Ornithol Sci 9: 135–140 (2010)

ORIGINAL ARTICLE Habitat selection among nesting, foraging, and singing sites of the Gray-cheeked morrisonia in northeastern Taiwan

Pei-Yin LEE1,2, Lih-Jih WANG1, Huang-Che HSU3, Lien-Siang CHOU3 and Chao-Chieh CHEN4,#

1 School of Forestry and Resource Conservation, National Taiwan University, 1, Sec. 4, Roosevelt Rd., Taipei 10617, Taiwan 2 Hsinchu Forest District Office, Forestry Bureau, 2, Chungshan Rd., Hsinchu 30046, Taiwan 3 Institute of Ecology and Evolutionary Biology, National Taiwan University, 1, Sec. 4, Roosevelt Rd., Taipei 10617, Taiwan 4 Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, 100, Shihchuan 1st Rd., Kaohsiung 80742, Taiwan

Abstract This study compared microhabitat characteristics among nesting, forag- ORNITHOLOGICAL ing, and singing sites of the Gray-cheeked Fulvetta Alcippe morrisonia in the Fushan SCIENCE Experimental Forest, northeastern Taiwan. Habitat variables, including height above © The Ornithological Society ground, vegetation level, vegetation density at locations where these three types of be- of Japan 2010 havior occurred, and structure, height and diameter at breast height (dbh) of the plant used were recorded from March to July of 2002. The Gray-cheeked Fulvetta predomi- nantly nested in bushes and among herbs (86.7%), but usually foraged and sang in trees (70.8% and 78.3%, respectively). Consequently, significant differences were found in the structure of plants and vegetation level used among nesting, foraging, and singing behavior. Gray-cheeked built their nests at an average height of 1.05 m; however, they foraged around 3.75 m and sang at 5.30 m above ground. On the other hand, nests were situated within the most concealed area, with an average vegetation density of 74%, significantly greater than those of the foraging and singing sites (45%, 38%, respectively). The differential use of microhabitat among these three types of behavior strongly exhibits the divergent adaptation of different behaviors to a ’s environment. This is the first report on habitat selection of various behaviors of the Gray-cheeked Fulvetta, and will contribute to our understanding of the ’ dominant role in most lowland forests in Taiwan.

Key words Behavior, Forest bird, Fushan Experimental Forest, Microhabitat, Timaliidae

Habitat use of forest is usually studied at the the breeding season (Steele 1993). community level (Robinson & Holmes 1982; Martin Each type of behavior has its function and is often 1998), and each member species often occupies a carried out in a particular habitat to fulfill that pur- particular ecological niche in the habitat (MacArthur pose (Martin 1993; Badyaev & Leaf 1997). For ex- 1958; Krebs 2009). However, at the species level, dif- ample, nest building is for the laying of eggs and pro- ferent microhabitats are exploited when birds conduct viding the young with safe places to grow (Braden different types of behavior. For example, male Great 1999; Gibson & Moehrenschlager 2008), singing for Tits Parus major sing and forage at different height signaling its sounds to the receiver (Kroodsma 1996; levels within their territory (Hunter 1980), and Black- Doutrelant et al. 1999), and foraging for finding food throated Blue Warblers Dendroica caerulescens use for themselves or their conspecifics (Remsen & very different habitat for nesting and foraging during Robinson 1990; Thiele et al. 2008). Consequently, suitable habitats that can meet the requirements of (Received 10 January 2010; Accepted 11 September 2010) each type of behavior will differ (Cody 1985; Sergio # Corresponding author, E-mail: [email protected] et al. 2003), and each behavior appears to be associ-

135 P.-Y. LEE et al. ated with a particular set of microhabitats (Steele Fushan Experimental Forest is a humid, subtropi- 1993). For example, male Varied Thrushes Ixoreus cal forest, the canopy of which is dominated by trees naevia use song posts with low foliage density and of the Lauraceae and Fagaceae families. Especially close to the top of large conifers, whereas they forage prevalent are: Castanopsis carlesii, Machilus thun- predominantly on the ground (Beck & George 2000). bergii, Engelhardtia roxburghiana, Meliosma squim- The Gray-cheeked Fulvetta Alcippe morrisonia, a ulata, and Litsea acuminate. Plants of the Myrsi- babbler (Timaliidae), occurs mainly in subtropical naceae (e.g. Maesa tenera), Melastomataceae (e.g. forests from Myanmar to Taiwan (Robson 2000; Zou Melastoma candidum), and Rubiaceae (Lasianthus et al. 2007). The Gray-cheeked Fulvetta is the most fordii) families are common in the understory. Epi- dominant forest bird species in Taiwan’s lowland phytes such as Asplenium antiquum, Pseudodrynaria forests (Yen 1990; Chou et al. 1998), and can be coronans, Aeschynanthus acuminatus, and Hoya found up to 2800 m above sea level in montane carnosa are also very common in Fushan, possibly forests (Zhai 1977; Yen 1990). Many aspects of the due to the forest’s high humidity. A detailed descrip- Gray-cheeked Fulvetta’s ecology and behavior have tion of the study site can be found in King and Hsia been studied in detail, including: diet (Chou et al. (1997). The average canopy height is about 15 m, and 1998; Chen & Chou 1999, 2008), reproductive be- is relatively low compared with other areas in Tai- havior (Lin 1996; Kuoh 2000), flocking behavior wan. Lin et al. (1999) considered that typhoons and (Chen & Hsieh 2002), and molecular phylogeny (Pas- the northeasterly winds may be responsible for the re- quet et al. 2006; Zou 2007). Concerning habitat use, pression of canopy height at Fushan. Lin (1996) considered that pairs of Gray-cheeked Fieldwork, conducted from dawn to dusk from Fulvettas do not occupy clear breeding territories, March to July 2002, consisted of nest searching, and given that two nests were found within five meters of observations of foraging and singing. Most foraging each other. Chen and Chou (2008) showed that the data were collected during the morning hours, be- Gray-cheeked Fulvetta is a generalized frugivore that tween 0600 and 1000, with some additional data col- consumes a high proportion of fruit in its diet and lected from two hours before dusk. Singing, however, prefers to take fruit from bushes especially during the was recorded almost always during the morning. non-breeding season. Hsu (2003) reported that nests Birds were observed with binoculars from a system are built at an average height of 1.40 m and that nest of five trails, totaling about 15 km in length, which ra- site characteristics do not differ between successful diate out from the administrative center of the forest and failed nests. Despite the body of knowledge and run in different directions through three major about the Gray-cheeked Fulvetta, rather little is parts of the study site: botanical garden, administra- known about its habitat selection. tion area, and natural forests. When a Gray-cheeked In this study, we investigated the habitat character- Fulvetta was detected, the observer followed it istics of locations used as nesting, foraging, and closely with binoculars until a nest was found or for- singing sites by the Gray-cheeked Fulvetta at Fushan aging or singing behavior could clearly be observed. Experimental Forest in the breeding season of 2002. Then the habitat characteristics of that location, in- cluding vegetation density, vegetation level, and METHODS height above ground were recorded. In addition, the height, structure, and diameter at breast height (dbh) This study was conducted in the Fushan Experi- of the plants were noted. Vegetation density, modified mental Forest (24°34N, 121°34E), a research site of from Remsen and Robinson (1990), was estimated as the Taiwan Forestry Research Institute, Ilan County, the percentage of a 1-m sphere centered on the loca- northeastern Taiwan. The study area was located at an tion, occupied by foliage. The vegetation density was elevation of 600–800 m above sea level. Fushan’s an- estimated at intervals of 10%. We divided the vegeta- nual average temperature is 18.2°C. Summers, from tion into two levels: canopy and understory, roughly June to August, are characterized by heavy rains, fre- divided at a height of four meters depending on the quently coupled with Typhoons. In addition, there are location. We recorded average canopy height of a many rainy days in winter too owing to the northeast- 100 m2 circle centered at the location; then we calcu- erly winds. As a result, the yearly precipitation is up lated a relative vertical position by dividing the height to 4,900 mm, and the average number of rainy days is of the bird which had performed the behavior by the as high as 220 days per year (Lin et al. 1999). average canopy height. All height measurements

136 Habitat selection of Gray-cheeked Fulvettas were estimated to the nearest meter, and dbh was esti- mated to the nearest centimeter. Plants were desig- nated into different categories defined by their struc- ture such as tree, bush, herb (grass, fern), vine, and epiphyte. Chi-square tests (SAS Institute 1999) were per- formed to determine if there was any association be- tween plant structure or vegetation levels used and the three types of behavior. Here, we grouped the structure of plants into trees and non-trees in the chi- square test. The category of non-trees included bushes, herbs, vines, and epiphytes. The analysis of Fig. 1. Percentages of different plant structures (trees vs. variance (ANOVA) with Tukey’s test (SAS Institute non-trees) used by the Gray-cheeked Fulvetta as nesting, 1999) was performed for each numerical variable to singing, and foraging sites in the Fushan Experimental Forest, northeastern Taiwan. determine if the three types of behavior took place in different microhabitats. The significance level was set at 0.05 for all statistical tests, and all values reported below are meanSE.

RESULTS Fifteen Gray-cheeked Fulvetta nests were found from mid March to mid June in 2002. Two of them were built in sapling trees, and 13 in non-trees (in- cluding bushes and herbs). However, the Gray- cheeked Fulvetta foraged and sang mainly in trees (70.8%, N 147 and 78.3%, N 60, respectively). A Fig. 2. Percentages of vegetation levels used by the Gray- significant association was found with plant structure cheeked Fulvetta as nesting, singing, and foraging sites in the (trees vs. non-trees) used and behavior type (nesting, Fushan Experimental Forest, northeastern Taiwan. foraging, and singing) (c 224.35, df2, P0.0001; Fig. 1). vegetation level used and nesting, foraging, and All nests were found in the understory level (Fig. singing behavior (c 219.45, df2, P0.0001; Fig. 2), whereas singing was more frequently recorded in 2). the canopy than in the understory. Foraging took The Gray-cheeked Fulvetta showed significant dif- place to similar extents in both the canopy and the ference (ANOVA, P0.001) in means of all five of understory levels. Accordingly, the Gray-cheeked the numerical habitat variables measured at nesting, Fulvetta exhibited a significant association between foraging and singing sites (Table 1). In further multi-

Table 1. Comparison of habitat characteristics (meanSE) among nesting, foraging, and singing sites of the Gray-cheeked Fulvetta in the Fushan Experimental Forest, northeastern Taiwan.

Habitat variables Nesting N Foraging N Singing N F a P

Vegetation density (%)b 74.05.3B 15 44.801.60A 147 37.602.70A 58 21.00 0.0001 Relative vertical position 0.150.02B 14 0.340.02A 147 0.430.03A 59 10.10 0.0001 Height (m) 1.050.11B 15 3.750.22A 147 5.300.52A 60 13.55 0.0001 Plant height (m) 1.900.17B 13 7.110.33A 140 8.150.63A 57 12.80 0.0001 Plant dbh (cm) 4.100.80B 13 18.101.10A 129 19.401.90A 55 8.24 0.001 a ANOVA. b Different letters indicate a significant difference between means in Tukey’s test. The letter “A,” appearing after the means of “Foraging” and “Singing,” indicates that the two means are not significantly different from each other. However, both means are significantly different from the mean of “Nesting,” which is labeled with a “B.”

137 P.-Y. LEE et al. ple comparison tests, mean measurements of nesting & Steidl 2000). Hsu (2003) found that 63.6% of nest sites were significantly different from both foraging losses for the Gray-cheeked Fulvetta are due to pre- and singing sites in all variables. Nests were situated dation at Fushan Experimental Forest. Dense foliage at an average height of 1.05 m; however, the Gray- around the nest can reduce the probability of preda- cheeked Fulvetta foraged at around 3.75 m and sang tion (Martin 1992, 1993), and many studies have at an average height of 5.30 m. The highest singing showed that nest sites usually have significant higher location recorded was at 18 m. Nests were built foliage density than randomly selected sites (e.g. within the most concealed locations, with an average Martin 1993; Martin and Roper 1988; Sergio et al. vegetation density of 74%. Foraging usually took 2003). The vegetation density around nest sites of the place at locations with a medium (45%) vegetation Gray-cheeked Fulvetta is much higher than that at density, whereas singing occurred in areas of rela- foraging and singing sites. This result is largely con- tively sparser vegetation, with an average density of sistent with the statement that forest birds usually 38%. Plant height and dbh combined were in accor- build their nests within concealed locations in order dance with the structure of plants used. For example, to protect their eggs and nestlings from rain, wind, Gray-cheeked Fulvettas nested in plants averaging and predators (Martin 1993; Braden 1999). 1.90 m in height and 4.1 cm in dbh. These measure- In contrast, when a bird sings, it will prefer using a ments imply that bushes are the main nesting sites more open perch in order to transmit its sounds out- and this is in agreement with results obtained from wards to reach its receivers (Morton 1975). The the plant structure used by the Gray-cheeked Ful- Gray-cheeked Fulvetta sang at a height of about vetta. In contrast, Gray-cheeked Fulvetta foraged in 5–6 m, which is within the lower part of the canopy. trees averaging 7.11 m in height and with a dbh of This height level is right above the dense understory 18.1 cm, and sang in trees averaging 8.15 m in height and below the tree crowns and is in a relatively and 19.4 cm in dbh. Apparently, the Gray-cheeked sparser horizontal zone within the forest (Wang Fulvetta both foraged and sang in trees, but they used 2002). Since sounds transmitted in forests are more relatively larger trees for singing from than for forag- affected by reverberation off leaves and branches ing. Compared with the average canopy height, the (Richards & Wiley 1980; Waser & Brown 1986), the relative vertical position for nest sites (0.15) is signif- Gray-cheeked Fulvetta may strategically use this icantly lower than those for foraging (0.34) and sparser level to reduce dissipation of its vocalizations. singing (0.43). In addition, the subcanopy level is an excellent arena for males to make themselves visible to potential DISCUSSION mates and opponent males. However, singing within this sparser area may also attract the attention of A strong association was found between habitat predators. Nevertheless, Krams (2001) reasoned that use and different behavior type in the Gray-cheeked a better view of the surroundings might compensate Fulvetta. This implies that they exploit different habi- for the risk of predation by allowing early detection tats for nesting, foraging, and singing. In particular, of an approaching predator. We found that Gray- fulvetta nests were found mainly in bushes and herbs cheeked Fulvettas frequently changed perches while of the understory level, foraging was observed in singing. In addition to broadcasting its vocalizations, trees of both the understory and canopy levels, and such erratic behavior may serve as a way to enhance singing occurred in trees mainly at the canopy level. predator detection. The divergent use of habitat for the different types of The Gray-cheeked Fulvetta used a much wider behavior strongly indicates the differential adaptation vegetation level in foraging than in nesting and of behavior to its surrounding environment in the singing. Accordingly, the habitat characteristics of its Gray-cheeked Fulvetta. This is in agreement with the foraging sites are broader and fell in between those of evolutionary point of view that each type of behavior its nesting and singing sites. That fact that habitat will be carried out within a particular microhabitat measurements of foraging sites are much closer to that best fulfills the function of that behavior (Martin those of singing sites instead of nesting sites may re- 1993; Badyaev & Leaf 1997). sult from singing sometimes taking place in the Nest predation alone accounts for about 80% of course of foraging. We considered this might be an nest losses on average across a wide range of habitats energy saving strategy since it would be a great chal- and geographic regions (Martin 1992, 1993; Powell lenge for birds to accomplish all different types of be-

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