Breeding biology of the Grey-hooded Parrotbill (Paradoxornis zappeyi) at Wawushan, Sichuan, China.
Abstract: We found nine nests of the Grey-hooded Parrotbill (Paradoxornis zappeyi) during April through July 2003 at Wawushan Natural Reserve, Sichuan, southwestern China. This report is the first description of the nest sites, nests, eggs, and breeding behavior of this parrothill, and the first documentation of nestling growth from hatching until fledging. The nests were constructed mainly of bamboo (Bashania faberi) leaves, fibrous roots, and moss by both male and female. Nests were bowl shaped and in bamboo thickets 81-122 cm above ground, and 17-68 cm below the top of bamboo leaves. Clutch size was 3.1 eggs (n = 8 nests) and eggs were oval, pale blue in color with a mean mass of 1.3 g. Incubation and provisioning of nestlings were by both parents. The nestling period was 13-14 days with a hatching rate of 0.52 and mean reproductive success rate of 0.48 fledglings per nest.
Article Type: Report
Subject: Egg (Biology) (Analysis)
Birds (Breeding)
Birds (Research)
Birds (Eggs and nests)
Birds (Analysis)
Birds (Nestlings)
Birds (Physiological aspects)
Authors: Yingxin, Jiang
Yue-Hua, Sun
Nan, Lu
Zhonglin, Bi
Pub Date: 12/01/2009
Publication: Name: The Wilson Journal of Ornithology Publisher: Wilson Ornithological Society Audience: Academic Format: Magazine/Journal Subject: Biological sciences Copyright: COPYRIGHT 2009 Wilson Ornithological Society ISSN: 1559-4491
Issue: Date: Dec, 2009 Source Volume: 121 Source Issue: 4
Topic: Event Code: 310 Science & research
Geographic: Geographic Scope: China Geographic Code: 9CHIN China
Accession Number: 216267546
Full Text: The Grey-hooded Parrotbill (Paradoxornis zappeyi) is a rare Chinese endemic, one of five threatened members of a 10-species avian suite entirely restricted to the Central Sichuan Mountains Endemic Bird Area (Stattersfield et al. 1998) and listed as vulnerable by the IUCN (2008). Chinese ornithologists have also proposed it be listed as a nationally protected species (Zheng and Wang 1998). The Grey-hooded Parrotbill has a highly restricted range (Emeishan, Wawushan, Luding, Erlangshan, and Ebian mountains of central and western Sichuan, and Weining and Hezhang mountains of northwestern Guizhou) and its natural history is totally unknown (Lei and Lu 2006). Low density and restricted distributions are particularly correlated with species extinction (Manne et al. 1999, Groom et al. 2006), as such species may be at risk from stochastic events (Bonn et al. 2002). Paradoxornis comprises 18 species in China but almost nothing is known of their breeding behavior, except for the Vinous-throated Parrotbill (P. webbianus) (Guo et al. 2006). The objectives of our work were to: (1) find and describe the nests, eggs, and chicks of the Grey-hooded Parrotbill; and (2) describe its breeding behavior.

METHODS

Study Area.--We studied parrotbills at an elevation of ~2,830 m on the plateau of the Wawushan Natural Reserve, an isolated table mountain in Hongya County of Sichuan Province, southwest China (29[degrees] 25'-29[degrees] 34' N, 102[degrees] 49'-103[degrees] 00' E). The area is within the monsoon climatic belt with annual precipitation of 200 cm with most occurring in summer from June through August. The annual mean temperature of this area is 16.8[degrees] C (max = 36.2[degrees] C; min = -3.3[degrees] C). January and July mean temperatures are 6.6 and 25.7[degrees] C, respectively. The plateau is ~9 [km.sup.2] in size and is covered by forest dominated by Emei fir (Abies fabri), mixed with some birch (Betula utilis). Most of the fir are mature and young trees are extremely rare. The undergrowth is dominated by bamboo (Bashania faberi) and a wide variety of Rhododendron species forming low bushes, among them R. ambiguum and R. maculiferum. Bamboo thickets provide important local habitat for several other bird species, in addition to Grey-hooded Parrotbills, defined as "bamboo specialists" (Kratter 1997), including Fulvous Parrotbill (Paradoxornis fulvifrons), Streak-throated Fulvetta (Alcippe cinereiceps), and Spotted Laughingthrush (Garrulax ocellatus).

Field Procedures.--We searched for nests along the trails (~8 km) on the plateau between 26 April and 12 July 2003. We used vocal clues and following parents carrying nest materials or returning to the nest after an incubation break, or with food for nestlings. We monitored nests noting egg dimensions and fresh weights plus, on a daily basis, the mass and linear measurements (beak, wing, tarsus, and tail length) of nestlings. We also netted and measured three adults before egg laying.

RESULTS

Nest and Nest Building Behavior.--We found nine Grey-hooded Parrotbill nests, the first on 30 April (nest completed, and before egg laying), and the last on 26 June (during nestling period) (Table 1). Five were still under construction when found, two had partly incubated eggs, and two had nestlings (Table 1). All nests were in bamboo thickets from 81 to 122 cm above ground, and 17-68 cm below the top of the bamboo.

Nest materials were mainly bamboo leaves and stem sheaths with some moss on the exterior surface and a few fibrous roots lining the cup (Fig. 1). Nests were bowl-shaped with a mean ([+ or -] SD) inside depth of 55.6 [+ or -] 2.3 mm and a mean outside height of 78.8 [+ or -] 6.2 mm (n = 9). Four nests had circular openings with a mean inside diameter of 41.4 [+ or -] 3.1 mm, and a mean outside diameter of 72.5 [+ or -] 3.4 mm. The openings of the other five nests were slightly elliptical with mean inside short axis of 39.4 [+ or -] 3.2 mm (range = 34.7-43.7 mm) and long axis of 44.7 [+ or -] 4.0 mm (range = 39.0-49.1 mm). The mean outside short axis was 68.5 [+ or -] 7.9 mm (range = 62.1-81.9 mm), and the long axis was 80.1 [+ or -] 14.1 mm (range = 68.3-103.9 mm, n = 5).

Grey-hooded Parrotbills associated in small flocks with Fulvous Parrotbills outside the breeding season. We observed at least two separate parrotbill flocks between 27 April and 5 May numbering 3-6 individuals moving in unison through suitable habitat on seven different occasions. Paired individuals were observed at the beginning of the breeding period on occasions gathering nest materials and, at times calling to each other with notes we render as "chiahh ... chiahh". Birds bringing material to nests approached cautiously, pausing some 5 m from the nest for about 5 sec and inspecting the surroundings before entering the nest site.

Egg Laying and Incubation Rhythm.--We calculated minimum mean ([+ or -] SD) clutch size from the observed number of nestlings and or eggs in apparently complete clutches, assuming no unhatched eggs were removed from ongoing nests, as 3.1 [+ or -] 0.8 (n = 8 nests; Table 1). Seventeen eggs in six nests were oval in shape and pale blue in color. The mean egg length was 16.3 [+ or -] 0.5 mm (range = 15.6-17.0 mm), mean diameter was 12.4 [+ or -] 0.4 mm (range = 11.8-12.9 mm, n = 17), and mean fresh mass was 1.3 [+ or -] 0.1 g (range = 1.1-1.5 g, n = 14), excluding three eggs in the sixth nest because the parents had initiated incubation. Thirteen eggs hatched and 12 young fledged, giving an overall hatching rate of 0.52 (13/25), and fledging success rate of 0.48 (12/25). The mean number of fledglings per nest was 1.5 (2.4/ successful nest; Table 1).

Egg laying at two nests began 2 days after completion of the nest. Eggs were normally laid one per day although at one nest (nest # 3) we did not observe eggs laid on consecutive days. Incubation began when clutches were completed and lasted 14 days (n = 3). Both parents incubated, but lack of individual markers or distinguishing features prevented us from reliably quantifying any gender differences in individual effort.

Care of Nestlings.--Both parents participated in caring and feeding of nestlings. The parents at nest # 4 made 16 feeding visits in 240 min of observation through the nestling period with only one nestling for an average between-feeding interval of 15 min. The nestling left the nest on day 12 at this nest and on day 13 at nest # 5.

Three nestlings from two nests were weighed and measured every day until fledging (Table 2). Nestlings (Fig. 2) at hatching had a yellow complexion and the capital feather tract was dark; the spinal tract, wings, and legs darkened the next day. Wing and tail feathers emerged from their sheaths on the seventh or eighth day, and the sheaths had already appeared on other parts of the body. Ventral feather growth was still rudimentary when nestlings fledged at day 12 or 13, and feathers covered about 75% of the ventral surface. We obtained mean measurement values from two paired adult parrotbills and another of unknown gender due to no obvious sexual dimorphism: the mean mass was 10.0 g, beak = 7.9 mm, wing = 54.3 mm, tarsus length = 21.5 mm, and mean tail length = 76.5 mm.

DISCUSSION

Bamboo habitats appear to be key requirements for P. zappeyi; the birds were observed to feed (on insects) and nest exclusively in bamboo thickets, and their nests were also constructed within bamboo. Compared to P. webbianus, the Grey-hooded Parrotbill has a smaller clutch size (3.1 vs. 4~5), and smaller egg mass (1.3 vs. 1.5 g) (Guo et al. 2006). Only 13 of 25 eggs of P. zappeyi hatched due to nest loss of 37.5% (3/8; Table 1), and 12 young fledged, which was lower than reported by Guo et al. (2006) for P. webbianus (17 of 19 eggs hatched and fledged young). This might be due to different study sites (Guo et al.'s [2006] work was conducted mainly within the city with few ground predators) while it rained nearly every night on the plateau at our study site.

[FIGURE 1 OMITTED]

Habitats used by Grey-hooded Parrotbill were on top of the Wawushan Plateau surrounded by steep cliffs where the impact of human activities has traditionally been relatively low. Grey-hooded Parrotbills at Wawushan presently do not seem to be in danger as we detected 40 individuals (at least 18 pairs) along 5 km of trail where we counted all birds within 50 m to either side of the trail. This yields a minimum of 0.8 birds/ha.

Promotion of tourism has resulted in construction of a ski slope on the plateau, and the number of tourists is about 300,000/year and rapidly increasing. This has led to destruction of many prime bamboo thickets suitable for Grey-hooded Parrotbills. The increasing number of tourists may have an impact on wildlife species that live and forage close to the ground, particularly Grey-hooded Parrotbills. More detailed environmental assessments are needed to examine the impacts of increased development and visitors on Grey-hooded Parrotbills. The reserve's primary mandate is wildlife protection, particularly when it preserves a rare and restricted Chinese endemic such as the Grey-hooded Parrotbill.

[FIGURE 2 OMITTED]

Received 17 November 2008. Accepted 15 April 2009.

ACKNOWLEDGMENTS

We thank the staff of the Wawushan Natural Reserve for field assistance. This study was funded by the BP Conservation Programme and National Natural Science Foundation of China (30620130110). We sincerely thank two anonymous referees and the editor for their valuable comments.

LITERATURE CITED

BONN, A., A. S. L. RODRIGUES, AND K. J. GASTON. 2002. Threatened and endemic species: are they good indicators of patterns of biodiversity on a national scale. Ecology Letters 5:733-741.

GROOM, M. J., G. K. MEFFE, AND C. R. CARROLL. 2006. Principles of conservation biology. Third Edition. Sinauer Associates, Sunderland, Massachusetts, USA.

GUO, Z. M., W. CHEN, AND J. C. HU. 2006. Analysis on nest habitation factors and chick growth of Paradoxornis webbianus. Sichuan Journal of Zoology 25:858-861.

INTERNATIONAL UNION FOR THE CONSERVATION OF NATURE (IUCN). 2008. IUCN Red List of Threatened Species. www.iucnredlist.org (accessed 11 November 2008)

KRATTER, A. W. 1997. Bamboo specialization by Amazonian birds. Biotropica 29:100-110.

LEI, F. M. AND T. C. LU. 2006. China endemic birds. Science Press, Beijing, China.

MANNE, L. L., T. M. BROOKS, AND S. L. PIMM. 1999. Relative risk of extinction of passerine birds on continents and islands. Nature 399:258-261.

STATTERSFIELD, A. J., M. J. CROSBY, A. J. LONG, AND D. C. WEGE. 1998. Endemic bird areas of the world: priorities for conservation. Birdlife International, Cambridge, United Kingdom.

ZHENG, G. AND Q. WANG. 1998. China red data book of endangered animals, Ayes. National Environmental Protection Agency, Endangered Species Scientific Commission of the People's Republic of China, Science Press, Beijing, China.

Yingxin Jiang, (1) Yue-Hua Sun, (1,2) Nan Lu, 1 and Zhonglin Bi (1)

(1) Key Laboratory or Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China.

(2) Corresponding author; e-mail: sunyh@ioz.ac.cn
TABLE 1. Nests of Grey-hooded Parrotbill in Wawushan
Nature Reserve, Sichuan Province, China.

Nest #   Date found   Nest stage at discovery

1        30 Apr       Nest complete
2        14 May       Abandoned
3        21 May       Nest complete
4        29 May       Egg laying
5        1 Jun        Early construction
6        3 Jun        Incubation
7        11 Jun       Nestling period
8        16 Jun       Early construction
9        26 Jun       Nestling period

Nest #   Date of 1st egg   Clutch size   # Hatching   # Fledging

1             8 May             4            0            0
2
3            28 May             2            0            0
4                               2            1            1
5             7 Jun             3            2            2
6                               3            0            0
7                               4            4            4
8            24 Jun             3            3            3
9                               4            3            2

TABLE 2. Daily measurements and growth of three
Grey-hooded Parrotbill nestlings from two nests in
Wawushan Nature Reserve, Sichuan Province, China.

Nestling age     Mass    Beak    Wing     Tarsus    Tail
(day)            (g)     (mm)    (mm)      (mm)     (mm)

0                 1.0     2.9      1.7       5.4     1.4
1                 1.7     3.3      2.1       6.4     1.5
2                 2.4     3.8      3.2       7.4     1.7
3                 3.4     4.0      3.8       9.1     1.9
4                 4.3     4.2      5.6      11.1     2.1
5                 5.6     4.4      8.1      13.4     2.4
6                 6.4     4.7     12.3      14.9     2.7
7                 6.9     4.8     17.9      -5.6     3.0
8                 7.4     5.0     21.8      16.6     3.7
9                 7.9     5.5     25.1      18.4     4.7
10                8.1     5.4     28.3      19.2     6.0
11                8.2     5.6     30.9      19.5     7.2
12                8.2     5.8     33.4      19.8     8.5
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