Ornithol Sci 11: 9 – 19 (2012)

ORIGINAL ARTICLE Foraging behavior and diet of Streaked leucomelas rearing chicks on Mikura Island

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

1 Graduate School of Fisheries Sciences, Hokkaido University, 3–1–1 Minato-cho, Hakodate, Hokkaido 041–8611, Japan 2 Research Division, Yamashina Institute for Ornithology, 115 Konoyama, Abiko, Chiba 270–1145, Japan 3 Atmosphere and Ocean Research Institute, the University of Tokyo, Kashiwanoha 5–1–5, Kashiwa, Chiba 277–8564, Japan

Abstract Foraging behavior and diet of Streaked Shearwaters Calonectris leucomelas ORNITHOLOGICAL rearing chicks on Mikura Island was studied using depth and temperature recording SCIENCE data-loggers and stomach contents. Water mass where were foraging was esti- © The Ornithological Society mated using sea surface temperature experienced by birds. Birds spent 76–96% of of Japan 2012 their time at sea flying, 4–24% for landing on the water, and made a few (0.5–17.0 per day) shallow (<6 m) dives. Birds made many short (<2 days) and some long (4–10 days) trips. During short trips, birds stayed in the warmer Kuroshio and Kuroshio-Oyashio mixed regions, and fed on Japanese Engraulis japonicus, Common Todarodes pacificus and Flying Cypselurus hiraii. During long trips, birds stayed in the colder Oyashio region and fed on anchovy and Pacific Saury Cololabis saira. Birds made more dives during short trips than they did during long trips. Streaked Shearwaters breeding on the island in low—productive Kuroshio water, therefore, adopted dual foraging strategies, and changed their diet and dive frequencies in relation to water masses.

Key words Anchovy, Data-logger, Dual foraging, Oyashio

During chick rearing, parents of some of (Chaurand & Weimerskirch 1994; Weimerskirch et albatrosses and shearwaters often adopt dual foraging al. 1997, 2003). strategies, i.e. making short and long foraging trips to Streaked Calonectris leucomelas is foraging areas close to and distant from their breed- endemic to East Asia, breeding only around Japan ing site (Weimerskirch et al. 1994; Weimerskirch and southern Korea. Mikura Island (33°52′N, 1998). To feed chicks quickly, parents make many 139°14′E) supports one of the largest colonies short trips to low-productive waters near the colony, (1,750,000–3,500,000 birds, Oka 2004) and is but they make a few long trips to distant and high- located in a low-productive Kuroshio region 300– productive waters to restore their own energy reserves 800 km south of the high-productive Kuroshio- Oyashio mixed and the Oyashio region (Odate 1994; (Received 12 September 2011; Accepted 27 December 2011) Sugiura & Tsunogai 2005). Therefore, birds breeding # Corresponding author, E-mail: [email protected] * Present address: System Engineering Division, Kitami Insti- on this island may adopt dual foraging strategies tute of Technology, Koen-cho 165, Kitami, Hokkaido 090– (Ochi et al. 2010), though foraging behavior and diet 8507, Japan during long and short trips are unknown. ** Present address: National Research Institute of Far Seas Fish- To understand the pattern of exploitation of marine eries, Fisheries Research Agency, 5–7–1 Orido, Shimizu, Shizuoka 424–8633, Japan resources during the chick-rearing period, we studied *** Present address: School of Marine Science and Technology, the foraging behavior of Streaked Shearwaters rear- Tokai University, 3–20–1 Orido, Shimizu, Shizuoka 424– ing chicks on Mikura Island, using depth and tem- 8610, Japan perature recording data-loggers. We also examined **** Present address: Collection Center, National Museum of Nature and Sciences, 3–23–1 Hyakunin-cho, Shinjuku-ku, prey items found in their stomach contents in relation Tokyo 169–0073, Japan to foraging habitats.

9 K. MATSUMOTO et al.

STUDY AREA AND METHODS to record depth (0.1 m resolution, 0.5 m accuracy) and temperature (0.018°C resolution, 0.1°C accu- 1) Study site and year racy) every second. D2GTs recorded tail-head and Fieldwork was conducted in the Nango area on ventral-dorsal accelerations at 16 Hz also. Data were Mikura Island, Tokyo (Permit No. 462, Ministry of downloaded onto a laptop computer using Logger the Environment) in 2003, 2005, and 2006. We Tools ver. 3.1 (Marine Micro Technology) and were deployed data-loggers on birds to study foraging analyzed using Igor Pro ver. 4.04 (Wave Metrics Inc.). behavior in 2003 and 2006 and collected stomach To assess the impacts of logger attachments on contents in all three years. We measured trip duration chick growth (slopes of linear regressions of chick using behavioral data collected by data-loggers in mass against date), chicks of parents carrying loggers 2003 and 2006 and using the departure/arrival dates and those without loggers were weighed in the late determined by trapping birds in 2005 and 2006. afternoon every 3–5 days.

2) Data-logger deployment 3) Analyses of pressure and temperature In September and October, data-loggers were The loggers were attached on the middle of the attached to the shearwater breast feathers using Tesa ’s abdomen. We considered the birds to dive if tape (Tesa AG, Germany). Parents were caught by the depth of loggers was deeper than half of the total hand when they were staying with chicks (<26-day- length of birds (0.5 m). The temperature differences old) in nest boxes during the night, and weighed with between the air and the surface seawater were 0.4– a Pesola spring balance (±5 g). Sexes were deter- 6.3°C during the study period. Thus, we estimated mined using sex-specific calls (Arima & Sugawa that the birds were “landing on the water” during the 2004; Appendix), though we combined male and period between consecutive abrupt changes in tem- female data in this study since the sample size was perature (Fig. 1 b) following Tremblay et al. (2003). small. The birds were released in the nest boxes soon Fluctuation of the tail-head surge acceleration indi- after and recaptured in the nests at night 1–19 days cated that the birds were flapping their wings during later. these landing activities (Fig. 1a). The data-loggers (Little Leonardo, Tokyo) we used The birds made successive water-landings (bouts were DT (14–16 g weight, 47–53 mm length, 15–16 A, C, D, E, in Fig. 1a) or an extended period of land- mm diameter) and D2GT (20 g weight, 60 mm ing (bouts B, F in Fig. 1a) and both of these were length, 5–16 mm diameter). Both were programmed defined as “water-landing bouts”. When birds were

Fig. 1. Tail to head surge acceleration (a, in G), recorded temperature (b), and depth (c). Thick horizontal bar in (a) indicates water-landing bouts A–F. Horizontal lines in (b) represents the time when sea surface tempera- ture (SST) was given.

10 Foraging of Streaked Shearwater on the water for an extended period, the recorded their nests, trap doors were set at burrow entrances depths were 0.1–0.2 m (bouts B, F, Fig. 1a, c). Cri- and then the nests were inspected at 21:00–22:00 teria to separate water-landing bouts were calculated and 01:00–03:00 every day to recapture the parents. for each bird using the log-survivorship curves A stone was also placed at the nest chamber entrance (Gentry & Kooyman 1986) of the flight time between to interrupt the returning parents and allow their cap- water landing bouts and were 5.3–6.0 min. ture before they fed their chicks. The resolution of depth allowed us to identify Oils on the surface of stomach samples were col- pressure differences of 0.01 atm (10 hPa) in the air: lected and weighed to the nearest 0.1 g using an approximate pressure difference between sea level electric balance. Then stomach contents were sieved and 100 m altitude. Shearwaters usually fly close (<0.5 mm mesh) and weighed. Samples were pre- (<20 m) to the sea surface (Warham 1996; Pennycuick served in 60% isopropyl alcohol (in 2003) or frozen 2002). As the study site was about 300 m above sea (–20°C in 2005 and 2006). Prey items were identi- level, the rapid decrease and increase of the pressure fied using key external characteristics later in a labo- by 30–35 hPa (corresponding to about 0.3 m change ratory. For well-digested samples, hard parts of the in depth) recorded in the evening and morning, prey (otoliths, vertebrae, fish scales, and squid beaks) respectively, should relate to their arrival to and were used for identification. departure from the colony. To aid in the identification of prey species, partial Sea surface temperatures (SSTs) were recorded sequence data of mitochondrial DNA was extracted when birds were landing on the water. Since the tem- from the muscle tissue of fish in the stomach samples perature-response time (90% time constant) of log- using the phenol-chloroform method or an AquaPure gers between 0°C and 20°C was 12–30 s, we defined Genomic DNA Isolation kit (Bio-Rad). 413 bp in the the SST as the mean temperature during the period cytochrome-b and 320 bp in the 16S ribosomal RNA when the temperature was stable for at least 30 s genes were amplified using PCR. Double-stranded while birds were on the water (Fig. 1b). As Streaked PCR products of both genes, purified using the Shearwaters were rarely observed in waters east of ExoSAP-IT (USB), were subsequently used for 145°E in September and October (Kuroda 1991), we direct-cycle sequencing with dye-labeled terminators then estimated the water masses where birds were (Applied Biosystems). Sequences were detected by a foraging using the SSTs in the shelf area along the capillary type sequencer (ABI Prism 3100/3130), northeastern coast of Japan (http://www.data.kishou. using ABI Sequencing Analysis Software 3.7. We go.jp/kaiyou/shindan/c-1/wnp-sst.html) and the posi- aligned the sequences using DNASIS for Windows tions of the Oyashio and the Kuroshio fronts (http:// ver. 2.1 (Hitachi Software Inc.). We searched for www.data.kishou.go.jp/kaiyou/shindan/c_2/oyashio/ homology with known DNA data from MitoFish oyashio.html). (http://mitofish.ori.u-tokyo.ac.jp) using BLAST search (Altschul et al. 1990). 4) Stomach content analyses The stomach contents of parents returning to the 5) Statistics colony were sampled in 2003, 2005 and 2006. In Statistical significance was examined using SPSS 2003 and 2006, stomach contents were water-flushed. ver. 14. Non-parametric tests were used to examine A 12 mm diameter elastic tube was pushed down a the differences between birds with and without data- bird’s esophagus and then warm water (30–40°C) loggers. To examine the effects of year, trip type, and was poured into the stomach until the bird’s stomach time of day (day and night) on foraging behavior, contents began to flush our. This procedure was General Linear Model (GLM) or Linear Mixed Model repeated at least three times until the out-flowing (LMM) were used where logarithmic or square root water contained no further food items. In 2005, stom- transformations were applied to hold normality. Mea- ach contents were sampled by compressing the bird’s surements are given as means ±SD in the text. abdomen to facilitate regurgitation. If birds had empty stomachs, they were excluded from the analysis. RESULTS To collect stomach contents of birds that had made foraging trips of a known duration, in 2005 and 2006 1) Trip duration and chick growth in birds with parents with chicks were captured and leg-banded. and without data-loggers The following morning, after the parents had departed Parents made many 1- to 2-day trips and some 4-

11 K. MATSUMOTO et al. to 10-day trips in 2003, 2005 and 2006 (Fig. 2). There was no significant difference in the trip dura- tion among years (Kruskal-Wallis test, χ2=1.393, df=2, P=0.498). Four out of six birds with loggers were recaptured in 2003, and ten out of 12 in 2006. Trip duration did not differ between birds with loggers (3.3±2.9 d, n=29 [2003 and 2006 data combined]) and diet-sam- pling birds without loggers (3.8±2.9 d, n=38 [2005 and 2006 data combined]; U=464.0, P=0.55). Chick growth rates during the period of logger deployment did not differ between pairs with (–0.2±6.1 g d –1, n=4 in 2003; 10.2±25.9 g d –1, n=6 in 2006) and without loggers (1.7±7.7 g d –1, n=18, U=27.5, P=0.47 in 2003; 6.7±17.3 g d –1, n=9; U=26.0, P=0.91 in 2006).

2) Typical water mass utilization and foraging behavior During a typical 1-day trip in 2003, SSTs experi- enced by birds were warmer (>28°C) than that of the Kuroshio front (26°C, Fig. 3a, d). During a 2-day trip Fig. 2. Frequency distributions of the duration of foraging SSTs experienced by birds were 26–30°C and trips in 2003, 2005 and 2006. Samples with and without data- warmer than that of the Oyashio front (19°C in 2003, loggers in 2006 were combined.

Fig. 3. Typical changes of the time spent for landing on water (black bar) or flying (white) and mean sea surface temperatures (SST) (dot) per 2 h during a 1-day (a), 2-day (b) and 6-day (c) typical foraging trips in 2003. Horizontal dashed line indicates SST corresponding to the Oyashio front (19°C in 2003). Day (white horizontal bar) and night (black horizontal bar) times are indicated at the tops of panels. In (d), SSTs based on satellite image data during the corresponding period (line), the location of Mikura Island (star), and the Oyashio and the Kuroshio fronts (bold dashed lines labeled ‘OF’ and ‘KF’) are shown.

12 Foraging of Streaked Shearwater

trip data with activity data (Appendix 1), GLM was performed to examine the trip activity budget where bird identity was ignored. For each trip, time spent for flying increased with the time at sea (Fig. 6a).

Fig. 4. Changes in depth (thick line) and surge acceleration (dotted line) during deep dives.

Fig. 3b, d). During a 6-day trip SSTs experienced by birds were higher than that of the Kuroshio front (26°C) at the start and the end of the trip (traveling phase), but lower than that of the Oyashio front dur- ing the middle of the trip (foraging phase)(Fig. 3c, d). Each bird spent: 76–96% of trip time flying, and 4–24% landing on the water; made water-landing Fig. 5. Trip duration (in days) and the minimum and the bouts of 4.0–15.9 min duration both day and night maximum SSTs experienced by birds during each trip in 2003 (Fig. 3a–c), but rarely made dives (Appendix 1). and 2006. SSTs of Oyashio front in 2003 (19°C) and 2006 95% of dives occurred in daytime (sunrise to sunset). (23°C) are shown as horizontal broken lines. 96% of dives were shallower than 3 m, and the max- imum dive depth was 6 m and 88% of dives lasted only for 2–6 s and maximum dive duration was 18 s. All dives were V-shaped (Fig. 4). Long (>10 s) dives occurred in waters with variable SST (19– 28°C). Variable surge acceleration was recorded dur- ing the descent phase of long (>10 s) dives but not during the ascent phase (Fig. 4); indicating that birds only made a few active dives.

3) Activity during short and long foraging trips Water mass utilization patterns and activities were analyzed for birds with data-loggers in 2003 and 2006. Each bird produced 1–8 trip data, but in four trips temperature data were not obtained and hence activity was not analyzed (Appendix 1). Maximum SSTs experienced by birds during each trip were 25–30°C for all trips (Fig. 5). Minimum SSTs were 24–28°C during trips shorter than two days: indicating that birds were in the Kuroshio and/ or Kuroshio-Oyashio mixed regions. Minimum SSTs recorded during trips longer than four days, however, were lower than 19°C in 2003 and lower than 23°C in 2006 (Fig. 5): indicating that birds visited the Fig. 6. Relationships between the time at sea (precise trip duration determined by data-logger) and the time spent flying Oyashio region (see Fig. 3d). Trips shorter than two (a), the number of water-landing bouts (b), and the number of days, therefore, were designated as short and those dives (c). 2003 (open circles) and 2006 (crosses) data are longer than four days as long in this study. shown. Time at sea longer than 72 h (vertical broken line) Since nine out of 14 birds produced only single means a long trip (>4 d).

13 K. MATSUMOTO et al.

Table 1. Effects of year (2003 vs 2006) and trip type (short vs long) on the proportion of time flying, no. of landing bouts, no. of landings, and no. of dives per unit time at sea. Effects were examined with GLM, and parameter estimates (±SE), t-values, and P-values are shown.

Dependent Effects Parameter estimate t P Proportion of time flying Year –0.024±0.021 –1.121 0.274 Trip type –0.022±0.023 –0.960 0.348 No. bouts per time at sea Year –0.335±0.125 –2.677 0.014 Trip type –0.020±0.138 –0.144 0.887 No. landings per time at sea Year –1.073±0.418 –2.568 0.018 Trip type 0.258±0.462 0.558 0.582 No. dives per time at sea Year –0.033±0.094 –0.349 0.73 Trip type –0.239±0.104 –2.303 0.031

Year and trip type (short or long) did not affect the 2003 than 2006 (Fig. 7a, Table 2). The number of proportion of time flying (Table 1). The number of water landings per unit time of water landing bouts, water landing bouts increased with time at sea (Fig. did not differ significantly between long and short 6b). The number of water landing bouts per time at trips nor between night and day, but they were greater sea was greater in 2006 (1.3±0.4 times h –1) than in for 2006 than 2003 (Fig. 7b, Table 2). 2003 (0.9±0.2 times h –1) and the number of landings per time at sea were also greater in 2006 (3.5±1.2 times h –1) than in 2003 (2.5±0.8 times h –1), with no significant differences between long and short trips (Table 1). The number of dives did not depend on trip duration (Fig. 6c), thus the number of dives per unit time at sea was greater during short trips than long trips with no year effects (Table 1). As each bird made 19–351 water landing bouts, LMM was performed to examine the foraging bout characteristics where each bird was treated as a ran- Fig. 7. Water-landing bout duration (a) and the number of dom factor. The duration of water landing bouts did landings per unit time of landing-bouts during day (open cir- not differ significantly between long and short trips, cles) and night (closed circles) in 2003 and 2006. Mean±SE nor between night and day, but they were longer for are shown.

Table 2. Effects of year (2003 vs 2006), trip type (short vs long), and time of day (day or night) on the duration of water landing bouts and no. of landings per bout. Effects were examined with LMM, where bird identity was a random factor. Type-III F-values and P-values are shown.

Independent Effects F (dfs) P Duration of landing bout Year 8.043 (1, 9.564) 0.018 Trip type 0.289 (1, 91.845) 0.592 Time of day 2.851 (1,1679.633) 0.091 No. of landings per bout duration Year 14.947 (1, 10.547) 0.003 Trip type 0.468 (1, 163.722) 0.495 Time of day 2.376 (1.1678.377) 0.123

14 Foraging of Streaked Shearwater

4) Stomach contents DISCUSSION In total, 64 stomach samples were collected (26 in 2003, 21 in 2005, and 17 in 2006). Since there were 1) Effects of data-loggers no significant differences in the mass of stomach We did not find significant differences in trip dura- contents among years (2003 and 2006 with flushing, tion or chick growth between birds with and without and 2005 with regurgitation; Kruskal-Wallis test, loggers. Streaked Shearwaters made few dives, so χ2=0.086, df=1, P=0.77), we combined the three that hydrodynamic drag would be a less important year data. As the sample size for stomach contents factor for them compared with other species were rather small, three-day trips (n=4 samples) that dive frequently. The deployment of devices were categorized as short trips and used in the diet (1.5–2% body weight) on the related Cory’s Shear- analyses. water C. diomedea was not found to affect body con- The stomach content mass was greater for long dition, breeding success, or diet (Igual et al. 2005). trips (64.4±32.7 g, n=16) than for short trips (24.0± The proportional masses of our loggers (2–4%) 14.4 g, n=22; Mann-Whitney U-test, U=41.5, attached to Streaked Shearwaters (body mass, P<0.001). The results were the same if three-day 513±52 g [430–612 g], this study) were comparable trips were excluded. and smaller than the average (5–12%) and the maxi- Japanese anchovy Engraulis japonicus was the mum (27%) masses of stomach contents. Therefore, prey eaten often during both short and long trips the loggers were considered unlikely to have serious (Table 3). Flying Fish Cypselurus hiraii and Common adverse effects during the short deployment (1–19 Squid Todarodes pacificus (mantle length; 53.3±12.9 days) in this study. mm, 21.0–61.0 mm, n=15) were eaten during short trips, while Pacific Saury Cololabis saira was eaten 2) Feeding behavior during long trips (Table 3). Oil was the most impor- The dive frequency (0.5–17.0 dives d –1) and the tant component of stomach contents for long trips maximum dive depth (6.0 m) of Streaked Shearwa- reflecting the long digestion time. Oil was absent for ters were lower and shallower than those of Puffinus short trips. shearwaters (82.5 dives d –1, 26 m for Balearic P. mauretanicus, Aguilar et al. 2003: 68.2 m for Sooty

Table 3. Occurrence and mass proportion of each prey in stomach contents collected from birds returning to the colony after short and long trips. Data from birds with no trip information are also shown. Data for 2003, 2005, and 2006 were combined.

Short trip (n=22) Long trip (n=16) Unknown (n=26) Prey %Occ. %Mass %Occ. %Mass %Occ. %Mass FISH Anchovy Engraulis japonicus 50 48 50 24 23 23 False Halfbeak Oxyporhamphus micropterus – – – – 4 4 Flying Fish Cypselurus hiraii 18 22 6 3 – – Keeltail Needlefish Platybelone argalus – – – – 4 10 Pacific Saury Cololabis saira – – 19 13 4 5 Common Dolphinfish Coryphaena hippurus 5 1 6 3 – – Percoidei sp. 5 3 – – – – Chub Mackerel Scomber japonicus 5 0 13 9 4 9 Fregate Mackerel Auxis rochei 9 11 6 0 – – Ocean Triggerfish Canthidermis maculata – – – – 4 2 Unidentified –––– 15 9 SQUID Common Squid Todarodes pacificus 18 15 – – 23 11 CRAB – – – – 4 0 OIL – – 81 48 42 27

15 K. MATSUMOTO et al.

P. griseus, Shaffer et al. 2006: 58 m for Short-tailed phase that lasted for more than 14 h (Fig. 3c) during P. tenuirostris, Weimerskirch and Cherel 1998: 66.5 a 6-day long trip. So using the mean flight speed of m for Flesh-footed P. carneipes, Rayner et al. 2011: the Streaked Shearwater (34.5km h –1, Shiomi et al. 13 m for Wedge-tailed P. pacificus, Burger 2001: 21 2012), as a reference, it was possible for this species m for Black-vented P. opisthomelas, Keitt et al. to travel to the Oyashio front during long trips (Fig. 2000). Their dive depth was similar to the maximum 3d). dive depth of Cory’s Calonectris diomedea (0.3–5.5 Productivity in the Oyashio region (≥500 mg C m, Monteiro et al. 1996; Brooke 2004). m –2 d –1) is greater than that in the Kuroshio region Streaked Shearwaters spend 4–24% of their trip (≤400 mg C m –2 d –1) (Kameda 2003). The abun- time landing on the water, made repeated short flights dance of Japanese Anchovy, the main prey of the and landings, then flew for long periods until the next Streaked Shearwater, also is higher in the Oyashio water-landing bout (Fig. 1a, b). Therefore streaked region, especially near the front, than in the Kuroshio Shearwaters search for prey patches in flight, feed region during summer and autumn (Murase et al. from the surface mainly by surface seizing and dip- 2007). The Streaked Shearwaters at Mikura Island ping (Kei Matsumoto personal observation) and increased their body mass during longer trips but lost occasionally by plunging as described by Oka (1994), mass during shorter trips (Ochi et al. 2010). Thus though the quick change of surge acceleration they foraged in waters with high food abundance to recorded during the descent by D2GT (Fig. 4) indi- accumulate body fuel reserves during long trips, cate active diving to a few meters. Thus our study while they foraged in low-productive waters near supports the idea that Calonectris species are less their colony to provision chicks more quickly during adapted morphologically to an underwater aquatic short trips: indicating that they adopted dual foraging mode of feeding (Kuroda 1954). strategies. Streaked Shearwaters made water landings during Streaked Shearwaters fed on Common dur- both day and night (Fig. 3). They fed mainly on ing short trips. Based on mantle length (53 mm), the Japanese Anchovy. are often distributed squids in the diet were juvenile (Mori & Nakamura near the sea surface at night but in the mid-waters or 2003). In the vicinity of Mikura Island, Common near-bottom layers during the day (Ohshimo 1996). Squid likely spawn in the summer (Arimoto & Inada Dense schools of anchovy, however, are sometimes 2003), and juveniles would be available in September balled up to the surface by Baleen Whales (Balae- and October. Squid in the stomach samples were noptera acutorostrata, B. edeni) and Pacific Bluefin mostly retained minimally digested indicating that Tuna Thunnus thynnus in day-light hours (Tamura et the birds had fed on them shortly before returning to al. 1998; Tamura & Fujise 2002; Kitagawa et al. the island in the evening, when juvenile squid are 2004; Murase et al. 2007). Streaked Shearwaters more likely to occur in surface waters (Hamabe have been observed to gather over Skipjack 1964). The Pacific Saury that was found in the stom- Katsuwonus palamis or Chub Mackerel Scomber achs of birds after long trips is abundant in the japonicus fishing sites during the day-light hours, Oyashio region (Sugisaki & Kurita 2004). Thus prey waiting in the air, before plunging to feed on , items taken during short and long trips reflect differ- possibly anchovy (Takahashi 2000; Wakabayashi ences in foraging areas. 2004). These behaviors (exploiting other marine There were significant differences in foraging predators feeding on fish schools) partly explain the behavior between years, though factors affecting feeding behavior of Streaked Shearwaters observed these differences were unknown. The frequency and using data-loggers in this study, i.e. making water- duration of water-landing bouts did not differ between landing bouts of 4–16 min duration (Appendix 1) short and long trips; suggesting that the encounter during day and night. rate and quality of prey patches might be similar in the Kuroshio and Oyashio regions. However, Streaked 3) Dual foraging strategies Shearwaters dove more frequently during short trips, Birds rearing chicks on Mikura Island foraged in suggesting that birds may pursue fish into the waters the warm Kuroshio region and/or in the Kuroshio- of the Kuroshio region. Oyashio mixed region during short trips but visited In conclusion, Streaked Shearwaters breeding on the cold Oyashio region as well during long trips. Mikura Island fed mainly from the sea surface pre- Actually, a bird flew continuously during a traveling sumably in targeting schools of pelagic fish. They

16 Foraging of Streaked Shearwater adopted dual foraging strategies, i.e they foraged in Martínez-Abraín A, Hobson KA, Ruiz X & Oro D warm, less-productive Kuroshio and Kuroshio- (2005) Short-term effects of data-loggers on Cory’s Oyashio mixed regions during short trips and in cold, shearwater (Calonectris diomedea). Mar Biol 146: more productive Oyashio regions as well during long 619–624. trips, and changed their diet and dive frequencies in Kameda T (2003) Studies on Oceanic Production using relation to the water masses. Ocean Color Remoto Sensing Data. Bull Fish Res Agen 9: 118–148. Keitt BS, Croll DA & Tershy BR (2000) Dive depth and ACKNOWLEDGMENTS diet of the Black-vented shearwater (Puffinus opis- This research was supported by a Grant-in-Aid for Scien- thomelas). Auk 117: 507–510. tific Research from JSPS (Specially Designated Research Pro- Kitagawa T, Kimura S, Nakata H & Yamada H (2004) motion given to Yamashina Institute for Ornithology and Diving behavior of immature, feeding Pacific bluefin #14656074, #20241001). We thank Y. Baba for sexing birds, tuna (Thunnus thynnus orientalis) in relation to sea- M. Nishida for laboratory facilities, N. Takeuchi, A. Kajita, H. son and area: the East China Sea and the Kuroshio- Arima, and K. Kazama for their assistance in the field, and S. Oyashio transition region. Fish Oceanogr 13: 161– Kurimoto for housing. T. Deguchi provided useful advice in 180. planning and data analysis. Kuroda N (1954) On the Classification and Phylogeny of the Order Tubinares, Particularly the Shearwaters REFERENCES (Puffinus) with Special Considerations on Their Oste- ology and Habitat Differentiation (Aves). Published Aguilar JS, Benvenuti S, Dall’Antonia L, Mcminn- by the author, Tokyo. Grivé M & Mayol-Serra J (2003) Preliminary results Kuroda N (1991) Distributional patterns and seasonal on the foraging ecology of Balearic shearwaters movements of in the North Pacific. (Puffinus mauretanicus) from bird-borne data log- J Yamashina Inst Ornithol 23: 23–84. gers. Sci Mar 67: 129–134. Monteiro LR, Ramos JA, Furness RW & Nevo AJD Altschul SF, Gish W, Miller W, Myers EW & Lipman (1996) Movements, morphology, breeding, molt, diet DJ (1990) Basic local alignment search tool. J Mol and feeding of in the Azores. Colon Water- Biol 215: 403–410. bird 19: 82–97. Arima H & Sugawa H (2004) Correlation between the Mori K & Nakamura Y (2003) Distribution of juvenile pitch of calls and external measurements of Streaked Japanese common squid Todarodes pacificus around shearwaters Calonectris leucomelas breeding on the Kuroshio-Oyashio transition region. Nippon Kanmuri Island. Jpn J Ornithol 53: 40–44. Suisan Gakkai Shi 69: 23–29. Arimoto T & Inada H (2003) Surume-ika no sekai (The Murase H, Tamura T, Kiwada H, Fujise Y, Watanabe H, World of Japanese common squid). Seizando, Tokyo Ohizumi H, Yonezaki S, Okamura H & Kawahara S (in Japanese). (2007) Prey selection of common minke (Balaenop- Brooke M (2004) Albatrosses and Petrels across the tera acutorostrata) and Bryde’s (Balaenoptera edeni) World. Oxford University Press, Oxford, pp 499. whales in the western North Pacific in 2000 and Burger AE (2001) Diving Depths of shearwaters. Auk 2001. Fish Oceanogr 16: 186–201. 118: 755–759. Ochi D, Oka N & Watanuki Y (2010) Foraging trip Chaurand T & Weimerskirch H (1994) The regular decisions by the Streaked Shearwater (Calonectris alternation of short and long foraging trips in the blue leucomelas) depend on both parental and chick state. petrel Halobaena caerulea: a previously undescribed J Ethol 28: 313–321. strategy of food provisioning in a pelagic seabird. J Odate K (1994) Zooplankton biomass and its long-term Anim Ecol 63: 275–282. variation in the western north Pacific Ocean, Tohoku Gentry RL & Kooyman GL (1986) Methods of Dive sea area, Japan. Bull Tohoku Nat Fish Res Inst 56: Analysis. In Gentry RL & Kooyman GL (eds) Fur 115–173. Seals: Maternal Strategies on Land and at Sea. Ohshimo S (1996) Acoustic Estimation of Biomass and Princeton University Press, Princeton, New Jersey. School character of Anchovy Engraulis japonicus in Hamabe M (1964) Study on the migration of squid the East China Sea and the Yellow Sea. Fish Sci 62: (Ommastrephes sloani pacificus STEENSTRUP) 344–349. with reference to the age of the moon. Nippon Suisan Oka N (1994) Underwater feeding of the three shearwa- Gakkai Shi 30: 209–215. ters: Pale-footed (Puffinus carneipes), Sooty (Puffi- Igual JM, Forero MG, Tavecchia G, González-Solis J, nus griseus) and Streaked (Calonectris leucomelas)

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18 Foraging of Streaked Shearwater 11 11 14 10 8 12 5 2 15 5 3 5 18 dur. (s) dur. Max. dive 5±3 6±3 5±2 4±2 6±3 5±3 3±1 2±0 7±4 4±1 3±1 3±2 7±5 Dive dur. (s) dur. 2.5 2.1 depth (m) Max. dive Dive 0.7±0.5 2.1±0.2 2.7 0.9±0.8 2.7 depth(m) 9 4 0.4±0.3 0.8 8±11 2± 2 1.2±1.1 4.3 3± 3 1.2±1.4 6 3± 4 1.0±0.6 8± 7 1.1±0.8 3.1 5± 4 3± 2 0.7±0.3 1 1± 1 0.3 0.3 2 2 No. of 11 ±

10± 2 1.2±1.0 3

dives (n/d) 4±11 9±13 6± 6 9±15 6± 9 6 1.6±0.1 1.6 4± 4 17 1.7±1.3 4.2 6± 75± 7 3 0.7±0.4 1.1 4± 5 6± 8 6±10 11±12

16±53 10±19

Water-landing Water-landing bout dur. (min) bout dur. 3±11 3±13 4±13 3± 5 2± 2 2± 4 2± 5 1± 3 1± 2 1± 22± 4 1± 2 2± 2 2± 3 dur. (min) dur. Water-landing Water-landing 42 58 39±8 (n/d)

45±15 51±15 96±45 95±49 57±31 Landing 11 11 11 12 60±41 17 69±41 12 6 10 10 69 9 9 70 4 13 60±18 24 118±74 Time on Time water (%) 3 2 7 2 2 1 1 1 1 1 1 1 1 1 activity data No. of trips with 2 trips No. of 11 14 3 3 2 1 1 1 2 1 2 2 1 Days of deployment 518 520 540 530 545 522 593 Feeding behaviour of individual Streaked Shearwaters rearing chicks on Mikura Island. Mean±SDShearwaters rearing Streaked of individual Feeding behaviour are shown. 2006 DT F 430 3 2 2006 D2GT F 482 2 2 Bird Year Logger Sex Mass 1 2003 DT M 2 2003 DT M 3 2003 DT F 480 19 8 4 2003 DT M 5 6 2006 DT M 482 10 1 7 2006 DT M 612 1 1 9 2006 D2GT M 8 2006 DT F 498 4 1 10 2006 D2GT M 11 12 2006 D2GT M 13 2006 D2GT M 14 2006 D2GT F 430 2 1 Appendix 1.

19