by the birds in each breeding season were assessed. The density of small pelagic fish within the birds’ foraging area was calculated from the annual hydroacoustic surveys using ArcView 3.2 (ESRI). The centres of gravity of the birds’ foraging positions and of the distributions of sardine and the anchovy were calculated for each season. The centre of gravity is represented by a centroid and major axes. The centroid is the weighted mean position of birds’ feeding positions or fish density, and the axes represent the variance of those positions (details in Fairweather et al. 2006a). Energetic modelling and breeding success The energy content of the main prey items of Cape gannets (sardine, anchovy and hakes Merluccius spp. discarded by

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trawlers) was analysed in a bomb calorimeter from samples collected in October 2006. At least 300 g (wet mass) of whole fish, collected from several regurgitations, were analysed for each prey item. No saury (Scomberesox saurus), another main prey species, was found in the diet of the birds in October 2006, so the energy content reported by Batchelor and Ross (1984) was used in calculations. This information was used to calculate the average energetic value of the gannets’ diet for each season. We calculated the metabolic scope [average metabolic rate expressed as a multiple of basal metabolic rate (BMR)] of adult Cape gannets provisioning chicks following Enstipp et al. (2006). This model establishes time-energy budgets, taking account of the BMR and the energy expenditure associated with different behaviours (Adams et al. 1991), the energy requirements of the chicks (R. Navarro, unpublished data), time-budget information from our data logger recordings and the average adult body mass (2,600 g, Crawford 2005). Cape gannet breeding success at the Malgas colony was assessed for each breeding season via monthly and bimonthly checks (at the beginning and towards the end of the season, respectively) of nests marked throughout the colony from egg-laying (September) until fledging (February of the following year). Statistical analyses We performed a balanced ANOVA on normally distributed variables (after square-root transformation) with equal variance, with bird foraging parameters as response variables and the main diet in a given period (‘A’ or ‘B’) as the explanatory variable. Periods were defined according to the percentage contribution by mass of sardine and anchovy to the diet of the birds: period A when these prey contributed to [50% of their diet (seasons 2002/2003–2003/2004) and period B when they formed \25% (seasons 2004/2005– 2005/2006). Non-normally distributed variables were analysed using Kruskal–Wallis tests. The threshold for statistical significance (a) was 5%.

Results A total of 96 GPS tracks and 1,161 stomach regurgitations were collected from Cape gannets over the four consecutive breeding seasons. There were clear differences in the foraging behaviour of the birds between these breeding seasons. Average foraging trip duration was 20.7 h for the first two seasons (period ‘A’), increasing to 30.2 h during the last two seasons (period ‘B’) (Table 1). In concert with this, the average length of the foraging path increased steadily from 369 km in 2002/2003 to 514 km in 2005/

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Table 1 Foraging parameters, foraging area, reproductive success, average daily metabolism (as a multiple of BMR) for breeding Cape gannets (Morus capensis) at Malgas Island, South Africa, and

abundance of sardines (Sardinops sagax) and anchovies (Engraulis capensis) separately, and then summed as small pelagic fish, in the birds’ foraging range between 2002/2003 and 2005/2006

Season (and period)

2002/2003 (A)

2003/2004 (A)

2004/2005 (B)

2005/2006 (B)

Significance

N (GPS tracks)

26

20

14

36

ND

Trip duration (h)

23.1 ± 9.7 (3.3–47.9)

18.3 ± 13.2 (4.7–48.0)

31.3 ± 14.1 (6.8–51.2)

29.1 ± 12.7 (4.7–55)

***

Path length (km)

368.6 ± 200.2 (84.9–955.9)

412.7 ± 323.1 (107.5–1,322.2)

476.9 ± 199.5 (186.5–855.5)

514.4 ± 234.8 (130.0–1,085.5)

**

Maximum distance from colony (km)

105.8 ± 59.0 (16.8–241.5)

114.5 ± 82.7 (27.6–324.7)

122.8 ± 55.9 (34.9–225.6)

132.6 ± 62.7 (31.5–303.0)

NS

Time spent flying per trip (h)

7.96 ± 2.66 (2.7–15.8)

5.01 ± 4.55 (0.9–17.8)

9.39 ± 4.04 (3.9–17.1)

10.13 ± 4.48 (2.4–22.0)

***

% Of time spent flying per trip

38.1 ± 14.2 (20–80)

28.0 ± 11.9 (10–50)

32.5 ± 10.7 (15–61)

36.3 ± 10.7 (10–73)

NS

Foraging area (km2)

9,000

6,900

13,700

14,300

ND

Breeding success (chicks fledged per pair)

0.43

0.42

0.42

0.02

ND

Percentage of small pelagic fish in gannet diet

73.4

55.3

23.8

13.7

ND

Average daily metabolism (9BMR)

4.32

4.33

4.45

4.70

ND

Abundance of sardines (g m-2)

19.5 ± 64.9

45.6 ± 108.6

7.3 ± 21.7

4.3 ± 26.6

ND

Abundance of anchovies (g m-2)

12.8 ± 28.5

17.4 ± 36.7

3.0 ± 10.2

16.8 ± 45.5

ND

Abundance of small pelagics (g m-2)

32.3 ± 68.5

63.0 ± 124.6

10.3 ± 26.3

21.4 ± 52.5

ND

Values are mean ± SD NS not significant, ND not determined * P \ 0.05, ** P \ 0.01, *** P \ 0.001

2006 (Table 1). There was also a clear movement of sardine and anchovy to the south and east during the study period, and a large decrease in the abundance of small pelagic fish (sardines and anchovies combined) in the gannets’ foraging range (Fig. 1; Table 1). Nonetheless, gannets did not change their main foraging area during our studied period, as shown from the centres of gravity and the polygons of their entire foraging positions (MCP 100%) from years when they fed predominantly on natural prey (2002/2003 and 2003/2004) compared to subsequent years (2004/2005, 2005/2006; see below, Fig. 1), although there was a tendency for birds to feed farther south in 2003/2004 than in other seasons (Fig. 1). The birds appeared to follow the south and eastward movement of sardine and anchovy in 2003/2004, but as these species became ever more distant from the colony the gannets shifted their foraging ranges north and west in 2004/2005 and 2005/2006 (Fig. 1). This shift in the foraging dispersion of the gannets coincided with a switch in diet from pelagic shoaling fish to fishery discards (hake—Berruti et al. 1993) and saury (Fig. 2). The hake fishery from which the birds scavenged operates mainly along the continental shelf edge north of Malgas Island (Fairweather et al. 2006b). In 2002/2003 and 2003/2004, the average density of small pelagic fish within the birds’ foraging range was 48.7 g m-2, and in these

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years sardine and anchovy together made up more than 50% of their diet. This value decreased to \25% in 2004/ 2005 and 2005/2006, when the average density of small pelagic fish fell to 15.9 g m-2. The mass-specific energetic reward gained from saury and hakes is 25% less than that of sardine and anchovy (Table 2). During seasons of low prey availability (period B), when small pelagic fish comprised less than 25% of the gannets’ diet, the birds’ foraging effort increased significantly (Fig. 3). Foraging trips lasted longer (H1.96 = 11.93, P \ 0.001) and covered greater distances (F1.96 = 7.51, P \ 0.01). However, the birds did not increase the proportion of time spent flying per trip (H1.96 = 1.47, P = 0.225), or their maximum foraging distance form the island (F1.96 = 3.57, P = 0.067), which is confirmed by their centres of gravity being located in the same broad area (Fig. 1). Although foraging behaviour differed between years, average metabolic demand increased by just 8% between the 2002/2003 and 2005/2006 seasons (Table 1). Despite this, the gannets’ predicted metabolic rate was consistently [4 9 BMR. During the 2005/2006 season, when the birds’ energy expenditure was greatest and the density of pelagic fish in their foraging range was very low, the gannets’ reproductive success was an order of magnitude lower than in previous years, falling to only one chick per 50 pairs (Table 1).

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541

Fig. 1 Centres of gravity of the foraging positions of Cape gannets (Morus capensis) breeding on Malgas Island, South Africa, during the four consecutive breeding seasons from 2002/2003 to 2005/2006, and their foraging areas (MCP 100%) during periods ‘A’ and ‘B’ (see ‘‘Results’’ for details). The centres of gravity, with their variances, and average density of sardines and anchovies off the South African coast are also shown, as well as the 200- and 1,000-m isobaths

Fig. 2 Percentage contribution by mass of the five main food items in the diet of Cape gannets (Morus capensis) from Malgas Island, South Africa, during four consecutive breeding seasons

100

Percentage (%)

80

60

40

20

0

2002/03

other

Discussion During the study period, Cape gannets faced a situation in which their favoured, natural prey became increasingly scarce (Fig. 1). Breeding Cape gannets were sufficiently flexible in their foraging behaviour to increase foraging effort during years when natural prey were scarce (Fig. 3), although the benefits of this did not necessarily translate to successful reproduction. In the 1980s, prior to deterioration of the food supply, artificial twinning experiments

2003/04

saury

hake

2004/05

sardine

2005/06

anchovy

demonstrated that some gannets were able to raise two chicks (Navarro 1991). At the same time, foraging trips of gannets from Malgas Island lasted \10 h (Adams and Navarro 2005), 34–55% of the average duration of trips during 2002–2005 (Table 1). During our study, gannets probably reached their maximum working capacity, as their metabolic rate was consistently estimated [4 9 BMR (Table 1), at the limit to sustained energy expenditure by breeding birds (Drent and Daan 1980). Gannets were unable to increase their energy expenditure any further

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Table 2 Energetic content of the dry mass (in kJ g-1) of the main prey of Cape gannets (Morus capensis) from Malgas Island, South Africa Energetic content (kJ g-1) Sardine (Sardinops sagax)

7.0

Anchovy (Engraulis encrasicolus)

7.2

Hake discards (Merluccius sp.) Saury (Scomber scombrus)

5.5 6.2

(Table 1), which prevented them from extending their foraging range to follow the eastward shift in their prey (Fig. 3). The same constraint has been documented for black-browed albatrosses (Diomedea melanophris) from the Kerguelen Islands which also did not extend their foraging range during years of low prey availability, probably because they were working at their maximum capacity (Weimerskirch et al. 1997). Remaining largely within the same foraging range, gannets fed on fishery discards when pelagic fish were scarce (Fig. 2), demonstrating further flexibility in foraging behaviour. However, although the birds can adapt their diet (Fig. 2, Berruti et al. 1993), their population dynamics are linked to the availability of their preferred prey (Crawford 1999; Crawford et al. 2008). When fed predominantly on low-energy fishery discards, gannets chicks survival was extremely low (Gre´millet et al. 2008). Breeding success was low throughout our study (Table 1) in comparison to previous studies performed at the same breeding site (e.g. 0.69 ± 0.07 chicks fledged per pair during 1986–1988, Navarro 1991). During 2005/2006, Fig. 3 Foraging parameters of breeding Cape gannets (Morus capensis) from Malgas Island, South Africa, during periods ‘A’ or ‘B’, i.e. their diet comprised [50 or \25% of combined sardines and anchovies, respectively. Values are mean ± SE

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when parental energy expenditure was greatest and the density of preferred fish was very low within the gannets’ foraging area, breeding failure was almost complete (Table 1) even though hatching success averaged 82% (Staverees et al. 2008). This result may have been exacerbated by low food availability the previous season (Table 1). In 2005/2006, when high-quality food was scarce, gannets probably acted as prudent parents, favouring their own survival over that of their growing young (Erikstad et al. 1998). It seems, therefore, that even though gannets did exhibit flexibility in both foraging behaviour and diet, this was insufficient to cope with the magnitude of environmental change. When long-lived birds are faced with tenuous energy budgets during the breeding season, a primary strategy is to reduce breeding frequency (Erikstad et al. 1998). However, if poor breeding conditions persist, predators should emigrate to follow their prey (the Red-Queen hypothesis, Ridley 1994). In the southern Benguela, the eastward shift of sardines has persisted for several years (Coetzee et al. 2008). There are possible islands closer to these pelagic fish stocks than is Malgas, yet gannets at Malgas Island remain faithful to their breeding site, despite their population steadily decreasing (Crawford 2007, Marine and Coastal Management, unpublished data). Because the entire population of Cape gannets breeds at only six sites, this very strong site fidelity renders the species vulnerable to demographic collapse and even local extinction (Kristan 2003; Matthiopoulos et al. 2005). Such demographic collapse has occurred previously. Facing severe depletion of sardine and anchovy off Namibia in the 1960s, most Cape gannets persisted in breeding at three traditional localities,

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although some young gannets apparently recruited to colonies off the South African West coast (Crawford 1999). As a consequence, the Namibian gannet population decreased by 95% between 1950 and 2005, and shows no evidence of recovery (Crawford 2007). Cape gannets are now classified as vulnerable (IUCN 2006). During our 4year study, the numbers of breeding gannets at the Malgas Island colony (the world’s second largest [Crawford 2005]) decreased by 40% (Marine and Coastal Management, unpublished data). The cause of the distributional shift of the sardine population off South Africa remains unclear (Coetzee et al. 2008). Roy et al. (2007) suggested that the abrupt eastward shift in anchovy in 1996 resulted from a sudden rather than a gradual change in environmental conditions. Such a rapid change in the distribution of small pelagic fishes reflects their dependence on short, plankton-based food chains, plankton themselves being highly sensitive to changes in oceanographic conditions (see Bakun 2006). Species that are short-lived (Berteaux et al. 2004) with the potential for quick genetic turnover (Peters and Lovejoy 1992) or a capacity to modify their distributional range (Oro et al. 2004) are better adapted to cope with rapid environmental change. Given the high reproductive output, short lifespan and mobility of most small pelagic fish, it is unsurprising that they reacted rapidly to the changing environmental conditions. However, one level higher up the food chain, long-lived, slow-reproducing, site-faithful birds such as gannets may seemingly take years to respond to such distributional shifts, assuming there are appropriate resources available (e.g. suitable breeding sites) (Kokko and Sutherland 2001). There are several examples of severe decreases in seabird populations following prolonged scarcity of small pelagic prey due to either environmental changes and/or overfishing (e.g. Furness and Tasker 2000; Frederiksen et al. 2004; Crawford 2007). The combined effects of rapid climate change and industrial-scale fishing have greatly increased the pace at which the marine environments change (Jackson et al. 2001; Pauly et al. 2002; Parmesan 2006). Under evolutionary time-scales, rates of change favoured short-term conservatism with medium-term flexibility, i.e. mediated through parental fidelity but scope for emigrating recruits (Doligez et al. 2003). However, rate of change is now so rapid that parental conservatism is maladaptive. Colonial, island-breeding top predators may be unable to adapt to rapid, unidirectional environmental change at the same rate as smaller species lower in the food chain on which they depend. In the future, we can expect an increasing frequency of spatial mismatches between these top predators and their prey, possibly resulting in local predator extinction.

543 Acknowledgments This study was funded by a studentship of the French Ministry of Research to LP, by the Centre National de la Recherche National via an ACI jeunes chercheuses et jeunes chercheurs to DG and by the DEPE-IPHC-CNRS. We thank South African National Parks for granting access to protected areas and the University of Cape Town for transport and logistic support. Marine and Coastal Management kindly provided logistical support in the field. We warmly thank P
H.R. Hockey, C. Gilbert and M. Enstipp and three anonymous referee for scientific input, and R. Navarro, J.P. Robin, L. Phiegeland, L. Drapeau, T. Fairweather, J. Coetzee, S. Lewis, G. Dell’Omo, S. Sari, J. Fort and R. Mullers for essential help in gathering and analysing the data.

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