Ornithol Sci 15: 213 – 225 (2016)

ORIGINAL ARTICLE Dual foraging strategy and chick growth of Streaked leucomelas at two colonies in different oceanographic environments

Daisuke OCHI1,#,*, Kei MATSUMOTO1,**, Nariko OKA2, Tomohiro DEGUCHI2, Katsufumi SATO3, Takashi P. SATOH3,***, Fumihito MUTO3,**** and Yutaka WATANUKI1

1 Graduate School of Fisheries Sciences, Hokkaido University, 3–1–1, Minato-cho, Hakodate, Hokkaido 041–8611, Japan 2 Yamashina Institute for Ornithology, 115 Konoyama Abiko, Chiba 270–1145, Japan 3 Atmosphere and Ocean Research Institute, the University of Tokyo, 5–1–5, Kashiwanoha, Kashiwa, Chiba 277–8568, Japan

ORNITHOLOGICAL Abstract Parent alternate between long-range foraging trips to feed in distant productive marine areas and short-range trips to feed in less productive SCIENCE areas around their breeding colony. Foraging trip duration, diet, energy expenditure, © The Ornithological Society and chick growth of Streaked Calonectris leucomelas were compared of Japan 2016 between two colonies, one on Mikura Island located in the warm and less productive waters of the Kuroshio current, and the other on Sangan Island located in the cold and more productive waters of the Kuroshio/Oyashio transition zone. Parent shearwaters breeding on Mikura alternated between short (≤3 days) trips to Kuroshio waters in order to provision their chicks and long (>3 days) trips to the cold Oyashio region in order to accumulate energy reserves for themselves. Shearwaters breeding on Sangan mainly took short trips (≤2 days) to the nearby Kuroshio/Oyashio transition zone, but also took longer trips (>2 days) to the cold Oyashio region. Parent shearwaters breeding on Mikura, however, made more frequent long trips (24%) than those breed- ing on Sangan (9%). Parents at both colonies commonly brought Japanese Engraulis japonica and Darkedged-wing Flyingfish Cypselurus hiraii for their young, while parents on Mikura also brought Pacific Saury Cololabis saira and stomach oil after long trips. Parents on Mikura delivered energy at a lower rate, resulting in lower chick growth rates and smaller fledging masses than on Sangan. Unlike other Procellariiformes , shearwater parents on Sangan accumulate their own body reserves even during the chick rearing period because of better foraging efficiency than on Mikura. This may indicate that chicks were satiated by the meals delivered to them allowing parents to utilize the remaining provisions for their own body reserves.

Key words Colonial breeding, Energy intake, Feeding behavior, Foraging strategy, Marine environment

Among Procellariiformes seabirds, the distances (Received 27 July 2015; Accepted 28 April 2016) travelled by parents to productive feeding areas is # Corresponding author, E-mail: [email protected] * Present address: National Research Institute of Far Seas highly variable across colonies since they sometimes Fisheries, Fisheries Research and Education Agency, 5–7–1 breed on isolated islands where ocean productivity in Orido, Shimizu, Shizuoka 424–8633, Japan the surrounding waters is poor and must forage in areas ** Present address: Department of Civil and Environmental distant from their colonies (Baduini & Hyrenbach Engineering, Kitami Institute of Technology, Koen-cho 165, Kitami, Hokkaido 090– 8507, Japan 2003; Peck & Congdon 2005). Thus parents attempt *** Present address: Collection Center, National Museum of to compensate for any such feeding deficit by adopting Nature and Science, 4–1–1 Amakubo, Tsukuba, Ibaraki a “dual foraging” strategy (Weimerskirch et al. 1994; 305–0005, Japan Falk et al. 2002; Baduini & Hyrenbach 2003) when **** Present address: School of Marine Science and Technology, Tokai University, 3–20–1 Orido, Shimizu, Shizuoka 424–8610, breed at colonies surrounded by poorly productive Japan waters. They take short-range foraging trips (“short

213 D. OCHI et al. trips”) to the waters with low productivity around 2010; Matsumoto et al. 2012). In contrast, parents their colonies, allowing them to feed their chicks on Sangan were expected to take mainly short forag- frequently, but depleting their own energy reserves ing trips. while they do so. They also take long-range trips The aim of this study was to understand how (“long trips”) to distant, highly productivity waters, the distance to productive waters affects the forag- allowing them to recover their own energy reserves ing and breeding ecology of Streaked Shearwaters, while feeding their chicks intermittently. By adopting and to extend further the data for the Mikura colony this dual foraging strategy, parents are able to main- described by Matsumoto et al. (2012). We examined tain their own energy reserves while ensuring their the oceanographic features around the Mikura and chicks’ growth. Furthermore, parents attempt to bring Sangan colonies, duration of foraging trips, sea sur- energy-concentrated prey items containing abundant face temperature where parents were foraging, body lipids (“stomach oil”) back from long trips (Chaurand mass of parents, prey brought back to chicks, prey & Weimerskirch 1994; Warham 1996). Stomach oil energy density, and chick growth. We expected that: is specifically found in the Procellariiformes; it is (1) parents breeding on Mikura would take long produced in the proventriculus by extracting lipids trips to Oyashio and short trips to Kuroshio waters, from ingested food (Warham 1977, 1996). whereas parents breeding on Sangan would forage The Streaked Shearwater Calonectris leucomelas only in the Kuroshio/Oyashio transition zone around breeds in temperate and sub-tropical regions of the their colony; (2) because of the long distance to Japanese Archipelago, the Koreaan Peninsula, China productive waters, parents on Mikura would deliver and Russia (Oka 2004). Mikura Island (33°52′N, energy at a lower rate (energy brought back to the 139°14′E) is an offshore island situated in the warm chicks per trip-day) and with lower foraging effi- Kuroshio Current, while Sangan Island (39°18′N, ciency (energy intake per trip-day); and therefore, (3) 141°58′E) is a coastal island situated in the transi- chick growth rate and fledgling mass would be lower tion zone of the warm Kuroshio and the cold Oyas- at Mikura than at Sangan. hio currents. Approximately 770,000 adults breed on Mikura and about 72,000–110,000 adults Sangan MATERIALS AND METHODS (Matsumoto et al. 2007; Japanese Ministry of the Environment 2013). Such differences in the foraging 1) Oceanography environment of each colony provide an opportunity The locations of the Kuroshio front and the distal to examine the effects of distance to feeding areas portions of the Oyashio front were estimated based on shearwater foraging and breeding ecology. During on sub-surface sea temperatures obtained from the the chick rearing season of September and October, NEAR-GOOS Regional Delayed Mode Data Base the availability of potential prey (including web site (MOVE/adjsubs; http://near-goos1.jodc. Japanese Anchovy Engraulis japonica and Pacific go.jp/). The Kuroshio front was defined by the 14 Saury Cololabis saira; Matsumoto et al. 2012) is °C isotherm at a depth of 200 m (Kawai 1969) and high in the Kuroshio/Oyashio transition zone and the Oyashio water was defined as <5 °C water at a the distal portions of the Oyashio front (Sugimoto depth of 100 m (Murakami 1994). The spatial pat- & Tameishi 1992; Okazaki 2004; Sakurai 2007). In tern of sea surface temperature (SST) was obtained contrast, primary production, zooplankton density, from the AVHRR-OI database calculated by the and pelagic abundance are lower in the waters NOAA National Center for Environmental Infor- of the Kuroshio current (Odate 1994; Okazaki 2004). mation (http://www.ncdc.noaa.gov/oisst/). Primary The distal portion of the Oyashio front is usually productivity (mg C m−2 day−1) was provided by the situated off northeast Honshu (Ogawa et al. 1987), Ocean Productivity web site http://www.science. hence the distance travelled to highly productive oregonstate.edu/ocean.productivity/standard.product. waters was expected to be shorter for the breed- php (Beherenfeld & Falkowski 1997). Daily SST and ing on Sangan than for those breeding on Mikura. primary productivity were averaged for September Previous studies have shown that parents breeding and October each year from 2003 to 2006. Primary on Mikura take short trips to Kuroshio waters and production was log-transformed. All calculations feed their chicks frequently and take long trips to using oceanographic data were made using R 3.1.3 the productive Kuroshio/Oyashio transition zone software with raster and sp packages (R Develop- and re-fuel their own energy reserves (Ochi et al. ment Core Team).

214 Feeding strategies of Streaked Shearwater

2) Field work cal with a domed top, weighing 14–16 g, 47–53 mm Field work was carried out during the chick rear- long, and 15–16 mm in diameter) or an M190-D2GT ing period (September and October) on Mikura Island (cylindrical container with a domed top, weighing from 2003 to 2006 and on Sangan Island in 2005 (see 20 g, and 60 mm long); Little Leonardo, Tokyo) was Table 1). Research was conducted with permission attached to parents breeding in natural burrows on from the Tokyo Metropolitan Government, the Min- Mikura in 2003 (N=6) and 2006 (N=12), and on istry of the Environment, and the Agency for Cultural Sangan in 2005 (N=8). No other research was carried Affairs, Japan. out on these birds. The data loggers were attached to the breast feathers of the birds using tesa tape 3) Foraging trip duration, parental mass, and (Nos. 4657, 4651; Tesa AG, Germany) and quick-set meal mass epoxy glue (Loctite 401; Henkel, Yokohama, Japan). Meal mass, parental body mass during the for- M190-D2GT data loggers recorded temperature and aging trip in breeding nests were monitored by an air/water pressure every second and accelerations at automated identification and weighing system which 16–32 Hz for up to three days, whereas M190-DT was installed into shearwater nest boxes (Ochi et al. data loggers recorded temperature and pressure every 2006). Nest boxes were in two parts, an entrance second for up to 13 days. Birds fitted with data log- ‘tunnel’ and an inner box; built into each inner box gers were recaptured after 1–19 days of deployment was a weighing system that measured chick mass and the loggers were removed. The recovery rate every second and recorded weight data to the nearest for attached data loggers was 77.8% (14 birds) on 1 g. Parent and meal masses were calculated from Mikura and 100% (8 birds) on Sangan. the changes in the weight measured during paren- Departures from and arrivals at the colony were tal attendance at the nest (Ochi et al. 2006, 2010). determined using the acceleration of the 14 birds car- Parents rearing chicks in nest boxes were captured rying the D2GT loggers and using pressure changes at night (between 1800 and 0300 JST). Each for the eight birds carrying DT loggers. Birds were was weighed and banded with a plastic leg band (3 defined as being on their breeding island when their cm long; <3 g, <1% of adult body mass) with a acceleration was stable and the atmospheric pressure small cylindrical magnet attached (3 cm long and 0.5 was around 30 hPa, which corresponded with the mm in diameter) using Tesa tape (No. 4657, 4651, height of the colony (300 m asl; Matsumoto et al. Tesa AG, Germany). The polarity of the magnets was 2012). The data loggers recorded SSTs where birds reversed for each individual in a pair so as to be able landed on the sea surface. In the laboratory, data log- to identify the entrance and exit behavior of each gers took 12–30 seconds to register 90% of actual mate using Hall sensors (HW-300A, Asahi-Kasei temperature change (0°C to 20°C). Therefore, the Electronics Co., Ltd., Tokyo, Japan). Nest attendance average temperature during a period when the tem- and weights were recorded for nine birds at five nests perature was stable for at least 30 s after landing was and 56 bird-days on Mikura in 2006, and for 8 birds defined as the SST where the bird was foraging. Since at 4 nests and 116 bird-days at Sangan in 2005. At a parents from the Sangan and Mikura Island colonies nest in Mikura, one parent failed to be captured so its do not travel to the Sea of Japan (Matsumoto 2008), attendance and weights could not be recorded. all birds were assumed to forage only in the Pacific Foraging trip duration was defined as the number Ocean. of days between two successive nest attendances. The distribution of trip duration was statistically - 5) Prey analysis egorized as either a unimodal or a bimodal pattern Parent shearwaters were captured in their nest bur- (see statistical analysis section). The lower end of rows between 1800 and 0300 JST after they returned the bimodal distribution was defined as short trips from foraging trips. Parents on Mikura in 2005 (described as SHORT TRIP) and the higher end as (N=21) and 2006 (N=17) and on Sangan in 2005 long trips (described as LONG TRIP; Weimerskirch (N=40) were banded with numbered metal rings, and et al. 1994). released into their burrows. In the early morning after the banded birds departed their nests, walk-in traps 4) Sea surface temperature at the foraging were set at the burrow entrances. Stones were placed grounds over the burrow entrances to prevent parents from A micro data-logger (either an M190-DT (cylindri- feeding their chicks. Then nests were checked every

215 D. OCHI et al. night and the parents were re-captured. Stomach con- where n was the number of prey types contained in tents were collected using a stomach-flushing method each stomach sample, i was prey type, Di was the (Wilson 1984). In 2005 only, stomach contents were energy density of prey type i (KJ/g in wet mass), Wi collected without water flushing by palpating the was the wet mass of prey type i (g), and Wmwas the abdomen. Stomach content masses collected did wet mass of the stomach sample (g). not differ between the two methods (t-test: t=0.43, df=36, P=0.67), so samples were combined for anal- 6) Foraging efficiency and energy delivery rate ysis. Stomach content samples were filtered using Foraging efficiency during each tripall (E , energy a 0.5 mm nylon mesh screen, then weighed (to the intake per day, KJ/day) was calculated as, nearest 0.1 g) using an electronic balance. The liquid EE=+E fraction (a mixture of water and stomach oil) was allcp left for 15 minutes, then the oil was removed using where Ec was the energy delivery rate to the chick a spoon and weighed. Samples were frozen at −5°C and Ep was the energy assimilation rate. Ec was cal- and transported to the laboratory. culated as, Prey species were identified in the laboratory by MDmm means of the key external characteristics of durable Ec = remains (otoliths, vertebrae, fish scales, and T beaks). When we were unable to identify prey species where Mm was the meal mass obtained by the auto- by this means, we used partial sequencing of mito- mated weighing system and Dm was the average chondrial DNA. Genomic DNA was extracted from energy density of a meal calculated for stomach muscle tissue using the phenol-chloroform method samples. Ep was calculated as: or a Bio-Rad Aqua Pure Genomic DNA Isolation kit. rT Extracted DNA was amplified using a PCR targeting bMp + k bMp r 413 bp in cytochrome b and 320 bp in the 16 S ribo- Ep = =+ T T k somal RNA genes. Double-stranded PCR products from both genes, purified using ExoSAP-IT (USB), where b is the energy density of body tissue (kJ/g), were subsequently used for direct-cycle sequencing Mp is parental mass change during the trip (g) with dye-labeled terminators (Applied Biosystems). obtained using the automated weighing system, r is Sequences were analyzed using a capillary type field metabolic rate (kJ/day), T is trip duration (days) sequencer (ABI Prism 3100/3130) and ABI Sequenc- obtained using the automated weighing system, and ing Analysis Software 3.7. The sequences were then k is the digestion rate (assimilated energy per energy aligned by hand using DNASIS for Windows ver. value of food). The letters b, k and r were assumed to 2.1 (Hitachi Software, Inc.). The sequence similarity represent averages among 14 Procellariiformes spe- search was carried out using BLAST (Altschul et cies (22.3 kJ/g, Ellis & Gabrielsen 2003), also of the al. 1990) on a fish mitochondrial genome database similar-sized White-chinned Petrel Procellaria aequi- (MitoFish; http://mitofish.aori.u-tokyo.ac.jp). noctialis (0.76; Jackson 1986), and that obtained pre- The energy densities of each prey species and stom- viously from the Streaked Shearwater (0.0634×24× ach oil were measured from collected prey samples. [Body Mass (g)] kJ/d, Shirai et al. 2012). Samples of the Common Dolphinfish Coryphaena hippurus, Chub Mackerel Scomber japonicus, and 7) Chick growth and fledging mass Ocean Sunfish Mola mola were obtained from a fish To monitor their growth, chicks were weighed market in Otsuchi town near Sangan. Each sample between 9 September and 14 October 2004 on Mikura was freeze-dried using a VD-80 machine (TAITEC, (N=29) and between 9 September and 3 October Saitama) for 7–12 hours. The energy value of each 2005 on Sangan (N=16). Chicks were weighed 1–6 prey item was measured using a bomb calorimeter times on Mikura and 3–5 times at Sangan using (1013S-1, Yoshida Seisakusho Co. Ltd., Tokyo). a spring balance (Pesola AG, Baar, Switzerland). The energy density of each stomach sample (Dm, Wing lengths were measured using vernier calipers KJ/g in wet mass) was calculated as: and used to determine chick age using the formula n given by Oka et al. (2002). The masses of pre-fledg- 1 Dm = DWii ing chicks were measured on 3 November 2005 on W ∑ m i=1 Mikura (N=26) and on 6 and 11 November 2005

216 Feeding strategies of Streaked Shearwater on Sangan (N=29). During the pre-fledging period, using a linear mixed model with normal error dis- chicks walking or flying around the colony were cap- tribution (lmer in lme4 package) analysis. In these tured arbitrarily and their body masses, and head, models, breeding colony and trip types were included tarsus and wing lengths were measured. as explanatory variables and the effect of parent iden- tity was included as a random effect. Parameter esti- 8) Statistical analyses mation, for models with all possible combinations of In order to verify the distributions of trip durations explanatory variables, was carried out and appropri- as either unimodal or bimodal, two models were con- ate models were considered by AIC. Differences in structed and fitted to observations. Prior to analysis, seasonal body mass change of parents and chick mass trip duration was adjusted by −1 to fit Poisson distri- growth during the rearing period on the two islands bution. As a model of unimodal distribution, a simple were also examined by linear mixed model analy- Poisson distribution was taken; sis. Body mass of parents or chicks was included as a dependent variable; and actual date in each year, λ xe−λ px( ) = breeding colony and the interaction between date and x! colony were included as explanatory variables and where p(x) means probability of taking x+1 days individual identity was included as a random effect. trip. Parameters of the model were estimated by Appropriate models were considered by AIC. Differ- the maximum likelihood method (mle function in ences in the body mass, head length, tarsus length, stats4 package) separately for parents on Mikura and and wing length of pre-fledging chicks and the esti- Sangan. As a model of bimodal distribution, a mixed mated body mass of fledglings between islands were Poisson distribution was taken; checked by a liner model. In these analyses, each measurement was set as a response variable and col- xx−−λλ12  λ1 e   λ2 e  ony was included as an explanation variable. px( ) = π1 + π 2 ,  x!!  x  All statistical analyses were conducted using R ππ≥≥00,,ππ+=11, λλ≤ 3.1.3 software (R Development Core Team). The 12, 12 12 level of statistical significance was set at P<0.05. Parameters of the mixed Poisson distribution model For model selection, the model that had the smallest were estimated by the maximum likelihood method AIC was adopted as optimal. Mean values of all data with EM algorism (Bishop 2006) and 100 bootstrap were presented as mean±SD. samples were used to calculate standard errors of those estimated parameters (Train 2008). Then an RESULTS appropriate model was selected by AIC. If the bimodal pattern was selected, we divided 1) Marine environment every foraging trip into SHORT and LONG trip with During the chick rearing seasons (September and its responsibility γ (Bishop 2006), which was given October) of 2003–2006, the Kuroshio front was by; located from 32°N to 36°N, thus Mikura Island was located within 100 km of the Kuroshio front (Fig. x −λ1  λ1 e  π1 1). The southern limit of the distal portion of the  x!  γ = Oyashio front was within or near 100 km of Sangan xx−−λλ12  λ1 e   λ2 e  Island every year (Fig. 1). SST within 100 km of π1 + π 2  x!!  x  Mikura was 23–27°C and within 100 km of Sangan it was 17–21°C. Primary productivity was low in We defined trips with a duration of 0.5 or more γ the Kuroshio region (<106 mg m−2 day−1), high in value as SHORT, and all others as LONG. the Kuroshio/Oyashio transition zone (106 −107 mg Differences in the rate of parental mass change m−2 day−1), and extremely high in Oyashio intrusions during a foraging trip (change of body mass dur- (>107 mg m−2 day−1, Fig. 1). ing trip duration, g/day), chick provisioning rate (meal mass per trip day, g/d), energy assimilation 2) Trip duration rate (kJ/d), energy delivery rate (kJ/d) and foraging A bimodal pattern of trip duration was found both efficiency (kJ/d) between SHORT and LONG trips, at Mikura and Sangan (Table 2; Fig. 2). For parents and between Mikura and Sangan, were examined at Mikura, trips of one to three days were defined

217 D. OCHI et al.

(a) 45N 2003 45N 2004 45N 2005 45N 2006 Oyashio Oyashio Oyashio Oyashio Intrusions Intrusions Intrusions 15 Intrusions 15 15 15 40N 40N 40N 40N 200 20

20 20

Kuroshio 25 35N 25 35N Kuroshio 25 35N Kuroshio 35N front 25 Kuroshio front front front

140E 145E 140E 145E 140E 145E 140E 145E (b) 3.2 45N 2003 45N 2004 45N 2005 45N 2006 3.4 3.4 3.4 3.4 3.2 3.2 3.2 3 3.2 3 2.8 3 Log−transformed 3 net primary productivity 2 40N 40N 2.8 40N 2.8 40N (log10(mgC/m /day)) 4.0 3.6 3.6 3.6 2.6 3.2 2.8 2.8 2.6 2.6 2.4 35N 2.6 35N 35N 35N 2.4 2.4 2.0 2.4 2.4 2.2 2.2 2.2 2.2 140E 145E 140E 145E 140E 145E 140E 145E

Fig. 1. Locations of the Oyashio intrusion and the Kuroshio front, and contours of surface seawater temperature (SST) (a) and the primary productivity (b) in the autumn chick rearing season of Streaked Shearwaters in 2003– 2006. Daily SST and primary productivity were averaged during September and October. Primary productivity was log-transformed after averaging. The thin broken line indicates the location of the Oyashio intrusion and the bold broken line indicates the Kuroshio front. The solid circle shows the location of Mikura Island, and the diamond indicates Sangan Island. Shaded circles show the areas within 100 km of Mikura and Sangan.

(a) Mikura Island as SHORT TRIP and trips of more than three days 30 were defined as LONG TRIP, whereas for parents 25 at Sangan, trips of one or two days were defined as

20 SHORT TRIP and trips of more than two days were defined as LONG TRIP (Table 3, Fig 2). Both λ1 and 15 λ2 for Mikura trips were higher than those for Sangan Frequency 10 trips, (Table 2), indicating that parents from Mikura 5 took relatively longer SHORT and LONG TRIPs 0 than those of the parents from Sangan. Lower values 0 2 4 6 8 10 12 Trip duration (day) of π1 for parents from Mikura indicate that they took LONG TRIPs more likely than parents from Sangan. (b) Sangan Island 90 3) Water masses where parents were foraging 80 Parents from Mikura Island spent most of their 70 60 time in warm waters (>24 °C) during SHORT TRIPs 50 both in 2003 and 2006, indicating that they stayed 40 primarily in the Kuroshio around the colony or in Frequency 30 20 the southern part of the Kuroshio/Oyashio transi- 10 tion zone (Fig. 1, 3ab). During LONG TRIPs, how- 0 0 2 4 6 8 10 12 ever, they stayed in cool waters (14–22°C) most of Trip duration (day) the time, indicating that they visited the Kuroshio/ Fig. 2. Difference in distribution of duration of foraging trips Oyashio transition zone or the Oyashio (Fig. 1, 3de). for parents from Mikura in 2006 (a) and those from Sangan in Parents from Sangan Island stayed mainly in waters 2005 (b). Trip durations were recorded automatically. of 22–24°C during SHORT TRIPs in 2005 (Fig. 1,

218 Feeding strategies of Streaked Shearwater

(a) Mikura 2003 (b) Mikura 2006 (c) Sangan 2005 SHORT TRIPs SHORT TRIPs SHORT TRIPs 60 (N = 535) 60 (N = 773) 60 (N = 335) 50 50 50 40 40 40 30 30 30 20 20 20 10 10 10 0 0 0 12 16 20 24 28 32 12 16 20 24 28 32 12 16 20 24 28 32

(d) Mikura 2003 (e) Mikura 2006 (f) Sangan 2005 LONG TRIPs LONG TRIPs LONG TRIPs 60 (N = 2013) 60 (N = 1302) 60 (N = 495)

Percentage of landings 50 50 50 40 40 40 30 30 30 20 20 20 10 10 10 0 0 0 12 16 20 24 28 32 12 16 20 24 28 32 12 16 20 24 28 32 Average sea surface temperature at each landing ( )

Fig. 3. The sea surface temperature (SST) at each landing location of Streaked Shearwaters during SHORT TRIPs (a: Mikura 2003, b: Mikura 2006, c: Sangan 2005) and LONG TRIPs (d: Mikura 2003, e: Mikura 2006 and f: Sangan 2005).

3e), indicating that they were likely to forage in the Kuroshio/Oyashio transition zone near the colony (Fig 1, 3c). During LONG TRIPs, they stayed in cool 100 and warm waters (14°C and 22–24 °C), indicating that they visited the northern part of the Kuroshio/ Island Oyashio transition zone and also the Oyashio (Fig. Mikura 0 1, 3f). Sangan

4) Prey contents and prey energy value The mean masses of stomach content samples Amount of body mass change(g) −100 were 11.1±16.4 g (N=22), 25.7±36.3 g, (N=16) for SHORT and LONG TRIPs for Mikura, and 22.8±16.4 13579 g (N=13), 12.1±16.5 g (N=3), for SHORT and Trip duration(day) LONG TRIPs for Sangan birds, respectively. Parents from both colonies mainly fed on Japanese Anchovy Fig. 4. The relationship between foraging trip duration and amount of parent body mass change before/after trips from and Darkedged-wing Flyingfish (Table 4). Common Mikura (solid circles) and Sangan (crosses). Lines show esti- Dolphinfish, Bullet Tuna Auxis rochei and Japanese mates from liner models. The solid line indicates the esti- Flying Squid Todarodes pacificus were less common mate for Mikura and the dashed line indicates the estimate for in the diet (Table 4). Parents from Mikura fed also on Sangan. an unidentified percoid fish during SHORT TRIP and Chub Mackerel during SHORT and LONG TRIPs energy density three to ten times greater than that of and brought back Pacific Saury, molluscan decapods other prey (Table 4). and stomach oil after LONG TRIPs. Parents from Sangan brought back pieces of ocean sunfish after 5) Parental mass change and meal mass SHORT TRIPs. The rate of change of parental mass was explained The energy densities of Pacific Saury and Chub well by the models including colony and trip type Mackerel were two to five times greater than those as explanatory factors (Fig 4, Table 6). Parents from of other prey species, whereas stomach oil had an Sangan increased their body masses faster than those

219 D. OCHI et al.

700

600 Island ● Mikura Sangan Body mass(g) 500

400 0 10 20 30 40 Days from 1−Sep.

Fig. 5. The change in parental body mass along with chick rearing (from 1 September) between Mikura (solid circles) and Sangan (crosses). Lines indicate estimates of body mass from liner models. The solid line indicates the estimation for Mikura and the dashed line the estimation for Sangan.

from Mikura and parents lost body mass faster during 850 SHORT TRIPs than LONG TRIPs. The body mass 800 of Sangan parents tended to increase throughout the 750 breeding season, in contrast with parents from Mikura, 700 650 which tended to retain initial weight at capturing (Fig 600 5, Table 7). Provisioning rate was explained by trip 550 type and the parents provisioned faster when they 500 took SHORT TRIPs (Table 6). Overall the provision- 450 Chick body mass (g) ing rate for Mikura (36.5 g/day) was lower than for 400 Sangan (46.4 g/day) considering the difference in the 350 10-Sep. 15-Sep. 20-Sep. 25-Sep. 30-Sep. 10-Oct. 15-Oct.

300 5-Oct. proportion of SHORT TRIPs for both colonies (0.76 for Mikura and 0.91 for Sangan; Table 2). The mean energy densities of stomach contents Date were 5.8 KJ/g, 25.1 KJ/g after SHORT and LONG TRIPs for parents from Mikura, and 8.7 KJ/g, 6.7 Fig. 6. Changes in average chick mass in 2004 on Mikura KJ/g after SHORT and LONG TRIPs for parents (closed circles) and in 2005 on Sangan (open circles). Error from Sangan, respectively. The energy delivery rate bars indicate standard errors. to chicks (Ec) was well explained by the models including trip type as an explanatory factor (Table 6) and parents achieved higher energy delivery rates colonies that took SHORT TRIPs (Table 2), the over- when they took SHORT trips (Table 5). Parental all energy delivery rate for Mikura (259.2 KJ/day) energy assimilation rate (Ep) was well explained by was lower than for Sangan (391.3 KJ/day). The over- the models including colony as an explanatory factor all results of the model selection are shown in detail (Table 6) and parents from Sangan achieved a higher in Appendix 1. assimilation rate (Table 5). Foraging efficiency (Eall) was also well explained by the models including 6) Chick growth and body size at fledging colony as an explanatory factor and parents from No statistical difference was found between the Sangan exhibited higher foraging efficiency (Table hatching dates between Mikura (9.5±6.6 Aug, N=32) 5). Considering the proportion of birds from both and Sangan (15.1±5.0 Aug, N=27; t-test, t=0.87,

220 Feeding strategies of Streaked Shearwater df=53, P=0.39). Chick body mass was explained LONG TRIPs but also foraged near their colony dur- well by the model including date, colony and interac- ing SHORT TRIPs. On the other hand, parents from tion (Table 7), and Mikura chicks were a little heavier Sangan took shorter SHORT TRIPs to the Kuroshio/ at first, but then lighter than Sangan chicks later (Fig. Oyashio transition zone and LONG TRIPs to Oyashio 6, Table 7). The pre-fledging chicks on Sangan were waters. Sangan parents took mostly SHORT TRIPs, heavier and longer winged than those on Mikura. utilizing relatively closer foraging grounds, in con- Tarsus length, head length, bill length and bill depth trast with Mikura parents, which took LONG TRIPs of pre-fledging chicks did not differ between the two to distant foraging grounds. islands (Table 8). The overall results of the model The inter-colonial difference in prey composition selection are shown in detail in Appendix 2. reflected the different oceanographic features of the foraging grounds. Parents from both islands fed on DISCUSSION Japanese Anchovy, which are widely distributed in waters of various temperatures (7–20 °C; Tsuruta & In the Kuroshio/Oyashio transition zone north of Takahashi 1997; Mihara 1998) in both the Kuroshio Cape Inubo (35°42′N, 140°52′E), warm core rings and the Kuroshio/Oyashio transition zone (Kondo (warm water eddies originating from the Kuroshio 1966). In the spring, eggs and larvae are transported extension; Sugimoto & Tameishi 1992) occur contin- from the spawning grounds in the coastal and off- uously. When the warm core rings move northwards, shore areas along the Kuroshio Current and trapped the primary production rises considerably because of in the warm core rings (Itoh 2009). The larvae hatch- the upwelling of cold and nutrient-rich water orig- ing in the warm rings grows faster and with lower inating from deeper Oyashio water (Kimura et al. mortality than in the Kuroshio region (Takahashi et 1997; Itoh &Yasuda 2010). The high abundance of al. 2001; Okazaki 2004). The abundance and body pelagic fish and squid in this region is likely linked to size of Japanese Anchovy increase in the Kuroshio/ such high primary production (Sugimoto & Tameishi Oyashio transition zone interacting with these warm 1992). The average primary production during the core rings during August and September (Mitani two month of shearwater breeding season is con- 1988; Murase et al. 2007), thus food availability for sidered sufficient to be able to ignore the short-term parents from Sangan was relatively higher than for time lag between the spawning of the phytoplankton parents from Mikura. and the increasing abundance of pelagic (e.g. Parents from Mikura fed on Pacific Saury during spring blooming; Miller & Wheeler 2012). Sangan LONG TRIPs to Oyashio water. Pacific Saury occurs Island is located within the productive cold waters mainly in the Oyashio or in related areas of cold of the Kuroshio/Oyashio transition zone and the dis- water (14–18°C SST) during the autumn (Matsumiya tal portion of Oyashio front during the chick-rearing & Tanaka 1976; Sugisaki & Kurita 2004). It is likely season. In contrast, Mikura Island is situated within that Sangan parents bring back Pacific Saury, but diet the less productive warm water of the Kuroshio. samples from LONG TRIPs were few (N=3). Sangan Therefore, parents from Sangan had more ready parents were observed bringing back Pacific Saury access to highly productive water than did parents in 2005; however, there was no associated informa- from Mikura. The marine environments around these tion about trip duration was available (Daisuke Ochi, two colonies varied during the years 2003–2006, but personal observation). Parents from Mikura brought there were no extreme conditions affecting the shear- back stomach oil only after LONG TRIPs (21% of water breeding environment (Fig. 1). Thus although all trips), indicating that it takes more than three days data for Streaked Shearwaters were unavailable for to extract the lipid fraction of prey in the stomach some years, inter-annual variation in the oceanogra- (Warham 1996; Weimerskirch & Cherel 1998; Cherel phy in this region is not considered sufficiently great et al. 2002). Parents from Sangan did not bring back to affect our main conclusions. stomach oil, perhaps because foraging trips of more The distribution of trip duration and water tem- than three days were rare (6% of all trips). Parents perature where parents foraged, revealed that parents from both Mikura and Sangan were able to forage from both Mikura and Sangan Islands adopted dual opportunisticly on Japanese Flying Squid, a species foraging strategies. On the one hand, parents from that is commonly distributed in coastal waters off Mikura travelled long distances to the Kuroshio/ Honshu in autumn (Sakurai 2000). The Ocean Sun- Oyashio transition zone in order to forage during fish found in waters off Honshu are too large (250–

221 D. OCHI et al.

2,700 mm long; Nakatsubo et al. 2007) to form prey those of Mikura parents. In our study, it was dif- for Streaked Shearwaters. However, off northeast ficult to explain the very limited difference in body Honshu Ocean Sunfish is fished for using set nets or size between pre-fledging chicks from Mikura and harpoons and the inedible parts are discarded at sea Sangan because there are complicated factors relat- (Sawai et al. 2011). Our observations of this species ing to considerable sexual and inter-colonial vari- in the diet of the Streaked Shearwater indicates that ation in body size (Arima et al. 2014; Yamamoto in addition to their normal prey they will also take et al. 2015). However, the difference in body mass discards from the fishing industry. should reflect the overall amount of feeding from Parents delivered meals to their chicks more the parents directly, because chicks are unable to quickly following SHORT TRIPs and accumulated feed themselves. As in other avian species, the body their own body mass faster during LONG TRIPS as mass of fledgling shearwaters is strongly associated has been observed for many Procellariiform species, with post-fledging survival (Sagar & Horning 1998). including for example the Blue Petrel Halobaena Therefore, the greater distance at which parents from caerulea (Chaurand & Weimerskirch 1994), Short- Mikura forage, compared with those from Sangan, tailed Shearwater Puffinus tenuirostris (Weimerskirch may explain their poor breeding performance. & Cherel 1998), and Sooty Shearwater Puffinus gri- Our study, therefore, implies that Sangan Island seus (Weimerskirch 1998). This is a typical feature was a better site for chick feeding than Mikura. How- of the dual foraging strategy. Parents from Mikura ever, further consideration is necessary to conclude were less efficient foragers during both LONG and whether certain breeding sites are more adaptive SHORT TRIPs resulting in a lower energy delivery than others for this species, because data on other rate. This low performance can be explained by the comparable breeding parameters (such as egg lay- long distances they were forced to travel to highly ing rate, hatching success and chick mortality) have productive foraging grounds. not been available. Yamamoto et al. (2011) reported Parents from Sangan tended to increase their body that parents from Mikura mostly foraged around the mass even during the chick rearing period whereas Kuroshio front during April, May and June, and sug- parents from Mikura tended only to retain their mass. gested that most pelagic fishes stay in the Kuroshio Avian parents typically lose or retain their mass region during this season because the water temper- while raising young because of the energetic costs ature in the Oyashio and in the Kuroshio/Oyashio of breeding (Ricklefs 1974; Drent & Daan 1980) transition zone is still too low for them. Therefore, and such trends also have been found among the shearwaters may benefit from access to a large prey Procellariiformes (Chaurand & Weimerskirch 1994; resource close to Mikura Island during the pre-laying Weimerskirch 1998; Niizuma et al. 2001). This can be period, enabling them to store body reserves for egg explained by the fact that the high rate of provision- production. Chastel et al. (1995) reported that the ing at Sangan provides excess capacity for chicks; Blue Petrel had better mating success and experi- any food that they refuse is available for parents to enced lower egg desertion when their body condition utilize allowing them to gain weight. In the case of was high during the pre-breeding period, and Bolton the Streaked Shearwater, when both parents return et al. (1992) reported that extra food available dur- to their nest during the same night they cannot both ing the pre-laying period leads to increased egg and pass on all of their food to their offspring, they one hatchling size in the Lesser Black-backed Gull Larus or both parents may retain the excess (Ogawa et al. fuscus. To better understand the adaptive responses 2015). In the case of the Sangan Island colony, such of the Streaked Shearwater to variable oceanographic excess delivery may occur frequently because of the characteristics during their breeding season, research high feeding frequency, therefore parents gradually needs to be expanded to include the whole breed- gain weight through the chick rearing period. ing season and parental breeding behavior should be Both provisioning rates and energy delivery rates monitored more inclusively. differ between SHORT and LONG TRIPs. These result reflects that Streaked Shearwater parents may ACKNOWLEDGMENTS not coordinate their amount of food that each pro- vides during nest attendance (Ogawa et al. 2015), We thank R. Yamashita, Y. Inoue, T. Tokunaga, H. Fujii, hence the chicks of Sangan parents that took SHORT T. Yamamoto, N. Katsumata, T. Narasaki, K. Shimatani, S. TRIPs more frequently had higher growth rates than Watanabe and S. Kurimoto for logistical support during the

222 Feeding strategies of Streaked Shearwater fieldwork, Y. Okazaki for instruction on the analysis of ocean- Murres breeding in different sectors of the north ographic data, M. Nishida for help with identification of prey water polynya: an inter-colony comparison. Mar Ecol species. And we also thank M. Brazil for checking English Prog Ser 231: 293–302. writing of this manuscript and anonymous reviewers. This Itoh S (2009) Transport and environmental tempera- study was supported by grants from the Japan Society for the ture variability of eggs and larvae of the Japanese Promotion of Science to the Yamashina Institute for Ornithol- anchovy (Engraulis japonicus) and Japanese sar- ogy, Y. W., and the COE program (Neo-natural history) led by N. Okada (Hokkaido University). Field study at Sangan Island dine (Sardinops melanostictus) in the western North was supported by the Cooperative Program of Atmosphere Pacific estimated via numerical particle-tracking and Ocean Research Institute, University of Tokyo. experiments. Fish Oceanogr 18: 118–133. Itoh S & Yasuda I (2010) Water mass structure of warm REFERENCES and cold anticyclonic eddies in the western boundary region of the subarctic north Pacific. J Phys Oceanogr Altschul SF, Gish W, Miller W, Myers EW & Lipman 40: 2624–2642. DJ (1990) Basic local alignment search tool. J Mol Jackson S (1986) Assimilation efficiencies of White- Biol 215: 403–410. chinned Petrels (Procellaria aequinoctialis) fed dif- Arima H, Oka N, Baba Y, Sugawa H & Ota T (2014) ferent prey. Comp Biochem Physiol B Comp Bio- Gender identification by calls and body size of the chem 85: 301–303. Streaked Shearwater examined by CHD genes. Orni- Japanese Ministry of the Environment (2013) The report thol Sci 13: 9–17. on the census in the ‘Monitoring-Site 1000’ Baduini CL & Hyrenbach D (2003) Biogeography of project. The Ministry of the Environment, Tokyo, Procellariiform foraging strategies: does ocean pro- Japan. ductivity influence provisioning? Mar Ornithol 31: Kawai H (1969) Statistical estimation of isotherms 101–112. indicative of the Kuroshio axis. Deep Sea Res Suppl Beherenfeld MJ & Falkowski PG (1997) Photosynthetic to 16: 109–115. rates derived from satellite-based chlorophyll concen- Kimura S, Kasai A, Nakata H, Sugimoto T, Simpson tration. Limnol Oceanogr 42: 1–20. JH & Cheok JVS (1997) Biological productivity of Bishop CM (2006) Pattern recognition and machine meso-scale eddies caused by frontal disturbances in learning. Springer, Cambridge. the Kuroshio. ICES J Mar Sci 54: 179–192. Bolton M, Houston D & Monaghan P (1992) Nutri- Kondo K (1966) Mode of life of the Japanese anchovy, tional constraints on egg formation in the Lesser Engraulis japonica (Houttuyn) – I. Aggregation of Black-backed Gull: an experimental study. J Anim postlarvae and juveniles of the Pacific fraction along Ecol 61: 521–532. Houshu. Bull Tokai Reg Fish Res Lab 47: 51–84. Chastel O, Weimerskirch H & Jouventin P (1995) Body Matsumiya Y & Tanaka S (1976) Numerical implica- condition and seabird reproductive performance: a tion between the distribution of surface temperature study of three petrel species. Ecology 76: 2240–2246. and the saury fishing ground in the Pacific Ocean off Chaurand T & Weimerskirch H (1994) The regular northern Japan. Bull Japanese Soc Fish Oceanogr 29: alternation of short and long foraging trips in the 30–40. Blue Petrel Halobaena caerulea – A previously Matsumoto K (2008) Ikusuki ni okeru oomizunagidori undescribed strategy of food provisioning in a pelagic no tyou, tankyori saisyokusennryaku to kaiyoukann- seabird. J Anim Ecol 63: 275–282. kyou tono kannkei (Relationships between long-short Cherel Y, Weimerskirch H & Trouve C (2002) Dietary range foraging strategy of streaked shearwater during evidence for spatial foraging segregation in sympatric chick rearing period and oceanographic characteris- albatrosses (Diomedea spp.) rearing chicks at Iles tics). Ph.D thesis, Hokkaido University (in Japanese). Nuageuses, Kerguelen. Mar Biol 141: 1117–1129. Matsumoto K, Kazama K, Sato K & Oka N (2007) Drent RH & Daan S (1980) The prudent parent: ener- Estimation of breeding population size of Streaked getic adjustments in avian breeding. Ardea 68: 225– Shearwaters on Sangan Island, Iwate, based on 3D 252. topography by GIS. Japanese J Ornithol 56: 170–175. Ellis HI & Gabrielsen GW (2003) Energetics of free- Matsumoto K, Oka N, Ochi D, Muto F, Satoh TP & ranging seabirds. In: Schreiber EA & Burger J (eds) Watanuki Y (2012) Foraging behavior and diet of Biology of marine birds. pp 293–302. CRC press, Streaked Shearwaters Calonectris leucomelas rearing Boca Raton. chicks on Mikura Island. Ornithol Sci 11: 9–19. Falk K, Benvenuti S, Dall’Antonia L, Gilchrist G & Mihara Y (1998) Distribution of the Japanese Anchovy, Kampp K (2002) Foraging behaviour of Thick-billed Engraulis japonicus, off southeastern Hokkaido. Sci

223 D. OCHI et al.

Reports Hokkaido Fish Exp Stn 53: 9–14. Shearwaters Calonectris leucomelas on Mikura Island Miller CB & Wheeler PA (2012) Biological oceanogra- for two breeding seasons. J Yamashina Inst Ornithol phy. 2nd ed. Willey-Blackwell, Hoboken, USA. 34: 39–59. Mitani I (1988) Foundation and verification of forecast- Okazaki Y (2004) Shigyo no seizan ni hatasu Kuroshio ing on the description and abundance of sardine and furonto no eikyou (The effects of the Kuroshio front anchovy off Kanagawa Prefecture– V. Estimation of on survival of larvae of pelagic fishes). In: Sugimoto Japanese Anchovy in autumn. Bull Kanagawa Prefect T (ed) Kaiyo To Seibutu Shigen (Please provide the Fish Exp Stn 9: 27–34. translated English title). pp 101–111. Seizando, Murakami M (1994) On long-term variations in hydro- Tokyo (in Japanese). graphic conditions in the Tohoku area. Bull Tohoku Peck DR & Congdon BC (2005) Colony-specific forag- Natl Fish Res Inst 56: 47–56. ing behaviour and co-ordinated divergence of chick Murase H, Tamura T, Kiwada H, Fujise Y, Watanabe development in the Wedge-tailed Shearwater Puffinus H, Ohizumi H, Yonezaki S, Okamura H & Kawahara pacificus. Mar Ecol Prog Ser 299: 289–296. S (2007) Prey selection of common minke (Balae- Ricklefs RE (1974) Energetics of reproduction in birds. noptera acutorostrata) and Bryde’s (Balaenoptera Avian Energ 15: 152–292. edeni) whales in the western North Pacific in 2000 Sagar PM & Horning DS (1998) Mass-related survival and 2001. Fish Oceanogr 16: 186–201. of fledgling Sooty Shearwaters Puffinus griseus at the Nakatsubo T, Kawachi M, Mano N & Hirose H (2007) Snares, New Zealand. Ibis 140: 329–331. Spawning period of ocean sunfish Mola mola in Sakurai Y (2000) Changes in inferred spawning areas of waters of the eastern Kanto region, Japan. Aquac Sci Todarodes pacificus (Cephalopoda: Ommastrephidae) 55: 613–618. due to changing environmental conditions. ICES J Niizuma Y, Takahashi A, Sasaki N, Hayama S, Tokita Mar Sci 57: 24–30. N & Watanuki Y (2001) Benefits of mass reduction Sakurai Y (2007) An overview of the Oyashio ecosys- for commuting flight with heavy food load in Leach’s tem. Deep Sea Res Part II Top Stud Oceanogr 54: Storm-petrel, Oceanodroma leucorhoa. Ecol Res 16: 2526–2542. 197–203. Sawai E, Yamanoue Y, Yoshida Y, Sakai Y & Hashimoto Ochi D, Matsumoto K, Watanuki Y & Oka N (2006) H (2011) Seasonal occurrence patterns of Mola sun- Automated weighing and nest attendance recording fishes (Mola spp. A and B; Molidae) in waters off the systems for the study of the feeding ecology of the Sanriku region, eastern Japan. Japanese J Ichthyol 58: Streaked Shearwater. Japanese J Ornithol 55: 24–28. 181–187. Ochi D, Oka N & Watanuki Y (2010) Foraging trip Shirai M, Yamamoto M, Ebine N, Yamamoto T, Trathan decisions by the Sreaked Shearwater Calonectris leu- PN, Yoda K, Oka N & Niizuma Y (2012) Basal and comelas depend on both parental and chick state. J field metabolic rates of Streaked Shearwater during Ethol 28: 313–321. the chick-rearing period. Ornithol Sci 11: 47–55. Odate K (1994) Zooplankton biomass and its long-term Sugimoto T & Tameishi H (1992) Warm-core rings, variation in the western north Pacific Ocean, Tohoku streamers and their role on the fishing ground forma- sea area, Japan. Bull Tohoku Natl Fish Res Inst 56: tion around Japan. Deep Sea Res Part A Oceanogr 115–173. Res Pap 39: S183–S201. Ogawa M, Shiozaki T, Shirai M, Muller MS, Yamamoto Sugisaki H & Kurita Y (2004) Daily rhythm and sea- M & Yoda K (2015) How do biparental species opti- sonal variation of feeding habit of Pacific Saury mally provision young when begging is honest? (Cololabis saira) in relation to their migration and Behav Ecol 26: 885–899. oceanographic conditions off Japan. Fish Oceanogr Ogawa Y, Mitsuyuki H & Yasuda I (1987) Fluctuations 13: 63–73. of the first Oyashio intrusion and it’s influences on Takahashi M, Wataname Y, Kinoshita T & Watanabe C coastal fishery-resources. Bull Tohoku Reg Fish Res (2001) Growth of larval and early juvenile Japanese Agency 49: 1–15. anchovy, Engraulis japonicus, in the Kuroshio- Oka N (2004) The distribution of Streaked Shearwater Oyashio transition region. Fish Oceanogr 10: 235– (Calonectris leucomelas) colonies, with special atten- 247. tion to population size, area of sea where located and Train K (2008) EM algorithms for nonparametric esti- surface water temperature. J Yamashina Inst Ornithol mation of mixing distributions. J Choice Model 1: 35: 164–188. 40–69. Oka N, Suginome H, Jida N & Maruyama N (2002) Tsuruta Y & Takahashi A (1997) Reproductive ecology Chick growth and fledgling performance of Streaked of the Japanese Anchovy (Engraulis japonicus H.) in

224 Feeding strategies of Streaked Shearwater

the Kuroshio extension and the mixed water region. Short-tailed Shearwaters: breeding in Tasmania and Bull Hokkaido Natl Fish Res Inst 61: 9–15. foraging in the Antarctic? Mar Ecol Prog Ser 167: Warham J (1977) The incidence, functions and ecologi- 261–274. cal significance of petrel stomach oils. Proc New Zeal Wilson RP (1984) An improved stomach pump for pen- Ecol Soc 24: 84–93. guins and other seabirds. J F Ornithol 55: 109–112. Warham J (1996) The behaviour, population biol- Yamamoto T, Kohno H, Mizutani A, Yoda K, Matsumoto ogy and physiology of the petrels. Academic Press, S, Kawabe R, Watanabe S, Oka N, Sato K, Yamamoto London, San Diego. M, Sugawa H, Karino K, Shiomi K, Yonehara Y & Weimerskirch H (1998) How can a pelagic seabird Takahashi, A (2016) Geographical variation in body provision its chick when relying on a distant food size of a pelagic seabird, the streaked shearwater resource? Cyclic attendance at the colony, foraging Calonectris leucomelas. J Biogeogr 43: 801–808. decision and body condition in Sooty Shearwaters. J Yamamoto T, Takahashi A, Oka N, Iida T, Katsumata Anim Ecol 67: 99–109. N, Sato K & Trathan PN (2011) Foraging areas of Weimerskirch H, Chastel O, Ackermann L, Chaurand T, Streaked Shearwaters in relation to seasonal changes Cuenotchaillet F, Hindermeyer X & Judas J (1994) in the marine environment of the Northwestern Alternate long and short foraging trips in pelagic sea- Pacific: inter-colony and sex-related differences. Mar bird parents. Anim Behav 47: 472–476. Ecol Prog Ser 424: 191–204. Weimerskirch H & Cherel Y (1998) Feeding ecology of

225