Rapid Change in Song Structure in Introduced Japanese Bush-Warblers (Cettia Diphone) in Hawaii1

Rapid change in song structure in introduced Japanese Bush-warblers (Cettia diphone) in Hawaii1

By Shoji Hamao

Abstract Song birds that have been artificially introduced to isolated areas are fruitful material for investigating the changeability of songs within a limited period of time. I studied the songs of Japanese Bush-warblers, Cettia diphone, which were introduced from Japan to the island of Oahu (Hawain Islands) ca. 80 years ago . The warblers on Oahu sang acoustically simpler songs at lower frequencies than the warblers on Honshu, the main island of Japan. Previous studies found similar tendencies on small peripheral Japanese islands. Morphological characteristics indicated that the warblers on the Hawaiian Islands did not originate from insular subspecies in Japan. Therefore, the acoustic structure of their songs may have changed during their 80 years on Oahu. Possible factors driving this rapid change are relaxed sexual selection and/or the sound transmission properties of the island.

Introduction

The acoustic structure of bird songs evolves under various selection pressures from ecological and social factors (Kroodsma and Miller 1996). Because song structure is a culturally transmitted trait in oscine passerines (Beecher and Brenowitz 2005), it can change rapidly relative to genetic

1Manuscript accepted 9 May 2014. Pacific Science, vol. 69, no. 1 1 July 24, 2014 (Early view) traits (Wilkins et al. 2013). Song birds that have been artificially introduced to isolated areas

(e.g., islands) are fruitful material for investigating the changeability of songs within a limited period of time (Baker and Jenkins 1987). For example, the New Zealand population of chaffinches, Fringilla coelebs, was introduced from England about 100 years ago, and their songs have fewer trills and conclude with a more elaborate structure. This indicates that their songs changed within approximately 100 years, likely due to the sound transmission properties of the dense pine forests in New Zealand (Jenkins and Baker 1984).

The Japanese Bush-warbler, Cettia diphone, was introduced to the island of Oahu

(Hawaiian Islands) from Japan multiple times between 1929 and 1933 (Caum 1933), and it currently inhabits many of the Hawaiian Islands (Pratt et al. 1987, Nelson and Vits 1998). In this study, I examined whether the acoustic structure of songs differs between Oahu and Japan. To assess the origin of the warblers in Hawaii, I also compared their morphology with that of

Japanese Bush-warblers in Japan. Finally, I discuss the possibility of song structure having changed in Hawaii since their introduction and the factors responsible for such changes. I predicted that song structure would differ between the Hawaiian and Japanese populations due to rapid changes in songs in Hawaii during the ca. 80 years since colonization.

Materials and Methods

Field work

I conducted the study in Hawaii and Japan. Four study sites on Oahu were used in Hawaii:

Honolulu Watershed Forest Reserve (21°20'N, 157°50'W), Pupukea Forest Reserve (21°38'N,

158°01'W), Marconi Road (21°42'N, 157°59'W), and Mokuleia Forest Reserve (21°32'N,

158°11'W). At these sites, broad-leaved evergreen forests were the dominant vegetation. The study site in Japan was located at Ranzan (36°01' – 06'N, 139°18' – 20'E), in central Honshu, the

2 largest island of Japan, where deciduous forests and bamboo thickets are the dominant vegetation.

I collected song recordings from 24 males on Oahu during the breeding season (March 19

– 22) in 2010, and from 38 males at Ranzan during the breeding season (May 26 – June 16) in

2003. The songs sung by a male were recorded for at least 5 min. Each recording was sufficient to obtain all song types of the male, as the repertoires of this species were small (2 – 5 song types; Momose 1999), and the males sang very frequently (interval between songs: 14.7 s;

Hamao and Ueda 2000) and tended to avoid repetition of the same song types (Momose 1999). I used a Sony (Tokyo, Japan) PCM-D50 digital recorder equipped with a Sony ECM-G5M directional microphone on Oahu, and a Sony TCD-D7 DAT-recorder with a Sony ECM-G3M directional microphone at Ranzan. To avoid duplicate sampling of the same male, I walked along roads and recorded new birds when I encountered them. I used each route only once. Because male territories were often contiguous, and males sang very frequently, I often heard the songs of two or more males at the same time and therefore could identify individuals. Moreover, 84% of males have a unique song type repertoire, which is useful for individual identification (Hamao

1993). Therefore, I could confirm whether a male was a new bird.

For body measurements, I captured 16 warblers using mist-nets at Ranzan during the breeding seasons (end of April to end of July) between 2002 and 2004. I measured the lengths of the wing (wing unflattened), tail, tarsus, and bill (exposed culmen) to the nearest 0.01 mm using calipers. To obtain measurements of warblers in Hawaii, I used 15 specimens that were preserved in the Bishop Museum, Honolulu. The measurements were made on March 20, 2010, of specimens that had been collected from Oahu (1 male), Molokai (3), Hawaii (4), Maui (4), and

Kauai Islands (3) in 1992 (1 male), 2004 (7) and 2005 (7). The lengths of the wing, tail, and tarsus were measured to the nearest 0.1 mm using dividers, and bill length was measured to the

3 nearest 0.01 mm using calipers. I obtained measurements only from males because capturing females proved difficult and the museum contained few female specimens.

Song analyses

All recorded songs were analyzed using the Avisoft SASLab Pro software (ver. 5.1, Avisoft

Bioacoustics, Berlin, Germany). Sounds were displayed as sound spectrograms. Fast Fourier transform (FFT) lengths of 256 and 1,024 were used to produce plots for temporal and frequency measurements, respectively. The songs of Japanese Bush-warblers consist of an initial constant frequency (CF) and subsequent frequency modulation (FM) portions (Hamao 1993, Momose

1999). The warblers have two basic song types: a type-H song and a type-L song. Type-H songs contain one long whistle in the CF part, whereas type-L songs contain several short whistles

(Hamao 1993, Momose 1999; Figure 1). In Japan, individual males sing two to five different song types that include at least one type-H and one type-L song, respectively (Momose 1999). I recorded the number of song types for each male and quantified five acoustic variables in the FM part of each song type. Maximum and minimum frequencies (Hz) were the highest and lowest frequencies, respectively. I also measured the number of notes, the number of frequency inflections [i.e., the number of changes in the sign of the derivative (slope) of the frequency on the sound spectrogram], and song length (duration; Figure 1a). A note is a discrete song element, and a continuous trace on a spectrogram (Catchpole 1980, Baker 1996).

Statistics

To compare song structure between Oahu and Ranzan, I used generalized linear mixed models

(GLMMs). The maximum and minimum frequencies, and the length of the FM parts were analyzed using a GLMM with an identity link and a Gaussian error distribution. The number of

4 notes and frequency inflections were analyzed using a GLMM with a log link and a Poisson error distribution. I included site (Oahu or Ranzan) as a fixed factor and male identity as a random factor. To compare the number of song types among males, I used a generalized linear model

(GLM) with a log link and a Poisson error distribution. For these analyses, I created separate models for type-H and type-L songs. To test the significance of any effects, I used likelihood ratio tests.

To compare morphological measurements between Hawaii and Ranzan, I used independent samples t-tests. In all analyses, the significance level was set at 0.05, and all analyses were conducted using R software (ver. 3.0.1, R Core Team 2013).

Results

Songs sung by individual males on Oahu and at Ranzan included at least one type-H and one type-L song, respectively (Figure 1, Supplemental Material: Media files S1 and S2). All five FM part acoustic variables differed significantly between songs sung on Oahu and those sung at

Ranzan for both type-H and type-L songs (all P < 0.01). The maximum and minimum frequencies were lower on Oahu than at Ranzan (Figure 2a, b). The length of the FM parts was shorter on Oahu (Figure 2c). Both the numbers of notes and inflections were smaller on Oahu than at Ranzan (Figure 2d, e). Thus, songs on Oahu had a lower frequency and a simpler acoustic

2 structure. The song type repertoire was larger on Oahu than at Ranzan for type-H songs (χ 1 =

2 8.03, P < 0.01), but there was no difference between the sites for type-L songs (χ 1 = 1.51, P =

0.22; Figure 2f).

In the body measurements of male warblers, wing, tail, and bill lengths were shorter in the Hawaiian Islands than at Ranzan, whereas tarsus length was longer in the Hawaiian Islands

(Table 1). The plumage color of males at Ranzan was olive brown or slightly dark brown on the

5 upperparts and dirty white on the underparts. Hawaiian males had similar coloration, but they were slightly more grayish on the upperparts.

Discussion

Japanese Bush-warblers on Oahu sang acoustically simpler songs at a lower frequency than the warblers on Honshu, the main island of Japan (Figure 2). Previous studies using similar analyses showed that the songs of warblers on small peripheral Japanese islands also had a simpler structure compared with the songs sung on Honshu (Izu Islands, Ryukyu Archipelago: Hamao

2013, Ogasawara Islands: Hamao and Ueda 2000). Among these populations, birds on Honshu and the Izu Islands belong to the subspecies cantans, and birds on the Ryukyu and Ogasawara

Islands belong to restricta and diphone, respectively (OSJ 2012).

The Japanese Bush-warbler includes six subspecies (OSJ 2012), but the subspecies or source population of the warblers that were introduced to Hawaii was not recorded. However, the plumage color and morphology of the subspecies provide some information about their identity.

Of the six subspecies, I excluded subspecies riukiuensis and borealis as candidates because the former is thought to be a synonym of other subspecies (sakhalinensis and/or cantans: Kajita et al.

2002, Brazil 2009) and the latter is an accidental visitor to Japan (OSJ 2012). Subspecies diphone differs from the birds in Hawaii in plumage color; it has a rufous-brown forehead and crown, and a yellowish white underpart (Yamashina 1941, Brazil 2009). Also, diphone is much smaller than the warblers in Hawaii (wing length of male diphone: 56.6 – 59.9 mm, n = 5,

Hamao unpubl. data). Subspecies restricta is similar to the warblers in Hawaii in body size (wing length of male restricta: 60.6 – 66.7 mm, n = 36, Hamao unpubl. data). However, the plumage color differs; the forehead, wing, and tail of this subspecies have a strong red-brown tone

(Yamashina 1941, Brazil 2009). Although the plumage colors of older (>50 years) museum

6 specimens are degraded, especially in UV wavelengths (McNett and Marchetti 2005, Armenta et al. 2008), I was able to compare the colors of live birds and museum specimens in this study because the specimens were collected recently (5 – 6 years ago, with one exception of 18 years ago; see Materials and Methods) and because the differences in coloration between subspecies were very clear. Thus, the Japanese Bush-warblers that were introduced to Hawaii appear to belong to the subspecies sakhalinensis and/or cantans. The body size and plumage color of the birds in Hawaii are consistent with those subspecies, although statistical analyses showed that the wing, tail, and bill lengths were shorter, and tarsus length was longer in Hawaii than observed in cantans in Japan (Table 1). These small differences may have been caused by shrinkages of specimens (Winker 1993) or by the morphological changes as reported in Laysan finches,

Telespyza cantans (Conant 1988). DNA analyses will help to identify the origin of the Japanese

Bush-warblers that were introduced to Hawaii, but differences in genetic structure have not been found among populations of cantans and sakhalinensis in analyses using the mitochondrial cyt b region (Kajita 2002) or the CO1 region (Emura et al. 2013).

The songs sung in some insular populations of cantans have an acoustically simpler structure than songs in the mainland population. Songs on Miyake-jima and Nii-jima Islands consist of shorter FM parts and contain notes with fewer inflections than songs on Honshu

(Hamao 2013), which is similar to the tendency observed in the songs on Oahu (Figure 2). These islands are located 150 – 180 km south of Tokyo. Access to these islands would not have been easy at the time when the warblers were introduced to Hawaii (ca. 80 years ago). Japanese Bush- warblers were systematically introduced to Oahu multiple times by the Board of Agriculture and

Forestry and Hui Manu, a group that imported song birds (Caum 1933). It is reasonable to conclude that the warblers on Oahu originated from populations on the mainland of Japan, and

7 that their songs have changed during the past 80 years, although I cannot rule out the possibility that the Hawaiian warblers were brought from small peripheral Japanese islands.

A factor related to the simplified songs on Oahu may be the residency of the birds. In mainland Japan, Japanese Bush-warblers move seasonally and males establish breeding territories every spring (Hamao 1992, Yamashina Institute for Ornithology 2002). Moreover, territorial males are frequently replaced (Hamao 1992). Males are exposed to strong male-male competition. In contrast, competition may be weaker among males on Oahu because they do not migrate and their density is relatively low (S. H., pers. obs.). As complex songs indicate high- quality males (Behr et al. 2006, Cardoso et al. 2012) and are therefore considered advantageous in male–male competition, the simplified songs on Oahu may be the result of relaxed male–male competition. In Japan, insular populations of Japanese Bush-warblers show a small degree of sexual size dimorphism, suggesting that sexual selection is relaxed on the islands (Hamao 2013).

Studies of the territoriality and sexual dimorphism in the Hawaiian population are required.

Song structure is also shaped by the sound transmission properties of the habitat (Jenkins and Baker 1984, Kroodsma 1985). Birds inhabiting forests with dense foliage use pure tone-like, low-frequency sounds that attenuate less in their habitats (Morton 1975, Richard and Wiley

1980). The warblers inhabit broad-leaved evergreen forests on Oahu, but deciduous forests and bamboo thickets on the mainland of Japan. It is possible that the vegetation structure on Oahu affects sound transmission and has driven the change to low-frequency, less modulated songs.

More information is required about vegetation structure and sound transmission in the habitats on Oahu and in Japan.

Characteristics of introduced populations are often restricted because of the small number of colonizing individuals (founder effect). For example, the chaffinches that colonized the

Chatham Islands in about 1900 have a smaller number of syllable types than the source

8 population in New Zealand (Baker and Jenkins 1987). Although the song type repertoire has not been investigated at the population level in Japanese Bush-warblers, individual males on Oahu had a larger number of song types than males in Japan (Figure 2f). It is doubtful that this pattern can be explained by the founder effect.

It is possible that the observed changes were the result of random cultural drift (Baker et al. 2001, Benedict and Bowie 2009). However, I consider this unlikely, as multiple acoustic variables, including shorter duration, fewer notes, and less modulation, indicated a simplified song structure.

Cultural evolution of songs can occur rapidly. The acoustic structure of the songs of white-crowned sparrows, Zonotrichia leucophrys oriantha, changed within 26 years in California

(Harbison et al. 1999). The white-crowned sparrows, Z. l. pugetensis, in Oregon and Washington had six song dialects but showed little genetic differentiation in four microsatellite loci (Soha et al. 2004). Therefore, it is likely that, during the 80 years since colonization, the songs of

Japanese Bush-warblers on Oahu have undergone acoustic changes.

Acknowledgments

I thank Lydia Garetano for allowing me to measure specimens in the Bishop Museum, and Jeff

Foster for providing me a lot of useful information and literatures. I am indebted to Eric

VanderWerf and Hiroshi Uchida for their support during my field work, and two anonymous reviewers for their constructive comments. This study was supported by funds from the

Yamashina Foundation for Wildlife Conservation Research.

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TABLE 1 Differences in body measurements of male Japanese Bush-warblers between the Hawaiian Islands and Ranzan on the Japanese mainland. Means and ranges (mm) are shown for each variable. Numbers in parentheses are the numbers of individuals. Asterisks indicate significant differences detected by t-tests: ** P < 0.01, *** P < 0.001.

Tarsus Wing1 Tail Bill2

Hawaiian Islands 25.8 61.3 62.2 10.9 (15)3 24.7 – 27.9 59.4 – 64.0 55.7 – 67.2 10.1 – 11.4

Ranzan 25.0** 63.3*** 68.0*** 11.6*** (16)4 23.7 – 25.9 59.7 – 65.4 65.4 – 71.8 10.9 – 12.4

1 Wing unflattened.. 2 Exposed culmen. 3 Measurements of tarsus and culmen were obtained from 14 males, because the specimens were damaged. 4 Measurements of tail were obtained from 14 males, because two males were molting their tails.

Pacific Science, vol. 69, no. 1 14 July 24, 2014 (Early view)

Figure 1. Spectrograms of Japanese Bush-warbler songs showing two basic song types and the parameters analyzed. (a) A type-H song and (b) a type-L song from a male on the island of Oahu. The type-H song contains two notes and two inflections in its frequency modulated (FM) portion. See the supplemental material that includes the sounds of these songs.

Figure 2. Differences in song structure and repertoire size in Japanese Bush-warblers between the island of Oahu and Japan: maximum frequency (a), minimum frequency (b), song length (duration; c), number of notes (d), number of inflections (e), and number of song types (f). The acoustic variables (a-e) were obtained in FM portions of songs. Means +- 1SD are shown. White and gray bars indicate type-H and type-L songs, respectively. Horizontal solid and dotted lines indicate significant differences in type-H and -L songs, respectively (** P < 0.01, *** P < 0.001).

Supplementary material associated with this article is available.

S1 (MS1213_spl1.mp3)

A type-H song from a Japanese Bush-warbler on the island of Oahu. This sound corresponds with the song in Figure 1a.

S2 (MS1213_spl2.mp3)

A type-L song from a Japanese Bush-warbler that is the same male in S1. This sound corresponds with the song in Figure 1b.