Michele PANUCCIO, Nicolantonio AGOSTINI. 2010: Comparison of the water-crossing behavior of Western Marsh Harriers (Circus aeruginosus) and European Honey Buzzards (Pernis apivorus) during autumn migration. Avian Research, 1(1): 30-35. DOI: 10.5122/cbirds.2009.0003
Citation: Michele PANUCCIO, Nicolantonio AGOSTINI. 2010: Comparison of the water-crossing behavior of Western Marsh Harriers (Circus aeruginosus) and European Honey Buzzards (Pernis apivorus) during autumn migration. Avian Research, 1(1): 30-35. DOI: 10.5122/cbirds.2009.0003

Comparison of the water-crossing behavior of Western Marsh Harriers (Circus aeruginosus) and European Honey Buzzards (Pernis apivorus) during autumn migration

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  • Corresponding author:

    (N. Agostini), nicolantonioa@tiscalinet.it

  • Received Date: 28 Oct 2009
  • Accepted Date: 09 Dec 2009
  • Available Online: 12 May 2023
  • We investigated the water-crossing behavior of Western Marsh Harriers (Circus aeruginosus), mostly adults, and European Honey Buzzards (Pernis apivorus), mostly juveniles, in relation to wind conditions, time of the day, flocking and age classes, at a watchsite in central Italy during the autumn migration en route to Africa. Although European Honey Buzzards are less suited than Western Marsh Harriers to undertake long sea crossings, they were more inclined to leave the coast when migrating in flocks. Few birds of both species chose to fly along the coast. Western Marsh Harriers, such as European Honey Buzzards migrating alone, undertook the water crossing rather than stopping migration (birds roosting at the site or flying back inland) during the absence of wind and vice versa during head winds. Conversely, European Honey Buzzards migrating in flocks were not affected in their decision (crossing or stopping migration) by wind direction. Both species undertook the water crossing rather than stopping migration during mornings and vice versa during afternoons. Finally, in both species, adults and juveniles showed the same behavior in front of a water barrier. This result was expected in the case of the Western Marsh Harrier but not from the European Honey Buzzard since, in this species, the water-crossing tendency is age dependent with adults avoiding sea crossings. Our study confirms that flocking significantly affects the water-crossing behavior of European Honey Buzzards during migration. Moreover, in this species, inexperience of juveniles and presumably younger adults, about the high energetic costs of long powered flight and about the existence of shorter routes over water, might explain the strong water-crossing tendency shown by migrants independently from their age.

  • Habitat fragmentation is always a current issue in research by conservation biologists and ecologists (Lord and Norton, 1990; Robinson et al., 1995; Crooks et al., 1999; Fahrig, 2003; Castellón and Sieving, 2006; Ewers and Didham, 2007). Including birds, many species are affected by fragmented habitats (Andrén, 1994b; Herkert, 1994; Souza and Brown, 1994; Lens et al., 2002). During the last two decades, a number of studies have been conducted on, such as, species richness and abundance on fragmented habitats (Terborgh et al., 2001), the minimum living area of birds (Winter and Faaborg, 1999) and birds migration between fragmented habitats (Wiens, 1994). As well, the pattern of species distribution on fragmented habitats has been widely researched, where nested analysis is the most common method to investigate species distribution patterns on various fragmented habitats (Blake, 1991; Honnay et al., 1999; Lomolino and Perault, 2000; Lindenmayer et al., 2002, 2003; Fischer and Lindenmayer, 2005; Wethered and Lawes, 2005; Feeley et al., 2007). One of the patterns that has been identified is the nestedness of insular biotas; isolated communities often form nested subsets, with species on species-poor islands constituting subsets of those present on richer islands (Patterson and Atmar, 1986). A group of species assemblages is said to be completely nested when the all species making up smaller biotas are also found in all larger ones. It has been shown that nested structures are widely present in all organisms and habitat islands (Wright et al., 1998). To account for nested patterns of species distribution, four general hypotheses have been proposed: 1) passive sampling (Andrén, 1994a; Nielsen and Bascompte, 2007), 2) selective extinction (Patterson, 1984; Lomolino, 1996), 3) selective colonization (Cook and Quinn, 1995; Conroy et al., 1999; Mac Nally et al., 2002) and 4) habitat nestedness (Blake, 1991; Calmé and Desrochers, 1999; Honnay et al., 1999). As passive sampling hypothesis is related to the diversity between species and sampling effect, the others are related to habitat features and species life-history traits.

    The most typical karst landscape in the world is found in southwestern Guangxi of China. Karst environments are fragile and very sensitive to human impact and very difficult to restore when destroyed (Tuyet, 2001; Shu et al., 2009). Many of the original local tropical forests have been damaged to varying degrees, causing the forest area and the number of small forest stands to continue to decline, resulting in a shrinkage of species habitat areas (Wu, 2009). At present, the best protected forest areas are in nature reserves in the form of habitat fragments, hence it is a huge challenge to protect species diversity, including birds. Nested analysis of species communities is of special importance in species protection (Patterson, 1987), offering a new perspective on their protection (Chen and Wang, 2004). We have studied distribution patterns of birds in fragmented habitats of the karst area of southwestern Guangxi to explore: 1) if nested patterns of birds in the karst area of southwestern Guangxi exist or not, 2) the factors which are correlated with a nested pattern and the effect of factors on the formation of these nested patterns and 3) some suggestions for the protection of bird species diversity in this karst area.

    The karst area is located at 105°29′–108°6′E and 22°9′–23°41′N in the southwest of the Guangxi Zhuang Autonomous Region in China (Fig. 1), adjacent to the Socialist Republic of Vietnam. This area includes nine cities and counties, i.e., the counties Long'an of Nanning city, Jiangzhou, Fusui, Daxing, Tiandeng and Longzhou of Chongzuo city as well as the counties Jingxi, Debao and Napo of Baise city. The total area covers about 1300 km2 (Table 1), of which 56% is of a karst landform. This area is the most typical karst landscape in the world and a global biodiversity hotspot (Myers et al., 2000), with rich north tropical biological karst resources. The karst area of southwestern Guangxi is the most important site of global significance among other biodiversity hotspots in China (Chen, 1993). The major landform of southwestern Guangxi is the typical limestone, besides the shale and sandstone landscape. The area is located south of the tropic of cancer and has a north tropical monsoon climate, with an average annual temperature of 18 to 22℃ and rainfall of 1100 –1500 mm. The vegetation is mainly that of a north tropical forest, with small areas of subtropical evergreen broad-leaved forests. Because of rapid social and economic development, the original forest vegetation has deteriorated considerably. The remainder of the original forest vegetation is largely preserved in nature reserves in the form of fragmented areas.

    Figure  1.  Map of the limestone area in southwestern Guangxi with sites surveyed. N.P. = Napo; D.B. = Debao; L.A. = Long'an; J.X. = Jingxi; T.D. = Tiandeng; D.X. = Daxing; F.S. = Fusui; L.Z. = Longzhou; J.Z. = Jiangzhou; P.X. = Pingxiang; N.M. = Ningming. For the nature reserve numbers, see information in Table 1.
    Table  1.  Habitat features of the 13 sites
    Habitat fragment Nature reserve Area (km2) Distance to nearest larger fragment (m) Vegetation richness
    1 Qinglongshan nature reserve 57.2 18.7 1100
    2 Nonggang nature reserve * 54.2 7.5 1340
    3 Bangliang nature reserve 50.7 20.4 956
    4 Chunxiu nature reserve 44.3 20.3 900
    5 Huanglianshan nature reserve 43.6 7.5 1166
    6 Gulongshan nature reserve 40.5 34.9 1065
    7 Xialei nature reserve 35.4 52.1 1004
    8 Laohutiao nature reserve 31.1 22.7 520
    9 Encheng nature reserve 28.7 34.9 927
    10 Longhushan nature reserve 22.5 10.2 870
    11 Bapen nature reserve 20.6 37.1 231
    12 Banli nature reserve 16.8 15.2 550
    13 Diding nature reserve 11.5 17.1 1000
    * Refers to a national nature reserve, the others are regional nature reserves.
     | Show Table
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    There are 13 nature reserves in the study area (Nonggang, Chunxiu, Qinglongshan, Bangliang, Diding, Encheng, Xialei, Gulongshan, Longhushan, Laohutiao, Banli, Bapen and Huanglianshan Nature Reserves), from which 13 relatively isolated fragmented areas with less human intervention and well-forested area were selected as our study sites, numbered by size from 1 to 13. Site 3 is in the Sino-Vietnam border area and fragments on both sides of the border were selected as one site. Because of its continuous forest, only the result of our bird survey, conducted on the Guangxi side, was used, but the entire area on both sides of the border was treated as a whole area.

    The cover of the study area is dominated by six vegetation types: 1) tropical rain forest, 2) broad-leaved forest, 3) shrub-forest, 4) shrub-grass, 5) farmland and 6) wetland. At each site, line transect method was used for bird survey. Two transect lines were sampled on the wetland, farmland and shrub-grass respectively and four transect lines were sampled on the rain forest, broad-leaved forest and shrub-forest respectively. The main area was covered by these transect lines. During the survey the length and direction of each transect line were adjusted according to the shape and size of each site in order to obtain accurate results.

    This study was conducted between June 2009 and September 2010. Days with persistent rain and strong winds were avoided, for under those conditions it would be difficult to record birds. Bird surveys were carried out by using 8 × 42 binoculars from 06:00–10:00 and from 15:00–18:00 local time. Observation points along each 1500 m transect line were arranged and birds observed on both sides of transect and habitat type was recorded at each site. In order to survey the birds accurately in the shrubs, we set 3 m × 5 m mist nets on the edge of the shrubs. Three or five mist nets were set for 3–5 days as a group between 06:00 and 18:00. The mist nets were checked every hour and any birds trapped were recorded and then released. Considering that raptors and water birds are strong flyers with the ability to migrate between fragmented areas, the study was only conducted on resident and breeding birds while omitting raptors and water birds from our survey at each site.

    Three habitat variables, area, isolation and vegetation richness of a habitat are commonly considered to greatly affect the distribution pattern of birds (Lomolino and Perault, 2000; Fischer and Lindenmayer, 2005; Wethered and Lawes, 2005; Wang et al., 2010). For our study, three factors are selected as habitat features: area, distance to the nearest larger fragmented area and vegetation richness. We interpreted the distance to the nearest larger fragment as the straight line distance between one fragment and the nearest larger fragment. Vegetation richness is the number of plant species at each fragment, the data was obtained from the scientific survey report of each reserve and several references (Liang et al., 1985; Xie et al., 1994). Google Earth Pro 5.1 was used to evaluate the area and the distance between fragments and vegetation richness was obtained from survey data and a few references (Liang et al., 1985; Xie et al., 1994).

    Bird life-history traits have also been proved to affect bird distribution patterns (Cook and Quinn, 1995; Kadmon, 1995; Fischer and Lindenmayer, 2005; Feeley et al., 2007; Wang et al., 2010). The activity ability and body size of birds, and habitat specificity were used to analyze the nested pattern of the birds. The activity ability is interpreted as the mobility of a given species, defined as the dispersal ratio ("dp"; Woinarski, 1989) and calculated for each bird by dividing its mean wing length (mm) by the cubic root of its mean mass (g) (Fischer and Lindenmayer, 2005); the larger the "dp" value, the stronger the mobility of a bird. The body size of birds was obtained from the record of specimens at Guangxi University, Guangxi Academy of Sciences and The Avifauna of Yunnan China, The Avifauna of Guizhou, Fauna Sinica Aves and several references (Zhou and Jiang, 2008; Alström et al., 2010). Habitat specificity refers to the number of habitat types (six habitat types in the current landscape) where each bird species lives. For example, the habitat specificity of one species only found in one habitat type was given the value 1, which meant the species has a narrow distribution range and vice versa.

    Based on the data of our bird survey, sites were initially sorted by species richness which determines the ordering of rows, while fragments were sorted by their size, determining the ordering of columns. Given these procedures, a binary code "1/0" was used to show presence/absence of species in each fragment. In the end, a presence-absence matrix was constructed for birds (see Supplementary Table S1).

    Species nestedness is currently calculated with the nestedness temperature T, used in the algorithm implemented by the calculator BINMATNEST (binary matrix nestedness temperature calculator; Rodríguez-Gironés and Santamaria, 2006). T provides a standardized measure of matrix disorder by assessing the deviation of an observed matrix from the completely nested. T thus ranges from 0 for a completely nested matrix to 100 for one that is completely disordered (Boecklen, 1997; Wright et al., 1998). The calculator first computes an isocline of perfect order, which is a curve in a completely nested matrix of the same size. BINMATNEST creates three null models to compute the temperature of each random matrix and returns the proportion of matrices with temperature lower than or equal to the temperature of the input matrix. Among these, null model 3 was considered to be able to avoid the effect of passive sampling (Rodríguez-Gironés and Santamaria, 2006; Moore and Swihart, 2007).

    The effect of habitat features and species life-history traits on forming a nested pattern was evaluated by a Spearman's rank correlation analysis (Fernández-Juricic, 2004; Schouten et al., 2007).

    We used Microsoft Excel 2003 for data calculation and arrangement and other statistical analyses from SPSS 17.0. We followed the usual convention that p < 0.05 means statistically significant differences, p < 0.01 means strongly significant differences and p > 0.05 signifies non-significant differences.

    A total of 248 bird species were recorded, belonging to 42 families and 9 orders, including 191 Passeriformes bird species from 30 families. The number of bird species in each fragment ranges between 113 and 183 (see Supplementary Table S1). Among these, 25 bird species, such as the White Wagtail (Motacilla alba), Rufousnecked Scimitar Babbler (Pomatorhinus ruficollis), Redwhiskered Bulbul (Pycnonotus jocosus), Barn Swallow (Hirundo rustica), Spotted Dove (Streptopelia chinensis), Greater Coucal (Centropus sinensis) and so on were recorded in all fragments; 42 bird species were only found in one fragment, while 181 bird species were recorded in more than one fragment.

    The habitat features of the 13 fragments were recorded as data. The sampling sites ranged from 11.5 to 57.2 km2 in size. The distance of each fragment to the nearest larger fragment was between 7.5 and 52.1 m; the vegetation richness of each fragment was between 231 and 1340 species (Table 1).

    It can be seen from Table 2 that bird body weight ranged from 5 to 1400 g, body length was between 81 and 885 mm, the "dp" value ranged from 14.22 to 52.58 and habitat specificity from 1–5; most birds were found in habitat types 2 and 3.

    Table  2.  Life-history traits of bird species in southwestern Guangxi
    Species Body weight (g) Body length (mm) Wing length (mm) dp Habitat specificity
    Chinese Francolin (Francolinus pintadeanus) 365.0 320 145 20.29 3
    Spotted Dove (Streptopelia chinensis) 182.0 322 159 28.06 4
    Large Green-billed Malkoha (Phaenicophaeus tristis) 117.5 502 150 30.63 2
    Common Coucal (Centropus sinensis) 266.6 184 217 33.72 4
    Lesser Coucal (Centropus bengalensis) 99.8 330 160 34.49 3
    Common Kingfisher (Alcedo atthis) 27.2 165 70 23.28 1
    White-throated Kingfisher (Halcyon smyrnensis) 89.6 265 117 26.15 2
    Barn Swallow (Hirundo rustica) 15.6 171 109 43.62 4
    Red-rumped Swallow (Hirundo daurica) 20.6 180 117 42.68 4
    White Wagtail (Motacilla alba) 21.2 181 90 32.52 4
    Scarlet Minivet (Pericrocotus flammeus) 29.2 205 100 32.47 3
    Red-whiskered Bulbul (Pycnonotus jocosus) 30.7 194 86 27.47 4
    Chinese Bulbul (Pycnonotus sinensis) 35.5 190 90 27.38 4
    Black Bulbul (Hypsipetes leucocephalus) 54.6 237 121 31.89 3
    Long-tailed Shrike (Lanius schach) 58.3 261 105 27.08 3
    Red-billed Blue Magpie (Urocissa erythrorhyncha) 170.8 555 190 34.24 3
    Taiwan Whistling Thrush (Myophoneus caeruleus) 184.0 303 173 30.42 2
    Hwamei (Garrulax canorus) 68.4 233 93 22.74 3
    Rufous-necked Scimitar Babbler (Pomatorhinus ruficollis) 25.1 190 74 25.27 5
    Rufous-capped Babbler (Stachyris ruficeps) 9.6 109 52 24.47 5
    Grey-cheeked Fulvetta (Alcippe morrisonia) 16.0 136 63 25.00 3
    Yellow-bellied Prinia (Prinia flaviventris) 7.4 136 44 22.58 4
    Common Tailorbird (Orthotomus sutorius) 8.0 113 45 22.50 5
    Japanese White-eye (Zosterops japonicus) 10.5 104 55 25.12 3
    Great Tit (Parus major) 13.7 129 67 28.00 5
    Hair-crested Drongo (Dicrurus hottentottus) 88.8 311 172 38.55 2
    Crested Myna (Acridotheres cristatellus) 125.2 243 138 27.59 3
    Fork-tailed Sunbird (Aethopyga christinae) 6.2 103 49 26.67 3
    Silver Pheasant (Lophura nycthemera) 1400.0 885 250 22.35 3
    White-breasted Waterhen (Amaurornis phoenicurus) 246.0 322 170 27.13 3
    White-throated Bulbul (Alophoixus pallidus) 50.8 235 110 29.70 2
    Green-winged Bulbul (Hypsipetes mcclellandii) 40.3 232 106 30.92 2
    Grey Bushchat (Saxicola ferrea) 12.3 136 64 27.73 3
    Hill Prinia (Prinia atrogularis) 10.6 163 46 20.94 3
    Plain Prinia (Prinia inornata) 9.9 149 45 20.96 3
    Black-throated Tit (Aegithalos concinnus) 6.4 100 48 25.85 3
    Black-naped Oriole (Oriolus chinensis) 78.3 247 152 35.53 3
    Red Junglefowl (Gallus gallus) 990.0 633 224 22.48 3
    Indian Cuckoo (Cuculus micropterus) 103.0 324 189 40.32 2
    Drongo Cuckoo (Surniculus lugubris) 37.2 254 136 40.74 2
    House Swift (Apus nipalensis) 26.6 139 132 44.22 3
    Sooty-headed Bulbul (Pycnonotus aurigaster) 48.7 211 97 26.56 3
    Magpie Robin (Copsychus saularis) 38.4 204 96 28.46 3
    Hainan Blue Flycatcher (Niltava hainanus) 13.9 138 69 28.70 3
    Black-naped Monarch (Hypothymis azurea) 12.5 143 72 31.02 3
    Striated Yuhina (Yuhina castaniceps) 13.0 130 56 23.82 2
    Plain Flowerpecker (Dicaeum concolor) 6.8 81 46 24.28 3
    Blue Rock Thrush (Monticola solitarius) 49.4 211 120 32.70 3
    Grey-chinned Minivet (Pericrocotus solaris) 17.3 181 84 32.48 2
    Collared Finchbill (Spizixos semitorques) 40.5 196 90 26.21 2
    Chestnut Bulbul (Hemixos castanonotus) 34.7 206 101 30.97 3
    Black-throated Laughingthrush (Garrulax chinensis) 91.0 230 110 24.46 2
    Orange-bellied Leafbird (Chloropsis hardwickii) 33.5 185 90 27.92 2
    Dollarbird (Eurystomus orientalis) 131.7 264 185 36.36 2
    Large-billed Crow (Corvus macrorhynchos) 525.6 475 326 40.40 3
    Great Barbet (Megalaima virens) 190.2 333 140 24.34 2
    Black-winged Cuckoo Shrike (Coracina melaschistos) 37.6 227 117 34.92 2
    Blyth's Leaf Warbler (Phylloscopus reguloides) 7.6 104 60 30.52 3
    Crow-billed Drongo (Dicrurus annectans) 60.5 269 142 36.17 2
    Silver-eared Mesia (Leiothrix argentauris) 26.0 168 76 25.65 2
    Red-billed Leiothrix (Leiothrix lutea) 21.5 142 66 23.74 2
    Larger white-rumped Swift (Apus pacificus) 37.5 178 176 52.58 3
    Ring-necked Pheasant (Phasianus colchicus) 1135.0 747 232 22.24 2
    Chinese Bamboo Partridge (Bambusicola thoracica) 271.0 308 131 20.24 3
    Grey-headed Woodpecker (Picus canus) 144.7 304 150 28.57 2
    Rosy Minivet (Pericrocotus roseus) 19.1 186 88 32.92 2
    Rusty-capped Fulvetta (Alcippe dubia) 20.0 146 62 22.84 2
    White-bellied Yuhina (Yuhina zantholeuca) 12.5 118 67 28.87 2
    White-browed Rufous (Piculet Sasia ochracea) 8.5 89 55 26.95 3
    Bianchi's Warbler (Seicercus valentini) 7.3 110 54 27.84 3
    Small Niltava (Niltava macgrigoriae) 11.0 128 64 28.78 3
    Yellow-bellied Sunbird (Cinnyris jugularis) 7.5 107 51 26.05 2
    Ashy Wood Swallow (Artamus fuscus) 40.0 178 127 37.14 3
    Emerald Dove (Chalcophaps indica) 121.0 233 139 28.10 2
    White-throated Fantail (Rhipidura albicollis) 11.0 177 78 35.07 2
    Blue-winged Siva (Minla cyanouroptera) 18.0 151 64 24.42 3
    Spectacled Laughingthrush (Eudynamys scolopaceus) 218.0 427 202 33.56 3
    Yellow-billed Bay Woodpecker (Blythipicus pyrrhotis) 117.0 254 135 27.60 2
    Striped Tit Babbler (Macronous gularis) 10.7 123 54 24.51 3
    Rufous Woodpecker (Celeus brachyurus) 92.0 230 120 26.58 2
    Fujian Niltava (Niltava davidi) 24.8 170 91 31.20 3
    Sulphur-breasted Warbler (Phylloscopus ricketti) 7.0 97 57 29.80 2
    Bar-winged Flycatcher Shrike (Hemipus picatus) 9.4 139 64 30.33 3
    Red Turtle Dove (Streptopelia tranquebarica) 111.3 231 138 28.69 2
    Golden-throated Barbet (Megalaima franklinii) 81.8 217 98 22.58 2
    Grey-headed Canary Flycatcher (Culicicapa ceylonensis) 10.4 120 62 28.40 3
    Crimson Sunbird (Aethopyga siparaja) 7.0 137 55 28.75 2
    Common Cuckoo (Cuculus canorus) 100.8 332 228 48.99 2
    Speckled Piculet (Picumnus innominatus) 12.8 103 57 24.37 2
    Plumbeous Water Redstart (Rhyacornis fuliginosus) 16.5 119 72 28.28 1
    Sultan Tit (Melanochlora sultanea) 40.6 195 105 30.55 2
    Short-tailed Wren Babbler (Napothera brevicaudata) 27.0 146 66 22.00 2
    Black-headed Babbler (Stachyris nigriceps) 18.0 117 60 22.89 3
    Eurasian Hoopoe (Upupa epops) 75.9 274 148 34.96 2
    Crested Kingfisher (Ceryle rudis) 302.0 398 188 28.02 1
    Lesser Racket-tailed Drongo (Dicrurus remifer) 46.3 543 158 44.00 2
    Snowy-browed Flycatcher (Ficedula hyperythra) 8.4 103 59 29.02 2
    Plaintive Cuckoo (Cacomantis merulinus) 29.2 232 113 36.70 1
    Great Pied Woodpecker (Picoides major) 73.4 250 134 32.00 2
    Pygmy Wren Babbler (Pnoepyga pusilla) 11.5 87 47 20.82 3
    Black-crested Bulbul (Pycnonotus melanicterus) 31.6 193 87 27.52 2
    Lesser Pied Kingfisher (Megaceryle lugubris) 93.0 290 136 30.02 1
    Oriental Yellow-eyed Babbler (Chrysomma sinense) 23.3 182 69 24.16 2
    Brown-breasted Bulbul (Pycnonotus xanthorrhous) 31.8 194 88 27.78 2
    White-bellied Green Pigeon (Treron sieboldii) 290.0 300 173 26.14 2
    White-rumped Munia (Lonchura striata) 10.5 109 50 22.83 3
    Crested Bunting (Melophus lathami) 22.0 140 79 28.19 3
    Blackbird (Turdus merula) 102.0 271 150 32.10 3
    Spotted Munia (Lonchura punctulata) 15.0 116 54 21.90 3
    Pale Blue Flycatcher (Niltava unicolor) 19.0 168 84 31.48 2
    Yellow-cheeked Tit (Parus spilonotus) 18.3 137 76 28.84 3
    Gray Treepie (Dendrocitta formosae) 99.1 368 141 30.47 2
    Ashy Drongo (Dicrurus leucophaeus) 46.8 271 143 39.68 2
    Franklin's Prinia (Prinia hodgsonii) 6.1 110 45 24.63 3
    Gould's Sunbird (Aethopyga gouldiae) 6.8 145 55 29.03 2
    Tree Sparrow (Passer montanus) 21.2 139 68 24.57 3
    Scarlet-backed Flowerpecker (Dicaeum c.cruentatum) 6.6 88 48 25.59 2
    Azure-winged Magpie (Pica pica) 232.4 450 209 33.99 3
    Blue-and-white Flycatcher (Cyanoptila cyanomelana) 10.5 170 61 27.86 2
    Eastern Crowned Warbler (Phylloscopus coronatus) 9.0 116 61 29.33 2
    White-rumped Shama (Copsychus malabaricus) 26.4 243 89 29.89 2
    Blue-throated Barbet (Megalaima asiatica) 86.7 229 100 22.59 2
    White-browed Laughingthrush (Garrulax sannio) 67.5 228 97 23.82 3
    Ashy Lauthingthrush (Garrulax cineraceus) 52.0 226 87 23.31 2
    White-winged Magpie (Urocissa whiteheadi) 260.0 450 211 33.06 3
    Yellow-bellied Warbler (Seicercus superciliaris) 6.5 100 49 26.26 2
    Dark-crowned Prinia (Prinia rufescens) 7.1 108 42 21.85 3
    Spot-necked Babbler (Stachyris striolata) 26.4 152 63 21.16 3
    Grey-bellied Tesia (Tesia cyaniventer) 8.5 82 49 24.01 2
    Nonggang Babbler (Stachyris nonggangensis) 35.5 165 89 27.08 3
    Black Drongo (Dicrurus macrocercus) 49.5 276 143 38.95 3
    Chestnut-crowned Warbler (Seicercus castaniceps) 5.0 96 51 29.82 2
    Long-tailed Broadbill (Psarisomus dalhousiae) 60.0 257 100 25.54 2
    Asian Paradise Flycatcher (Terpsiphone paradisi) 27.7 300 92 30.41 2
    White-tailed Warbler (Phylloscopus davisoni) 6.2 104 53 28.85 2
    White-bellied Jungle Babbler (Pellorneum albiventre) 17.0 140 53 20.61 2
    Limestone Leaf Warbler (Phylloscopus calciatilis) 5.6 95 53 29.85 2
    White-tailed Blue Robin (Cinclidium leucurum) 23.0 174 91 32.00 2
    Golden Babbler (Stachyris chrysaea) 8.0 108 48 24.00 2
    Velvet-fronted Nuthatch (Sitta frontalis) 13.1 116 74 31.39 2
    Gould's Fulvetta (Alcippe brunnea) 19.5 135 60 22.29 2
    Red-winged Crested Cuckoo (Clamator coromandus) 88.4 380 158 35.47 2
    Large Scimitar Babbler (Pomatorhinus hypoleucos) 85.0 257 96 21.83 2
    Malabar Pied Hornbill (Anthracoceros albirostris) 786.1 788 300 32.51 2
    Golden Mountain Thrush (Zoothera dauma) 127.0 285 163 32.43 2
    Chestnut-tailed Starling (Sturnia malabaricua) 44.0 196 103 29.18 3
    Blue-rumped Pitta (Pitta soror) 110.0 229 108 22.54 2
    Dusky Warbler (Phylloscopus fuscatus) 8.8 118 61 29.55 3
    Olive-backed Pipit (Anthus hodgsoni) 21.7 153 83 29.76 4
    Brown Shrike (Lanius cristatus) 31.9 192 89 28.06 2
    Yellow-breasted Green Magpie (Cissa hypoleuca) 156.2 328 143 26.55 2
    Grey-backed Thrush (Turdus hortulorum) 75.0 240 129 30.59 3
    Brown-chested Jungle Flycatcher (Rhinomyias brunneata) 17.0 150 80 31.11 2
    Two-barred Greenish Warbler (Phylloscopus plumbeitarsu) 7.6 108 58 29.50 3
    Black-necked Tailorbird (Orthotomus atrogularis) 5.9 115 43 23.80 2
    Red-headed Trogon (Harpactes erythrocephalus) 97.0 341 154 33.52 2
    Oriental White-eye (Zosterops palpebrosus) 8.9 100 51 24.61 3
    Large Hawk Cuckoo (Cuculus sparverioides) 147.5 388 236 44.67 2
    Fire-breasted Flowerpecker (Dicaeum ignipectus) 6.9 83 49 25.74 2
    Black-throated Sunbird (Aethopyga saturate) 5.5 141 53 30.03 3
    Orange-headed Ground Thrush (Zoothera citrine) 55.0 205 113 29.71 2
    Brown-breasted Flycatcher (Muscicapa muttui) 13.5 125 75 31.50 2
    Large Niltava (Niltava grandis) 36.4 204 103 31.08 2
    Verditer Flycatcher (Eumyias thalassina) 17.7 156 86 33.00 2
    Asian House Martin (Delichon dasypus) 11.7 113 111 48.89 3
    Vivid Niltava (Niltava vivida) 21.0 145 82 29.72 2
    Mountain Tailorbird (Orthotomus cuculatus) 6.9 112 46 24.16 2
    Oriental Turtle Dove (Streptopelia orientalis) 238.0 331 198 31.95 2
    Hill Blue Flycatcher (Niltava banyumas) 14.3 144 71 29.25 2
    Bronzed Drongo (Dicrurus aeneus) 29.2 235 127 41.24 2
    Russet Sparrow (Passer rutilans) 22.0 135 75 26.77 3
    Fairy Pitta (Pitta nympha) 59.5 189 119 30.48 2
    Grey-crowned Woodpecker (Picoides canicapillus) 25.3 154 95 32.36 2
    Red-winged Shrike Babbler (Pteruthius flaviscapis) 36.0 169 83 25.14 2
    Black-capped Kingfisher (Halcyon pileata) 96.3 277 126 27.49 3
    Rusty-cheeked Scimitar Babbler (Pomatorhinus erythrogenys) 69.1 228 91 22.18 2
    White-spectacled Warbler (Seicercus affinis) 5.0 110 50 29.24 2
    Little Spiderhunter (Arachnothera longirostra) 13.5 147 67 28.14 2
    Pin-tailed Green Pigeon (Treron apicauda) 230.0 381 154 25.13 1
    Silver-breasted Broadbill (Serilophus lunatus) 30.2 170 84 26.97 2
    Dusky Crag Swallow (Ptyonoprogne concolor) 18.0 125 105 40.06 1
    Large Cuckoo Shrike (Coracina novaehollandiae) 109.2 312 180 37.66 2
    Brown-rumped Minivet (Pericrocotus divaricatus) 22.2 192 94 33.45 2
    Short-billed Minivet (Pericrocotus brevirostris) 19.0 185 87 32.60 2
    Yellow-bellied Bulbul (Alophoixus flaveolus) 54.2 219 104 27.48 2
    Grey-backed Shrike (Lanius tephronotus) 47.1 231 100 27.69 2
    Slaty-blue Flycatcher (Ficedula tricolor) 9.4 113 60 28.43 2
    Streak-breasted Jungle Babbler (Pellorneum ruficeps) 24.5 155 67 23.07 2
    Grey-cheeked Warbler (Seicercus poliogenys) 6.0 105 51 28.07 2
    Broad-billed Warbler (Seicercus hodgsoni) 6.0 102 47 25.87 2
    Rufous-faced Warbler (Abroscopus albogularis) 5.0 96 48 28.07 2
    Red-tailed Laughingthrush (Garrulax milnei) 81.5 253 96 22.14 2
    Barred Buttonquail (Turnix suscitator) 74.0 161 87 20.72 2
    Spectacled Laughingthrush (Garrulax perspicillatus) 123.6 290 123 24.69 3
    Lesser Necklaced Laughingthrush (Garrulax pectoralis) 133.5 300 135 26.41 2
    Grey-headed Parrotbill (Paradoxornis gularis) 27.0 175 80 26.67 3
    Slaty-breasted Banded Rail (Gallirallus striatus) 140.0 256 126 24.27 2
    Black-collared Starling (Gracupica nigricollis) 164.0 285 164 29.96 3
    Little Pied Flycatcher (Ficedula westermanni) 7.2 108 58 30.04 2
    Chinese Babax (Babax lanceolatus) 63.0 239 90 22.62 2
    Burmese Shrike (Lanius collurioides) 31.7 190 87 27.49 2
    Streaked Spiderhunter (Arachnothera magna) 33.1 188 91 28.34 2
    Silver-backed Spinetail Swift (Hirundapus cochinchinensis) 95.0 190 168 36.82 2
    Vinous-throated Parrotbill (Paradoxornis webbianus) 10.2 120 54 24.90 2
    Zitting Cisticola (Cisticola juncidis) 8.2 105 51 25.29 3
    Water Rail (Rallus aquaticus) 160.0 270 130 23.95 2
    Brownish-flanked Bush Warbler (Cettia fortipes davidiana) 10.8 116 53 23.98 2
    Lesser Cuckoo (Cuculus poliocephalus) 54.8 255 160 42.12 2
    Blue-winged Leafbird (Chloropsis cochinchinensis) 24.0 169 81 28.08 1
    Eurasian Jay (Garrulus glandarius) 159.3 336 180 33.20 2
    Yellow-browed Warbler (Phylloscopus inornatus) 6.5 100 50 26.79 3
    Blue-breasted Quail (Coturnix chinensis) 62.0 120 70 17.69 3
    Small Buttonquail (Turnix sylvatica) 46.0 110 66 18.42 2
    Himalayan Greenfinch (Carduelis sinica) 20.0 123 81 29.84 3
    Brown Crake (Amaurornis akool) 184.0 277 127 22.33 2
    Spectacled Barwing (Actinodura ramsayi) 39.0 177 83 24.48 2
    Ruddy-breasted Crake (Porzana fusca) 76.0 220 110 25.97 2
    Rufous-bellied Woodpecker (Picoides hyperythrus) 47.2 203 122 33.76 2
    Richard's Pipit (Anthus richerdi) 30.3 178 97 31.11 2
    Tree Pipit (Anthus trivialis) 23.2 147 86 30.15 2
    Long-tailed Minivet (Pericrocotus ethologus) 16.9 190 90 35.07 2
    Tiger Shrike (Lanius tigrinus) 28.9 170 84 27.37 2
    Hill Myna (Gracula religiosa) 211.0 280 163 27.38 2
    Stonechat (Saxicola torquata) 13.0 129 67 28.49 3
    Giant Babax (Babax waddelli) 74.5 143 130 30.90 2
    Pale-rumped Warbler (Phylloscopus proregulus) 6.5 93 51 27.33 3
    Buff-bellied Warbler (Phylloscopus subaffinis) 6.7 99 53 28.11 2
    Grey Laughingthrush (Garrulax maesi) 112.7 290 134 27.74 2
    Blue-tailed Bee-eater (Merops philippinus) 93.0 295 134 29.58 2
    Forest Wagtail (Dendronanthus indicus) 17.6 165 79 30.37 3
    White-shouldered Starling (Sturnia sinensis) 45.0 187 103 28.96 3
    Silky Starling (Sturnus sericeus) 77.6 207 120 28.13 3
    Chestnut-headed Fulvetta (Alcippe castaneceps) 8.5 107 55 26.95 2
    Brown Hill Prinia (Prinia polychroa) 7.8 127 47 23.70 3
    Yellowish-bellied Bush Warbler (Seicercus superciliaris) 9.0 107 42 20.19 2
    Pale-footed Bush Warbler (Cettia pallidipes) 9.8 117 48 22.43 2
    Brown Bush Warbler (Bradypterus luteoventris) 12.4 127 51 22.03 2
    Green-backed Tit (Parus monticolus) 18.1 125 67 25.52 3
    Watercock (Gallicrex cinerea) 380.0 385 103 14.22 2
    Green Imperial Pigeon (Ducula badia) 487.5 433 228 28.97 1
    Chestnut-capped Babbler (Timalia pileata) 23.0 165 62 21.80 2
    Japanese Bush Warbler (Cettia diphone) 23.4 148 73 25.52 2
    Brown-breasted Hill Partridge (Arborophila brunneopectus) 310.0 220 130 19.21 3
    Flavescent Green Bulbul (Pycnonotus flavescens) 33.8 206 87 26.91 2
    White-crowned Forktail (Enicurus leschenaultia) 45.0 250 109 30.64 2
    Crimson-winged Liocichla (Liocichla phoenicea) 50.0 221 91 24.70 3
    Black-chinned Yuhina (Yuhina nigrimenta) 11.0 120 58 26.08 2
    Black-headed Sibia (Heterophasia melanoleuca) 36.0 195 90 27.26 2
     | Show Table
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    The results of the nestedness are shown by BINMATNEST. The nestedness temperature T of bird communities in southwestern Guangxi was 39.78℃. The degree of nestedness for all three models shows highly significant differences (p < 0.001). These results show that birds in the karst area of southwestern Guangxi have nested patterns (Table 3).

    Table  3.  Nestedness of the bird matrix
    Null model p value Mean temperature (℃) Variance
    1 < 0.01 70.71 2.26
    2 < 0.01 62.43 3.45
    3 < 0.01 57.61 2.70
    Note: Nestedness temperature 39.78℃.
     | Show Table
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    Spearman's rank correlation coefficients indicate that the three habitat features (area: r = 0.121, p > 0.05; distance to the nearest larger fragment: r = 0.115, p  >  0.154; vegetation richness: r = 0.055, p > 0.05) and the three life-history traits (body weight: r = 0.026, p > 0.05; body length: r = 0.069, p > 0.05; dp: r = 0.062, p > 0.05) had no significant effect on bird nestedness. The only factor correlated with bird nestedness was bird habitat specificity (r = 0.339, p < 0.01). For more details please see Table 4.

    Table  4.  Correlation coefficients of habitat features and life-history traits of birds
    Habitat features Life-history traits
    Area Distance to the nearest larger fragment Vegetation richness Body weight Body length dp Habitat specificity
    r 0.121 0.115 −0.055 0.026 0.069 0.062 0.339**
    p 0.694 0.707 0.859 0.848 0.281 0.332 < 0.01
    ** p < 0.01
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    As with nested patterns of birds at other fragmented habitats (or islands) (Blake et al., 1991; Davidar et al., 2002; Amparo Lázaro et al., 2005; Fischer and Lindenmayer, 2005; Feeley et al., 2007; Louzada et al., 2010; Wang et al., 2010; 2011), we obtained similar result, i.e., strongly nested pattern in bird assemblages in the karst area of southwestern Guangxi. Our result provides further proof that statistically significant nestedness is common (Wright et al., 1998) and is present in almost all types of biological groups and fragmented habitats (islands).

    However, from the results of Spearman's rank correlation analysis, we conclude that none of the three habitat features (area, distance to nearest larger fragment, vegetation richness) was statistically significant (p > 0.05), despite the fact that "area" has always been considered to be statistically significant to nested patterns of species (Lomolino and Perault, 2000; Fischer and Lindenmayer, 2005; Wethered and Lawes, 2005). Isolation is not significant to generating nestedness probably because the range of isolation is small in our study. Although the habitat features were not significant in the nested patterns, this does not mean that habitat features do not affect bird assemblages. Single factor cannot affect the distribution pattern of the birds (Schoener and Schoener, 1983a, 1983b). The following reasons should be considered for analyzing the results.

    Our study area, i.e., the karst area of southwestern Guangxi, is in a northern tropical area where the main vegetation consists of seasonal tropical rain forests and some broad-leaved forests. On the large scale, fragments are distributed in the region about 2310000 km2, hence differences between fragmented habitats in this large scale landscape can be expected. Some fragments had good protection with a high proportion of a rain forest (e.g. fragments 2, 3, 7, 10–13), but the vegetation of other fragments consisted mainly of broad-leaved forests (e.g. fragments 1, 4–6, 8, 9).

    The investigations of tropical forests by Hubbell (2005a; 2005b; 2006) show that it is difficult to explain the diversity often observed in these species-rich communities. Hubbell and other ecologists have proposed the neutral theory (Hubbell, 1979, 2001, 2005a, 2006; Hubbell and Foster, 1983, 1986). They argued that the number of species in a community of a tropical forest is greater than in other forests. Based on our study of the 13 fragment habitats, the number of species in seasonal tropical rain forests was beyond its carrying capacity; for example, fragment 13 had the smallest area, but its number of birds was greater than that of some larger fragments. That "area" was not significant in our study may be the reason for this result.

    Habitat specificity was statistically significant to nested patterns of birds. Because vegetation in seasonal tropical rain forest is often unique, with special and a greater variety of habitats, compared with broad-leaved forests, the habitat choice for birds provide for greater differences. Some tropical birds are mainly found in fragments 2, 3 and 13, consisting of larger tropical forests; these include the Red-headed Trogon (Harpactes erythrocephalus), Long-tailed Broadbill (Psarisomus dalhousiae), Blackthroated Sunbird (Aethopyga saturate), Little Spiderhunter (Arachnothera longirostris) and others. In contrast, some birds can adapt to and are found in several habitats, such as the White Wagtail (Motacilla alba), Redwhiskered Bulbul (Pycnonotus jocosus), Spotted Dove (Streptopelia chinensis), as well as other birds. Simultaneously it should be noted that the result, that vegetation richness was not significant on nested bird patterns, might be a function of the vegetation in each fragment. Seasonal tropical rain forests have larger food resources and provide more habitat types for greater numbers of bird species, especially the high specificity species.

    Among the three bird life-history traits, only habitat specificity was statistically significant on nested bird patterns. Because many species have a bias in favor of one type of habitat and not all types of habitats are randomly found in each fragment, there are nested habitat patterns, hence the nest pattern of habitats caused the nest pattern of species (Calmé and Desrochers, 1999). Different species select different habitats; low habitat specific species can adapt more readily to different kinds of habitat, including large and small fragments. In contrast, high habitat specific species only live in large fragmented habitats.

    However, our study have some limitations, for example, the analysis methods for the quantification of nestedness have been developed rapidly, although BINMATNEST remains popular, some other rigorous programs, such as NODF and BR, have also been developed recently. So, it is necessary for us to have further study on bird assemblages of southwestern Guangxi and better to confirm the nested result.

    In other words, birds have significant nested patterns in the karst area of southwestern Guangxi by our analysis. In these nested patterns, large habitat fragments always have a high richness vegetation and heterogeneity, i.e., more species, which need strong protection (Zhang, 2008). But many studies, including ours, also prove that even species distributions have significant nestedness; the total number of species in several small fragments was often greater than that of one large fragment, with the same area, as the total area of the small fragments (Beckon, 1993; Cook, 1995; Skaggs and Boecklen, 1996). Hence, for the protection of the diversity of birds in the karst area of southwestern Guangxi, we advocate that, while close attention should also be paid to large fragmented habitats, rich in vegetation, but even more care should be lavished on the kinds of species found in the smaller fragmented habitats, i.e. in the nature reserves.

    The study was financed by the National Nature Science Foundation of China (Grant Nos. 30970381, 31172123). We thank the Forestry Departments of Guangxi Zhuang Autonomous Region for their support and collaboration. Field assistance and logistic support were provided by the staff of all the nature reserve administrations. We also thank Aiwu JIANG, Gang YANG, Chenxing YU, Dong LI, Yinghuan WU and Dongdong ZHAO for their help with fieldwork.

    Available on Chinese Birds website, links at http://www.chinesebirds.net, including

    Table S1

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