J. Zool., Lond. (2001) 254, 391±404 # 2001 The Zoological Society of London Printed in the United Kingdom

Foraging destinations of three low-latitude (Phoebastria)

Patricia FernaÂndez1, David J. Anderson1*, Paul R. Sievert2 and Kathryn P. Huyvaert1 1 Department of Biology, Wake Forest University, Winston-Salem, NC 27109-7325, U.S.A. 2 Department of Natural Resources Conservation, University of Massachusetts, Amherst, MA 01003-4210, U.S.A. (Accepted 6 September 2000)

Abstract Satellite telemetry was used to identify the foraging distributions of three congeneric species of that nest in the tropics/subtropics. Breeding waved albatrosses Phoebastria irrorata from the GalaÂpagos Islands travelled to the productive upwelling near the Peruvian coast and nearby areas during the rearing period in 1996. Black-footed albatrosses P. nigripes and Laysan albatrosses P. immutabilis nesting in the Hawaiian Islands and tracked during the 1997±98 and 1998±99 breeding seasons also performed long foraging trips, to continental shelf areas of North America. In both years, breeding black-footed albatrosses made long trips to the west coast of North America (British Columbia to California). In 1997±98, breeding Laysan albatrosses travelled primarily to the north of the Hawaiian Islands and reached the waters of the Aleutian Islands and the Gulf of . In 1998±99, Laysan albatrosses had a complete breeding failure, and no long trips by breeders were tracked as a result. These three species mixed short and long trips during the chick-rearing period, but not the brooding period nor incubation period. Waved albatrosses made only long trips during the incubation period. Analysis of movement patterns showed that the core feeding areas during long trips were located over the continental shelves of North and South America. The data on foraging biology of these species have implications for assessing risk in commercial ®sheries.

Key words: albatross, Phoebastria, foraging, bycatch

INTRODUCTION particularly distribution of albatrosses at sea in relation to bycatch risk in ®sheries operations (Croxall & Prince, Recent advances in satellite telemetry have opened a 1996; Brothers et al., 1998; Prince, Croxall et al., 1998). window on the previously obscure life of albatrosses at Most of the albatross species that have been tracked sea. They have shown, for example, that breeding by satellite nest on high-latitude islands in the Southern wandering albatrosses Diomedea exulans can cover Ocean. Little is known about the foraging characteris- between 3600 and 15 000 km between visits to their tics of the albatross species nesting in the tropics and chick, reaching speeds of up to 80 km/h over distances subtropics; these species comprise the Phoebas- of up to 900 km/day (Jouventin & Weimerskirch, 1990). tria, the `North Paci®c' albatross (see Robertson This technique has been applied to various studies of & Nunn, 1998). Of these species, the black-footed foraging , documenting resource parti- albatross P. nigripes and P. immut- tioning between sympatric species (Waugh et al., 1999) abilis nest primarily in the Hawaiian Islands and are and between sexes (Prince, Wood et al., 1992), changes sympatric on most of their breeding islands. The short- in foraging behaviour through the breeding season tailed albatross P. albatrus, currently limited to a single (Weimerskirch, Salamolard et al., 1993; Arnould et al., breeding population on Torishima Island, Japan, and 1996; Weimerskirch, Wilson & Lys, 1997), biotic and the P. irrorata of the GalaÂpagos Islands abiotic properties of the feeding site (Rodhouse & are the remaining members of the genus. The objective Prince, 1993; Weimerskirch, Doncaster et al., 1994; of this study was to use satellite telemetry to identify the Cherel & Weimerskirch, 1995; Weimerskirch, Wilson, foraging areas of three of these species: black-footed, Guinet et al., 1995; Hull, Hindell & Michael, 1997), and Laysan, and waved albatrosses. Ship-based sightings show that Laysan albatrosses *All correspondence to: D. J. Anderson. are observed and recovered in greatest numbers in the E-mail: [email protected] north-western part of the Paci®c during their breeding 392 P. FernA ndez ET AL. season, whereas the number of black-footed albatrosses Laysan albatrosses, also during brooding. One set of 16 increases to the south-east and east, to the North were tracked through their entire breeding effort, American coast, during the same period (Shuntov, but transmitters recovered from 3 birds whose chicks 1974). The distribution data used to reach these conclu- died was mounted on 3 other individuals (2 black- sions depended in part on the distribution of boats footed and 1 Laysan albatross). Therefore, in 1998±99, bearing observers, with the resulting potential for sam- a total of 10 black-footed albatrosses and 9 Laysan pling bias. Satellite tracking overcomes this bias by albatrosses were tracked. Overall, a total of 48 alba- having no geographical limits on observers. Satellite trosses (25 black-footed and 23 Laysan) were tracked tracking also allows the study of movements of speci®c for 4±182 days (x = 57 days). No was tracked in individuals of known status throughout their entire trip, both seasons. Transmitters in both seasons used 8 h on : which is not possible using non-telemetric methods. For 24 h off duty cycles. example, in a preliminary study satellite tracking was Previous satellite tracking studies of albatrosses have used to study movements of waved albatrosses during concluded that the PTT does not affect the perfor- the incubation period in 1995 (Anderson, Schwandt & mance of the bird measurably during the breeding Douglas, 1998). All tracked birds `commuted' c. 1200 km season (Jouventin & Weimerskirch, 1990; Prince, Wood from the breeding site on Isla EspanÄola, GalaÂpagos to et al., 1992; Wiemerskirch & Robertson, 1994; Arnould the cold upwelling area over the western South Amer- et al., 1996; Anderson et al., 1998). Moreover, innova- ican continental shelf, off the coasts of Peru and tions in the design of the transmitters have reduced Ecuador. While movement between GalaÂpagos and the their size; the mass of our transmitters (32 g) was c.1% continental shelf was direct and rapid, movement within of the bird's own mass, and was unlikely to impose a the upwelling zone was slow with frequent turning. signi®cant energetic cost on tagged birds (Anderson Simple distribution data would indicate that waved et al., 1998). Nevertheless, to identify any effect of albatrosses occupy the entire area between GalaÂpagos transmitters on the birds' reproductive success, we and the continent, while the satellite tracking data monitored nest histories of 20 time-matched nests, revealed the area-speci®c behaviour of the birds. located near the nests of tagged birds, that served as controls. We demonstrated that length accurately indicates gender by associating cloacal distension, at MATERIALS AND METHODS the time of laying, with beak length. Within Laysan albatross breeding pairs, 20/21 (95.2%) of males had Seven waved albatrosses breeding on Isla EspanÄola, longer than their mates did. Similarly, 33/33 GalaÂpagos (1822'S, 89839'W) were tracked between (100%) of black-footed albatross males had longer 4 June and 13 October 1996, during the brooding beaks than their mates did. Beak length of both (hatching to chick age 18 days) and rearing (chick age members of a pair was used to determine the gender of > 18 days; Harris, 1973; Whittow, 1993a,b) periods as a the birds tracked in this study. In both the GalaÂpagos complement to work in the previous breeding season and studies birds were chosen for tracking and during the incubation period, using the methods of for controls using only 2 criteria: they had a nest in the Anderson et al. (1998). PTT100 (Platform Transmitter area designated for the study and they had hatched Terminals; Microwave Telemetry, Columbia, MD) their egg. We are not aware of any other bias in our transmitters were attached to dorsal contour choice of study or assignment to tracked or using epoxy glue. The signals from these transmitters control groups. were received by orbiting TIROS-N satellites, passed to Argos System performance on Tern Island was Argos System ground stations (Service Argos, Largo ground-truthed by comparing the reported locations of MD), and forwarded to us by electronic mail. all transmitters during 5 days with a known, stationary The two Hawaiian albatross species breeding on Tern location (by GPS). Anderson et al. (1998) conducted a Island (23852'N, 166817'W), French Frigate Shoals, similar exercise at the GalaÂpagos nesting site. To north-west Hawaiian Islands were also studied. Tape analyse the performance of the transmitters at different attachment, rather than glue, was used to ®x the trans- locations and years, we calculated the mean number of mitters to the mid-dorsal feathers of the mantle signals received per transmitter per day during each year (FernaÂndez, 1999). In January 1998, 12 PTT100 units of the study. These means were pooled and their were mounted on 6 Laysan and 6 black-footed alba- average calculated; the variation in reception frequency trosses during the brooding part (hatching to chick age is expressed with the standard error (se), as is commonly 18 days) of the nesting cycle. The transmitters were used to present the standard deviation of statistics removed from the ®rst set of birds after 10±16 days and (Sokal & Rohlf, 1995). re-mounted on a second set of 12 breeding adults. Five Descriptions of the movement parameters (distance, of these transmitters were recovered for deployment on maximum range, and days spent at sea) during the a third set of breeders, as a result of which, we were able breeding season were based on complete round-trips to track a total of 15 black-footed and 14 Laysan only. However, all those trips in which the transmitter albatrosses during the 1997±98 breeding season. In the fell off or the battery died (for 1997±98, 2 black-footed subsequent breeding season in January 1999, 8 transmit- albatrosses and 5 Laysan albatrosses; for 1998±99, 4 ters were mounted on black-footed albatrosses and 8 on black-footed albatrosses, 5 Laysan albatrosses) were Foraging destinations of three low-latitude albatross species 393 used to determine locations of foraging sites and dis- tribution at sea during these 2 years. (a) 1998 n = 37 The distance travelled was calculated by summing the 200 distance between every pair of consecutive locations 150 within a trip, using the Great Circle Formula (Fitzpa- n = 59 trick & Modlin, 1986). Speed was calculated using 2 n = 140 consecutive locations separated by at least 2 h. This 100 method prevented spurious calculations of high speeds over short time intervals that resulted from the inherent 50 n = 20 n = 60 n = 142 error of satellite ®xes. We also excluded pairs of points separated by > 8 h; because of the duty cycle of the 0 PTTs, pairs were separated by  8hor 24 h. Turning (b) 1999 n = 82 Error (km) angles were calculated using 3 consecutive locations 200 n = 160 within a single trip. 150 n = 86 RESULTS 100

50 Argos system performance n = 33 n = 94 n = 187

Since the transmitters used a duty cycle of 8 h on : 24 h 0 off, they operated only 25% of the total time that they 3210AB Location quality were deployed. On Tern Island, we received an average Fig. 1. Box plot of the error associated with each location of 3.03 (se= 0.17) locations per transmitter per day and quality provided by the Argos System (from the higher to the a total of 5417 locations during the 1997±98 breeding season, and 4.10 (se= 0.46) locations per transmitter per lower accuracy: 3, 2, 1, 0, A, B). Median, line; 25th and 75th day and a total of 5411 locations during the 1998±99 percentiles, box; points, outliers; error bars also shown. Data season. Due to the length and extent of the trips, the from: (a) 1997±98; (b) 1998±99. duty cycle of the transmitters did not limit the character- ization of the foraging trips of these species. The Argos System assigns six different qualities (from that ¯edged 14/14 (100%) offspring (Yates corrected the most accurate to the least: 3, 2, 1, 0, A, B) to w2 = 10.49, d.f. = 2, P < 0.05). In 1998±99 all nine control locations based on an evaluation of transmitter signal and all nine tagged Laysan albatross nests failed. In strength. Ground-truthing data for the Hawaiian 1997±98 control black-footed albatrosses ¯edged 18/20 species (Fig. 1) showed that location quality B had a (90%) offspring compared to transmitter-bearing birds markedly higher degree of error than other quality that ¯edged 13/15 (87%) offspring (Yates corrected classes did: thus we omitted these data from our analysis w2 = 0.05, d.f. = 2, P=0.82). In 1998±99 control black- and used 3506 (85.6%) and 4636 (85.7%) of the 1997±98 footed albatrosses ¯edged 7/8 (88%) offspring compared and 1998±99 locations, respectively. to transmitter-bearing birds that ¯edged 5/8 (63%) This work includes a follow-up study on waved alba- offspring (Yates corrected w2 = 0.33, d.f. = 2, P=0.56). tross foraging behaviour (Anderson et al., 1998). We These data offer no evidence of a negative effect of analysed the data from the 1996 brooding period, when transmitters on breeding albatrosses. It was not possible 465 locations were received. The average frequency of to document the success of the waved albatrosses to the reception from waved albatrosses was low (1.28 end of the breeding season, but our previous experience (se= 0.08) locations per transmitter per day), because indicates no negative effect of transmitters (Anderson the girth of the Earth at the equator limits the number of et al., 1998). satellite passes per day (Service Argos, 1988). Thus we used all the locations that were collected regardless of their location quality. As a result, 30% of the GalaÂpagos Waved albatross movements locations were of the lowest location quality with an average error of 17.8 km (Anderson et al., 1998). The 1996 rearing period accuracy of the Argos System in the GalaÂpagos study (Anderson et al., 1998) was similar to or better than that A total of 19 trips was recorded (in three of these trips further north in the Paci®c Ocean (Fig. 1). the transmitter ceased operation) from seven indivi- duals. The results from this study were similar to those of Anderson et al. (1998) during the incubation period Effects of transmitters on breeding performance when waved albatrosses travelled to the continental shelf off the western South American coast, reaching the In 1997±98, control Laysan albatrosses ¯edged 8/20 waters of Peru and Ecuador. During the rearing period (40%) offspring compared to transmitter-bearing birds of 1996, they also travelled primarily to the same area 394 P. FernA ndez ET AL.

90° 85° 80° 75° 0.5 Brooding period Isla Chick-rearing period Española 0.4 ° 0 0.3 Ecuador 0.2 Frequency 0.1 5° 0 0 500 1000 1500 2000 2500 3000 3500 Perú Distance travelled (km) Fig. 3. Frequency distribution of distance travelled by waved 10° albatrosses Phoebastria irrorata during foraging trips in the 1996 breeding season.

Black-footed albatross movements during the breeding 15° 150 km season

Fig. 2. Distribution at sea of breeding waved albatrosses 1997±98 breeding season Phoebastria irrorata during the 1996 chick-rearing period. During this period 77 complete trips were recorded from this species. Black-footed albatrosses travelled (Fig. 2). The maximum foraging range during this mostly to the north and north-east of the nesting site period was 1228 km from EspanÄola Island. They (Fig. 4) during the breeding season. They ranged from covered waters between 0o±118S and 788W±918W. tropical to subarctic latitudes (188N±488N) and over a However, we also documented short trips during the broad range of longitude in the eastern north Paci®c brooding period lasting < 5 days around the tropical (1218W±1728W). waters of the GalaÂpagos Islands (Fig. 3). Later in the The time spent at sea and the distance travelled from season short (< 5 days at sea) and long trips (> 7 days at the nesting grounds changed during the breeding season sea) were also mixed (Fig. 3), as during the brooding (Table 2). During the brooding period, when chicks are period. The median of maximum ranges during the attended very closely, parents remained in the vicinity of brooding period (n = 6) was 430 km and the median the nesting site (Fig. 5) on trips lasting a maximum of distance covered was 1245 km (Table 1). During the 11 days and reached a median maximum range of rearing period the median of maximum ranges was 303 km and travelled a median distance of 692 km 730 km and the median distance covered per round trip (Table 2). When we compared distance of consecutive was 1764 km, not signi®cantly different from values trips, we found no signi®cant correlation during either during the brooding period (Table 1). Both the distance the brooding (rs = 0.11, n = 29, P = 0.57) or rearing covered and the maximum range were positively periods (rs = 70.21, n = 29, P = 0.27); that is, trips correlated with trip duration (n = 10; for distance rs =0.85, neither became increasingly longer nor were alternated P < 0.01; for maximum range rs =0.76, P =0.01). Short in a short±long fashion. Instead, dramatically longer trips comprised 50% of all trips during both the brooding trips began to occur at the transition from the brooding period (3/6) and the rearing period (5/10). to the rearing period: the median trip distances during

Table 1. Descriptive statistics of waved albatross Phoebastria irrorata foraging trips during the 1996 breeding season. The median of all trips was calculated using every trip recorded during this period. The median of all birds was calculated using each individual bird's median as a data point. None of the comparisons between brooding and chick-rearing period was signi®cantly different at P < 0.05 level

Distance travelled (km) Maximum range (km) Trip duration (days)

Period Median, trips Median by bird Median, trips Median by bird Median, trips Median by bird (chick age) Min±max n Min±max n Min±max n Min±max n Min±max n Min±max n

Brooding 1245 1409 430 539 10 11.5 (0±18 days) 75±3129 75±3129 35±1228 35±1228 1±21 1±20 646464 Chick-rearing 1563 1588 730 730 6 6 (> 18 days) 144±3078 237±3053 72±1296 74±1296 1±27 3±27 10 6 10 6 10 6 Foraging destinations of three low-latitude albatross species 395

Table 2. Descriptive statistics of black-footed albatross Phoebastria nigripes foraging trips during the 1998 breeding season. The median of all trips was calculated using every trip recorded during this period. The median of all birds was calculated using each individual bird's median as a data point. Bold numbers are signi®cantly different

Distance travelled (km) Maximum range (km) Trip duration (days)

Period Mediana, trips Median by birds Medianb, trips Median, by birds Medianc, trips Median by birds (chick age) Min±max n Min±max n Min±max n Min±max n Min±max n Min±max n

Brooding 692 684 303 301 2 2 (0±18 days) 195±3569 457±1402 97±1099 133±559 1±11 1.5±3.5 42 12 42 12 42 12 Chick-rearing 3,424 4,117 1,174 1,556 9 9.5 (> 18 days) 153±14 212 1660±14 212 73±4523 658±4436 1±28 4±26 35 8 35 8 35 8 a Mann±Whitney U = 263, n 1 = 42, n2 = 35, P < 0.01. b Mann±Whitney U=261, n1 = 42, n2 = 35, P < 0.01. c Mann±Whiney U = 324, n1 = 42, n2 = 35, P < 0.01.

175°E 165°W 145°W 125°W suggesting that they may have been following boats; others foraged up and down the continental shelf. Males N. America and females seemed to have similar foraging behaviour during this period, but de®nitive conclusions cannot be made since females are over-represented in the sample (two males, six females; Fig. 4). One of the two males also approached the coast of North America, high- 40° lighting the importance of this zone as a foraging destination for both male and female black-footed albatrosses. Trip distance and maximum range were positively correlated with the duration of foraging trips (brooding period, distance rs = 0.76, n = 42, P < 0.01 and maximum range rs = 0.73, n =42, P < 0.01; rearing period, distance ° rs = 0.92, n = 35, P < 0.01 and maximum range, rs = 0.89, 20 n = 35, P < 0.01). It is important to note that during the Tern Island rearing period the maximum range reached a plateau of Female 4500 km when birds arrived at the west coast of North Male 500 km America; the minimum time for such a round-trip was 15 days. Fig. 4. Distribution of male and female black-footed alba- trosses Phoebastria nigripes in the north Paci®c Ocean during the 1998 breeding season. 1998±99 breeding season

To determine if movement patterns were similar across these two periods were signi®cantly different (Mann± years we intended to track the same birds in two Whitney U = 263, n1 = 42, n2 =35, P < 0.01) as were the different years, but during the 1998±99 breeding season maximum ranges and trip durations (maximum range: we did not encounter most of the individuals tracked in Mann±Whitney U = 261, n 1 = 42, n 2 = 35, P < 0.01; trip the previous season, and the ones that were encountered duration: Mann±Whitney U = 324, n 1 = 42, n 2 = 35, had a high hatching failure. Therefore, during the 1998± P < 0.01). 99 breeding season 10 new breeders were tracked (®ve During the rearing period, black-footed albatrosses birds of each sex). During this period, 46 complete trips mixed short trips near Hawaii with long trips over were recorded, and in four other trips the transmitters pelagic waters, frequently reaching the continental shelf stopped functioning, probably as a result of attachment of North America (Table 2, Fig. 5). Of the eight failure. During two trips, the forager's chick died but individuals followed during the rearing period, six of the parents presumably did not know this fact and them approached the continental shelf of North behaved in a similar way as during the preceding trips, America (California to British Columbia) from 348Nto including returning to the nest to end the trip. We 488N. Most of these trips followed a looping route. included these two trips in the following analysis. Remarkably, some of the individuals reached the same In general, the direction of the trips was very similar location several times (see Fig. 6), and in some of these to that of the previous year; black-footed albatrosses trips they ¯ew on a straight line to San Francisco Bay, ranged from 198N±518N and 1238W±1758W (Fig. 7), 396 P. FernAÂ ndez ET AL.

155°E 165°W 125°W

500 km

40°N

Tern Island

° Flight speed (km/h) 20 N

(a) (b) Chick-brooding period Chick-rearing period ) ° Turn angle ( Turn

(c) (d)

Fig. 5. Black-footed albatross Phoebastria nigripes ¯ight speeds and turning angles at known locations during: (a), (c) brooding periods; (b), (d) rearing periods. (a), (b) Speeds: 0±15 km/h, closed circles; > 15 km/h, open circles. (c), (d) Turning angles: 0±90o, closed circles; > 90o, open circles. approaching the west coast of North America. Their to the previous year's results, these two types of trip movements changed in some respects through the dif- were easily distinguishable in 1998±99: short trips lasted ferent stages of the breeding cycle. During the 1998±99 0±3 days and long trips lasted 8±23 days. We docu- brooding period they travelled for longer periods mented no trips of 4±7 days. No statistically signi®cant (Tables 2 & 3) and reached more distant points than relationship existed between the distance covered during during the previous year's brooding period (for distance, consecutive trips during the rearing period (rs =70.21, Mann±Whitney U = 397, n1 = 42, n2 = 30, P < 0.01; n =10, P = 0.56), but a suggestion exists in the negative maximum range, Mann±Whitney U = 418, n 1 = 42, correlation coef®cient of alternating short and long n 2 = 30, P = 0.02; trip duration, Mann±Whitney trips. In contrast to the results for the brooding period, U = 412, n1 = 42, n2 = 30, P = 0.01). Exceptionally for trips during the rearing period covered similar distances this stage, one female ¯ew to the continental shelf, for similar durations in the two seasons (distance reaching the waters off Oregon and California. This trip Mann±Whitney U = 322, n 1 = 37, n 2 = 18, P = < 0.85; started when the chick was 16 days old and the chick maximum range Mann±Whitney U = 319, n1 = 37, died before the female returned. During the brooding n2 = 18, P = 0.80; trip duration Mann±Whitney U = 296, period, duration of foraging trips was positively corre- n1 = 37, n2 = 18, P = 0.51). Combining all trips, 5/16 lated with the total distance covered and with maximum (31%) trips during the brooding period were short trips. range (brooding period, distance rs = 0.90, n = 29, P < 0.01 and maximum range, rs = 0.88, n = 29, P < 0.01; rearing period, distance rs = 0.82, n = 16, P < 0.01 and Post-breeding movements maximum range, rs = 0.80, n = 16, P < 0.01). The dis- tances of consecutive trips during the brooding period The nestling stage lasts 140 days (Whittow, 1993a), and were positively correlated (rs = 0.56, n = 20, P = 0.01); after this period in 1997±98 one female was followed but that is, breeders did not alternate short and long trips. the trip was recorded incompletely because the During the rearing period, both short and long trips transmitter ceased operation. This female's destination occurred, as in the 1997±98 breeding season. Contrary was primarily along the coasts of Oregon and Foraging destinations of three low-latitude albatross species 397

Table 3. Descriptive statistics of black-footed Phoebastria nigripes albatross foraging trips during the 1999 breeding season. The median of all trips was calculated using every trip recorded during this period. The median of all birds was calculated using each individual bird's median as a data point. Bold numbers in the same column are signi®cantly different

Distance travelled (km) Maximum range (km) Trip duration (days)

Period Mediana, trips Median by bird Medianb, trips Median by bird Medianc, trips Median by bird (chick age) Min±max n Min±max n Min±max n Min±max n Min±max n Min±max n

Brooding 2198 969 497 407 3 3 (0±18 days) 142±17 428 533±4432 66.6±4442 239±1566 1±35 1.5±8.5 30 10 30 10 30 10 Chick-rearing 5341 5520 1732 2003 12 12.5 (>18 days) 333±14 844 1206±10 642 99±4455 432±3121 1±23 2±18 16 6 16 6 16 6 a Mann±Whitney U = 148, n1 = 30, n2 = 16, P < 0.05. b Mann±Whitney U = 152, n1 = 30, n2 = 16, P < 0.05. c Mann±Whitney U = 126.5, n1 = 30, n2 = 16, P < 0.05.

175°E 165°W 145°W 125°W

3 40° 4 2 1

20° Tern Island

Daytime locations 300 km Night time locations

Fig. 6. Four consecutive long foraging trips of female black-footed albatross Phoebastria nigripes 51C, 26 February±1 June 1998.

California, from the mouth of the Columbia River Laysan albatross movements during the breeding season (47842'N, 124841'W) to Monterey Bay (37844'N, 123826'W). After spending 1 month (May) around the 1997±98 breeding season Columbia River mouth, she travelled to the south along the coast of California and spent 5 days outside San Laysan albatrosses travelled primarily north and north- Francisco Bay. west of Tern Island (n = 54 trips; Fig. 8), reaching the Birds were not followed after they ®nished breeding Gulf of Alaska and the Aleutian Islands and covering in 1998±99, since most of the PTTs ceased operation from 208Nto608N and 1558E to 1258W. The character- before black-footed albatross offspring ¯edged. istics of foraging trips varied through the breeding 398 P. FernAÂ ndez ET AL.

155°E 165°W 125°W 155°E 165°W 125°W

40°N 40°

20°N 20° Tern Island Tern Island Female Laysan albatross Male 500 km Black-footed albatross 500 km

Fig. 7. Hawaiian albatross distribution at sea during the Fig. 8. Distribution at sea of male and female Laysan alba- brooding (Phoebastria immutabilis and P. nigripes) and rearing trosses Phoebastria immutabilis during the 1998 nestling period (black-footed albatross P. nigripes), 1999. period. season. During the brooding period, Laysan albatrosses a shorter range than during the brooding period remained relatively close to the nesting site on Tern (Mann±Whitney U = 44, n1 = 32, n2 =6, P = 0.04). Island: the median distance travelled during this stage During the rearing period we did not ®nd a signi®cant was 1079 km. The foraging range covered during this relationship between the distances of consecutive trips period was similar to that of black-footed albatrosses (rs =70.21, n = 15, P = 0.44), indicating that while (Figs 5 & 9). The distances covered on consecutive trips Laysan albatrosses mix long and short trips during the were positively correlated (rs = 0.79, n = 22, P < 0.01), rearing period, they do not alternate those trips regu- indicating a tendency to increase trip length as the larly. The duration of Laysan albatross trips was brooding period progressed. correlated with both maximum range and distance Trip distance, maximum range, and trip duration travelled in both brooding and rearing period (brooding increased as the breeding season progressed; compari- period, distance rs = 0.80, n = 32, P < 0.01 and maximum sons of brooding period and rearing period values range, rs = 0.80, n = 32, P < 0.01; rearing period, distance revealed signi®cant differences in each parameter rs = 0.89, n = 22, P < 0.01 and maximum range rs = 0.73, (Table 4). During the rearing period, Laysan albatrosses n =22, P < 0.01). Combining all trips, 6/22 (27%) trips mixed short and long trips, which were clearly separable during the brooding period were short trips. as short (1±4 days) and long (12±29 days). The median During the long trips, Laysan albatrosses ¯ew con- distance travelled during the short foraging bouts (n =6) tinuously over great distances, primarily straight north was 879 km and the median maximum range reached of the nesting site, in both looping and linear courses. was 431 km. Therefore, during this stage short trips had The median distance covered during these trips was

Table 4. Descriptive statistics of Laysan albatross Phoebastria irrorata foraging trips during the 1998 breeding season. The median of all trips was calculated using every trip recorded during this period. The median of all birds was calculated using each individual bird's median as a data point. Bold numbers in the same column are signi®cantly different

Distance travelled (km) Maximum range (km) Trip duration (days)

Period Mediana, trips Median by bird Medianb, trips Median by bird Medianc, trips Median by bird (chick age) Min±max n Min±max n Min±max n Min±max n Min±max n Min±max n

Brooding 1079 1411 510 608 3 3 (0±18 days) 291±10 283 473±6347 131±3733 208±2380 1±22 2±13.5 32 12 32 12 32 12 Chick-rearing 7789 8347 2675 2722 14.5 17 (> 18 days) 114±12 609 4854±12 609 51±4010 1639±4010 1±29 9.5±28 22 7 22 7 22 7 a Mann±Whitney U = 168, P < 0.01, n1 = 32, n2 = 22. b Mann±Whitney U = 174, P < 0.01, n1 = 32, n2 = 22. c Mann±Whitney U = 165, P < 0.01, n1 = 32, n2 = 22. Foraging destinations of three low-latitude albatross species 399

155°E 165°W 125°W

500 km

40°N

Tern Island

Flight speed (km/h) 20°N

(a) (b)

Chick-brooding period Chick-rearing period ) ° Turn angle ( Turn

(c) (d)

Fig. 9. Laysan albatross Phoebastria immutabilis ¯ight speeds and turning angles at known locations during: (a), (c) brooding periods; (b), (d) rearing periods. (a), (b) Speeds: 0±15 km/h, closed circles; > 15 km/h, open circles. (c), (d) Turning angles: 0±90o, closed circles; > 90o, open circles.

5012 km and the median of maximum ranges was the Japan current (35845'N, 178841'W) and later moved 1694 km (n = 16). In contrast to black-footed alba- farther north-west, near the Kuril Islands (45855'N, trosses, only one Laysan albatross commuted repeatedly 154853'E). to a speci®c place. This male returned to the neritic waters around two Aleutian Islands (Umnak Island (53810'N, 169808'W) and Unalaska Island (53830'N, 1998±99 breeding season 166820'W)) on four consecutive trips. This bird did not make short trips between these long trips. This breeding season was characterized by high breeding Males and females showed similar movements during failure in the entire Laysan albatross population of Tern foraging trips. During the brooding period, both males Island and other islands in the Hawaiian archipelago and females travelled in the vicinity of the Hawaiian (A. Asquith, pers. comm.). None of the birds tracked in Islands (n = 6 individuals of each sex). During the 1998±99 (n = 9) raised a chick to ¯edging and most rearing period, three females and four males were offspring died early in the breeding season. For the tracked; the genders behaved in like manner, travelling analysis of the data of breeding birds, only complete primarily to the north of the nesting site and over trips initiated when the parent's chick was alive were similar distances (median distance for males = 8602 km; used. The six birds tracked during the brooding period for females = 6124 km; Mann±Whitney U = 39, n 1 = 12, had a median trip duration of 3.5 days at sea (Table 5). n 2 = 10, P = 0.17; Fig. 8). Trip duration was positively related to trip distance and maximum range (distance, rs = 0.82, n = 10, P < 0.01; maximum foraging range, rs = 0.82, n = 10, P < 0.01). 1997±98 post-breeding movements Male Laysan albatrosses travelled a median distance of 1799 km (n = 10); only one female was tracked during One female was still being tracked after its chick ¯edged this season and the mean distance travelled was 2569 km in July. This female travelled north of Tern Island along (n = 2 trips). 400 P. FernAÂ ndez ET AL.

Table 5. Descriptive statistics of breeding and non-breeding Laysan albatross Phoebastria nigripes foraging trips during the 1999 breeding season. The median of all trips was calculated using every trip recorded during this period. The median of all birds was calculated using the bird's median as a data point

Distance travelled (km) Maximum range (km) Trip duration (days)

Period Median, trips Median by bird Median, trips Median by bird Median, trips Median by bird (chick age) Min±max n Min±max n Min±max n Min±max n Min±max n Min±max n

Brooding 1799 2379 722 920 3 3.5 (0±18 days) 416±4972 416±3848 171±1845 171±1497 2±7 3±7 10 6 10 6 10 6 Non-breeding 5329 7755 2197 2430 9 16 birds 363±14 005 1669±14 005 164±3847 766±3847 2±36 4±36 757575

155°E 165°W 125°W (a) Black-footed 0.25 Laysan 40° 0.20

0.15

0.10

0.05

0.00 0 10 20 30 40 50 60 70 80 90 100 20° Flight speed (km/h)

0.15 Frequency (b) Black-footed Laysan

Tern Island 0.10

500 km 0.05 Fig. 10. Distribution at sea of Laysan albatrosses Phoebastria immutabilis after their breeding failure, February±June 1999. 0.00 0 20 40 60 80 100 120 140 160 180 Turning angle (°) Laysan albatross foraging patterns and the areas Fig. 11. Frequency distributions of: (a) ¯ight speeds; (b) covered differed from those of the previous year. Even turning angles, of black-footed Phoebastria nigripes and when the data from the individuals that failed during Laysan albatrosses Phoebastria immutabilis during the 1998 breeding (and so were free to move away from the breeding island) was included in the analysis, we found breeding season. Dotted lines, criteria used to identify speed that they did not travel as far north in 1998±99 as in and turning angle classes in Figs 5 & 9. 1997±98. The farthest northern point reached was 46847'N, 162822'W and none of the birds reached the Analysis of foraging behaviour to determine core feeding waters around the Aleutian Islands in 1998±99. In sites addition, they extended their longitudinal foraging range markedly (Fig. 10). However, the trip durations, To separate foraging from travelling behaviour using distances, and maximum ranges did not differ between our movement data, we assumed that the birds engage years for parents of living nestlings during the brooding in area-restricted searches (Curio, 1976) after locating period (trip distance Mann±Whitney U = 135, n1 = 32, patchily distributed prey, both reducing speed and n2 = 11, P = 0.25; maximum range Mann±Whitney turning at sharper angles when foraging in comparison U = 129, n1 = 32, n2 =11, P = 0.19; trip duration Mann± with travelling. Both parameters can be estimated from Whitney U = 135.5, n1 = 32, n2 = 11, P = 0.25). After the our data, and they are negatively correlated as expected death of their chicks, most of the birds spent a great under this assumption (waved albatrosses, 1996 rearing part of their foraging time along the east coast of Japan period: rs =70.24, n = 221, P < 0.01; black-footed (around 1408E). One female extended her foraging albatrosses, 1997±98 brooding and rearing periods: range to the east to 348N, 1328W. rs =70.38, n = 272, P < 0.01; Laysan albatrosses, Foraging destinations of three low-latitude albatross species 401

1997±98 brooding and rearing periods: rs =70.32, in this species (Whittow, 1993a; Veit et al., 1996). Six n = 786, P < 0.01). In addition, we have found a negative out of 11 foraging trips that we documented included correlation between speed of movement and frequency long, straight tracks from oceanic waters to San of landing on the water (a prerequisite for foraging) in Francisco Bay, perhaps indicating further ship- Laysan and black-footed albatrosses (FernaÂndez & An- following. derson, 2000). Flight speed and turning angle were used as indicators of activity to identify foraging sites. Speeds  15 km/h (58% of the total recorded) were classi®ed as Laysan albatross low speed (Fig. 11a), and turning angles  908 were classi®ed as sharp (Fig. 11b). Figures 5 & 9 show the This species travelled primarily to the north during the spatial distribution of ¯ight speed and turning angle of 1997±98 breeding season, reaching the Aleutian Islands the two Hawaiian species during the 1997±98 brooding and the Gulf of Alaska. In the majority of the trips and rearing period; waved albatrosses in 1996 did not recorded Laysan albatrosses travelled to northern provide enough information for this analysis. During pelagic waters, but the northerly distribution was more the brooding period both species were concentrated in restricted during 1998±99, a year with very low repro- areas around the nesting site where both classes of speed ductive success at the population level. and angle of turn were observed. During the rearing Following offspring death, but still during the period, area-restricted searches were performed most breeding season, the birds extended their foraging range often over the North American continental shelf, in to the west, reaching the east coast of Japan where the species-speci®c areas. We have already shown that these cold waters of the Oyashio current mix with the warmer same areas appeared to be the destinations of the waters of the Kuroshio current. Previous studies at sea longest trips. As a body, these data indicate that areas have identi®ed this area as an important feeding site for over the continental shelves are the principal foraging Laysan albatrosses during the non-breeding season sites of these species during the rearing part of the (Fisher & Fisher, 1972; Shuntov, 1974). It is noteworthy breeding cycle. that we did not record a single individual approaching the coast of California, where Laysan albatrosses have been seen mainly over deeper water offshore, especially DISCUSSION from October to February (Whittow, 1993b); these observations may be of non-breeders or pre-breeders. General features of the foraging movements

Waved albatross Changes in foraging through the breeding season

This study extends the results of Anderson et al. (1998), We established that most, but not all, breeding indivi- indicating that waved albatrosses travel to the cold duals of these three Phoebastria species mix short and upwelling region off the coast of Peru and Ecuador long trips during the nestling period. When parents throughout the breeding season. During the rearing brood alternately they make short trips close to the period, trips were found to have both linear and looping colony. Beginning at approximately chick age 18 days, courses. Also, they performed short trips around the many make both short and long trips. This dual strategy GalaÂpagos Islands during the brooding period and later has been found not only in the family Diomedeidae but in the season they mixed them with long trips. Anderson also in other families of the . et al. (1998) did not ®nd differences in behaviour of Weimerskirch, Chastel et al. (1994) found that long trips males and females during the incubation period. In this of wandering albatrosses were initiated when adult body study, the sex of the individuals was not identi®ed and condition was poor, and short trips were initiated when therefore conclusions about differences in behaviour the chick had not been fed recently. Tveraa et al. (1998) between sexes cannot be made. found that the body condition of parent Antarctic plays a major role in allocation of resources between reproduction and survival. The mixture of Black-footed albatross short and long trips re¯ects a trade-off experienced by breeders between offspring nutrition and parental Breeding black-footed albatrosses directed their condition. foraging ¯ights to waters located east and north-east of the nesting site. These results agree with Shuntov's (1974) data based on boat observations. During both Differences in foraging behaviour between species years of study this species travelled to the west coast of North America during long trips. In both 1997±98 and Tern Island albatross populations covered much of the 1998±99, we received reports of our tagged birds (the Paci®c Ocean north of 238N during their foraging antenna visible on the dorsal surface) following ships activities. Based on 131 complete trips from both hundreds of kilometres from Tern Island (P. Banko & species, we found that they occupy largely non- J. Dutton, pers. comm.), which is a common behaviour overlapping areas of the ocean during the foraging trips 402 P. FernA ndez ET AL.

(Figs 4 & 8), differing in both latitude (black- of the North Paci®c Ocean. The change from El NinÄo footed albatross median = 288N; Laysan albatross (ENSO) conditions, with unusual warm water tempera- median = 418N) and longitude (black-footed albatross tures at the Equatorial Paci®c during 1997±98, to La median = 1618W; Laysan albatross median = 1678W). NinÄa conditions in 1998±99, which have an opposite Water characteristics of the Paci®c Ocean may partly effect on climate, may have affected the reproductive explain the spatial distribution of the Hawaiian species. success of these species. ENSOs are associated with The north-western part of the Paci®c contains subarctic mass mortality in equatorial . Schreiber & waters with a cold intermediary layer, and is typically Schreiber (1989) estimated that during the 1982±83 colder than the north-eastern part (Bigg, 1996). Laysan ENSO 75±90% of the 10 million birds nesting on albatross behaviour is particularly interesting since Christmas Island (108S, 1058E) died as a consequence of nesting on a subtropical island and making trips to the this phenomenon. However, the same study did not ®nd boreal and arctic waters far north signify great tolerance any obvious effects on the reproductive output of of temperature change. Laysan and black-footed albatross nesting on Midway Black-footed albatrosses started making long trips at Atoll, Hawaii (288N, 1798W). Shea & Ricklefs (1996) older offspring ages than did either Laysan or waved also found that most other Hawaiian seabirds were not albatrosses. Studies of food allocation in albatrosses demonstrably affected by the 1982±83 ENSO event, and (Weimerskirch, Cherel et al., 1997) have found that long they concluded that the ENSO effect on tropical sea- trips are energetically poor for the offspring but pro®t- birds did not extend to subtropical North Paci®c able for the parents, while short trips are the opposite. populations. In the ®rst year of this study, during the Therefore, the fact that Laysan and waved albatrosses 1997±98 ENSO, the reproductive success of black- initiated long trips as soon as the chick could be left footed albatrosses did not decrease in comparison to alone, may indicate lower foraging ef®ciency during other years (¯edging success = 68.3%, mean of previous short trips for these species. Black-footed albatrosses years = 68.8% (1984±97); A. Viggiano, pers. comm.), but are known to supplement their diet with ®sheries offal Laysan albatrosses did experience a decline (¯edging (Whittow, 1993a; Gould et al., 1998), and may have a success = 32.8%, the third worst year in 16 years of higher rate of prey catch during short trips among the population studies at the island from 1984 to 1999). Hawaiian Islands-based commercial ®shery than the Laysan albatross chicks that died showed signs of mal- other two species do during short trips. nutrition and the chicks that survived grew slowly in The foraging ranges of the two species contracted comparison to black-footed albatross chicks. For black- during the short chick-brooding period, with both footed albatrosses, we suspect that our data from species performing short trips near Tern Island. 1997±98 represent foraging under typical conditions; the However, the spatial overlap of these two species during situation is less clear for Laysan albatrosses. this stage was only partial since black-footed albatrosses During 1998±99, unusually warm weather occurred at hatch their 2 weeks earlier than Laysan albatrosses Tern Island during normally cool months, followed by (Whittow, 1993a) and so were switching to longer trips signi®cant storms during the period when the chicks at about the time of Laysan albatross egg hatching. were very young (F. Juola & L. Carsten, pers. comm.). Therefore, Laysan albatrosses used the waters close to In addition, La NinÄa conditions included a higher water the nesting site later than did black-footed albatrosses. temperature around the coast of Alaska and a coinci- dent decrease in marine productivity (SeaWiFs, 1999). As a result, the breeding success of both species was low Comparison between years in comparison to previous years, especially for Laysan albatrosses, whose reproductive success (9.0%) for The foraging destinations of the two Hawaiian species 1998±99 was the lowest recorded for the Tern Island during the 1998±99 brooding period were generally population in 16 years of studies of population similar to those of the previous year and the fact that dynamics at the island (1984±99; A. Viggiano, pers. new individuals were used during that year supports the comm.). Between-year comparisons revealed longer idea that an easterly foraging pattern of black-footed foraging trips in 1998±99, both in distance and time, albatrosses and a northerly pattern for Laysan alba- only by black-footed albatrosses and only during the trosses are probably observed in most breeding seasons brooding period. Laysan albatrosses did not perform for the populations at Tern Island. However, in 1998± longer trips in 1999 even though they were experiencing 99, Laysan albatross behaviour changed later in the a dramatic breeding failure. It is possible that the season when the parents lost their chicks, becoming foraging characteristics of Laysan albatrosses revealed failed breeders. None of the individuals tracked tra- by satellite telemetry in both seasons are typical of velled to the Aleutian Islands and their distribution periods of food stress, since reproductive success of this resembled the description of non-breeder behaviour species was low in both seasons. Further studies inte- based on boat observations. grating measures of chlorophyll concentration in the The poor reproductive success of both species, espe- North Paci®c Ocean during the period of study with our cially Laysan albatrosses, during 1998±99 and the documented foraging movements will be useful to expansion of the foraging range during the brooding explain the changes in foraging behaviour and the low period may have been related to changes in the weather reproductive success in this species. Foraging destinations of three low-latitude albatross species 403

Foraging zones of this species is mainly determined by the spatial distribution of these activities in the North Paci®c This is only the second study (after Anderson et al., Ocean. Therefore, it is important to study the distribu- 1998) to use satellite telemetry to provide data on the tion of long-line ®sheries and their impact on black- foraging behaviour of tropical/subtropical albatrosses. footed albatross populations, as well as aspects of diet The changes in movement patterns (decreased ¯ight (Harrison et al., 1983) and diel vs nocturnal foraging speed and sharper turning angles over periods of several behaviour (FernaÂndez & Anderson, 2000). The data hours) during foraging trips suggest that the core provided by this study are invaluable in this respect in feeding areas used by these species during long trips are identifying areas to which Hawaiian albatrosses direct frequently continental shelves. Veit & Prince (1997) their foraging ¯ights. suggested that albatrosses use a form of area-restricted search, in which individuals follow a straight line when they are searching for food; once prey is located they Acknowledgements adopt a circular motion, enhancing the probability of ®nding additional food patches. This switch in foraging We thank L. Carsten, F. Juola, A. Viggiano, and behaviour has been directly related to food ingestion S. Wang for ®eld assistance, and D. Hyrenbach and two using stomach temperature sensors (Weimerskirch, anonymous reviewers for comments on a previous draft. Wilson & Lys, 1997), corroborating the idea that this Funding was provided by National Science Foundation behaviour is associated with feeding activity rather than grants DEB 9304579 and DEB 9629539 and National a response to environmental characteristics of shelves Geographic Society grant 5435-95 to DJA, the US (i.e. changes in wind patterns near land). 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