Individual Foraging Site Fidelity in Lactating New Zealand Fur Seals

MARINE MAMMAL SCIENCE, **(*): ***–*** (*** 2011) C 2011 by the Society for Marine Mammalogy DOI: 10.1111/j.1748-7692.2011.00487.x

Individual foraging site ﬁdelity in lactating New Zealand fur seals: Continental shelf vs. oceanic habitats

ALASTAIR M. M. BAYLIS South Australian Research and Development Institute, (Aquatic Sciences), PO Box 120, Henley Beach, Adelaide, South Australia 5022, Australia and School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia and Falklands Conservation, PO Box 41, Stanley, FIQQ1ZZ, Falkland Islands E-mail: [email protected]

BRAD PAGE JANE MCKENZIE SIMON D. GOLDSWORTHY South Australian Research and Development Institute, (Aquatic Sciences), PO Box 120, Henley Beach, Adelaide, South Australia 5022, Australia

ABSTRACT Wide-ranging marine central place foragers often exhibit foraging site fidelity to oceanographic features over differing spatial scales (i.e., localized coastal upwellings and oceanic fronts). Few studies have tested how the degree of site fidelity to foraging areas varies in relation to the type of ocean features used. In order to determine how foraging site fidelity varied between continental shelf and oceanic foraging habitats, 31 lactating New Zealand fur seals (Arctocephalus australis forsteri1)were satellite tracked over consecutive foraging trips (14–108 d). Thirty-seven foraging trips were recorded from 11 females that foraged on the continental shelf, in a region

1Currently the Marine Mammal Society’s Ad-hoc Committee on Taxonomy (Committee on Taxonomy 2009) lists New Zealand fur seals as Arctocepahlus australis forsteri based on the ﬁndings presented in Brunner et al. (2004). This taxonomic revision did not include a more recent analysis of the molecular phylogeny and divergence of the pinnipeds by Higdon et al. (2007), which identiﬁed A. forsteri being basal to A. australis, and limited support for the two taxa being subspecies. Based on this study, we believe the full species name A. forsteri should be retained.

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associated with a coastal upwelling, while 65 foraging trips were recorded from 20 females that foraged in oceanic waters. There were no significant differences in the mean bearings (to maximum distance) of individual’s consecutive foraging trips, suggesting individual fidelity to foraging areas. However, overlap in area and time spent in area varied considerably between continental shelf and oceanic foragers. Females that foraged on the continental shelf had significantly greater overlap in consecutive foraging trips when compared to females that foraged in oceanic waters (overlap in 5 × 5 km grid cells visited on consecutive trips 55.9% ± 20.4% and 13.4% ± 7.6%, respectively). Females that foraged on the continental shelf also spent significantly more time within the same grid cell than females that foraged in oceanic waters (maximum time spent in 5 × 5 km grid cells: 14% ± 5% and 4% ± 2%, respectively). This comparatively high foraging site fidelity may reflect the concentration of productivity associated with a coastal upwelling system, the Bonney Upwelling. Lower foraging site fidelity recorded by seals that foraged in oceanic waters implies a lower density/larger scale habitat, where prey are more dispersed or less predictable at fine scales, when compared to the continental shelf region. Key words: foraging behavior, marine mammals, pinnipeds, Bonney Upwelling, Subtropical Front, South Australia.

Central place foragers are constrained in foraging distance and duration by the fasting abilities of their offspring (Orians and Pearson 1979). Accordingly, foraging strategies have evolved to maximize the efficiency and rate of energy gain (Ydenberg et al. 1992). The tendency for an individual to repeatedly return to the same area to forage has been widely documented among marine central place foragers (e.g., Irons 1998, Bonadonna et al. 2001, Hedd et al. 2001, Broderick et al. 2007, Chilvers 2008). From an optimal foraging perspective, foraging site fidelity is likely to be advantageous in long-lived species that exhibit breeding site fidelity and forage in regions where resources are to some degree predictable over both spatial and temporal scales (Irons 1998, Weimerskirch 2007). In such situations, familiarity with predictable resources may enhance foraging efficiency and foraging success, and maximize energy gain over the lifetime of an animal (Gentry 1998, Irons 1998, Bradshaw et al. 2004, Gende and Sigler 2006). However, wide-ranging central place foragers such as seals and seabirds often use multiple oceanographic features over varying spatial scales (Lea and Dubroca 2003, Beauplet et al. 2004, Weimerskirch 2007, Baylis and Nichols 2009). For example, Australian sea lions (Neophoca cinerea) forage in both inshore (shallow) and outer-shelf (deep) habitats (Baylis et al. 2009), whereas lactating Antarctic (Arctocephalus gazella) and northern (Callorhinus ursinus) fur seals utilize both continental shelf and oceanic habitats (Staniland and Boyd 2003, Robson et al. 2004), and short tailed shearwaters (Puffinus tenuirostris) employ a dual-foraging strategy to exploit both continental shelf and distant frontal zones (Einoder 2010). Distinguishing how foraging site fidelity varies between discrete habitats provides insights into foraging plasticity that may have important ecological, conservation, and evolutionary implications. Few studies have tested the degree to which foraging site fidelity is influenced by the type of ocean feature utilized. New Zealand fur seals (A. australis forsteri) breeding in the state of South Australia provide a unique opportunity to test how foraging site fidelity varies in relation to discrete oceanographic features. Lactating New Zealand fur seals are wide-ranging central place foragers that display a high degree of philopatry (McKenzie 2006). BAYLIS ET AL.: NEW ZEALAND FUR SEAL FORAGING SITE FIDELITY 3

During their 8–11 mo lactation period, females regularly alternate between foraging at sea and nursing their pup ashore (Goldsworthy 2006). Females forage in association with two distinct oceanographic features. A nearby (36–190 km) but seasonally variable (occurs in summer/autumn) wind-driven coastal upwelling, the Bonney Upwelling (Lewis 1981) and a distant (380–1,000 km) but permanent oceanic front, the Subtropical Front (STF) (Tomczak et al. 2004, Baylis et al. 2008a). Previous studies have revealed lactating seals that foraged on the continental shelf performed both shallow (<30 m) and deep dives (50–80 m) and preyed mainly on redbait (Emmelichthys nitidus) and Gould’s squid (Notodarus gouldi) (Page et al. 2006, Baylis et al. 2008b, Baylis and Nichols 2009). In contrast, lactating seals that foraged in association with the STF performed predominantly shallow dives (<30 m) almost exclusively during night hours and were thought to have preyed mainly on myc- tophids (Baylis et al. 2008b, Baylis and Nichols 2009). Differences in diet and dive behavior suggest foraging strategies are influenced by prey type, distribution, and prey behavior, which vary according to continental shelf and oceanic habitats. In addition, the vast difference in travel distances to utilize nearby continental habitats compared to distant oceanic habitats also implies that foraging site fidelity will vary between these two habitats. Identifying the degree of New Zealand fur seal foraging site fidelity to discrete oceanographic features is of particular interest because five colonies within ca. 200 km (Liguanea Island, North and South Neptune Island, Cape du Couedic, and Cape Gantheuame) account for 82% of the Australian population (ca. 85,000 individuals; Goldsworthy and Page 2007). The relatively small area in which the population is concentrated makes the Australian population of New Zealand fur seals potentially vulnerable to changes within this region of critical breeding and foraging habitat. The degree of foraging site fidelity exhibited has potentially important implications for species management and conservation because foraging site fidelity may affect an individual’s ability to respond to changes in the distribution of prey or to broad-scale environmental changes (Chilvers 2008). Recent studies at four key colonies have described New Zealand fur seal foraging site fidelity based on directional persistence of consecutive foraging trips, but within the context of colony specific foraging areas (Baylis et al. 2008a). In general, females from the Cape Gantheaume colony exploited continental shelf waters associated with the Bonney Upwelling during autumn and shifted foraging effort to the STF during winter months (Baylis et al. 2008b). Over the same time period of autumn and winter, females from Cape du Couedic, North Neptune Island, and Liguanea Island colonies almost exclusively foraged in distant oceanic waters associated with the STF (Baylis et al. 2008a). The current study compares foraging site fidelity of lactating New Zealand fur seals that foraged in continental shelf waters to those that foraged in distant oceanic waters.

MATERIALS AND METHODS Study Site and Animal Handling This study was conducted in 2005 and 2006 at four sites; in March–September 2005 at Cape Gantheaume (36◦04S, 137◦27E) and Cape du Couedic (36◦03S, 136◦42E) on Kangaroo Island and in April–August 2006 at Cape du Couedic, North Neptune Island (35◦13S, 136◦03E), and Liguanea Island (34◦59S, 135◦37E) (Fig. 1). This study was conducted as part of a concomitant study presented in 4 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2011

Figure 1. (A) The four study sites: Cape Gantheaume, CG; Cape du Couedic, DC; North Neptune Island, NN; and Liguanea Island, LIG and examples of consecutive foraging trips (FTs) recorded from lactating New Zealand fur seals that foraged in oceanic waters. Also presented is an example of the Subtropical Front that is typically located between 39◦ and 42◦S. It is deﬁned here by the 14◦C isotherm in April (shaded area). (B) Examples of consecutive FTs recorded from lactating New Zealand fur seals that foraged in continental shelf waters from Cape Gantheaume. Also presented is an example of a seasonal change in oceanic FT distance, recorded by a lactating New Zealand fur seal from Cape du Couedic. BAYLIS ET AL.: NEW ZEALAND FUR SEAL FORAGING SITE FIDELITY 5

Baylis et al. (2008a, 2008b) and Baylis and Nichols (2009). The foraging locations and directional movements of females were monitored using satellite platform transmitter terminals (PTT; Sirtrack KiwiSat 101, Havelock North, New Zealand). PTTs were programmed to transmit location information every 45 s, except when the seal was on land or diving. Lactating adult females selected were captured using a hoop net and manually restrained. Upon capture, anesthesia was induced and maintained using Isoflurane (Veterinary Companies of Australia, Artarmon, New South Wales, Australia), administered via a portable gas anesthetic machine (Komesaroff Small Animal Anes- thetic Machine, Medical Developments Australia, Melbourne, Australia). PTTs were attached to guard hairs on the mid-dorsal line using a flexible araldite epoxy (Araldite 2017, Vantico, Basel, Switzerland). The instruments were removed by cutting guard hairs attached to the unit using a scalpel blade. For certain re- captures, females were first immobilized with Zoletil (dose 2 mg/kg; Virbac, Sydney, Australia), administered using 0.5 cc barbless darts (Pneu-Dart, Williamsport, PA), fired from a CO2-powered tranquillizer gun (Taipan 2000, Tran- quil Arms Company, Melbourne, Australia). The lightly anaesthetized females were then captured using a hoop net and manually restrained.

Foraging Trip Data The duration of a foraging trip was defined as the period of time between a seal’s departure from the breeding site and its return to land. Satellite location data was obtained through the Argos satellite system. The location-class B and Z positions were omitted due to the magnitude of their error (Page et al. 2006, Arnould and Kirkwood 2008). To further improve the accuracy of satellite tracks, we applied the filter described by McConnell et al. (1992) using the timeTrack package (version 1.0–9, M. D. Sumner, University of Tasmania, Hobart, Australia) and R (version 2.0.1, R Development Core Team, R Foundation for Statistical Computing, Vienna), based on a maximum horizontal speed of 7 km/h (Page et al. 2006). The importance in choosing the appropriate analytical spatial scale has been stressed by several authors (e.g., Jaquet and Whitehead 1996, Guinet et al. 2001). Intuitively, the degree of spatial overlap between consecutive foraging trips will be influenced by the spatial scale (size of grid cells) used. The majority of locations received were class A and class 0 (60%). We analyzed location data using a 5 × 5km spatial scale, because class A and class 0 locations are typically inaccurate and do not support analysis at spatial scales finer than 5 × 5 km (Robson et al. 2004). Each foraging trip was summarized as a proportion of the total time spent in 5 × 5 km grid cells. To determine the number of different 5 × 5 km grid cells entered on each foraging trip and the proportion of time they spent in different cells, we assumed a constant horizontal speed between the filtered locations and linearly interpolated a new position for each hour of time along the satellite track using R statistical software and the timeTrack package (Page et al. 2006). The number of original and interpolated positions, which were located within 5 × 5 km cells of a predetermined grid, were then summed and assigned to a central point. For comparisons of the relative time spent in particular grid cells on consecutive trips, values for individual trips were converted to a proportion. Along with time spent in 5 × 5 km grid cells, several additional foraging trip parameters were calculated to summarize foraging behavior on each foraging trip. 6 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2011

These were: (1) maximum straight-line distance (from the colony to the furthest point reached); (2) cumulative distance traveled (sum of distances between locations); (3) mean bearing of locations from the colony to the maximum distance travelled; and (4) horizontal travel speed (the distance between consecutive locations, divided by duration [60 min]).

Individual Site Fidelity Individual site fidelity was assessed using: (1) Directional persistence between consecutive foraging trips. For each individual, a mean bearing was calculated for each foraging trip and a preferred direction of travel was analyzed by calculating the statistic r, a measure of angular dispersion ranging from 0 (no mean angle) to 1 (data concentrated in the same direction) (Zar 1996). (2) Consistency of the maximum straight-line distance traveled on consecutive foraging trips (Hamer et al. 2001), which was quantified as the coefficient of variation (CV).

Continental Shelf vs. Oceanic Habitats and Colony Differences Differences in site fidelity between lactating seals that foraged on the continental shelf compared to those that foraged in oceanic habitats and colony differences in oceanic foraging site fidelity were assessed using: (1) Overlap in foraging area between consecutive foraging trips: measured by comparing the overlap in 5 × 5 km grid cells entered. (2) Overlap in time spent in area between consecutive foraging trips: measured by comparing the overlap in time spent within 5 × 5 km grid cells. All statistical tests were conducted using SPSS 15.0 (SPSS Inc., Chicago, IL) and Oriana (V d.02c, Kovach Computing Service, Pentreath, Wales, U.K.). We used linear mixed models (LMMs) to analyze area-overlap and overlap in time spent in area, from consecutive foraging trips using foraging trip as the repeated observation and seal identity as a random factor. Akaike’s Information Criterion (AIC) values were used to determine the covariance structure that best suited the model. The LMM does not assume homogeneity of variances and only assumes a moderately normal distribution of the residuals from the entire model. Normality was assessed using the Kolmogorov–Smirnov test. For all other tests, transformations to meet assumptions of normality and homogeneity of variances were performed as necessary. If normality could not be achieved, then equivalent nonparametric tests were used. All values are given as mean ± SD and considered significant at the P < 0.05 level.

RESULTS Excluding class B and class Z, we received 4,592 at-sea locations from service Argos. Filtering removed 231 locations, leaving 4,361 locations for analysis (Cape Gantheaume: 1,908; Cape du Couedic: 1,259; North Neptune: 429; and Liguanea Island: 765 locations). The average number of locations received for individuals foraging on the continental shelf ranged from 19 to 50, while the average number of locations received for individuals foraging in oceanic waters ranged from 24 to 142 (Table 1). A total of 31 lactating females were satellite tracked over 102 consecutive foraging trips (range 2–8 foraging trips per female) (Table 1). Consecutive foraging trips were recorded from 17 females from Cape Gantheaume, 7 from Cape du Couedic, 3 from BAYLIS ET AL.: NEW ZEALAND FUR SEAL FORAGING SITE FIDELITY 7 value r- (Continued) 13.3 0.994 11.1 0.996 ± ± )CV ◦ 13 21.9 0.982 2 15.0 1.000 1 15.9 1.000 3 10.8 0.999 5 26.5 0.996 4 8.0 0.998 2 9.2 1.000 3 33.2 0.999 7 34.8 0.995 7 32.8 0.995 929 22.3 37.5 0.993 9 18.5 0.992 12 29.3 0.986 3 6.0 0.999 4 41.7 0.998 1016 12.8 19.9 0.990 1 10.9 1.000 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 1 144 23 132 9 192 8 116 7 125 6 122 5 121 17 192 26 112 7 133 811 117 137 11 191 7 152 35 150 46 152 4232 150 160 4 167 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 9.50 29 8.10 63 ± ± SD. Foraging Deployment At-sea Mean ± Foraging trip parameters including, total duration of deployment, bearing, at-sea locations and coefﬁcient of variation (CV) in maximum Table 1. distances traveled recorded from 31and lactating Liguanea New Island, Zealand LIG. fur All seals values from are Cape mean Gantheaume, CG; Cape du Couedic, DC; North Neptune Island, NN; Colony ID Season location duration (d) FT locations bearing ( CG 68 Winter Shelf 40.25 3 48 CG 691 Autumn Shelf 14.50 2 26 CG 692 Autumn Shelf 14.25 3 23 CG 693 Winter Shelf 39.46 5 23 CG 702 Autumn Shelf 29.58 5 23 CG 711 Autumn Shelf 22.67 4 19 CG 712 Autumn Shelf 20.67 2 39 CG 721 Autumn Shelf 17.63 4 24 CG 723 Winter Shelf 31.21 3 50 CG 731 Autumn Shelf 15.88 3 25 CG 732 Autumn Shelf 20.42 3 24 Mean CG 24.23 CG 74 Autumn/winter Oceanic 36.08 3 34 CG 76 Autumn/winter Oceanic 34.63 3 24 CG 703 Autumn/winter Oceanic 47.63 2 52 CG 713 Autumn/winter Oceanic 49.54 3 85 CG 722 Autumn/winter Oceanic 55.21 3 63 CG 733 Autumn/winter Oceanic 41.17 2 119 Mean CG 44.04 8 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2011 value r- 17.7 0.989 11.1 0.970 18.5 0.988 8.4 0.996 15.2 0.970 ± ± ± ± ± )CV ◦ 12 39.7 29 22.3 9118811 25.4 38.1716 32.7 67.2 53.6 0.991 0.988 46.6 14.3 0.993 0.994 0.974 0.995 0.986 7 9.2 0.997 27 32.2 9315 25.9 18.2 19.510 0.994 0.999 48.3 28171920 35.8 70.5 42.6 44.4 0.993 0.969 0.963 0.955 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 9 182 11 137 20 189 22223718 195 14 180 17 173 161 188 186 16 216 33 187 458 187 208 44 204 50 224 8381410 233 232 211 222 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 18.03 43 19.26 59 10.4918.54 71 9.50 72 29 ± ± ± ± ± Table 1. (Continued) Foraging Deployment At-sea Mean DC 69 Autumn/winter Oceanic 72.13 4 42 DCDCDCDC 70DC 74DC 75Mean Autumn/winter DC 76 Autumn/winter 77 Autumn/winter Oceanic 36 Autumn/winter Oceanic Autumn/winter Oceanic Autumn/winter Oceanic Oceanic 51.04 Oceanic 65.21 58.79 41.46 17.63 3 57.63 5 8 40 3 32 2 61 4 45 37 51.98 45 NN 73 Autumn Oceanic 51.42 2 66 Colony ID Season location duration (d) FT locations bearing ( NNNN 75 53 Autumn Autumn Oceanic Oceanic 38.58 59.38 2 3 118 29 Oceanic 55.03 Mean NNLIGLIGLIGLIG 68Mean LIG 72 56Shelf Autumn/winter 61 Autumn/winter Autumn/winter Oceanic Autumn/winter Oceanic Oceanic Oceanic 73.33 70.67 70.54 108.50 2 49.79 3 4 142 4 71 51 25 80.76 24.23 BAYLIS ET AL.: NEW ZEALAND FUR SEAL FORAGING SITE FIDELITY 9

North Neptune Island, and 4 from Liguanea Island. Of the 102 foraging trips, 37 were recorded from 11 females that foraged on the continental shelf, while 65 foraging trips were recorded from 20 females that foraged in oceanic waters. Cape Gantheaume was the only colony where seals foraged in adjacent continental shelf waters. Examples of consecutive foraging trips to continental shelf and oceanic waters are presented in Figure 1.

Individual Foraging Site Fidelity Lactating females recorded high r values (range 0.95–1.0) derived from foraging trip mean bearings, indicating directional fidelity to foraging sites (Table 1). However, maximum trip distances and durations were variable between consecutive foraging trips, as reflected in CV values (range 6%–70.5%; Table 1, 2). Individu- als from Cape du Couedic and Liguanea Island recorded the greatest variability in maximum distances between foraging trips, as indicated by high CV values. This reflects seasonal variation in foraging trip distances that ranged from 385 ± 135 km in autumn to 263 ± 102 km in winter for Cape du Couedic (LMM: F1,23.4 = 5.5, P = 0.027) and 727 ± 102 km in autumn compared to 343 ± 120 km in winter for Liguanea Island (LMM: F1,4.7 = 12.1, P = 0.019). While directional fidelity was evident, foraging route overlap varied between consecutive foraging trips, ranging between 1.1% and 93.1% in 5 × 5 km area overlap and 0.7%–77.5% overlap in time spent in area (Table 3).

Continental Shelf vs. Oceanic Habitats Maximum distance from the colony was correlated with the cumulative total distance traveled (r2 = 0.97, P < 0.001) and foraging trip duration (r2 = 0.81, P < 0.001). Continental shelf foraging trips were shorter in both distance (124 ± 50 km and 458 ± 134 km, respectively, LMM: F1,22.9 = 60.8, P < 0.001) and duration than oceanic foraging trips (7.5 ± 2.8 d and 18.3 ± 6.9 d, respectively; F1,23.9 = 11.4, P = 0.002). Foraging route overlap varied in relation to the habitat used. Cape Gantheaume females that foraged on the continental shelf had signiﬁcantly more overlap in foraging area (area: 55.9% ± 20.4% and 13.4% ± 7.6%, respectively; LMM: F1,26.3 = 32.3, P < 0.001) and time spent in area (43.7% ± 16.8% and 9.0% ± 5.7%, respectively; LMM : F1,28.0 = 26.9, P < 0.001), when compared to females that foraged in oceanic waters (Table 3). Females that foraged on the continental shelf also spent signiﬁcantly more time in the same grid cell than oceanic foragers (maximum time spent in 5 × 5 km grid cell: 14% ± 5% and 4% ± 2%, respectively; LMM: F1,26.9 = 18.9, P < 0.001).

Colony Differences

For females that foraged in oceanic waters, the maximum distance (LMM: F3,43.1 = 7.5, P < 0.001) and duration of foraging trips (LMM: F3,16.1 = 5.1, P = 0.01) differed signiﬁcantly between colonies (Table 2). In addition, the mean foraging route overlap between consecutive foraging trips to oceanic waters also varied signiﬁcantly between colonies (LMM: F3,45 = 4.2, P = 0.010). The mean overlap recorded from Cape Gantheaume and Cape du Couedic was 18% ± 11% and 16% ± 12%, respectively, 10 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2011 0.7 0.5 0.8 0.5 0.5 0.2 0.1 0.3 0.4 0.2 0.7 0.5 0.4 0.3 0.4 0.6 0.0 0.2 0.5 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± (Continued) 42.3 61.8 33.1 01.9 41.9 32.1 91.7 82.7 82.1 31.8 02.1 52.5 32.1 32.4 23.0 62.8 92.8 82.9 62.2 ...... 2 2 0 2 2 0 0 1 4 2 4 1 1 2 6 2 2 3 7 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 4 3 7 9 9 8 3 4 1 4 3 8 5 5 0 4 6 5 8 ...... 95 4 48 10 30 5 100 5 48 7 57 4 107 7 60 13 283 17 155 10 110 5 126 6 128 7 549 16 142 12 134 18 216 20 249 11 115 23 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 101 236 391 269 213 , , , , , 19 36–82 197 19 190–211 560 7 78–94 226 40 109–197 410 10 51–71 194 15 128–164 325 18 105–130 328 40 143–222 529 96 1 52 89–181 483 36 72–144 310 49 48–187 342 46 355 67 448–569 1 55 470–548 1 28 454–494 1 187 271–643 1 53102 226–329 256–456 686 810 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± Mean Range of Cumulative Foraging maximum maximum total distance Mean Mean SD. ± Maximum distance traveled from the colony, cumulative total distance, foraging trip duration, and mean foraging trip speed (km/h) Table 2. recorded from 31 lactatingIsland, New LIG. All Zealand values fur are seals mean from Cape Gantheaume, CG; Cape du Couedic, DC; North Neptune Island, NN; and Liguanea CG 721 4 Autumn Shelf 58 CG 712 2 Autumn Shelf 203 CG 711 4 Autumn Shelf 88 CG 702 5 Autumn Shelf 151 CG 692 3 Autumn Shelf 61 CG 693 5 Winter Shelf 143 CG 691 2 Autumn Shelf 118 Colony ID FT Season location distance (km) distance (km) traveled (km) duration (d) speed (km/h) CG 68 3 Winter Shelf 181 CG 722 3 Autumn/winter Oceanic 526 CG 733 2 Autumn/winter Oceanic 509 Mean CG 431 CG 723 3 Winter Shelf 149 CG 731 3 Autumn Shelf 110 CG 732 3 Autumn Shelf 131 Mean CG 127 CGCG 74 76 3 3 Autumn/winter Autumn/winter Oceanic Oceanic 285 346 CG 703 2 Autumn/winter Oceanic 474 CG 713 3 Autumn/winter Oceanic 448 BAYLIS ET AL.: NEW ZEALAND FUR SEAL FORAGING SITE FIDELITY 11 0.6 0.4 0.4 0.7 0.2 0.7 1.3 0.5 0.4 0.7 0.5 0.8 0.4 0.7 0.3 0.6 0.3 0.3 0.6 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 12.7 02.9 . . 92.6 82.1 82.7 72.5 02.7 52.3 71.7 93.0 92.7 73.2 22.3 53.5 62.6 63.1 62.9 62.9 02.3 ...... 3 2 7 6 8 7 2 1 6 7 2 2 11 4 3 3 3 6 10 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 2 5 2 7 0 0 5 3 3 0 8 1 4 3 8 6 8 6 7 ...... 146 13 128 7 293 25 285 17 368 23 388 26 390 18 345 19 172 18 229 13 547 27 709387 8 14 307 19 206 21 292 7 187 13 63 36 887 17 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 605 180 750 006 744 452 298 518 354 006 591 287 , , , , , , , , , , , , 63 639–728 1 112 331–572 1 126 219–467 860 54 1 134 1 144 455–658 1 101 197–430 707 73 859 246 355–887 1 46 355 174193 111–414 350–459 893 920 116 475–707 1 65 1 11860 136–383 186–636 622 1 232 136–811 2 380 227–1023 1 268 320–798 1 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± Mean Range of Cumulative Table 2. (Continued) Foraging maximum maximum total distance Mean Mean NN 73 2 Autumn Oceanic 684 DC 69 4 Autumn/winter Oceanic 440 DC 70 3 Autumn/winter Oceanic 330 NN 75 2 Autumn Oceanic 556 Colony ID FT Season location distance (km) distance (km) traveled (km) duration (d) speed (km/h) DC 74 5 Autumn/winter Oceanic 308 LIG 61 4 Autumn/winter Oceanic 554 Mean Oceanic 458 DCDC 75 76 8 3 Autumn/winter Autumn/winter Oceanic Oceanic 259 360 Mean LIG 592 NN 53 3 Autumn Oceanic 594 DCDC 77 36 2 4 Autumn/winter Autumn/winter Oceanic Oceanic 253 420 Mean DC 339 Mean Shelf 127 Mean NN 611 LIG 68 2 Autumn Oceanic 647 LIG 72 3 Autumn/winter Oceanic 539 LIG 56 4 Autumn/winter Oceanic 630 12 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2011

Table 3. The overlap in area and time spent in area between consecutive foraging trips. Also presented is the maximum time spent in one 5 × 5 km area, recorded from 31 lactating New Zealand fur seals from Cape Gantheaume, CG; Cape du Couedic, DC; North Neptune Island, NN; and Liguanea Island, LIG. All values are mean ± SD.

Overlap in Maximum time Foraging Overlap in time spent spent in area Colony ID FT location area (%) in area (%) (% total time) CG 68 3 Shelf 24.5 ± 4.224.3 ± 14.89.9 ± 5.9 CG 691 2 Shelf 78.7 42.7 19.1 ± 4.8 CG 692 3 Shelf 68.9 ± 10.255.9 ± 16.316.1 ± 1.1 CG 693 5 Shelf 62.9 ± 4.858.3 ± 16.513.0 ± 4.2 CG 702 5 Shelf 53.6 ± 16.748.8 ± 19.58.2 ± 2.8 CG 711 4 Shelf 76.7 ± 14.266.8 ± 17.818.3 ± 11.0 CG 712 2 Shelf 58.6 42.5 13.4 ± 8.9 CG 721 4 Shelf 54.4 ± 34.545.7 ± 33.725.2 ± 7.3 CG 723 3 Shelf 58.9 ± 2.743.3 ± 13.714.7 ± 12.2 CG 731 3 Shelf 65.6 ± 13.347.6 ± 12.29.0 ± 6.9 CG 732 3 Shelf 12.5 ± 7.35.1 ± 2.611.8 ± 5.4 Mean CG 55.9 ± 20.443.7 ± 16.814.4 ± 5 CG 74 3 Oceanic 12.3 ± 6.18.3 ± 5.98.1 ± 2.1 CG 76 3 Oceanic 19.0 ± 4.618.0 ± 10.22.8 ± 0.2 CG 703 2 Oceanic 25.0 23.4 2.5 ± 0.5 CG 713 3 Oceanic 10.9 ± 2.26.0 ± 2.53.4 ± 2.2 CG 722 3 Oceanic 9.0 ± 10 4.5 ± 3.32.6 ± 1.7 CG 733 2 Oceanic 34.5 15.7 3.0 ± 1.9 Mean CG 18.5 ± 10.812.7 ± 7.83.7 ± 2.2 DC 69 4 Oceanic 21.2 ± 30.315.8 ± 19.92.5 ± 0.7 DC 70 3 Oceanic 13.3 ± 2.28.1 ± 3.25.0 ± 2.3 DC 74 5 Oceanic 14.4 ± 8.210.9 ± 4.83.0 ± 0.5 DC 75 8 Oceanic 17.3 ± 9.112.7 ± 6.16.8 ± 5.9 DC 76 3 Oceanic 16.1 ± 20.612.0 ± 16.04.9 ± 4.0 DC 77 2 Oceanic 16.6 7.9 6.5 ± 3.8 DC 36 4 Oceanic 12.9 ± 16.0 ± 2.74.5 ± 0.4 Mean DC 16.0 ± 11.910.5 ± 8.54.7 ± 1.6 NN 73 2 Oceanic 7.5 ± 0.14.0 ± 0.12.9 ± 0.4 NN 75 2 Oceanic 11.4 5.0 4.3 ± 1.1 NN 53 3 Oceanic 8.0 ± 0.67.8 ± 6.65.5 ± 1.9 Mean NN 9.0 ± 1.75.6 ± 3.84.2 ± 1.3 LIG 68 2 Oceanic 2.9 2.8 3.3 ± 0.2 LIG 72 3 Oceanic 4.5 ± 3.02.9 ± 0.82.3 ± 0.3 LIG 56 4 Oceanic 5.6 ± 3.74.6 ± 3.35.1 ± 2.6 LIG 61 4 Oceanic 5.8 ± 3.74.9 ± 3.72.4 ± 0.4 Mean LIG 4.7 ± 1.43.6 ± 1.32.7 ± 1.0 Mean shelf 55.9 ± 20.443.7 ± 16.814.4 ± 5 Mean oceanic 13.4 ± 7.69.0 ± 5.74.0 ± 1.7 BAYLIS ET AL.: NEW ZEALAND FUR SEAL FORAGING SITE FIDELITY 13

Figure 2. The relationship between the mean maximum distance traveled and the mean overlap in consecutive foraging trips (r2 = 0.59, P = 0.006), recorded by 20 lactating New Zealand fur seals that foraged in oceanic waters. which were greater than the 9% ± 2% and 4.7% ± 1.4% recorded from North Neptune Island and Liguanea Island, respectively. Differences in foraging route overlap were correlated with the distance and duration of foraging trips. There was a signiﬁcant negative correlation between mean distance and successive foraging route overlap for oceanic females (r2 = 0.59, P = 0.006). In general, the further an individual traveled the lower the spatial overlap (Fig. 2). Despite differences in distance and duration between seals foraging in oceanic waters, the mean speed traveled was not signiﬁcantly different between colonies (LMM: F3,25.6 = 0.26, P = 0.8) (Table 1).

DISCUSSION The current study demonstrates a degree of foraging site fidelity by individual New Zealand fur seals that varied in relation to the continental shelf and oceanic habitats exploited. Fidelity to foraging sites in New Zealand fur seals also exists at the colony level (see Baylis et al. 2008a and Fig. 1) and this is also the case for Northern fur seals (Robson et al. 2004, Call et al. 2008). However, the degree of foraging site fidelity may vary depending on the spatial scale used in analysis. Accordingly, our use of 5 × 5 km cells to explore foraging route overlap limits our ability to make broad conclusions, because foraging route overlap maybe more or less at different scales. We were unable to conduct analyses of fine scale movements because of the relatively large error associated with the predominantly low class of 14 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2011

Argos ﬁxes (classes 0 and A) and the limited number of at-sea locations for some individuals. Nevertheless, this study provides a compelling example of foraging site ﬁdelity in contrasting habitats.

Individual Foraging Site Fidelity Lactating New Zealand fur seals recorded similar average bearings on repeat foraging trips, indicating directional fidelity to foraging areas. Although speculative, we suggest that New Zealand fur seals learn the direction of travel to a predictable foraging region and initiate a foraging trip on that bearing; as has been previously hypothesized for other pinniped species (Bonadonna et al. 2001, Bradshaw et al. 2004, Robson et al. 2004, Call et al. 2008). This memory-based knowledge would be valuable from an optimal foraging perspective because it would allow individuals to travel directly to foraging regions, presumably maximizing the time spent in regions where the chance of encountering preferred prey is higher (Bonadonna et al. 2001, Bradshaw et al. 2004, Staniland et al. 2004). Females from two of the four colonies studied (Cape du Couedic and Liguanea Island), recorded shorter foraging trip distance and duration over time (between autumn and winter) but maintained directional fidelity to foraging areas. Although the reasons for this seasonal shift remain unclear, we assume prey encountered by females during outbound journeys were sufficient to negate the need for longer foraging trips. This may reflect productive foraging regions, perhaps associated with a temporal fluctuation in the location of the STF, becoming available closer to continental Australia during winter months. These findings indicate that an individual’s actual foraging route is likely to be influenced by a number of factors, including previous foraging trip success and prey encounter rates, which are related to distributions, densities, and the renewal rates of prey encountered (Irons 1998, Boyd 1999, Bradshaw et al. 2004).

Continental Shelf vs. Oceanic Habitats and Colony Differences The degree of foraging site fidelity (as measured by the spatial overlap between consecutive foraging routes) was influenced by the type of habitat exploited (shelf or oceanic) and the distance traveled. New Zealand fur seals that utilized continental shelf waters recorded relatively high spatial overlap between consecutive foraging trips and comparatively short foraging trip distances and durations, when compared to females that foraged in oceanic waters. Conversely, females that foraged in oceanic waters recorded limited spatial overlap between consecutive foraging trips, with the degree of spatial overlap correlated to foraging trip distance and duration which varied between seasons (Fig. 2). These findings are consistent with Bonadonna et al. (2001) who reported a higher “fidelity-index” (based on foraging trip bearing) for lactating Antarctic fur seals on short foraging trips. Given that foraging routes are ultimately influenced by the distributions, densities, and renewal rates of prey encountered, the observed differences in foraging route overlap and in time spent in area between seals that foraged in continental shelf and oceanic waters may reflect differences in both the spatial scale of the habitats and the physical processes that operate within these habitats. For example, the continental shelf region to the southeast of Cape Gantheaume is confined to a relatively small area that is characterized by a highly productive and seasonally predictable (November–April) coastal upwelling (Ward et al. 2006, Nieblas BAYLIS ET AL.: NEW ZEALAND FUR SEAL FORAGING SITE FIDELITY 15 et al. 2009). A concomitant study by Baylis et al. (2008b) found that thermoclines (a surrogate measure for upwelling activity) were recorded on 81% of foraging nights in autumn. The high foraging site fidelity recorded by seals that foraged on the continental shelf during autumn may therefore reflect concentrations of productivity resulting from the Bonney Upwelling system (Ward et al. 2006). This would support previous studies that suggest high foraging site fidelity occurs in regions where there is strong physical forcing (Irons 1988, Weimerskirch 2007). However, during winter, the continental shelf region is characterized by a predominantly isothermal water column and presumably low productivity (limited enrichment of shelf waters) (Ward et al. 2006, Baylis et al. 2008b, van Ruth et al. 2010). Nevertheless, the high foraging site fidelity recorded in winter by seals that foraged on the continental shelf does indicate preferred prey was available and predictable over winter. In addition, lactating fur seals that forage on the continental shelf are able to access preferred prey at or near the benthos (Page et al. 2005, Baylis et al. 2008b). It is possible that foraging site fidelity on the continental shelf is facilitated by benthic foraging (Cook et al. 2006). Benthic foraging could aid consecutive foraging trip navigation via topographic cues, if these were linked with location or quality of prey (Cook et al. 2006). In contrast to the continental shelf region, oceanic waters utilized by lactating seals were associated with the STF, a major ocean boundary that separates warm, saline, nutrient poor subtropical waters to the north of the STF, from relatively cool, less-saline, nutrient rich subantarctic waters to the south (Bradford-Grieve et al. 1999). The STF is a continuous east-west oceanographic feature to the south of Australia (Tomczak et al. 2004). It is characterized by cold and warm water filaments, intrusions, and subsurface anomalies associated with the mixed layer, indicating some degree of spatial variability exists (Tomczak et al. 2004). Although seals that foraged in oceanic waters had similar bearings on consecutive foraging trips, they did not focus their foraging effort within a particular area but tended to cover more area, presumably in search of prey. A similar finding was also reported for Antarctic fur seals on “long” foraging trips (Bonadonna et al. 2001). This implies oceanic foraging habitats frequented by New Zealand fur seals may be characterized by lower density/larger scale resource “patches”, where prey is more dispersed or less predictable at finer scales, when compared to the continental shelf region. Additionally, the longer foraging trip durations required to reach oceanic foraging regions increase the probability that resources have been depleted or have moved actively or passively, before seals return to the same region (Fauchald 1999, Weimerskirch 2007). Therefore, the increased time between consecutive foraging trips may also result in reduced overlap in both area and time spent in area (Weimerskirch 2007). This is supported by the differences recorded in oceanic foraging site fidelity between colonies, which was correlated to foraging trip duration. In the current study, Cape Gantheaume and Cape du Couedic recorded the shortest oceanic foraging trips, and also recorded a higher degree of foraging site fidelity when compared to North Neptune and Liguanea Islands. Lactating New Zealand fur seals that foraged in oceanic waters traveled in excess of 1,000 km from their colonies and had significantly longer foraging trip durations compared to seals that foraged on the continental shelf (maximum distance from colony: 222 km and duration: 15 d vs. 42 d, respectively). Extended foraging trips to oceanic waters come at a potential cost to both lactating females (increases the time and energy required to reach foraging grounds) and nutritionally dependent pups (longer fasting period due to extended trip duration). Given that lactating females are constrained in foraging trip distance and duration by the fasting abilities 16 MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2011 of their pup, they are expected to forage optimally and to maximize the rate of energy delivery to their pup (i.e., pup growth rate) (Orians and Pearson 1979). Studies on seals and seabirds have found that long foraging trips to distant oceanic fronts have a higher energy yield than short foraging trips to continental shelf and shelf-break waters (Weimerskirch and Cherel 1998, Staniland et al. 2007). While we cannot compare caloric values of prey between continental shelf and oceanic habitats, the fact that lactating females repeatedly foraged in oceanic waters indicates prey resources must be more predictable, accessible, and/or profitable in oceanic waters adjacent to Liguanea Isand, North Neptune Island, and Cape du Couedic, when compared to continental shelf waters in autumn and winter. Accordingly, temporal and spatial resource predictability is an important tenet within central place foraging theory. Foraging success and subsequent breeding success are ultimately determined by the ability of predators to locate and effectively exploit resources (e.g., Lea et al. 2006). A degree of resource predictability over broad spatial scales may allow New Zealand fur seals to conduct long foraging trips to distant oceanic waters, while still maintaining a suitable rate of milk delivery to dependent offspring and meeting their own energy requirements. Current population trends indicate that the Cape Gantheaume, Cape du Couedic, North Neptune Island, and Liguanea Island colonies are increasing (reflecting population recovery from 19th and 20th century sealing) (Ling 1999).2 Given all populations are increasing, the differences in foraging trip distance and durations between: (1) seals that foraged in continental shelf and oceanic habitats, (2) colonies, and (3) seals that foraged in oceanic waters, highlights the remarkable plasticity in both foraging and provisioning strategies in this species. Variability in foraging trip durations suggests that a range of maternal attendance patterns is used to maximize fitness, as hypothesized by Georges and Guinet (2000) for subantarctic fur seals (A. tropicalis). Plasticity in foraging strategies is likely to be necessary to cope with seasonal changes in ocean productivity over long pup-rearing periods (Beauplet et al. 2004, Baylis et al. 2008b). This is the first study to explore fur seal foraging site fidelity to continental shelf and oceanic habitats. The level of individual fidelity to discrete oceanographic features described in this study is a key factor to consider when interpreting the habitat size or the foraging distributions of New Zealand fur seals. Our study also highlights that lactating females undertake intrinsically long foraging trips to oceanic waters. It is unclear if foraging trips to oceanic waters are at the “limit” of this central place forager. However, it does raise some compelling questions for future studies. Specifically, are female fitness, offspring growth, and/or survival compromised in years when lactating seals are forced to travel further to reach oceanic foraging grounds? Because the intensity of seasonal upwellings and presumably oceanic fronts change from year to year and because different individuals rely on different habitats, future studies could resolve how foraging location and interannual environmental variability affects maternal provisioning strategies and pup growth.

ACKNOWLEDGMENTS This study was supported through the Fisheries Research and Development Corporation (FRDC) Grants Scheme (PN 2005/031), Nature Foundation SA, Wildlife Conservation Fund,

2Unpublished data provided by Simon. D. Goldsworthy, South Australian Research and Development Institute (Aquatic Sciences), P.O. Box 120, Henley Beach, Adelaide, South Australia 5022, Australia. BAYLIS ET AL.: NEW ZEALAND FUR SEAL FORAGING SITE FIDELITY 17

Holsworth Wildlife Fund, MA Ingram Trust, and the Sea World Research and Rescue Foundation. A. M. M. Baylis received an Australian Postgraduate Award to conduct this project. We thank T. Ward for securing FRDC funding and D. Paton for his support. We also thank the many people that assisted with ﬁeldwork including N. Bool, C. Irriarte, P. Dodd, J. Stuart-smith, D. Illiot, L. Mackenzie, D. Lierch, C. Plueis, L. Einoder, and C. Einoder. This research was conducted under Adelaide University animal ethics Permit S80–2004 and Department of Environment and Natural Resources Permit A24684–3. Four anonymous reviewers provided insightful comments that improved this manuscript.

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Received: 16 June 2010 Accepted: 17 February 2011