Ornithol Sci 7: 123–134 (2008)
ORIGINAL ARTICLE Food-niche differentiation in sympatric species of kingfishers, the Common Kingfisher Alcedo atthis and the Greater Pied Kingfisher Ceryle lugubris
Satoe KASAHARA# and Kazuhiro KATOH
Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1051 Hata-machi, Hanamigawa-ku, Chiba 262–0018, Japan
Abstract The Common Kingfisher Alcedo atthis and the Greater Pied Kingfisher ORNITHOLOGICAL Ceryle lugubris breed sympatrically along the Chikuma River in central Japan. These SCIENCE kingfisher species differ in body size, with the latter being much larger than the for- © The Ornithological Society mer. To understand the potential mechanisms that might play a role in food-niche dif- of Japan 2008 ferentiation between these two species, we studied their foraging ecology in the breeding seasons of 2005 and 2006. Specifically, we compared the foraging habitat, foraging behavior, and food delivered to nestlings between the two kingfishers. We video-recorded the food delivered to nestlings during the day, and our results indi- cated that these species differed in their foraging ecology in several respects: (1) Common Kingfishers caught prey at sites where the water flow was calm, while Greater Pied Kingfishers hunted at sites where the water flowed rapidly; (2) Greater Pied Kingfishers dove from a higher position and caught fish in deeper water than Common Kingfishers; and (3) Common Kingfishers preferred smaller fish than Greater Pied Kingfishers. Overall, Common Kingfishers used a wider variety of for- aging sites and food types than Greater Pied Kingfishers in the study area. As inter- specific territorially and aggressive interactions between the two species were rarely observed, the food-niche differentiation between the two species was not likely the outcome of competitive exclusion. We conclude that the realized food-niches of the two kingfisher species reflect their respective body sizes.
Key words Alcedo atthis, Ceryle lugubris, Diet, Foraging ecology, Kingfisher
Species with similar resource requirements are 2004; Martínes 2004). Food resource partitioning often allopatric, occupying separate geographical based on prey type or prey size and segregation of the areas that abut or overlap over part of the range foraging area are important mechanisms that reduce (Newton 1998). In the area adjoining or overlapping the possibility of competition and/or allow related their distribution, niche differentiation or resource bird species to coexist in the same area (Lack 1971; partitioning is necessary to avoid competition and to Cody 1985; Newton 1998; Garcia & Arroyo 2005). allow their stable coexistence (Newton 1998). Re- Many studies have focused on congeneric species lated sympatric species often show segregation of the (e.g. Moskát & Fuisz 2002; Dale & Manceau 2003; habitat, such as nesting or feeding sites (Lack 1971; Garcia & Arroyo 2005). According to the concept of Cody 1985; Newton 1998). The mechanisms allow- the guild, i.e., a group of species that exploit a class ing coexistence of related species have long intrigued of environmental resources in a similar way (Root ecologists and have been studied in a wide range of 1967), food-niche differentiation could play an im- bird species, including songbirds (Moskát & Fuisz portant role in the coexistence of heterogeneric 2002; Dale & Manceau 2003), raptors (Garcia & Ar- species with similar niche requirements (e.g. Libois royo 2005), and waterfowl (Libois & Laudelout & Laudelout 2004; Martínes 2004). To understand the mechanisms underlying such co- (Received 12 July 2008; Accepted 5 October 2008) existence, it is important to study how sympatric # Corresponding author, E-mail: [email protected] species share food resources and foraging habitats
123 S. KASAHARA and K. KATOH during the breeding season, which is associated with habitats (Nishimura 1979; Jimbo et al. 1986a, b). The a demand for greater amounts and larger food items overlapping distribution of the two kingfisher species (e.g. Libois & Laudelout 2004) for the brood than could make them potential resource competitors. consumed by the parents. As larger birds need more With the exception of Nishimura (1979), who com- and/or larger prey to obtain energy to support the in- pared nest site preferences between the two king- creased body size (Reyer et al. 1988; Marti et al. fisher species in an area of southwest Kyoto Prefec- 1993), many studies have shown that food size could ture, central Japan, no other studies have compared be one aspect of differentiation among congeneric or food or foraging sites or examined interspecific terri- heterogeneric species that differ in body size (e.g. Li- torial interactions between these two species within a bois & Laudelout 2004; Garcia & Arroyo 2005). As single area. The present study was performed to iden- food size, food type, and foraging site selection are tify differences in foraging sites and prey, and to un- mutually interrelated (Kelly 1996; Libois & Laude- derstand the potential mechanisms that may play a lout 2004; Sullivan et al. 2006), it is important to role in food-niche differentiation between these two identify these factors in the same research to evaluate species. We compared foraging habitats, foraging be- food-niche overlap or partitioning between species. havior, and food sources for nestlings between the However, few studies have included detailed compar- species in a sympatric breeding area. isons between species with regard to habitat selection and foraging behavior with data on diet (e.g. Chap- MATERIALS AND METHODS man & Rosenberg 1991). The Common Kingfisher (Alcedo atthis) and the 1) Study Area Greater Pied Kingfisher (Ceryle lugubris) are resi- We carried out field surveys between late March dents of Honshu, the main island of Japan. Both and late July in both 2005 and 2006, coinciding with species regularly nest on riverbanks and are primarily the breeding season of both Common and Greater piscivorous. Although the two kingfisher species be- Pied Kingfishers (Satoe Kasahara unpublished data). long to different families, they have a similar bill The study site was located along the middle course of form and foraging ecology in that they perch on the Chikuma River, Nagano Prefecture, central Japan. branches or rocks and hover in the sky before diving The upstream and downstream ends of the study site into the water. The average body size and weight were Sakaki (36°25 N, 138°11 E, 405 m elevation) range of the Common Kingfisher are 16 cm and and Nagano (36°32 N, 138°6 E, 360 m elevation), re- 34–44 g, respectively, while those of the Greater Pied spectively. The length of the river channel was about Kingfisher are 41–43 cm and 230–280 g, respectively 25 km (Fig. 1). (Fry et al. 1992). The Greater Pied Kingfisher is now In this area, the major land use along the river is considered a threatened species in 32 of the 47 pre- agricultural, and the river partly flows through urban- fectures in Japan because its population size and dis- ized areas. As the riverbed, riverbanks, and river tribution have decreased markedly due to large-scale channels have been artificially altered only slightly, habitat loss (e.g. Red Data Books of Nagasaki Prefec- the natural features and topography are still largely ture 2001; Aichi Prefecture 2002; Kyoto Prefecture intact in and along the river. The flow rate in the 2002; and Nagano Prefecture 2004). Common King- study area fluctuated widely. Although the flow rate fishers hold near-threatened status in 12 prefectures during irregular floods that occur once every one or in Japan (e.g. Red Data Books of Osaka Prefecture two decades is up to 30-fold greater than the normal 2000 and Tottori Prefecture 2001) for similar reasons. flow rate (Okino 2006), no such flooding occurred However, Common Kingfisher populations have re- during the study period. Sandbars are formed within covered and their distribution has recently expanded and along the main channel. The sandbars have no or into anthropogenic habitats, such as ponds in urban only sparse vegetation cover, consisting of willow parks (Norinomiya et al. 1991; Yano 1994). (Salix spp.) or reed (Phragmites spp. and Miscanthus The habitats of the two kingfishers in Japan are sacchariflorus) communities. Major vegetation types often separated: Greater Pied Kingfishers live along within the riparian area, other than sandbars, are rivers at higher altitudes, while Common Kingfishers Phragmites japonica grasslands and Salix shrubs in usually inhabit areas at middle or lower altitudes the lower areas (i.e., closer to the river) and Robinia (Nakamura & Nakamura 1995). On the other hand, pseudoacacia woods in higher areas. Some of the they coexist in some regions and have similar nesting higher land has been converted to agricultural fields
124 Food-niches of two sympatric kingfishers
Fig. 1. Study area. Branching lines represent the watercourse of the Chikuma River, and the shaded area shows the water area. Solid rectangles and the broken line show the study areas for Common Kingfishers and Greater Pied Kingfishers, respectively. or playgrounds. Small channels and ponds form 2) Field Observations within reed grasslands in the lower riparian area. We searched for nests of the two kingfisher species Most ponds are not connected to the main channel in three study areas at the beginning of the study pe- except during floods. riod each year. The locations of all nests were We established two study sites for the Common recorded on a map drawn based on aerial photos at a Kingfisher surveys. The first, located in Sakaki, scale of 1 : 12,500. We observed each nest every 7 to measured 400 3500 m, while the second was an area 10 days with 10 binoculars and a 20–60 telescope of 500 1000 m in Nagano (Fig. 1). For the surveys to determine if the pair was rearing nestlings. The of Greater Pied Kingfishers, we used the two Com- day on which a parent began to carry food to the nest mon Kingfisher survey study sites as well as the en- was regarded as the beginning of the brooding period. tire riparian area between the two sites, because the Yano (1994) reported that the size of food items home range of Greater Pied Kingfishers spans 3–7 km brought by Common Kingfishers to their brood along a watercourse (Ishibe 1997) and is much larger changed during the nestling period; minnows that than that of Common Kingfishers, which is ca. 1 km were shorter than the bill length of the parents were along a river (Boag 1982). Both kingfisher species brought in the early nestling period (up to 7 days were observed at all three study sites. after hatching), with larger fish brought later. The Great Pied Kingfisher shows a similar pattern (Jimbo
125 S. KASAHARA and K. KATOH
1997). To identify food items by more accurate channel in protected areas), or paddy field within recording, we considered the beginning of the late areas protected by a levee. (7) Flow conditions: riffle nestling stage to be 12 and 17 days after hatching for (surface always choppy), shallows (bubbles almost the Common Kingfisher and the Greater Pied King- inconspicuous), deep (surface quite smooth, although fisher, respectively, based on the time at which the fast current), shoal (near shore), or standing (water food size changed, because the average lengths of the did not flow; e.g. temporal pools). nestling period are 23 and 32–36 days, respectively Differences in habitat use between the two king- (Nakamura & Nakamura 1995). fisher species could be derived from interspecific To determine the foraging points of individuals competition. We recorded any interactions between from each nest, we captured 18 Common Kingfishers the two species during tracking of focal individuals to between late April and late May in 2005 and 2006 examine the importance of interspecific competition using mist nets near the foraging sites. Birds were in determining habitat use of the two species. captured soon after we detected a brood and away from any nests to avoid severely disturbing breeding 3) Foods Delivered to Nestlings activities. We marked each captured individual with We chose seven Common Kingfisher nests and five two colored plastic bands (A. C. Hughes Ltd.) in a Greater Pied Kingfisher nests to record foods deliv- unique combination. Further, to facilitate identifica- ered to the nestlings. Recording was carried out dur- tion of individuals, less than one-third of the bill of ing the day, for about 12–14 h per day. The average each bird was painted with water-resistant nail polish, recording periods per nest were 69 21.5 h for Com- which came off after 1–2 months (H. Uchida personal mon Kingfishers and 88.6 55.6 h for Greater Pied communication). We did not capture and mark Kingfishers. Nesting birds use regular perches around Greater Pied Kingfishers because they are secretive the nest when bringing food to the nestlings (Kuroda birds (Fry et al. 1992) and their nests were scattered 1991; Yano 1994); therefore, we created a perch near widely along the river. We estimated the nests of each nest for nesting individuals. We expected that focal individuals based on their flight direction and birds would perch at the site with food in their bills territorial behavior. Foraging by eight individuals was before bringing it to the nest, which facilitated identi- observed. In 2005, we observed both species only in fication of food items supplied to nestlings (Naka- Sakaki. In 2006, we observed the Common Kingfish- mura & Kashiwagi 1989). A wooden stake was ers in two study areas (i.e., Sakaki and Nagano), and placed in the ground near each nest, and the height of the Greater Pied Kingfishers throughout the whole the stake was adjusted to the height of the nest. To study area. The average total observation time per record the food items brought into the nest, an 8-mm pair was 63.3 12.4 h (mean SD, N 9) for Com- videotape recorder (Sony CCD-TRV126) was set mon Kingfishers and 58.0 23.7 h (N 4) for Greater about 2–4 m from the nest with suitable camouflage Pied Kingfishers. and waterproof coverings. We recorded the following attributes for each for- To compare the sizes of food items between the aging trial (i.e., diving) for marked or traced individ- two species at the same nestling stage, recordings of uals. (1) Height of individual (perching or hovering) food items were conducted at the late nestling stage above the water surface at the beginning of the trial; (12 and 17 days after hatching) for each nest between height was estimated visually. (2) Type of foraging late May and late July. We identified prey animals at behavior: diving from a perch or diving after hover- least to the family level. Most fish were identified to ing. (3) Type of perch: rock, woody debris, tree or species based on Kawanabe et al. (1989). In some shrub, aquatic plant (mainly reeds), or artificial mate- difficult cases, we sought the advice of researchers at rial (mainly concrete tetrapod units or bridge piers). the Fisheries Experiment Station in Suwa, Japan. We (4) Results of the trial: success or failure. (5) Water estimated the length of food items from the exposed depth at the diving point: measured with a ruler at the culmen length when the bird held the food. Exposed visually determined point after the foraging individ- culmen lengths of 3.75 and 6.65 cm were used for the ual had flown away. (6) Type of foraging site: main Common Kingfisher and the Greater Pied Kingfisher, channel, small channel (connected to the main chan- respectively, based on Kiyosu (1978). Shrimp were nel, less than 2 m wide), temporal pool (isolated from excluded from the food size analysis for two reasons. the main channel except during flood periods), water First, their bodies were always bent, which makes it channel within areas protected by a levee (hereafter, difficult to reliably estimate body length. Second,
126 Food-niches of two sympatric kingfishers shrimp accounted for less than 1% of the total num- and nine Greater Pied Kingfisher nests in the study ber of prey. Recordings were conducted for both areas. The distance from one nest to the nearest con- species at all study sites in both years. specific nest was 436 184 m (N 14) for Common Kingfishers and 2887 1676 m (N 9) for Greater 4) Statistical Analyses Pied Kingfishers. Inter-nest distance could not be cal- We examined whether the two kingfishers used dif- culated for nests located in peripheral areas. The dis- ferent types of foraging site by c 2 test. We also used tance between heterospecific nests was 181 89 m the c 2 test to determine whether they preferred the (N 5). We observed nests of both species sometimes same flow conditions. Both tests used foraging trial constructed on the same riverbank. The ranges of data and treated each trial as one sample. Foraging conspecific foraging sites scarcely overlapped, while success was compared among flow conditions for those of heterospecific foraging sites showed a large each species. The heights from which focal individu- degree of overlap in Sakaki (Fig. 2). Here, we do not als dove were compared between the species and be- show the hunting sites of the two kingfishers in tween the types of foraging behavior. We also com- Nagano because only one pair of Common Kingfish- pared water depths of foraging sites in the same man- ers bred there. Only one incidence of interspecific ag- ner. The Mann-Whitney U-test was used for these gression was seen, whereas intraspecific aggression analyses because our data deviated from a normal was observed 902 times among Common Kingfishers distribution. We compared food length using Welch’s and four times among Greater Pied Kingfishers dur- t-test because the data were normally distributed but ing the two breeding seasons. had uneven variance. All measured values are shown We observed 18 Common Kingfishers and eight as means SD. The analyses described above were Greater Pied Kingfishers attending nine and four conducted using SPSS ver. 14 (SPSS Inc. 2005). nests, respectively. Common Kingfishers mainly used We performed correspondence analysis (CA; Hill the main channel, small channels, and temporal pools 1973) to describe the differences in delivered food for foraging (Table 1). They also caught prey in the composition between the two kingfishers. Although channels in protected areas and paddy fields. In con- this method is known as a species composition analy- trast, Greater Pied Kingfishers hunted mostly in the sis tool in ecology, it was originally developed for de- main channel and marginally used small channels or composing contingency tables of counts into a small temporal pools (Table 1). The frequency of use be- number of summary variables (Quinn & Keough tween the two species was different among the three 2002). It is a type of multivariate analysis for display- common foraging site types (c 2 148.8, P 0.0001). ing the rows and columns (here, nest and food items) There were no differences in foraging success of of a two-way contingency table as points in a low-di- Common Kingfishers among the three main foraging mensional space (shown as joint plots). This analysis sites (c 2 3.7, P 0.16). Common Kingfishers mainly can produce a comprehensive view of the table, hunted in shoals, followed by shallow water and which is useful for understanding the structure of standing water (Table 2). Greater Pied Kingfishers data in the table. The positions of the row and column points indicate the associations between rows and Table 1. Proportions of foraging sites used by Common columns; the distance between row points and that Kingfishers and Greater Pied Kingfishers on the Chikuma between column points indicate resemblance between River, Japan. The numbers of foraging trials for 18 Common rows and between columns, respectively. We re- Kingfishers and eight Greater Pied Kingfishers are shown in garded each nest as a sample and each food item cat- parentheses. MC, SC, TP, CPA, and PFPA indicate main chan- nel, small channel, temporal pool, channels in protected areas, egory (see Table 5) as a variable. Data are given as and paddy field within areas protected by a levee, respectively. the numbers of food items brought to the nest. Food item categories that were brought to more than one Utilization of foraging site (%) nest were included in the analysis. Calculations were performed using PC-ORD ver. 4.3 (McCune & Mef- MC SC TP CPA PFPA ford 1999). Common Kingfisher 49.0 30.2 18.8 0.7 1.4 (N 586) RESULTS Greater Pied Kingfisher 97.6 0.5 1.9 0 0 1) Foraging Site and Behavior (N 209) We found a total of 16 Common Kingfisher nests
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Fig. 2. Home ranges of Common Kingfishers (solid lines) and Greater Pied Kingfishers (dashed lines) in Sakaki in (a) 2005 and (b) 2006. Open squares, crosses, open circles, shaded triangles, and open rhombuses indicate for- aging points for Common Kingfishers and closed circles indicate foraging sites for Greater Pied Kingfishers. The same symbols are not used for the same individual in different years. Gray lines and the shaded area indicate the levee and the water area, respectively.
Table 2. Proportion of flow conditions used by Common Kingfishers and Greater Pied Kingfishers in the Chikuma River, Japan.
Utilization of flow condition (%)
Standing Shoal Shallows Deep Riffle
Common Kingfisher 20.3 42.8 33.8 1.9 1.2 (N 586) Greater Pied Kingfisher 1.9 40.2 24.4 13.9 19.6 (N 209) hunted in shoals, followed by shallow water, riffles, (Table 3). Foraging success from a perch was 77.6% and deep water (Table 2). The two species hunted in for Common Kingfishers and 70.7% for Greater Pied each of the flow conditions at significantly different Kingfishers, whereas foraging success for diving after frequencies (c 2 169.0, P 0.0001). We found no dif- hovering was 60.5 and 50.0%, respectively. Greater ferences in foraging success of Common Kingfishers Pied Kingfishers tended to dive from higher positions among the three most commonly used flow condi- than Common Kingfishers, regardless of their forag- tions (shoal, shallow, and standing water; c 2 3.9, ing behavior (Mann-Whitney U-test; diving from P 0.14). There were no differences in the foraging perch site, Z 17.73, P 0.0001; diving after hover- success of Greater Pied Kingfishers among the four ing, Z 3.03, P 0.0001; Fig. 3a). Common King- most commonly used flow conditions (shoal, shallow, fishers used mainly aquatic plants (e.g. reeds), while riffle, and deep water; c 2 1.8, P 0.62). Greater Pied Kingfishers used mainly trees or shrubs Diving from perch sites was observed more fre- as perch sites (Table 4). Greater Pied Kingfishers oc- quently than diving after hovering in both species casionally dove into the water from about 10 m using
128 Food-niches of two sympatric kingfishers
Table 3. Comparison of the proportion of hunting tech- niques of the two kingfishers on the Chikuma River, Japan.
Hunting techniques (%)
Perch Hovering Fly
Common Kingfisher 79.3 20.3 3.4 (N 586) Greater Pied Kingfisher 90.0 8.6 1.4 (N 209) a bridge pier as a perch site. Greater Pied Kingfishers caught food at significantly deeper sites than Com- mon Kingfishers regardless of their foraging behavior (Mann-Whitney U-test; diving from perch site, Z 16.22, P 0.0001; diving following hovering, Z 6.44, P 0.0001; Fig. 3b).
2) Food Composition The compositions of food delivered to nestlings by the two species are summarized in Table 5. Common Kingfishers delivered at least 18 species of fish, tad- poles (Anura spp.), crayfish (Astacidae), shrimp (De- capoda), and dragonfly larvae (Odonata spp.). Pale Chub (Zacco platypus) was the dominant food species, followed by Japanese Dace (Tribolodon hakonensis) and loaches (Misgurnus spp.; Table 5). In contrast, Greater Pied Kingfishers caught only fish, consisting of ten species. Japanese Dace was predom- inant, followed by Pale Chub (Table 5). The two kingfishers caught six fish species in common (see Table 5). With the exception of Barbel Steed (Hemibarbus barbus), which was brought to the nests of both species at a rate of less than 1%, the ratio of each species delivered to nestlings was significantly different (c 2 253.3, P 0.0001). Figure 4 shows a joint plot of the first two axes of the correspondence analysis, which explained 25.1% Fig. 3. (a) Height above the water surface of individual and 16.1% of the variance of the original matrix perches immediately before diving and (b) water depth at the (nests food items), respectively. Food item composi- diving point for 18 Common Kingfishers and eight Greater tions of the two kingfishers were similar among the Pied Kingfishers when diving from perch sites (open squares) and after hovering (shaded squares) at the Chikuma River, nests of the same species, but were different between Japan. The number of foraging trials is shown in parentheses. the two species. The results of the correspondence Error bars indicate the 75th and 25th percentiles, the line in- analysis also indicated that Ayu (Plecoglossus al- side each box indicates the median, and lines represent the tivelis altivelis) was brought selectively to the nests maxima and minima (excluding outliers). Open circles repre- of Greater Pied Kingfisher, because Ayu was plotted sent outliers between one-half and three times the interquartile close to the cluster of the plots that represent the range, and stars represent outliers more than three times the in- nests of Greater Pied Kingfishers in the joint plot. On terquartile range. the other hand, Pale Chub, Amur Minnow (Phoxinus logowski steindachneri), Stone Moroko (Pseudorasb-
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Table 4. Proportion of perch sites for diving used by the two kingfishers along the Chikuma River, Japan. The numbers of perches for 18 Common Kingfishers and eight Greater Pied Kingfishers are shown in parentheses.
Utilization of perch sites (%)
Rocks Woody debris Aquatic plants Trees or shrubs Artificial material
Common Kingfisher 13.3 13.8 44.5 24.9 3.4 (N 465) Greater Pied Kingfisher 6.4 17.6 0 64.4 11.7 (N 188)
Table 5. Delivered food composition indicated as percentages of the number of each food item to the total number of food items brought to nestlings along the Chikuma River, Japan. Data are from seven Common Kingfisher nests and five Greater Pied Kingfisher nests.
Common Greater Pied English names Scientific names Kingfisher Kingfisher
Fish Plecoglossidae Ayu Plecoglossus altivelis altivelis 0.4 5.9 Cyprinidae Pale Chub Zacco platypus 56.7 25.0 Japanese Dace Tribolodon hakonensis 15.4 63.5 Amur Minnow Phoxinus logowski steindachneri 1.0 0 Field Gudgeon Gnathopogon elongatus elongatus 0.1 0 Stone Moroko Pseudorasbora parva 3.2 0 Smooth Oriental Photinia Pseudogobio esocinus esocinus 0.1 0 Barbel Steed Hemibarbus barbus 0.4 0.3 Common Carp Cyprinus carpio 0 0.3 Crucian Carp Carassius spp. 0.4 2.3 Bitterling Acheilognathinae spp. 0.1 0 Cobitidae Loach Misgurnus spp. 10.1 0.7 Amblycipitidae Reddish Bullhead Liobagrus reini 0 0.7 Siluridae Japanese common catfish Silurus asotus 0 0.3 Centrarchidae Largemouth Bass Micropterus salmoides 0.1 0 Bluegill Lepomis macrochirus 0.1 0 Gobiidae Freshwater Goby Rhinogobius spp. 1.0 0 Goby Gobiidae spp. 0 0.3 Unknown fish 8.9 0.6 Other taxon Tadpole 0.3 0 Crayfish 0.1 0 Shrimp 0.3 0 Larva of dragonfly 0.1 0 Sample size 683 304
130 Food-niches of two sympatric kingfishers
Fig. 4. Joint plot of the first two axes from correspondence analysis (variance is shown in parentheses). Closed and open squares indicate nests of Common Kingfisher and Greater Pied Kingfisher, respectively. Shaded circles indicate food item categories. Nests are located according to delivered food composition: closely located nests on the plot mean that food composition delivered to the nests was similar. Food item categories are also plotted. Dis- tance between a food item and a nest indicates the strength of the relationship between the item and the nest: a shorter distance indicates that the food item was brought to the nest more frequently. Twelve nests of the two king- fishers and ten food item categories that were recorded in two or more nests were included in the analysis. ora parva), loaches, and Freshwater Goby (Rhinogo- mon Kingfisher (Boag 1982). Libois and Laudelout bius spp.) were mainly brought to the nests of Com- (2004) suggested a similar trend of foraging site se- mon Kingfishers. lection by comparing food types between kingfisher The estimated length of fish delivered by Common species with different body sizes. Bonnington et al. Kingfishers was 7.5 1.5 cm (2.5–12.0 cm, N 620) (2008) documented Cerylidae species favoring forag- and that by Greater Pied Kingfishers was 12.8 2.5 ing areas with higher perch sites and deeper rivers, cm (7.0–21.0 cm, N 304); thus, Greater Pied King- while Alcedinidae species preferred lower perch sites fishers delivered significantly larger food items near shallow water. Our results are consistent with (Welch’s t-test, t 33.89, P 0.0001). these studies. Common Kingfishers could not dive into deep DISCUSSION water because of their small body size. The weight of the Common Kingfisher is about one-seventh that of 1) Interspecific Differences in Foraging Habitat the Greater Pied Kingfisher. The Greater Pied King- Our results indicated that the Common Kingfisher fisher preyed on large fishes that tend to inhabit deep foraged frequently in small channels and temporal waters (e.g. Japanese Dace and Ayu; Sakai 1989; pools, and sometimes hunted away from the river, Nishida 1989). Although an individual with larger i.e., within areas protected by a levee (Table 1). This body size can dive to deeper water (e.g. Kato et al. species tended to hunt in sites where the water flow 1999; Cook et al. 2007), diving from a higher perch was calm (Table 2) and preferred shallow water sites is advantageous to gain potential energy or momen- (Fig. 3b). In contrast, the Greater Pied Kingfisher, tum to dive into deep and/or rapid water. Greater Pied which is much larger than the Common Kingfisher, Kingfishers dove from a higher position when they hunted mostly in the main channel (Table 1). This used perch sites than when hovering, while Common species hunted at sites where the water flowed rapidly Kingfishers showed the inverse trend (Fig. 3). These (Table 2), and it chose deeper waters (Fig. 3b). Our results may explain why Greater Pied Kingfishers results agreed with previous descriptions of the Com- hovered less frequently than Common Kingfishers.
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During the breeding season, interspecific aggres- availability of each food type (Campos et al. 2000), sion includes defense of food resources and the nest reflecting the abundance of each prey species or their site (Orians & Willson 1964), and territory owners accessibility in the habitat (Wanink & Goudswaard exclude intruders from the defended area by aggres- 1994). In this study, both Pale Chub and Japanese sive behaviors. However, we have little evidence to Dace were dominant species (Denda et al. 2002). support interspecific competitive exclusion between Smaller fish, which were caught more frequently by these two kingfisher species. First, the distance be- Common Kingfishers than by Greater Pied Kingfish- tween heterospecific nests was shorter than that be- ers, inhabit temporal waters and small channels with tween conspecific nests, indicating that interspecific calm or standing water (Halyk & Balon 1983). How- competition around nest sites is not severe. It is un- ever, such waters likely provide insufficient food re- likely that the two species compete for nest sites. sources for Greater Pied Kingfishers because these Second, the overlapping distribution of foraging sites birds require larger fish for the brood compared to of the two species indicated that interspecific compe- those consumed by the parents (Libois & Laudelout tition for foraging sites does not occur, whereas in- 2004). Differences in foraging habitats between the traspecific competition influenced the location of for- two kingfisher species reflected the distributions of aging sites. Thus, interspecific territoriality (Orians & their prey. Willson 1964) between two kingfisher species was Reynolds and Hinge (1996) and Campos et al. less certain. (2000) showed that prey size of Common Kingfishers Interspecific agonistic interactions were rarely ob- is relatively constant, although they exploit a diverse served during the two breeding seasons. If this low number of fish species. Kelly (1996) and Ishibe interspecific interaction was derived from competi- (1997) reported a similar pattern in Cerylidae species. tion, spatial partitioning of foraging sites between In this study, the two kingfisher species caught fish of species would have occurred (e.g. Gerstell & Bednarz a relatively fixed size, regardless of fish species, indi- 1999). However, this was not detected in the present cating that the fish species they catch is determined study. Niche segregation with lack of interspecific by size. In the present study, the maximum prey size territoriality or aggression was also reported previ- of Common Kingfishers was 12.0 cm, which corre- ously (Dale & Manceau 2003). Therefore, it appears sponds to three-quarters of the body length of adults that the interspecific difference in foraging sites be- and was less than the average food length of Greater tween the two kingfishers is not the outcome of com- Pied Kingfishers. Maximum prey size of Greater Pied petitive exclusion, but may be a result of differences Kingfishers was 21.0 cm, which was about half the in their foraging site preferences. body length of the adults and exceeded the body length of adult Common Kingfishers. These observa- 2) Interspecific Differences in Food Resources tions suggest that the prey brought to Greater Pied Foraging site selection of a species is often closely Kingfisher nestlings are too large for adult Common related to food type and size (Kelly 1996; Libois & Kingfishers to handle. Therefore, the size of fish Laudelout 2004; Sullivan et al. 2006). The two king- caught by the two kingfisher species seemed to reflect fisher species examined in the present study preyed their respective body size. on different types of food, and the sizes of the food Many studies have shown food-niche segregation items differed between the two species. between species based on prey size derived from Common Kingfishers preferred the Pale Chub, body size differences (e.g. Libois & Laudelout 2004; which lives in shallow areas (5–15 cm deep) of rivers Martínes 2004; Garcia & Arroyo 2005). In this study, near the shore (Mori & Nagoshi 1989). Loaches, on we found that prey size partitioning between the two which Common Kingfishers also preyed frequently, kingfisher species leads to differentiation in prey type prefer calm or standing water (Saito 1989; Kimitsuka and microhabitat use in the same area. This segrega- 1989; Kawanabe et al. 1989). On the other hand, the tion of prey size is probably associated with the re- Japanese Dace, which was the fish caught most fre- quirements of each kingfisher species during the quently by Greater Pied Kingfishers, mainly inhabits brooding period. Thus, niche partitioning could re- deep parts of rivers (Sakai 1989). Japanese Dace and duce the possibility of competition and allow coexis- Ayu inhabit the main channels of rivers (Sakai 1989; tence of these two sympatric kingfisher species. Nishida 1989). Previous studies have indicated that the food sources of Alcedinidae vary according to the
132 Food-niches of two sympatric kingfishers
ACKNOWLEDGMENTS Gerstell A & Bednarz JC (1999) Competition and pat- terns of resource use by two sympatric raptors. Con- We thank Hiroshi Nakamura and Hiroshi Uchida for help dor 101: 557–565. with fieldwork, and Maria Kurokawa, Fumio Miyabara, and Halyk LC & Balon EK (1983) Structure and ecological the staff of the Fisheries Experiment Station in Suwa for help production of fish taxocene of a small floodplain sys- with fish identification. We are grateful to Masanobu Hotta for tem. Can J Zool 61: 2446–2464. document acquisition and the Chikuma River Office, Hill MO (1973) Reciprocal averaging: an eigenvector Hokuriku Regional Development Bureau, Ministry of Land method of ordination. J Ecol 61: 237–249. Infrastructure and Transport, for providing aerial photographs. We are also grateful to Keisuke Ueda, Kenya Ukawa, Yuichi Ishibe H (1997) Yamasemi (Greater Pied Kingfisher). Yamaura, and Koji Itoh for their suggestions on an earlier draft In: Higuchi H, Morioka H & Yamagishi S (eds) The of the manuscript. We thank Sadao Imanishi for help with both Encyclopedia of Animals in Japan. Vol. 4: Birds. II. fieldwork and advice on the manuscript. We thank the anony- pp 48–50, 56. Heibonsya, Tokyo (in Japanese). mous referees for their critical comments on this manuscript. Jimbo K (1997) Yamasemi no Kurashi (Life of Greater This study was partially supported by the River Ecology Re- Pied Kingfisher). Bun-ichi Co. Ltd., Tokyo (in Japan- search Group of Japan (Chikuma River Group), the River En- ese). vironment Fund of the Foundation of River Watershed Envi- Jimbo K, Jimbo S & Yamazaki R (1986a) Ecological ronment Management, Japan. Survey of Japanese Pied Kingfisher in Atugi. Nat Hist Rep Kanagawa 7: 15–18 (in Japanese). REFERENCES Jimbo K, Jimbo S & Yamazaki R (1986b) Notes on the Japanese Pied Kingfisher in the Hinata River (3) Its Aichi Prefecture (2002) Red data book Aichi. Aichi Pre- response against other birds. Bull Kanagawa Pref Nat fecture, Nagoya (in Japanese). Conserv Cent 3: 13–18 (in Japanese). Boag D (1982) The kingfisher. Blandford Press, UK. Kato A, Watanuki Y, Shaughnessy P, Maho YL & Naito Bonnington C, Weaver D. & Fanning E (2008) The Y (1999) Intersexual differences in the diving behav- habitat preference of four kingfisher species along a ior of foraging Subantarctic Cormorant (Phalacroco- branch of the Kilombero River, southern Tanzania. rax albiventer) and Japanese Cormorant (P. filamento- Afr J Ecol 46: 424–427. sus). C R Acad Sci Paris Sciences de la via 322: 557– Campos F, Fernández A, Gutiérrez-Corchero F, Martin- 562. Santos F & Santos P (2000) Diet of the Eurasian Kawanabe H, Mizuno N & Hosoya K (1989) The Fresh- kingfisher (Alcedo atthis) in northern Spain. Folia water Fish of Japan. YAMA-KEI Publishers. Co. Zool 49: 115–121. Ltd., Tokyo (in Japanese). Chapman A & Rosenberg KV (1991) Diet of four sym- Kelly JF (1996) Effects of substrate on prey use by patric Amazonian woodcreepers (Dendrocolaptidae). belted kingfishers (Ceryle alcyon): a test of the prey Condor 93: 904–915. abundance—availability assumption. Can J Zool 74: Cody ML (1985) An introduction to habitat selection in 693–697. birds. In: Cody ML (ed.) Habitat selection in birds. Kimitsuka Y (1989) Cobitis biwae. In: Kawanabe H, pp 3–56. Academic Press, San Diego. Mizuno N & Hosoya K (eds) The Freshwater Fish of Cook TR, Cherel Y, Bost C-A & Tremblay Y (2007) Japan. pp 392–393. YAMA-KEI Publishers. Co. Ltd., Chick-rearing Crozet Shags (Phalacrocorax Tokyo (in Japanese). melanogenis) display sex-specific foraging behavior. Kiyosu Y (1978) The Birds of Japan. Kodansya, Tokyo Antarc Sci 19: 55–63. (in Japanese). Dale S & Manceau N (2003) Habitat selection of two Kuroda H (1991) Perch selection of the Pied kingfisher locally sympatric species of Emberiza buntings (E. Ceryle lugubris. Strix 10: 51–61 (in Japanese with citronella and E. hortulana). J Ornithol 144: 58–68. English Summary). Denda M, Yamashita S, Ozawa T & Shimatani Y (2002) Kyoto Prefecture (2001) Red data book of Kyoto prefec- Backwaters and fish community—on environmental ture. Kyoto Prefecture, Kyoto (in Japanese). factors affecting fish community in backwaters. Jpn J Lack D (1971) Ecological Isolation in Birds. Harvard Ecol 52: 287–294 (in Japanese). Univ Press, Cambridge. Fry CH, Fry K & Harris A (1992) Kingfishers, bee- Libois R & Laudelout A (2004) Food niche segregation eaters, and rollers. Princeton Univ Press, Princeton. between the Malachite Kingfisher, Alcedo cristata, Garcia JT & Arroyo BE (2005) Food-niche differentia- and the Pied Kingfisher, Ceryle rudis, at Lake Nok- tion in sympatric Hen Circus cyaneus and Montagu’s oue, Benin. Ostrich 75: 32–38. Harriers Circus pygargus. Ibis 147: 144–154. Marti CD, Steenhof K, Kochert MN & Marks JS (1993)
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