CSIRO PUBLISHING
Emu, 2012, 112, 343–349 http://dx.doi.org/10.1071/MU12012
The complex systematics of the Acrocephalus of the Mariana Islands, western Pacific Takema Saitoh A, Alice Cibois B,D, Sayaka Kobayashi A, Eric Pasquet C and Jean-Claude Thibault C A
Yamashina Institute for Ornithology, 115 Konoyama, Abiko, Chiba, 270-1145, Japan. Natural History Museum of Geneva, Department of Mammalogy and Ornithology, CP 6434, CH-1211 Geneva 6, Switzerland. C Muséum National d’Histoire Naturelle, Département Systématique et Evolution, UMR7205 Origine, Structure et Evolution de la Biodiversité, 55 rue Buffon, and Service de Systématique Moléculaire, UMS2700-CNRS, 43 rue Cuvier, F-75005 Paris, France. D Corresponding author. Email:
[email protected] B
Abstract. The Nightingale Reed-Warbler (Acrocephalus luscinius) is known from six islands of the Mariana Archipelago in the Pacific Ocean. A recent phylogeny of the reed-warblers of the Pacific islands suggested however that the species was polyphyletic, the result of at least three independent colonisations. We present here a complete phylogeny of the Mariana reed-warblers that includes two populations, from Alamagan and Aguiguan, not yet studied using molecular techniques. Both of these populations belong to the Pacific Acrocephalus radiation, with birds from Alamagan closely related to the Saipan population, and those from Aguiguan having unresolved relationships within the Micronesian clade. These results suggest that the Mariana Islands experienced multiple colonisations by reed-warblers. We use a combination of molecular phylogeny and biometry of museum specimens to propose a new species-level taxonomy for Acrocephalus of the Marianas. These results have conservation implications for the two remaining populations, on Alamagan and Saipan, which probably belong to the same taxon, Acrocephalus hiwae (Nightingale Reed-Warbler). Received 15 February 2012, accepted 25 June 2012, published online 19 September 2012
Introduction The reed-warblers (Acrocephalus) comprise more than 35 species distributed in Eurasia, Africa, Australasia and Oceania. In the Pacific Ocean, they are found from Australia and Micronesia, including the Mariana Islands, to the north-western Hawaiian Islands and eastern Polynesia (Kennerley and Pearson 2010). Located in northern Micronesia, the Mariana Archipelago (16370 000 N, 145370 000 E) comprises an arc of 15 islands: 10 younger volcanic islands, some of which are still active, in the north and five older islands with more complex geology, including uplifted coral limestone, in the south (Fig. 1). The islands are from 1 million to 43 million years old (Gillespie and Clague 2009). Their sizes vary from volcanoes just emerging above the sea with areas of a few square kilometres to the largest island of Guam (541 km2). Reed-warblers are known from six islands in the Marianas, with museum specimens for populations from five islands – Pagan, Alamagan, Saipan, Aguiguan and Guam – but reed-warblers from the sixth island, Tinian, are known only from subfossil remains (Steadman 1999). The reed-warblers on Pagan, Aguiguan, Guam and Tinian are all extinct (see Discussion for details). A recent phylogeny (Cibois et al. 2011) of the reed-warblers of the Pacific islands hypothesised independent colonisations of Journal compilation BirdLife Australia 2012
Guam, Pagan and Saipan, whose populations had traditionally been considered conspecific based on morphological characters (Yamashina 1942; Baker 1951). According to the molecular phylogeny, the nominate form from Guam (traditionally A. luscinius luscinius (Quoy and Gaimard, 1830); Yamashina 1942; Watson et al. 1986; for spelling of specific name see David and Gosselin 2002) is not part of the Pacific radiation but belongs to a clade that groups the Pacific taxa with the Clamorous Reed-Warbler (A. stentoreus), the Oriental Reed-Warbler (A. orientalis) and the Great Reed-Warbler (A. arundinaceus), with no clear resolution among them. The reed-warblers from Saipan (formerly A. luscinius hiwae (Yamashina, 1942)) are basal in one of the two main clades of Pacific reed-warblers, and the birds from Pagan (formerly A. luscinius yamashinae (Takatsukasa, 1931)) belong to the other, which includes birds from Nauru, the Line Islands and the southern Marquesas. Thus, the Mariana Islands may have played a key role in the diversification of the reed-warblers across the Pacific Ocean with both ancient and recent lineages from different sources. However, a complete picture of the biogeography of reed-warblers in the Marianas requires consideration of the remaining populations not yet studied using molecular techniques: those on Alamagan, classified under the nominate subspecies luscinius (Baker 1951; www.publish.csiro.au/journals/emu
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Fig. 1. Map of the Mariana Archipelago and illustration of the bills of the Acrocephalus of the islands.
Watson et al. 1986) or hiwae (Yamashina 1942); and those on Aguiguan, placed in the subspecies nijoi (Yamashina 1942). The Yamashina Institute for Ornithology (YIO), Chiba, Japan, holds the only specimens from these localities, collected in the 1930s and 1940s. Our goal is to present a complete phylogeny of the five populations of Acrocephalus in the Mariana Islands for which specimens are available, using mitochondrial (mtDNA) sequence data. Combined with the biometry of specimens from the YIO, the Muséum National d’Histoire Naturelle, Paris, France (MNHN), the National Museum of Natural History, Washington, DC, USA (NMNH), and the American Museum of Natural History, New York, USA (AMNH), we used the molecular results to propose new species limits among the reed-warblers of the Mariana Islands. Material and methods We examined two specimens from Alamagan (YIO27840 female, YIO27841 male; both collected 1931), and two specimens from Aguiguan (YIO27844 female, YIO27843 male; both collected 1940). T. Saitoh extracted and sequenced DNA at the YIO. Samples of toe-pad (0.5–1.0 mm2 of skin) were washed with sterile water before extraction, and total genomic DNA was extracted using a commercial kit (DNeasy Tissue Kit, Qiagen, Valencia, CA). Standard extraction protocols were followed except that the time of proteinase digestion was increased from 2 to 12 h, with an additional volume (20 mL) of proteinase K. All tubes and reagents were UV-treated for 30 min before use and extraction tubes containing no sample were used as a control for contamination. We amplified two regions of two mtDNA subunits: ATP synthase subunit 8 (ATP8) and cytochrome b. DNA extracted from museum specimens was degraded, so fragment
sizes for amplification were small (~200 base pairs, bp). Specific primers designed for Pacific Ocean reed-warblers are given by Cibois et al. (2007), and sections of both genes were amplified using overlapping fragments. PCR amplifications were performed in 25 mL reactions with 2 mL of template and 0.4 mM final concentration for primers. The thermocycling procedure started with an initial denaturation of 3 min at 95C, followed by 40 cycles of 30 s at 95C, 40 s at annealing temperature (4650C), and 40 s at 72C for elongation. PCR products were purified using a Qiagen purification kit and sequenced directly (ABI Prism 377 or 3100 automated DNA Sequencer, Life Technologies Ltd, Paisley UK) using the same primers. Contiguous sequences derived from the set of sequence fragments were created using SEQUENCHER (Genecodes, Ann Arbor, MI, USA), ATGC v. 4.0.8 and GENETYX-MAC v.10.1 (GENETYX Corp., Tokyo, Japan). We aligned sequences to Pacific and continental Acrocephalus sequences available in GenBank (Leisler et al. 1997; Helbig and Seibold 1999; Cibois et al. 2011), and subjected the data to Bayesian inference using MRBAYES 3.1.2 (Ronquist and Huelsenbeck 2003), with models selected using MRMODELLTEST 2.3 and the AIC criterion (Nylander 2004). We conducted two independent runs of 1 106 generations, each with four Markov chains. Markov chains were sampled every 100 generations, with a 10% burnin period. We used TRACER 1.4.1 (Rambaut and Drummond 2007) to check that we reached convergence for the posterior distributions of the parameter estimates. Using MRBAYES, we explicitly tested the monophyly of the Mariana Islands reedwarblers with and without the lineage of Guam. We conducted searches using these hypotheses of monophyly to constrain the tree and evaluated the likelihood of these constraint trees with the topology obtained with no constraint with Bayes
Reed-warblers of the Mariana Islands
factors (BF) (Kass and Raftery 1995) computed using the harmonic mean from the sump command in MRBAYES (Brandley et al. 2005). We measured specimens of reed-warblers from the Mariana Islands (A. Cibois at AMNH, MNHN and NMNH; J.-C. Thibault at YIO) and compared them to other Pacific Acrocephalus. The following parameters were measured: wing-length, from the carpal joint to the tip of the flattened wing, bill-length, from tip of the bill to the skull; bill-length, from the tip of the bill to the rear edge of the nostril; bill-depth, at the rear edge of the nostril; billwidth at the rear edge of the nostril; tarsal length, from the notch of the intertarsal joint to the lower edge of the last complete scale; length of the hindclaw, measuring the chord from the tip of the claw to the edge of the skin of nail; and tail-length, from insertion of the central pair of rectrices to the tip of the longest rectrix. We compared only males to control for possible sexual dimorphism in size. Because the dataset was too small to conduct principal components analysis, we presented only simple comparisons between the populations. Results Molecular phylogeny We successfully extracted DNA and obtained mitochondrial sequences for two specimens: 900 bp of cytochrome b and 195 bp of ATP8 for YIO27840 from Alamagan, and 900 bp of cyto-
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chrome b from YIO27843 from Aguiguan. Unfortunately we did not obtain positive results for the two other specimens. New sequences were deposited in GenBank under accession numbers JX073653–655. The alignments were straightforward with no indels, as expected for protein-coding genes. We detected no contamination in the negative controls. We translated the nucleotide sequences to proteins using MEGA (Tamura et al. 2011) and found no stop-codons or indels, suggesting that we did not amplify pseudo-genes (Allende et al. 2001). The ATP8 sequence of YIO27840 (Alamagan) was identical to that of individuals from Saipan, and their cytochrome b sequences differed by 10 bases (1.1% uncorrected sequence divergence). The cytochrome b sequence of YIO27843 (Aguiguan) differed from YIO27840 (Alamagan) by 16 bases (1.7% uncorrected sequence divergence) and on average by 19 bases from individuals from Saipan (2.1% uncorrected sequence divergence). Results from the AIC criterion in MRMODELLTEST supported the GTR+G model for the dataset. The phylogenetic tree obtained using MRBAYES is presented in Fig. 2. Results for the main Pacific Ocean reedwarbler lineages were consistent with the results of previous studies, although the tree was less resolved than the phylogeny presented in Cibois et al. (2011), probably because fewer genes were available. Here we focussed only on the placement of the two additional taxa. Both were placed within the Pacific reed-warbler radiation and belonged with high support to the Micronesian clade (1.0 Bayesian posterior probabilities, PP), which includes
Fig. 2. Phylogenetic tree of the reed-warblers of the Mariana Islands based on cytochrome b and ATP8 sequence data, estimated using Bayesian inference. Asterisks indicate nodes supported by posterior probabilities 0.95.
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birds from Micronesia (Saipan and Pagan in the Mariana Islands, and Nauru and the Caroline Islands) and Polynesia (Line Islands and southern Marquesas; Cibois et al. 2011). The bird from Alamagan was closely related to individuals from Saipan (clade supported with 1.0 PP), whereas the position of the bird from Aguiguan was not resolved among other members of the Micronesian clade. We found significant differences between the constrained trees and the unconstrained tree (Fig. 2). The harmonic mean of the log-likelihood of the unconstrained analysis was –3861.59. When we constrained the monophyly of all Mariana reed-warblers, including Guam, the harmonic mean was –3908.10 and 2 ln BF was 93.02; when we constrained the monophyly of Mariana reed-warblers without Guam, the harmonic mean was –3873.59 and 2 ln BF was 24; and when we constrained the monophyly of the birds from Aguiguan and Pagan, the harmonic mean was –3867.91 and 2 ln BF was 12.64. All 2 ln BF values were >10 and thus were strong evidence against the constrained trees (Kass and Raftery 1995). These results favoured the rejection of previous hypotheses of a monophyletic Acrocephalus group in the Mariana Islands. Comparative morphology Specimens from the Mariana Islands are so similarly coloured with olive-brown upperparts and creamy underparts that populations cannot be distinguished on colour of plumage alone (Kennerley and Pearson 2010). Measurements, however, clearly differentiate the smaller form on Pagan (Table 1, Figs 1, 3). The larger populations differ from each other in their bill proportions. Fig. 4 shows an increase in bill-length and bill-depth from the smallest Pagan birds to the largest individuals from Guam and Saipan, with the birds from Alamagan and Aguiguan intermediate. Birds from Saipan, our largest series with 18 individuals, show wide individual variation. The overlap between populations (except Pagan) suggests that isolated specimens could not be attributed to an individual island based solely on phenotypic characters.
2011). Thus, this archipelago may have played an important role in the diversification of the reed-warblers, with an ancient lineage on Guam and independent more recent colonisations of the other islands. A similar situation has been found for the Mariana Islands white-eyes (Zosterops spp.), with multiple colonisations of the archipelago occurring at different times (Slikas et al. 2000). The position of the individual from Aguiguan is not well resolved within a clade that also includes birds from Pagan. However, the constraint analyses suggested that they are not closely related. Morphologically, the individuals from Aguiguan are larger than all Pagan birds, with slightly deeper bills (Table 1, Figs 3, 4). Birds from Aguiguan are within the range of size and bill-shape of birds from Saipan but genetically they are not closely related, suggesting morphological convergence or small-sample bias. The genetically distinct but morphologically indistinguishable populations of Guam and Saipan must be an example of convergence, similar to that found in the Marquesas (Cibois et al. 2007). Leisler and Schulze-Hagen (2011) suggested that the evolution towards larger bills occurred frequently in insular reed-warblers, possibly in association with the adaptation to the diverse habitats found on islands and to a prey spectrum wider than those of continental birds. The mtDNA tree (Fig. 2) strongly supports the Alamagan bird being sister to those of Saipan. The two are also similar in size (Table 1, Fig. 3). On average, birds from Saipan have a deeper bill than the individual from Alamagan, but the bill-size of the latter lies within the range of variation in the larger Saipan series (Fig. 4), in agreement with Yamashina’s (1942) description of the two populations. Despite our single sample from Alamagan, we are confident that reed-warblers from Alamagan and Saipan share a recent common ancestor and do not warrant even subspecific separation. On the basis of our findings, we suggest recognition of four distinct reed-warbler species in the Mariana Islands: *
*
Discussion *
Phylogeny and systematics This phylogeny shows that the taxa from Aguiguan and Alamagan belong to the same large clade within the Pacific Acrocephalus radiation but are not closely related and do not form a clade with the birds from Pagan (Fig. 2). These results suggest that the Mariana Archipelago was colonised several times by reed-warblers during their spread across the Pacific Ocean (Cibois et al.
*
A. yamashinae (Takatsukasa, 1931) – Pagan Reed-Warbler, Pagan A. hiwae (Yamashina, 1942) – Nightingale Reed-Warbler, Saipan, Alamagan A. nijoi (Yamashina, 1940) – Aguiguan Reed-Warbler, Aguiguan A. luscinius (Quoy and Gaimard, 1830) – Guam Reed-Warbler, Guam
For A. hiwae, the sole surviving species, we suggest retention of the English name Nightingale Reed-Warbler – the only name it as ever had – in order to maintain consistency in the literature and
Table 1. Measurements (mm) of specimens (all males) of Acrocephalus taxa from the Mariana Islands (in AMNH, MNHN, NMNH and YIO) Taxon
Island
yamashinae hiwae hiwae nijoi luscinius
Pagan Alamagan Saipan Aguiguan Guam
Number of individuals
Wing-length
Bill-length (tip to skull)
Bill-length (tip to rear edge of nostril)
Bill-depth
Bill-width
Tarsal length
Length of hindclaw
Tail-length
11 1 21 3 7
78.0 ± 1.5 91.0 87.0 ± 2.5 86.3 ± 4.6 85.6 ± 3.2
21.9 ± 1.9 30.2 33.9 ± 2.7 28.0 ± 1.7 37.1 ± 1.8
14.2 ± 0.7 21.5 22.6 ± 1.4 19.8 ± 1.5 25.0 ± 1.1
4.1 ± 0.2 4.5 5.0 ± 0.3 4.3 ± 0.1 5.0 ± 0.3
4.3 ± 0.3 4.8 5.0 ± 0.3 4.7 ± 0.3 4.7 ± 0.4
28.0 ± 1.3 32.3 30.1 ± 1.0 29.4 ± 1.9 29.8 ± 1.2
8.9 ± 0.8 10.6 10.1 ± 0.9 10.2 ± 0.0 9.8 ± 0.2
73.0 ± 5.1 80.0 82.5 ± 4.4 79.7 ± 4.3 85.9 ± 4.2
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45
Aguigan Alamagan
40
Guam
35
Bill-length
Emu
Pagan
30
Saipan
25 20 15 10 70
75
80
85
90
95
Wing-length Fig. 3. Bill-length (from tip to skull) v. wing-length (mm) for male specimens of Acrocephalus from the Mariana Islands (see Table 1).
6.0
Aguigan Alamagan
Bill-depth
5.5
Guam Pagan
5.0
Saipan
4.5 4.0 3.5 3.0 15
20
25
30
35
40
45
Bill-length Fig. 4. Bill-depth v. bill-length (from tip to skull) (mm) for male specimens of Acrocephalus from the Mariana Islands (see Table 1).
to avoid nomenclatural confusion, and because a single-island name would be inappropriate. Extinctions in the Mariana Islands The four endemic reed-warblers on Pagan, Tinian, Aguiguan and Guam, representing at least three distinct taxa, are all extinct. Here, we review how these extinctions may have occurred. Little is known of the former distribution and abundance of the Pagan Reed-Warbler. Marche collected 10 specimens in 1887 (Oustalet 1895; seven specimens are in the MNHN) and Orii collected nine in 1931 for the YIO. Reed-warblers were last observed in wetlands on Pagan in the 1960s and searches in the 1980s and 1990s failed to find any (Reichel et al. 1992). Possible causes of extinction include destruction of wetlands for agriculture and cattle grazing, and recent volcanic eruptions. Reed-warblers were unknown in historical times on Tinian but lived there prehistorically (Steadman 1999). Subfossil remains do not allow determination of the species, which could be a subpopulation of either A. hiwae or A. nijoi, or a species endemic to Tinian. For now the remains can be classified as A. cf. hiwae/nijoi. Nijo first collected reed-warblers on Aguiguan in 1940, and sent five specimens to the YIO (Yamashina 1940). Surveys undertaken in the 1980s suggested that the remaining population was extremely small, with fewer than 15 individuals (Reichel
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et al. 1992). Craig and Chandran (1992) found only two singing males, and surveys in 2000 and 2002 found none, so this population is almost certainly extinct (Cruz et al. 2000a; Esselstyn et al. 2003). Craig and Chandran (1992) suggested that the last individuals seen on Aguiguan might have been colonists from Saipan, but our genetic results indicate little if any recent gene flow between the two islands, which are 35 km apart, with Tinian, where no reed-warblers have been seen in historic times, in between. Also, the population of reed-warblers on Saipan is declining (see below) and unlikely to produce emigrants. Thus the birds seen in 1992 on Aguiguan probably represented the last of their species. Aguiguan (7 km2) has no wetlands and reed-warblers lived in forest. Destruction of habitat for agriculture before World War II and later by feral goats probably caused the decline of reed-warblers (Reichel et al. 1992). Reed-warblers were first collected on Guam during Dumont D’Urville’s Antarctic Expedition in May 1828 (Dumont D’Urville 1842). Specimens in the MNHN, NMNH, and AMNH indicate that Marche visited the island in 1887, Owston in 1895, Seale in 1900, and Baker in 1945. The last sighting was in 1969 and searches in the 1970s and 1980s failed to find any (Pratt et al. 1979; Savidge 1987; Reichel et al. 1992). The Guam ReedWarbler was historically rare and found almost exclusively in wetlands, a restricted habitat on the island (Baker 1951). Progressive drainage of the largest wetland (Pratt et al. 1979) and frequent fires in reed beds, the preferred habitat of the birds (Baker 1951) contributed to their decline. The Brown Tree Snake (Boiga irregularis), a predator of birds that became abundant in the late 1960s and early 1970s, may have delivered the coup de grâce (Savidge 1987). Conservation concerns for the surviving Acrocephalus of the Mariana Islands The Nightingale Reed-Warbler (A. hiwae) inhabits Alamagan and Saipan, which are 279 km apart. Reed-warblers are unknown on the four islands between Alamagan and Saipan (Fig. 1): Guguan, Sarigan, Anatahan and Farallon de Medinilla (Cruz et al. 2000b; Lusk et al. 2000; Kessler 2011). Historically, habitats have been altered on these islands by the introduction of mammals on Sarigan and Anatahan (Kessler 2011), bombing exercises on Farallon de Medinilla (Lusk et al. 2000), and volcanic eruptions on Anatahan and Guguan (Trusdell et al. 2005; Siebert et al. 2010), so known distributions may be relictual. Despite its recent volcanic activities, Guguan still has a fairly well preserved native forest and several native Mariana landbirds are still common there (Cruz et al. 2000b). The population on uninhabited Alamagan (200–300 individuals) has remained fairly stable over the past 10 years in the absence of major disrupting elements (A. Marshall, unpubl. data). The vegetation on Saipan was highly modified after World War II and most of the remaining forest consists of non-native vegetation (Falanruw et al. 1989), notably Tangantangan (Leucaena leucophala), which was aerially seeded to prevent erosion (Fosberg 1960). Traditionally known to nest in wetlands, the Nightingale Reed-Warbler on Saipan apparently adopted this non-native vegetation and in recent surveys densities were higher in secondary vegetation than in native forests (Cruz and Williams
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2003). A significant decline, however, was observed between 1982 (estimated population of 6658 individuals, with a high density of 58 birds km–2) and 2007 (2742 individuals, 22 birds km–2) (Camp et al. 2009). Factors for this decline include destruction of habitats for development and predation by rats (Camp et al. 2009). In addition, the occurrence of the Brown Tree Snake on Saipan, with several sightings since 1986 suggesting the possibility of an incipient population, may constitute another threat for native landbirds (Rodda and Savidge 2007). Conservation plans for the Nightingale Reed-Warbler include the protection of natural habitats on Saipan, control of feral ungulates and predators, and translocations to predator-free islands (USFWS 1998). Acknowledgements Joel Cracraft and Paul Sweet (American Museum of Natural History, New York), Helen James, Gary Graves and Christopher Milensky (National Museum of Natural History, Washington, DC), and Takeshi Yamasaki (Yamashina Institute for Ornithology, Chiba) provided access to the collections in their charge. Florence Marteau (Muséum d’Histoire Naturelle de la ville de Genève, MHNG) provided assistance with the figures. H. Douglas Pratt and an anonymous reviewer provided helpful comments on the manuscript. We obtained financial support from the Collection Study Grant from the Frank M. Chapman Memorial Fund (AMNH), and from the French Agence Nationale de la Recherche (ANR) via the Biodiversity Research Grant BIONEOCAL (Principal Investigator: Philippe Grandcolas, MNHN). All are gratefully acknowledged.
References Allende, L. M., Rubio, I., Ruíz-del-Valle, V., Guillén, J., Martínez-Laso, J., Lowy, E., Varela, P., Zamora, J., and Arnaiz-Villena, A. (2001). The Old World sparrows (genus Passer): phylogeography and their relative abundance of nuclear mtDNA pseudogenes. Journal of Molecular Evolution 53, 144–154. Baker, R. H. (1951). The Avifauna of Micronesia. Its Origin, Evolution, and Distribution. University of Kansas Publication Museum of Natural History 3. University of Kansas, Lawrence, KS. Brandley, M. C., Schmitz, A., and Reeder, T. W. (2005). Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Systematic Biology 54, 373–390. doi:10.1080/ 10635150590946808 Camp, R. J., Pratt, T. K., Marshall, P., Amidon, F., and Williams, L. L. (2009). Recent status and trends of the land bird avifauna on Saipan, Mariana Islands, with emphasis on the endangered Nightingale Reed-Warbler Acrocephalus luscinia. Bird Conservation International 19, 323–337. doi:10.1017/S0959270909008417 Cibois, A., Thibault, J.-C., and Pasquet, E. (2007). Uniform phenotype conceals double colonization by reed-warblers of a remote Pacific archipelago. Journal of Biogeography 34, 1150–1166. doi:10.1111/j.13652699.2007.01703.x Cibois, A., Beadell, J. S., Graves, G. R., Pasquet, E., Slikas, B., Sonsthagen, S., Thibault, J.-C., and Fleischer, R. C. (2011). Charting the course of reed-warblers across the Pacific islands. Journal of Biogeography 38, 1963–1975. doi:10.1111/j.1365-2699.2011.02542.x Craig, R. J., and Chandran, R. (1992). Wildlife species recorded during the Aguiguan Expedition: 20–25 May, 1992. In ‘Proceedings of the First Marianas Research Symposium’, Saipan, Northern Mariana Islands. (Ed. R. J. Craig) pp. 1–7. (CNMI Division of Fish and Wildlife: Saipan.) Cruz, J., and Williams, L. L. (2003). Baseline avian and vegetation surveys: Saipan Upland Mitigation Bank 1999–2003. Technical Report Number 13, CNMI Division of Fish and Wildlife, Saipan.
T. Saitoh et al.
Cruz, J., Arriola, N., Johnson, N., and Beauprez, G. (2000a). Wildlife and vegetation surveys Aguiguan 2000. Technical Report Number 2, CNMI Division of Fish and Wildlife, Saipan. Cruz, J., Arriola, N., Johnson, N., and Beauprez, G. (2000b). Wildlife and vegetation surveys Guguan 2000. Technical Report Number 3, CNMI Division of Fish and Wildlife, Saipan. David, N., and Gosselin, M. (2002). Gender agreement of avian names. Bulletin of the British Ornithologists’ Club 122, 14–49. Dumont D’Urville, J. (1842). ‘Voyage au Pôle Sud et dans l’Océanie sur les Corvettes l’Astrolabe et la Zélée. Histoire du Voyage. Tome 2.’ (Gide: Paris.) Esselstyn, J., Cruz, J. B., Williams, L. L., and Hawley, N. (2003). Wildlife and vegetation surveys Aguiguan 2002. Technical Report Number 9, CNMI Division of Fish and Wildlife, Saipan. Falanruw, M., Cole, T., and Alan, A. (1989). Vegetation surveys of Rota, Tinian, and Saipan, Commonwealth of the Northern Mariana Islands. Resource Bulletin PSW-27, USDA Forest Service, Pacific Southwest Forest and Range Experiment Station, Berkeley, CA. Fosberg, F. R. (1960). The vegetation of Micronesia. Bulletin of the American Museum of Natural History 119, 54–76. Gillespie, R. G., and Clague, D. A. (2009). ‘Encyclopedia of Islands.’ (University of California Press: Berkeley, CA.) Helbig, A. J., and Seibold, I. (1999). Molecular phylogeny of PalearcticAfrican Acrocephalus and Hippolais warblers (Aves:Sylviidae). Molecular Phylogenetics and Evolution 11, 246–260. doi:10.1006/mpev. 1998.0571 Kass, R. E., and Raftery, A. E. (1995). Bayes factors. Journal of the American Statistical Association 90, 773–795. Kennerley, P. R., and Pearson, D. (2010). ‘Reed and Bush Warblers.’ (Christopher Helm: London.) Kessler, C. C. (2011). Invasive species removal and ecosystem recovery in the Mariana Islands. Challenges and outcomes on Sarigan and Anatahan. In ‘Island Invasives: Eradication and Management’. (Eds C. R. Veitch, M. N. Clout and D. R. Towns.) pp. 320–324. (IUCN: Gland, Switzerland.) Leisler, B., and Schulze-Hagen, K. (2011). ‘The Reed Warblers: Diversity in a Uniform Bird Family’. (KNNV Publishing: Zeist, Netherlands.) Leisler, B., Heidrich, P., Schulze-Hagen, K., and Wink, M. (1997). Taxonomy and phylogeny of reed warblers (genus Acrocephalus) based on mtDNA sequences and morphology. Journal fur Ornithologie 138, 469–496. doi:10.1007/BF01651381 Lusk, M. R., Bruner, P., and Kessler, C. (2000). The avifauna of Farallon de Medinilla, Mariana Islands. Journal of Field Ornithology 71, 22–33. Nylander, J. A. A. (2004). ‘MrModeltest v2.’ (Evolutionary Biology Center, Uppsala University: Uppsala, Sweden.) Oustalet, M. E. (1895). Les mammifères et les oiseaux des Iles Mariannes. Nouvelles archives du Muséum d’histoire naturelle – Serie 3 7, 141–228. Pratt, H. D., Bruner, P. L., and Berrett, D. G. (1979). America’s unknown avifauna: the birds of the Mariana Islands. North American Birds 33, 227–235. Rambaut, A., and Drummond, A. J. (2007). ‘Tracer v1.4.’ Available at http:// beast.bio.ed.ac.uk/Tracer [verified 24 August 2012]. Reichel, J. D., Wiles, G. J., and Glass, P. O. (1992). Island extinctions: the case of the endangered Nightingale Reed-Warbler. Wilson Bulletin 104, 44–54. Rodda, G. H., and Savidge, J. A. (2007). Biology and impacts of Pacific island invasive species. 2. Boiga irregularis, the Brown Tree Snake (Reptilia : Colubridae). Pacific Science 61, 307–324. doi:10.2984/1534-6188 (2007)61[307:BAIOPI]2.0.CO;2 Ronquist, F., and Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 1572–1574. doi:10.1093/bioinformatics/btg180 Savidge, J. A. (1987). Extinction of an island forest avifauna by introduced snake. Ecology 68, 660–668. doi:10.2307/1938471 Siebert, L., Simkin, T., and Kimberly, P. (2010). ‘Volcanoes of the World.’ (University of California Press: Berkeley, CA.)
Reed-warblers of the Mariana Islands
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Slikas, B., Jones, I. B., Derrickson, S. R., and Fleischer, R. C. (2000). Phylogenetic relationships of Micronesian white-eyes based on mitochondrial sequence data. Auk 117, 355–365. doi:10.1642/0004-8038 (2000)117[0355:PROMWE]2.0.CO;2 Steadman, D. W. (1999). The prehistory of vertebrates, especially birds, on Tinian, Aguiguan, and Rota, Northern Mariana Islands. Micronesica 31, 319–345. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739. doi:10.1093/ molbev/msr121 Trusdell, F. A., Moore, R. B., Sako, M., White, R. A., Koyanagi, S. K., Chong, R., and Camacho, J. T. (2005). The 2003 eruption of Anatahan volcano, Commonwealth of the Northern Mariana Islands: chronology, volcanology, and deformation. Journal of Volcanology and Geothermal Research 146, 184–207. doi:10.1016/j.jvolgeores.2004.12.010
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USFWS (1998). Recovery Plan for the Nightingale Reed-Warbler (Acrocephalus luscinia). US Fish and Wildlife Service, Portland, OR. Watson, G. E., Traylor, M. A. Jr, and Mayr, E. (1986). Family Sylviidae. In ‘A Check-list of Birds of the World: A Continuation of the Work of James L. Peters’. (Eds E. Mayr and G. W. Cottrell.) pp. 3–294. (Museum of Comparative Zoology: Cambridge, MA.) Yamashina, Y. (1940). Some additions to the ‘List of the Birds of Micronesia’. Tori 10, 673–679. Yamashina, Y. (1942). A new subspecies of Conopoderas luscinia from the Mariana islands. Bulletin of the Biogeographical Society of Japan 12, 81–83.
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