INTRODUCTION

Estuarine tidal flats in Japan and adjacent countries are important foraging places for many migratory shorebirds during the cold season (from autumn to spring), because these tidal flats are located along the East Asian-Australasian flyways of migratory birds (Akiyama, 1988; Hanawa and Takeishi, 2000; Sato and Koh, 2004). However, recent human impacts in Asian countries have caused severe loss or degradation of their habitats, endangering many bird species and their potential prey invertebrates (Wetlands International-Asia Pacific and International Waterfowl and Wetland Research Bureau-Japan Committee, 1996; Wada et al., 1996).

A stable food supply for shorebirds on tidal flats seems to be important to maintain their regular migration. Clarification of foraging habits (e.g., dietary items) of shorebirds is essential to knowing their carnivorous roles in the tidal flat ecosystem and to establish their effective conservation. Previous studies have revealed that macrobenthic invertebrates such as polychaetes, crustaceans, and mollusks constitute a major part of the diet of migratory shorebirds during the wintering period (see Akiyama, 1988). However, most such studies have been carried out in Europe, and little is known about the prey of shorebirds in Asian estuaries, though Nuka et al. (2005) revealed detailed foraging habits of the Sanderling (Calidris alba) in a Japanese sandy seashore. Although most previous studies on the prey items of shore-birds were carried out by analyses of stomach (gizzard) contents obtained from captured birds (Madon, 1935; Ehlert, 1964; Recher, 1966; Bengston and Svensson, 1968; Goss-Custard, 1969; Davidson, 1971; Kawaji and Shiraishi, 1979), there are other methods which do not require the killing of birds, i.e., watching the feeding behavior of representative individual birds through binoculars or telescope (e.g., Goss-Custard et al., 1977) and the analysis of regurgitated pellets (Worrall, 1984) or fecal droppings (Feare, 1966; Dit Durell and Kelly, 1990; Mouritsen, 1994; Akiyama, 2000; Nuka et al., 2005).

Fujimae-higata is 120-ha area of muddy tidal flats, located at the joined mouths of the Nikko-gawa and Shin-kawa Rivers in the innermost part of Ise Bay, Nagoya, central Japan (Fig. 1). In a survey of major Japanese tidal flats from 1988 to 1996 (Japanese Association for Preservation of Birds, 1997), the second highest number of migrating or over-wintering waders (6,950 individuals) was recorded in the estuary that includes Fujimae-higata. In monthly counts from April 1999 to March 2000 at Fujimae-higata, more than 500 Dunlin (Calidris alpina) and more than 50 Black-headed gulls (Larus ridibundus) were observed continuously from January to May and September to May, respectively (Nagoya City, 2001).

Fig. 1.

Maps showing the location of the study area in Japan (left) and the locations of the collecting stations (right). Stations 1 to 5 were on the tidal flats of Fujimae-higata, located at the joined mouths of the Nikko-gawa and Shin-kawa Rivers in the innermost part of Ise Bay, central Japan. Gray areas indicate tidal flats appearing at mean low water level on spring tides. Arrows indicate river flows into Ise Bay. B, Nikko-gawaohhashi Bridge.

The Dunlin is the most common wader species wintering in Japanese estuaries. Total numbers of wintering individuals of C. alpina counted in 90–97 major habitats in Japan ranged from 29,000 to 37,000 between 1999 and 2002, constituting 63 to 67% of the whole wader populations (World Wide Fund for Nature Japan, 2003).

The present study was conducted to describe the dietary items of the Dunlin and four other common species of estuarine shorebirds by monthly analyses of their fecal droppings and surveys of the macrobenthic fauna around a foraging site in Fujimae-higata throughout the wintering period.

MATERIALS AND METHODS

Analyses of fecal droppings

In the eastern part of Fujimae-higata (around stations 1–5 in Fig. 1) where high foraging activity of shorebirds had been observed, fecal droppings of five species of shorebirds were collected from the surface of exposed tidal flats around the lowest one of two low tides in months during two wintering periods. The lowest tides occur at night in winter (from November to February) and in the day in spring (from March to May). Wintering shorebirds usually feed regularly by day and night (Mouritsen, 1994). Prior to each sampling, locations of foraging populations of each species on the tidal flats were determined with binoculars from the edge of land, and then visited for sampling. Bird species could be identified even at night, because Fujimae-higata is continuously lighted by illumination from surrounding factories working at night. We sampled only droppings for which correct identification was ensured by examination of the size and shape of footprints around the droppings (Fig. 2). Footprints of the Dunlin (Calidris alpina; length of middle finger around 2.5 cm) were smaller than those of the Grey Plover (Pluvialis squatarola; around 3.5 cm) and Black-headed Gull (Larus ridibundus; around 5.5 cm).

Fig. 2.

Fecal droppings and the footprints of shorebirds on the tidal flats of Fujimae-higata. (a) Dunlin (Calidris alpina) on 18 January 1999. (b) Grey Plover (Pluvialis squatarola) on 18 January 1999. (c) Black-headed Gull (Larus ridibundus) on 18 January 1999. Scale, 1 cm.

During the first wintering period in 1999, several droppings from each species were pooled in a bottle and fixed in 80% ethanol. Sampling dates (time) and bird species from which droppings were excreted are as follows; 18 January (0:00–2:00), C. alpina, P. squatarola, and L. ridibundus; 22 March (14:00–16:00), C. alpina and L. ridibundus; 3 May (12:00–14:00), C. alpina and N. phaeopus which had a stopover here.

Part of each sample of droppings (0.05–0.1 cc) was placed on a glass slide and examined under a microscope. This examination was repeated five times for each sample.

During the second wintering period from 1999 to 2000, droppings were fixed individually. Examination under a microscope was repeated five times for each sample as mentioned above. Sampling dates and bird species from which droppings were obtained are as follows: 25 November 1999 (0:00–2:00), C. alpina (29 individuals) and L. ridibundus (1); 23 January 2000 (0:00–2:00), C. alpina (13), P. squatarola (5), and L. ridibundus (2); 20 February (0:00–2:00), C. alpina (4) and P. squatarola (3); 22 March (12:00–15:00), C. alpina (7) and L. ridibundus (5); 22 April (12:00–15:00), C. alpina (14) and the Red-necked Stint, C. ruficollis (5); 6 May (12:00–15:00), C. alpina (26).

RESULTS

Macrobenthic fauna in the tidal flats

A total of 27 species of macrobenthic organisms were collected (Appendix 1), including 16 polychaetes, four crustaceans and four bivalves.

Polychaetes were dominant throughout the year in terms of both density (maximum 8,850 individuals/m² in July 1999; Fig. 3) and biomass (maximum 392 g/m² in September 1999; Fig. 4). In summer (July and September), small, young individuals of a nereidid polychaete (Hediste diadroma) were densest. As the density of H. diadroma decreased during the following autumn and winter, its body size increased considerably (Fig. 5). Therefore, the biomass of H. diadroma was the greatest (40–370 g/m²) of all benthic organisms throughout the year, except for less than 1 g/m² in May 1999 and March 2000 (during or just after reproduction). During the reproductive period of H. diadroma (March 1999), we collected a large, nearly mature female that had eggs 110–140 μm in diameter in its coelom. The density (1,300–4,800 individuals/m²) and biomass (16–57 g/m²) of capitellid polychaetes (mainly Notomastus sp. and Heteromastus sp.) were also relatively high throughout the year. A relatively high density of a spionid polychaete (Prionospio (Minuspio) japonica) was recorded from winter to spring (300–2,100 individuals/m²).

Fig. 3.

Monthly changes in the density of polychaetes, crustaceans, and bivalves around station 4 or 5 on the tidal flats of Fujimae-higata from January to November 1999 and March 2000.

Fig. 4.

Monthly changes in the biomass of polychaetes, crustaceans, and bivalves around station 4 or 5 on the tidal flats of Fujimae-higata from January to November 1999 and March 2000.

Fig. 5.

(a) Monthly changes in the individual biomass (wet weight/individual) of representative macrobenthic organisms [Hediste diadroma (Polychaeta), capitellids (Polychaeta), and amphipods (Crustacea)] around station 4 or 5 on the tidal flats of Fujimae-higata from January to November 1999 and March 2000. (b) Monthly records of individual numbers of the Dunlin Calidris alpina (CA) and the Black-headed Gull Larus ridibundus (LR) observed in the same place from April 1999 to March 2000 (data from Nagoya City, 2001). Data from January to March (*) represent those in 2000. Black circles, more than 500 individuals; gray circles, 51–500 individuals; white circle, 11–50 individuals.

Among crustaceans, amphipods (mainly Grandidierella sp.) were dense from March to May (2.8–3.9 g/m²), and juveniles of Upogebia major were found in May and July (1.2–1.8 g/m²). Among bivalves, Corbicula japonica was dominant (maximum biomass 159 g/m²).

In April 1997, a nereidid polychaete (Neanthes succinea) was dominant in terms of biomass (55–87 g/m²) at four sites (stations 2–5), whereas a goniadid polychaete (Goniada sp.) (15 g/m²) and an amphipod (Grandidierella sp.) (14 g/m²) were dominant at station 1 (Fig. 6). Hediste diadroma was absent except for the occurrence of a juvenile at station 5. The biomass of capitellid polychaetes (mainly Notomastus sp. and Heteromastus sp.) was also large at station 4 (46 g/m²), and a large bivalve (C. japonica) was collected at station 5 (74 g/m²).

Fig. 6.

Variation in the (A) density and (B) biomass of polychaetes and crustaceans (all amphipods) at five stations on the tidal flats of Fujimae-higata on 25 April 1997.

Contents of droppings of Calidris alpina

During the first wintering period in 1999, body parts (chaetae, aciculae, or jaws) of nereidid polychaetes were commonly found in pooled samples of droppings from Calidris alpina (Fig. 2a) in January and March, but were not found in May (Table 1). Similar results were obtained during the second wintering period. Most (85–100%) of the droppings from C. alpina contained nereidid body parts from November 1999 to April 2000, whereas only 23% of droppings contained them in May 2000 (Table 1, Figs. 7A, 8a, c, d). The nereidid body parts included simple chaetae (Fig. 8c), which are specific to the posterior parapodia of the genus Hediste (Sato and Nakashima, 2003). The simple chaetae were found more frequently from November 1999 to February 2000 (28–70% of C. alpina droppings) than from March to May 2000 (8–21% of droppings) (Fig. 7A).

Table 1.

Occurrence of nereidid body parts in fecal droppings from 5 shorebird species (Calidris alpina, C. ruficollis, Pluvialis squatarola, Numenius phaeopus, Larus ridibundus). Values and symbols in perentheses indicate the occurrence of Hediste-specific simple chaetae.

Fig. 7.

Monthly changes in the percentage of fecal droppings from the Dunlin Calidris alpina containing (A) body parts of nereidid polychaetes, (B) chaetae of capitellid or spionid polychaetes, and (C) body parts of crustaceans. Black bars in A indicate the percentage of droppings containing simple chaetae of worms of the genus Hediste. The number at each bar in (C) indicates the number of droppings examined.

Fig. 8.

Micrographs of body parts of nereidid polychaetes found in fecal droppings from the Dunlin (Calidris alpina) (a, c, d) and Black-headed Gull (Larus ridibundus) (b). (a) A jaw, 23 January 2000. (b) Many compound chaetae and thick black aciculae, 22 March 2000. (c) A simple chaeta typical of worms of the genus Hediste, 18 January 1999. (d) A heterogomph falciger, 18 January 1999. Scale bars, 100 μm.

Capillary chaetae (Fig. 9a) and hooded hooks (Fig. 9b), which seemed to be derived from capitellid and spionid polychaetes, were found more frequently from January to April 2000 (38–86% of C. alpina droppings) than in November 1999 and May 2000 (0–19% of droppings) (Table 2, Fig. 7B)

Fig. 9.

Micrographs of chaetae of capitellid or spionid polychaetes found in fecal droppings of the Dunlin (Calidris alpina), 23 January 2000. (a) A capillary chaeta. (b) A hooded hook. Scale bars, 100 μm.

Table 2.

Occurrence of capitellid or spionid body parts in fecal droppings from 5 shorebird species. Values and symbols as shown in Table 1.

Crustacean body parts were also commonly found in droppings of C. alpina (Fig. 10). Some were identified as parts of the appendages of an amphipod, Grandidierella sp. (Fig. 10b). The crustacean body parts were found more frequently from March to May 2000 (86–100% of droppings) than from November 1999 to February 2000 (25–55% of droppings) (Table 3, Fig. 7C)

Fig. 10.

Micrographs of body parts of crustaceans found in fecal droppings from the Dunlin (Calidris alpina). (a) An appendage. (b) Probably a gnathopod from an amphipod. Scale bars, 100 μm.

Table 3.

Occurrence of crustacean body parts in fecal droppings from 5 shorebird species. Values and symbols as shown in Table 1.

DISCUSSION

Our results show that five species of shorebirds (Calidris alpina, C. ruficollis, Pluvialis squatarola, Numenius phaeopus, and Larus ridibundus) foraging in Fujimae-higata during migration or wintering exploit as food sources dominant macrobenthic invertebrates such as nereidids, capitellids, spionids (polychaetes), and an amphipod (crustacean). Of all the food sources, two nereidid species (Hediste diadroma and Neanthes succinea) with relatively large body size and large biomass in the tidal flats seemed to be the most important diet. A similar result was obtained on the tidal flats of the Ichinomiya-gawa estuary, central Japan, where nereidid (the genus Hediste) and capitellid polychaetes were dominant (Akiyama, 2000); nereidid body parts (chaetae or jaws) including Hediste simple chaetae were present in 78% of 100 droppings of C. alpina, and 44% of them also contained capitellid body parts (hooded hooks).

Calidris alpina subsists mainly on insects on Arctic breeding grounds (Holmes, 1966), whereas it feeds mainly on macrobenthic invertebrates on tidal flats during migration or wintering (Akiyama, 1988). Although the food items taken by C. alpina are somewhat variable depending on its wintering sites (Akiyama, 1988) or light conditions (diurnal or nocturnal) (Mouritsen, 1994), nereidid polychaetes represented by Hediste species seem to be the most important diet for C. alpina not only in Asia but also in Europe. In the inner part of the Ariake Sea, western Japan, Kawaji and Shiraishi (1979) found that jaws of a Hediste species, probably H. japonica (Sato and Nakashima, 2003), were most abundant in four stomachs of C. alpina, followed by shells of Fluviocingula nipponica (gastropod). In Ore-sound in southern Sweden (Bengtson and Svensson, 1968), the Danish Wadden Sea (Mouritsen, 1994), Mellum near Helgoland in Germany (Ehlert, 1964), and the Severn Estuary in South Wales (Worrall, 1984), Hediste diversicolor was judged from analyses of stomach contents and/or regurgitated pellets or fecal droppings to be by far the most important dietary item of C. alpina, although Hydrobia spp. (gastropods), Macoma balthica (a bivalve), and/or Corophium volutator (a crustacean) were also commonly found. Wolff (1969) showed that the distribution of C. alpina agreed very well with that of H. diversicolor in the Delta area of the Netherlands. In California, USA, another nereidid species, Neanthes succinea, which was dominant there, comprised the major component of gizzard contents of C. alpina (Recher, 1966).

Goss-Custard et al. (1977) found that H. diversicolor was also the most important prey species for the Redshank (Tringa tetanus) and Curlew (Numenius arquata), by direct observation of feeding behavior and surveys of macrobenthic fauna.

On the other hand, an analysis of fecal droppings demonstrated that H. diversicolor was not more important in the diet of C. alpina than other small polychaetes such as Nephtys spp., phyllodocid and spionid species, and mollusks such as Hydrobia ulvae, although H. diversicolor was the main prey item taken by the Grey Plover (Pluvialis squatarola) in the Wash, southeastern England (Dit Durell and Kelly, 1990). Small oligochaete worms seemed to be of considerable importance in the diet of C. alpina in the Wash (Dit Durell and Kelly, 1990) and Teesmouth (Evans et al., 1979).

Foraging habits of many shorebirds such as C. alpina seem to be closely related to the life histories of their major prey species, Hediste spp. In contrast to Europe, where Hediste worms consist of a single species (H. diversicolor), in Asia Hediste worms comprise three similar but morphologically distinct species (H. japonica, H. diadroma, and H. atoka); H. diadroma and H. atoka are commonly distributed across a wide range of Japanese estuaries and often occur sympatrically, whereas H. japonica is distributed in the inner part of the Ariake Sea in Japan and the coast of the Yellow Sea (Sato and Nakashima, 2003; Sato, 2004). All Hediste worms collected from Fujimae-higata during the present survey were identified as H. diadroma. The life span of this species is one year (Qiu and Wu, 1993, see Sato and Nakashima, 2003). At the end of its life, reproductive swarming occurs in winter or early spring: sexually mature males and females simultaneously swim up to the surface just after high tide at night during spring tides, and die after spawning (Sato and Tsuchiya, 1987; Sato, 1999; Hanafiah et al., 2006). In Fujimae-higata, reproductive swarming of H. diadroma was recorded on 28 February 2002 (Sato and Nakashima, 2003).

During the stay of many migratory shorebirds at Fujimae-higata, i.e., from autumn to the next spring, individuals of H. diadroma grew to almost maximum body size in the late phase of their life cycle, with their weight much larger than that of any other macrobenthic species (Fig. 5). The high percentage occurrence of Hediste chaetae in feces of C. alpina from November to February (Fig. 7) suggests that shorebirds selectively catch large individuals of H. diadroma, though the density of the latter was then relatively low (Fig. 3). After February, however, the percentage occurrence of Hediste chaetae decreased, and the percentage occurrence of smaller food items such as capitellids, spionids, or amphipods increased. This suggests that C. alpina changed its main prey species when the majority of large H. diadroma individuals disappeared after reproduction.

A high percentage occurrence of nereidid body parts in droppings of C. alpina was maintained even in March and April (Fig. 7), when most adults of H. diadroma disappeared from the tidal flats, suggesting that another nereidid, Neanthes succinea, may also be a main prey species during this period. During this time, N. succinea was dominant at many sites (Fig. 6), and it increased in individual body size just before its reproductive swarming from May to July (Imajima, 1996). The low percentage occurrence of nereidid chaetae in feces of C. alpina in May indicates that many N. succinea adults also disappeared after reproduction, and therefore, that nereidid prey for shorebirds may be limited in May, when many shorebirds migrate farther north. The involvement of different nereidid species with different life cycles on the same tidal flats appears to enhance their stability as a major food resource for migratory shorebirds, as implied by Sato and Nakashima (2003).

Larus ridibundus is an omnivorous species. The variety of items in its diet is always large, including invertebrates, plant material, fish, carrion and refuse (Fossi et al., 1995). Our results show that nereidid polychaetes and amphipods comprise the major food component for L. ridibundus at Fujimae-higata. The unusual abundance of nereidid chaetae in some feces of L. ridibundus (Fig. 8b) suggests that this species may catch swarming nereidid adults at the surface of the water. Swarming adults of not only H. diadroma (probable swarming period February to April) and N. succinea (May to July) but also Tylorrhynchus osawai (October to December; Hanafiah et al., 2006), which commonly inhabit the upper reaches of Japanese estuaries and move downstream on the ebb tide during swarming, seem to be available around Fujimae-higata.