Polar Biol (2017) 40:365–378 DOI 10.1007/s00300-016-1964-4

ORIGINAL PAPER

Important marine sectors for the top predator community around Kerguelen Archipelago

1 1 1 1 Laurie Thiers • Karine Delord • Charles-Andre´ Bost • Christophe Guinet • Henri Weimerskirch1

Received: 29 September 2015 / Revised: 22 April 2016 / Accepted: 10 May 2016 / Published online: 1 June 2016 Ó Springer-Verlag Berlin Heidelberg 2016

Abstract The French Kerguelen Archipelago represents Introduction an important breeding place for many species of marine top predators within the Southern Ocean, making the plateau Over the last century, marine organisms have faced an hosting the archipelago and surrounding waters (CCAMLR increasing number of threats such as climate change, pol- area 58.5) a crucial area to design conservation measures. lution, overfishing or introduced species (Derraik 2002; In this study, available tracking data from nine species of Bax et al. 2003; Coll et al. 2008; Hoegh-Guldberg and seabirds and marine mammals breeding at Kerguelen were Bruno 2010; Paleczny et al. 2015). Because of these fast analysed to define potential boundaries for a Marine Pro- changes, marine ecosystems are now undergoing important tected Area. Maps of time spent per square of each species disruptions (Halpern et al. 2008) that are likely to increase were first used to describe high-use areas within the Ker- in the near future, possibly leading to global marine bio- guelen Plateau. Habitat models were then developed for diversity loss (Cheung et al. 2009; Kolbert 2014). Conse- four species (Black-browed albatross, Wandering albatross, quently, it has become essential to identify persistent areas and ) chosen on the basis of of species concentration to design effective conservation their contrasted foraging ecology and diet to represent the measures. top predator community. Predictive models were then Setting up Marine Protected Areas (MPAs) has become applied to the main colonies of the four species for which a central part of marine conservation programmes (Bou- no tracking data were available to illustrate the most douresque et al. 2005; Can˜adas et al. 2005; Harris et al. important feeding areas at the scale of the entire study 2007). However, convincing the decision makers to design zone. An area delineated by the central part of the plateau MPAs remains the critical point and, to do so, prioritising and its slopes appeared to be of great importance for the top areas that require special protection is the first stage. To predators’ community and would appropriately complete tackle this issue, designation of biodiversity hotspots has the limits of the existing Australian marine reserve of been increasingly used (Mittermeier et al. 1998; Myers Heard and McDonald Islands. et al. 2000; Worm et al. 2003). This strategy is based on the identification of areas where a large number of endemic Keywords Distribution Á Habitat modelling Á Tracking Á species under conservation concern concentrates (Myers Seabirds Á Marine mammals 1988). The distribution of easily observable species such as mammals or birds is often considered as a good predictor Electronic supplementary material The online version of this of the location of others taxa on which they feed or asso- article (doi:10.1007/s00300-016-1964-4) contains supplementary material, which is available to authorized users. ciate (Reid 1998; Bost et al. 2009). These species often showed habitat preferences that encompass those of their & Laurie Thiers preys. As a consequence, top predators are preferred can- [email protected] didates in the identification of biodiversity hotspots. 1 Centre d’E´ tudes Biologiques de Chize´, UMR 7372 du CNRS- Here we studied the distribution of a community of Universite´ de La Rochelle, 79360 Villiers en Bois, marine top predators (high trophic level species) breeding 123 366 Polar Biol (2017) 40:365–378 on the in the sub-Antarctic area of the Pygoscelis papua (GEPE) and Macaroni southwestern Indian Ocean. This archipelago is located on penguin Eudyptes chrysolophus (MAPE); and pinnipeds: an extensive continental shelf, providing major bathymetric Antarctic fur seal Arctocephalus gazella (ANFS) and obstruction to the eastward flow of the Antarctic Circum- Southern elephant seal Mirounga leonina (SESE). The polar Current (ACC), significantly steering and channelling selected species are large ones that can be fitted with log- most of the deep-reaching ACC flow (Park et al. 2008; gers to track their movements and are common within the Sokolov and Rintoul 2009; Park and Vivier 2011). The study area, although Kerguelen is also used as a breeding juxtaposition of different water masses delimited by the area by other predator species (see Weimerskirch et al. Front, Polar Front and Southern ACC Front 1989). (Park et al. 2009), together with iron enrichment from the Individuals were equipped with a global positioning island and the peri-insular shelf (Blain et al. 2001, 2007), system (GPS) or ARGOS Platform Terminal Transmitters creates highly productive areas downstream of the plateau. (PTT), and all data used in this study were collected during As a highly productive and isolated structure within the the breeding season of the species except for the SESE, Southern Ocean, the Kerguelen Plateau hosts very high which were equipped during their post-breeding stage abundances of marine predators, including penguins, pet- (Online Resource 2). All species tracked during their rels and seals (Weimerskirch et al. 1989; Hindell et al. breeding period are central place foragers that regularly 2011). Kerguelen lies within the CCAMLR area of Ker- perform trips between foraging grounds and breeding sites guelen and Heard and McDonald Islands (CCAMLR area where they incubate their eggs or provision their young. All 58.5.1 and 58.5.2), where conservation measures should be birds were captured at nest by hand and tracking devices taken to protect the marine environment and could com- were fixed to the back feathers using TesaÒ tape (more plete the MPA that was declared in the Australian sector details in Weimerskirch et al. 2000) for flying birds and around Heard and McDonald Islands in October 2002 additionally, Loctite glue for penguins (Lescroe¨l and Bost (AAD 2005). Here, we used a long-term data set for nine 2005). Tracking data of WAAL from the nearby Crozet different top predator taxa from high-level trophic guilds Archipelago that foraged in the Kerguelen/Heard Plateau and various conservation statuses tracked during the were also included. Female SESEs were captured with a breeding season. First, we mapped the distribution for these canvas head-bag and anaesthetised before deployment of a species using telemetric data collected over two decades. In conductivity-temperature-depth instrument combined with a second step, four of the nine species were selected on the an ARGOS satellite transmitter (ARGOS-CTD) that was basis of their various diets and foraging behaviour to pre- fixed on the animal’s head (more details in Guinet et al. dict their distribution within the study area by developing 2014). Female ANFSs were captured using a hoop net and habitat models and applying the results to the main known restrained on a board before being equipped with a PTT breeding colonies, including those where no data were (more details in Guinet et al. 2001). The species studied available. Finally, using these predictions, we drew up a here have different foraging behaviours and diets. WAAL preliminary global map of the important at-sea areas for forages mostly on squids and fish (Weimerskirch et al. several marine top predators of the Kerguelen Archipelago. 1997a), alternating between short trips near the colony and long trips to pelagic waters (Weimerskirch et al. 1993). BBAL is a neritic forager that mainly feeds on fish and Methods cephalopods (Cherel et al. 2000). During the chick rearing period when they were tracked, WCPE alternated between Study species short (1–3 day) foraging trips over the Kerguelen/Heard Plateau and long trips commuting over distant Antarctic The study area corresponds to the French Kerguelen waters (5–20 days) (Pe´ron et al. 2010). Here we only Archipelago and the Australian Heard and MacDonald included short foraging trips over the Kerguelen shelf. Islands and surrounding waters (CCAMLR areas 58.5.1 KECO performed short-range foraging trips, with deep and 58.5.2). dives to access benthic fish (Cook et al. 2010). The diet of Tracking data were collected on nine species of top GEPE is mainly composed of neritic fish and crustaceans predators breeding at the Kerguelen Islands (Online (Lescroe¨l et al. 2004), preyed upon during shallow dives of Resource 1) including flying seabirds: Wandering albatross a few tens of metres (Lescroe¨l and Bost 2005). MAPE is Diomedea exulans (WAAL), Black-browed Albatross also a shallow diver, rarely exceeding 60 m to feed on Thalassarche melanophris (BBAL), White-chinned petrel euphausiid and myctophid fish (Green et al. 1998). KIPE Procellaria aequinoctialis (WCPE) and Kerguelen shag performed deep dives to access myctophid fish (Bost et al. Phalacrocorax verrucosus (KECO); flightless diving sea- 1997a, 2002) and ANFS also foraged on myctophid fish birds: King penguin Aptenodytes patagonicus (KIPE), (Cherel et al. 1997) during shallower dives (Lea et al. 2002). 123 Polar Biol (2017) 40:365–378 367

SESE forages mainly on myctophid fishes in the vicinity of Environmental variables were then extracted for both the Polar Front (Cherel et al. 2008) during extremely deep cells where animals were present and pseudo-absences. We dives (Hindell et al. 1991). used monthly composite environmental variables that were downloaded from the NOAA Coastwatch satellite (http:// coastwatch.pfeg.noaa.gov/erddap/griddap/index.html) and Distribution aggregated on a 0.25° cell grid. Dynamic variables were the chlorophyll a concentration (Chloa), sea surface tem- For each track, the start and end dates of foraging trips perature (SST), sea level anomaly (SLA) and associated were visually identified. On-land locations were then gradients; fixed variables were bathymetry (Bathy) and its excluded to avoid the overweighting of colonies in subse- gradient (Bathy_grad) and distance to the colony (DCol). quent analyses. An iterative backward/forward speed filter We used functions of the Biomod2 package to build routine was then applied to remove unrealistic locations ensemble modelling for each species of our chosen panel (McConnell et al. 1992). (Thuiller et al. 2013). As Biomod2 does not allow the The study area was divided into grid cells of inclusion of individuals as a random effect, we preliminarily 0.25° 9 0.25°, based on the resolution of the environmental checked for the capability of our available set of individuals data used for habitat modelling. Using the R package ‘‘trip’’, to represent the whole species distribution as extrapolations time spent per square (TSPS) was calculated as the total made from an insufficient number of individuals could be amount of time spent by an individual in each cell of the grid misleading (Gutowsky et al. 2015). To do this, for each during a foraging trip. These values were then standardised species, we ran 1000 random trip selections for different within species as the proportion of total trip duration spent in steps, from five trips to the total numbers of trips available, each cell of the grid in order to make trips comparable. and for each of these steps we calculated the numbers of Finally, the TSPS values obtained for each species were visited cells according to the number of trips considered summed, each species having the same weight, to highlight (Online Resource 4–7). If an asymptote is reached, it can be the most used zones over the study area. assumed that the number of individuals available is sufficient to represent the whole distribution of the species and that the Habitat modelling pattern observed is not biased toward individual strategies (Hindell et al. 2003). BBAL and KIPE presented a sufficient We used data from four of the nine species to represent foraging number of trips, as an asymptote can be observed showing areas, selected on the basis of their diet (demersal, benthic or that individuals present an overlap in their distribution range pelagic fish, macrozooplankton, squids), foraging behaviour (Online Resource 5 & 7), whereas it is less clear in WAAL (flying vs. diving species, neritic vs. oceanic), foraging range and ANFS, meaning that the results of model predictions for (wide enough to cover the study area) and the large sample size these two species could potentially be underestimated of the data sets in order to provide the most comprehensive (Soanes et al. 2013). approach of the top-predator community. These species were Biomod2 is a powerful tool as it allows the use and namely: WAAL (only individuals breeding in Kerguelen combination of nine modelling techniques: GLM, GAM, Archipelago were considered for model development), BBAL, RF, ANN, MARS, SRE, GBT, CT and FDA (see Hegel KIPE and ANFS. To validate the choice of this panel of species, et al. 2010 for review). The ensemble modelling developed using the Istat function of the SDMTools package, we per- in this package is particularly interesting for undertaking formed an I similarity test based on pair-wise differences multi-specific habitat modelling as the choice of a unique between the distribution of the standardised TSPS values for the model is often made difficult by the various shapes of four and nine species (Warren et al. 2008). As the value response that different species are likely to show. Biomod2 obtained showed a high degree of overlap between the two allows taking into account this potential inter-model distributions (I = 0.91), we considered the use of this panel variability. suitable to represent the whole community. For each species, we preliminarily calibrated all mod- Since tracking data only provide presence data, we elling techniques based on their predicting performance. selected pseudo-absences to provide a set of available Each modelling technique was then run 50 times and only conditions to the model with the aim to better understand models with ROC (receiver operating characteristic) values the parameters shaping presence records. For each trip, we over 0.70, considered as acceptable performance (Hosmer generated pseudo-absences by randomly choosing a num- and Lemeshow 2000), were kept to calculate the average ber of absence data equal to the number of presence data model. Predictions were finally calculated using parameters within cells that were not used by the given individual in an weighted on the basis of the performance of each remain- area delimitated by the mean maximum range of the spe- ing model. Using predictions calculated for each of the four cies during the breeding season (Online Resource 3). species on the climatology of the month of January 123 368 Polar Biol (2017) 40:365–378

(breeding period of all studied species) covering the whole Plateau, along the shelf break. The TSPS highest values study period, a map of mean presence probability was then occurred on the eastern and southern slopes close to the colony. generated to determine the common areas used during the breeding season. These predictions were then applied to the WCPE WCPEs performed trips mainly directed toward main known colonies where no tracking data were avail- the southeast and most of the present cells are restricted to able and summed for each of these species. The final map the peri-insular plateau (Online Resource 9). The area that was realised by summing the four species probabilities, was the most visited by birds tracked is located southward each species having the same weight. from the colony at the intersection of the Polar Front and the shelf break of the plateau.

Results KECO KECOs presented very short-range foraging trips (in the order of 8 km for the longest trip) that were per- At-sea distribution formed in a few hours (Online Resource 10). Thus, all tracks recorded were restricted to the colony cell. Flying seabirds Flightless diving seabirds WAAL WAALs tracked from both Kerguelen and Crozet Archipelagos were present in the study area. Individuals KIPEs Breeding KIPEs from the East Courbet Peninsula breeding at Kerguelen performed large oceanic foraging performed trips that were mainly directed toward the trips, often moving beyond the boundaries of this zone. southeast (Fig. 3). Most of them were located on the They are spread over a wide part of the study area, Kerguelen/Heard Plateau. The highest values of time spent although the southern and western parts are less used per square mostly occurred between the colony and the (Fig. 1). WAALs use shelf edges of the Kerguelen/Heard Polar Front, particularly in the area of the cold water flow Plateau intensively, concentrating the highest values of along the eastern part of the Kerguelen/Heard Plateau. time spent per square mainly in the northern and eastern part of the plateau. The vicinity of the colony is of course MAPE Most of MAPE breeding trips were directed highly used by birds commuting between the colony and toward the southeast (Online resource 11). They foraged foraging zones. Individuals from Crozet commuted over both over and outside the insular plateau. Time spent per long distances to forage in the northern and northwestern square was higher on the Polar Front, near the colony and part of the Kerguelen/Heard Plateau (Online Resource 8). offshore, eastward from the colony, in the cold water tongue from the ACC. BBAL BBALs were widely distributed over the study area, performing foraging trips all around the Kerguelen mainland GEPE GEPEs showed coastal foraging trips (Online (Fig. 2). Birds mainly concentrated on the Kerguelen/Heard Resource 12). Cells where individuals were present are

Fig. 1 Standardised time spent per square (TSPS) from Wandering albatross Diomedea exulans (WAAL) tracking data. Contours of the Kerguelen/ Heard Plateau, colony (green point), exclusive economic zones (solid lines) and fronts (PF Polar Front, SAF Sub- Antarctic Front, STSF Southern Sub-Tropical Front) (dashed lines) are represented

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Fig. 2 Standardised time spent per square (TSPS) from Black- browed albatross Thalassarche melanophris (BBAL) tracking data. Contours of the Kerguelen/ Heard Plateau, colony (green point), exclusive economic zones (solid lines) and fronts (PF Polar Front, SAF Sub- Antarctic Front, STSF Southern Sub-Tropical Front) (dashed lines) are represented

Fig. 3 Standardised time spent per square (TSPS) from King penguin Aptenodytes patagonicus (KIPE) tracking data. Contours of the Kerguelen/ Heard Plateau, colony (green point), exclusive economic zones (solid lines) and fronts (PF Polar Front, SAF Sub- Antarctic Front, STSF Southern Sub-Tropical Front) (dashed lines) are represented

comprised between the colony and eastward 500 m line peri-insular plateau of the Kerguelen Archipelago. Individ- slope of the plateau. uals from the Kerguelen mainland eastern colonies showed trips directed toward the southeast. On the contrary, indi- Pinnipeds viduals tracked from the colony of northwest Iles Nuageuses showed trips directed westward. The highest values of time SESE During the post-breeding season, after the weaning spent per square occurred close to the colonies and on the of the pups, female SESEs performed long foraging trips bathymetric slope, west of these colonies. broadly exceeding the study area boundaries. They dis- persed widely around Kerguelen Archipelago, mostly All species combined toward the south and east (Online Resource 13). A very few trips crossed the Sub-Antarctic Front. The vicinity of The highest TSPS values occurred in the vicinity of the the colony, at the 500 and 200 m line slope of the plateau, eastern island’s coasts (Fig. 5). High values also occurred concentrated the highest TSPS values for SESE. over the low bathymetry area, in the southeastern part of the Kerguelen/Heard Plateau, and to a lesser extent over oceanic ANFS ANFSs were tracked from three different colonies waters eastward from the plateau. Most of these values are (Fig. 4). They foraged indifferently over and outside the comprised between Kerguelen’s coasts and the Polar Front.

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Fig. 4 Standardised time spent per square (TSPS) from Antarctic fur seal Arctocephalus gazella (ANFS) tracking data. Contours of the Kerguelen/ Heard Plateau, colonies (green point), exclusive economic zones (solid lines) and fronts (PF Polar Front, SAF Sub- Antarctic Front, STSF Southern Sub-Tropical Front) (dashed lines) are represented

Panel species (WAAL, BBAL, KIPE, ANFS) WAAL

The map of TSPS of the four species (Fig. 6) showed a highly Predictions from the WAAL ensemble model are concen- similar pattern to the map of all species combined (Fig. 5), as trated over the Kerguelen/Heard Plateau and the sur- it was highlighted by the I similarity test. The four species are rounding oceanic waters, especially in the eastern part of distributed over a wide extent in the study area. The highest the study area (Fig. 7a), with the highest values located values are concentrated in the vicinities of the southeastern along the bathymetric slopes of the plateau. The variables coasts of the archipelago, mainly above the Polar Front. explaining WAAL presence predictions are, in the order of importance, DCol, SST and Chloa_grad (Online Resource Predictions 14). The ROC evaluation of the model is very good, with a value of 0.97 (Online Resource 15). Presence probability predictions were generated for four of The model predictions projected on WAAL from the the studied species (WAAL, BBAL, KIPE and ANFS). To other main colony of the Kerguelen Archipelago, located investigate the colony effect on these species distribution, on the western coast of the island, are very similar to we also modelled predictions for each species’ major those from the eastern colony (Fig. 7b). The highest colonies for which telemetric data were not available. valuesoccurredmainlyontheplateauandalongits

Fig. 5 Sum of the standardised time spent per square (TSPS) from all species tracking data. Contours of the Kerguelen/ Heard Plateau, exclusive economic zones (solid lines) and front zones (dashed lines) are represented

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Fig. 6 Sum of the standardised time spent per square (TSPS) from panel species (WAAL, BBAL, KIPE, ANFS) tracking data. Contours of the Kerguelen/ Heard Plateau, exclusive economic zones (solid lines) and front zones (dashed lines) are represented

Fig. 7 Predicted presence probability for Wandering albatross (WAAL) from a Pointe Morne colony, b Grande Coule´e colony and c Crozet Island. Contours of the Kerguelen/Heard Plateau (solid lines) and Polar Front (dashed lines) are represented 123 372 Polar Biol (2017) 40:365–378 slopes. Similarly, predictions for WAAL from Crozet ANFS Island, which is located west from Kerguelen, highlight a high use of the northern part of the Kerguelen Plateau ANFSs from Pointe Suzanne colony are predicted to be (Fig. 7c). present mostly in the middle part of the Kerguelen/Heard Plateau and in the surrounding oceanic waters, with the BBAL highest values along the eastern and western slope (Fig. 10a). The parameters driving this pattern are DCol, The ROC value associated with the model developed for SLA and SST (Online Resource 14). The model evaluation BBAL is 0.95, demonstrating that this model is highly is good (ROC value: 0.95), revealing a very good predic- relevant (Online Resource 15). The highest values are tion ability (Online Resource 15). located in the middle part of the Kerguelen/Heard Plateau, When applied to the second main colony of ANFS, in in the vicinity of the Canyon des Sourcils Noirs colony, Iles Nuageuses, northwest from Kerguelen, predicted along the western and eastern shelf edges and, to a lesser presence occurred mostly in the eastern part of the study extent, over oceanic waters near these slopes (Fig. 8a). The area, with the highest values along the slope of the plateau most important parameter driving BBAL presence is DCol and, to a lesser extent, along the eastern slope, close to the (Online Resource 14). Kerguelen mainland (Fig. 10b). When applied to the two main other colonies of BBAL in the Kerguelen/Heard Plateau, namely Cap Panel species (WAAL, BBAL, KIPE, ANFS) Franc¸ais and Heard and McDonald Islands, predicted probabilities show a very contrasted pattern between The highest probabilities occur in the central part of the the colonies, which are respectively located in the plateau and along the eastern and western slopes (Fig. 11). northwestern part of Kerguelen and in the Australian Most of the high values are located between the eastern island of Heard, in the southern extremity of the plateau coasts of Kerguelen and the Polar Front. The Sub-Antarctic (Fig. 8b, c). Predictions for these two sites showed very Front marks the northern limit of the predicted presence little overlap, but both sites share the same pattern as probabilities of the area. Some high presence probabilities predictions from Canyon des Sourcils Noirs, with the are predicted outside the plateau and are mostly located in highest values concentrated in the plateau and along the the eastern part of the study area. Values show a quite high shelf edges. overlap between habitats suitable for these four species.

KIPE Discussion Presence probabilities for KIPE appear to be mostly concentrated between Ratmanoff colony, located on the The Kerguelen/Heard Plateau represents one of the few eastern cost of Kerguelen, and the limit of the Polar bathymetric obstructions to the ACC, leading to a local Front (Fig. 9a), especially in the eastern part of the upwelling and enrichment in iron from the land masses plateau with some extensions in more oceanic waters, (Mongin et al. 2009). As such, the enhanced primary pro- east of the island. The parameters that determine these ductivity allows the maintenance of large abundances of probabilities are DCol, SST, SLA_grad and SLA (On- zooplankton, squids and fish. The importance of the Ker- line Resource 14). The ensemble model evaluation is guelen/Heard Plateau to the top predator community of the excellent with an ROC value of 0.99 (Online Resource southern ocean had already been identified, and as such this 15). area has already been identified as a highest priority area Concerning predictions applied to the second most for setting up an MPA (Harris et al. 2007). In particular, the important KIPE colony of the Kerguelen Islands, located at Kerguelen/Heard Plateau sustains an important community Baie du Feu de Joie, western coast of Kerguelen (Fig. S1), of albatrosses, petrels and penguins (Delord et al. 2014). A the distribution pattern of the predicted presence is similar previous study in the Australian area of the Heard and to that from Ratmanoff, with the main probabilities located McDonald Islands has also highlighted the key role of the between Kerguelen and the Polar Front and the highest 1000-m bathymetric contour and the area comprised values concentrated along the eastern slope of the plateau between the Kerguelen and Heard Islands, eastward of the (Fig. 9b). Predictions for Heard and McDonald Islands are plateau in a community of albatrosses, penguins and pin- mainly located in the part of the plateau surrounding the nipeds (Hindell et al. 2011). In this study, we investigated Australian islands and along the eastern slope of the Ker- the distribution of a community of species showing con- guelen/Heard Plateau, especially in the vicinity of the Polar trasted foraging behaviour and diet with the aim of iden- Front (Fig. 9c). tifying important areas at the scale of the whole top 123 Polar Biol (2017) 40:365–378 373

Fig. 8 Predicted presence probability for Black-browed albatross (BBAL) from a Canyon des Sourcils Noirs colony, b Cap Franc¸ais colony and c Heard and McDonald Islands colony. Contours of the Kerguelen/Heard Plateau (solid lines) and Polar Front (dashed lines) are represented predator community to suggest potential boundaries for an such as KECO or GEPE. As a consequence, surroundings MPA in the waters surrounding the Kerguelen of breeding colonies are transit areas with concentrations of Archipelago. many animals and high species diversity. In this study, The top predator species studied here presented con- most of the colonies where individuals were equipped are trasting distribution patterns. There were extensive differ- located on the eastern coast of the main island, leading to ences in the range, extent and use of the oceanographic high residence time in the vicinity of these colonies. Pre- features according to the species foraging ecology and at- dictions of presence probability for the three main colonies sea distribution, with WAAL showing a very large extent of BBAL, which are located in very distant locations, in their foraging range (some birds coming from the illustrate well the influence of colony on the at-sea distri- neighbouring Crozet Archipelago), whereas the other spe- bution of the species, with very different areas highlighted cies were mainly concentrated on the Kerguelen/Heard by each model predictions. Model predictions for Heard Plateau. Island are in very good agreement with tracking of BBAL As expected, colony has a strong effect on species dis- and KIPE from Heard Island and habitat modelling for tribution patterns (Garthe 1997). As central place foragers, these populations from a previous study (Hindell et al. breeding individuals performed foraging trips whose col- 2011). ony is the centre. Similarly, the vicinities of colonies are Slopes of the Kerguelen/Heard Plateau also appear to be important areas as they represent commuting corridors for a driving factor in the distribution of the majority of the animals moving from and to the colony to offshore waters study species. This is especially the case for BBALs, which as well as representing foraging areas for coastal species forage in the neritic waters of the shelf break (Cherel and

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Fig. 9 Predicted presence probability for King penguin (KIPE) from a Ratmanoff colony, b Baie du Feu de Joie colony and c Heard Island. Contours of the Kerguelen/Heard Plateau (solid lines) and Polar Front (dashed lines) are represented

Weimerskirch 1995; Cherel et al. 2000; Weimerskirch biomass. As a consequence, these features have long been et al. 1997b), but also for WCPEs, which used slopes recognised as important areas for foraging predators during short foraging trips (Catard et al. 2000;Pe´ron et al. (Schneider 1982; Jahncke et al. 2005; Bost et al. 2009). 2010), as well as WAALs and ANFSs (Croxall and Wood The zone east and southeast from the Kerguelen mainland 2002; Weimerskirch et al. 2002). appeared to be highly exploited by both seabirds and marine In this study, the Polar Front area and the cold water mammals in this study, particularly diving predators such as tongue from the ACC are preferentially targeted by KIPEs penguins and fur seals. Marine predators encounter here a and MAPEs, as was shown in previous studies (Bost et al. cold northwest flowing current increasing the local marine 1997b; Guinet et al. 1997; Barlow and Croxall 2002;Pu¨tz productivity (Charrassin et al. 2002). This area corresponds 2002). These penguins forage during incubation over the to the Kerguelen Plume, an area of high levels of primary wide shallow plateau and along the shelf break. This production within the Southern Ocean (Moore and Abbott preference could be explained by the preferential prey of 2000). This structure is produced by high primary produc- KIPE and MAPE, respectively, myctophid fish and crus- tivity of the plateau, probably due to the natural fertilisation taceans, which are largely distributed over the Polar Front of this water mass by iron inputs (Blain et al. 2001), taken Zone, but tend to concentrate in the Polar Front itself away by the eastward Antarctic Circumpolar Current. (Pakhomov et al. 1994; Pakhomov and McQuaid 1996). Here, the use of predictions applied to the major colo- Because of their characteristics in terms of temperature, nies for the species of interest allows us to avoid outputs salinity and density, but also because of the convergence of being biased toward areas where most of the telemetric processes, fronts often show increased productivity and studies were undertaken. Nevertheless, even when these

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predator community of the archipelago. Nonetheless, sat- uration curves calculated for WAAL and ANFS showed that more individuals would have been needed to appro- priately represent the complete home range of the species; therefore, it is possible that the predictions for these two species are slightly underestimated. Moreover, in this study, we considered that all individuals of a given species forage in the same way, whatever their colony. It is then possible that individuals from the colonies that were not tracked show feeding behaviour slightly different from the individuals used to develop our model because of intraspecific niche partitioning (Robson et al. 2004; Masello et al. 2010). Further work is thus needed to complete this study. First, it would be interesting to include foraging trips of indi- viduals from remote colonies in the habitat model. How- ever, the limited accessibility of these colonies does not allow the deployment of tracking devices at the moment. Second, as the species selected for our predicted map of presence do not represent all trophic guilds within the seabird community of the Kerguelen Archipelago, it could be valuable to include data for species that feed on lower trophic levels (e.g., small petrel species depending on microzooplancton), with the aim of validating the impor- tant area identified in this study. However, there is today a technological limit to tracking small species accurately. Fig. 10 Predicted presence probability for Antarctic fur seal (ANFS) from a Pointe Morne colony and b Iles Nuageuses colony. Contours In this study, predictions generated from the Biomod2 of the Kerguelen/Heard Plateau (solid lines) and Polar Front (dashed package for a panel of species selected for their foraging lines) are represented habits are concordant with the observed pattern for all nine species tracked. It appears that the monitoring of a few relevant species may be sufficient to identify important predictions are integrated, presence probability for the four areas at sea for the whole top predator community of the species highlighted the central part of the Kerguelen/Heard Kerguelen Archipelago. Selecting wide-ranging, high Plateau, next to the colonies from where most of the trophic level species showing various foraging and diet studied individuals were tracked, showing that this area is preferences, we are able to draw a predictive map of the of high importance not only for the individuals breeding important foraging areas besides commuting corridors close to this area, but probably also for the whole top between these areas and main colonies. Moreover,

Fig. 11 Sum of the predicted presence probabilities for four species (WAAL, BBAL, KIPE, ANFS) applied to the major colonies of each species. Contours of the Kerguelen/ Heard Plateau and fronts (PF Polar Front, SAF Sub-Antarctic Front) (dashed lines) are represented

123 376 Polar Biol (2017) 40:365–378 commuting areas that have been highlighted in this study Bost CA, Zorn T, Le Maho Y, Duhamel G (2002) Feeding of diving are likely to include feeding zones of short-range species predators and diel vertical migration of prey: King penguins’ diet versus trawl sampling at Kerguelen Islands. Mar Ecol Prog Ser that are traditionally concentrated in the vicinity of their 227:51–61 breeding colonies. For conservation purposes, this Bost C-A, Cotte´ C, Bailleul F, Cherel Y, Charrassin J-B, Guinet C, methodology would be the most efficient way to determine Ainley DG, Weimerskirch H (2009) The importance of oceano- crucial areas within the distribution of a community of top graphic fronts to marine birds and mammals of the southern oceans. J Mar Syst 78:363–376 predators, although in the case of wide-ranging species, Boudouresque CF, Cadiou G, Le Direac’h L (2005) Marine protected these areas would only protect the core of their foraging areas: a tool for coastal areas management. In: Levner E, Linkov range. I, Proth J-M (eds) Strategic management of marine ecosystems. The average output from four panel species highlights Springer, Nice, pp 29–52 Can˜adas A, Sagarminaga R, De Stephanis R, Urquiola E, Hammond the central part of the plateau and the eastern and western PS (2005) Habitat preference modelling as a conservation tool: slopes. With the aim of setting an MPA within the EEZ proposals for marine protected areas for cetaceans in southern area of the Kerguelen Islands, this area should be included Spanish waters. Aquat Conserv Mar Freshw Ecosyst 15:495–521 within the potential reserve limits that would adequately Catard A, Weimerskirch H, Cherel Y (2000) Exploitation of distant Antarctic waters and close shelf-break waters by white-chinned complete the existing Australian reserve of Heard and petrels rearing chicks. Mar Ecol Prog Ser 194:249–261 McDonald Islands. Charrassin J-B, Park Y-H, Maho YL, Bost C-A (2002) Penguins as oceanographers unravel hidden mechanisms of marine produc- Acknowledgments The project was supported financially and tivity. Ecol Lett 5:317–319 logistically by the Institut Polaire Franc¸ais (IPEV) (prog. 109, resp. Cherel Y, Weimerskirch H (1995) Seabirds as indicators of marine H. Weimerskirch and 394, resp. C.A Bost.), Terres Australes et resources: black-browed albatrosses feeding on ommastrephid Antarctiques Franc¸aises (TAAF), the ANR 05 REMIGE, ANR 07 squids in Kerguelen waters. Mar Ecol Prog Ser 129:295–300 Biodiv ‘Glides’, Prince Albert 2 de Monaco Foundation and Arg- Cherel Y, Guinet C, Tremblay Y (1997) Fish prey of Antarctic fur onautica (CNES) and the Agence des Aires Marines prote´ge´es seals Arctocephalus gazella at Ile de Croy. Kerguelen Polar Biol (AAMP). We would like to thank all the volunteers and colleagues 17:87–90 involved in the research on top predator ecology. LT was funded by Cherel Y, Weimerskirch H, Trouve´ C (2000) Food and feeding Foundation Albert 2 de Monaco and Re´gion Poitou-Charentes. We ecology of the neritic-slope forager black-browed albatross and thank David Pinaud, Baptiste Picard and Tiphaine Jeanniard du Dot its relationships with commercial fisheries in Kerguelen waters. for helping with data collection and analyses. Mar Ecol Prog Ser 207:183–199 Cherel Y, Ducatez S, Fontaine C, Richard P, Guinet C (2008) Stable isotopes reveal the trophic position and mesopelagic fish diet of female southern elephant seals breeding on the Kerguelen Islands. Mar Ecol Prog Ser 370:239–247 References Cheung WW, Lam VW, Sarmiento JL, Kearney K, Watson R, Pauly D (2009) Projecting global marine biodiversity impacts under AAD (2005) Heard Island and McDonald Islands marine reserve climate change scenarios. Fish Fish 10:235–251 management plan. Aust Antarct Div Dep Environ Herit Kingston Coll M, Libralato S, Tudela S, Palomera I, Pranovi F (2008) Tasman 1–198 Ecosystem overfishing in the ocean. PLoS ONE 3:e3881 Barlow KE, Croxall JP (2002) Seasonal and interannual variation in Cook TR, Kato A, Tanaka H, Ropert-Coudert Y, Bost C-A (2010) foraging range and habitat of macaroni penguins Eudyptes Buoyancy under control: underwater locomotor performance in a chrysolophus at South Georgia. Mar Ecol Prog Ser 232:291–304 deep diving seabird suggests respiratory strategies for reducing Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2003) foraging effort. PLoS ONE 5:e9839 Marine invasive alien species: a threat to global biodiversity. Croxall JP, Wood AG (2002) The importance of the Patagonian Shelf Mar Policy 27:313–323 for top predator species breeding at South Georgia. Aquat Blain S, Tre´guer P, Belviso S, Bucciarelli E, Denis M, Desabre S, Conserv Mar Freshw Ecosyst 12:101–118 Fiala M, Martin Je´ze´quel V, Le Fe`vre J, Mayzaud P et al (2001) Delord K, Barbraud C, Bost C-A, Deceuninck B, Lefebvre T, Lutz R, A biogeochemical study of the island mass effect in the context Micol T, Phillips RA, Trathan PN, Weimerskirch H (2014) of the iron hypothesis: Kerguelen Islands, Southern Ocean. Deep Areas of importance for seabirds tracked from French southern Sea Res Part Oceanogr Res Pap 48:163–187 territories, and recommendations for conservation. Mar Policy Blain S, Que´guiner B, Armand L, Belviso S, Bombled B, Bopp L, 48:1–13 Bowie A, Brunet C, Brussaard C, Carlotti F et al (2007) Effect of Derraik JGB (2002) The pollution of the marine environment by natural iron fertilization on carbon sequestration in the Southern plastic debris: a review. Mar Pollut Bull 44:842–852 Ocean. Nature 446:1070–1074 Garthe S (1997) Influence of hydrography, fishing activity, and Bost CA, Georges JY, Guinet C, Cherel Y, Pu¨tz K, Charrassin JB, colony location on summer seabird distribution in the south- Handrich Y, Zorn T, Lage J, Le Maho Y (1997a) Foraging eastern North Sea. ICES J Mar Sci J Cons 54:566–577 habitat and food intake of satellite-tracked king penguins during Green K, Williams R, Green MG (1998) Foraging ecology and diving the austral summer at Crozet Archipelago. Mar Ecol Prog Ser behaviour of macaroni penguins Eudyptes chrysolophus at Heard 150:21–33 Island. Mar Ornithol 26:27–34 Bost CA, Georges JY, Guinet C, Cherel Y, Pu¨tz K, Charrassin JB, Guinet C, Koudilz M, Bosts CA, Durbecz JP, Georges JY, Mouchot Handrich Y, Zorn T, Lage J, Le Maho Y (1997b) Foraging MC, Jouventin P (1997) Foraging behaviour of satellite-tracked habitat and food intake of satellite-tracked king penguins during king penguins in relation to sea-suriace temperatures. Mar Ecol the austral summer at Crozet Archipelago. Mar Ecol Prog Ser Prog Ser 150:11–20 150:21–33

123 Polar Biol (2017) 40:365–378 377

Guinet C, Dubroca L, Lea MA, Goldsworthy S, Cherel Y, Duhamel approaches to setting conservation priorities. Conserv Biol G, Bonadonna F, Donnay J-P (2001) Spatial distribution of 12:516–520 foraging in female Antarctic fur seals Arctocephalus gazella in Mongin MM, Abraham ER, Trull TW (2009) Winter advection of relation to oceanographic variables: a scale-dependent approach iron can explain the summer phytoplankton bloom that extends using geographic information systems. Mar Ecol Prog Ser 1000 km downstream of the Kerguelen Plateau in the Southern 219:251–264 Ocean. J Mar Res 67:225–237 Guinet C, Vacquie´-Garcia J, Picard B, Bessigneul G, Lebras Y, Moore JK, Abbott MR (2000) Phytoplankton chlorophyll distribu- Dragon A-C, Viviant M, Arnould JPY, Bailleul F (2014) tions and primary production in the Southern Ocean. J Geophys Southern elephant seal foraging success in relation to temper- Res Oceans 1978–2012(105):28709–28722 ature and light conditions: insight into prey distribution. Mar Myers N (1988) Threatened biotas:‘‘hot spots’’ in tropical forests. Ecol Prog Ser 499:285–301 Environmentalist 8:187–208 Gutowsky SE, Leonard ML, Conners MG, Shaffer SA, Jonsen ID Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J (2015) Individual-level variation and higher-level interpretations (2000) Biodiversity hotspots for conservation priorities. Nature of space use in wide-ranging species: an albatross case study of 403:853–858 sampling effects. Front Mar Sci 2:93 Pakhomov EA, McQuaid CD (1996) Distribution of surface zoo- Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, plankton and seabirds across the Southern Ocean. Polar Biol D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE et al (2008) 16:271–286 A global map of human impact on marine ecosystems. Science Pakhomov EA, Perissinotto R, McQuaid CD (1994) Comparative 319:948–952 structure of the macrozooplankton/micronekton communities of Harris J, Haward M, Jabour J, Woehler EJ (2007) A new approach to the Subtropical and Antarctic Polar Fronts. Mar Ecol Prog Ser selecting Marine Protected Areas (MPAs) in the Southern Oldendorf 111:155–169 Ocean. Antarct Sci 19:189–194 Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population Hegel TM, Cushman SA, Evans J, Huettmann F (2010) Current state trend of the World’s monitored seabirds, 1950–2010. PLoS ONE of the art for statistical modelling of species distributions. In: 10:e0129342 Cushman SA, Huettmann F (eds) Spatial complexity, informat- Park YH, Vivier F (2011) Circulation and hydrography over the ics, and wildlife conservation. Springer, pp 273–311 Kerguelen Plateau. Kerguelen Plateau Mar Ecosyst Fish, Hindell MA, Slip DJ, Burton HR (1991) The diving behavior of adult pp 43–55 male and female southern elephant seals, Mirounga-Leonina Park Y-H, Roquet F, Durand I, Fuda J-L (2008) Large-scale (Pinnipedia, Phocidae). Aust J Zool 39:595–619 circulation over and around the Northern Kerguelen Plateau. Hindell MA, Bradshaw CJA, Sumner MD, Michael KJ, Burton HR Deep Sea Res Part II Top Stud Oceanogr 55:566–581 (2003) Dispersal of female southern elephant seals and their prey Park Y-H, Vivier F, Roquet F, Kestenare E (2009) Direct observa- consumption during the austral summer: relevance to manage- tions of the ACC transport across the Kerguelen Plateau. ment and oceanographic zones. J Appl Ecol 40:703–715 Geophys Res Lett 36:L18603 Hindell MA, Lea M-A, Bost C-A., Charrassin J-B, Gales N, Pe´ron C, Delord K, Phillips RA, Charbonnier Y, Marteau C, Louzao Goldsworthy S, Page B, Robertson G, Wienecke B, O’Toole M, Weimerskirch H (2010) Seasonal variation in oceanographic M, et al (2011) Foraging habitats of top predators, and areas of habitat and behaviour of white-chinned petrels Procellaria ecological significance, on the Kerguelen Plateau. Kerguelen aequinoctialis from Kerguelen Island. Mar Ecol Prog Ser Plateau Mar Ecosyst Fish Socie´te´ Fr D’Ichtyologie Paris, 416:267–284 pp 203–215 Pu¨tz K (2002) Spatial and temporal variability in the foraging areas of Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change breeding king penguins. The Condor 104:528–538 on the world’s marine ecosystems. Science 328:1523–1528 Reid WV (1998) Biodiversity hotspots. Trends Ecol Evol 13:275–280 Hosmer DW, Lemeshow S (2000) Applied logistic regression. Wiley, Robson BW, Goebel ME, Baker JD, Ream RR, Loughlin TR, New York, pp 156–164 Francis RC, Antonelis GA, Costa DP (2004) Separation of Jahncke J, Coyle KO, Zeeman SI, Kachel NB, Hunt GL (2005) foraging habitat among breeding sites of a colonial marine Distribution of foraging shearwaters relative to inner front of SE predator, the northern fur seal (Callorhinus ursinus). Can J Bering Sea. Mar Ecol Prog Ser 305:219–233 Zool 82:20–29 Kolbert E (2014) The sixth extinction: an unnatural history. A&C Schneider D (1982) Fronts and seabird aggregations in the south- Black, London eastern Bering Sea. Mar Ecol Prog Ser Oldendorf 10:101–103 Lea M-A, Hindell M, Guinet C, Goldsworthy S (2002) Variability in Soanes LM, Arnould JPY, Dodd SG, Sumner MD, Green JA (2013) the diving activity of Antarctic fur seals, Arctocephalus gazella, How many seabirds do we need to track to define home-range at Iles Kerguelen. Polar Biol 25:269–279 area? J Appl Ecol 50:671–679 Lescroe¨l A, Bost C-A (2005) Foraging under contrasting oceano- Sokolov S, Rintoul SR (2009) Circumpolar structure and distribution graphic conditions: the gentoo penguin at Kerguelen archipe- of the Antarctic Circumpolar Current fronts: 2. Variability and lago. Mar Ecol Prog Ser 302:245–261 relationship to sea surface height. J Geophys Res Oceans Lescroe¨l A, Ridoux V, Bost CA (2004) Spatial and temporal variation 114:C11019 in the diet of the gentoo penguin (Pygoscelis papua)at Thuiller W, Georges D, Engler R (2013) biomod2: ensemble platform Kerguelen Islands. Polar Biol 27:206–216 for species distribution modeling. R Package Version 2:r560 Masello JF, Mundry R, Poisbleau M, Demongin L, Voigt CC, Warren DL, Glor RE, Turelli M (2008) Environmental niche Wikelski M, Quillfeldt P (2010) Diving seabirds share foraging equivalency versus conservatism: quantitative approaches to space and time within and among species. Ecosphere 1:art19 niche evolution. Evolution 62:2868–2883 McConnell BJ, Chambers C, Fedak MA (1992) Foraging ecology of Weimerskirch H, Zotier R, Jouventin P (1989) The avifauna of the southern elephant seals in relation to the bathymetry and Kerguelen Islands. Emu 89:15–29 productivity of the Southern Ocean. Antarct Sci 4:393 Weimerskirch H, Salamolard M, Sarrazin F, Jouventin P (1993) Mittermeier RA, Myers N, Thomsen JB, Da Fonseca GAB, Olivieri S Foraging strategy of wandering albatrosses through the breeding (1998) Biodiversity hotspots and major tropical wilderness areas: season: a study using satellite telemetry. The Auk 110:325–342

123 378 Polar Biol (2017) 40:365–378

Weimerskirch H, Cherel Y, Cuenot-Chaillet F, Ridoux V (1997a) Weimerskirch H, Guionnet T, Martin J, Shaffer SA, Costa DP (2000) Alternative foraging strategies and resource allocation by Fast and fuel efficient? Optimal use of wind by flying male and female wandering albatrosses. Ecology 78: albatrosses. Proc R Soc Lond B Biol Sci 267:1869–1874 2051–2063 Weimerskirch H, Bonadonna F, Bailleul F, Mabille G, Dell’Omo G, Weimerskirch H, Mougey T, Hindermeyer X (1997b) Foraging and Lipp H-P (2002) GPS tracking of foraging albatrosses. Science provisioning strategies of black-browed albatrosses in relation to 295:1259 the requirements of the chick: natural variation and experimental Worm B, Lotze HK, Myers RA (2003) Predator diversity hotspots in study. Behav Ecol 8:635–643 the blue ocean. Proc Natl Acad Sci 100:9884–9888

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