(0.8 Km East of Yururi Island) in 1981

山階鳥研報(J.Yamashina Inst.Ornith.),20:71-81,1988

Regional Difference in the Diet of Slaty-backed Gulls Breeding Around Hokkaido

Yutaka Watanuki*

Abstract Regional difference in the diet of Slaty-backed Gulls, Larus schistisagus was studied

at the colonies around Hokkaido, Japan. They fed their chicks with sardines Sardinops melanosticta , rock fish Sebastes spp., and seabird chicks on Teuri Island, sardines on Daikoku Island and sardines and sandlances Ammodytes sp. on Yururi Island. They preyed upon chicks of seabirds such as Black-tailed Gulls L. crassirostris, Rhinoceros Auklets Cerorhinca monocerata and conspecifics on Teuri Island, while they preyed upon adults of Leach's Storm-Petrels Oceanodroma leucorhoa on Daikoku, Yururi and Moyururi Islands. Although availability of conspecific chicks was higher on Daikoku, Yururi and Moyururi Islands than on Teuri Island, they preyed upon conspecific chicks

more frequently on Teuri Island than on Daikoku, Yururi and Moyururi Islands. Thus , availability of conspecific chicks did not explain the regional difference in the occurrence of predition attempts on conspecific chicks.

Introduction

Regional differences in the diet have been reported in many species of Larus gulls. These differences have been attributed to regional differences in the food availability (Harris 1965, Andersson 1970, Spaans 1971, Trapp 1979, Vermeer 1982 and Gotmark 1984). Among Great Skuas Catharacta skua, regional difference in food preference also affected regional difference in the diet (Furness 1979). In order to better understand of the factors responsible to regional diet difference among gulls, an additional study was made on Slaty-backed Gulls Larus schistisagus breeding around Hokkaido, Japan. They are ecological generalists that forage fish , marine invertebrates, garbage and seabird chicks (Watanuki 1984a). This paper describes the regional difference of their diet that was determined by food-loads delivered to chicks and pellets and food remains.

Study Area and Methods

1. Study area

The study was conducted on Teuri Island (44°25'N,141°19'E) in 1980,1984 and 1985,on Daikoku Island (42°56'N,144°52'E) in 1982 and on Yururi Island (43°13'N , 145°36'E) in 1983 (Fig.1). Additional data were obtained on these three islands in 1981 , on Teuri Island in 1979 and 1987, on Daikoku Island in 1986 and on Moyururi Island (0 .8 km east of Yururi Island) in 1981.

Received 1 February 1988 * Institute of Applied Zoology , Faculty of Agriculture, Hokkaido University, Kita-9, Nishi-9, Kita-ku, Sapporo 060, Japan Present address: National Institute of Polar Research, 9-10, Kaga 1-chome, Itabashi-ku, Tokyo 173, Japan

71 72 Y. Watanuki

Fig. 1. Map of Hokkaido showing the locations of the study colonies of Slaty-backed Gulls.

Teuri Island is located 28km off Haboro. About 3km of a total of 12km coast line is comprised of steep cliffs rising 80-100m above sea level. About 200-400 pairs of Slaty-backed Gulls, 20,000-30,000 pairs of Black-tailed Gulls L. crassirostris,172,000 pairs of Rhinoceros Auklets Cerorhinca monocerata and 500-700 pairs of Japanese Cormorants Phalacrocorax filamentosus bred on the island. Daikoku Island is located 1.8km off Tokotan. A total of 6.1km coast line of the island is comprised of cliffs, about 40-80m in height. About 3,500 pairs of Slaty-backed Gulls, 300 pairs of Japanese Cormorants and 415,000 pairs of Leach's Storm-Petrels Oceanodroma leucorhoa bred on the island. Yururi Island is located 3km off Konbumori, Nemuro together with Moyururi Island. Circum- ference of Yururi and Moyururi is 7.5km and 3km, respectively. The coast lines of both islands are comprised of cliffs of 30-40m height. About 800 pairs of Slaty-backed Gulls and 90 pairs of Japanese Cormorants bred on Yururi and about 1,200 pairs of Slaty- backed Gulls and 250-300 pairs of Japanese Cormorants bred on Moyururi. Further details of these islands can be found in Kuroda (1963) and Watanuki et al. (1986) for Teuri, in Kushiro Municipal Museum (1981) for Daikoku and in Fujimaki et al. (1976) and Kondo et al. (1986) for Yururi and Moyururi. Diet of Slaty-backed Gulls 73

2. Study plot On Teuri, one study plot containing 42-71 nests was set in a center of a subcolony on a gradual slope with sparse vegetation of Artemisia and Calamagrostis, and boulders. On Daikoku, I set four study plots; three were on relatively steep slopes covered with dense stands of Artemisia and Elymus and one was on a rocky slope with sparse vegetation. Each plot contained 14-42 nests. On Yururi, I set two study plots containing 45 and 42 nests, respectively on a beach strewn with boulders and several clumps of vegetation and one plot containing 15 nests on a maritime slope of a small headland covered with Elymus. Individual nests in the plots were marked with numbered wooden stakes after the first egg of a clutch was laid.

3. Diet analysis Every 5 days, I visited all the nests in the study plots and collected pellets, food remains and food-loads regurgitated by chicks or parents found in each territory. Following types of pellets and food remains were separated: fish, marine invertebrates (seashell, crab, seaurchin, starfish and squid), eggs of seabirds, adults and chicks of seabirds, rodents, insects, chicken meat bones, papers and seeds. Species of seabirds were recorded if possible. Food-loads were preserved in 10% formaldehyde and weighed in a laboratory. Pellets and food remains that were collected from one nest per one visit, were combined. Then the combined sample was defined as a "nest-sample". One or more remains of single food type that were found in a nest-sample was counted as one point of that food type. Then, % occurrence of each food type was calculated as the proportion of the sum of the point of it. Gulls usually regurgitate larger portions of inedible parts of foods as pellets and food remains when they eat marine invertebrates or seabirds than they do when they eat fish or earthworms (Spaans, 1971; Watanuki, 1984b). Hence, the occurrence of marine invertebrates and seabirds in pellets and food remains shows a larger value than that in food-loads. Foods for chicks differed from those for parents own in Great Skuas (Furness & Hislop, 1981). However, it would be reasonable to compare the diets among colonies using occurrence of food items in the pellets and food remains. As no food-loads was collected on Daikoku Island, I recorded the occurrence of food items in food-loads by observing about ten breeding pairs with binoculars during the chick raising period in 1986. I also recorded the predation attempts by Slaty-backed Gulls ad libitum. I assumed a "predation attempt" when the gull attacked potential prey at least one time. I excluded attacks on adults of Black-tailed Gulls and conspecific chicks in the context of territorial aggressions. Differences between predatory behaviors on conspecific chicks and attacks by neighbor adults on chicks in the context of territorial aggression are described in Watanuki (in press). The number of remains of seabird species including wings, feet and bones was counted. Then % composition of the remains of esch species was calculated. The prey preference was evaluated by Ivlev's Elective Index (Ei), calculated from % composition of i th seabird species (or type) available (Ni) and % composition of the i th species in the 74 Y. Watanuki pellets and the food remains (ri), Ei=(ri-Ni)/(ri+Ni), : (Ivlev, 1965). Positive Ei (<1.0) suggests that the gulls kill i th prey more frequently than expected from the % composition of available prey (or the gulls "prefer" i th item). Furness and Hislop (1981) reported that Great Skuas tore the body of prey into three or four portions when they killed large seabirds, hence possibly regurgitate three or four pellets. Slaty-backed Gulls swallowed eggs and small chicks of gulls and chicks of Rhinoceros Auklets, while they tore large chicks or fledglings of gulls. Hence, the number of large chicks killed by Slaty-backed Gulls might be overestimated. Although I could not determine the relationship between the number of pellets and the size of prey in this study, I assumed that there was no regional difference in this relationship and believe that it is reasonable to compare the Ei s between colonies. The number of available prey was estimated from the number of breeding pairs, the mean clutch size and the brood size of the species (Watanuki et al., 1986; Kondo et al., 1986; Watanuki, 1987).

4. Body size Morphometric measurements were made on adult Slaty-backed Gulls on Teuri and Daikoku. Breeding adults were captured with box traps on Teuri during their incubation period. Sexes were determined from their courtship and copulation behaviors following Tinbergen (1959) and Burger and Beer (1975). Additional data were obtained from dead birds collected on Teuri and Daikoku, in which the sexes were determined by dissection. Food load size and body size of Slaty-backed Gulls are shown as the mean±SD and sample size in parentheses. Difference between values were examined with Mann-Whitney U-test.

Results

1. Diet The seabird remains occurred frequently on Teuri and Daikoku, while rarely occurred on Yururi(Table 1). Most of items found in the pellets and food remains on Yururi were bones and scales of fish. Marine invertebrates were minor foods on every islands. Among invertebrates, crabs (Pugettia sp. and Pagurus sp.) and molluscans (Tugalina spp. and Cellana spp.) occurred frequently on Teuri, and chiton Cryptochiton stelleri and a crab Telmessus sp. occurred frequently on Daikoku and Yururi. Cryptochiton and Telmessus are distributed along the eastern coast of Hokkaido but do not along the north west side of it. More than half of the diet brought to chicks by parents was sardines Sardinops melanosticta on Daikoku and Yururi, while the parents fed their chicks with wasted bottom-living fish such as rock fich Sebastes spp. and Japan Sea greenling Pleurogrammus azonus as well as sardines and sandlances Ammodytes personatus on Teuri (Table 2). The Slaty-backed Gulls foraged on these bottom-living fish at docks when the fishermen wasted these fishes. Diet of Slaty-backed Gulls 75

Table 1. Percentage occurrence of food items in pellets and food remains of Slaty-backed Gulls found in their territories on Teuri, Daikoku, Yururi and Moyururi Islands between June and August.

Table 2. Prey items found in food-loads of Slaty-backed Gulls. Percentage occurrence (% occ.) and percentage wet weight (% wt.) are shown.

Seabird chicks were the other primary foods on Teuri (Table 2). The occurrence of adult Leach's Storm-Petrels in food loads was much smaller than that in pellets and food remains on Daikoku (Tables 1 and 2). This is because the inedible parts of the adult Leach's Storm-Petrel was much more than that of fish (Watanuki, 1984b). Thus, Slaty-backed Gulls fed their chicks mostly with pelagic fish on Daikoku and Yururi, while 76 Y. Watanuki they fed wasted bottom-living fish and seabird chicks also on Teuri.

Wet weight of food-loads with sardines collected on Teuri(37.8±20.0g (6))was not different from that on Yururi (34.5±12.8g (19))(U=58, N.S.). Wet weight of food-loads with sandlances collected on Teuri (16.7±10.8g (4))was not different from that on Yururi (26.2±15.5g (6)) also (U=17, N.S.)

2. Composition of seabird prey Slaty-backed Gulls preyed upon chicks of Black-tailed Gulls and Rhinoceros Auklets frequently on Teuri and adults of Leach's Storm-Petrel on Daikoku, and Yururi & Moyururi. Although they preyed upon conspecific chicks on Teuri, they rarely did on Daikoku and Yururi & Moyururi (Table 3). One foot of a Japanese Cormorant occurred on Teuri (Table 3). As the size of the foot was similar to that of an adult, it was possibly the foot of a fledgling or a dead adult. Although the remains of adults of Rhinoceros Auklets, a Common Murre Uria aalge, and a Tufted Puffin Lunda cirrhata occurred in the pellets and food remains (Table 3), I did not observe successful predation attempts on these seabird adults by Slaty-backed Gulls (see Table 4). The gulls might scavenge dead adults of these large alcids. Slaty-backed Gulls killed chicks and fledglings of Black-tailed Gulls and Rhinoceros Auklet chicks, and conspecific chicks on Teuri, while they preyed upon mostly adult Leach's Storm-Petrels on Daikoku (Tabe 4). A Slaty-backed Gull took a small chick of Japanese Cormorant on Moyururi. Success rate of predation on chicks of Black-tailed Gulls (79% or 49/62) was higher than that on the fledglings (38% or 5/13). That on Rhinoceros Auklet chicks (75% or

Table 3. Number of seabird remains found in pellets and food remains of Slaty-backed Gulls on Teuri (1979-1985), Daikoku (1981-1982) and Yururi (1983) & Moyururi (1981) Islands. Data collected on Moyururi were combined with those on Yururi since the sample sizes were small and the compositions of prey species found on these islands were smilar. Diet of Slaty-backed Gulls 77

Table 4. Frequency of successful (S) and unsuccessful (F) predation attempts and foraging behaviors on freshly dead seabirds in parenthesis by Slaty-backed Gulls on Teuri (1979- 1987), Daikoku (1981-1982) and Moyururi (1982) Islands. Data on Teuri include 1979-1981 data in Watanuki (1983).

Table 5. Percentage composition of potentially available prey and prey preference shown by Ivlev's Elective Index (Ei) in parentheses. Seabirds were assumed to be potentially availabe to Slaty-backed Gulls when the successful predation attempt on these prey were observed at least one of the islands. Positive Ei (<1.0) suggests that the gulls kill ith prey more frequently than expected from the % composition of potentially available prey.

3/4) was similar to that on Black-tailed Gull chicks or was higher (95% or 20/21) when the foraging on freshly dead chicks were included as successful predation attempts. Slaty-backed Gulls strongly preferred chicks of Slaty-backed Gulls and Black-tailed Gulls and weakly preferred chicks of Rhinoceros Auklets on Teuri. However, they did not prefer chicks of two species of gulls on Daikoku and Yururi & Moyururi (Table 5). They preferred Leach's Strom-Petrel adults on Daikoku and Yururi & Moyururi. Although Leach's Storm-Petrels did not breed on Yururi and Moyururi, they frequently visited these islands at night during the summer (Kondo et al. 1986). Rhinoceros Auklet chicks were less preferred on Daikoku and Yururi & Moyururi than on Teuri. The Eis for 78 Y. Watanuki

Table 6. Measurements of Slaty-backed Gulls on Teuri and Daikoku Isla nds. The mean±S.D. and sample size in parentheses . Male and female data were combined .

chicks of Japanese Cormorants were negative on all the islands. Slaty-backed Gulls rarely took seabird eggs.

3. Morphology I measured bill length, bill depth, wing length and tarsus length of 21 adults (9 males and 12 females) on Teuri and 8 adults (3 males, 3 females and 2 sex unknown) on Daikoku. There were no significant differences between Daikoku and Teuri in bill length (U=93, N.S. ), bill depth (U=99, N.S. ), wing length (U=94, N.S.) and tarsus length (U =91 .5, N.S.) (Table 6).

Discussion

Among five species of European Larus gulls, large species such as Great Black-backed Gulls L. marinus frequently preyed upon eggs and chicks of seabirds, while small ones such as Black-headed Gulls L. ridibundus did not (Harris, 1965; Gotmark 1984). In the regional comparison among Slaty-backed Gulls, about 40% of food-loads were seabird chicks on Teuri, while only 5% were Leach's Storm-Petrel adults on Daikoku Island (Table 2). However, body sizes of Slaty-backed Gulls on Teuri and Daikoku were not different (Table 6). Hence, regional difference in the diet was not attributed to the difference in the body size. Regional difference of food availability has been found to be the primary factor relating to regional difference in the diet of gulls (Harris 1965, Andersson 1970, Spaans 1971, Trapp 1979, Vermeer 1982). Slaty-backed Gulls foraged on Cryptochiton and Telmessus at two colonies in eastern Hokkaido (Daikoku and Yururi), where these marine invertebrates are available. They preyed upon chicks of Black-tailed Gulls and Rhinoceros Auklets chicks on Teuri where these two species were abundant (Table 3). Regional difference in Evlev's Elective Index for seabird prey (Table 5) indicates regional difference in prey preference. Slaty-backed Gulls rarely preyed upon conspecific chicks on Daikoku, Yururi and Moyururi, while they preferred conspecific chicks on Teuri where their colony size was the smallest among these islands (Table 3). Nesting habitats and parental care of Slaty-backed Gulls on Yururi and those on Teuri were not different (Watanuki, in press, 1987): suggesting that chicks were potentially vulnerable to conspecific adults on Yururi also. Furness (1979) suggested that certain feeding skills have spread within colonies by imitative learning and develop in some areas but not in Diet of Slaty-backed Gulls 79 others in Great Skuas. For example, the Great Skuas killed large number of fledglings of Kittiwakes Rissa tridactyla in a certain region but in other regions they took eggs and small chicks of Kittiwakes. In Slaty-backed Gulls also, skills of intraspecific predation might spread within the Teuri population but not develop in the Daikoku, Yururi and Moyururi populations. On Teuri Island, some males specialized on seabird chicks and other males specialized on fish, and females rarely killed seabird chicks (Watanuki, 1987, submitted). Therefore, the predatory habit was not acquired by almost all the members of the regional population. Individual feeding specialization on the prey species was found in Great Skuas also (Bayes et al., 1964; Furness, 1979). Furness (1979) said that imitative learning assumed a certain degree of specializaion of individual feeding habits. During the development of a certain feeding skill in a population, a few individuals may have that skill but others may not. However, in Slaty-backed Gulls, there was no evidence indicating the spread of predatory habits within the Teuri population. Percentage occurrence of seabird remains in pellets and food remains did not increase between 1979 and 1985 chick raising periods (47.2% in 1979, 45.0% in 1980, 53.6% in 1981, 32.1% in 1984 and 33.0% in 1985). Further data on long term change of individual feeding specialization and on a mechanism of the transmission of certain feeding skills are needed to substantiate this hypothesis. Another explanation is that the skill of killing conspecific chicks is similar to that of killing chicks of Black-tailed Gulls that have similar breeding habitats and similar anti-predatory behaviors (Watanuki, 1983, 1987, submitted). Hence, Slaty-backed Gulls preyed upon conspecific chicks on Teuri where Black-tailed Gull chicks were abundant. These two hypotheses are not exclusive each other. In Slaty-backed Gulls, specialists on seabird chicks usually killed Black-tailed Gull chicks and conspecific chicks and others killed Rhinoceros Auklet chicks (Watanuki, 1987, submitted). Among pairs feeding their chicks with seabird chicks more frequently than the average portion, cannibal ones usually preyed upon Black-tailed Gull chicks, while non cannibal ones frequently preyed upon Rhinoceros Auklet chicks (Waranuki, in press).

Acknowledgments

I would like to thank M. Aotsuka and the Nogami family on Teuri Island, Akkeshi Marine Biological Station, H. Uno, S. Urano and the staffs of the light house on Daikoku Island and N. Kondo, T. Hino and the Yamazaki family on Yururi and Moyururi Islands for their gracious hospitality and logistical support on these islands. Thanks are also due to H. Mori and H. Abe for advice and encouragement during the course of the study. The Agency for Cultural Affairs and the Environment Agency gave permits to work on these islands. This study was partly supported by JSPS Fellowships for Japanese Junior Scientists.

References

Andersson, Å 1970. Food habits and predation of an inland-breeding population of Herring Gull, Larus 80 Y. Watanuki

argentatus in Southern Sweden. Ornis Scand. 1: 75-81. Bayes, J. C., M. J. Dawson & G. R. Potts. 1964. The food and feeding behavior of the Great Skua in the Faeroes. Bird Study 11: 272-279. Burger, J & C. G. Beer. 1975. Territoriality in the Laughing Gull, Larus atricilla. Behaviour 55: 20-32. Fujimaki, Y., T. Hyakutake & S. Matsuoka. 1976. Birds of Yururi and Moyururi Islands, eastern Hokkaido in summer; 1, cormorants and anserine birds. Miscellaneous Rep. Yamashina Inst. Ornithol. Zool. 8: 68-88. (In Japanese with English summary) Furness, R. W. 1979. Food of Great Skuas, Catharacta skua, at North Atlantic breeding localities. Ibis 121: 86-92. Furness, R. W. & J. R. G. Hislop. 1981. Diets and feeding ecology of Great Skuas, Catharacta skua, during the breeding season in Shetland. J. Zool. Lond. 195: 1-23. Gotmark, F. 1984. Food and foraging in five European Larus gulls in the breeding season: a comparative review. Ornis Fennica 61: 6-18. Harris, M. P. 1965. The food of some Larus gulls. Ibis 107: 43-53. Ivlev, B. C. 1965. Experimental Ecology of Nutrition of Fishes. (Translated into Japanese by Kodama & Yoshihara). Tatarashobo, Yonago. Kondo, N., M. Hashimoto & Y. Watanuki. 1986. Change of birds on Yururi and Moyururi Islands. Memoirs of the Preparative Office of Nemuro Municipal Museum 1: 33-46. (In Japanese with English abstract). Kuroda, N. 1963. A survey of sea birds of Teuri I, Hokkaido, with notes on land birds. Miscellaneous Rep. Yamashina Inst. Ornithol. Zool. 3: 363-383. (In Japanese with English summary). Kushiro Municipal Museum, 1981. A Report of the scientific survey of Daikoku Island and surrounding areas. Kushiro Municipal Museum, Spec. Publ. (In Japanese). Spaans, A. L. 1971. On the feeding ecology of the Herring Gull, Larus argentatus Pont. in the northern part of the Netherlands. Ardea 59: 73-188. Tinbergen, N. 1959. Comparative studies of the behaviour of gulls (Laridae): a progress report. Behaviour 15: 1-70. Trapp, J. T. 1979. Variation in summer diets of Glaucous-winged Gulls in the Western Aleutian Islands: an ecological interpretation. Wilson Bul. 91: 412-419. Vermeer, K. 1982. Comparison of the diets of Glaucous-winged Gull on the east and west coast of Vancouver Island. Murrelt 63: 80-85. Watanuki, Y. 1983. Predation and anti-predation behaviour in seabirds on Teuri Island, Hokkaido. J. Yamashina Inst. Ornithol. 15: 167-174. Watanuki, Y. 1984a. Food of Slaty-backed Gulls around Hokkaido during breeding season. Kaiyou Kagaku 16: 212-216. (In Japanese). Watanuki, Y. 1984b. Food intake and pellets of Black-tailed Gull Larus crassirostris. J. Yamashina Inst. Ornithol. 16: 168-169. Watanuki, Y. 1987. Interspecific, inter- and intracolony differences in food habits and breeding of Larus gulls. Unpublished Ph. D. Thesis, Hokkaido University. (In Japanese). Watanuki, Y. in press. Intraspecific predation and chick survival: comparison among colonies of Slaty-backed Gulls. Oikos 53. Watanuki, Y. submitted. Sex and individual differences in the diet of Slaty-backed Gulls bulls breeding on Teuri Island, Hokkaido. Watanuki, Y., M. Aotsuka & T. Terasawa.1986. Status of seabirds breeding on Teuri Island. Tori 34: 146-150. (In Japanese). Diet of Slaty-backed Gulls 81

北海道周辺におけるオオセグロカモメの食性の地域間の変異

オオセグロカモメLarus schistisagusの食性を北海道のいくつかの繁殖地で調査した。天売島ではマイワ

シSardinops melanosticta,メバルSebastes spp.,および海鳥の雛,大黒島ではマイワシ,ユルリ島ではマイワ

シとイカナゴ,Ammodytes sp.が雛に与える主要な餌であった。天売島ではウミネコL.crassirostrisの雛,ウ

トウCerorhinca monocerataの雛およびオオセグロカモメの雛が主要な獲物であったのに,大黒島,ユルリ

島及びモユルリ島ではコシジロウミツバメOceanodroma leucorhoaの成鳥を捕食していた。同種の雛の現存量は大黒島,ユルリ及びモユルリ島のほうが天売島よりも大きかったが,オオセグロカモメは天売島で,より頻繁に同種の雛を捕食していた。よって,同種の雛の捕食頻度の地域差は,獲物の現存量の地域差からは説明できなかった。

綿貫豊:北海道大学農学部応用動物学教室,〒060札幌市北区北9条西9丁目現在:国立極地研究所,〒173東京都板橋区加賀1-9-10